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Phytoplankton functional groups indicators of environmental conditions in floodplain rivers and lakes of the Paraná Basin

Grupos funcionais fitoplanctônicos indicadores de condições ambientais em rios e lagos de planície de inundação

Abstracts

Abstract

Aim: The objective of this study was to evaluate the efficacy of phytoplankton functional groups as indicators of environmental conditions in floodplain rivers and lakes with different trophic state and connectivity degree to the Paraná River. Phytoplankton functional groups (FGs) cluster sensitive species to environmental variation and can be an alternative for environmental monitoring.

Methods

Samples were performed quarterly from 2010 to 2013 in the Ivinhema, Paraná and Baia Rivers and in three lakes permanently connected to each river.

Results

419 taxa were identified, and those taxa that had values greater than 5% of the total biovolume were classified into FGs (P, C, A, B, MP, H1, W1, J, TD, LO, and N). The lakes presented higher biovolume and were more productive than rivers, especially in the dry periods. The rivers presented light limitation and low phytoplankton development. The FG LO was an indicator in rainy seasons. Both rivers and lakes were mostly oligotrophic. We registered FG indicators only for the lakes (A, B, C, E, LO, P, and W1) and mesotrophic environments (A, B, C, E, J, LO, and P).

Conclusion

The FGs reflected the seasonal variation and the trophic state of environments in the upper Paraná River floodplain, mainly in the lentic environments. The species-environment relationship (FGs as indicators) was clearer in the lakes, probably because of the longer water retention that allows evidencing the response of the phytoplankton community to environmental factors. On the other hand, the absence of FGs as indicators in the rivers could be due to the high water flow that promotes dispersal stochasticity and masks the relationship between the environmental factors and the phytoplankton community. Thus, phytoplankton FGs proved to be a viable tool to evaluate the environmental conditions in a floodplain.

Keywords:
connectivity; trophy; rainy season; dry season; hydrosedimentological regime


Resumo

Objetivo: O objetivo deste estudo foi avaliar a eficácia do uso de grupos funcionais fitoplanctônicos como indicadores das condições ambientais em rios e lagos de planície de inundação de diferente estado trófico e grau de conectividade ao rio Paraná. Os grupos funcionais (GFs) fitoplanctônicos reúnem espécies sensíveis às mudanças ambientais e podem ser uma alternativa para o monitoramento ambiental.

Métodos

Foram realizadas amostragens trimestrais entre 2010 a 2013 nos rios Ivinhema, Paraná e Baía, e em três lagos conectados permanentemente a cada rio.

Resultados

Foram identificados 419 táxons. Maiores valores de biovolume fitoplanctônico foram verificados nos lagos comparado aos rios, principalmente no período seco e estiveram associados a maior disponibilidade luminosa. Foram registrados 11 GFs (P, C, A, B, MP, H1, W1, J, TD, LO e N). O GF LO foi indicador dos períodos de chuva. Os rios mantiveram-se oligotróficos em grande parte do período de estudo, enquanto os lagos mantiveram-se mesotróficos. Os GFs A, B, C, E, LO, P e W1 foram indicadores dos lagos e os GFs A, B, C, E, J, LO e P indicaram características mesotróficas.

Conclusão

Os GFs refletiram a variação sazonal e o estado trófico dos ambientes na planície de inundação do Alto Rio Paraná, especialmente nos ambientes lênticos. A relação espécie-ambiente (GFs indicadores) foi mais evidente nos lagos devido, provavelmente, ao maior tempo de retenção da água que permite evidenciar a resposta da comunidade fitoplanctônica aos fatores ambientais. Por outro lado, a ausência de GFs como indicadores nos rios provavelmente deveu-se ao alto fluxo de água que promove estocasticidade na dispersão e mascara a relação entre os fatores ambientais e a comunidade fitoplanctônica. Assim, GFs do fitoplâncton provaram ser uma ferramenta viável para avaliar as condições ambientais em uma planície de inundação.

Palavras-chave:
conectividade; trofía; período chuvoso; período seco; regime hidrossedimentológico


1. Introduction

Periodic flooding affects the environmental and biological characteristics of floodplain systems (Neiff, 1990NEIFF, J.J. Ideas Para La Interpretación Ecológica Del Paraná. Interciencia, 1990, 15(6), 424-441.) because water-level fluctuation drives the exchange of organisms and nutrients among the main channel, tributaries, and lakes. Thus, flooding is an important event that drives the dynamics of materials and species in floodplains (Neiff, 1990NEIFF, J.J. Ideas Para La Interpretación Ecológica Del Paraná. Interciencia, 1990, 15(6), 424-441.). However, the effect of the water level variation of the main channel on their associated environments depends on the size, position and the connection degree of these environments (Junk et al., 1989JUNK, W.J., BAYLEY, P.B. and SPARKS, R.E. The flood pulse concept in river-floodplain systems. Ottawa: Fisheries and Oceans Canada, 1989, pp. 110-127. Canadian Special Publication of Fisheries and Aquatic Sciences, vol. 106.).

The environments in floodplain show high connectivity and environmental homogeneity in flood periods (Thomaz et al., 2007THOMAZ, S.M., BINI, L.M. and BOZELLI, R.L. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia, 2007, 579(1), 1-13. http://dx.doi.org/10.1007/s10750-006-0285-y.
http://dx.doi.org/10.1007/s10750-006-028...
). In dry periods, when the connectivity is lower, the floodplain shows high environmental heterogeneity. The diversity patterns of the aquatic communities response to the temporal variation of the environmental conditions of floodplains (Neiff, 1990NEIFF, J.J. Ideas Para La Interpretación Ecológica Del Paraná. Interciencia, 1990, 15(6), 424-441.). For instance, phytoplankton presents higher diversity in dry periods than in flooding (Devercelli, 2006DEVERCELLI, M. Phytoplankton of the Middle Paraná River during an anomalous hydrological period: a morphological and functional approach. Hydrobiologia, 2006, 563(1), 465-478. http://dx.doi.org/10.1007/s10750-006-0036-0.
http://dx.doi.org/10.1007/s10750-006-003...
, 2010DEVERCELLI, M. Changes in phytoplankton morpho-functional groups induced by extreme hydroclimatic events in the Middle Paraná River (Argentina). Hydrobiologia, 2010, 639(1), 5-19. http://dx.doi.org/10.1007/s10750-009-0020-6.
http://dx.doi.org/10.1007/s10750-009-002...
; Nabout et al., 2006NABOUT, J.C., NOGUEIRA, I.S. and OLIVEIRA, L.G. Phytoplankton community of floodplain lakes of the Araguaia River, Brazil, in the rainy and dry seasons. Journal of Plankton Research, 2006, 28(2), 181-193. http://dx.doi.org/10.1093/plankt/fbi111.
http://dx.doi.org/10.1093/plankt/fbi111...
; Lasne et al., 2007LASNE, E., LEK, S. and LAFFAILLE, P. Patterns in fish assemblages in the Loire floodplain: the role of hydrological connectivity and implications for conservation. Biological Conservation, 2007, 139(3-4), 258-268. http://dx.doi.org/10.1016/j.biocon.2007.07.002.
http://dx.doi.org/10.1016/j.biocon.2007....
; Loverde-Oliveira et al., 2007LOVERDE-OLIVEIRA, S.M., HUSZAR, V.L.M. and FANTIN-CRUZ, I. Implications of the flood pulse on morphometry of a Pantanal lake (Mato Grosso state, Central Brazil). Acta Limnologica Brasiliensia, 2007, 19(4), 453-461.; Stanković et al., 2012STANKOVIĆ, I., VLAHOVIĆ, T., GLIGORA UDOVIČ, M., VÁRBÍRÓ, G. and BORICS, G. Phytoplankton functional and morpho-functional approach in large floodplain rivers. Hydrobiologia, 2012, 698(1), 217-231. http://dx.doi.org/10.1007/s10750-012-1148-3.
http://dx.doi.org/10.1007/s10750-012-114...
; Bovo-Scomparin et al., 2013BOVO-SCOMPARIN, V.M., TRAIN, S. and RODRIGUES, L.C. Influence of reservoirs on phytoplankton dispersion and functional traits: a case study in the Upper Paraná River, Brazil. Hydrobiologia, 2013, 702(1), 115-127. http://dx.doi.org/10.1007/s10750-012-1313-8.
http://dx.doi.org/10.1007/s10750-012-131...
).

The upper Paraná River floodplain is affected by several anthropic activities, and the construction of reservoirs is one of the most important (Agostinho et al., 2004AGOSTINHO, A.A., GOMES, L.C., THOMAZ, S.M. and HAHN, N.S. The upper Paraná River and its floodplain: main characteristics and perspectives for management and conservation. In: S.M. THOMAZ, A. AGOSTINHO and N.S. HANH, eds. The upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers, 2004, 394 p.). Dams cause intense modifications in the fluvial system (Souza Filho, 2009SOUZA FILHO, E. Evaluation of the Upper Paraná River discharge controlled by reservoirs. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2), 707-716, Supplement. PMid:19738976. http://dx.doi.org/10.1590/S1519-69842009000300024.
http://dx.doi.org/10.1590/S1519-69842009...
). For example, dams operations promote daily variation on the water level (Agostinho et al., 2008AGOSTINHO, A.A., PELICICE, F.M. and GOMES, L.C. Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2008, 68(4), 1119-1132. http://dx.doi.org/10.1590/S1519-69842008000500019.
http://dx.doi.org/10.1590/S1519-69842008...
; Souza Filho, 2009SOUZA FILHO, E. Evaluation of the Upper Paraná River discharge controlled by reservoirs. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2), 707-716, Supplement. PMid:19738976. http://dx.doi.org/10.1590/S1519-69842009000300024.
http://dx.doi.org/10.1590/S1519-69842009...
), cause interference in the nutrient balance and increase the downstream water transparency (Roberto et al., 2009ROBERTO, M.C., SANTANA, N.N. and THOMAZ, S.M. Limnology in the Upper Paraná River floodplain: large-scale spatial and temporal patterns, and the influence of reservoirs. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2), 717-725, Supplement. http://dx.doi.org/10.1590/S1519-69842009000300025.
http://dx.doi.org/10.1590/S1519-69842009...
).

Each environment associated with floodplain have different factors that influence the structure and dynamic of aquatic communities. Lakes have a high productivity-diversity ratio and an important role in the maintaining the biodiversity and system integrity (Korhonen et al., 2011KORHONEN, J.J., WANG, J. and SOININEN, J. Productivity-diversity relationships in lake plankton communities. PLoS One, 2011, 6(8), 1-11. PMid:21850218. http://dx.doi.org/10.1371/journal.pone.0022041.
http://dx.doi.org/10.1371/journal.pone.0...
; Stomp et al., 2011STOMP, M., HUISMAN, J., MITTELBACH, G.G., LITCHMAN, E. and KLAUSMEIER, C.A. Large-scale biodiversity patterns in freshwater phytoplankton. Ecology, 2011, 92(11), 2096-2107. PMid:22164834. http://dx.doi.org/10.1890/10-1023.1.
http://dx.doi.org/10.1890/10-1023.1...
; Borics et al., 2012BORICS, G., TÓTHMÉRÉSZ, B., LUKÁCS, B.A. and VÁRBÍRÓ, G. Functional groups of phytoplankton shaping diversity of shallow lake ecosystems. Hydrobiologia, 2012, 698(1), 251-262. http://dx.doi.org/10.1007/s10750-012-1129-6.
http://dx.doi.org/10.1007/s10750-012-112...
). On the other hand, highly dynamic rivers select species that are adapted to high flow and turbidity (Devercelli & O’Farrell, 2013DEVERCELLI, M. and O’FARRELL, I. Factors affecting the structure and maintenance of phytoplankton functional groups in a nutrient rich lowland river. Limnologica, 2013, 43(2), 67-78. http://dx.doi.org/10.1016/j.limno.2012.05.001.
http://dx.doi.org/10.1016/j.limno.2012.0...
; Fraisse et al., 2013FRAISSE, S., BORMANS, M. and LAGADEUC, Y. Morphofunctional traits reflect differences in phytoplankton community between rivers of contrasting flow regime. Aquatic Ecology, 2013, 47(3), 315-327. http://dx.doi.org/10.1007/s10452-013-9446-z.
http://dx.doi.org/10.1007/s10452-013-944...
).

Phytoplankton presents temporal patterns related to environmental changes (Huszar et al., 1998HUSZAR, V.L.M., SILVA, L.H.S., DOMINGOS, P., MARINHO, M. and MELO, S. The relationship between phytoplankton composition and physical-chemical variables: a comparison of taxonomic and morphological-functional descriptors in six temperate lakes. Hydrobiologia, 1998, 369–370(0), 59-71. http://dx.doi.org/10.1023/A:1017047221384.
http://dx.doi.org/10.1023/A:101704722138...
; Borges & Train, 2009BORGES, P.A.F. and TRAIN, S. Phytoplankton diversity in the Upper Paraná River floodplain during two years of drought (2000 and 2001). Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2, 637-647, Supplement. PMid:19738970. http://dx.doi.org/10.1590/S1519-69842009000300018.
http://dx.doi.org/10.1590/S1519-69842009...
), and the processes acting on this community operates on a reduced timescale. Therefore, phytoplankton is an important ecological tool to obtain short-term responses (Reynolds, 2002REYNOLDS, C.S. Ecological pattern and ecosystem theory. Ecological Modelling, 2002, 158(3), 181-200. http://dx.doi.org/10.1016/S0304-3800(02)00230-2.
http://dx.doi.org/10.1016/S0304-3800(02)...
; Rodrigues et al., 2002RODRIGUES, L.C., TRAIN, S., ROBERTO, M. and PAGIORO, T.A. Seasonal fluctuation of some limnological variables on a floodplain lake (Patos lagoon) of the Upper Paraná River, Mato Grosso do Sul State, Brazil. Brazilian Archives of Biology and Technology, 2002, 45(4), 499-513. http://dx.doi.org/10.1590/S1516-89132002000600014.
http://dx.doi.org/10.1590/S1516-89132002...
).

Environmental filters give a structured to phytoplankton community through the selection of species characteristics (Padisák et al., 2003PADISÁK, J., BARBOSA, F., KOSCHEL, R. and KRIENITZ, L. Deep layer cyanoprokaryota maxima in temperate and tropical lakes. Advances in Limnology, 2003, 58, 175-199.; Naselli-Flores et al., 2007NASELLI-FLORES, L., PADISÁK, J. and ALBAY, M. Shape and size in phytoplankton ecology: Do they matter? Hydrobiologia, 2007, 578(1), 157-161. http://dx.doi.org/10.1007/s10750-006-2815-z.
http://dx.doi.org/10.1007/s10750-006-281...
; Brasil & Huszar, 2011BRASIL, J. and HUSZAR, V.L.M. O papel dos traços funcionais na ecologia do fitoplâncton continental. Oecologia Australis, 2011, 15(4), 799-834. http://dx.doi.org/10.4257/oeco.2011.1504.04.
http://dx.doi.org/10.4257/oeco.2011.1504...
; Zhang et al., 2015ZHANG, H., QI, W., JOHN, R., WANG, W., SONG, F. and ZHOU, S. Using functional trait diversity to evaluate the contribution of multiple ecological processes to community assembly during succession. Ecography, 2015, 38(1), 1176-1186. http://dx.doi.org/10.1111/ecog.01123.
http://dx.doi.org/10.1111/ecog.01123...
). Hence, the phytoplankton functional approach is justified to understand the key processes that drive the community assemblage. In this context, species can be grouped into groups based on the species functional features. This Functional Groups (FGs), grouped species with shared physiological, morphological and phenological characteristics, independent of phylogenetic relationships (Petchey & Gaston, 2006PETCHEY, O.L. and GASTON, K.J. Functional diversity: Back to basics and looking forward. Ecology Letters, 2006, 9(6), 741-758. PMid:16706917. http://dx.doi.org/10.1111/j.1461-0248.2006.00924.x.
http://dx.doi.org/10.1111/j.1461-0248.20...
; Litchman et al., 2010LITCHMAN, E., PINTO, P.T., KLAUSMEIER, C.A., THOMAS, M.K. and YOSHIYAMA, K. Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia, 2010, 653(1), 15-28. http://dx.doi.org/10.1007/s10750-010-0341-5.
http://dx.doi.org/10.1007/s10750-010-034...
). Based on this assumption, Reynolds et al. (2002)REYNOLDS, C.S., HUSZAR, V., KRUK, C., NASELLI-FLORES, L. and MELO, S. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research, 2002, 24(5), 417-428. http://dx.doi.org/10.1093/plankt/24.5.417.
http://dx.doi.org/10.1093/plankt/24.5.41...
proposed the approach of phytoplankton FGs to cluster species sensitive to environmental changes (Padisák et al., 2009PADISÁK, J., CROSSETTI, L.O. and NASELLI-FLORES, L. Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia, 2009, 621(1), 1-19. http://dx.doi.org/10.1007/s10750-008-9645-0.
http://dx.doi.org/10.1007/s10750-008-964...
) and simplify extensive taxonomic lists. Phytoplankton FGs are sensitivity to environmental variation, hence efficient to predict environmental conditions (Kruk et al., 2002KRUK, C., MAZZEO, N., LACEROT, G. and REYNOLDS, C.S. Classification schemes for phytoplankton: a local validation of a functional approach to the analysis of species temporal replacement. Journal of Plankton Research, 2002, 24(9), 901-912. http://dx.doi.org/10.1093/plankt/24.9.901.
http://dx.doi.org/10.1093/plankt/24.9.90...
; Nabout et al., 2006NABOUT, J.C., NOGUEIRA, I.S. and OLIVEIRA, L.G. Phytoplankton community of floodplain lakes of the Araguaia River, Brazil, in the rainy and dry seasons. Journal of Plankton Research, 2006, 28(2), 181-193. http://dx.doi.org/10.1093/plankt/fbi111.
http://dx.doi.org/10.1093/plankt/fbi111...
; Becker et al., 2009BECKER, V., HUSZAR, V.L.M. and CROSSETTI, L.O. Responses of phytoplankton functional groups to the mixing regime in a deep subtropical reservoir. Hydrobiologia, 2009, 628(1), 137-151. http://dx.doi.org/10.1007/s10750-009-9751-7.
http://dx.doi.org/10.1007/s10750-009-975...
; Bovo-Scomparin et al., 2013BOVO-SCOMPARIN, V.M., TRAIN, S. and RODRIGUES, L.C. Influence of reservoirs on phytoplankton dispersion and functional traits: a case study in the Upper Paraná River, Brazil. Hydrobiologia, 2013, 702(1), 115-127. http://dx.doi.org/10.1007/s10750-012-1313-8.
http://dx.doi.org/10.1007/s10750-012-131...
; Crossetti et al., 2013CROSSETTI, L.O., BECKER, V., CARDOSO, L.D.S., RODRIGUES, L.R., COSTA, L.S. and MOTTA-MARQUES, D. Is phytoplankton functional classification a suitable tool to investigate spatial heterogeneity in a subtropical shallow lake? Limnologica, 2013, 43(3), 157-163. http://dx.doi.org/10.1016/j.limno.2012.08.010.
http://dx.doi.org/10.1016/j.limno.2012.0...
; Bortolini et al., 2014BORTOLINI, J.C., RODRIGUES, L.C., JATI, S. and TRAIN, S. Phytoplankton functional and morphological groups as indicators of environmental variability in a lateral channel of the Upper Paraná River floodplain. Acta Limnologica Brasiliensia, 2014, 26(1), 98-108. http://dx.doi.org/10.1590/S2179-975X2014000100011.
http://dx.doi.org/10.1590/S2179-975X2014...
).

This study aimed to verify the efficacy of phytoplankton FGs as indicators of environmental conditions in floodplain and the effects of the connectivity of the environments to the main river on phytoplankton variation. Therefore, we hypothesized that (i) the phytoplankton FGs respond to the environmental conditions of each sampled site and its trophic state; (ii) the FGs indicators will be different in each hydrological periods.

2. Material and Methods

2.1. Study area

The Paraná River is the second largest river in South America (4,965 km), the tenth largest river worldwide in water discharge (9,900 m3/s) and the fourth in drainage area (2.8 × 106 km2) (Agostinho et al., 2008AGOSTINHO, A.A., PELICICE, F.M. and GOMES, L.C. Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2008, 68(4), 1119-1132. http://dx.doi.org/10.1590/S1519-69842008000500019.
http://dx.doi.org/10.1590/S1519-69842008...
). The Ivinhema and Baia Rivers are the main tributaries of Paraná River. The Ivinhema State Park is an important area of environmental protection. Ivinhema State Park is located in the distal portion of the Ivinhema River. This study was developed in the upper Paraná River floodplain, located downstream of the Porto Primavera reservoir and upstream of the Itaipu Reservoir. This region is important for the regional biodiversity because it is the last damming-free stretch in all Brazilian territory.

We sampled the main channel of Paraná River (R1 - 22°45’S; 53°15’W), Ivinhema River (R2 - 22º47’S; 53º32’W), Baía River (R3 - 22º43’S; 53º17’W), and three lakes permanently connected to these rivers. The Garças lake (L1 - 22°43’S; 53°13’W) is connected to the Paraná river by a channel approximately 50m longer and has an extension with 3,8ha. The Guaraná lake (L2 - 22º43’S; 53º18’W) has dark watercolor, 4.2ha and is connected to the Ivinhema river by a 70m channel. The Patos lake (L3 - 23º49’S; 53º33’W) has a large extension with 113.8ha and has a short connection channel a 10m length to Baia river (Figure 1).

Figure 1
Map and localization of sampling sites in the upper Paraná River floodplain (R1: Paraná River; R2: Baia River; R3: Ivinhema River; L1: Garças lake; L2: Guaraná lake; L3: Patos lake).

2.2. Methodological procedures

Samples were taken quarterly to analyze the phytoplankton community and environmental variables from March 2010 to December 2013. Thus, in each one of the six environments were collected 16 samples in total (n = 96). Total phytoplankton was collected with flasks at the subsurface (20 cm depth) of the pelagic zone. The samples were preserved with 1% Lugol solution (Bicudo & Menezes, 2006BICUDO, C.E.M.C.E. and MENEZES, M. Gêneros de algas de águas continentais do Brasil: chave para identificação e descrições. São Carlos: RIMA, 2006.).

The randomly counting were performed in transect per field using an inverted microscope (400x magnification) (Lund et al., 1958LUND, J.W.G., KIPLING, C. and LE CREN, E.D. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia, 1958, 11(2), 980-985. http://dx.doi.org/10.1007/BF00007865.
http://dx.doi.org/10.1007/BF00007865...
; Utermöhl, 1958UTERMÖHL, H. Zur Vervollkommnung der quantitativen Phytoplankton-methodik. Mitteilungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie, 1958, 9, 1-38.). Phytoplankton biomass was estimated from the biovolume (mm3.L-1), by multiplying the density of each species by its respective volume. The volume of each cell was calculated by approximate individuals to geometric shapes such as cylinders, spheres, and ellipses (Hillebrand et al., 1999HILLEBRAND, H., DÜRSELEN, C.-D., KIRSCHTEL, D., POLLINGHER, U. and ZOHARY, T. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 1999, 35(2), 403-424. http://dx.doi.org/10.1046/j.1529-8817.1999.3520403.x.
http://dx.doi.org/10.1046/j.1529-8817.19...
; Sun & Liu, 2003SUN, J. and LIU, D. Geometric models for calculating cell biovolume and surface area for phytoplankton. Journal of Plankton Research, 2003, 25(11), 1331-1346. http://dx.doi.org/10.1093/plankt/fbg096.
http://dx.doi.org/10.1093/plankt/fbg096...
). Phytoplankton taxa with contribution greater than 5% to the total biovolume of each sample were classified into FGs, according to Reynolds et al. (2002)REYNOLDS, C.S., HUSZAR, V., KRUK, C., NASELLI-FLORES, L. and MELO, S. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research, 2002, 24(5), 417-428. http://dx.doi.org/10.1093/plankt/24.5.417.
http://dx.doi.org/10.1093/plankt/24.5.41...
and Padisák et al. (2009)PADISÁK, J., CROSSETTI, L.O. and NASELLI-FLORES, L. Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia, 2009, 621(1), 1-19. http://dx.doi.org/10.1007/s10750-008-9645-0.
http://dx.doi.org/10.1007/s10750-008-964...
.

We measured water temperature (WT, °C), pH, electrical conductivity (EC, µS.cm-1) and dissolved oxygen (DO, mg.L-1) using digital portable potentiometers. Total phosphorus (TP, µm.L-1), soluble reactive phosphorus (SRP, µm.L-1), nitrate (NO3-N, µm.L-1), nitrite (NO2-N, µm.L-1), inorganic soluble material (ISM, mg.L-1) and ammonium (NH4-N, µm.L-1) were measured following Bovo-Scomparin et al. (2013)BOVO-SCOMPARIN, V.M., TRAIN, S. and RODRIGUES, L.C. Influence of reservoirs on phytoplankton dispersion and functional traits: a case study in the Upper Paraná River, Brazil. Hydrobiologia, 2013, 702(1), 115-127. http://dx.doi.org/10.1007/s10750-012-1313-8.
http://dx.doi.org/10.1007/s10750-012-131...
. The dissolved inorganic nitrogen (DIN, µm.L-1) was calculated as the sum of the NH4-N, NO2-N and NO3-N concentrations. We measured the maximum depth (Zmax, m), and the euphotic zone (Zeu, m) was calculated as 2.7 times the Secchi-disk depth (Cole, 1994COLE, A.G. Textbook of limnology. 4th ed. Illinois: Waveland Press, 1994.). The mixing zone (Zmix, m) was calculated according to the thermal profile. The Itaipu Binational (Itaipu Binacional), National Water Agency (Agência Nacional de Águas – ANA) and the Limnology, Ichthyology, and Aquaculture Research Center (Núcleo de Pesquisas em Limnologia, Ictiologia, e Aquicultura - Nupélia) provided the daily water levels (WL) of Ivinhema and Paraná Rivers. Rainy periods were considered when the water level of Paraná River was ≥ 3.5m (Souza Filho et al., 2004SOUZA FILHO, E.E., ROCHA, P.C., COMUNELLO, E. and STEVAUX, J.C. Effects of the Porto Primavera dam on physical environment of the downstream floodplain. In: S.M. THOMAZ, A.A. AGOSTINHO and N.S. HANH, eds. The upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers, 2004, 393 p.). For each lake, we calculated the temporal water level variation (ΔZmax) as the difference between the water level registered in a sampling and the previous sampling.

2.3. Numerical analysis

Principal Component Analysis (PCA) was used to characterize spatially and temporally the environmental variation. An Indicator Value Analysis (IndVal – Dufrêne & Legendre, 1997DUFRÊNE, M. and LEGENDRE, P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs, 1997, 67(3), 345-366.) was applied to verify if FGs are indicators of environmental conditions. The indicator value makes possible to predict the association of a given FG with a specific habitat or particular environmental conditions. The indicator value was statistically tested using random Monte Carlo allocations. For this analysis, we used a matrix of the FGs and as environmental conditions, we included the hydrological period (dry and rainy), environment type (as river and lake) and trophic state. The trophic state was characterized according to OECD (1982)ORGANISATION FOR ECONOMIC CO-OPERATION AND DEVELOPMENT – OECD. Eutrophication of water: monitoring assessment and control. Paris: Environment Directorate, 1982. Technical Report., by using chlorophyll (oligotrophic: < 8 µg L-1, mesotrophic: 8-25 µg L-1 and eutrophic: >25 µg L-1) and TP (oligotrophic: < 10 µg L-1, mesotrophic: 10-35 µg L-1 and eutrophic: 35 µg L-1).

The PCA and IndVal analysis were performed using PC-Ord program (Mccune & Mefford, 1999MCCUNE, B. and MEFFORD, M.J. PC-ORD: multivariate analysis of ecological data, version 4 [software]. Gleneden Beach: MjM Software Design, 1999.). Graphs were generated using the software STATISTICA version 7.1 (Statsoft, 2005STATSOFT. Statistica: data analysis software system, version 7.1 [software]. Tulsa: StatSoft, 2005 [viewed 15 June 2017]. Available from: www.statsoft.inc).

3. Results

3.1. Water level and depth

The upper Paraná River showed the highest water level in March 2010 and 2011, which is characterized as rainy periods, according to Souza Filho (2009)SOUZA FILHO, E. Evaluation of the Upper Paraná River discharge controlled by reservoirs. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2), 707-716, Supplement. PMid:19738976. http://dx.doi.org/10.1590/S1519-69842009000300024.
http://dx.doi.org/10.1590/S1519-69842009...
. The maximum depth of lakes was influenced by the water level of the rivers (Figure 2). A similar variation occurred in the lakes associated with the sites R1 and R2. The highest depth was registered in the lake associated with the site R3 (Figure 3).

Figure 2
Paraná River (R1) and Ivinhema River (R2) daily water levels and maximum depth (Zmax) of the lakes (L1: Garças lake; L2: Guaraná Lake; L3: Patos lake) from March 2010 to January 2014.
Figure 3
Temporal variation of the water level (ΔZmax) of lakes in the upper Paraná River floodplain from March 2010 to December 2013. For each lake, the variation was considered as the difference between the water level registered in a sampling and the previous sampling.

3.2. Limnological characterization

The two first axes of the PCA were selected by the broken stick criterion and explained 45% of the total environmental variation. Temporal and spatial gradients were observed. The rainy periods were associated with the highest water level. The site R1 was related to greater values of Zeu, Zmix, Zmax, EC, and DIN. The site R3 was associated with ISM and DO. The sites R2 and L2 were related to the highest SRP, PT, and TN concentrations (Table 1 and Figure 4). Lakes showed total mixing of the water-column in almost all the hydrological periods, and stratification occurred in some rainy periods. The lakes had mesotrophic characteristics in most of the study, and most of the samples of rivers showed oligotrophic characteristics.

Table 1
Mean values and coefficient of variation (% - CV) of the limnological variables in the studied environments. Water temperature – WT (°C), soluble reactive phosphorus – SRP (µg.L-1), total nitrogen – TN (µg.L-1), dissolved inorganic nitrogen – DIN (µg.L-1), dissolved oxygen – DO (mg.L-1), electrical conductivity – EC (µS.cm-1), inorganic soluble material – ISM (mg. L-1), mixing zone – Zmix (m) and euphotic zone – Zeu (m).
Figure 4
First two axes generated by Principal Component Analysis (PCA) on the studied environments. Water level (WL), Water temperature (WT), Soluble reactive phosphorus (SRP), Total nitrogen (TN), Dissolved inorganic nitrogen (DIN), Dissolved oxygen (DO), Electrical conductivity (EC), Chlorophyll a (Chla), Inorganic soluble material (ISM), Mixture zone (Zmix), Euphotic zone (Zeu), Depth (Zmax).

3.3. Phytoplankton community

We registered the highest biovolume values in the dry periods. The biomass was high in the lakes and R2, and low in R1 and R3. Cyanobacteria dominated in the sites L3, L2, and R2; Chrysophyceans dominated in L1. In the Paraná River dinoflagellates, cryptophyceans, diatoms, and cyanobacteria showed the highest biovolume.

We classified 419 taxa into 13 FGs (Figure 5). The FGs P, B, C and A were the most representative in the lakes in the rainy periods, and the FGs A, C, H1, MP, and P were the most expressive in dry periods (Figure 5a-c). In rivers, the FGs A, Lo, M, N, P, and MP were the most representative FGs in rainy periods and the FGs A, J, H1, MP e P in dry periods (Figure 5d-f).

Figure 5
Biovolume of the phytoplankton FGs in the sampling sites from March 2010 to December 2013 (a = L1; b = L2; c = L3; d = R3; e = R2; f = R1. <5% - Total biovolume of taxa with less than 5%; white bar= dry; black bar= rainy).

The main representatives of the FGs were: P, Aulacoseira granulata (Ehr.) Sim. var. granulata; FG C, Aulacoseira ambigua (Grun.) Sim. var. ambigua; FG A, Urosolenia eriensis (H. L. Sm.) Round & Craw. and Acanthoceras zachariasii (Brun) Sim.; FG B Aulacoseira herzogii (Lemm.) Sim.; FG E, Dinobryon sertularia Ehr. and Dinobryon divergens Imh.; FG MP Nitzschia acicularis (Kütz.) W. Smith, Synedra goulardii Bréb. and Amphipleura lindheimeri Grun.; FG H1 Dolichospermum planctonicum (Brunn.) Wacklin et al., Dolichospermum solitarium (Kleb.) Wacklin et al., and Dolichospermum spiroides (Kleb.) Wacklin et al.; FG W1 Lepocinclis ovum var. ovum (Ehr.) Lemm. and Phacus sp.; FG J Pediastrum duplex Mey.; FG TD Onychonema laeve Nordst. and Gonatozygon aculeatum Hast.; FG LO, Peridinium sp. and Radiocystis fernandoi Kom. & Kom. Legn.; and FG N Cosmarium decoratum West and G. S. West.

3.4. IndVal for FGs

We registered the FG LO as an indicator group of rainy periods. Considering the trophic state, only the mesotrophic state presented FGs indicator (A, B, C, E, J, Lo, P). For the environment type, only the lakes exhibited FGs indicators (A, B, C, E, Lo, P, W1) (Table 2).

Table 2
Phytoplankton FGs indicators of hydrological periods (Rain and Dry), environment type (river and lake), and trophic state (Oligotrophic and Mesotrophic).

4. Discussion

Our results show that the phytoplankton functional groups reflect the environmental characteristics of the analyzed floodplain environments. Our findings suggest that the analyses of biovolume variation of functional groups can be a useful tool for monitoring the trophic state of floodplain lakes.

The studied environments presented high variation in light availability and nutrient concentrations, which probably influenced the spatial distribution of phytoplankton biovolume (Oliver & Merrick, 2006OLIVER, R.L. and MERRICK, C.J. Partitioning of river metabolism identifies phytoplankton as a major contributor in the regulated Murray River (Australia). Freshwater Biology, 2006, 51(6), 1131-1148. http://dx.doi.org/10.1111/j.1365-2427.2006.01562.x.
http://dx.doi.org/10.1111/j.1365-2427.20...
; Devercelli, 2010DEVERCELLI, M. Changes in phytoplankton morpho-functional groups induced by extreme hydroclimatic events in the Middle Paraná River (Argentina). Hydrobiologia, 2010, 639(1), 5-19. http://dx.doi.org/10.1007/s10750-009-0020-6.
http://dx.doi.org/10.1007/s10750-009-002...
; Istvánovics et al., 2010ISTVÁNOVICS, V., HONTI, M., VÖRÖS, L. and KOZMA, Z. Phytoplankton dynamics in relation to connectivity, flow dynamics and resource availability-the case of a large, lowland river, the Hungarian Tisza. Hydrobiologia, 2010, 637(1), 121-141. http://dx.doi.org/10.1007/s10750-009-9991-6.
http://dx.doi.org/10.1007/s10750-009-999...
; Soares et al., 2012SOARES, M.C.S., MARINHO, M.M., AZEVEDO, S.M.O.F., BRANCO, C.W.C. and HUSZAR, V.L.M. Eutrophication and retention time affecting spatial heterogeneity in a tropical reservoir. Limnologica, 2012, 42(3), 197-203. http://dx.doi.org/10.1016/j.limno.2011.11.002.
http://dx.doi.org/10.1016/j.limno.2011.1...
). The site R1 (Paraná River) showed the lowest phytoplankton biovolume, probably influenced by high water-flow and low nutrient concentration. As the dams built in the Paraná River have increased the transparency and decreased the nutrient concentration, studies suggest that the oligotrophic characteristics of Paraná River negatively affect the primary productivity (Zalocar de Domitrovic et al., 2007ZALOCAR DE DOMITROVIC, Y., POI DE NEIFF, S.G., CASCO, S.L., DOMITROVIC, Z. and NEIFF, P. Abundance and diversity of phytoplankton in the Paraná River (Argentina) 220 km downstream of the Yacyretá reservoir. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2007, 67(1), 53-63. PMid:17505750. http://dx.doi.org/10.1590/S1519-69842007000100008.
http://dx.doi.org/10.1590/S1519-69842007...
; Agostinho et al., 2008AGOSTINHO, A.A., PELICICE, F.M. and GOMES, L.C. Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2008, 68(4), 1119-1132. http://dx.doi.org/10.1590/S1519-69842008000500019.
http://dx.doi.org/10.1590/S1519-69842008...
; Roberto et al., 2009ROBERTO, M.C., SANTANA, N.N. and THOMAZ, S.M. Limnology in the Upper Paraná River floodplain: large-scale spatial and temporal patterns, and the influence of reservoirs. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2), 717-725, Supplement. http://dx.doi.org/10.1590/S1519-69842009000300025.
http://dx.doi.org/10.1590/S1519-69842009...
; Souza Filho, 2009SOUZA FILHO, E. Evaluation of the Upper Paraná River discharge controlled by reservoirs. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2), 707-716, Supplement. PMid:19738976. http://dx.doi.org/10.1590/S1519-69842009000300024.
http://dx.doi.org/10.1590/S1519-69842009...
; Bovo-Scomparin et al., 2013BOVO-SCOMPARIN, V.M., TRAIN, S. and RODRIGUES, L.C. Influence of reservoirs on phytoplankton dispersion and functional traits: a case study in the Upper Paraná River, Brazil. Hydrobiologia, 2013, 702(1), 115-127. http://dx.doi.org/10.1007/s10750-012-1313-8.
http://dx.doi.org/10.1007/s10750-012-131...
).

In several periods, the lakes and the Ivinhema and Baía Rivers presented similar nutrient concentration. However, lakes showed the highest phytoplankton biovolume. Although rivers can present optimal nutrient concentrations for phytoplankton development (Jones & Elliott, 2007JONES, I.D. and ELLIOTT, J.A. Modelling the effects of changing retention time on abundance and composition of phytoplankton species in a small lake. Freshwater Biology, 2007, 52(6), 988-997. http://dx.doi.org/10.1111/j.1365-2427.2007.01746.x.
http://dx.doi.org/10.1111/j.1365-2427.20...
; Fantin-Cruz et al., 2016FANTIN-CRUZ, I., PEDROLLO, O., GIRARD, P., ZEILHOFER, P. and HAMILTON, S.K. Changes in river water quality caused by a diversion hydropower dam bordering the Pantanal floodplain. Hydrobiologia, 2016, 768(1), 223-238. http://dx.doi.org/10.1007/s10750-015-2550-4.
http://dx.doi.org/10.1007/s10750-015-255...
), they can limit the phytoplankton because of the low light availability and short water-retention time (Reynolds & Descy, 1996REYNOLDS, C. and DESCY, J. The production, biomass and structure of phytoplankton in large rivers. Archiv für Hydrobiologie, 1996, 10(1-4), 161-187.; Devercelli, 2010DEVERCELLI, M. Changes in phytoplankton morpho-functional groups induced by extreme hydroclimatic events in the Middle Paraná River (Argentina). Hydrobiologia, 2010, 639(1), 5-19. http://dx.doi.org/10.1007/s10750-009-0020-6.
http://dx.doi.org/10.1007/s10750-009-002...
; Fraisse et al., 2013FRAISSE, S., BORMANS, M. and LAGADEUC, Y. Morphofunctional traits reflect differences in phytoplankton community between rivers of contrasting flow regime. Aquatic Ecology, 2013, 47(3), 315-327. http://dx.doi.org/10.1007/s10452-013-9446-z.
http://dx.doi.org/10.1007/s10452-013-944...
). Systems with short water-retention time (e.g., continuously flushed systems) can present high loss of phytoplankton biomass attributed to wash-out, hence difficult the establishment of planktonic organisms (Fraisse et al., 2015FRAISSE, S., BORMANS, M. and LAGADEUC, Y. Turbulence effects on phytoplankton morphofunctional traits selection. Limnology and Oceanography, 2015, 60(3), 872-884. http://dx.doi.org/10.1002/lno.10066.
http://dx.doi.org/10.1002/lno.10066...
). In the other hand, phytoplankton biomass was favored in the studied lakes probably because of the high stability of water column and high nutrient concentration.

The FGs responded to the environmental conditions and it could be an important tool for environmental monitoring, hence we accepted the first hypothesis. The results showed that the phytoplankton biomass responds to temporal environmental variation and suggest that the predictability of the phytoplankton structure depends on the analyzed climatic period. For instance, we registered FG as indicators only for the rainy period. The higher connection among environments probably guaranteed the FG LO to reach all the studied sites in the rainy period. On the other hand, we did not register FG indicator of the dry periods, probably because of the higher environmental heterogeneity in dry periods (Thomaz et al., 2007THOMAZ, S.M., BINI, L.M. and BOZELLI, R.L. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia, 2007, 579(1), 1-13. http://dx.doi.org/10.1007/s10750-006-0285-y.
http://dx.doi.org/10.1007/s10750-006-028...
) that favored different organisms in each environment.

The dinoflagellates included in the FG LO present mobility and can tolerate the nutrient losses (Reynolds et al., 2002REYNOLDS, C.S., HUSZAR, V., KRUK, C., NASELLI-FLORES, L. and MELO, S. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research, 2002, 24(5), 417-428. http://dx.doi.org/10.1093/plankt/24.5.417.
http://dx.doi.org/10.1093/plankt/24.5.41...
) caused by the water-column stratification in rainy periods (Becker et al., 2008BECKER, V., HUSZAR, V.L.M., NASELLI-FLORES, L. and PADISÁK, J. Phytoplankton equilibrium phases during thermal stratification in a deep subtropical reservoir. Freshwater Biology, 2008, 53(5), 952-963. http://dx.doi.org/10.1111/j.1365-2427.2008.01957.x.
http://dx.doi.org/10.1111/j.1365-2427.20...
; Mihaljević et al., 2013MIHALJEVIĆ, M., ŠPOLJARIĆ, D., STEVIĆ, F. and ŽUNA PFEIFFER, T. Assessment of flood-induced changes of phytoplankton along a river-floodplain system using the morpho-functional approach. Environmental Monitoring and Assessment, 2013, 185(10), 8601-8619. PMid:23604727. http://dx.doi.org/10.1007/s10661-013-3198-z.
http://dx.doi.org/10.1007/s10661-013-319...
). In stratified environments, these organisms are good competitors (Bellinger & Sigee, 2011BELLINGER, E.G. and SIGEE, D.C. Freshwater algae: identification and use as bioindicators. Chichester: John Wiley & Sons, 2011.) because they can migrate in the water column to find resources (Rangel et al., 2009RANGEL, L.M., SILVA, L.H.S., ARCIFA, M.S. and PERTICARRARI, A. Driving forces of the diel distribution of phytoplankton functional groups in a shallow tropical lake. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(1), 75-85. http://dx.doi.org/10.1590/S1519-69842009000100009.
http://dx.doi.org/10.1590/S1519-69842009...
). Whereas the low FG LO biovolume registered in periods with high water-column mixing (dry periods) could be explained by the sensitivity of these organisms to deep (e.g. reservoirs) and prolonged mixing (Reynolds et al., 2002REYNOLDS, C.S., HUSZAR, V., KRUK, C., NASELLI-FLORES, L. and MELO, S. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research, 2002, 24(5), 417-428. http://dx.doi.org/10.1093/plankt/24.5.417.
http://dx.doi.org/10.1093/plankt/24.5.41...
; Padisák et al., 2009PADISÁK, J., CROSSETTI, L.O. and NASELLI-FLORES, L. Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia, 2009, 621(1), 1-19. http://dx.doi.org/10.1007/s10750-008-9645-0.
http://dx.doi.org/10.1007/s10750-008-964...
; Borics et al., 2012BORICS, G., TÓTHMÉRÉSZ, B., LUKÁCS, B.A. and VÁRBÍRÓ, G. Functional groups of phytoplankton shaping diversity of shallow lake ecosystems. Hydrobiologia, 2012, 698(1), 251-262. http://dx.doi.org/10.1007/s10750-012-1129-6.
http://dx.doi.org/10.1007/s10750-012-112...
). We do not disregard the possibility that the high contribution of FG LO in the rivers could be related to the influence of the upstream reservoirs in the Paraná and Paranapanema Rivers, as the dispersion of organisms from the reservoir can influence the structure in downstream (Bovo-Scomparin et al., 2013BOVO-SCOMPARIN, V.M., TRAIN, S. and RODRIGUES, L.C. Influence of reservoirs on phytoplankton dispersion and functional traits: a case study in the Upper Paraná River, Brazil. Hydrobiologia, 2013, 702(1), 115-127. http://dx.doi.org/10.1007/s10750-012-1313-8.
http://dx.doi.org/10.1007/s10750-012-131...
).

The same FGs indicators of the trophic state were associated with the type of environment, because of almost all rivers were categorized as oligotrophic and the lakes as mesotrophic. Only lakes (or mesotrophic environments) presented FG indicators. In fact, the FGs indicators of the trophic state that we registered were organisms mostly associated with lentic conditions. Moreover, lakes present large water-retention time that favors the establishment and development of phytoplankters and could explain why more FGs were related to lakes than to rivers (Margalef, 1978MARGALEF, R. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta, 1978, 1(4), 493-509.; Bortolini et al., 2014BORTOLINI, J.C., RODRIGUES, L.C., JATI, S. and TRAIN, S. Phytoplankton functional and morphological groups as indicators of environmental variability in a lateral channel of the Upper Paraná River floodplain. Acta Limnologica Brasiliensia, 2014, 26(1), 98-108. http://dx.doi.org/10.1590/S2179-975X2014000100011.
http://dx.doi.org/10.1590/S2179-975X2014...
; Török et al., 2016TÖRÖK, P., T-KRASZNAI, E., B-BÉRES, V., BÁCSI, I., BORICS, G. and TÓTHMÉRÉSZ, B. Functional diversity supports the biomass-diversity humped-back relationship in phytoplankton assemblages. Functional Ecology, 2016, 30(9), 1593-1602. http://dx.doi.org/10.1111/1365-2435.12631.
http://dx.doi.org/10.1111/1365-2435.1263...
; Moresco et al., 2017MORESCO, G.A., BORTOLINI, J.C., DIAS, J.D., PINEDA, A., JATI, S. and RODRIGUES, L.C. Drivers of phytoplankton richness and diversity components in Neotropical floodplain lakes, from small to large spatial scales. Hydrobiologia, 2017, 799(1), 203-215. http://dx.doi.org/10.1007/s10750-017-3214-3.
http://dx.doi.org/10.1007/s10750-017-321...
).

Some of the FGs indicators of the mesotrophic state have been originally associated with oligotrophic (FGs A and E) or eutrophic (FGs P, C, and J) environments (Reynolds et al., 2002REYNOLDS, C.S., HUSZAR, V., KRUK, C., NASELLI-FLORES, L. and MELO, S. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research, 2002, 24(5), 417-428. http://dx.doi.org/10.1093/plankt/24.5.417.
http://dx.doi.org/10.1093/plankt/24.5.41...
; Padisák et al., 2009PADISÁK, J., CROSSETTI, L.O. and NASELLI-FLORES, L. Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia, 2009, 621(1), 1-19. http://dx.doi.org/10.1007/s10750-008-9645-0.
http://dx.doi.org/10.1007/s10750-008-964...
). Our results suggest that representatives of these FGs exhibit a broader trophic range than thought.

The representatives of the FGs E and W1 can present both autotrophic and heterotrophic nutrition (Alves-de-Souza et al., 2006ALVES-DE-SOUZA, C., MENEZES, M. and HUSZAR, V. Phytoplankton composition and functional groups in a tropical humic coastal lagoon, Brazil. Acta Botanica Brasílica, 2006, 20(3), 701-708. http://dx.doi.org/10.1590/S0102-33062006000300019.
http://dx.doi.org/10.1590/S0102-33062006...
), and their association with the lakes was probably favored by the registered high inorganic material in these environments. In the case of FG A (diatoms related to clear waters), the high biovolume registered in the lakes suggests that light did not limit the phytoplankton development in these environments (Cellamare et al., 2013CELLAMARE, M., PINTO, P. T., LEITÃO, M., COSTE, M., BOUTRY, S. and HAURY, J. Using functional approaches to study phytoplankton communities in a temperate region exposed to tropical species dispersal. Hydrobiologia, 2013, 702(1), 267-282. http://dx.doi.org/10.1007/s10750-012-1330-7.
http://dx.doi.org/10.1007/s10750-012-133...
). The lakes also presented high water-column mixing as suggested by the high biovolume of FGs B, C, and P (diatoms). Species belonging to these groups are good competitors in nutrient-enriched conditions and associated with well-mixing environments (Reynolds, 1998REYNOLDS, C.S. What factors influence the species composition of phytoplankton in lakes of different trophic status? Hydrobiologia, 1998, 369/370, 11-26. http://dx.doi.org/10.1023/A:1017062213207.
http://dx.doi.org/10.1023/A:101706221320...
). These organisms have a siliceous wall and present a high sedimentation rate, and they are dependent on the water mixing to maintain their high biomass (Reynolds et al., 1994REYNOLDS, C.S., DESCY, J.P. and PADISÁK, J. Are phytoplankton dynamics in rivers so different from those in shallow lakes? Hydrobiologia, 1994, 289(1–3), 1-7. http://dx.doi.org/10.1007/BF00007404.
http://dx.doi.org/10.1007/BF00007404...
; Stević et al., 2013STEVIĆ, F., MIHALJEVIĆ, M. and ŠPOLJARIĆ, D. Changes of phytoplankton functional groups in a floodplain lake associated with hydrological perturbations. Hydrobiologia, 2013, 709(1), 143-158. http://dx.doi.org/10.1007/s10750-013-1444-6.
http://dx.doi.org/10.1007/s10750-013-144...
). A high water-column mixing promotes materials resuspension and guarantees the position of phytoplankters in the euphotic zone (Padisák et al., 2010PADISÁK, J., HAJNAL, É., KRIENITZ, L., LAKNER, J. and UVEGES, V. Rarity, ecological memory, rate of floral change in phytoplankton-and the mystery of the Red Cock. Hydrobiologia, 2010, 653(1), 45-64. http://dx.doi.org/10.1007/s10750-010-0344-2.
http://dx.doi.org/10.1007/s10750-010-034...
). Centric diatoms (e.g., FG B - Aulacoseira spp.) are common in rivers and lakes of floodplain (Bovo-Scomparin & Train, 2008BOVO-SCOMPARIN, V.M. and TRAIN, S. Long-term variability of the phytoplankton community in an isolated floodplain lake of the Ivinhema River State Park, Brazil. Hydrobiologia, 2008, 610(1), 331-344. http://dx.doi.org/10.1007/s10750-008-9448-3.
http://dx.doi.org/10.1007/s10750-008-944...
; Borges & Train, 2009BORGES, P.A.F. and TRAIN, S. Phytoplankton diversity in the Upper Paraná River floodplain during two years of drought (2000 and 2001). Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2, 637-647, Supplement. PMid:19738970. http://dx.doi.org/10.1590/S1519-69842009000300018.
http://dx.doi.org/10.1590/S1519-69842009...
) because these organisms are adapted to turbulence and have a life cycle related to the regime of the water-column mixing (Lund, 1965LUND, J.W.G. The ecology of the freshwater phytoplankton. Biological Reviews of the Cambridge Philosophical Society, 1965, 40(2), 231-290. http://dx.doi.org/10.1111/j.1469-185X.1965.tb00803.x.
http://dx.doi.org/10.1111/j.1469-185X.19...
).

Although rivers and lakes presented particular physical, chemical, and biological differences, only the lakes presented FG indicators. Determine patterns of phytoplankton distribution may be difficult because microorganisms distribution is strongly influenced by dispersal stochasticity (Nabout et al., 2009NABOUT, J.C., SIQUEIRA, T., BINI, L.M. and NOGUEIRA, I. de S. No evidence for environmental and spatial processes in structuring phytoplankton communities. Acta Oecologica, 2009, 35(5), 720-726. http://dx.doi.org/10.1016/j.actao.2009.07.002.
http://dx.doi.org/10.1016/j.actao.2009.0...
). The species-environment relationship (FGs as indicators) was clearer in the lakes, probably because of the longer water retention that allows evidencing the response of the phytoplankton community to environmental factors (Rodrigues et al., 2017RODRIGUES, L.C., PIVATO, B.M., VIEIRA, L.C.G., BOVO-SCOMPARIN, V.M., BORTOLINI, J.C., PINEDA, A. and TRAIN, S. Use of phytoplankton functional groups as a model of spatial and temporal patterns in reservoirs: a case study in a reservoir of central Brazil. Hydrobiologia, 2017. In press. http://dx.doi.org/10.1007/s10750-017-3289-x.
http://dx.doi.org/10.1007/s10750-017-328...
). In rivers, phytoplankton is especially affected by stochastic processes associated to flow and flood pulse (Thorp, 2010THORP, J.H. Models of ecological processes in riverine ecosystems. In: G.E. LIKENS, ed. River ecosystem ecology. San Diego: Academic Press, 2010, pp. 212-219.). In this sense, the absence of FGs as indicators in the rivers was probably due to the high water flow that promotes dispersal stochasticity and prevents to determine the relationship between the environmental conditions and the phytoplankton distribution (Rodrigues et al., 2017RODRIGUES, L.C., PIVATO, B.M., VIEIRA, L.C.G., BOVO-SCOMPARIN, V.M., BORTOLINI, J.C., PINEDA, A. and TRAIN, S. Use of phytoplankton functional groups as a model of spatial and temporal patterns in reservoirs: a case study in a reservoir of central Brazil. Hydrobiologia, 2017. In press. http://dx.doi.org/10.1007/s10750-017-3289-x.
http://dx.doi.org/10.1007/s10750-017-328...
). Moreover, the hydrodynamics of the rivers difficult the phytoplankton establishment because of the wash-out that increases the biovolume losses (Abonyi et al., 2012ABONYI, A., LEITÃO, M., LANÇON, A.M. and PADISÁK, J. Phytoplankton functional groups as indicators of human impacts along the River Loire (France). Hydrobiologia, 2012, 698(1), 233-249. http://dx.doi.org/10.1007/s10750-012-1130-0.
http://dx.doi.org/10.1007/s10750-012-113...
; Stanković et al., 2012STANKOVIĆ, I., VLAHOVIĆ, T., GLIGORA UDOVIČ, M., VÁRBÍRÓ, G. and BORICS, G. Phytoplankton functional and morpho-functional approach in large floodplain rivers. Hydrobiologia, 2012, 698(1), 217-231. http://dx.doi.org/10.1007/s10750-012-1148-3.
http://dx.doi.org/10.1007/s10750-012-114...
; Devercelli & O’Farrell, 2013DEVERCELLI, M. and O’FARRELL, I. Factors affecting the structure and maintenance of phytoplankton functional groups in a nutrient rich lowland river. Limnologica, 2013, 43(2), 67-78. http://dx.doi.org/10.1016/j.limno.2012.05.001.
http://dx.doi.org/10.1016/j.limno.2012.0...
; Fraisse et al., 2013FRAISSE, S., BORMANS, M. and LAGADEUC, Y. Morphofunctional traits reflect differences in phytoplankton community between rivers of contrasting flow regime. Aquatic Ecology, 2013, 47(3), 315-327. http://dx.doi.org/10.1007/s10452-013-9446-z.
http://dx.doi.org/10.1007/s10452-013-944...
). This study demonstrated that the use of phytoplankton FGs is an alternative to obtain ecological and environments responses in the floodplain since the FGs were efficient indicators of hydrological periods and the environmental conditions in lakes and rivers.

Acknowledgements

The authors are grateful to Coordination of Personal Improvement of Superior Education (Coordenação de Aperfeiçoamento Pessoal de Nível Superior – CAPES) and Council of Research and Development (Conselho Nacional de Pesquisa e Desenvolvimento – CNPq) for providing pos-graduate scholarship and the resources which contributed to realizing this research and Nupelia (Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura) for logistic support and the physical and chemical laboratory of water for data supply.

  • Cite as: Zanco, B.F. et al. Phytoplankton functional groups indicators of environmental conditions in floodplain rivers and lakes of the Paraná Basin. Acta Limnologica Brasiliensia, 2017, vol. 29, e119.

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Publication Dates

  • Publication in this collection
    2017

History

  • Received
    15 June 2017
  • Accepted
    10 Nov 2017
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