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Periphytic community structure of Ostracoda (Crustacea) in the river-floodplain system of the Upper Paraná River

Estrutura da comunidade de Ostracoda (Crustacea) perifíticos no sistema rio-planície de inundação do alto rio Paraná

Abstracts

Abstract

Aim: We assessed the effect of environmental factors on the structure of periphytic ostracods communities along the river-floodplain system of the Upper Paraná River. We predict that the higher distance from Porto Primavera dam downstream would lead to higher diversity and density of the ostracods.

Methods

Periphytic ostracods (associated with root systems of the floating Eichhornia spp) were sampled during November 2013 to May 2015. Three samples were collected at each sampling site (channel of the Paraná River, tributaries and lakes). Eichhornia plants were removed from the water by hand and the plants were placed in a plastic bucket. Roots were washed for the removal of ostracods, and samples were filtered through a hand net with 160 µm mesh size.

Results

The faunistic survey recorded 44 ostracods species and richness estimators indicated that sampling effort appears to be suitable to reveal the diversity of ostracods in this studied area. The highest richness and density were observed in the stretch downstream of the dam in the main channel of Paraná River and in the lakes. Beta diversity was not significantly different along the longitudinal gradient downstream and higher similarity of ostracods species composition was observed in the lakes located in the stretch downstream of the dam.

Conclusions

An increase in the richness and density of ostracods were recorded in the sections downstream of the Paraná River, evidencing the importance of undammed tributaries on the ostracods community. The similarity of beta diversity amongst sampling sites may be owing to permanent hydrological connectivity amongst these environments, favouring the exchange of organisms mainly through the drift of free-floating macrophytes, and owing to the passive dispersal of drought resistant eggs of ostracods. Local abiotic factors had significant effects on abundance and distribution of some ostracod species.

Keywords:
microcrustaceans; macrophytes; regulated river; oligotrophication; connected lakes


Resumo

Objetivo: Avaliou-se o efeito dos fatores ambientais sobre a estrutura da comunidade de ostrácodes perifíticos ao longo do sistema rio-planície de inundação do alto rio Paraná. Foi predito que quanto maior a distância a jusante da barragem de Porto Primavera, maior a diversidade e densidade de ostrácodes.

Métodos

Ostrácodes perifíticos (associados aos sistemas radiculares da macrófita flutuante Eichhornia spp) foram amostrados durante novembro de 2013 a maio de 2015. Três amostras foram coletadas em cada ponto de amostragem (canal principal do rio Paraná, tributários e lagoas). Plantas de Eichhornia foram removidas da água manualmente e colocadas em balde plástico. As raízes foram lavadas para a remoção dos ostrácodes, e as amostras foram filtradas através de uma rede de mão de 160 µm de abertura de malha.

Resultados

O levantamento faunístico registrou 44 espécies de ostrácodes e os estimadores de riqueza indicaram que o esforço amostral pareceu ser adequado para revelar a diversidade de ostrácodes nesta área de estudo. A maior riqueza e densidade foram observadas no trecho a jusante da barragem no canal principal do rio Paraná e nas lagoas. A diversidade beta não foi significativamente diferente ao longo do gradiente longitudinal a jusante e a maior similaridade na composição de espécies de ostrácodes foi observada nas lagoas localizadas no trecho a jusante da barragem.

Conclusões

Um aumento na riqueza e densidade de ostrácodes foram registrados nas seções do rio Paraná, a jusante da barragem, evidenciando a importância dos tributários não represados sobre alguns atributos da comunidade de ostrácodes. A similaridade da diversidade beta entre os pontos de amostragem pode ser devido à permanente conectividade hidrológica entre estes ambientes, favorecendo a troca de organismos principalmente através da deriva de macrófitas flutuantes livres, e devido a dispersão passiva dos ovos de ostrácodes resistentes a seca. Os fatores abióticos locais tiveram efeitos significativos sobre a abundância e distribuição de algumas espécies de ostrácodes.

Palavras-chave:
microcrustáceos; macrófitas; rio regulado; oligotrofização; lagoas conectadas


1. Introduction

River-floodplain systems include both lentic and lotic habitats, such as rivers, canals, tributaries, permanently connected and isolated lakes (Thomaz et al., 2004THOMAZ, S.M., PAGIORO, T.A., BINI, L.M., ROBERTO, M.C. and ROCHA, R.R.A. Limnological characterization of the aquatic environments and the influence of hydrometric levels. In: S.M. THOMAZ, A.A. AGOSTINHO and N.S. HAHN, eds. The Upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers, 2004, pp. 75-102.; Higuti et al., 2010HIGUTI, J., DECLERCK, S.A.J., LANSAC-TÔHA, F.A., VELHO, L.F.M. and MARTENS, K. Variation in ostracod (Crustacea, Ostracoda) communities in the alluvial valley of the upper Paraná River (Brazil) in relation to substrate. Hydrobiologia, 2010, 644(2), 261-278. http://dx.doi.org/10.1007/s10750-010-0122-1.
http://dx.doi.org/10.1007/s10750-010-012...
). The degree of connectivity between these environments and their hydrological dynamics maintain the integrity of the environments and their ecosystems (Poff et al., 1997POFF, L., ALLAN, J.D., BAIN, M.B., KARR, J.R., PRESTEGAARD, K.L., RICHTER, B.D., SPARKS, R.E. and STROMBERG, J.C. The natural Flow regime. Bioscience, 1997, 47(11), 769-784. http://dx.doi.org/10.2307/1313099.
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; Wantzen et al., 2008WANTZEN, K.M., YULE, C.M., TOCKNER, T. and JUNK, W.G. Riparian wetlands of tropical streams. In: D. DUDGEON, ed. Tropical stream ecology. London: Academic Press, 2008, pp. 199-217.).

One of the threats to global freshwater biodiversity is modification of water flow regime, caused by the construction of dams and the resulting human control of discharges of water for hydroelectric power production (Dudgeon et al., 2006DUDGEON, D., ARTHINGTON, A.H., GESSNER, M.O., KAWABATA, Z.I., KNOWLER, D., LÉVEQUÊ, C., NAIMAN, R.J., PRIEUR-RICHARD, A.H., SOTO, D., STIASSNY, M.L. and SULLIVAN, C.A. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews of the Cambridge Philosophical Society, 2006, 81(2), 163-182. PMid:16336747. http://dx.doi.org/10.1017/S1464793105006950.
http://dx.doi.org/10.1017/S1464793105006...
).The construction of several reservoirs along a river (named “reservoirs in cascade”), might intensify the retention of sediment, organic matter and nutrients, turning the river water into an oligotrophic state downstream of the dam (Roberto et al., 2009ROBERTO, M.C., SANTANA, N.F. and THOMAZ, S.M. Limnology in the Upper Parana River Floodplain: large-scale spatial and temporal pattern, and the influence of reservoirs. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2, Suppl), 717-725. PMid:19738977. http://dx.doi.org/10.1590/S1519-69842009000300025.
http://dx.doi.org/10.1590/S1519-69842009...
; Vörösmarty et al., 2003VÖRÖSMARTY, C.J., MEYBECK, M., FEKETE, B., SHARMA, K., GREEN, P. and SYVITSKI, J.P. Anthropogenic sediment retention: major global impact from registered river impoundments. Global and Planetary Change, 2003, 39(1), 169-190. http://dx.doi.org/10.1016/S0921-8181(03)00023-7.
http://dx.doi.org/10.1016/S0921-8181(03)...
), and leading to discontinuity in physical, chemical and biological characteristics (Ward & Stanford, 1995WARD, J.V. and STANFORD, J.A. The serial discontinuity concept: extending the model to floodplain rivers. Regulated Rivers: Research and Management, 1995, 10(2-4), 159-168. http://dx.doi.org/10.1002/rrr.3450100211.
http://dx.doi.org/10.1002/rrr.3450100211...
; Vannote et al., 1980VANNOTE, R.L., MINSHALL, G.W., CUMMINS, K.W., SEDELL, J.R. and CUSHING, C.E. The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences, 1980, 37(1), 130-137. http://dx.doi.org/10.1139/f80-017.
http://dx.doi.org/10.1139/f80-017...
). These effects can change the structure of aquatic communities, e.g. of macrophytes (Schwarz & Hawes, 1997SCHWARZ, A.M. and HAWES, I. Effects of changing water clarity on characean biomass and species composition in a large oligotrophic lake. Aquatic Botany, 1997, 56(3-4), 169-181. http://dx.doi.org/10.1016/S0304-3770(96)01114-X.
http://dx.doi.org/10.1016/S0304-3770(96)...
), macroinvertebrates (King & Richardson, 2007KING, R.S. and RICHARDSON, C.J. Subsidy-stress response of macroinvertebrate community biomass to a phosphorus gradient in an oligotrophic wetland ecosystem. Journal of the North American Benthological Society, 2007, 26(3), 491-508. http://dx.doi.org/10.1899/06-002R.1.
http://dx.doi.org/10.1899/06-002R.1...
) as well as the biomass of phytoplankton, zooplankton and of fish (Jeppesen et al., 2002JEPPESEN, E., JENSEN, J.P. and SONDERGAARD, M. Response of phytoplankton, zooplankton, and fish to re-oligotrophication: an 11 year study of 23 Danish lakes. Aquatic Ecosystem Health & Management, 2002, 5(1), 31-43. http://dx.doi.org/10.1080/14634980260199945.
http://dx.doi.org/10.1080/14634980260199...
).

Ostracods are small bivalved crustaceans (0.3-5.0 mm) with a calcified carapace. They can be found in most inland water bodies, where they abound in the benthic and aquatic vegetation (periphytic animal) communities (Martens & Behen, 1994MARTENS, K. and BEHEN, F. A checklist of the recent non-marine ostracods (Crustacea, Ostracoda) from the inland waters of South America and adjacent islands. Travaux Scientifiques Du Musée National d’Histoire Naturelle Du Luxembourg, 1994, 22, 1-83.; Martens et al., 2008MARTENS, K., SCHÖN, I., MEISCH, C. and HORNE, D.J. Global diversity of ostracods (Ostracoda, Crustacea) in freshwater. Hydrobiologia, 2008, 595(1), 185-193. http://dx.doi.org/10.1007/s10750-007-9245-4.
http://dx.doi.org/10.1007/s10750-007-924...
).

Aquatic macrophytes are important biotopes for ostracods, which use this microhabitat for breeding, feeding and protection against predators (Higuti et al., 2007HIGUTI, J., VELHO, L.F.M., LANSAC-TÔHA, F.A. and MARTENS, K. Pleuston communities are buffered from regional flood pulses: The example of ostracods in the Paraná River floodplain, Brazil. Freshwater Biology, 2007, 52(10), 1930-1943. http://dx.doi.org/10.1111/j.1365-2427.2007.01821.x.
http://dx.doi.org/10.1111/j.1365-2427.20...
, 2010HIGUTI, J., DECLERCK, S.A.J., LANSAC-TÔHA, F.A., VELHO, L.F.M. and MARTENS, K. Variation in ostracod (Crustacea, Ostracoda) communities in the alluvial valley of the upper Paraná River (Brazil) in relation to substrate. Hydrobiologia, 2010, 644(2), 261-278. http://dx.doi.org/10.1007/s10750-010-0122-1.
http://dx.doi.org/10.1007/s10750-010-012...
; Liberto et al., 2012LIBERTO, R., MESQUITA-JOANES, F. and CÉSAR, I. Dynamics of pleustonic ostracod populations in small ponds on the Island of Martín García (Rio de la Plata, Argentina). Hydrobiologia, 2012, 688(1), 47-61. http://dx.doi.org/10.1007/s10750-011-0600-0.
http://dx.doi.org/10.1007/s10750-011-060...
; Szlauer‐Łukaszewska, 2012SZLAUER‐ŁUKASZEWSKA, A. Ostracod assemblages in relation to littoral plant communities of a shallow lake (Lake Świdwie, Poland). International Review of Hydrobiology, 2012, 97(4), 262-275. http://dx.doi.org/10.1002/iroh.201111491.
http://dx.doi.org/10.1002/iroh.201111491...
; Higuti & Martens, 2016HIGUTI, J. and MARTENS, K. Invasive South American floating plants are a successful substrate for native Central African pleuston. Biological Invasions, 2016, 18(4), 1191-1201. http://dx.doi.org/10.1007/s10530-016-1061-1.
http://dx.doi.org/10.1007/s10530-016-106...
; Matsuda et al., 2015MATSUDA, J.T., LANSAC-TÔHA, F.A., MARTENS, K., VELHO, L.F.M., MORMUL, R.P. and HIGUTI, J. Association of body size and behavior of freshwater ostracods (Crustacea, Ostracoda) with aquatic macrophytes. Aquatic Ecology, 2015, 2015(49), 321-331. http://dx.doi.org/10.1007/s10452-015-9527-2.
http://dx.doi.org/10.1007/s10452-015-952...
; Pereira et al., 2017PEREIRA, L.C., LANSAC-TÔHA, F.A., MARTENS, K. and HIGUTI, J. Biodiversity of ostracod communities (Crustacea, Ostracoda) in a tropical floodplain. Inland Waters, 2017, 7(3), 323-332. http://dx.doi.org/10.1080/20442041.2017.1329913.
http://dx.doi.org/10.1080/20442041.2017....
).

Several studies have evaluated the effects of environmental factors on diversity, abundance and distribution of ostracod species in different aquatic ecosystems. The positive correlation of temperature, pH and dissolved oxygen with ostracods abundance was evidenced by Nagorskaya & Keyser (2005)NAGORSKAYA, L. and KEYSER, D. Habitat diversity and ostracod distribution patterns in Belarus. Hydrobiologia, 2005, 538(1-3), 167-178. http://dx.doi.org/10.1007/s10750-004-4959-z.
http://dx.doi.org/10.1007/s10750-004-495...
, whereas oxygen content and variables related with substratum and discharge showed negative influence on ostracod presence, abundance and species richness at a local scale (Poquet & Mesquita-Joanes, 2011POQUET, J.M. and MESQUITA-JOANES, F. Combined effects of local environment and continental biogeography on the distribution of Ostracoda. Freshwater Biology, 2011, 56(3), 448-469. http://dx.doi.org/10.1111/j.1365-2427.2010.02511.x.
http://dx.doi.org/10.1111/j.1365-2427.20...
). Besides the effect of the abiotic variables, also the presence and coverage of the vegetation can have significant effects on the distribution and abundance of ostracod species (Kiss, 2007KISS, A. Factors affecting spatial and temporal distribution of Ostracoda assemblages in different macrophyte habitats of a shallow lake (Lake Fehér, Hungary). Hydrobiologia, 2007, 585(1), 89-98. http://dx.doi.org/10.1007/s10750-007-0631-8.
http://dx.doi.org/10.1007/s10750-007-063...
), while the structural complexity of aquatic macrophytes might be an important determining factor for ostracod community composition (Matsuda et al., 2015MATSUDA, J.T., LANSAC-TÔHA, F.A., MARTENS, K., VELHO, L.F.M., MORMUL, R.P. and HIGUTI, J. Association of body size and behavior of freshwater ostracods (Crustacea, Ostracoda) with aquatic macrophytes. Aquatic Ecology, 2015, 2015(49), 321-331. http://dx.doi.org/10.1007/s10452-015-9527-2.
http://dx.doi.org/10.1007/s10452-015-952...
).

Here, we assessed the effect of environmental factors on periphytic ostracod communities along the river-floodplain system of the Upper Paraná River. According to the Concept of Serial Discontinuity, tributaries are responsible for the addition of nutrients to the main river, contributing to the recovery of environments previous under oligotrophic conditions (Stanford & Ward, 2001STANFORD, J.A. and WARD, J.V. Revisiting the serial discontinuity concept. Regulated Rivers: Research and Management, 2001, 17(4-5), 303-310. http://dx.doi.org/10.1002/rrr.659.
http://dx.doi.org/10.1002/rrr.659...
). We hypothesize that ostracod communities will show higher diversities and densities, the further downstream they occur from the Porto Primavera dam.

2. Material and Methods

2.1. Study area

The Paraná River is formed by the junction of the rivers Grande and Paranaíba in South-central Brazil. The first third part of this basin is named Upper Paraná River and most of it runs inside the Brazilian territory. The Upper Paraná River presented an extensive floodplain on its west side, which is 230 km long and more than 20 km wide between the Porto Primavera Dam and the beginning of the Itaipu Reservoir. This represents the only extensive dam-free stretch of the Paraná River in Brazilian territory (Agostinho et al., 2004aAGOSTINHO, 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.A. AGOSTINHO and N.S. HAHN, eds. The Upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers, 2004a, pp. 381-393.). In this area, three conservation units were created: “Área de Proteção Ambiental das Ilhas e Várzeas do Rio Paraná” (Environmental Protection Area), the “Parque Nacional de Ilha Grande” (National Park), and the “Parque Estadual do Ivinheima” (State Park) (Agostinho & Zalewski, 1996AGOSTINHO, A.A. and ZALEWSKI, M. A planície de alagável do Alto Rio Paraná: importância e preservação. Maringá: EDUEM, 1996.; Agostinho et al., 2004aAGOSTINHO, 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.A. AGOSTINHO and N.S. HAHN, eds. The Upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers, 2004a, pp. 381-393.).

The study area is a river-floodplain system, which encompasses the main river (Paraná River), and several secondary rivers (named here tributaries), as well as connecting channels, isolated and connected lakes. We selected eight sampling points in the Paraná River (P1 to P8, distributed on the left (P1, P3, P6, P7) and right (P2, P4, P5, P8) banks of the Paraná River), four tributaries (P9: Baía, P10 and P11: Ivinhema, P12: Amambaí and P13: Iguatemi Rivers) and seven permanently connected lakes (P14: Garças, P15: Xirica, P16: Pombas, P17: Ivaí, P18: São João, P19: Pavão and P20: Saraiva) (Figure 1).

Figure 1
Sampling sites in the Paraná River (1-8), tributaries (9-13) and lakes (14-20) in the river-floodplain system of the Upper Paraná River. Locality codes are the same as shown in Table 1.

2.2. Sampling and laboratory analysis

Periphytic ostracods (associated with aquatic macrophytes, Eichhornia crassipes (Mart.) Solms and E. azurea (Swartz) Kunth were sampled between November 2013 and May 2015, totaling 7 collections in the dam-free stretch of the Upper Paraná River. In the upper section of the Paraná River (near the Porto Primavera Dam) there are no fixed and free floating aquatic macrophytes, only submerged plants. Therefore, ostracods associated with Eichhornia were sampled only in the lower section of the Paraná River. All the tributaries selected are located on the left bank (west side) of the Paraná River, because no fixed or free floating aquatic macrophytes were found in the tributaries of the right bank (east side) of the Paraná River during the whole collection period. The entire sampling period was characterized as dry hydrological period.

Three samples were collected at each sampling site (points of Paraná River, tributaries, lakes). Individual Eichhornia plants were removed from the water by hand and were immediately placed in a plastic bucket (Campos et al., 2017CAMPOS, R., CONCEIÇÃO, E.O., PINTO, M.B., BERTONCIN, A.P.S., HIGUTI, J. and MARTENS, K. Evaluation of quantitative sampling methods in pleuston an example from ostracod communities. Limnologica, 2017, 63, 36-41. http://dx.doi.org/10.1016/j.limno.2017.01.002.
http://dx.doi.org/10.1016/j.limno.2017.0...
). The roots were washed in the bucket itself for the removal of ostracods (and other animals) and the sample was thoroughly washed through a hand net with 160 µm mesh size. The samples were preserved in 70° ethanol. The roots were stored in plastic bags, previously labelled and subsequently dried and weighted in the lab. The emerging parts of the plants were disguarded.

The ostracod samples were divided with the Folsom fractionator. ¼ of the samples were quantified and the remaining 3/4 were used to identify species that were absent from the first sub-sample. Ostracods were sorted under a stereoscopic microscope and the organisms were identified following Martens & Behen (1994)MARTENS, K. and BEHEN, F. A checklist of the recent non-marine ostracods (Crustacea, Ostracoda) from the inland waters of South America and adjacent islands. Travaux Scientifiques Du Musée National d’Histoire Naturelle Du Luxembourg, 1994, 22, 1-83. and articles comprised therein, Rossetti & Martens (1998)ROSSETTI, G. and MARTENS, K. Taxonomic revision of the Recent and Holocene representatives of the Family Darwinulidae (Crustacea, Ostracoda), with a description of three new genera. Bulletin - Institut royal des sciences naturelles de Belgique. Biologie, 1998, 68, 55-110., Higuti & Martens (2012aHIGUTI, J. and MARTENS, K. Description of new genus and species of new genus and species of Candonopsini (Crustacea, Ostracoda, Candoninae) from the alluvial valley of the Upper Paranpa River (Brazil, South America). European Journal of Taxonomy, 2012a, 33, 1-31., bHIGUTI, J. and MARTENS, K. On a new cypridopsine genus (Crustacea, Ostracoda, Cyprididae) from the Upper Paraná River Floodplain (Brazil). Zootaxa, 2012b, 3391, 23-38., 2014HIGUTI, J. and MARTENS, K. Five new species of Candoninae (Crustacea, Ostracoda) from the alluvial valley of the Upper Paraná River (Brazil, South America). European Journal of Taxonomy, 2014, 106, 1-36.), Higuti et al. (2013)HIGUTI, J., SCHÖN, I., AUDENAERT, L. and MARTENS, K. On the Strandesia obtusata/elliptica lineage (Ostracoda, Cyprididae) in the alluvial valley of the Paraná River (Brazil), with the description of three new species. Crustaceana, 2013, 86, 182-211. http://dx.doi.org/10.1163/15685403-00003160.
http://dx.doi.org/10.1163/15685403-00003...
.

In order to assess the abiotic environment, several chemical and physical variables were measured in the field, such as water temperature (°C) and dissolved oxygen (mg.L-1) (both using YSI oximeter 550A), pH and electrical conductivity (µS.cm-1) (both using YSI multiparameter 63) and turbidity (NTU, using turbidimeter). Alkalinity (µg.L-1), total nitrogen (µg L-1) and total phosphorus (µg L-1) were determined according to methods proposed by Mackereth et al. (1978)MACKERETH, F.J.H., HERON, J. and TALLING, J.F. Water analysis: some revised methods for limnologists. Freshwater Biological Association, 1978, 36, 117. in the Laboratory of Limnology of Nupelia from the State University of Maringá.

2.3. Data analysis

Ostracod densities were calculated as the number of individuals per gram of root dry mass (ind g-1 DW). Three estimators were used to describe values of species richness, in order to evaluate whether observed species richness in the present survey is representative of the total ostracod diversity for the dam-free stretch of the upper Paraná River. These estimators were Chao 1, Jackknife 1 (first order) and Bootstrap. The first one is based on species abundance and the other two species richness estimators are based on species incidence.

The environmental heterogeneity and beta diversity were analyzed through the Multivariate Permutational dispersion test (PERMDISP, Anderson et al., 2006ANDERSON, M.J., ELLINGSEN, K.E. and MCARDLE, B.H. Multivariate dispersion as a measure of beta diversity. Ecology Letters, 2006, 9(6), 683-693. PMid:16706913. http://dx.doi.org/10.1111/j.1461-0248.2006.00926.x.
http://dx.doi.org/10.1111/j.1461-0248.20...
) in each sampling sites of Paraná River, tributaries and lakes. Environmental heterogeneity was defined from the Euclidean distance of limnological variables (water temperature, dissolved oxygen, pH, electrical conductivity, turbidity, alkalinity, total nitrogen and total phosphorus). To evaluate species composition variability (beta diversity) we used a data matrix of presence / absence of the ostracod species. PERMDISP calculates a centroid for each sampling sites, based on Jaccard distance. The test is based on the mean distance between the environmental variables (environmental heterogeneity) and their centroid group using a dissimilarity measure, within a dimensional space calculated through Principal Coordinate Analysis (PCoA, Legendre & Legendre, 1998LEGENDRE, P. and LEGENDRE, L. Numerical ecology. Amsterdam: Elsevier Science, 1998.). The same protocol was used to species composition (beta diversity). The higher average distance to the centroid corresponds to a higher environmental heterogeneity and higher dissimilarity in ostracod species composition. PERMDISP uses a 999 permutations ANOVA to test for significant differences (p <0.05).

Rarefaction curves were performed according to the number of individuals, in order to compare the species richness amongst the sampling sites at comparable levels of density (Gotelli & Colwell, 2001GOTELLI, N.J. and COLWELL, R.K. Quantifyninf biodiversity: procedures and pitfalls in the measurement and comparasion of species richness. Ecology Letters, 2001, 4(4), 379-391. http://dx.doi.org/10.1046/j.1461-0248.2001.00230.x.
http://dx.doi.org/10.1046/j.1461-0248.20...
).

A parametric analysis of variance (ANOVA) was performed to test for significance of differences in species richness, density, beta diversity and environmental heterogeneity amongst sampling sites in the Paraná River, tributaries and lakes. When the normality and homogeneity assumption required for ANOVA was not fulfilled, a non-parametric Kruskal-Wallis test was used. In case of significant differences; a Tukey test was performed a posteriori.

We performed a Redundancy Analysis - RDA (Legendre & Legendre, 1998LEGENDRE, P. and LEGENDRE, L. Numerical ecology. Amsterdam: Elsevier Science, 1998.) to evaluate the relationships between environmental variables and ostracod communities. This method is considered an extension of PCA, since the main axes are constrained to be linear combinations of the environmental variables. Multiple linear regressions of the ordination scores against environmental variables are then used to examine the relationship between community structure and the set of explanatory variables (Ramette, 2007RAMETTE, A. Multivariate analyses in microbial ecology. FEMS Microbiology Ecology, 2007, 62(2), 142-160. PMid:17892477. http://dx.doi.org/10.1111/j.1574-6941.2007.00375.x.
http://dx.doi.org/10.1111/j.1574-6941.20...
). Significance was determined by 999 permutations. The model was selected with the environmental variables that best predict the characteristics of the community-using step forward (Blanchet et al., 2008BLANCHET, F.G., LEGENDRE, P. and BORCARD, D. Forward selection of explanatory variables. Ecology, 2008, 89(9), 2623-2632. PMid:18831183. http://dx.doi.org/10.1890/07-0986.1.
http://dx.doi.org/10.1890/07-0986.1...
).

Richness estimators, PCoA, PERMDISP and RDA were performed in the software R 3.2.4 (R Development Core Team, 2013R DEVELOPMENT CORE TEAM. R: a language and environment for statistical computing [online]. Vienna: R Foundation for Statistical Computing, 2013 [viewed 20 Sep. 2017]. Available from: http:// www.R-project.org
http:// www.R-project.org...
) using the BiodiversityR (Kindt & Coe, 2005KINDT, R. and COE, R. Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. Nairobi: World Agroforestry Centre, ICRAF, 2005. 196 p.), vegan (Oksanen et al., 2017OKSANEN, J., BLANCHET, G.F., FRIENDLY, M., KINDIT, R., LEGENDRE, P., MCGLINN, D., MINCHIN, P.R.O., O’HARA, R.N., SIMPSON, G.L., SOLYMOS, P., STEVENS, M.H.H., SZOECS, E. and WAGNER, H. Vegan: community ecology package. R package version 2.4-0 [online]. 2017 [viewed 20 Sep. 2017]. Available from: https://CRAN.R-project.org/package=vegan
https://CRAN.R-project.org/package=vegan...
) and permute packages (Simpson, 2017SIMPSON, G.L. Permute: functions for generating restricted permutations of data [online]. R Package, version 0.7-0, 2017 [viewed 20 Sep. 2017]. Available from: http://cran.rproject.org/package=permute
http://cran.rproject.org/package=permute...
). Analyses of variance and Tukey test were performed in Statistica 7.1 (Statsoft Inc., 2005STATSOFT INC. Statistica for Windows: data analysis software system. Version 7.1 [software]. Tulsa: Statsoft Inc., 2005 [viewed 20 Sep. 2017]. Available from: www.statsoft.com
www.statsoft.com...
).

3. Results

3.1. Abiotic variables and environmental heterogeneity

In general, an increase in turbidity and nutrient enrichment (nitrogen and phosphorus) and a decrease in pH were observed along the longitudinal downstream gradient of the Paraná River. Lower values of electrical conductivity were recorded in the tributaries, and more turbid waters in the Amambaí and Iguatemi rivers. Waters that are more alkaline, higher nutrient contents and lower dissolved oxygen concentrations were found in the lakes (Table 1).

Table 1
Mean and standard deviation of the abiotic variables and type of substrate in the river-floodplain system of the Upper Paraná River.

The Paraná River and lakes were the most heterogenous environments. A trend in increasing environmental heterogeneity was observed downstream in the Paraná River and in the lakes. No significant differences were recorded amongst the sampling points of the Paraná River. The tributaries differed significantly (F = 3.38, p = 0.01) between Ivinhema (IV1) and Iguatemi, and significant differences were also found between the lakes Pavão and Pombas (F = 2.84, p = 0.01 - Figure 2)

Figure 2
Mean values, deviation and standard error of environmental heterogeneity of the sampling sites in the river-floodplain system of the Upper Paraná River.

3.2. Composition, diversity and density of ostracod communities

We recorded 44 species of ostracods associated with E. crassipes and E. azurea, between November 2013 and May 2015 in the dam-free stretch of the Upper Paraná River, between Porto Primavera and Itaipu reservoirs. The ostracod communities comprised five families: Cyprididae, Candonidae, Limnocytheridae, Ilyocyprididae and Darwinulidae. The family Ilyocyprididae was recorded for the first time in the Upper Paraná River, in addition, several new species of ostracods were found (see Table 2). Of the 44 species, 31 occurred in the Paraná River, 27 in the tributaries and 40 in the permanently connected lakes (Table 2). The most frequent species were Cypricercus centrura (Klie, 1940) and Stenocypris malayica Victor & Fernando, 1981 in the river-floodplain system of the Upper Paraná River. Diaphanocypris meridana (Furtos, 1936) and C. centrura were the most abundant species in Paraná River and lakes, apart from the high abundance of Bradleytriebella lineata (Victor & Fernando, 1981) in the lakes. Cypretta costata (G. W. Müller, 1898) and Cytheridella ilosvayi (Daday, 1905) were the most abundant species in the tributaries.

Table 2
Mean values of ostracod species density of the sampling sites (P1 to P8) of the Paraná River, tributaries and lakes.

Species richness estimations were higher than the observed result (44 species), however, values of estimated richness were very close to observed richness. The bootstrap estimations approached the observed species richness most closely (Figure 3).

Figure 3
Accumulation curves of ostracods species resulting from different species richness estimators in the river-floodplain system of the Upper Paraná River.

The variation of richness and density of ostracods in different sampling sites (Paraná River, tributaries and lakes) is shown in Figure 4. Higher values of richness and density were recorded in lentic environments (lakes) followed by the lotic environments (rivers). In the main river we observed an increase in the values of both attributes according to the river longitudinal gradient from the upper to lower sections on the left (P1, P3, P6, P7) and right (P2, P4, P5, P8) banks of the Paraná River. Significant differences (H = 28.02, p = 0.000) were found for richness, mainly amongst sampling sites located in the upper (P2, P4) and lower (P8) sections of the right bank of the Paraná River, and. between the sampling points P6 and P7 on the left bank of the river (H = 13.30, p = 0.004). Density of ostracods differed significant (H = 13.33, p = 0.004) between points P2 and P8 on the right bank of the Paraná River.

Figure 4
Mean values, deviation and standard error of richness and density of ostracods in (A, B) Paraná River, (C, D) tributaries and (E, F) lakes in the river-floodplain system of the Upper Paraná River.

On the other hand, richness and density were higher in the tributaries located in an upstream stretch of the Paraná River (Baía and Ivinhema (IV1 and IV2) rivers), when compared to the tributaries located further downstream (Amambaí and Iguatemi rivers) of the Paraná River. Significant differences were observed for richness (H = 14.63, p = 0.005) and density (H = 20.70, p = 0.000) between Iguatemi and Baía, and Iguatemi and Ivinhema (IV2).

Lower ostracod species richness was recorded in the lake Garças, Xirica and Pombas, while higher ostracod densities were found in the lakes Pombas (floodplain), Ivaí and Saraiva (downstream stretch of the Paraná River). Significant differences (H = 64.97, p = 0.000) were found only for ostracod species richness between the lakes Ivaí and Garças, Xirica, Pombas, São João, between Pavão and Garças, Xirica, Pombas, São João, and between Garças and Saraiva lakes.

The rarefaction curves showed that ostracod richness reached an asymptote in the sampling sites of Paraná River, tributaries and lakes. Higher numbers of ostracod species were recorded in the lakes, while species richness in the Paraná River and tributary sites were similar.

Beta diversities were similar in the Paraná River and no significant differences were observed amongst the sampling points. Higher diversities were recorded in the Iguatemi River, and significant differences (F = 2.736, p = 0.033) were found between Iguatemi and Baía rivers. Higher beta diversities were recorded in lakes Garças and Xirica, located in the upstream stretch of the Paraná River (floodplain), which differed (F = 7.70, p = 0.000) than in lakes Ivaí and Saraiva, which are located in the downstream stretch of the Paraná River (Figure 5).

Figure 5
Mean values, deviation and standard error of beta diversity of ostracods in (A) Paraná River, (B) tributaries and (C) lakes in the river-floodplain system of the Upper Paraná River.

3.3. Environmental effects on the distribution of ostracods

First and second axes of RDA analyses which were performed using all environments (Paraná River, tributaries and lakes) together as well as each type of environment separately were all significant (p<0.005) and were retained for interpretation. The variables selected in the ordination explained 11.26% (all environments), 11.8% (Paraná River), 13.08% (tributaries) and 27.9% (lakes) of the species data variability. When all environments (Paraná River, tributaries and lakes) were analyzed together, turbidity, pH, water temperature, dissolved oxygen, electrical conductivity and total phosphorous were the factors that showed significant influence on ostracod distributions. Some associations between certain species of ostracods and limnological factors were observed when we analyzed the environments separately. In the Paraná River, Diaphanocypris meridana, Cypricercus centura and Bradleytriebella lineata were associated with higher values of electrical conductivity, whereas Vestalenula pagliolii (Pinto & Kotzian, 1961) and Cypretta costata were related to the lower values of this variable. Stenocypris malayica was associated with higher values of alkalinity in Paraná River. Diaphanocypris meridana, Cypricercus centrura and Cypridopsis vidua (O. F. Müller, 1776) were associated with lower turbidity values in Baía River. pH seems to have important effects on the abundance and distribution of some ostracods species in the tributaries, such as Cypretta costata (Amambaí and Baía rivers) and Cytheridella ilosvayi (Iguatemi River). In addition, D. meridana, B. lineata and C. vidua were abundant in the lakes associated with higher pH (neutral-basic) and higher conductivity values. On the other hand, Alicenula serricaudata (Klie, 1935) and Vestalenula pagliolii (Darwinulidae), Pseudocandona agostinhoi Higuti & Martens, 2014 and Candobrasilopsis elongata Higuti & Martens, 2014 (Candonidae) were associated with lower pH values (neutral-acid) recorded in the lakes located downstream of Paraná River (Figure 6).

Figure 6
Biplot of the redundancy analysis (RDA) showing the association between ostracod community structure and limnological variables in (A) all environments, (B) Paraná River, (C) tributaries and (D) lakes. WT = water temperature, EC = electrical conductivity, DO = dissolved oxygen, TURB = turbidity, TP = total phosphorus. Dm = Diaphanocypris meridana, Cc = Cypricercus centrura, Bl = Bradleytriebella lineata, Sml = Stenocypris malayica, Cco = Cypretta costata, Cv = Cypridopsis vidua, Ciy = Cytheridella ilosvayi, Vp = Vestalenula pagliolii, As = Alicenula serricaudata, Pa = Pseudocandona agostinhoi, Ce = Candobrasilopsis elongata, Ch = Cabelodopsis hispida.

4. Discussion

4.1. Abiotic variables and environmental heterogeneity

The Upper Paraná River has four dams along its length, with Porto Primavera and Itaipu being the last dams in this part of the river (Stevaux et al., 2009STEVAUX, J.C., MARTINS, D.P. and MEURER, M. Changes in a large regulated tropical river: the Paraná River downstream from the Porto Primavera Dam, Brazil. Geomorphology, 2009, 113(3-4), 230-238. http://dx.doi.org/10.1016/j.geomorph.2009.03.015.
http://dx.doi.org/10.1016/j.geomorph.200...
). These cascade reservoirs act as filters retaining organic matter, thus increasing the water transparency and reducing the nitrogen and phosphorus concentrations of the water downstream (Roberto et al., 2009ROBERTO, M.C., SANTANA, N.F. and THOMAZ, S.M. Limnology in the Upper Parana River Floodplain: large-scale spatial and temporal pattern, and the influence of reservoirs. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2, Suppl), 717-725. PMid:19738977. http://dx.doi.org/10.1590/S1519-69842009000300025.
http://dx.doi.org/10.1590/S1519-69842009...
). The effect of the Porto Primavera dam on water quality and diverse aquatic communities of the Upper Paraná River floodplain has been widely reported (e.g. Agostinho et al., 2004bAGOSTINHO, A.A., THOMAZ, S.M. and GOMES, L.C. Threats for biodiversity in the floodplain of the Upper Paraná River: effects of hydrological regulation by dams. Ecohydrology & Hydrobiology, 2004b, 4(3), 255-256.; 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...
). This effect would tend to increase along the longitudinal gradient, however, tributaries (without dams) and floodplains contribute organic and inorganic particulate matter to the river water, restoring the natural attributes that have been degraded by upstream reservoir regulation (Rice & Church, 2001RICE, S.P. and CHURCH, M. Longitudinal profiles in simple alluvial systems. Water Resources Research, 2001, 37(2), 417-426. http://dx.doi.org/10.1029/2000WR900266.
http://dx.doi.org/10.1029/2000WR900266...
; Stanford & Ward, 2001STANFORD, J.A. and WARD, J.V. Revisiting the serial discontinuity concept. Regulated Rivers: Research and Management, 2001, 17(4-5), 303-310. http://dx.doi.org/10.1002/rrr.659.
http://dx.doi.org/10.1002/rrr.659...
; Portinho et al., 2016PORTINHO, J.L., PERBICHE-NEVES, G. and NOGUEIRA, M.G. Zooplankton community and tributary effects in free-flowing section downstream a large tropical reservoir. International Review of Hydrobiology, 2016, 101(1-2), 48-56. http://dx.doi.org/10.1002/iroh.201501798.
http://dx.doi.org/10.1002/iroh.201501798...
). We observed a similar trend along the longitudinal gradient of the Paraná River in both banks (right and left), due the presence of several tributaries.

Environmental heterogeneity was similar in the Paraná River, the tributaries and the lakes. This is as expected, because the environments are connected to each other: tributaries and lakes are connected to the Paraná River. On the other hand, studies have shown that a lack of hydrological connectivity reduces the flow of organic and inorganic material (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...
), thus increasing the heterogeneity between them (Lopes et al., 2014LOPES, P.M., BINI, L.M., DECLERCK, S.A.J., FARJALLA, V.F., VIEIRA, L.C.G., BONECKER, C.C., LANSAC-TÔHA, F.A., ESTEVES, F.A. and BOZELLI, R.L. Correlates of zooplankton beta diversity in tropical lake systems. PLoS One, 2014, 9(10), e109581. PMid:25330034. http://dx.doi.org/10.1371/journal.pone.0109581.
http://dx.doi.org/10.1371/journal.pone.0...
; Bozelli et al., 2015BOZELLI, R.L., THOMAZ, S.M., PADIAL, A.A., LOPES, P.M. and BINI, L.M. Floods decrease zooplankton beta diversity and environmental heterogeneity in an Amazonian floodplain system. Hydrobiologia, 2015, 753(1), 233-241. http://dx.doi.org/10.1007/s10750-015-2209-1.
http://dx.doi.org/10.1007/s10750-015-220...
). The confluence of tributaries with the main river channel minimizes these effects along the longitudinal gradient of the river, as it contributes to the increase of the organic and inorganic material, at the same time also increasing the environmental heterogeneity (Katano et al., 2009KATANO, I., NEGISHI, J.N., MINAGAWA, T., DOI, H., KAWAGUCHI, Y. and KAYABA, Y. Longitudinal macroinvertebrate organization over contrasting discontinuities: effects of a dam and a tributary. Journal of the North American Benthological Society, 2009, 28(2), 331-351. http://dx.doi.org/10.1899/08-010.1.
http://dx.doi.org/10.1899/08-010.1...
).

Flood pulses (sudden increases in water level, mainly owing to water release from the dams) are an important factor for limnological changes in floodplain lakes (Thomaz et al., 2004THOMAZ, S.M., PAGIORO, T.A., BINI, L.M., ROBERTO, M.C. and ROCHA, R.R.A. Limnological characterization of the aquatic environments and the influence of hydrometric levels. In: S.M. THOMAZ, A.A. AGOSTINHO and N.S. HAHN, eds. The Upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers, 2004, pp. 75-102.; Conceição et al., 2017aCONCEIÇÃO, E.O., HIGUTI, J., CAMPOS, R. and MARTENS, K. Effects of flood pulses on persistence and variability of pleuston communities in a tropical floodplain lake. Hydrobiologia, 2017a, 1-14. https://doi.org/10.1007/s10750-017-3392-z.
https://doi.org/10.1007/s10750-017-3392-...
). During high waters, the lakes increase the extent of their margins, and thus also the decomposition of organic matter and with resulting increasing nutrient values (Thomaz et al., 2004THOMAZ, S.M., PAGIORO, T.A., BINI, L.M., ROBERTO, M.C. and ROCHA, R.R.A. Limnological characterization of the aquatic environments and the influence of hydrometric levels. In: S.M. THOMAZ, A.A. AGOSTINHO and N.S. HAHN, eds. The Upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers, 2004, pp. 75-102.). However, flood pulses of high amplitude, which were not observed during the present study, can reduce the environmental heterogeneity in floodplain lakes (GAR, XIR, POM, see Figure 4).

4.2. Composition, diversity and density of ostracod communities

Gamma diversity of freshwater ostracods was comparatively high in the river-floodplain system of the Upper Paraná River, as 44 species were recorded, compared to 48 species found in other studies about diversities of ostracods in this floodplain (Higuti et al., 2010HIGUTI, J., DECLERCK, S.A.J., LANSAC-TÔHA, F.A., VELHO, L.F.M. and MARTENS, K. Variation in ostracod (Crustacea, Ostracoda) communities in the alluvial valley of the upper Paraná River (Brazil) in relation to substrate. Hydrobiologia, 2010, 644(2), 261-278. http://dx.doi.org/10.1007/s10750-010-0122-1.
http://dx.doi.org/10.1007/s10750-010-012...
, 2013HIGUTI, J., SCHÖN, I., AUDENAERT, L. and MARTENS, K. On the Strandesia obtusata/elliptica lineage (Ostracoda, Cyprididae) in the alluvial valley of the Paraná River (Brazil), with the description of three new species. Crustaceana, 2013, 86, 182-211. http://dx.doi.org/10.1163/15685403-00003160.
http://dx.doi.org/10.1163/15685403-00003...
). Sampling efforts appear to be suitable to reveal the diversity of ostracods, because of similar values amongst expected and observed estimators, while all richness estimators have already reached an asymptote.

The highest richness and densities were recorded in the lentic environments (approximately 91% of the total richness found throughout the study), compared to lotic environment (main channel of Paraná River and tributaries). This difference might be attributed to the lower water flow and higher stability within the lentic environments. This stability provides greater habitat complexity and larger food resources (Schindler & Scheuerell, 2002SCHINDLER, D.E. and SCHEUERELL, M.D. Habitat coupling in lake ecosystems. Oikos, 2002, 98(2), 177-189. http://dx.doi.org/10.1034/j.1600-0706.2002.980201.x.
http://dx.doi.org/10.1034/j.1600-0706.20...
). Both of these features can lead to an increase of development of ostracods in the roots of aquatic macrophytes. On the other hand, in lotic environments, the water flow may affect the establishment of the organisms which could be washed out from amongst macrophytes (Grabowska et al., 2013GRABOWSKA, M., EJSMONT-KARABIN, J. and KARPOWICZ, M. Reservoir-river relationships in lowland, shallow, eutrophic systems: an impact of zooplankton from hypertrophic reservoir on river zooplankton. Polish Journal of Ecology, 2013, 61(4), 759-768.).

The highest richness and density observed in the region downstream of the dam in the main channel of Paraná River (P6, P7, P8), may be attributed to effects of the tributaries, owing to the increase of environmental heterogeneity in these sampling sites. Several studies confirm the importance of the tributaries in attenuating the effects of oligotrophication in the main channels caused by dams. For example, the increase of taxonomic richness and density of macroinvertebrates along a longitudinal gradient in the Dam-regulated River in Japan was related to the confluence of a tributary, owing to the increase of environmental heterogeneity, food resources and recruitment of colonizers (Katano et al., 2009KATANO, I., NEGISHI, J.N., MINAGAWA, T., DOI, H., KAWAGUCHI, Y. and KAYABA, Y. Longitudinal macroinvertebrate organization over contrasting discontinuities: effects of a dam and a tributary. Journal of the North American Benthological Society, 2009, 28(2), 331-351. http://dx.doi.org/10.1899/08-010.1.
http://dx.doi.org/10.1899/08-010.1...
). In addition, an increase of nutrient concentrations in the main channel by the confluence of the tributaries showed a positive relation with density of macroinvertebrates downstream of the dam (Kiffney et al., 2006KIFFNEY, P.M., GREENE, C.M., HALL, J.E. and DAVIES, J.R. Tributary streams create spatial discontinuities in habitat, biological productivity, and diversity in mainstem rivers. Canadian Journal of Fisheries and Aquatic Sciences, 2006, 23(11), 2518-2530. http://dx.doi.org/10.1139/f06-138.
http://dx.doi.org/10.1139/f06-138...
).

The similarity of beta diversity amongst Paraná River, tributaries and lakes may be owing to permanent hydrological connectivity amongst these environments, favouring the exchange of organisms and species. Low variation in beta diversity may then be caused by the absence of significant water flows during the dry season (Bonecker et al., 2005BONECKER, C.C., COSTA, C.L., VELHO, L.F.M. and LANSAC-TÔHA, F.A. Diversity and abundance of the planktonic rotifers in different environments of the Upper Parana River floodplain (Parana State – Mato Grosso do Sul State, Brazil). Hydrobiologia, 2005, 546(1), 405-414. http://dx.doi.org/10.1007/s10750-005-4283-2.
http://dx.doi.org/10.1007/s10750-005-428...
; Conceição et al., 2017bCONCEIÇÃO, E.O., HIGUTI, J. and MARTENS, K. Variability in ostracod communities (Crustacea, Ostracoda) in connected and isolated tropical floodplain lakes. Annales de Limnologie - International. Journal of Limnology, 2017b, 53, 325-332. http://dx.doi.org/10.1051/limn/2017016.
http://dx.doi.org/10.1051/limn/2017016...
).

Higher environmental heterogeneity may lead to an increase in beta diversity (Anderson et al., 2006ANDERSON, M.J., ELLINGSEN, K.E. and MCARDLE, B.H. Multivariate dispersion as a measure of beta diversity. Ecology Letters, 2006, 9(6), 683-693. PMid:16706913. http://dx.doi.org/10.1111/j.1461-0248.2006.00926.x.
http://dx.doi.org/10.1111/j.1461-0248.20...
; Astorga et al., 2014ASTORGA, A., DEATH, R., DEATH, F., PAAVOLA, R., CHAKRABORTY, M. and MUOTKA, T. Habitat heterogeneity drives the geographical distribution of beta diversity the case of New Zeland stream invertebrates. Ecology and Evolution, 2014, 4(13), 2693-2702. PMid:25077020. http://dx.doi.org/10.1002/ece3.1124.
http://dx.doi.org/10.1002/ece3.1124...
). In contrast, our study did not show a positive correlation between environmental heterogeneity and beta diversity, which is in agreement with other studies (Heino et al., 2013HEINO, J., GRÖNROOS, M., ILMONEN, J., KARHU, T., NIVA, M. and PAASIVIRTA, L. Environmental heterogeneity and β diversity of stream macroinvertebrate communities at intermediate spatial scales. Freshwater Science, 2013, 32(1), 142-154. http://dx.doi.org/10.1899/12-083.1.
http://dx.doi.org/10.1899/12-083.1...
; Bini et al., 2014BINI, L.M., LANDEIRO, V.L., PADIAL, A.A., SIQUEIRA, T. and HEINO, J. Nutrient enrichment is related to two facets of beta diversity for stream invertebrates across the United States. Ecology, 2014, 95(6), 1569-1578. PMid:25039221. http://dx.doi.org/10.1890/13-0656.1.
http://dx.doi.org/10.1890/13-0656.1...
; Heino et al., 2015HEINO, J., MELO, A.S. and BINI, L.M. Reconceptualising the beta diversity-environmental heterogeneity relationship in running water systems. Freshwater Biology, 2015, 60(2), 223-235. http://dx.doi.org/10.1111/fwb.12502.
http://dx.doi.org/10.1111/fwb.12502...
; Zorzal-Almeida et al., 2017ZORZAL-ALMEIDA, S., BINI, L.M. and BICUDO, D.C. Beta diversity of diatoms is driven by environmental heterogeneity, spatial extent and productivity. Hydrobiologia, 2017, 800(1), 7-16. http://dx.doi.org/10.1007/s10750-017-3117-3.
http://dx.doi.org/10.1007/s10750-017-311...
). Heino et al. (2015)HEINO, J., MELO, A.S. and BINI, L.M. Reconceptualising the beta diversity-environmental heterogeneity relationship in running water systems. Freshwater Biology, 2015, 60(2), 223-235. http://dx.doi.org/10.1111/fwb.12502.
http://dx.doi.org/10.1111/fwb.12502...
postulate that environments with high dispersal rates can mask local environmental effects. This may therefore reduce the relationship between environmental heterogeneity and beta diversity amongst small regional units on a larger spatial scale.

Along the longitudinal gradient of Paraná River, its tributaries and lakes, one of dispersal routes of ostracods might be through drift of free floating macrophytes (and hitch-hiking pleustonic faunas) downstream, thus homogenizing the fauna. In addition, there are other dispersal ways such as wind (Vanschoenwinkel et al., 2008VANSCHOENWINKEL, B., GIELEN, S., SEAMAN, M. and BRENDONCK, L. Any way the wind blows – frequent wind dispersal drives species sorting in ephemeral aquatic communities. Oikos, 2008, 117(1), 125-134. http://dx.doi.org/10.1111/j.2007.0030-1299.16349.x.
http://dx.doi.org/10.1111/j.2007.0030-12...
), birds (Brochet et al., 2010BROCHET, A.L., GAUTHIER-CLERC, M., GUILLEMAIN, M., FRITZ, H., WATERKEYN, A., BALTANÁS, Á. and GREEN, A.J. Field evidence of dispersal of branchiopods, ostracods and bryozoans by teal (Anas crecca) in the Camargue (southern France). Hydrobiologia, 2010, 637(1), 255-261. http://dx.doi.org/10.1007/s10750-009-9975-6.
http://dx.doi.org/10.1007/s10750-009-997...
) and human (Waterkeyn et al., 2010WATERKEYN, A., VANSCHOENWINKEL, B., ELSEN, S., ANTON-PARDO, M., GRILLAS, P. and BRENDONCK, L. Unintentional dispersal of aquatic invertebrates via footwear and motor vehicles in a Mediterranean wetland area. Aquatic Conservation, 2010, 20(5), 580-587. http://dx.doi.org/10.1002/aqc.1122.
http://dx.doi.org/10.1002/aqc.1122...
) carrying the drought resistant eggs. Local abiotic factors probably had the largest influence on the variability of ostracod species composition amongst tributaries and amongst lakes, and less so in the main river channel.

4.3. Environmental effects on the distribution of ostracods

Physical and chemical properties of water are factors that generally have important effects on the distribution of ostracod species. However, we observed no such strong relationships in the river-floodplain system of upper Paraná River. Electrical conductivity ranges influenced the distributions of some ostracods species in the Paraná River and lakes, such as in other studies that showed conductivity as a factor determining ostracod communities (Liberto et al., 2012LIBERTO, R., MESQUITA-JOANES, F. and CÉSAR, I. Dynamics of pleustonic ostracod populations in small ponds on the Island of Martín García (Rio de la Plata, Argentina). Hydrobiologia, 2012, 688(1), 47-61. http://dx.doi.org/10.1007/s10750-011-0600-0.
http://dx.doi.org/10.1007/s10750-011-060...
; Zhai et al., 2015ZHAI, M., NOVÁCEK, O., VÝRAVSKÝ, D., SYROVÁTKA, V., BOJKOVÁ, J. and HELESIC, J. Environmental and spatial control of ostracod assemblages in the Western Carpathian spring fens. Hydrobiologia, 2015, 745(1), 225-239. http://dx.doi.org/10.1007/s10750-014-2104-1.
http://dx.doi.org/10.1007/s10750-014-210...
).

The lotic environments have a higher flow velocity compared to the lentic environments. Consequently, this higher hydrodynamics increases sediment movement, making the water more turbid in the tributaries, except in the Baía River, where the current flow velocity is much smaller. Relatively transparent environments may benefit the abundance of some species with different strategies, e.g., swimming species (D. meridana, C. centrura and C. vidua), smaller species (C. vidua), or the presence of spines (C. centrura) to prevent predation.

Ostracods need to calcify their valves 9 times moult (during each moult) and this imposes important physiological stress if HCO3 levels and pH are low (Higuti et al., 2010HIGUTI, J., DECLERCK, S.A.J., LANSAC-TÔHA, F.A., VELHO, L.F.M. and MARTENS, K. Variation in ostracod (Crustacea, Ostracoda) communities in the alluvial valley of the upper Paraná River (Brazil) in relation to substrate. Hydrobiologia, 2010, 644(2), 261-278. http://dx.doi.org/10.1007/s10750-010-0122-1.
http://dx.doi.org/10.1007/s10750-010-012...
). pH seems to be the most important variable on abundance and distribution of some ostracods species in tributaries, despite the small amplitude of variation of this variable amongst the sampling sites. Liberto et al. (2012)LIBERTO, R., MESQUITA-JOANES, F. and CÉSAR, I. Dynamics of pleustonic ostracod populations in small ponds on the Island of Martín García (Rio de la Plata, Argentina). Hydrobiologia, 2012, 688(1), 47-61. http://dx.doi.org/10.1007/s10750-011-0600-0.
http://dx.doi.org/10.1007/s10750-011-060...
also found a relation between the ostracods species with higher and lower pH variation. In addition, according Zhai et al. (2015)ZHAI, M., NOVÁCEK, O., VÝRAVSKÝ, D., SYROVÁTKA, V., BOJKOVÁ, J. and HELESIC, J. Environmental and spatial control of ostracod assemblages in the Western Carpathian spring fens. Hydrobiologia, 2015, 745(1), 225-239. http://dx.doi.org/10.1007/s10750-014-2104-1.
http://dx.doi.org/10.1007/s10750-014-210...
, the range of pH tolerance depends on the niche of the species, some species tolerating higher and/or lower pH values.

Acknowledgements

We thank the Ministry of Science and Technology (MCT) / National Council for Scientific and Technological Development (CNPq) / Fundacão Araucária for financial support to the project (Process: 478629/2012-5) and to Long-Term Ecological Research - LTER. We thanks to Dr. Luiz Felipe Machado Velho, coordinator of this project, for the valuable comments and suggestions to improve the manuscript. We thank the Research Centre in Limnology, Ichthyology and Aquaculture (Nupelia) and the Post-Graduate Program in Ecology of Aquatic Continental Environments (PEA) of the State University of Maringá (UEM), Academic Excellency Program (Proex) / Coordination for the Improvement of Higher Education Personnel (CAPES), USACUCAR, CORIPA, ICMBio for the logistic support. We also thank the laboratory of Limnology of Nupelia (UEM), in special Maria do Carmo Roberto and Natália Fernanda Santana, for provide abiotic data and Jaime Luiz Lopes Pereira (Nupelia) for the production of the map. The MSc students amongst the present authors would like to thank CNPq and CAPES for granting their scholarship. Dr Moacyr Serafim Junior (Universidade Federal do Recôncavo da Bahia) and Analia R. Díaz (Instituto de Limnología “Dr. Raúl A. Ringuelet”) for the important suggestions in the manuscript. The Universidade Estadual de Maringá, (UEM, Maringá) and the Royal Belgian Institute of natural Sciences (RBINS, Brussels) have a bilateral Memorandum of Understanding regarding collaborative Scientific Research.

  • Cite as: Higuti, J. et al. Periphytic community structure of Ostracoda (Crustacea) in the river-floodplain system of the Upper Paraná River. Acta Limnologica Brasiliensia, 2017, vol. 29, e120.

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Publication Dates

  • Publication in this collection
    2017

History

  • Received
    11 June 2017
  • Accepted
    13 Nov 2017
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