Abstract:

We present here the first study that analyzed the composition and richness of rotifers of the entire La Plata River basin, the second largest in South America, based on simultaneous and standardized sampling. Fifteen large reservoirs and eight river stretches were selected in the upper, middle, and lower portions of the Paraná, Paraguay, and Uruguay Rivers, which are the major rivers of the La Plata basin. We took a total of 86 samples (open water habitats) in 2010. A mean of 27±11 species per sub-basin was found, with the highest richness in the Lower Paraná (41 species), followed by the Paranapanema (40 species) and Lower Uruguay (38 species). Low richness was observed in the Middle Uruguay and Middle Paraná. We found 106 species belonging to 21 families and two orders. The family with the highest number of species was Lecanidae (21), followed by Brachionidae (20), Trichocercidae (9), and Synchaetidae (8). The species with higher occurrences were Conochilus dossuarius, Kellicottia bostoniensis, Keratella americana, Keratella cochlearis and Hexarthra mira. New occurrences of rotifers were registered for Brazil (Colurella adriatica), São Paulo State (Enteroplea lacustris), and Argentina (Gastropus hyptopus, Harringia rousseleti and Lecane thienemanni). Spearman correlation between the number of species and physical and chemical variables demonstrated positive correlation with chlorophyll and temperature, and negative correlation with dissolved oxygen. We extend the distribution list for some native (Lecane ludwigii) and non-native species of rotifers (K. bostoniensis). We also list the monogonont rotifer species found at the sampling stations.

Keywords:
Biodiversity; Rotifera; Survey; New records; Lotic; Lentic environments

Resumo:

Apresentamos aqui o primeiro estudo que analisou a composição e riqueza de rotíferos de toda a bacia do Rio da Prata, a segunda maior da América do Sul, com amostragens simultâneas e padronizadas. Quinze grandes reservatórios e oito trechos lóticos foram selecionados nas porções alta, média e baixa dos rios Paraná, Paraguai e Uruguai, que atuam como os principais formadores da bacia do Prata. Coletamos um total de 86 amostras (habitats de águas abertas) em 2010. Foi encontrada uma média de 27 ± 11 espécies por sub-bacia, com maior riqueza no Baixo Paraná (41 espécies), seguido por Paranapanema (40 espécies) e Baixo Uruguai (38 espécies). Uma baixa riqueza foi observada no Médio Uruguai e no Médio Paraná. Encontramos 106 espécies pertencentes a 21 famílias e duas ordens. A família com maior número de espécies foi Lecanidae (21), seguida por Brachionidae (20), Trichocercidae (9) e Synchaetidae (8). As espécies com maior ocorrência foram Conochilus dossuarius, Kellicottia bostoniensis, Keratella americana, Keratella cochlearis e Hexarthra mira. Novas ocorrências de rotíferos foram registradas para o Brasil (Colurella adriatica), Estado de São Paulo (Enteroplea lacustris) e Argentina (Gastropus hyptopus, Harringia rousseleti e Lecane thienemanni). A correlação de Spearman entre o número de espécies e as variáveis físicas e químicas demonstrou correlação positiva com clorofila e temperatura, e correlação negativa com oxigênio dissolvido. Estendemos a lista de distribuição para algumas espécies nativas (Lecane ludwigii) e não-nativas de rotíferos (K. bostoniensis). Disponibilizamos também uma lista de espécies de rotíferos Monogononta encontrados nas estações amostradas.

Palavras-chave:
Biodiversidade; Rotifera; Levantamento; Novos Registros; Lótico; Ambientes lênticos

Introduction

Species inventories are important tools for conservation measures and management, especially in areas imperiled by human actions. It is also useful to show gaps in the scientific knowledge about zooplankton diversity and directions for future research.

There have been surveys of Rotifera diversity in the La Plata River basin, the second largest in South America. However, these surveys have focused on regions such as in the Upper Paraná floodplain (Lansac-Tôha et al. 2009), waterbodies of São Paulo State (Souza-Soares et al. 2011SOUZA-SOARES, F., TUNDISI, J.G., MATSUMURA-TUNDISI, T., SOARES, F.S., TUNDISI, J.G. & MATSUMURA-TUNDISI, T. 2011. Checklist de Rotifera de água doce do Estado de São Paulo, Brasil. Biota Neotrop. 11(1a):515-539.), and a few tributaries (Neschuk et al. 2002NESCHUK, N., CLAPS, M. & GABELLONE, N. 2002. Planktonic rotifers of a saline-lowland river: the Salado River (Argentina). Ann. Limnol. Int. J. Limnol. 38(3):191-198., Kuczynski 2017KUCZYNSKI, D. 2017. Zooplankton from the Reconquista River (Buenos Aires, Argentina): composition, density and seasonal variation. Rev. Investig. Científicas la Universdad Morón 1(1):29-38.). There have been no basin-wide surveys that included all the countries drained by the basin.

The La Plata River basin has very distinct environments, with extensively dammed and undammed reaches. For example, there are reservoirs in more than half of the upper reaches in the Paraná River basin, leaving few truly lotic reaches; the opposite occurs in its middle and lower reaches (Agostinho et al. 2007AGOSTINHO, A.A., GOMES, L.C. & PELICICE, F.M. 2007. Ecologia e manejo de recursos pesqueiros em reservatórios do Brasil. Eduem, Maringá.). The situation is very similar for the Uruguay River. However, there are no reservoirs in the Paraguay River (Perbiche-Neves et al. 2016PERBICHE-NEVES, G., SAITO, V.S., PREVIATTELLI, D., DA ROCHA, C.E.F. & NOGUEIRA, M.G. 2016. Cyclopoid copepods as bioindicators of eutrophication in reservoirs: Do patterns hold for large spatial extents? Ecol. Indic. 70: 340-347.). This results in different habitats with distinct limnological features, which may favor differences in rotifer species composition among lotic and lentic regions.

There have been multiple studies of rotifer richness and distribution in Brazilian and Argentinian waters of the La Plata River basin. For example, Garraffoni & Lourenço (2012GARRAFFONI, A.R.S. & LOURENÇO, A.P. 2012. Synthesis of Brazilian Rotifera: An updated list of species. Check List 8(3):375-401.) surveyed rotifer species throughout Brazil. Other rotifer surveys were less extensive, such in Mato Grosso do Sul (Roche & Silva 2017ROCHE, K.F. & SILVA, W.M. 2017. Checklist dos Rotifera (Animalia) do Estado de Mato Grosso do Sul, Brasil. Iheringia. Série Zool. 107(suppl):1-10.), São Paulo (Souza-Soares et al. 2011SOUZA-SOARES, F., TUNDISI, J.G., MATSUMURA-TUNDISI, T., SOARES, F.S., TUNDISI, J.G. & MATSUMURA-TUNDISI, T. 2011. Checklist de Rotifera de água doce do Estado de São Paulo, Brasil. Biota Neotrop. 11(1a):515-539.), the Upper Tietê River basin (Lucinda et al. 2004LUCINDA, L., MORENO, I.H., MELÃO, M.G.G. & MATSUMURA-TUNDISI, T. 2004. Rotifers in freshwater habitats in the Upper Tietê River Basin, São Paulo State, Brazil. Acta Limnol. Bras. 16(3):203-224.), and Paranoá Reservoir (Padovesi & Andreoni 2011PADOVESI, C.F. & ANDREONI, C.B. 2011. Rotifera, Paranoá reservoir, Brasília, central Brazil. Check List 7(3):248-252.). Despite those surveys, the number of rotifer surveys are underrepresented (Souza et al. 2018SOUZA, C.A., GOMES, L.F., NABOUT, J.C., VELHO, L.F.M. & VIEIRA, L.C.G. 2018. Temporal trends of scientific literature about zooplankton community. Neotrop. Biol. Conserv. 13(4):274-286.), when compared to other groups of zooplankton such as copepods (Silva et al. 2009SILVA, W.M., ROCHE, K.F., EILERS, V. & OLIVEIRA, M.D. 2009. Copepod (Crustacea) distribution in the freshwater and hyposaline lakes of the Pantanal of Nhecolandia (Mato Grosso do Sul, Brazil). Acta Limnol. Bras. 21(3): 327-331., Matsumura-Tundisi & Tundisi 2011MATSUMURA-TUNDISI, T. & TUNDISI, J.G. 2011. Checklist dos Copepoda Calanoida de água doce do Estado de São Paulo. Biota Neotrop. 11(suppl 1):551-557., Perbiche-Neves et al. 2014PERBICHE-NEVES, G., ROCHA, C.E.F. da & NOGUEIRA, M.G. 2014. Estimating cyclopoid copepod species richness and geographical distribution (Crustacea) across a large hydrographical basin: comparing between samples from water column (plankton) and macrophyte stands. Zool. 31(3):239-244.).

For Argentina, José de Paggi (1990)JOSÉ DE PAGGI, S. 1990. Ecological and biogeogvaphical remarks on the rotifer fauna of Argentina. Rev. Hydrobiol. Trop. 23(4):297-311. listed 279 rotifer taxa. Most rotifer surveys have been in the Paraná River floodplains (Aoyagui & Bonecker 2004AOYAGUI, A.S.M. & BONECKER, C.C. 2004. The art status of rotifer studies in natural environments of South America: floodplains. Acta Sci. Biol. Sci. 26(4):385-406.) and La Plata River tributaries (Macluf et al. 1998MACLUF, C.C., CLAPS, M.C. & SOLARI, L.C. 1998. Plankton of an undisturbed plain’s stream (Buenos Aires, Argentina). SIL Proceedings, 1922-2010 26(3):1057-1061., Modenutti 1998MODENUTTI, B.E. 1998. Planktonic rotifers of Samborombon River Basin (Argentina). Hydrobiologia 387/388: 259-265., Bazzuri et al. 2020BAZZURI, M.E., GABELLONE, N.A. & SOLARI, L.C. 2020. Zooplankton - population dynamics in the Salado - River basin ( Buenos Aires , Argentina ) in relation to hydraulic works and resulting wetland function. Aquat. Sci. 82(48):1-18.). Recently, Ferrando & Claps (2016)FERRANDO, N.S. & CLAPS, M.C. 2016. A revised and updated checklist of Monogononta rotifers from Argentina. Check List 12(4):1-26. updated the checklist of Argentinian Rotifera, including a reporting 35 species of monogonont rotifers. According to the authors, “[...] the majority of reports were restricted to the provinces of Santa Fe (68% of the total records), Corrientes and Buenos Aires (50% of the total records), Río Negro and Formosa (30% of the total records)” (Ferrando & Claps 2016FERRANDO, N.S. & CLAPS, M.C. 2016. A revised and updated checklist of Monogononta rotifers from Argentina. Check List 12(4):1-26.; p.2). The rotifer species which are more commonly found in Argentinian Paraná River reaches and La Plata River tributaries were Keratella cochlearis (Gosse, 1851), K. americana Carlin, 1943 and Brachionus calyciflorus Pallas, 1776 (Modenutti 1998MODENUTTI, B.E. 1998. Planktonic rotifers of Samborombon River Basin (Argentina). Hydrobiologia 387/388: 259-265., Bonetto & Wais 2006BONETTO, A.A. & WAIS, I.R. 2006. Southern South American Streams and Rivers. In River and Stream Ecosystems of the World: With a New Introduction (M. G. W. Cushing C.E., Cummins K.W., ed.) University of California Press, Berkeley, p.257-293.).

Knowledge of the diversity and distribution of rotifers in the Paraguay River basin is scarce and concentrated in Brazil and Argentina, including rivers in the Pantanal (Branco et al. 2018BRANCO, C.W.C., SILVEIRA, R. de M.L. & MARINHO, M.M. 2018. Flood pulse acting on a zooplankton community in a tropical river (Upper Paraguay river, northern Pantanal, Brazil). Fundam. Appl. Limnol. 192(1):23-42., Brito et al. 2020BRITO, M.T. S., HEINO, J., POZZOBOM, U.M. & LANDEIRO, V.L. 2020. Ecological uniqueness and species richness of zooplankton in subtropical floodplain lakes. Aquat. Sci. 82(43):1-13.) and those joining the Paraná River (Frutos et al. 2006FRUTOS, S.M., POI DE NEIFF, A.S.G. & NEIFF, J.J. 2006. Zooplankton of the Paraguay River: A comparison between sections and hydrological phases. Ann. Limnol. 42(4):277-288.). Similarly, few rotifer surveys have been conducted in the Uruguay River basin (e.g., José de Paggi 1978JOSÉ DE PAGGI, S. 1978. First observations on longitudinal succession of zooplankton in the main course of the Paraná River between Santa Fe and Buenos Aires Harbour. Stud. Neotrop. Fauna E. 13(3-4): 143-156.; Picapedra et al. 2019PICAPEDRA, P.H. S., FERNANDES, C. & BAUMGARTNER, G. 2019. Structure and ecological aspects of zooplankton (Testate amoebae, Rotifera, Cladocera and Copepoda) in highland streams in southern Brazil. Acta Limnol. Bras. 31(e5).).

Therefore, we provide for the first time a spatially extensive survey of Rotifera species found in the lentic and lotic stretches of the La Plata River basin to characterize its species diversity patterns. In addition, we have expanded the distribution of some Rotifera species not yet reported in the literature, thus contributing to the general knowledge of the diversity of the group in the region.

Materials and Methods

1. Study area

The La Plata River basin has an area of 3.1 million km² (Cuya et al. 2013CUYA, D.G.P., BRANDIMARTE, L., POPESCU, I., ALTERACH, J. & PEVIANI, M. 2013. A GIS-based assessment of maximum potential hydropower production in La Plata basin under global changes. Renew. Energy 50: 103-114.) and drains portions of five countries: Brazil, Paraguay, Uruguay, Argentina, and Bolivia. The main sub-basins are the Paraná, Paraguay, and Uruguay River basins. The Paraná basin is the largest, covering 48.7% of the basin, followed by the Paraguay (35.3%) and Uruguay (11.8%) basins (Cuya et al. 2013CUYA, D.G.P., BRANDIMARTE, L., POPESCU, I., ALTERACH, J. & PEVIANI, M. 2013. A GIS-based assessment of maximum potential hydropower production in La Plata basin under global changes. Renew. Energy 50: 103-114.).

2. Sampling

A total of 86 samples were collected at 43 stations, including 15 reservoirs (in dam and upriver zones) and 13 lotic stretches distributed in the three main sub-basins of La Plata River (Figure 1, Table 1). Sites (open water - littoral habitats were not included) were sampled in January (summer - wet season) and July (winter- dry season) 2010. Ten water quality variables were measured at each sampling station during each visit following Perbiche-Neves et al. (2016)PERBICHE-NEVES, G., SAITO, V.S., PREVIATTELLI, D., DA ROCHA, C.E.F. & NOGUEIRA, M.G. 2016. Cyclopoid copepods as bioindicators of eutrophication in reservoirs: Do patterns hold for large spatial extents? Ecol. Indic. 70: 340-347. and Pessotto & Nogueira (2018)PESSOTTO, M.A. & NOGUEIRA, M.G. 2018. More than two decades after the introduction of Limnoperna fortunei ( Dunker 1857 ) in La Plata Basin. Braz. J. Biol. 78(4):773-784.: total phosphorus and nitrogen, temperature, transparency, turbidity, conductivity, pH, dissolved oxygen, depth, and total chlorophyll.

Figure 1
Locations of the 43 sites in La Plata River basin, with data of water retention time (WRT) and water velocity of the river stretches. For codes see Table 1. Adapted from Perbiche-Neves et al. (2016)PERBICHE-NEVES, G., SAITO, V.S., PREVIATTELLI, D., DA ROCHA, C.E.F. & NOGUEIRA, M.G. 2016. Cyclopoid copepods as bioindicators of eutrophication in reservoirs: Do patterns hold for large spatial extents? Ecol. Indic. 70: 340-347..

We sampled rotifers through vertical hauls by using a 50 µm mesh conical plankton net. In deep sites, the maximum depth hauled was 40 m (Perbiche-Neves et al. 2019PERBICHE-NEVES, G., SAITO, V.S., SIMÕES, N.R., DEBASTIANI-JÚNIOR, J.R., NALIATO, D.A. de O. & NOGUEIRA, M.G. 2019. Distinct responses of Copepoda and Cladocera diversity to climatic, environmental, and geographic filters in the La Plata River basin. Hydrobiologia 826(1):113-127.). The sampled rotifers were subsequently packed, labeled, and fixed with 4% formalin solution. Identifications were conducted with an optical microscope (Zeiss Axio Imager.A2m) and by using species keys (Edmondson 1959EDMONDSON, W.T. 1959. Rotifera. In reshwater Biology (W. T. Edmondson, ed.) Wiley and Sons, New York, p.420-484., Koste 1978KOSTE, W. 1978. Rotatoria, die Rädertiere Mitteleuropas : Überordnung Monogononta: ein Bestimmungswerk. Gebrüder Borntraeger, Berlin., Nogrady et al. 1995NOGRADY, T., POURRIOT, R. & SEGERS, H. 1995. Rotifera 3. Notommatidae and Scaridiidae. In Guides to the Identification of the Microinvertebrates of the Continental Waters of the World 8. (H. J. Dumont & T. Nogrady , eds) SPB Academic Publishing BV, p.248p., Segers & Dumont 1995SEGERS, H. & DUMONT, H.J. 1995. 102+ rotifer species (Rotifera: Monogononta) in Broa reservoir (SP., Brazil) on 26 August 1994, with the description of three new species. Hydrobiologia 316(3):183-197., Smet & Pourriot 1997SMET, W.H. & POURRIOT, R. 1997. Rotifera, vol. 5: The Dicranophoridae and the Ituridae (Monogononta). In Guides to the identification of the microinvertebrates of the continental waters of the world. (H. J. Dumont, ed.) SPB Academic Publishing BV, Netherlands, p.344., Nogrady 2002NOGRADY, T. 2002. Rotifera 6: Asplanchnidae, Gastropodidae, Lindiidae, Microcodidae, Synchaetidae, Trochosphaeridae and Filinia. In Guides to the Identification of the Microinvertebrates of the Continental Waters of the World 18 (H. J. Dumont, ed.) Backhuys, p.264., Wallace et al. 2019WALLACE, R.L.; SNELL, T.W.; WALSH, E.J.; SARMA, S.S.S; SEGERS, H. 2019. Phylum Rotifera. In Thorp and Covich’s Freshwater Invertebrates: Volume 4: Keys to Palaearctic Fauna (J. H. Rogers, D. C., & Thorp , ed.) Elsevier.). Voucher specimens were deposited in the Laboratory of Continental Waters Ecology, Institute of Biosciences of Botucatu at the Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Brazil. The number of species was correlated with water quality variables by using non-parametric Spearman correlation and a logarithmic transformation in R Cran Project 3.3.0 (2016) using the Hmisc package of R.

Results

The mean rotifer richness was 27±11 species. The sub-basins with higher richness were the Lower Paraná (41 species), followed by the Paranapanema (40 species) and Tietê (35 species). The basins with lower richness were the Middle Paraná and Lower Uruguay (Figure 2A).

Figure 2
Rotifer richness per basin for species (A) and family (B).

The Rotifera fauna of the La Plata River basin was composed of 106 species, distributed in 21 families and 37 genera (Table 2, Figure 2B). The most representative family in the basin is the Lecanidae (21 species), followed by the Brachionidae (20), Trichocercidae (9), and Synchaetidae (8) (Figure 2B). The most speciose genera are Lecane Nitzsch, 1827 and Brachionus Pallas, 1766 with 21 and 10 species, respectively. We found 44 rotifer species in summer and 17 in winter. These seasonal periods share a combined 45 rotifer species (Figure 3).

Figure 3
Species collected in the summer, winter and shared in both seasons.

Regarding individual sites, we found a wide range in species richness. Barra Bonita Reservoir (BBON-D; 12) in the Tietê River had the greatest species richness (22). The lowest richness was observed in the Lower (RURU-L; 40) and Middle (RURU-M1; 36) Uruguay River (3 species each; Table 2). The species occurring in >40% of the lotic and lentic sites evaluated were Conochilus dossuarius Hudson, 1885, Kellicottia bostoniensis (Rousselet, 1908), Keratella americana Carlin, 1943 K. cochlearis (Gosse, 1851) and Hexarthra mira (Hudson, 1871).

Our results indicate greater distribution ranges for several species. Colurella adriatica Ehrenberg, 1831, from the Foz do Areia Reservoir, is a new record for Brazil. Gastropus hyptopus (Ehrenberg, 1838) in the La Plata River and Harringia rousseleti de Beauchamp, 1912 and Lecane thienemanni (Hauer, 1938) in the Paraná River, are their first reports in Argentina. Finally, we expand the range of Enteroplea lacustris Ehrenberg, 1830, in São Paulo State (Brazil) and Lecane ludwigii (Eckstein, 1883) in Buenos Aires Province (Argentina).

Almost all the species are native, except Kellicottia bostoniensis which occurred in a new locality. Seven other species are Neotropical endemics (Table 2): Brachionus dolabratus Harring, 1914, B. mirus Daday, 1905, B. zahniseri Ahlstrom 1934, K. americana, Lecane amazonica (Murray, 1913), L. proiecta Hauer, 1956 and Testudinella ohlei Koste, 1972.

The mean ± standard deviations of water quality variables (Table 3) stratified by sub-basin reveals that the Tietê River has higher levels of total nitrogen, phosphorus, chlorophyll, and electrical conductivity. The Lower Paraná River also demonstrates high values for these variables except for nitrogen. Higher temperatures were found in the Paraguay and Iguaçu Rivers. The lowest levels of dissolved oxygen occurred in the Paraguay River. Spearman correlations indicated that total chlorophyll and water temperature were positively correlated with species richness; dissolved oxygen demonstrated a negative correlation (Table 4).

Discussion

We found a total of 106 rotifer species in the La Plata basin. Our data represent 14% of the rotifer species richness known to Brazil (Garraffoni & Lourenço 2012GARRAFFONI, A.R.S. & LOURENÇO, A.P. 2012. Synthesis of Brazilian Rotifera: An updated list of species. Check List 8(3):375-401.), 37% of that for São Paulo State (Souza-Soares et al. 2011SOUZA-SOARES, F., TUNDISI, J.G., MATSUMURA-TUNDISI, T., SOARES, F.S., TUNDISI, J.G. & MATSUMURA-TUNDISI, T. 2011. Checklist de Rotifera de água doce do Estado de São Paulo, Brasil. Biota Neotrop. 11(1a):515-539.), 30% of that for the Upper Paraná (Lansac-Tôha et al. 2009LANSAC-TÔHA, F.A., BONECKER, C.C., VELHO, L.F.M., SIMÕES, N.R., DIAS, J.D., ALVES, G.M. & TAKAHASHI, E.M. 2009. Biodiversity of zooplankton communities in the Upper Paraná River floodplain: interannual variation from long-term studies. Braz. J. Biol. 69(2 Suppl):539-49.), and 40% for the Upper Paraguay River (Branco et al. 2018BRANCO, C.W.C., SILVEIRA, R. de M.L. & MARINHO, M.M. 2018. Flood pulse acting on a zooplankton community in a tropical river (Upper Paraguay river, northern Pantanal, Brazil). Fundam. Appl. Limnol. 192(1):23-42.). Data from other inventories show that the rotifer fauna in the La Plata River basin is richer than what was demonstrated in our study, possibly because we sampled in few Uruguay and Paraguay River stretches, and exclusively in open water habitats, not in littoral. Therefore, as recommended by Ferrando & Claps (2016)FERRANDO, N.S. & CLAPS, M.C. 2016. A revised and updated checklist of Monogononta rotifers from Argentina. Check List 12(4):1-26., further investigations should be carried out to expand the distribution list of species in the La Plata River Basin.

The most diverse families were Lecanidae (21 spp.) and Brachionidae (20 spp.). These two families compose most rotifer species throughout Brazil and Argentina (Garraffoni & Lourenço, 2012GARRAFFONI, A.R.S. & LOURENÇO, A.P. 2012. Synthesis of Brazilian Rotifera: An updated list of species. Check List 8(3):375-401.; Ferrando & Claps, 2016FERRANDO, N.S. & CLAPS, M.C. 2016. A revised and updated checklist of Monogononta rotifers from Argentina. Check List 12(4):1-26.), supporting our findings.

The higher summer (wet season) rotifer richness may be associated with the concentrated rainfall events that occur during this season. Summer rains can carry nutrients and organic matter from the margins of aquatic environments resulting in increased food concentration and a reduction in competition for resources. The same tendency was observed for the rainy season in a study performed on a tropical lake in Mexico (Jiménez-Contreras et al. 2018JIMÉNEZ-CONTRERAS, J., NANDINI, S. & SARMA, S.S.S. 2018. Diversity of Rotifera (Monogononta) and Egg Ratio of Selected Taxa in the Canals of Xochimilco (Mexico City). Wetlands 38: 1033-1044.). Richness may also be related to the sediment mixture caused by intense rains. This process provides a favorable condition for hatching of dormant stages (i.e., resting eggs), resulting in an increase in rotifer species richness.

Greater rotifer species richness was observed in the Lower Paraná sub-basin. Rotifers have low locomotion capacity and are carried by drifting through the central channel of the river and consequently the species richness increase towards downstream.

Barra Bonita Reservoir in the Tietê River sub-basin was the site with the greatest richness. Despite being a reservoir with a high degree of anthropogenic disturbance, including eutrophication (Tundisi et al. 2008TUNDISI, J.G., MATSUMURA-TUNDISI & ABE. 2008. The ecological dynamics of Barra Bonita (Tietê River, SP, Brazil) reservoir: implications for its biodiversity. Braz. J. Biol 68(4):1079-1098.), many studies have shown high biodiversity for other groups, which include rotifers (Matsumura-Tundisi & Tundisi 2005MATSUMURA-TUNDISI, T. & TUNDISI, J.G. 2005. Plankton richness in a eutrophic reservoir (Barra Bonita Reservoir, SP, Brazil). Hydrobiologia 542(1):367-378., Rocha et al. 2006ROCHA, O., TAVARES, K.S., BRANCO, M.B.C., PAMPLIN, P.A.Z., ESPINDOLA, E.L.G. & MARCHESE, M. 2006. Biodiversity in reservoirs and relationships with the eutrophication processes. In: . In Eutrophication in South America: causes, consequences, and technologies for management and control ( C. Tundisi, J.G., Matsumura-Tundisi, T, Sidagis Galli, ed.) IIE; IIEGA; Brazilian Academy of Sciences; IANAS; IAP, São Carlos, Brazil, p.531.). In the Barra Bonita Reservoir, Matsumura-Tundisi & Tundisi (2005)MATSUMURA-TUNDISI, T. & TUNDISI, J.G. 2005. Plankton richness in a eutrophic reservoir (Barra Bonita Reservoir, SP, Brazil). Hydrobiologia 542(1):367-378. found 32 species of rotifers. However, in our work we found 22 species. The Spearman correlation suggested a positive relation between richness and chlorophyll levels, with Barra Bonita Reservoir demonstrating the highest values of observed chlorophyll. Presumably, this higher richness is a result of greater numbers of tolerant rotifer species (Allen et al. 1999ALLEN, A.P., WHITTIER, T.R., KAUFMANN, P.R., LARSEN, D.P., O’CONNOR, R.J., HUGHES, R.M., STEMBERGER, R.S., DIXIT, S.S., BRINKHURST, R.O, HERLIHY, A.T. & PAULSEN, S. G. 1999. Concordance of taxonomic richness patterns across multiple assemblages in lakes of the northeastern United States. Can. J. Fish. Aquat. Sci. 56(5): 739-747.).

The commonest species in the La Plata basin were Keratella americana, K. cochlearis, and Hexarthra mira. Others have reported the occurrence these species in the Uruguay (Di Persia & Neiff 1986DI PERSIA, D.H. & NEIFF, J.J. 1986. The Uruguay River system. In The ecology of river systems (W. K. F. Davies B.R., ed.) Springer Netherlands, The Netherlands, p.599-629.), Paraguay (Frutos et al. 2006FRUTOS, S.M., POI DE NEIFF, A.S.G. & NEIFF, J.J. 2006. Zooplankton of the Paraguay River: A comparison between sections and hydrological phases. Ann. Limnol. 42(4):277-288., Branco et al. 2018BRANCO, C.W.C., SILVEIRA, R. de M.L. & MARINHO, M.M. 2018. Flood pulse acting on a zooplankton community in a tropical river (Upper Paraguay river, northern Pantanal, Brazil). Fundam. Appl. Limnol. 192(1):23-42.) and Upper Paraná Rivers (Bonetto & Wais 2006BONETTO, A.A. & WAIS, I.R. 2006. Southern South American Streams and Rivers. In River and Stream Ecosystems of the World: With a New Introduction (M. G. W. Cushing C.E., Cummins K.W., ed.) University of California Press, Berkeley, p.257-293.), indicating the wide distribution of these rotifers in the study area.

Colurella has been found in several inland waters (Arroyo-Castro et al. 2019ARROYO-CASTRO, J., ALVARADO-FLORES, J., UH-MOO, J.C. & KOH-PASOS, C.G. 2019. Monogonot rotifers species of the island Cozumel, Quintana Roo, México. Biodivers. Data J. 7(e34719):1-13., Tasevska et al. 2019TASEVSKA, O., GUSESKA, D. & KOSTOSKI, G. 2019. A Checklist of Monogonont Rotifers ( Rotifera : Monogononta ) of Lake Ohrid , Republic of Macedonia. Acta Zool. Bulg. Suppl. 13: 57-62., Wei et al. 2019WEI, N., JERSABEK, C.D., XU, R. & YANG, Y. 2019. New species and records of Colurella (Rotifera: Lepadellidae) from South China, with a key to Chinese colurella. Zootaxa 4586(3):475-490. ). In the La Plata Basin we found two species of this genus: Colurella adriatica Ehrenberg, 1831 and C. obtusa (Gosse, 1886). Colurella adriatica originates in the Adriatic Sea and has been described as endemic (Ehrenberg 1831), but it is now widely distributed, including in Neotropical regions (Segers 2007SEGERS, H. 2007. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564(1):1-104.). We found it in Foz do Areia Reservoir, in the Iguaçu sub-basin, Paraná State, which is its first record in Brazil.

Enteroplea lacustris is widely distributed in the Australasia, Neoarctic, Neotropical, Oriental, and Paleoarctic regions (Segers 2007SEGERS, H. 2007. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564(1):1-104.). In Brazil, it occurs in Mato Grosso do Sul (Roche & Silva 2017ROCHE, K.F. & SILVA, W.M. 2017. Checklist dos Rotifera (Animalia) do Estado de Mato Grosso do Sul, Brasil. Iheringia. Série Zool. 107(suppl):1-10.) and Paraná States in the Paranapanema River basin (Dias et al. 2011DIAS, J.D., TAKAHASHI, É.M., SANTANA, N.F. & BONECKER, C.C. 2011. Impact of fish cage-culture on the community structure of zooplankton in a tropical reservoir. Iheringia. Série Zool. 101(1-2):75-84., Roche & Silva 2017ROCHE, K.F. & SILVA, W.M. 2017. Checklist dos Rotifera (Animalia) do Estado de Mato Grosso do Sul, Brasil. Iheringia. Série Zool. 107(suppl):1-10.). We found it in Três Irmãos Reservoir, Tietê sub-basin, São Paulo State, near the Paraná River, indicating a gap in previous studies of this region.

For Argentina, Ferrando & Claps (2016)FERRANDO, N.S. & CLAPS, M.C. 2016. A revised and updated checklist of Monogononta rotifers from Argentina. Check List 12(4):1-26. recorded 351 species of monogonont rotifers from lotic and lentic environments. Among the species they recorded, we found 43 (12.2%). Three other species of rotifers (Gastropus hyptopus, Harringia rousseleti, and Lecane thienemanni) found in our study are new records for Argentina. Gastropus hyptopus was found in the La Plata River Basin, in Rosario, Argentina. In Brazil, it had been registered in several regions (Serafim Jr. et al. 2003SERAFIM JR., M., LANSAC-TÔHA, F.A., PAGGI, J.C., VELHO, L.F.M. & ROBERTSON, B. 2003. Cladocera fauna composition in a river-lagoon system of the upper Paraná River floodplain, with a new record for Brazil. Braz. J. Biol. 63(2):349-356., Bonecker et al. 2005BONECKER, C.C., DA COSTA, C.L., MACHADO VELHO, L.F. & LANSAC-TÔHA, F.A. 2005. Diversity and abundance of the planktonic rotifers in different environments of the Upper Paraná River floodplain (Paraná State - Mato Grosso do Sul State, Brazil). Hydrobiologia 546(1):405-414., Serafim-Júnior et al. 2010SERAFIM-JÚNIOR, M., PERBICHE-NEVES, G., BRITO, L. De, GHIDINI, A.R. & CASANOVA, S.M.C. 2010. Variação espaço-temporal de Rotifera em um reservatório eutrofizado no sul do Brasil. Iheringia. Série Zool. 100(3):233-241., Souza-Soares et al. 2011SOUZA-SOARES, F., TUNDISI, J.G., MATSUMURA-TUNDISI, T., SOARES, F.S., TUNDISI, J.G. & MATSUMURA-TUNDISI, T. 2011. Checklist de Rotifera de água doce do Estado de São Paulo, Brasil. Biota Neotrop. 11(1a):515-539.). Harringia rousseleti and L. thienemanni were recorded for the first time in Argentine reaches of the Paraná River, in the Bella Vista municipality. A new locality was found for L. ludwigii, which had been recorded in Corrientes Province (José de Paggi 1996JOSÉ DE PAGGI, S. 1996. Rotifera (Monogononta) diversity in subtropical waters of Argentina. Annls Limnol 32(4):209-220.); however, there is no previous record in the La Plata River estuary where we collected it.

We found a non-native species in the La Plata River basin, Kellicottia bostoniensis (Rousselet, 1908), which is native to North America (Edmondson 1959EDMONDSON, W.T. 1959. Rotifera. In reshwater Biology (W. T. Edmondson, ed.) Wiley and Sons, New York, p.420-484.). For Argentina, José de Paggi (2002)JOSÉ DE PAGGI, S. 2002. New data on the distribution of Kellicottia bostoniensis (Rousselet, 1908) (Rotifera: Monogononta: Brachionidae): Its presence in Argentina. Zool. Anz. 241(4):363-368. first recorded the species in the Iguaçu River and Salto Grande Reservoir. We found the species in the La Plata River (Uruguay and Argentina reach), where there were no prior records of it. We thus extended the known distribution of K. bostoniensis. It is possible that its occurrence in the La Plata basin is related to aquaculture activities as has occurred in other regions (Coelho & Henry 2017COELHO, P.N. & HENRY, R. 2017. The small foreigner: new laws will promote the introduction of non-native zooplankton in Brazilian aquatic environments. Acta Limnol. Bras. 29(e7).). In many reservoirs of the La Plata basin, there are aquaculture activities, mainly with non-native fish species (Azevedo-Santos et al. 2011AZEVEDO-SANTOS, V.M., RIGOLIN-SÁ, O. & PELICICE, F.M. 2011. Growing, losing or introducing? Cage aquaculture as a vector for the introduction of non-native fish in Furnas Reservoir, Minas Gerais, Brazil. Neotrop. Ichthyol. 9(4):915-919., Nobile et al. 2018NOBILE, A.B., ZANATTA, A.S., BRANDÃO, H., ZICA, E.O.P., LIMA, F.P., FREITAS-SOUZA, D., CARVALHO, E.D., SILVA, R.J. da & RAMOS, I.P. 2018. Cage fish farm act as a source of changes in the fish community of a Neotropical reservoir. Aquaculture 495: 780-785.). This rotifer may be introduced from cage aquaculture in upstream rivers (e.g., Grande and Paranapanema Rivers) and reached downstream areas where we captured it.

Seven Neotropical endemic species (sensu José de Paggi 1996JOSÉ DE PAGGI, S. 1996. Rotifera (Monogononta) diversity in subtropical waters of Argentina. Annls Limnol 32(4):209-220.) were found in the La Plata River basin. Their presence highlights the importance of preserving the condition of these ecosystems. However, anthropogenic stressors imperil many areas where these seven species occur. For example, in the Barra Bonita and Três Irmãos Reservoirs, where Brachionus dolobratus, B. mirus, and L. proiecta were captured, waters are polluted (Rodgher et al. 2005RODGHER, S., ESPÍNDOLA, E.L., ROCHA, O., FRACÁCIO, R., PEREIRA, R.H. & RODRIGUES, M.H. 2005. Limnological and ecotoxicological studies in the cascade of reservoirs in the Tietê River (São Paulo, Brazil). Braz. J. Biol. 65(4):697-710., Favaro et al. 2018FAVARO, D.I.T., ROCHA, F.R., ANGELINI, M., A HENRIQUES, H.R., SOARES, J.S., SILVA, P.S.C. & OLIVEIRA, S.M.B. 2018. Metal and trace element assessments of bottom sediments from medium Tietê River basin, São Paulo State, Brazil: part II. J. Radioanal. Nucl. Chem. 316: 805-818.). Similarly, eutrophic tributaries in the Grande River sub-basin (Melo et al. 2017MELO, R.R.R., COELHO, P.N., SANTOS-WISNIEWSKI, M.J., WISNIEWSKI, C. & MAGALHÃES, C.S. 2017. Morphological abnormalities in cladocerans related to eutrophication of a tropic reservoir. J. Limnol. 76(1):94-102.) may affect endemic rotifer species. Another example is the occurrence of L. amazonica in the La Plata River; which also receives water from these polluted river basins. Conservation policies must be discussed for the entire La Plata system because of fluvial connectivity (Azevedo-Santos et al. 2019AZEVEDO-SANTOS, V.M., FREDERICO, R.G., FAGUNDES, C.K., POMPEU, P.S., PELICICE, F.M., PADIAL, A. A., NOGUEIRA, M.G., FEARNSIDE, P.M., LIMA, L.B., DAGA, V.S., OLIVEIRA, F.J.M., VITULE, J.R.S., CALLISTO, M., AGOSTINHO, A.A., ESTEVES, F.A., LIMA-JUNIOR, D.P., MAGALHÃES, A.LB., SABINO, J., MORMUL, R.P., GRASEL, D., ZUANON, J., VILELLA, F. & HENRY, R. 2019. Protected areas: A focus on Brazilian freshwater biodiversity. Divers. Distrib. 25:442-448.).

In conclusion, surveys covering wide spatial extents, such as in our study, are important for increasing the knowledge of species diversity and distribution. Our findings may contribute to future monitoring studies as well as management and conservation programs for the La Plata River basin. Finally, we recommend that future rotifer surveys should be concentrated in Paraguay and Uruguay River reaches because of the scarcity of data from them.

Acknowledgments

We are grateful for the three anonymous reviewers, for important suggestions and R. M. Hughes for English editing. This work was supported by: FAPESP 2008/02015-7 and 2009/00014-6; CAPES #88882.180513/2018-01; and CNPq 141323/2018-3

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