Ictiofauna de riachos da bacia do baixo rio Iguaçu, estado do Paraná, Brasil

bn Biota Neotropica Biota Neotrop. 1676-0611 Instituto Virtual da Biodiversidade | BIOTA - FAPESP Resumo As drenagens da bacia do rio Iguaçu, bem como o canal principal do rio, possuem características peculiares resultantes de processos geomorfológicos dessa área, incluindo a formação das Cataratas do rio Iguaçu. Esse desnível na porção inferior da bacia constitui uma barreira biogeográfica para muitos organismos. Neste trabalho inventariamos a fauna de peixes de riachos na porção do baixo rio Iguaçu, avaliando possíveis diferenças na composição de espécies acima e abaixo dessa barreira biogeográfica. Entre 2004 e 2013, foram amostrados cinco riachos, sendo três localizados acima das Cataratas do Iguaçu e dois abaixo, por meio de pesca elétrica. Para investigar possíveis padrões de agrupamentos de fauna similares entre os riachos amostrados foi realizada uma análise nMDS, cujos escores foram testados quanto à significância dos agrupamentos utilizando o teste de T2 de Hotelling. O valor indicador (IndVal) foi usado para detectar a distribuição das espécies entre os grupos de riachos. Foram amostrados 18.908 indivíduos, pertencentes a seis ordens, 11 famílias e 40 espécies. As ordens Siluriformes e Characiformes destacaram-se em riqueza de espécies; Cyprinodontiformes apresentou maior abundância. Do total de espécies amostradas, 21 são consideradas nativas da bacia do rio Iguaçu, sendo 15 delas endêmicas e registradas somente nos riachos acima das Cataratas do rio Iguaçu. Outras 18 espécies foram registradas somente nos riachos que desembocam abaixo das cataratas. Quatro espécies foram comuns em ambos os ambientes. A dimensão do eixo 1 da análise nMDS resultou na separação de dois grupos: riachos acima (S1, S2 e S3) e riachos abaixo das cataratas (S4 e S5). A análise de espécies indicadoras também indicou a distinção entre os grupos de riachos, sendo que esses agrupamentos foram significativamente diferentes (Hotelling's T2 = 234.36, p ˂ 0.0001). O número de espécies endêmicas registrado nos riachos acima das cataratas (15 spp.), demonstra um significativo efeito de isolamento da fauna proporcionado pelas Cataratas do rio Iguaçu e confirmam o papel dessa barreira nos processos vicariantes e endemismos característicos dessa bacia. Esses resultados ressaltam a importância da preservação desses ecossistemas, pois a extinção de espécies nessa região significa a perda global dessas entidades biológicas. Introduction The Paraná State, Southern Brazil, has 16 basins (Parolin et al. 2010), including the Iguaçu River basin, formed by the longest river in the Paraná State with approximately 1,080 km (Garavello et al. 2012). The formation of its basin dates back to the Mesozoic era and the beginning of the Paleozoic and was associated with staggered movements of uplift of the Serra do Mar (Parolin et al. 2010). Considering the confluence of the Atuba and Iraí rivers as its origin, the Iguaçu River runs in the east-west direction from its headwaters in the Serra do Mar to its mouth on the Paraná River (Baumgartner et al. 2012). Along its course, it crosses different geological and geomorphological units, with an altitude range of 830 m, considered as a typical plateau river, with numerous rapids and falls. Among these, stands out the Iguaçu River Falls with 82 meters, in addition to other hundreds of waterfalls in the basin, which result from the geological structure caused by basaltic spills. The Iguaçu River and its tributaries features a fauna of small-sized fish, with a high degree of endemism (Vicari et al. 2006), possibly due to the geographical isolation given by the Iguaçu River Falls that isolated this river from the lower Paraná River basin (Baumgartner et al. 2012). Biogeographical barriers are a key factor in the composition of regional faunas and especially in promoting endemism (Rahel 2007). Besides, the presence of barriers, such as waterfalls, promotes geographical isolation of habitats that increase the speciation rate in these isolated environments (Cracraft 1982), mainly by limiting gene flow, and promoting the diversification of species (Meeuwig et al. 2010). These barriers determine the degree of connectivity of water bodies within the basin, directing the speciation process by influencing the availability of habitats for aquatic species (Dias et al. 2012). The geological event that formed the Iguaçu River Falls back to the Cretaceous period 130 million years ago (Parolin et al. 2010), which has possibly generated a cladogenic event for most fish species of the Iguaçu River. According to Rahel (2007), the Iguaçu River Falls are classified as a barrier level three for the movement of fish, that is, they promote the isolation of the fish fauna within a basin, ensuring that these species do not colonize other regions unless by human intervention. In the Iguaçu River basin, 75% of fish species are endemic (Zawadzki et al. 1999), but this fauna has undergone changes mainly caused by human activities (Baumgartner et al. 2006). Rapid population growth leads to urban sprawl and expansion of agriculture increasingly closer to freshwater environments, affecting negatively the physical and biological structure of these environments (Cunico et al. 2006, Pereira et al. 2014). In this way, besides the threat that human activities cause, there are few studies on streams in the Paraná State (Pavanelli & Caramaschi 2003, Cunico et al. 2006, 2009, Galves et al. 2007, Araujo et al. 2011, Daga et al. 2012, Delariva & Silva 2013). In the Iguaçu River basin, stand out the studies conducted in the upper reach of the basin (Suzuki et al. 1997, Vitule & Abilhoa 2003) and surveys of species in streams of the lower Iguaçu River (Suzuki et al. 1997, Bifi et al. 2006, Baumgartner et al. 2012). Most rivers and streams forming the Iguaçu River basin are located upstream of the Iguaçu River Falls, but some streams have connection downstream of this barrier, which is located about 18 km upstream of the mouth of the Iguaçu River into the lower Paraná River basin. Although belonging to the Iguaçu River basin, these streams may have been affected by the same cladogenic event and hold a fish fauna similar to that observed for the Paraná River basin. In this sense, aiming to investigate the fish fauna composition of streams upstream and downstream of the Iguaçu River Falls, this study surveyed the fish fauna in first- and second-order streams of the lower Iguaçu River basin. Thus, this study provides a list of species, showing the occurrence and expansion of distribution and identified possible dissimilarities between the fish faunas located in these sections (up- and downstream of the falls). Material and Methods 1. Study Area The Iguaçu River basin encompasses an area of 55,108.04 km² in the Paraná State, covering 116 municipalities (Parolin et al. 2010) and is subdivided into three hydrographical units: upper, middle, and lower Iguaçu River. In the lower stretch is located the Iguaçu River Falls, in the municipality of Foz do Iguaçu, PR, considered the largest falls in volume of water on the planet, which fall through a deep crevice, with an gap of 72 meters and an average volume of 1.551 m³/second (SEMA 2013). On the Brazilian side of the Iguaçu River Falls and vicinity of the Iguaçu River in this region, is situated the Iguaçu National Park, a conservation unit essential for the country's biodiversity, because it protects the Iguaçu River Falls and constitutes the largest remnant area of preservation of semideciduous forest of the Paraná State. In the lower Iguaçu River region, the main economic activity is agriculture, especially the cultivation of soybeans and corn, and pastures, which was the prevailing scenario in the vicinity of the streams sampled. The basins of the studied streams drain, directly or indirectly, into the Iguaçu River, however, flow into upstream (S1, S2, S3) and downstream (S4 and S5) of the Iguaçu River Falls (Figure 1). So, they are separated and susceptible to geographic isolation generated by this natural barrier. Figure 1 Streams studied in the lower Iguaçu River basin, Paraná State, Brazil. 2. Fish sampling The sampling of the fish fauna was performed between 2004 and 2013 in five streams, totaling 11 sampling sites. Samplings were conducted in different periods: Padres River (S1) - quarterly at two sites, between July 2004 and December 2005, with two samplings in 2006 (March and May); Cascavel River (S2) - quarterly samples at two sites between August 2011 and February 2012; Jumelo Stream (S3) - an unique site on the headwaters in September and November 2011, March and July 2012 and July 2013; Poço Preto Stream (S4) and Arroio Dourado Stream (S5) - sampled at three sites every four months between May 2010 and April 2011. The main physical characteristics and geographical coordinates are shown in Table 1. Fish were collected by electrofishing technique with three paces of 40 minute in 50 meters length at each reach. The electrofishing equipment was powered by a portable generator (Honda, 2.5 kW, 220 V, 3 - 4 A) connected to a DC transformer, with two electrified net rings (anode and cathode). Output voltage varied from 400 to 600 V, and we installed blocking nets (mesh size 5 mm) at the ends of each reach to prevent the escape of fish. After sampling, specimens were sacrificed in a solution of clove oil (Eugenol, 2 drops per liter; cf. American Veterinary Medical Association 2001), and fixed in 10% formalin and then preserved in 70% alcohol. Table 1 Physical characteristics of the sampled sites in Iguaçu River basin, Paraná State. Brazil. S1, S2 until S5 = Stream's number. P1, P2, P3 until P11 = sampled portions SITES COORDINATES WIDTH (m) DEPTH (m) PREDOMINANT SUBSTRATE RIPARIAN VEGETATION PHYSIOGRAPHY CHANNEL OBSERVATIONS Padres River (S1) P1-25°40'34.81"S 52°37'6.05"W P2-25°39'34.777"S 52°38'2.514"W P1-2.00-4.10 P2-2.00- 4.10 P1-0.10-0.28 P2-0.10-0.55 Muddy alternated with argil in the lower stretch, rubble in the upper stretch, and small amount of shelters. Variables ranges of trees and shrubs Low-speed stream in both of the points. Wide range of soil devoid of vegetation, because is within of rural areas. Cascavel River (S2) P3-24°58'33.57"S 53°26'6.41"W P4-25°0'32.10"S 53°26'11.10"W P3-1.00-2.50 P4-1.00-3.00 P3-0.30-0.60 P4-0.40-0.70 Rubble predominant in both of the points. P3- present in only one of the edges; P4- present in both of the banks Low-speed stream in all of the sites sampled. The sites sampled are within of the urban areas. Jumelo (S3) (headwater stretch) P5-25°04'46.62"S 53°37'26.42" W P5-2.00-4.00 P5-0.20-1.00 Rocky, rubble, pebble and silt. Right bank with Riparian vegetation preserved. Left bank with range of trees and shrubs between 5 and 10 m. Rapids with mean depth of 0.30 m, and pools of up to 1.00 m in depth. The right bank belongs to Iguaçu National Park, a area of preservation. The left bank is within of rural areas. Poço Preto (S4) P6-25°36'48.04"S 54°25'54.09"W P7-25°37'19.3"S 54°26'52.6"W P8-25°37'40.5"S 54°26'53"W P6-1.00 -1.89 P7-1.60-2.88 P8-2.70-3.41 P6-0.20-0.49 P7-0.55-0.90 P8-2.30-2.95 Partially rocky substrate with different grain textures. Riparian vegetation on both banks composed of pionners formations of rainforest river influence. Predominance of rapids. Located inside of a area of preservation (Iguaçu National Park). Arroio Dourado (S5) P9-25°34'19.3"S 54°30'16.4"W P10- 25°34'16"S 54°30'19.2"W P11- 25°34'14.8"S 54°30'24.1"W P9-1.80-2.24 P10- 2.00- 2.96 P11- 2.50- 3.10 P9-0.10-0.29 P10- 0.22- 0.39 P11- 0.10- 0.15 Partially rocky substrate with different grain textures. Riparian vegetation on both banks composed of pionners formations of rainforest river influence. Predominance of rapids. Soil around mainly occupied by pastures. Specimens were identified according to Baumgartner et al. (2012), Garavello et al. (2012), Garavello & Sampaio (2010), and Graça & Pavanelli (2007). Voucher specimens were deposited at the fish collection of Nupélia (Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura), Universidade Estadual de Maringá- UEM, and at the fish collection of Gerpel (Grupo de Pesquisas em Recursos Pesqueiros e Limnologia) - Universidade Estadual do Oeste do Paraná - UNIOESTE. 3. Data Analysis To identify possible groupings of similar fauna between streams, we applied a non-metric multidimensional scaling analysis (nMDS) to summarize the composition of fish assemblages using the Jaccard distance and following the general nMDS procedure proposed by McCune & Grace (2002). We obtained a confidence index (Stress), which determines the degree of proximity of the graphical representation to the real data. Stress values below 0.20 allow potential two-dimensional (2D) use of the nMDS. Data were randomized 100 times, and the stability criterion was 0.005 standard deviations in the stress after 200 iterations. This analysis was carried out using the numerical abundance matrix of each sampling site and month. To test the null hypothesis of no difference in composition of the fish assemblage between sites upstream and downstream of the falls summarized by the nMDS, we used a multivariate pairwise comparisons between two groups (upstream and downstream of the falls), using the Hotelling T2 test. This analysis indicates whether a multidimensional sample belongs to a particular multidimensional group. As closer sites have a higher chance to be similar, we applied a Euclidean distance on UTM (site coordinates), obtaining proportional geographic distances between them. We used a Mantel's test on the distances between fish assemblage abundances matrix (nMDS) and geographic distances matrix with the objective of controlling possible geographical effects. Both results were reported based on 10.000 permutations. The indicator value method (IndVal; Dufrêne & Legendre 1997) was used to detect how differently each species is distributed among the groups of the streams upstream and downstream of the Iguaçu River Falls. The indicator value of a species varies from 0 to 100, and it reaches its maximum value when all individuals of a species occur in all sites within a single nMDS group. All analyses were run in the software Past (Hammer et al. 2001), except the indicator value method, performed in the PCOrd® 6.0 (McCune & Mefford 2011). Results In total, we collected 18,908 individuals belonging to six orders, 11 families, and 40 species (Table 2). Siluriformes was the most representative with 50% of the species richness, followed by Characiformes (31%). As to numerical abundance, the most representative was Cyprinodontiformes (64%), followed by Characiformes (23%) and Siluriformes (11%). Characidae and Loricariidae were the highest in number of species (22% each). The largest-sized species was Synbranchus cf. marmoratus Bloch, 1795 (53.7 cm total length), and the smallest specimen was Phalloceros harpagos Lucinda, 2008, with standard length (SL) of 0.6 cm. Table 2 List of fish species and their respective abundances at sampling stations in Iguaçu River basin. Systematic positions were based on Nelson (2006) to all orders, and Siluriformes families; Reis et al. (2003) to others families, except Characidae that follow Mirande (2009). The column "Origin" refers to species classified in native (N) and non-native (NN) to the of lower Paraná River and Iguaçu River basins. S = sites of sampling. NUP - vouchers specimens deposited in Fish Collection of Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura - Nupélia; and CIG - vouchers specimens deposited in Fish Collection of Grupo de Pesquisas em Recursos Pesqueiros e Limnologia - Gerpel. Taxon Common name Origin Voucher specimens Lower Paraná River Iguaçu River S1 S2 S3 S4 S5 Total CHARACIFORMES Crenuchidae Characidium sp. 1 N NN x x 42 CIG 1410, CIG 1422 Characidium sp. 2 NN N x 27 NUP 2110 Characidae Astyanax sp. 1 N NN x x 621 CIG 2277 Astyanax sp. 2 N NN x 77 CIG 2259, CIG 2283 Astyanax sp. 3 N NN x 154 CIG 2284 Astyanax lacustris (Lütken, 1875) ex Astyanax altiparanae Garutti & Britski, 2000 (Lucena & Soares, 2016) "lambari-do-rabo-amarelo" N N x x 30 CIG 1480 Astyanax bifasciatus Garavello & Sampaio, 2010 "lambari-do-rabo-vermelho" NN N x x x 3764 CIG 2239, NUP 16945 Astyanax dissimilis Garavello & Sampaio, 2010 "lambari" NN N x 7 NUP 16940 Astyanax serratus Garavello & Sampaio, 2010 "lambari" NN N x 11 CIG 2381 Bryconamericus iheringii (Boulenger, 1887) "lambarizinho" N NN x 13 CIG 1445 Oligosarcus longirostris Menezes & Géry, 1983 "saicanga" NN N x 1 NUP 11856 Bryconamericus pyahu Azpelicueta, Casciotta & Almirón, 2003 "lambarizinho" NN N x 2 NUP 12089 Erythrinidae Hoplias aff. malabaricus (Bloch, 1794) "traíra" N N x x 15 CIG 2242 Erythrinus erythrinus (Block & Schneider, 1801) "jejú" N NN x 2 CIG 1446 SILURIFORMES Trichomycteridae Trichomycterus sp. 1 "candiru" NN N x 317 NUP 12660 Trichomycterus sp. 2 "candiru" NN N x 83 NUP 12661 Trichomycterus sp. 3 "candiru" N NN x x 126 CIG 1416, CIG 1432 Trichomycterus davisi (Haseman, 1911) "candiru" NN N x 186 CIG 2241, CIG 2245 Trichomycterus taroba Wosiacki & Garavello, 2004 "candiru" N N x 169 NUP 3125 Callichthyidae Corydoras sp. "limpa-vidro" N NN x 151 NUP 14261 Loricariidae Ancistrus sp. "cascudo-roseta" NN N x 30 NUP 4140, NUP 4489 Ancistrus mullerae Bifi, Pavanelli & Zawadzki, 2009 "cascudo-roseta" NN N x 489 NUP 16942 Hisonotus sp. "cascudinho limpa-vidro" NN N x x 43 CIG 2261 Hypostomus ancistroides (Ihering, 1911) "cascudo" N NN x 2 CIG 1448 Hypostomus albopunctatus (Regan, 1908) "cascudo" N N x x 15 CIG 1444 Hypostomus derbyi (Haseman, 1911) "cascudo" NN N x x 129 NUP 4134 Hypostomus myersi (Gosline, 1947) "cascudo" NN N x 4 NUP 6239 Hypostomus sp. "cascudo" N NN x 4 CIG 1420, CIG 1485 Heptapteridae Heptapterus mustelinus (Valenciennes, 1835) "bagrinho, bagre-pedra" N NN x 46 CIG 1439 Rhamdia branneri Haseman, 1911 "bagre", "jundiá" NN N x x 23 CIG 2258, NUP 16941 Rhamdia voulezi Haseman, 1911 "bagre", "jundiá" NN N x x 54 NUP 11185, NUP 5678 Rhamdia aff. quelen (Quoy & Gaimard, 1824) "bagre", "jundiá" N NN x x 119 CIG 1475, CIG 1418 GYMNOTIFORMES Gymnotidae Gymnotus sylvius Albert & Fernandes-Matioli, 1999 "morenita" NN NN x x 123 CIG 1442 Gymnotus inaequilabiatus (Valenciennes, 1839) "morenita" N NN x 10 CIG 1441 Gymnotus pantanal Fernandes, Albert, Daniel-Silva, Lopes, Crampton & Almeida-Toledo, 2005 "morenita" N NN x 9 CIG 1451 CYPRINODONTIFORMES Poeciliidae Phalloceros harpagos Lucinda, 2008 "barrigudinho", "guaru" N N x x x x 11940 CIG 1427, NUP16943 Poecilia reticulata Peters, 1859 "barrigudinho", "guaru" NN NN x 10 CIG 2272 SYNBRANCHIFORMES Synbranchidae Synbranchus cf. marmoratus Bloch, 1795 "muçum" N NN x x x 16 CIG 1449, CIG 1434 PERCIFORMES Cichlidae Crenicichla britskii Kullander, 1982 "joaninha" N NN x x 21 CIG 1483 Oreochromis niloticus (Linnaeus, 1758) "tilápia" NN NN x x 23 CIG 2273 Total number 15826 262 1056 1270 494 18908 Richness 40 Among the species sampled, 12 are possibly not described, already that they presented morphological characters different from their congeners currently described for the region. In such cases, Characidium sp. 2, Trichomycterus sp. 1, Trichomycterus sp. 2, and Ancistrus sp. were sensuBaumgartner et al. (2012), and Characidium sp. 1 was sensuGraça & Pavanelli (2007). Regarding the origin of the species, 21 were native to the Iguaçu River basin (Table 2). In terms of occurrence, 27 species have already been recorded in previous studies and other 13 are new records for the Iguaçu River basin (Astyanax sp. 3, Bryconamericus iheringii (Boulenger, 1887), Hoplias aff. Malabaricus (Bloch, 1794), Erythrinus erythrinus (Block & Schneider, 1801), Trichomycterus sp. 3, Corydoras sp., Hypostomus ancistroides (Ihering, 1911), Hypostomus sp., Heptapterus mustelinus (Valenciennes, 1835), Rhamdia aff. quelen (Quoy & Gaimard, 1824), Gymnotus pantanal Fernandes, Albert, Daniel-Silva, Lopes, Crampton & Almeida-Toledo, 2005, Poecilia reticulata Peters, 1859, and Crenicichla britskii Kullander, 1982). Of the total species sampled, 15 were endemic to the Iguaçu River basin, and observed only in streams which discharge into upstream of the Iguaçu River Falls. Still, 18 species were sampled only in streams which flow into downstream of this barrier. Only four species were common to both environments (Gymnotus sylvius Albert & Fernandes-Matioli, 1999, Oreochromis niloticus (Linnaeus, 1758), Phalloceros harpagos, and Synbranchus cf. marmoratus). In the stream S1, we collected 12 species, where the most abundant in number was Phalloceros harpagos and in biomass was Astyanax bifasciatusGaravello & Sampaio, 2010. The high numerical abundance of Phalloceros harpagos in this stream gave greater prominence to Cyprinodontiformes. Of the 12 species recorded in this stream, nine are endemic and the other three (Hoplias aff. malabaricus, Trichomycterus davisi (Haseman, 1911), and Phalloceros harpagos) are considered autochthones species (with distribution in other basins). Among the endemic species, two are considered not described (Ancistrus sp. e Characidium sp. 2) and are in the process of description (Baumgartner, D., pers. comm.). In the stream S2, we sampled eight species, wherein Astyanax bifasciatus was the most abundant in number (45%), and Gymnotus sylvius showed the highest biomass. This environment contained only one species endemic to the Iguaçu basin (Astyanax bifasciatus). Among the others, two are native with distribution in other basins (Hoplias aff. malabaricus and Phalloceros harpagos) and four were considered introduced (Gymnotus sylvius, Poecilia reticulata, Oreochromis niloticus, and Synbranchus cf. marmoratus). For the stream S3, we identified 10 species, including Ancistrus mulleraeBifi, Pavanelli & Zawadzki, 2009, a species endemic to the lower Iguaçu River, with the highest abundance, both in number and biomass (46% and 37%, respectively). In this study, it was only registered in this stream. All species caught in this stream were considered endemic, except for Phalloceros harpagos, with wide distribution in other basins. Two species (Trichomycterus sp. 1 e Trichomycterus sp. 2) are still possibly not described (sensuBaumgartner et al. 2012). In the stream S4, we captured 11 species: Astyanax sp. 1 presented higher abundances both number and biomass (48% and 41%, respectively). Of the species caught, five were identified only to the genus level and probably they are still not described, because they do not present the same morphological characters of other already found in the literature (Astyanax, Characidium, Corydoras, Hisonotus, and Trichomycterus). It should be noted that Corydoras sp. has been recorded exclusively in this stream (Tencatt, L. pers. comm.). In the stream S5, we sampled 21 species, and observed high numerical abundance of the Astyanax sp. 3 and higher biomass of Gymnotus sylvius (28% and 24%, respectively). In this stream, as in the stream S4, seven species have possibly not been described. Six species were considered as non-native, one exotic (Oreochromis niloticus) and five allochthonous (Bryconamericus iheringii, Erythrinus erythrinus, Gymnotus inaequilabiaus (Valenciennes, 1839), Gymnotus sylvius and Gymnotus pantanal) (Graça & Pavanelli 2007, Langeani et al. 2007, Baumgartner et al. 2012). Six species (Astyanax altiparanae Garutti & Britski, 2000, Hypostomus albopunctatus (Regan, 1908), Gymnotus sylvius, Gymnotus inaequilabiatus, Synbranchus cf. marmoratus and Oreochromis niloticus) were previously recorded in the lower Iguaçu River (sensuBaumgartner et al. 2012). Nevertheless, none of them is considered endemic to this basin. Only two species are native to the Iguaçu River, but widely found in the Paraná River. The NMDS summarized the composition of the fish assemblages and separated the studied streams (Figure 2). After 200 iterations, the stability criterion was met with a final stress of 0.12 (Monte Carlo test, p < 0.004) for the two-dimensional solution. The proportion of variance represented by each axis, based on the R2 between distance in the ordination space and distance in the original space, was 0.50 for the axis 1 and 0.16 for the axis 2. The distribution of points along the axis 1 segregated the streams upstream and downstream of the Iguaçu River Falls at the multidimensional space, suggesting that the composition of fish assemblages were highly affected by the geographical barrier (Iguaçu River Falls). We found significant differences in the composition of fish assemblages between the group of streams upstream and downstream of the falls (Hotelling's T2 = 234.36, p ˂ 0.0001). These results are corroborated by the Mantel test that evidenced no correlation between the similarity matrix of fish fauna composition and geographical distances among the sampled streams (Mantel r = 0.024, p = 0.5), demonstrating that the clusters formed in the nMDS axis 1 were not influenced by spatial autocorrelation arising from the proximity of streams. Figure 2 Non-metric multidimensional scaling (nMDS) ordination of the fish assemblages in the streams sampled in lower Iguaçu River basin, Paraná State, Brazil. In general, the indicator species analysis also indicated a distinction between the groups of streams. The streams upstream and downstream were characterized by different sets of indicator species (IndVal; Table 3). Six species characterized the streams upstream of the falls, except for Phalloceros harpagos, all these species were endemic to the Iguaçu basin. On the other hand, the streams flow into downstream of such biogeographical barrier were characterized by 15 indicator species, and with exception of Synbranchus cf. marmoratus, all were exclusive to these streams. Table 3 Summary of the indicator species analysis: relative abundance, relative frequency, and indicator value for the groups of streams (up and downstream of Iguaçu River Falls) studied in lower Iguaçu River basin, Paraná State, Brazil. Only species with significant values are shown. Values in boldface indicate significant indicator values (p < 0.05, Monte Carlo test). Species Groups Relative abundance Relative frequency Indicators values Astyanax bifasciatus 1 100 0 94 0 94 0 Trichomycterus davisi 1 100 0 50 0 50 0 Trichomycterus taroba 1 100 0 50 0 50 0 Hypostomus derbyi 1 100 0 56 0 56 0 Rhamdia voulezi 1 100 0 50 0 50 0 Phalloceros harpagos 1 97 3 94 50 91 2 Characidium sp. 1 2 0 100 0 63 0 63 Astyanax sp. 1 2 0 100 0 75 0 75 Astyanax sp. 2 2 0 100 0 50 0 50 Astyanax sp. 3 2 0 100 0 50 0 50 Astyanax lacustris 2 0 100 0 50 0 50 Briconamericus iheringii 2 0 100 0 50 0 50 Trichomycterus sp. 3 2 0 100 0 63 0 63 Corydoras sp. 2 0 100 0 50 0 50 Hisonotus sp. 2 0 100 0 63 0 63 Hypostomus albopunctatus 2 0 100 0 63 0 63 Heptapterus mustelinus 2 0 100 0 50 0 50 Rhamdia aff. quelen 2 0 100 0 100 0 100 Gymnotus pantanal 2 0 100 0 38 0 38 Synbranchus cf. marmoratus 2 7 93 13 75 1 70 Crenicichla britskii 2 0 100 0 50 0 50 Discussion The number of species observed in this study (40 spp.) can be considered high, especially if evaluated some issues: (i) the number of species recorded for other water bodies with similar size in the Neotropics (Bertaco 2009, Couto & Aquino 2011, Marceniuk et al. 2011, Oyakawa & Menezes 2011, Cetra et al. 2012, Daga et al. 2012), as well in other streams in the Paraná State (Araújo et al. 2011, Delariva & Silva 2013, Gubiani et al. 2010); (ii) the proportion of species registered herein represents 37.7% of the total number of species recorded for the Iguaçu River basin (106 spp.), including those observed in the main channel of the river (Baumgartner et al. 2012). This high number of species is because two streams (S4 and S5) belong to the Iguaçu River basin but flow into it downstream of the Iguaçu River Falls, thus have greater connection and exchange with the fish fauna of the Paraná River basin; (iii) besides the considerable number of species that have not yet been described. Moreover, most of the records held in the Iguaçu River basin compiled in Baumgartner et al. (2012) refers to surveys in the main channel of the Iguaçu River, with the use of other fishing gears, i.e., the majority of streams in this basin have never been sampled. This condition combined with the geomorphological characteristics of the basin provides the record of species of which there is no confirmation if they are only new records or are still unknown to science. The highest richness of the Siluriformes and Characiformes, as well as the families Characidae and Loricariidae, is a common observation in streams in the Neotropics (Lowe-McConnell 1999, Shibatta et al. 2002, Buckup et al. 2007; Langeani et al. 2007), and corroborates studies in small streams in other basins of the Paraná State (Galves et al. 2007, Cunico et al. 2009; Gubiani et al. 2010, Araújo et al. 2011, Pagotto et al. 2012, Delariva & Silva 2013). However, for the lower Iguaçu River, were registered 11 Astyanax spp., popularly known as "lambari", of which eight species are endemic, and two possibly endemic to this basin (Baumgartner et al. 2012). In our study, we recorded four Astyanax spp., three possibly endemic. Other three species are possibly new, totaling seven Astyanax spp., which explains the high contribution of Characidae in our study. Most of the species verified in this study is considered small size, which is expected to small water bodies (Bifi et al. 2006, Araújo et al. 2011, Cionek et al. 2012). According to Castro (1999), this pattern is shared by the fauna of South American streams and is mainly related to historical and evolutionary factors. It is noteworthy that a high number of small-sized species is even more evident in the fish fauna of the Iguaçu basin, even considering the species occurring in the main channel of the river. According to Garavello et al. (1997), the scarcity of rheophilic or large migratory species in this basin can be attributed to the formation of the Iguaçu River Falls, with an abrupt elevation, which interrupted the faunal exchange with the Paraná River basin. In general, a high degree of endemism is reported to streams (Castro 1999, Casatti 2010). However, it was more evident in the fauna of the Iguaçu River, with about 70% of endemic fish (Baumgartner et al. 2012). The formation of the falls isolated the upper from the lower reach of the Iguaçu River basin (Parolin et al. 2010), providing different scenarios for the evolution of species. This resulted in species with unique characteristics in the upper section. The indicator species for the two groups of streams corroborate this hypothesis, especially, because all indicator species of the group of streams upstream of the falls are endemic to the Iguaçu River. On the other hand, downstream of the falls was observed a higher number of indicator species, wherein, except Synbranchus cf. marmoratus, all were common to the fauna of the Paraná River. The occurrence of the distinct species in downstream indicates that the streams S4 and S5 remained connected below of the falls. In this way, although these streams belong to the Iguaçu River basin, its fish fauna evolved following similar patterns those observed for the Paraná River basin. This result strongly supports the hypothesis of distinction between the stream fish fauna upstream and downstream of the Iguaçu River Falls. Accordingly, corroborates with the already postulated effects of biogeographical barriers in the differentiation of the fish fauna and especially in endemism (Olden et al. 2010, Torrente-Vilara et al. 2011, Dias et al. 2012, Vitule et al. 2012). Despite these general patterns, the fish fauna of each stream can be considered exclusive to their microbasins, as demonstrated by the high number of species not yet described. The presence of species common to both environments, such as Gymnotus sylvius, Oreochromis niloticus, Phalloceros harpagos, and Synbranchus cf. marmoratus, should be considered with reservation, because except for Phalloceros harpagos, for the other species there is the possibility of escapes or introductions via their use as bait (Graça & Pavanelli 2007, Baumgartner et al. 2012). Regarding the differences in fish composition between streams upstream of the barrier (Iguaçu River Falls), it may be associated with conditions of preservation of streams sampled. For example, we have a high numerical abundance of Phalloceros harpagos in one of the streams (S1), where, besides the activity of livestock, human activities, such as the construction of a bridge, altered the normal course of the river, favoring the proliferation of less demanding species (Bifi et al. 2006, Lange et al. 2014). On the other hand, the presence of Poecilia reticulata in the stream S2, is possibly because to its location, near the urban center of municipality of Cascavel, since this species could be released or escape from aquarium. Tolerant non-native species in altered streams were recorded in several studies in streams of other basins in the Paraná State (Cunico et al. 2009, Araújo et al. 2011, Pagotto et al. 2012). The presence of non-native species is considered a major factor in the reduction of the native community (Jackson 2002, Di Prinzio et al. 2009, Eros et al. 2014, Zeni & Casatti 2014). In this study, the occurrences of Gymnotus and Synbranchus species can be attributed to the use of species of such genera as live bait (Graça & Pavanelli 2007, Baumgartner et al. 2012). These results confirm that huge changes in the use and occupation of land can cause changes in native fish assemblages in inland freshwater ecosystems. Furthermore, despite having completely different fish fauna composition, the streams S3 and S4 showed a high number of native species (to the Iguaçu River and Paraná River, respectively). In addition, these streams are located near the 'Parque Nacional do Iguaçu', which suggests a higher degree of preservation. This fact shows that preserved environments offers better conditions for the permanence of native species (Lyons et al. 1995, Saunders et al. 2002, Casatti et al. 2012), which are more sensitive to changes, ensuring the preservation of endemism of this fish fauna. The results summarized in this study show strongly the significant effect of the Iguaçu River Falls as a natural biogeographic barrier for speciation of fish species and endemism in streams of the Iguaçu River basin, leading to the development of distinct faunas in water bodies located upstream and downstream of such waterfalls. Although others studies had shown that geologic processes provide the capture of headwaters by adjacent basins (Ribeiro 2006; Dagosta et al. 2014), this seems not to be the case of this study. So, the main insight of our study is related to fact that differentiation has occurred in species composition between streams up and downstream and that these follow a similar pattern for the registered to the fish fauna of the principal channel. Thereby, it is stressed the importance of further surveys in headwaters streams, especially in the Iguaçu River to confirm and consolidate this findings. Peculiarities of this basin as the presence of geographical barriers (falls) with different levels of isolation, should provide different scenarios for speciation of the fish fauna. The high number of endemic species not yet described deserves the attention of researchers and experts, so that they can be recognized by science and thus conserved, in order to maintain the biodiversity of freshwater ecosystems. In this context, we confirm the claim of Nogueira et al. (2010) who reported that a comprehensive strategy for the conservation of freshwater fish species in Brazil needs to address studies for restricted-range endemic species. Also, the presence of non-native species was more closely associated with streams under the influence of adjacent urban areas. These findings, along with urban sprawl in the lower Iguaçu River region, reinforce the imminent need for knowledge of this fauna, considering that the extinction of species in this region means the irreparable loss of them. In addition, considering that the basic unit of management is the basin, we suggested that it should be considered geographical spaces delimited by natural or artificial barriers as units separated in the basin when developing and implementing monitoring programs, impact studies and conservation plans. Acknowledgments We thank the researches of GERPEL for helping in the sampling and the Universidade Estadual do Oeste do Paraná for providing logistical support for sampling. We also thank to researchers of the Ichthyology Collection of Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, of the Universidade Estadual de Maringá, in special to Luiz Tencatt, for helping to identify the Corydoras species. References ARAÚJO, M.I., DELARIVA, R.L., BONATO, K.O. & SILVA, J.C. 2011. Fishes in first order stream in Ivaí River drainage basin, upper Paraná River Basin, Paraná state, Brazil. Check List 7(6): 774-777. ARAÚJO M.I. DELARIVA R.L. BONATO K.O. SILVA J.C. 2011 Fishes in first order stream in Ivaí River drainage basin, upper Paraná River Basin, Paraná state, Brazil Check List 7 6 774 777 BAUMGARTNER, D., BAUMGARTNER, G., PAVANELLI, C.S., SILVA, P.R.L., FRANA, V.A., OLIVEIRA, L.C. & MICHELON, M.R. 2006. Fish, Salto Osório Reservoir, rio Iguaçu basin, Paraná State, Brazil. Check List 2(1):1-4. AUMGARTNER D. BAUMGARTNER G. PAVANELLI C.S. SILVA P.R.L. FRANA V.A. OLIVEIRA L.C. MICHELON M.R. 2006 Fish, Salto Osório Reservoir, rio Iguaçu basin, Paraná State, Brazil Check List 2 1 1 4 BAUMGARTNER, G., PAVANELLI, C.S., BAUMGARTNER, D., BIFI, A.G., DEBONA, T. & FRANA, V.A. 2012. Peixes do baixo Rio Iguaçu. Eduem, Maringá. BAUMGARTNER G. PAVANELLI C.S. BAUMGARTNER D. BIFI A.G. DEBONA T. FRANA V.A. 2012 Peixes do baixo Rio Iguaçu Eduem Maringá BERTACO, V.A. 2009. Freshwater Fishes, Ilha de Santa Catarina, southern coastal drainage of the state of Santa Catarina, Brazil. Check List 5(4): 898-902. BERTACO V.A. 2009 Freshwater Fishes, Ilha de Santa Catarina, southern coastal drainage of the state of Santa Catarina, Brazil Check List 5 4 898 902 BIFI, A.G., BAUMGARTNER, D., BAUMGARTNER, G., FRANA, V.A. & DEBONA, T. 2006. Composição específica e abundância da ictiofauna do rio dos Padres, bacia do rio Iguaçu, Brasil. Acta Scient. Biol. Sci. 28(3): 203-211. BIFI A.G. BAUMGARTNER D. BAUMGARTNER G. FRANA V.A. DEBONA T. 2006 Composição específica e abundância da ictiofauna do rio dos Padres, bacia do rio Iguaçu, Brasil Acta Scient. Biol. Sci. 28 3 203 211 BUCKUP, P.A., MENEZES, N.A. & GHAZZI, M.S. 2007. Catálogo das espécies de peixes de água doce do Brasil. Museu Nacional, Rio de Janeiro. BUCKUP P.A. MENEZES N.A. GHAZZI M.S. 2007 Catálogo das espécies de peixes de água doce do Brasil Museu Nacional Rio de Janeiro CASATTI, L. 2010. Alterações no Código Florestal Brasileiro: impactos potenciais sobre a ictiofauna. Biota Neotrop. 10(4): 30-34 http://www.biotaneotropica.org.br/v10n4/en/abstract?article+bn00310042010 (last access at 17/11/2015) CASATTI L. 2010 Alterações no Código Florestal Brasileiro: impactos potenciais sobre a ictiofauna Biota Neotrop 10 4 30 34 10(4): 30-34 http://www.biotaneotropica.org.br/v10n4/en/abstract?article+bn00310042010 17/11/2015 CASATTI, L., TERESA, F.B., GONÇALVES-SOUZA, T., BESSA, E., MANZOTTI, A.R., GONÇALVES, C.S. & ZENI, J.O. 2012. From forests to cattail: how does the riparian zone influence stream fish? Neotrop. Ichthyol. 10: 205-214. CASATTI L. TERESA F.B. GONÇALVES-SOUZA T. BESSA E. MANZOTTI A.R. GONÇALVES C.S. ZENI J.O. 2012 From forests to cattail: how does the riparian zone influence stream fish? Neotrop. Ichthyol 10 205 214 CASTRO, R.M.C. 1999. Evolução da ictiofauna de riachos Sul-Americanos: Padrões gerais e possíveis processos casuais. In Ecologia de Peixes de Riachos: Estado Atual e Perspectivas (E.P. Caramaschi, R. Mazzoni, C.R.S.F. Bizerril & P.R. Peres-Neto, eds.). Oecol. Bras., Rio de Janeiro, p.139-155. CASTRO R.M.C. 1999 Evolução da ictiofauna de riachos Sul-Americanos: Padrões gerais e possíveis processos casuais. In Ecologia de Peixes de Riachos: Estado Atual e Perspectivas (E.P. Caramaschi, R. Mazzoni, C.R.S.F. Bizerril & P.R. Peres-Neto, eds.) Oecol. Bras. Rio de Janeiro 139 155 CETRA, M., BARRELLA, W., LANGEANI, F., MARTINS, A.G., MELLO, B.J. & ALMEIDA, R.S. 2012. Fish fauna of headwater streams that cross the Atlantic Forest of south São Paulo state. Check List 8(3): 421-425. CETRA M. BARRELLA W. LANGEANI F. MARTINS A.G. MELLO B.J. ALMEIDA R.S. 2012 Fish fauna of headwater streams that cross the Atlantic Forest of south São Paulo state Check List 8 3 421 425 CIONEK, V.M., SACRAMENTO, P.A., ZANATTA, N., OTA, R.P., CORBETTA, D.F. & BENEDITO, E. 2012. Fishes from first order streams of lower Paranapanema and Ivaí rivers, upper Paraná River basin, Paraná, Brazil. Check List 8(6): 1158-1162. CIONEK V.M. SACRAMENTO P.A. ZANATTA N. OTA R.P. CORBETTA D.F. BENEDITO E. 2012 Fishes from first order streams of lower Paranapanema and Ivaí rivers, upper Paraná River basin, Paraná, Brazil Check List 8 6 1158 1162 COUTO, T.B.A & AQUINO, P.P.U. 2011. Structure and integrity of fish assemblages in streams associated to conservation units in Central Brazil. Neotrop. ichthyol. 9(2): 445-454. COUTO T.B.A AQUINO P.P.U. 2011 Structure and integrity of fish assemblages in streams associated to conservation units in Central Brazil Neotrop. ichthyol. 9 2 445 454 CRACRAFT, J. 1982. A nonequilibrium theory for the rate-control of speciation and extinction and the origin of macroevolutionary patterns. Syst. Biol. 31: 348-365. CRACRAFT J. 1982 A nonequilibrium theory for the rate-control of speciation and extinction and the origin of macroevolutionary patterns Syst. Biol. 31 348 365 CUNICO, A.M., AGOSTINHO, A.A. & LATINI, J.D. 2006. Influência da urbanização sobre as assembleias de peixes em três córregos de Maringá, Paraná. Rev. Bras. Zool. 23(4): 1101-1110. CUNICO A.M. AGOSTINHO A.A. LATINI J.D. 2006 Influência da urbanização sobre as assembleias de peixes em três córregos de Maringá, Paraná Rev. Bras. Zool. 23 4 1101 1110 CUNICO, A.M., GRAÇA, W.J., AGOSTINHO, A.A., DOMINGUES, V.M. & LATINI, J.D. 2009. Fish, Maringá Urban Streams, Pirapó river drainage, upper Paraná river basin, Paraná State, Brazil. Check List 5(2): 273-280. CUNICO A.M. GRAÇA W.J. AGOSTINHO A.A. DOMINGUES V.M. LATINI J.D. 2009 Fish, Maringá Urban Streams, Pirapó river drainage, upper Paraná river basin, Paraná State, Brazil Check List 5 2 273 280 DAGA, V.S., GUBIANI, E.A., CUNICO, A.M. & BAUMGARTNER, G. 2012. Effects of abiotic variables on the distribution of fish assemblages in streams with different anthropogenic activities in southern Brazil. Neotrop. ichthyol. 10(3): 643-652. DAGA V.S. GUBIANI E.A. CUNICO A.M. BAUMGARTNER G. 2012 Effects of abiotic variables on the distribution of fish assemblages in streams with different anthropogenic activities in southern Brazil Neotrop. ichthyol. 10 3 643 652 DAGOSTA, F.C.P., MARINHO, M.M.F. & CAMELIER, P. 2014. A new species of Hyphessobrycon Durbin (Characiformes: Characidae) from the middle rio São Francisco and upper and middle rio Tocantins basins, Brazil, with comments on its biogeographic history. Neotrop. ichthyol. 12(2): 365-375. DAGOSTA F.C.P. MARINHO M.M.F. CAMELIER P. 2014 A new species of Hyphessobrycon Durbin (Characiformes: Characidae) from the middle rio São Francisco and upper and middle rio Tocantins basins, Brazil, with comments on its biogeographic history Neotrop. ichthyol. 12 2 365 375 DELARIVA, R.L. & SILVA, J.C. 2013. Fish fauna of headwater streams of Perobas Biological Reserve, a conservation unit in the Atlantic Forest of the Northwestern Paraná State, Brazil. Check List 9(3): 549-554. DELARIVA R.L. SILVA J.C. 2013 Fish fauna of headwater streams of Perobas Biological Reserve, a conservation unit in the Atlantic Forest of the Northwestern Paraná State, Brazil Check List 9 3 549 554 DI PRINZIO, C.Y., CASAUX, R.J. & MISERENDINO, M.L. 2009. Effects of land use on fish assemblages in Patagonian low order streams. Int. J. Limnol. 45(04): 267-277. DI PRINZIO C.Y. CASAUX R.J. MISERENDINO M.L. 2009 Effects of land use on fish assemblages in Patagonian low order streams Int. J. Limnol. 45 04 267 277 DIAS, M.S., CORNU, J.F., OBERDORFF, T., LASSO, C.A. & TEDESCO, P.A. 2012. Natural fragmentation in river networks as a driver of speciation for freshwater fishes. Ecography 35: 001-007. DIAS M.S. CORNU J.F. OBERDORFF T. LASSO C.A. TEDESCO P.A. 2012 Natural fragmentation in river networks as a driver of speciation for freshwater fishes Ecography 35 001 007 DUFRÊNE, M. & LEGENDRE, P. 1997. Species assemblages and Indicator Species: the need for a flexible symmetrical approach. Ecol. monogr. 67: 345-366. DUFRÊNE M. LEGENDRE P. 1997 Species assemblages and Indicator Species: the need for a flexible symmetrical approach Ecol. monogr. 67 345 366 EROS, T., SÁLY, P., TAKÁCS, P., HIGGINS, C.L., BÍRÓ, P. & SCHMERA, D. 2014. Quantifying temporal variability in the metacommunity structure of stream fishes: the influence of non-native species and environmental drivers. Hydrobiologia 722: 31-43. EROS T. SÁLY P. TAKÁCS P. HIGGINS C.L. BÍRÓ P. SCHMERA D. 2014 Quantifying temporal variability in the metacommunity structure of stream fishes: the influence of non-native species and environmental drivers Hydrobiologia 722 31 43 GALVES, W., JEREP, F.C. & SHIBATTA, O.A. 2007. Estudo da condição ambiental pelo levantamento da fauna de três riachos na região do Parque Estadual Mata dos Godoy (PEMG), Londrina, PR, Brasil. PanamJAS 2(1): 55-65. GALVES W. JEREP F.C. SHIBATTA O.A. 2007 Estudo da condição ambiental pelo levantamento da fauna de três riachos na região do Parque Estadual Mata dos Godoy (PEMG), Londrina, PR, Brasil PanamJAS 2 1 55 65 GARAVELLO, J.C., BRITSKI, H.A. & ZAWADZKI, C.H. 2012. The cascudos of the genus Hypostomus Lacépède (Osteichthyes: Loricariidae) from the rio Iguaçu basin. Neotrop. ichthyol. 10(2): 263-283. GARAVELLO J.C. BRITSKI H.A. ZAWADZKI C.H. 2012 The cascudos of the genus Hypostomus Lacépède (Osteichthyes: Loricariidae) from the rio Iguaçu basin Neotrop. ichthyol. 10 2 263 283 GARAVELLO, J.C. & SAMPAIO, F.A.A. 2010. Five new species of genus Astyanax Baird & Girard, 1854 from Rio Iguaçu, Paraná, Brazil (Ostariophysi, Characiformes, Characidae). Braz. J. Biol. 70(3): 847-865. GARAVELLO J.C. SAMPAIO F.A.A. 2010 Five new species of genus Astyanax Baird & Girard, 1854 from Rio Iguaçu, Paraná, Brazil (Ostariophysi, Characiformes, Characidae) Braz. J. Biol. 70 3 847 865 GARAVELLO, J.C., PAVANELLI, C.S., SUZUKI, H.I. 1997. Caracterização da ictiofauna do rio Iguaçu. In Reservatório de Segredo, bases ecológicas para o manejo (A.A. Agostinho & L.C. Gomes, eds.). Eduem, Maringá, p. 61-84. GARAVELLO J.C. PAVANELLI C.S. SUZUKI H.I. 1997 Caracterização da ictiofauna do rio Iguaçu. In Reservatório de Segredo, bases ecológicas para o manejo (A.A. Agostinho & L.C. Gomes, eds.) Eduem Maringá 61 84 GRAÇA, W.J. & PAVANELLI, C.S. 2007. Peixes da Planície de inundação do Alto rio Paraná e áreas adjacentes. 1 ed. Eduem, Maringá. GRAÇA W.J. PAVANELLI C.S. 2007 Peixes da Planície de inundação do Alto rio Paraná e áreas adjacentes 1 ed Eduem Maringá GUBIANI, E.A., DAGA, V.S., FRANA, V.A. & GRAÇA, W.J. 2010. Fish, Toledo urban streams, São Francisco Verdadeiro River drainage, upper Paraná River basin, state of Paraná, Brazil. Check List 6(1): 45-48. GUBIANI E.A. DAGA V.S. FRANA V.A. GRAÇA W.J. 2010 Fish, Toledo urban streams, São Francisco Verdadeiro River drainage, upper Paraná River basin, state of Paraná, Brazil Check List 6 1 45 48 HAMMER, D.A., HARPER, T. & RYAN, P.D. 2001. PAST: Paleotological Statistics Software package for education and data analysis. Paleontol. Electron. 4: 1-9. HAMMER D.A. HARPER T. RYAN P.D. 2001 PAST: Paleotological Statistics Software package for education and data analysis Paleontol. Electron 4 1 9 JACKSON, D.A. 2002. Ecological effects of Micropterus introductions: the dark side of black bass. In: Black Bass: Ecology, Conservation and Management (D.P. Phillip & M.S. Ridgway, eds.). American Fisheries Society Symposium 31: 221-232. JACKSON D.A. 2002 Ecological effects of Micropterus introductions: the dark side of black bass Black Bass: Ecology, Conservation and Management Phillip D.P. Ridgway M.S. American Fisheries Society Symposium 31 221 232 LANGE, K., TOWNSEND, C.R., GABRIELSSON, R., CHANUT, P.C.M. & MATTHAEI, C.D. 2014. Responses of stream fish populations to farming intensity and water abstraction in an agricultural catchment. Freshw. biol. 59(2): 286-299. LANGE K. TOWNSEND C.R. GABRIELSSON R. CHANUT P.C.M. MATTHAEI C.D. 2014 Responses of stream fish populations to farming intensity and water abstraction in an agricultural catchment Freshw. biol. 59 2 286 299 LANGEANI, F., CASTRO, R.M.C., OYAKAWA, O.T., SHIBATTA, O.A., PAVANELLI, C.S. & CASATTI, L. 2007. Diversidade da ictiofauna do Alto Rio Paraná: composição atual e perspectivas futuras. Biota Neotrop. 7(3): 1-17 http://www.biotaneotropica.org.br/v7n3/pt/abstract?article+bn03407032007 (last access at 14/01/2016) LANGEANI F. CASTRO R.M.C. OYAKAWA O.T. SHIBATTA O.A. PAVANELLI C.S. CASATTI L. 2007 Diversidade da ictiofauna do Alto Rio Paraná: composição atual e perspectivas futuras Biota Neotrop 7 3 1 17 7(3): 1-17 http://www.biotaneotropica.org.br/v7n3/pt/abstract?article+bn03407032007 14/01/2016 LOWE-MCCONNELL, R.H. 1999. Estudos Ecológicos de Comunidades de peixes tropicais. Coleção Base, Edusp, São Paulo. LOWE-MCCONNELL R.H. 1999 Estudos Ecológicos de Comunidades de peixes tropicais Coleção Base Edusp São Paulo LYONS, J., NAVARRO-PÉREZ, S., COCHRAN, P.A., SANTANA, C. & GUZMÁN-ARROYO, M. 1995. Index of biotic integrity based on fish assemblages for the conservation of streams and rivers in west-central México. Conserv. biol. 9(3): 569-584. LYONS J. NAVARRO-PÉREZ S. COCHRAN P.A. SANTANA C. GUZMÁN-ARROYO M. 1995 Index of biotic integrity based on fish assemblages for the conservation of streams and rivers in west-central México Conserv. biol. 9 3 569 584 MARCENIUK, A.P., HILSDORF, A.W.S. & LANGEANI, F. 2011. The ichthyofauna from the headwaters of the rio Tietê, São Paulo, Brazil. Biota Neotrop. 11(3) http://www.biotaneotropica.org.br/v11n3/en/abstract?inventory+bn00311032011 (last access at 05/09/2015) MARCENIUK A.P. HILSDORF A.W.S. LANGEANI F. 2011 The ichthyofauna from the headwaters of the rio Tietê, São Paulo, Brazil Biota Neotrop. 11 3 11(3) http://www.biotaneotropica.org.br/v11n3/en/abstract?inventory+bn00311032011 05/09/2015 MCCUNE, B. & GRACE, J.B. 2002. Analysis of ecological communities. MjM Software Design, Gleneden Beach, Oregon, USA. MCCUNE B. GRACE J.B. 2002 Analysis of ecological communities MjM Software Design Gleneden Beach, Oregon, USA MCCUNE, B. & MEFFORD, M.J. 2011. PC-ORD. Multivariate analysis of ecological data.Version 6.0. MjM Software, Gleneden Beach, Oregon, USA. MCCUNE B. MEFFORD M.J. 2011 PC-ORD. Multivariate analysis of ecological data Version 6.0 MjM Software Gleneden Beach, Oregon, USA MEEUWIG, M.H., GUY, C.S., KALINOWSKI, S.T. & FREDENBERG, W.A. 2010. Landscape influences on genetic differentiation among bull trout populations in a stream-lake network. Mol. ecol. 19: 3620-3633. MEEUWIG M.H. GUY C.S. KALINOWSKI S.T. FREDENBERG W.A. 2010 Landscape influences on genetic differentiation among bull trout populations in a stream-lake network Mol. ecol. 19 3620 3633 MIRANDE, J.M. 2009. Weighted parsimony phylogeny of the family Characidae (Teleostei: Characiformes). Cladistics 25(6): 574-613. MIRANDE J.M. 2009 Weighted parsimony phylogeny of the family Characidae (Teleostei: Characiformes) Cladistics 25 6 574 613 NELSON, J.S. 2006. Fishes of the world. John Wiley & Sons, New York. NELSON J.S. 2006 Fishes of the world John Wiley & Sons New York NOGUEIRA, C., BUCKUP, P.A., MENEZES, N.A., OYAKAWA, O.T., KASECKER, T.P., RAMOS NETO, M.B. & SILVA, J.M.C. 2010. Restricted-range fishes and the conservation of Brazilian freshwaters. PLoS One 5(6): e11390. NOGUEIRA C. BUCKUP P.A. MENEZES N.A. OYAKAWA O.T. KASECKER T.P. RAMOS M.B. NETO SILVA J.M.C. 2010 Restricted-range fishes and the conservation of Brazilian freshwaters PLoS One 5 6 e11390 OLDEN, D.J., KENNARD, M.J., LEPRIEUR, F., TEDESCO, P.A., WINEMILLER, K.O. & GARCÍA-BERTHOU, E. 2010. Conservation biogeography of freshwater fishes: recent progress and future challenges. Divers. distrib. 16(3): 496-513. OLDEN D.J. KENNARD M.J. LEPRIEUR F. TEDESCO P.A. WINEMILLER K.O. GARCÍA-BERTHOU E. 2010 Conservation biogeography of freshwater fishes: recent progress and future challenges Divers. distrib. 16 3 496 513 OYAKAWA, O.T. & MENEZES, N.A. 2011. Checklist of fresh water fishes from São Paulo State, Brazil. Biota Neotrop. 11, 19-32. http://www.biotaneotropica.org.br/v11n1a/en/abstract?inventory+bn0021101a2011 (last access at 17/03/2015) OYAKAWA O.T. MENEZES N.A. 2011 Checklist of fresh water fishes from São Paulo State, Brazil Biota Neotrop. 11 19 32 http://www.biotaneotropica.org.br/v11n1a/en/abstract?inventory+bn0021101a2011 17/03/2015 PAGOTTO, J.P.A., VERÍSSIMO, S., GOULART, E. & MISE. F.T. 2012. Fishes (Osteichthyes: Actinopterygii) from the Pirapó River drainage, upper Paraná River basin, Paraná state, Brazil. Check List 8(3): 463-468. PAGOTTO J.P.A. VERÍSSIMO S. GOULART E. MISE F.T. 2012 Fishes (Osteichthyes: Actinopterygii) from the Pirapó River drainage, upper Paraná River basin, Paraná state, Brazil Check List 8 3 463 468 PAROLIN, M., RIBEIRO, C.V. & LEANDRINI, J.A 2010. Abordagem ambiental interdisciplinar em bacias hidrográficas no Estado do Paraná. Editora da Fecilcam, Campo Mourão. PAROLIN M. RIBEIRO C.V. LEANDRINI J.A. 2010 Abordagem ambiental interdisciplinar em bacias hidrográficas no Estado do Paraná Editora da Fecilcam Campo Mourão PAVANELLI, C.S. & CARAMASCHI, E.P. 2003. Temporal and spatial distribution of the ichthyofauna in two streams of the upper rio Paraná basin. Braz. Arch. Biol. Technol. 46: 271-280. PAVANELLI C.S. CARAMASCHI E.P. 2003 Temporal and spatial distribution of the ichthyofauna in two streams of the upper rio Paraná basin Braz. Arch. Biol. Technol. 46 271 280 RAHEL, F.J. 2007. Biogeographic barriers, connectivity and homogenization of freshwater faunas: it's a small world after all. Freshw. biol. 52: 696-710. RAHEL F.J. 2007 Biogeographic barriers, connectivity and homogenization of freshwater faunas: it's a small world after all Freshw. biol. 52 696 710 REIS, R.E., KULLANDER, S.O. & FERRARIS JR., C.J. 2003. Check list of freshwater fishes of South and Central America. Edipucrs, Porto Alegre. REIS R.E. KULLANDER S.O. FERRARIS JR. C.J. 2003 Check list of freshwater fishes of South and Central America Edipucrs Porto Alegre RIBEIRO, A.C. 2006. Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: an example of faunal evolution associated with a divergent continental margin. Neotrop. ichthyol. 4(2): 225-246. RIBEIRO A.C. 2006 Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: an example of faunal evolution associated with a divergent continental margin Neotrop. ichthyol. 4 2 225 246 SAUNDERS, D.L., MEEUWIG, J.J. & VINCENT, A.C.J. 2002. Freshwater protected areas: strategies for conservation. Conserv. biol. 16(1): 30-41. SAUNDERS D.L. MEEUWIG J.J. VINCENT A.C.J. 2002 Freshwater protected areas: strategies for conservation Conserv. biol. 16 1 30 41 SEMA, Secretaria de Estado do Meio Ambiente e Recursos Hídricos. 2013. Bacias Hidrográficas do Paraná. Série Histórica, 2 ed, Curitiba. SEMA, Secretaria de Estado do Meio Ambiente e Recursos Hídricos 2013 Bacias Hidrográficas do Paraná Série Histórica 2 ed Curitiba SHIBATTA, O.A., ORSI, M.L., BENNEMANN, S.T. & SILVA-SOUZA, A.T. 2002. Diversidade e distribuição de peixes na bacia do rio Tibagi. In A bacia do rio Tibagi (M.E. Medri, E. Bianchini, O.A. Shibatta & J.A. Pimenta, eds.). Universidade Estadual de Londrina, Londrina. p. 403-423. HIBATTA O.A. ORSI M.L. BENNEMANN S.T. SILVA-SOUZA A.T. 2002 Diversidade e distribuição de peixes na bacia do rio Tibagi. In A bacia do rio Tibagi Medri M.E. Bianchini E. Shibatta O.A. Pimenta J.A. Universidade Estadual de Londrina Londrina 403 423 SUZUKI, H.I., PAVANELLI, C.S., FUGI, R., BINI, L.M. & AGOSTINHO, A.A. 1997. Ictiofauna de quatro tributários do reservatório de Segredo. In: Reservatório de segredo: bases ecológicas para o manejo (A.A. Agostinho & L.C. Gomes, eds.). Eduem, Maringá. p. 259-273. SUZUKI H.I. PAVANELLI C.S. FUGI R. BINI L.M. AGOSTINHO A.A. 1997 Ictiofauna de quatro tributários do reservatório de Segredo Reservatório de segredo: bases ecológicas para o manejo Agostinho A.A. Gomes L.C. Eduem Maringá 259 273 TORRENTE-VILLARA, G., ZUANON, J., LEPRIEUR, F., OBERDORFF, T. & TEDESCO, P.A. 2011. Effects of natural rapids and waterfalls on fish assemblage structure in the Madeira River (Amazon Basin). Ecol. freshw. fish 20: 588-597. TORRENTE-VILLARA G. ZUANON J. LEPRIEUR F. OBERDORFF T. TEDESCO P.A. 2011 Effects of natural rapids and waterfalls on fish assemblage structure in the Madeira River (Amazon Basin) Ecol. freshw. fish 20 588 597 VICARI, M.R., PAZZA, R., ARTONI, R.F., MARGARIDO, V.P. & BERTOLLO, L.A.C. 2006. Cytogenetics and Biogeography: considerations about the Natural Origin of Hoplias malabaricus (Characiformes, Erythrinidae) on the Iguaçu River. Braz. Arch. Biol. Technol. 49(2): 297-303. VICARI M.R. PAZZA R. ARTONI R.F. MARGARIDO V.P. BERTOLLO L.A.C. 2006 Cytogenetics and Biogeography: considerations about the Natural Origin of Hoplias malabaricus (Characiformes, Erythrinidae) on the Iguaçu River Braz. Arch. Biol. Technol. 49 2 297 303 VITULE, J.R.S. & ABILHOA, V.A. 2003. Composição da ictiofauna na bacia hidrográfica do rio Piraquara, alto rio Iguaçu, Região Metropolitana de Curitiba, Paraná, Brasil. Estud. Biol. 25(52): 43-49. VITULE J.R.S. ABILHOA V.A. 2003 Composição da ictiofauna na bacia hidrográfica do rio Piraquara, alto rio Iguaçu, Região Metropolitana de Curitiba, Paraná, Brasil Estud. Biol. 25 52 43 49 VITULE, J.R.S., FREIRE, C.A., VAZQUEZ, D.P., NUÑEZ, M.A. & SIMBERLOFF, D. 2012. Revisiting the Potential Conservation Value of Non-Native Species. Conserv. biol. 26(6): 1153-1155. VITULE J.R.S. FREIRE C.A. VAZQUEZ D.P. NUÑEZ M.A. SIMBERLOFF D. 2012 Revisiting the Potential Conservation Value of Non-Native Species Conserv. biol. 26 6 1153 1155 ZAWADZKI, D.H., RENESTRO, E. & BINI, L.M. 1999. Genetic and morphometric analysis of three species of the genus Hypostomus Lacépède, 1803 (Osteichthyes: Loricariidae) from the Rio Iguaçu basin (Brazil). Rev. suisse zool. 106(1): 91-105. ZAWADZKI D.H. RENESTRO E. BINI L.M. 1999 Genetic and morphometric analysis of three species of the genus Hypostomus Lacépède, 1803 (Osteichthyes: Loricariidae) from the Rio Iguaçu basin (Brazil) Rev. suisse zool. 106 1 91 105 ZENI, J.O. & CASATTI, L. 2014. The influence of habitat homogenization on the trophic structure of fish fauna in tropical streams. Hydrobiologia 726: 259-270. ZENI J.O. CASATTI L. 2014 The influence of habitat homogenization on the trophic structure of fish fauna in tropical streams Hydrobiologia 726 259 270