Abstract

The South America ichthyofauna encompasses the highest diversity of the world, however is highly threatened by anthropogenic actions. The fish fauna of nine low-order streams, tributaries of the Piquiri River and impacted by aquaculture, agriculture and urbanization were sampled in the present study. Samplings were done quarterly from December 2017 to September 2018 at three sites in each stream, using a portable electric fishing device in 50-meter segments. A total of 14,507 individuals were collected, belonging to six orders, 20 families, 46 genera, and 70 species. The highest richness and abundance were found for the orders Characiformes and Siluriformes. In this study, nine species that had not been recorded were found, totaling 163 for the basin. In addition, 14 non-native species were captured. The presented list of species contributes to the existing database of ichthyofauna distribution in Neotropical streams, denoting that it is underestimated in the region, mainly in low-order tributaries. The present study reinforces the importance of inventories and monitoring in environments with high biodiversity and sensitive to anthropogenic actions.

Keywords:
Biodiversity; Streams; Land use

Resumo

A ictiofauna sul-americana abrange a maior diversidade do planeta, no entanto, encontra-se altamente ameaçada pela ação antrópica. Nesse estudo, a fauna de peixes de nove riachos de pequena ordem foi amostrada. Esses riachos são afluentes do Rio Piquiri e afetados pela atividade aquícola, agrícola e urbanização. As coletas foram realizadas trimestralmente de dezembro/2017 a setembro/2018 em três pontos amostrais de cada riacho, utilizando-se equipamento portátil de pesca elétrica em segmentos delimitados de 50 metros. Foram coletados 14.507 indivíduos, pertencentes a seis ordens, 20 famílias, 46 gêneros e 70 espécies. Os maiores valores de riqueza e de abundância foram obtidos nas ordens Characiformes e Siluriformes. Neste estudo, foram encontradas nove espécies ainda não registradas, totalizando 163 para a bacia. Além disso, 14 espécies não-nativas foram capturadas. Ressalta-se que a lista de espécies apresentada contribui com o banco de dados existente sobre os padrões de distribuição da ictiofauna em riachos Neotropicais e demonstra como a mesma ainda pode ser subestimada na região, principalmente em tributários de pequena ordem. Esse estudo reforça a importância de inventários e do monitoramento em ambientes altamente diversos e sensíveis à ação antrópica.

Palavras-chave:
Biodiversidade; Riachos; Uso do solo

Introduction

South America has the highest fish diversity of the world, which encompasses more than nine thousand described species and approximately one third of all freshwater fish species (Reis et al. 2016REIS, R.E., ALBERT, J.S., DI DARIOS, F., MINCARONES, M.M., PETRY, P., & ROCHA, L.A. 2016. Fish biodiversity and conservation in South America. J. Fish Biol. 89(1): 12-47. https://doi.org/10.1111/jfb.13016
https://doi.org/10.1111/jfb.13016... ). However, the conservation of the continental ichthyofauna of South America is an increasing challenge because of continuous losses of habitats caused by anthropogenic changes resulted from different soil uses, such as urbanization, agriculture, mining and hydroelectric dams (Pelicice et al. 2017PELICICE, F.M., AZEVEDO-SANTOS, V.M., VITULE, J.R.S., ORSI, M.L., LIMA-JUNIOR, D.P., MAGALHÃES, A.L.B., POMPEU, P.S., PETRERE-JUNIOR, M., & AGOSTINHO, A.A. 2017. Neotropical freshwater fishes imperilled by unsustainable policies. Fish Fish 18: 1119-1133. https://doi.org/10.1111/faf.12228
https://doi.org/10.1111/faf.12228... ), as well as overfishing and introduction of non-native species (Rios-Touma & Ramírez 2019). Therefore, the rate of species extinction can be higher than the actual information of number of species and their geographical distribution. Thus, ichthyofauna inventories are essential for a significant analysis of the biodiversity, especially in environments that have no significant sampling of their fauna, such as low-order streams (Frota et al. 2019FROTA, A., MESSAGE, H. J., OLIVEIRA, R. C., BENEDITO, E., & GRAÇA, W. J. 2019. Ichthyofauna of headwater streams from the rio Ribeira de Iguape basin, at the boundaries of the Ponta Grossa Arch, Parana, Brazil. Biota Neotropica 19(1): 1-12. https://doi.org/10.1590/1676-0611-bn-2018-0666 (last acess in: 5/3/2021)
https://doi.org/10.1590/1676-0611-bn-201... ).

The Piquiri River basin comprises a drainage area of 31,000 km² in the Upper Paraná Ecoregion (Abell et al. 2008ABELL, R., THIEME, M.L., REVENGA, C., BRYER, M., KOTTELAT, M., BOGUTSKAYA, N. et al. 2008. Freshwater ecoregions of the world: A new map of biogeographic units for freshwater biodiversity conservation. BioScience 58: 403-414. https://dx.doi.org/doi: 10.1641/B580507
https://dx.doi.org/doi: 10.1641/B580507... ), its sources are located in the São João Mountains and it runs 485 km before reaching the Paraná River, forming the third largest hydrographic basin in the State of Paraná, Brazil. The Piquiri River is one of the last tributaries free of damming in the Upper Paraná River basin, which reinforces its ecological importance (Agostinho et al. 2004AGOSTINHO, A.A., GOMES, L.C., VERÍSSIMO, S., & OKADA, E.K. 2004b. Flood regime, dam regulation and fish in the Upper Parana River: effects on assemblage attributes, reproduction and recruitment. Rev. Fish Biol. Fish. 14: 11-19.a, Affonso et al. 2015AFFONSO, I.P., AZEVEDO, R. F., SANTOS, N.L.C., DIAS, R.M., AGOSTINHO, A.A., & GOMES, L.C. 2015. Pulling the plug: strategies to preclude expansion of dams in Brazilian rivers with high-priority for conservation. Nat. Conserv. 13: 199-203. https://dx.doi.org/10.1016/j.ncon.2015.11.008
https://dx.doi.org/10.1016/j.ncon.2015.1... ) and makes it an important environment for migratory species (Gubiani et al. 2010GUBIANI, E.A., GOMES, L.C., AGOSTINHO, A.A., & BAUMGARTER, G. 2010. Variations in fish assemblages in a tributary of the upper Paraná River, Brazil: a comparison between pre and post-closure phases of dams. River Res Appl. 26: 848-865. https://doi.org/10.1002/rra.1298
https://doi.org/10.1002/rra.1298... ). Considering its importance for the conservation of the Brazilian continental ichthyofauna and the occurrence of 152 fish species in this river basin in research developed by Cavalli et al. (2018)CAVALLI, D., FROTA, A., LIRA, A.D., GUBIANI, E.A., MARGARIDO, V. P., & GRAÇA, W. J. 2018. Update on the ichthyofauna of the Piquiri River basin, Parana, Brazil: a conservation priority area. Biota neotropica 18(2): e20170350. https://doi.org/10.1590/1676-0611-bn-2017-0350 (last acess in: 23/12/2020)
https://doi.org/10.1590/1676-0611-bn-201... , and 154 according to Reis et al. (2020)REIS, R.B., FROTA, A., DEPRÁ, G.C., OTA, R.R., & GRAÇA, W.J. 2020. Freshwater fishes from Paraná State, Brazil: an annotated list, with comments on biogeographic patterns, threats, and future perspectives. Zootaxa 4868(4): 451-494. https://doi.org/10.11646/zootaxa.4868.4.1
https://doi.org/10.11646/zootaxa.4868.4.... , studies on low-order streams are necessary, mainly because of their importance for freshwater biodiversity, role in contributing to ecosystem service and sensitivity and vulnerability to anthropogenic disturbances (Biggs et al. 2017BIGGS, J., von FUMETTI, S., & KELLY-QUINN, M. 2017. The importance of small waterbodies for biodiversity and ecosystem services: implications for policy makers. Hydrobiologia 793: 3-39. http://dx.doi.org/10.1007/s10750-016-3007-0
http://dx.doi.org/10.1007/s10750-016-300... ).

Rivers and streams of the region are intensely affected by the increased environmental degradation resulted from human activities, such as agricultural production (intensive crop production, livestock, and aquaculture) and urbanization (industrial and household effluents, and habitat changes) (Gubiani et al. 2010GUBIANI, E.A., GOMES, L.C., AGOSTINHO, A.A., & BAUMGARTER, G. 2010. Variations in fish assemblages in a tributary of the upper Paraná River, Brazil: a comparison between pre and post-closure phases of dams. River Res Appl. 26: 848-865. https://doi.org/10.1002/rra.1298
https://doi.org/10.1002/rra.1298... , Pereira et al. 2014PEREIRA, A.L., RIBEIRO, V.R., GUBIANI, E.A., ZACARKIM, C.E., & CUNICO, A.M. 2014. Ichthyofauna of urban streams in the western region of Parana State, Brazil. Check list 10(3): .550-555. https://doi.org/10.15560/10.3.550
https://doi.org/10.15560/10.3.550... ). Thus, a continuous monitoring and inventorying of their ichthyofauna are essential for the development of a database that contributes to a better understanding of the species distribution in changed environments, and assists in defining and implementing practices for biodiversity management and conservation.

Thus, the objective of the present study was to survey the ichthyofauna of nine low-order streams (second and third orders; Strahler, 1957STRAHLER, A.N. 1957. Quantitative analysis of watershed geomorphology. New Halen. Transactions: American Geophysical Union 38: 913-920.) that compose the Piquiri River basin (Upper Paraná Ecoregion) and are affected by agricultural, aquaculture and urbanization activities, and to inventory the occurring fish species in these environments to contribute to the improvement of information about the biodiversity of the region.

Material and Methods

1. Study area

The study was conducted in nine second and third-order streams that compose the Piquiri River basin and are located in the West and Northwest of the state of Paraná, South of Brazil (Figure 1). These regions comprise an area of 47,000 km² (23% of the total area of the state) and encompass 111 municipalities (IPARDES 2019). The regions have a humid subtropical climate, and its soil was classified as dystrophic Typic Hapludox (Latossolo Vermelho-Escuro; EMBRAPA - SNLCS 1984), which has good fertility and is highly favorable to agriculture (Pereira et al. 2014PEREIRA, A.L., RIBEIRO, V.R., GUBIANI, E.A., ZACARKIM, C.E., & CUNICO, A.M. 2014. Ichthyofauna of urban streams in the western region of Parana State, Brazil. Check list 10(3): .550-555. https://doi.org/10.15560/10.3.550
https://doi.org/10.15560/10.3.550... ). The main economic activity in the regions is agriculture, but aquaculture is also an important activity. The West region is the main aquaculture production center of the state (Marengoni et al. 2007MARENGONI, N.G., BERNARDI, A., & GONÇALVES-JÚNIOR, A.C. 2007. Tilapicultura vs. Culturas da soja e do milho na região Oeste do Paraná. Informações Econômicas 37: 41-49.) and one of the three highest national aquaculture production regions (Becker et al. 2015BECKER, E., SANTOS, J.A.A., SCHMIDT, C.A., & ZANDONA, E.T.P. 2015. Análise do processo de produção de filés de Tilápia por meio de simulação: Um estudo de caso. Engevista 17(4): 531-539.). The main produced species in this region is Oreochromis niloticus L. (1758) (Nile tilapia). The aquaculture is less expressive in the Northwest region (SEAB 2018).

Figure 1
Sampled streams in the Piquiri River basin, Paraná, Brazil: 1) Córrego Tapera; 2) Córrego Taquari; 3) Rio do Bagre; 4) Sanga 16 de Janeiro Stream; 5) Rio Baiano; 6) Rio das Antas; 7) Arroio Santa Fe; 8) Arroio Pioneiro; and 9) Córrego Tatu. Dots indicate local of samplings over the longitudinal gradient of the streams (headwater, middle and mouth).

2. Ichthyofauna sampling and data analysis

The ichthyofauna was sampled quarterly from December 2017 to September 2018 at three sites of each stream in their longitudinal gradient (headwater, middle and mouth - Table 1). Fish assemblages were sampled using an electrofishing equipment (portable generator of alternating current of 2.5 kW, 400 V, 2A) in 50-meter segments delimited by multifilament nets f 0.5-centimeter mesh. Three successive downstream-to-upstream catches were established in each segment (Esteves & Lobón-Cerviá 2001ESTEVES, K.E., & LOBÓN-CERVIÁ, J. 2001. Composition and trophic structure of a fish community of a clear water Atlantic rainforest stream in southeastern Brazil.Environ. Biol. Fishes 62(4): 429-440. https://doi.org/10.1023/A:1012249313341
https://doi.org/10.1023/A:1012249313341... ).

The captured specimens were anesthetized in a eugenol solution (100 mg. L^-1) and fixed in a 10% formalin solution. The fishes were identified in a laboratory, according to Ota et al. (2018OTA, R.R., DEPRÁ, G.C., GRAÇA, W.J., & PAVANELLI, C.S. 2018. Peixes da planície de inundação do alto rio Parana e áreas adjacentes: revised, annotated and updated. Neotrop Ichthyol 16(2):1-111. http://dx.doi.org/10.1590/1982-0224-20170094
http://dx.doi.org/10.1590/1982-0224-2017... ). Sample specimens were preserved in 70% alcohol and deposited in the ichthyological collection of the Nucleus of Research in Limnology, Ichthyology and Aquaculture (NUPELIA) of the State University of Maringá, Paraná State, Brazil. The sampling of the biological material was authorized by the Chico Mendes Institute for Conservation of Biodiversity (ICMBIO; License no. 24680-1). The sampling protocol used in the present study was subjected to a process of ethical review and approved by the Ethics Committee on the Use of Animals of the Federal University of Paraná (CEUA - UFPR), in Palotina, PR, Brazil, under the Protocol no. 01/2018.

The sampling efficiency was evaluated based on data of total abundance, using the Chao 1 and Jackknife 1 richness estimators, which consider the actual number of species richness based on rare species shared between groups of samples. Subsequently, species accumulation curves were developed. All analyses were made in the Estimates 9.0 program (Colwell 2013COLWELL, R.K. 2013. EstimateS: Statistical estimation of species richness and shared species from samples. Version 9.0. User’s Guide and application. Accessible at: http://viceroy.eeb.uconn.edu/estimates/
http://viceroy.eeb.uconn.edu/estimates/... ).

Results

A total of 14,507 individuals were collected in the nine streams evaluated. Specimens were from six orders, 20 families, 46 genera, and 70 species (Table 2). The highest species richness was found for the orders Characiformes (34 species) and Siluriformes (21 species), which represented 80% of the total species sampled in the streams evaluated. The families that presented higher species richness were Characidae (18 species), Loricariidae (nine species), and Heptapteridae (seven species), representing 49% of the total species richness (Figure 2).

Figure 2
Richness of species by order and family identified in the nine sampled streams of the Piquiri River basin, Paraná, Brazil.

The streams with higher species richness were the Córrego Tapera (48 species), followed by the Córrego Taquari and Rio do Bagre, both presenting 42 species. Low species richness was found in the Córrego Tatu and Rio das Antas (16 species each). Among the species collected, six were captured in all streams evaluated, while 11 were found exclusively in one of the streams (Table 2).

The highest abundances were found for the orders Siluriformes (42%) and Characiformes (37%). Pimelodella avanhandavae and Psalidodon aff. paranae were the most representatives, with approximately 23% of the total abundance found. Psalidodon aff. paranae and Phalloceros harpagos were more abundant in the Rio das Antas, presenting 51% and 25% total abundance found, respectively. Pimelodella avanhandavae represented 61% of the total abundance found in the Arroio Pioneiro Stream, whereas Poecilia reticulata represented 66% of the abundance in the Córrego Tatu. Hypostomus cf. tietensis represented 27% of the abundance in Córrego Santa Fé. All species found in the others streams presented relative abundances lower than 24%.

Nine species identified in the samplings of the present study had not yet been recorded in the basin by other studies, namely Aequidens plagiozonatus, Apteronotus cf. caudimaculosus, Coptodon rendalli, Erythrinus erythrinus, Hoplias misionera, Moenkhausia australe, M. bonita, Pyrrhulina australis and Steindachnerina brevipinna.

Regarding the origin of the ichthyofauna studied, 14 species were classified as non-native to the Piquiri River basin (Table 2), which represented 14% of the total abundance found. Poecilia reticulata, Bryconamericus exodon, Oreochromis niloticus, Aequidens plagiozonatus and Gymnotus pantanal presented the highest abundances among these non-native species.

The estimators of richness used indicated a good sampling efficiency, presenting similar values to those found in the samplings (Figure 3).

Figure 3
Species accumulation curves (Robs) and richness estimations (Chao 1 and Jackknife 1) for fish samples collected quarterly in streams of the Piquiri River basin, Paraná, Brazil, from December 2017 to September 2018. Sanga 16 de Janeiro (A); Rio das Antas (B); Rio do Bagre (C); Rio Baiano (D); Arroio Pioneiro (E); Arroio Santa Fé (F); Córrego Tapera (G); Córrego Taquari (H); and Córrego Tatu (I).

Discussion

The non-parametric richness estimators indicated a good efficiency in the samplings, since the estimated values ​​of richness approximate the real number of species recorded in each stream. These estimators, despite being sensitive to changes in the distribution of abundance and despite providing estimates of the lower limit of richness at a local scale, consider environmental heterogeneity (Gotelli & Chao 2013GOTELLI, N.J., & CHAO, A. 2013. Measuring and estimating species richness, species diversity, and biotic similarity from sampling data. In S. A. Levin (Ed.), Encyclopedia of biodiversity, 2nd ed., vol. 5, pp. 195-211. Waltham: Academic Press., Gwinn et al. 2016GWINN, D.C., ALLEN, M.S., BONVECHIO, K.I., HOYER, M.V., & BEESLEY, L.S. 2016. Evaluating estimators of species richness: The importance of considering statistical error rates. Methods Ecol. Evol. 7: 294-302. https://doi.org/10.1111/2041-210X.12462
https://doi.org/10.1111/2041-210X.12462... , Bevilacqua et al. 2017BEVILACQUA, S., UGLAND, K.I., PLICANTI, A., SCUDERI, D., & TERLIZZI, A. 2017. An approach based on the total-species accumulation curve and higher taxon richness to estimate realistic upper limits in regional species richness. Ecol. Evol. 8: 405-415. https://doi.org/10.1002/ece3.3570
https://doi.org/10.1002/ece3.3570... ). This is an important factor in the present study, given the number of sampling sites and the fact that they have different watershed land uses. In this way, nine species identified in the present study had not yet been recorded in the Piquiri River basin, even considering recent studies that updated the ichthyofauna composition of this basin and reported the occurrence of 152 (Cavalli et al. 2018CAVALLI, D., FROTA, A., LIRA, A.D., GUBIANI, E.A., MARGARIDO, V. P., & GRAÇA, W. J. 2018. Update on the ichthyofauna of the Piquiri River basin, Parana, Brazil: a conservation priority area. Biota neotropica 18(2): e20170350. https://doi.org/10.1590/1676-0611-bn-2017-0350 (last acess in: 23/12/2020)
https://doi.org/10.1590/1676-0611-bn-201... ) and 154 fish species (Reis et al. 2020REIS, R.B., FROTA, A., DEPRÁ, G.C., OTA, R.R., & GRAÇA, W.J. 2020. Freshwater fishes from Paraná State, Brazil: an annotated list, with comments on biogeographic patterns, threats, and future perspectives. Zootaxa 4868(4): 451-494. https://doi.org/10.11646/zootaxa.4868.4.1
https://doi.org/10.11646/zootaxa.4868.4.... ). This indicates that the ichthyofauna diversity of the Piquiri River basin is underestimated, especially that of its low-order tributaries, and denotes a need for continuous researches in these environments. Although the information about ichthyofauna diversity in Neotropical streams has been improved over the years, several species are still unknown to science (Ota et al. 2015OTA, R.R., MESSAGE, H.J., GRAÇA, W.J. & PAVANELLI, C.S. 2015. Neotropical Siluriformes as a model for insights on determining biodiversity of animal groups. PLoS ONE 10(7): 1-13. https://doi.org/10.1371/journal.pone.0132913
https://doi.org/10.1371/journal.pone.013... , Frota et al. 2019FROTA, A., MESSAGE, H. J., OLIVEIRA, R. C., BENEDITO, E., & GRAÇA, W. J. 2019. Ichthyofauna of headwater streams from the rio Ribeira de Iguape basin, at the boundaries of the Ponta Grossa Arch, Parana, Brazil. Biota Neotropica 19(1): 1-12. https://doi.org/10.1590/1676-0611-bn-2018-0666 (last acess in: 5/3/2021)
https://doi.org/10.1590/1676-0611-bn-201... , Mezzaroba et al. 2021MEZZAROBA, L., DEBONA, T., FROTA, A., GRAÇA, W.J., & GUBIANI, E.A. 2021. From the headwaters to the Iguassu Falls: Inventory of the ichthyofauna in the Iguassu River basin shows increasing percentages of nonnative species. Biota Neotropica 21(2): 1-14. https://doi.org/10.1590/1676-0611-BN-2020-1083 (last acess in: 26/5/2021)
https://doi.org/10.1590/1676-0611-BN-202... ).

Neotropical streams in South America are characterized by the occurrence of a high fish diversity due to the geographic isolation of this continent and its drainage basins, and the high diversity of habitats over its longitudinal gradient, with predominance of species from the orders Characiformes and Siluriformes (Lowe-McConnell 1999, Agostinho et al. 2007AGOSTINHO, A.A., GOMES, L.C., & PELICICE, F.M. 2007. Ecologia e manejo de recursos pesqueiros em reservatórios do Brasil. Maringá, Eduem. 501p.). The predominance of these orders has been recorded for the Upper Paraná Ecoregion (Langeani et al. 2007LANGEANI, 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 Neotropica 7: 181-197. https://doi.org/10.1590/S1676-06032007000300020 (last acess in: 23/12/2020)
https://doi.org/10.1590/S1676-0603200700... , Cavalli et al. 2018CAVALLI, D., FROTA, A., LIRA, A.D., GUBIANI, E.A., MARGARIDO, V. P., & GRAÇA, W. J. 2018. Update on the ichthyofauna of the Piquiri River basin, Parana, Brazil: a conservation priority area. Biota neotropica 18(2): e20170350. https://doi.org/10.1590/1676-0611-bn-2017-0350 (last acess in: 23/12/2020)
https://doi.org/10.1590/1676-0611-bn-201... ), as found in the present study.

Regarding the order Characiformes, a high occurrence of small-size species from Characidae was observed, which is highly distributed in freshwater environments, encompasses a large proportion of stream fish species, and presents diverse feeding and reproductive habits (Britski 1972BRITSKI, H.A. 1972. Peixes de água doce do estado de São Paulo. In: Comissão Internacional da Bacia Parana - Paraguai. Poluição e piscicultura. São Paulo, Faculdade de Saúde Pública da USP e Instituto de Pesca, p.79-108., Lowe-McConnell 1999). The predominance of species of the order Siluriformes is related to habitat characteristics, such as presence of riffles and boulders in the stream bed substrate, which favor the occurrence of Loricariidae and Heptapteridae. The latter is associated with environments near rapids and that have submersed marginal vegetation and cracks between rocks (Bockmann and Guazzelli 2003BOCKMANN, F.A., & GUAZZELLI, G.M. 2003. Family Heptapteridae. In: REIS, R.E., KULLANDER, S.O., & FERRARIS, C.J. Check list of the freshwater fishes of South and Central America, Porto Alegre, EDIPUCRS. p.406-431., Pagotto et al. 2011PAGOTTO, J.P.A., GOULART, E., OLIVEIRA, E.F., & YAMAMURA, C.B. 2011. Trophic ecomorphology of Siluriformes (Pisces, Osteichthyes) from a tropical stream. Braz. J. Biol. 71(2): 469-479. http://dx.doi.org/10.1590/S1519-69842011000300017
http://dx.doi.org/10.1590/S1519-69842011... ).

The predominance of the Psalidodon aff. paranae and Phalloceros harpagos in the Rio das Antas, whose was dammed to supply water for aquaculture systems, indicates the plasticity of these species in modified habitats by human actions. Phalloceros harpagos and species of Psalidodon are common in streams of the Upper Paraná River basin (Langeani et al. 2007LANGEANI, 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 Neotropica 7: 181-197. https://doi.org/10.1590/S1676-06032007000300020 (last acess in: 23/12/2020)
https://doi.org/10.1590/S1676-0603200700... , Gubiani et al. 2010GUBIANI, E.A., GOMES, L.C., AGOSTINHO, A.A., & BAUMGARTER, G. 2010. Variations in fish assemblages in a tributary of the upper Paraná River, Brazil: a comparison between pre and post-closure phases of dams. River Res Appl. 26: 848-865. https://doi.org/10.1002/rra.1298
https://doi.org/10.1002/rra.1298... ) and their wide plasticity allows them to explore efficiently changed habitats (Monaco et al. 2014MONACO, I.A., SÚREZ, Y.R., & LIMA-JUNIOR, S.E. 2014. Influence of environmental integrity on feeding, condition and reproduction of Phalloceros harpagos Lucinda, 2008 in the Tarumã stream micro-basin. Acta Sci Biol Sci 36: 181-188. https://doi.org/10.4025/actascibiolsci.v36i2.21394
https://doi.org/10.4025/actascibiolsci.v... , Pereira et al. 2014PEREIRA, A.L., RIBEIRO, V.R., GUBIANI, E.A., ZACARKIM, C.E., & CUNICO, A.M. 2014. Ichthyofauna of urban streams in the western region of Parana State, Brazil. Check list 10(3): .550-555. https://doi.org/10.15560/10.3.550
https://doi.org/10.15560/10.3.550... ). The predominance of the non-native species Poecilia reticulata in the Córrego Tatu, where environmental changes occurred due to urbanization near the headwater reach, denotes the plasticity of this species to explore changed environments. Previous studies indicate similar patterns, with predominance of P. reticulata in environments that were affected by urbanization (Cunico et al. 2006CUNICO, 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: 1101-1110. https://doi.org/10.1590/S0101-81752006000400018
https://doi.org/10.1590/S0101-8175200600... , Gubiani et al. 2010). Urban development is one of the main factors for biodiversity changes in streams because it fragments natural landscapes, changing hydrological regimes, matter flow, and nutrient cycling. It is associated with the establishment of non-native species that can increase their abundance and dominance under adverse environmental conditions (Cunico et al. 2012).

The occurrence of the non-native Oreochromis niloticus and Coptodon rendalli is related to the intense aquaculture activity in the region. Aquaculture is the main vector for introducing non-native species into environments around the world (Lima et al. 2018LIMA, L.B., OLIVEIRA, F.J.M., GIACOMINI, H.C., & LIMA-JUNIOR, D.P. 2018. Expansion of aquaculture parks in the increasing risk of non-native species invasions in Brazil. Rev Aquac 10: 111-122. https://doi.org/10.1111/raq.12150
https://doi.org/10.1111/raq.12150... ), and highly frequent introductions have great potential of negatively effects on the diversity of native species and the ecosystem services (Pelicice et al. 2017PELICICE, F.M., AZEVEDO-SANTOS, V.M., VITULE, J.R.S., ORSI, M.L., LIMA-JUNIOR, D.P., MAGALHÃES, A.L.B., POMPEU, P.S., PETRERE-JUNIOR, M., & AGOSTINHO, A.A. 2017. Neotropical freshwater fishes imperilled by unsustainable policies. Fish Fish 18: 1119-1133. https://doi.org/10.1111/faf.12228
https://doi.org/10.1111/faf.12228... ). The high abundance of O. niloticus and occurrence of C. rendalli found in the streams evaluated are due to escapes from ponds used for aquaculture activities, denoting the need for efficient escape containment mechanisms (Nobile et al. 2019NOBILE, A.B., CUNICO, A.M., VITULE, J.R.S., QUEIROZ, J., VIDOTTO- MAGNONI, A.P., GARCIA, D.A.Z., ORSI, M.L., LIMA, F.P., ACOSTA, A.A., DA SILVA, R.J., PRADO, F., PORTO-FORESTI, F., BRANDÃO, H., FORESTI, F., OLIVEIRA, C., & RAMOS, I.P. 2019. Status and recommendations for sustainable freshwater aquaculture in Brazil. Rev Aquac: 1-23. https://doi.org/10.1111/raq.12393
https://doi.org/10.1111/raq.12393... ). The occurrence of non-native species due to aquaculture activities is also reported by others studies on the region and can be attributed to the low distances between fish ponds and streams, which allows escapes through effluent waters under inadequate management, rupture or overflow in rainy periods, and intentional releases (Orsi & Agostinho 1999ORSI, M.L., & AGOSTINHO, A.A. 1999. Introdução de peixes por escape acidental de tanques de cultura em rios da Bacia do Rio Paraná. Rev. Bras. Zool. 16: 557-560., Forneck et al. 2016FORNECK, S.C., DUTRA, F.M., ZACARKIM, C.E., & CUNICO, A.M. 2016. Invasions risk by non-native freshwater fishes due to aquaculture activity in neotropical a river. Hydrobiologia 773(1): 193-205. https://doi.org/10.1007/s10750-016-2699-5
https://doi.org/10.1007/s10750-016-2699-... , Ribeiro et al. 2018RIBEIRO, V.R., GUBIANI, E.A., & CUNICO, A.M. 2018. Occurrence of non-native fish species in a Neotropical River under the influence of aquaculture activities. Bol. Inst. Pesca, São Paulo 44(1): 80-90. https://doi.org/10.20950/1678-2305.2018.288
https://doi.org/10.20950/1678-2305.2018.... , Casimiro et al. 2018CASIMIRO, A.C.R., GARCIA, D.A.Z., VIDOTTO-MAGNONI, A.P., BRITTON, J.R., AGOSTINHO, A.A., ALMEIDA, F.S., & ORSI, M.L. 2018. Escapes of non-native fish from flooded aquaculture facilities: the case of Paranapanema River, southern Brazil. Zoologia 35: 1-6. https://doi.org/10.3897/zoologia.35.e14638
https://doi.org/10.3897/zoologia.35.e146... , Forneck et al. 2020).

Other non-native species were found in the present study due to different vectors of species introduction in the basin. The occurrence of Bryconamericus exodon is associated with the transposition channel of the Itaipu Hydroelectric Power Plant, which connects the downstream region of the reservoir to the upstream region of the dam (Ota et al. 2018OTA, R.R., DEPRÁ, G.C., GRAÇA, W.J., & PAVANELLI, C.S. 2018. Peixes da planície de inundação do alto rio Parana e áreas adjacentes: revised, annotated and updated. Neotrop Ichthyol 16(2):1-111. http://dx.doi.org/10.1590/1982-0224-20170094
http://dx.doi.org/10.1590/1982-0224-2017... ). The presence of the Gymnotus pantanal is probably because of accidental introductions due to use of live baits for fishing, and floods in biogeographic barriers, as in the Salto de Sete Quedas, which resulted from the formation of the Itaipu reservoir. The presence of Aequidens plagiozonatus is possibly because of the ornamental fish trade. This species is found in the Upper Parana River basin since 2014 (Ota et al. 2018) and was found in all streams evaluated in the present study.

Regarding the native species found, Prochilodus lineatus and Leporinus friderici stand out. These species are abundant in the Upper Paraná River basin, present ecological and economical importance, and are long-distance migratory species that move from feeding areas to breeding areas (Agostinho et al. 2004AGOSTINHO, A.A., GOMES, L.C., VERÍSSIMO, S., & OKADA, E.K. 2004b. Flood regime, dam regulation and fish in the Upper Parana River: effects on assemblage attributes, reproduction and recruitment. Rev. Fish Biol. Fish. 14: 11-19.b, Agostinho et al. 2007, Makrakis et al. 2012MAKRAKIS, M.C, MIRANDA, L.E., MAKRAKIS, S., FONTES-JUNIOR, H.M., MORLIS, W.G., DIAS, J.H.P., & GARCIA, O.J. 2012. Diversity in migratory patterns among Neotropical fishes in a highly regulated river basin. J. Fish Biol. 81: 866-881. https://doi.org/10.1111/J.1095-8649.2012.03346.X
https://doi.org/10.1111/J.1095-8649.2012... , Silva et al. 2015SILVA, P.S., MAKRAKIS, M.C., MIRANDA, L.E., MAKRAKIS, S., ASSUMPÇÃO, L., PAULA, S., DIAS, J.H.P., & MARQUES, H. 2015. Importance of reservoir tributaries to spawning of migratory fish in the upper Parana River. River Res Appl 31: 313-322. https://doi.org/10.1002/rra.2755
https://doi.org/10.1002/rra.2755... , Bido et al. 2018BIDO, A.F., URBINATI, E.C., MAKRAKIS, M.C., CELESTINO, L.F., SERRA, M., & MAKRAKIS, S. 2018. Stress indicators for Prochilodus lineatus (Characiformes: Prochilodontidae) breeders during passage through a fish ladder. Mar. Freshw. Res.:1-8. http://dx.doi.org/10.1071/MF18087
http://dx.doi.org/10.1071/MF18087... ). The presence of juveniles of these species in the sampled streams reinforces the need to maintain the Piquiri River basin free from hydroelectric dams, since these barriers hinder migration routes, preventing those juveniles of these species access environments where migratory species breed and grow (Agostinho et al. 2008, Silva et al. 2015).

In view of the results obtained and in agreement with other researches carried out recently in the basin (Cavalli et al. 2018CAVALLI, D., FROTA, A., LIRA, A.D., GUBIANI, E.A., MARGARIDO, V. P., & GRAÇA, W. J. 2018. Update on the ichthyofauna of the Piquiri River basin, Parana, Brazil: a conservation priority area. Biota neotropica 18(2): e20170350. https://doi.org/10.1590/1676-0611-bn-2017-0350 (last acess in: 23/12/2020)
https://doi.org/10.1590/1676-0611-bn-201... , Reis et al. 2020REIS, R.B., FROTA, A., DEPRÁ, G.C., OTA, R.R., & GRAÇA, W.J. 2020. Freshwater fishes from Paraná State, Brazil: an annotated list, with comments on biogeographic patterns, threats, and future perspectives. Zootaxa 4868(4): 451-494. https://doi.org/10.11646/zootaxa.4868.4.1
https://doi.org/10.11646/zootaxa.4868.4.... ), 163 fish species are recorded in the Piquiri River basin. Regarding the number of non-native species, it is worth mentioning that Cavalli et al. (2018) recorded 30 species among the 152 sampled and that Reis et al. (2020) recorded 41 species among the 154. Despite the high number already registered, in the present study, five of the nine new records are of non-native species, totaling 48 in the referred basin, which reinforces the importance of knowledge and monitoring of streams that are under strong anthropogenic pressure.

The list of species found in the present study contributes to the existing database of ichthyofauna distribution in Neotropical streams, considering that it shows the presence of species that had been not yet registered for the Piquiri River basin, and a high occurrence of non-native species in the basin. The study basin is in the last stretch free from hydroelectric dams of the Upper Paraná River basin, which is essential for the integrity of biological processes in this environment. Therefore, this study reinforces the importance of inventories and monitoring of highly sensitive environments to anthropogenic changes.

Acknowledgements

The authors thank the National Council for Scientific and Technological Development (CNPq) for the financial support (Process no. 405766/2016-5, Coordinator A. M. Cunico) and the scholarship (Process no. 141159/2018-9, M. P. Camargo). We also thank the researchers of the Center of Research in Limnology, Ichthyology and Aquaculture (Nupélia) of the State University of Maringá for their contributions in the taxonomic identification of the individuals collected.

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