Update on the ichthyofauna of the Piquiri River basin , Paraná , Brazil : a conservation priority area

Knowledge of the fish species in river basins is among the minimum requirements for the management of water and fish resources. Therefore, the aim of this study was to update the fish species composition of the Piquiri River basin, upper Paraná River basin. Data were gathered from recent information published in specialized literature and records for ichthyology collections. This update reports the occurrence of 152 fish species distributed in 8 orders, 31 families, and 89 genera. Non-native species accounted for 20% of all species, and the construction of the Itaipu Power Plant and its fish ladder were the main vectors of introduction. Three percent of the species were endangered, and 11% were classified as migratory. The Piquiri River basin harbors a large number of species, some of which are rare, endangered, migratory, endemic, and even unknown by science. Because of this, maintaining the integrity of this river basin will support the persistence of regional biodiversity.


Introduction
Knowing the fish species in a river basin is essential for any amount of water and fishery management (Oliveira et al. 2014, Agostinho et al. 2016).Spatial and temporal fish assemblage patterns can be understood by biotic, abiotic and spatial factors that determine fish assemblage biodiversity (Jackson et al. 2001), enabling the assessment of the environmental quality of a river system.Although much sampling has been carried out in basins to record existing ichthyofaunal compositions, several species are still unknown by science (Langeani et al. 2007, Galves et al. 2009, Frota et al. 2016a).Recent fish inventories in previously sampled areas have revealed new species (Pavanelli 2006, Frota et al. 2016a); consequently, the number of descriptions of new species has increased in recent years.It is thought that a full description of existing species is still far from being achieved (Ota et al. 2015).
In this regard, the upper Paraná River basin is no different; although recent studies have recorded 310 valid fish species and approximately 50 likely new fish species (Langeani et al. 2007), little is known about the fish fauna of the main tributaries of the upper Paraná River basin (Galves et al. 2009).Thus, information on fish assemblages, especially in the tributaries, is still scarce and most likely should be greater than currently known.
The Piquiri River is one of the main tributaries of the left bank of the upper Paraná River basin (Affonso et al. 2015), the third largest drainage area in the State of Paraná.It is highlighted as one of the last tributaries free of damming in the upper Paraná River basin (Agostinho et al. 2004, Gubiani et al. 2010, Affonso et al. 2015).This area is one of the last environments used by migratory fish during breeding displacement (Gogola et al. 2010, 2013, Gubiani et al. 2010).Despite its importance for fish assemblages, studies on its ichthyofauna composition are still scarce.Agostinho et al. (1997Agostinho et al. ( , 2004) registered 57 species.In Gubiani et al. (2006), the number increased to 62 species.Later, in Gubiani et al. (2010), 69 species were recorded.Additionally, recent studies have sampled small-order streams and larger tributaries of this river, increasing the specific richness of fish in the basin (Delariva & Silva 2013, Dei Tos et al. 2014).
In view of the abovementioned, this study aims to update the fish species composition of the Piquiri River, upper Paraná River basin, by scrutinizing the latest information in the literature and species records from ichthyology collections.In addition, the threat level, origin, biogeography, migratory behavior, and main current and future human impacts that may affect fish biodiversity in the basin are also discussed.

Study area
The Piquiri River basin comprises a drainage area of approximately 25,000 km 2 (SEMA, 2010), the third largest in the State of Paraná (geographical coordinates 23°65' -25°25' S and 51°59' -54°07' W; Figure 1), which is approximately 12% of the Paraná state area (SEMA 2010).According to Maack (2012), its sources are located at an altitude of 1,237 m in the São João Mountains at the third plateau, south-central region of the state, and it runs 485 km before reaching the Paraná River on the border between the municipalities of Altônia and Terra Roxa.The river comprises several rapids, waterfalls, and narrow stretches, with a total fall of approximately 1,000 m from its headwaters to its mouth (Agostinho & Júlio Jr. 1999).The main tributaries of the Piquiri River are the Cantú, Tricolor, Goioerê, and Xambrê rivers on the right bank and the Sapucaia and Melissa rivers on the left bank (Paiva 1982).
Local land use is based on farming, fish farming and livestock, and soybeans, wheat, corn, sugarcane, and cassava are the primary crops.The industrial segment is related to livestock and includes industries such as dairy and cold stores.The region has undergone several changes, with few forest remnants near the municipalities of Guaraniaçu, Laranjal, and Altamira do Paraná.In the basin, there are key conservation units, such as the São Camilo Biological Reserve in Palotina, the Area of Relevant Ecological Interest of São Domingos between Roncador and Nova Cantú (Paraná 2010), and the Perobas Biological Reserve, which is located in the municipalities of Cianorte and Tuneiras do Oeste (Delariva & Silva 2013).The landscape is divided into intensive farming areas, artificial grasslands, and natural fields with small forest, urban, and industrial areas.The urban population living in the basin is approximately half a million inhabitants, of which 99% have a public water supply and only 28% have domestic effluent collection services (SEMA 2010).

Database
The update of the fish species was performed by consulting fish collections with a vast amount of material such as the Londrina State University Museum in Londrina (MZUEL), the Museum of Zoology of the University of São Paulo in São Paulo (MZUSP), the Capão da Imbuia Natural History Museum in Curitiba (MHNCI), the PUCRS Museum of Science and Technology in Porto Alegre (MCP), the Nupélia Ichthyology Collection of the State University of Maringá in Maringá (NUP), and the Ichthyology Collection of GERPEL of the Western Paraná State University in Toledo (CIG).The species records of these collections came from online databases, e.g., Species Link, which is an information distribution network integrating live data from diverse scientific collections (CRIA 2016).In addition, to complement the information, in September 2016, bibliographical research was performed using articles in the Thomson Reuters (ISI Web of Knowledge, apps.isiknowledge.com),Elsevier -ScienceDirect (http://www.sciencedirect.com), and Scielo (http://www.scielo.org)databases that addressed the topic of "ichthyofauna of the Piquiri River basin."The search terms in the "Topic" field were "fish* OR ichthyo* OR check list AND Piquiri River", and the searched timespan included all years up to the date of the search.The search was then refined according to the following research areas: Environmental Sciences, Ecology, Zoology, Freshwater Biology, Biodiversity, Conservation, and Fisheries and Water Resources.In addition, all articles including lists of fish species of the Piquiri River basin that were published in the journal Check List: Journal of Species Lists and Distributions, which is not indexed in the aforementioned databases were also included in our review.For this, the search was carried out using the option "search for articles" at the journal website (http://www.checklist.org.br/search) and searching all categories and volumes.
For a study to be included in this bibliographical research it needed to show a list of fish species caught in the Piquiri River, upper Paraná River basin, Brazil.Non-related articles were excluded based on their title, abstract or, if necessary, after a careful reading of the entire text.The articles that met the required criteria were selected and tabulated in a spreadsheet to compose the final list of fish species.After the final tabulation of the complete list of fish species recorded for the Piquiri River basin, the list was reviewed by experts to correct possible doubts about the occurrence or identification of fish species.
Fish species were classified based on Eschmeyer et al. (2016).However, the threat level for each species was set according to the Portaria do Ministério do Meio Ambiente, nº 445 (December 17 of 2014) (BRASIL 2014), which was amended by Decree nº 98 (April 28 of 2015) (BRASIL 2015).These regulations classify the endangered species of fish and aquatic invertebrates from the Brazilian fauna with the following categories: Extinct in the Wild (EW), Critically Endangered (CR), Endangered (EN), and Vulnerable (VU).In addition, the species were categorized by origin based on the Langeani et al. (2007) method and grouped into autochthonous (native to the upper Paraná River basin), allochthonous (introduced species belonging to the Neotropical region), and exotic (from other continents) categories.If introduced, the introduction vectors were determined based on the species occurrence and distribution, as well as relevant literature, according to Reis et al. (2003), Langeani et al. (2007), Graça & Pavanelli (2007), Júlio Jr. et al. (2009) and Frota et al. (2016a).The possible causes of the occurrence of these species in the Piquiri River basin were grouped into seven categories: 1) Itaipu, species first recorded shortly after the construction of the Itaipu Dam with its native populations from the lower Paraná River basin; 2) Itaipu channel, species also coming from the lower Paraná River basin and introduced as a result of the construction and operation of the Itaipu Piracema Channel; 3) aquaculture, species widely used in the fish farms in the region; 4) baiting, species introduced by the use of natural baits for sport fishing; 5) mosquito control and aquarium purposes, species introduced for mosquito population control and species highly represented in fishkeeping; 6) sport-fishing, species introduced for sport fishing; 7) stocking, species introduced for fish stocks.In addition, species were classified according to their migratory status as proposed by Vazzoler (1996), Nakatani et al. (2001), and Agostinho et al. (2003), although only species with migratory behavior were evaluated in this way and shown in the results.Lastly, to discuss the main current and future human impacts on the region, predictions for the construction of small power plants (SPPs) and power plants (PPs) in the Piquiri River basin were mapped and computed by geographic maps of the Brazilian electric power sector (ANEEL 2016).

Results
The update on ichthyofauna diversity for the Piquiri River basin revealed 152 species distributed in 8 orders, 31 families, and 89 genera (Table 1).The orders with the highest species richness were Siluriformes (69 species) and Characiformes (59 species), representing approximately 84% of all species recorded in the basin (Figure 2).The families showing the largest species richness were Loricariidae (26 species), Characidae (23 species), Pimelodidae (14 species), Anostomidae (12 species), and Heptapteridae (10 species), comprising nearly 56% of all species (Figure 2).Fifteen of the discovered species are believed to be new to science (Table 1), representing approximately 12% of the basin's total native species.

Discussion
The outcomes of the update reveal 152 fish species, many which have already been reported by Graça & Pavanelli (2007), in the floodplain of the upper Paraná River and bordering areas.Although the Piquiri River drainage basin is partly within this floodplain, our results point to an intimate association between the basin and the maintenance of ichthyofauna biodiversity in this stretch of the upper Paraná River.This is because the studied river is one of the last refuge areas for a great proportion of the remaining native ichthyofauna (Baumgartner et al. 2004, Antonio et al. 2007, Gubiani et al. 2010, Affonso et al. 2015).
Ichthyofauna survey.The current survey discloses a much higher number of fish species than that recorded by Gubiani et al. (2006Gubiani et al. ( , 2010)), who reported 62 and 69 species in 2006 and 2010, respectively.This new update represents a nearly 120% increase in the number of species recorded in the basin since the last list was released.When comparing the ichthyofauna found in the basins located in the State of Paraná, the Piquiri River basin has an absolute richness of fish species that is higher than the richness of the Pirapó basin (76 species, Pagotto et al. 2012), the Ivaí River basin (118 species, Frota et al. 2016a), the upper and lower Iguaçu River basin (41 and 106 species respectively, Ingenito et al. 2004, Baumgartner et al. 2012), and the Tibagi River basin (151 species, Raio & Bennemann 2010).Approximately 49% of the species listed here were coincident with those recorded for the upper Paraná River (see Langeani et al. 2007).
Introduced species.Most of the species introduced into the Piquiri River basin dispersed after the construction of the Itaipu Dam.After the dam was closed, the Sete Quedas, a natural geographic barrier separating two ichthyofauna provinces, was flooded.This area comprises the mid-lower and upper Paraná River within the city of Guaíra (Graça & Pavanelli 2007, Vitule et al. 2012).Consequently, many fish species previously isolated by this barrier were introduced into the upper Paraná River basin (Júlio Jr. et al. 2009, Vitule et al. 2012).Hence, after the closing of Itaipu Dam (see Júlio Jr. et al. 2009), 23 of the introduced species were recorded in the Piquiri River basin.Conversely, the occurrence of some species such as Bryconamericus exodon, Hemiodus orthonops, and Pimelodella taenioptera, is not related to the flooding of the Sete Quedas but is related to the functioning of the Itaipu Piracema channel, a passage for fish downstream and upstream of the Itaipu Dam (Graça & Pavanelli 2007, Júlio Jr. et al. 2009).This channel is envisaged as a continuous source of fish species introduced to the upper Paraná River basin (Agostinho et al. 2015).
Transposition systems that can be used as fish passages have been among the main strategies in an endeavor by the Brazilian authorities and electric power sector to reduce the damming effects on populations of migratory fish (Pompeu et al. 2012).Nonetheless, in addition to contributing to the rise of non-native fish, such systems have been identified as true ecological traps in some Brazilian dams, and their closure should be required (Pelicice & Agostinho 2008, Agostinho et al. 2012, Pompeu et al. 2012).These facts, which are related to the construction and functioning of the Itaipu Power Plant, are an indication that a biotic homogenization process is ongoing in the ichthyofauna of the upper Paraná River basin.These processes consequently lead to a decrease in taxonomic, genetic, and/or functional differences in the previously described biota (Olden 2006, Daga et al. 2015).Therefore, the construction of dams are a major form of global biodiversity loss and has been considered an unacceptable environmental alteration (Rockström et al. 2009, Stigall 2010, Vitule et al. 2012).
In addition, there are an alarming number of cases of species introduced by stocking, sport fishing, live bait use, control of mosquitoes, and fishkeeping (see Daga et al. 2015;Ribeiro et al. 2017).For instance, curvina (Plagioscion squamosissimus), a species introduced for stocking purposes, poses a threat to the other piscivorous species in the Piquiri River basin because it feeds on the same sources and is, most likely, a strong competitor (Pereira et al. 2015).The excellent visual predator, Cichla piquiti, has been illegally introduced throughout the country mainly for sport fishing and represents a threat to the diversity of native fish (Pelicice & Agostinho 2009;Pelicice et al. 2015) in the Piquiri River basin.All Gymnotus species are often used as live bait, which might cause releases between basins by ill-informed fishers.Although only G. pantanal is considered allochthonous, the other species of the genus have truly uncertain origins (Júlio Jr. et al. 2009).In addition, morphometric data show no differences among populations of G. inaequilabiatus from various sites of the upper Paraná River (Frota et al. 2014).Poecilia reticulata has been widespread worldwide as an ornamental animal and mosquito larvae control agent (Dussalt & Kramer 1981, Azevedo-Santos et al. 2016).This species is considered to be one of the most abundant in rural and urban streams at present (Oliveira & Bennemann 2005, Cunico et al. 2012, Pereira et al. 2014) likely because of its high resistance and resilience (Gomiero & Braga 2007, Daga et al. 2012) in addition to its high competitive efficiency against competition from invasive and native species (Pompeu & Alves 2003).
Another important vector of species introduction in aquatic environments is the escapes arising from fish farming.The Federal Law nº 5989 of 2009 intends to naturalize non-native fish species by decree in Brazil.Following this proposal, Cyprinus carpio and Oreochromis niloticus, which are non-native species, would end up being naturalized in the Piquiri River basin; therefore, they would be perceived as natural and can be used without legal restrictions in fish farming (Padial et al. 2017).Around the Piquiri River basin, innumerable fish farms are settled and breeding non-native species that show a high invasion risk (Lima Jr. et al. 2012, Pelicice et al. 2014, Forneck et al. 2016).Several authors have asserted the invading potential arising from fish farms and the negative effects of new introductions (Orsi & Agostinho 1999, Daga et al. 2015, Daga et al. 2016, Lima et al. 2016).
Endangered species.Environments with species listed in the vulnerable and endangered categories should be prioritized for conservation since the most likely evidence assigns them as highly and very highly endangered in the wild, respectively (IUCN 2017).The species of the Piquiri River basin listed in these categories are rare, so their population survival will depend narrowly on their tolerance to the biotic and abiotic changes occurring in the basin.Registered endangered species have rheophilic habits, are migratory (Brycon orbignyanus and Steindachneridion scriptum), and require allochthonous food sources (Brycon orbignyanus and Myloplus tiete) (Machado et al. 2008).The construction of dams, therefore, will lead to extreme changes in river habitats, turning rivers into semi-lentic systems, which exerts an intense negative effect on the fish species (Agostinho et al. 2016;Pelicice et al. 2017).
Migratory behavior and construction of electric power stations.Like other major tributaries of the floodplain of the upper Paraná River, the Piquiri River basin is used as a spawning ground for migratory fish (Baumgartner et al. 2004, Gubiani et al. 2010, Gogola et al. 2013).A vast majority of migratory species living in the basin are made up of large fish with relative ecological and economic importance to the region, such as pimelodida catfish, Salminus spp., Leporinus spp., Brycon orbignyanus, Piaractus mesopotamicus, and Prochilodus lineatus (Hoeinghaus et al. 2009).Recreational fishing of large migratory fish from the Piquiri River basin also poses a serious threat because it can alter the structure and production of the population stocks (Cooke & Cowx 2004).
In the coming years, the construction of 34 SPPs and 6 PPs, which must be installed within the main channel of the Piquiri River and its important tributaries, is expected (Figure 4).Some of these locations will continue to have no ichthyofaunal sampling prior to construction, particularly locations in Piquiri River tributaries such as the Sapucaia River (Figures 1 and 4).The electric power installations planned for the basin area would prevent fish access to ideal habitats, thus affecting fish distribution and reproduction and fishing in addition to influencing the basin landscape, causing serious ecosystemic effects (Affonso et al. 2015).The nature and intensity of the changes on aquatic biota are highly variable between reservoirs and should be studied on a case-bycase basis (Agostinho et al. 2016).However, overall, the dams cause extreme changes in the hydrological regime (Thomaz et al. 2004) as well as changes in the longitudinal distribution of fish species (Petry et al. 2011).Thus, electric power enterprises in the Piquiri River basin should be discussed in public hearings with joint initiatives undertaken by citizens, law specialists, and universities (Affonso et al. 2015).
New species and biogeography.The species recorded as new in this study account for a total percentage quite near that shown for the entire basin of the upper Paraná River (14% in Langeani et al. 2007).This shows that even with the increasing number of species descriptions over time, the knowledge of the actual number of animal species and respective geographical distributions in the area is far from complete (Ota et al. 2015).A great part of the new findings in the Piquiri River basin arose from an increased sampling effort for several scientific purposes.Therefore, the continuity of these samplings will undoubtedly reveal accurate data on new endangered populations.As such, similar efforts should be carefully extended to sites with no sampling efforts, and sites where the construction of PPs and SPPs are planned.
From an ichthyofaunal standpoint, the upper Paraná River basin encompasses a unique historical area, which is complex and partly shared with neighboring drainage areas (Langeani et al. 2007).One likely area of endemism exists in the headwater streams, mainly in the upper section of the Piquiri River basin.In such high altitudes, Trichomycterus cf.stawiarski and Planaltina sp. are shared, respectively, with the basins of the Jordão (lower Iguaçu River) and Ivaí (upper Paraná River) Rivers.The former species is reported as endemic to the Iguaçu River basin (Baumgartner et al. 2012), while the latter is regarded as endemic to the upper Ivaí River basin (Frota et al. 2016a).Therefore, the presence of these species in the Piquiri River basin suggests past connections between the upper courses of those basins that might have occurred prior to the uplift of Serra da Esperança, which caused the isolation of the respective headwaters (Frota et al. 2016b).Thus, the identification of an endemic zone in the neighboring region between the Piquiri, Ivaí, and Jordão basins would allow an improved understanding of the local biota evolution (Morrone 1994) in addition to a prioritization of its value for biodiversity conservation purposes (Löwenberg-Neto & Carvalho 2004).

Conclusions
In conclusion, the Piquiri River basin holds a large number of species, and some of these species are rare, endangered, migratory, endemic, and even unknown by science.This study and the various present and future threats to the fish biodiversity of the Piquiri River basin point to the potential disappearance of certain species before their actual distribution patterns are known or before they are known or formally described (e.g., Wallacean and Linnean shortfalls, Brown & Lomolino 1998).Therefore, this environment must be preserved so that the local and regional fish fauna biodiversity can be maintained, particularly since this area can be considered a high conservation area.Furthermore, ongoing studies on the systematics, biology, and ecology of fish species, as well as suitable strategies to mitigate potential ecological, sociological, and economic impacts on them, may help improve and accomplish the goals of conservationists.

Figure 1 .
Figure 1.Map of the Piquiri River basin showing its location in Brazil and in the state of Paraná.Yellow dots indicate the sampling sites within the basin that were georeferenced and cataloged in the ichthyologic collections.Each point may correspond to more than one sampling site.

Figure 2 .
Figure 2. Number of species per family of the ichthyofauna recorded for the Piquiri River basin, upper Paraná River, Brazil.Colors indicate the orders, namely from the most to the less specific.

Figure 3 .
Figure 3. Non-native fish species according to their introduction vectors into the Piquiri River basin, upper Paraná River, Brazil.

Figure 4 .
Figure 4. Map showing the locations of small power plants (SPPs, red dots) and power plants (PPs, yellow dots) predicted in Brazil, mainly within the Piquiri River basin (catchment area in blue).The number of localities within the Piquiri River basin represents 34 SPPs and 6 PPs.