Checklist and key for the identification of fish fauna of the Uberaba River, Upper Paraná River system, Brazil

Abstract The Uberaba River is an important right-bank tributary to the Grande River, in the Upper Paraná River system, Brazil, and the main water source for the public supply of the Uberaba city, Minas Gerais state. An inventory, an identification key, and photographs of the fish species of the Uberaba River are provided, based on samples made between 2012 and 2014 at 14 sampling sites in the river system. A total of 73 species was recorded from six orders, 20 families, and 49 genera. Characiformes and Siluriformes are the most speciose orders and Characidae and Loricariidae are the most commonly recorded families. Most species are autochthonous, nine are considered allochthonous, and two species are exotic. The Uberaba River has a diverse and heterogeneous ichthyofauna, typical of rheophilic environments, with endemic species and few non-native species.


Introduction
Approximately 34,797 species of fish have been formally described worldwide (Fricke et al. 2018), and recent estimates suggest that ca. 13,000 species are partially or exclusively freshwater (Nelson 2016). The Neotropical region has a unique and diverse freshwater fish fauna (Albert and Reis 2011), with 9,100 species exclusively distributed in South America (Reis et al. 2016), an impressive number when compared to the global estimates. Approximately 43% of the Neotropical fish diversity occurs in Brazil (Buckup et al. 2007), and the Amazon and La Plata river drainages bear the largest fish diversity in South America (Langeani et al. 2007).
tures (Candido et al. 2010;Cruz 2003;Valera et al. 2016). A dam located in the middle section of the Uberaba River, designed to capture and treat water for human consumption, significantly altered the natural characteristics and self-depuration capacity of the river (Sousa et al. 2016), even more aggravated by the high loads of raw sewage released into some river sections (Cruz 2003).
The fish fauna of the Uberaba River is only partially known, with only few sections sampled and no seasonal investigations (see SEMEA 2004;Souza et al. 2016). In this paper, we present an inventory of the fish fauna of the Uberaba River based on samples from several sections of the river system. In addition, an identification key and photographs of some species are presented.
The average annual precipitation in the region ranges between 1,300 mm and 1,700 mm, characterized by a rainy period of six to seven months (October to March) and the driest period (April to September) with less than 60 mm. The thermal regime is defined by an average annual temperature ranging from 20 to 24° Celsius, with a minimum of 18° C in colder months (June/July). These climatic factors characterize two major seasons in the region, one, cold and dry, between autumn and winter, and the other, hot and rainy, between spring and summer (Gomes et al. 1982).

Data
The collections were carried out between 2012 and 2014 in 14 sampling sites (Figures 1, 2; Table 1) along the entire system. Permission for collecting was provided by IEF / DPBIO / GPFF No.44551-1156. The samplings were performed both during the daytime and nighttime, using gill nets (2.5 to 120 mm mesh), dip nets (0.5 mm mesh), seines (1.5 mm mesh), and cast nets (2.5 to 100 mm mesh sizes). After sampling, the specimens were anesthetized in a solution containing 100 mg of eugenol by L -1 previously dissolved in 100% ethanol in proportion of 1:1 v/v, fixed in 10% formalin buffered with sodium phosphate (pH 7.0 and 0.2 Mol) for 24 to 72 hours, and then transferred to 70 o G.L. ethanol.
Specimens were identified using appropriate literature sources (e.g., Langeani et al. 2007;Langeani and Rêgo 2014;Castro et al. 2004;Ota et al. 2018) or by direct comparisons with specimens in museum collections. Vouchers are in the DZSJRP fish collection of the Departamento de Zoologia e Botânica do Instituto de Biociências, Letras  Table 1. e Ciências Exatas, Universidade Estadual Paulista 'Júlio de Mesquita Filho', São José do Rio Preto, SP, Brazil. Some groups are in need of a taxonomic revision, consequently the particle aff. (meaning "not the referred species, but very similar") is used. The morphometric measurements were taken on the left side of the body, using a digital caliper with an accuracy of 0.01 mm. Lower-level taxonomy and species names follow Fricke et al. (2018) and suprageneric taxonomic groups are those listed in Betancur et al. (2017), except for Cynolebiidae and Bryconidae that follow van der Laan (2016). Allochthonous species are those with their origins from any other hydrographic system in South America outside the Upper Paraná River as defined above. Exotic species are those with origins from any other continent.

Results
In total, 2,722 specimens were collected and assigned to 49 genera and 73 species. The identified taxa are listed in  (Linnaeus)). Six orders were recognized, of which Characiformes and Siluriformes were the most representative (90.3%), with eight families and 33 species for the former and five families and 27 species for the latter. Gymnotiformes (two families and three spp.), Cichliformes (one family and seven spp.), Cyprinodontiformes (two families and three spp.), and Synbranchiformes (one sp.) together represent 9.7% of the groups collected ( Figure 3). Characidae (48.8%) and Loricariidae (16.8%) correspond to the most abundant families ( Figure 4) and occur    Table 3. Species collected (X) in each site (S1 to S14) of the Uberaba River, Upper Paraná River system, Brazil.

Species
Sites S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 S13 S14 in the entire river system. The species richness suggested a longitudinal gradient, with more species in the lower reaches whereas in the upper reaches the richness does not exceed ten species ( Figure 5 and Table 3

Discussion
The diversity recorded in the Uberaba River (73) is slightly greater than in similar tributaries of the Grande River in São Paulo state, in which 64 species have been recorded in the tributaries of the Pardo, Turvo, and Sapucaí rivers (Castro et al. 2004). Our data increase the number of species previously recorded for the Uberaba River by 44, which corresponds to an increase of 150% of the species referred so far in the region (see more details in SEMEA 2004; Souza et al. 2016). However, these figures may reflect the differences in sampling methods used by us and the previous authors as well as a larger area investigated in this study. Estimates of species richness and diversity considerably depend on methods used as discussed by Oliveira et al. (2014). The number of species (73) recorded in the Uberaba River comprises ca. 19% of the total species number known in the Upper Paraná River system when compared to the data in Langeani et al. (2007). The ichthyofauna of the Uberaba River is composed mainly of autochthonous species, few allochthonous species and only two exotic species. The autochthonous origin of some of these species in the Upper Parana River still needs further research. For example, the scarcity of data on the origin or taxonomic status of some putative species such as Knodus aff. moenkhausii, Trichomycterus brasiliensis or Megalechis thoracata, does not allow to reasonably hypothesize on their origin. Some species recorded in the Uberaba River potentially correspond to new species and some considerations are provided. Astyanax fasciatus (Cuvier) is described for the São Francisco River basin and it is widely distributed in the Paraná-Paraguay drainage and coastal drainages of eastern of Brazil. However, based on the definitions by Eigenmann (1921) it is possible to infer the existence of a "A. fasciatus species complex" in the Paraná-Paraguay and other coastal drainages. Thus, the name A. fasciatus should be used strictly for the São Francisco River lineage (Melo and Buckup 2006). In the La Plata drainage, the Hoplias malabaricus species group is constantly corroborated by morphological, cytogenetic and molecular evidence, and a recognition and taxonomic delineating of new entities is currently in progress (Rosso et al. 2018). Additionally, the nominal   (Rosso et al. 2018). Similarly, some authors (see Buckup 1992) suggest that populations of Characidium zebra Eigenmann throughout South America represent more than one species. Characidium zebra was described in tributaries of the Branco River (Negro River system) in the Amazon. Recent evidence suggests that C. zebra popu-lations in the San Francisco and Paraná rivers correspond to the same species (Serrano et al. 2018) distinct from the C. zebra populations of the Amazon drainage.
Astyanax aff. paranae Eigenmann collected from the Uberaba River may represent a distinct species in the complex "Astyanax scabripinnis species complex" sensu Moreira-Filho and Bertollo (1991), a group with an underestimated diversity (Bertaco and Malabarba 2001) as it differs by a number of features (e.g., eye coloration and some measurements). Knodus moenkhausii (Eigenmann & Kennedy) was described from the Arroyo Trementina in the Paraguay River system. The specimens from the Upper Paraná River and identified so far as K. moenkhausii apparently represents an undescribed species (F. R. Carvalho pers. comm.).
The taxonomic boundaries of the Hypostomus species are unclear. Some species of the genus Hypostomus are highly variable morphologically and widely distributed. In addition, some important diagnostic characters, such as color pattern, cannot be seen at present in type specimens collected more than 100 years ago, making identification of the species difficult (Zawadzki et al. 2004). For example, Hypostomus hermanni Ihering is widely dis-  tributed within the Upper Paraná River system. A comparison of the specimens collected in the Uberaba River with specimens from other locations revealed a discrepancy in some meristic and color traits. The Uberaba specimens are especially different from specimens from the Piracicaba River, the type locality of H. hermanni. It has been also shown that different populations of Hypostomus paulinus (Ihering) are effectively reproductively isolated and characterized by a high degree of inbreeding (Zawadzki et al. 2004).
The occurrence of Metynnis lippincottianus may be a result of accidental introduction (Ota 2015). Among the allochthonous species, Poecilia reticulata was introduced to control mosquito larvae (Ota et al. 2018). Cichla piquiti was probably introduced for sport fishing (Langeani et al. 2007;Ota et al. 2018), and Gymnotus inaequilabiatus originally from the Lower Paraná River, Paraguay and Uruguay rivers (Maxime and Albert 2014), colonized the upper reaches of the Paraná River after the construction of the Itaipu hydroelectric dam in the 1980s. Ota et al. (2018) suggested that the occurrence of Hoplerythrinus unitaeniatus in the Upper Paraná River can be associated with its introduction as a live bait or after inundation of the Sete Quedas Falls after the construction of the Itaipu dam. Galeocharax gulo is widely distributed in almost all Upper Amazon River systems, also in the Orinoco, Oyapok, Araguaia-Tocantins, and Paraná rivers (Giovannetti et al. 2017). The occurrence of this species in the Upper Paraná system may be a result of natural dispersion. Coptodon rendalli and O. niloticus probably represent results of escapes from fish farms (Langeani et al. 2007;Ota et al. 2018) and the populations of both species are probably established in the region as they have been regularly registered since long ago. Finally, Souza et al. (2016) report the occurrence of Cyphocharax nagelii (Steindachner) and Steindachnerina brevipinna (Eigenmann & Eigenmann) in the system, but we could not confirm these data and refrained from including them in the species list. 1 Hypostomus aff. hermanni 2 Hypostomus fluviatilis 3 Rineloricaria latirostris 4 Proloricaria prolixa 5 Curculionichthys insperatus 6 Microlepdogaster dimorpha and 7 Loricaria lentiginosa (uncataloged). Photographs are of specimens presented in Table 2. Scale bar: 10 mm. New taxa have been described from the Uberaba River system over the past decade, e.g., Hasemania uberaba (Serra and Langeani 2015), Hyphessobrycon uaiso (Carvalho and Langeani 2013), and Microlepidogaster dimorpha (Martins and Langeani 2011). These newly described species are only known from their type localities or from a few localities corroborating several examples of endemism in the Upper Paraná River, previously indicated by some authors (e.g., Langeani et al. 2007). This clearly demonstrates the importance of inventories and consequent conservation measures. Two species registered in the Uberaba River are definitely threatened: Brycon nattereri Günther and Myloplus tiete (Eigenmann & Norris) are assigned to "Vulnerable" (VU) and " Endangered" (EN) respectively, on the IBAMA Red List of Endangered Species (ICMBio 2015). The main threats to the local fauna are related to changes in hydrological cycles and the loss of riparian vegetation, as well as overexploitation of natural stocks (Lima et al. 2008;Lima et al. 2015). In addition, the presence of migratory rheophilic species such as Prochilodus lineatus (Valenciennes), Leporinus friderici (Bloch), B. nattereri, and M. tiete, is because these species use local resources, at least partially, to complete their life cycle, as suggested by Carolsfeld et al. (2003). Considering all the factors discussed above, the Uberaba River contains a diverse and heterogeneous fish fauna, with two endemic species, H. uberaba and an undescribed crenuchid (a description is in the process by Ribeiro et al.) and a low number of allochthonous and exotic species. The Uberaba River has undergone several anthropogenic actions over the last decades, such as the increase of the area destined to grazing, resulting in only 17.7% of native vegetation remains (Valle-Junior et al. 2010) and the reduction of the lotic environments due to damming. The impact of human-induced environmental change is dramatic on the structure and composition of the local fauna. Development of management plans on conservation areas such as the implementation of "Area de Proteção Ambiental Rio Uberaba -APA-Rio Uberaba" project (SEMEA 2004) is necessary to mitigate the effects and help the sustainable use of local natural resources.