Freshwater fishes of the Bahia State, Northeastern Brazil

: This work was carried out from the assessment of the conservation status of the freshwater ichthyofauna from Bahia State. The inventory data and species distribution were obtained from the specialized scientific literature and representative ichthyological collections. A total of 281 native species was recorded in Bahia State, distributed in the Northeastern Mata Atlantica (NMA) and São Francisco (SFR) freshwater ecoregions. There was a larger number of species in the NMA (187 spp.), composed by several coastal basins, than in the SFR (134 spp.), composed by São Francisco river basin. Among the 30 families recorded, Characidae and Rivulidae were the most representative, with 53 and 48 species, respectively. The conservation status of 214 species was assessed and 33 of them (15%) were included in the IUCN threat categories. Of these, 11 species were classified as vulnerable (VU), 12 as endangered (EN), and 10 as critically endangered (CR). Most threatened species (n = 14) belongs to the family Rivulidae. The larger number of threatened species in the NMA: (n = 23) is mainly related to the high endemism of restricted-range species associated with the human occupation impacts along the coastal regions. In the SFR, most of threatened species are annual killifishes, which are locally disappearing due to increasing degradation of their temporary habitats.


Introduction
The Neotropical region harbors the most diverse freshwater fish fauna in the world, with more than 5,700 described species, although the final number may exceed 8,000 species , Reis 2013, Bertaco et al. 2016, Reis et al. 2016. Putting this number into perspective, Neotropical freshwater fishes account for about one in five of the world's fish species, or approximately 10% of all vertebrate species ). According to Ribeiro (2006), the reasons for such a marked diversity are likely to be both historical and ecological, a result of millions of years of evolution from the breakup of Gondwana to the present day.
It is often claimed that freshwater ecosystems are the most endangered in the world (Sala et al. 2000, Dudgeon et al. 2006, Nogueira et al. 2010. As in other freshwater regions, South American fishes are threatened by overexploitation, flow modification, habitat destruction, species invasion, pollution, eutrophication, and siltation (Lévêque et al. 2008). Several fish conservation initiatives are underway in South America, including an ambitious program that assesses the conservation status of all Brazilian fish species (Reis 2013). This program resulted in the Brazilian list of threatened fishes and aquatic invertebrates, known as the Brazilian Red List (MMA 2014). Along with this national task, some parallel regional projects of conservation assessment of continental fishes have also been conducted (e.g., Rosa et al. 2003, Alves & Leal 2010, Reis et al. 2016. In 2013, one of these regional initiatives was carried out in Bahia State, northeastern Brazil, and the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) in collaboration with the Secretaria do Meio Ambiente do Estado da Bahia (SEMA), and several ichthyologists completed a comprehensive conservation assessment of the freshwater ichthyofauna in the state. It is important to highlight that the results of this regional workshop became the basis for the publishing of the list of threatened freshwater fish species reported from Bahia state (SEMA 2017). Bahia, one of the 27 federative units of Brazil, is the fifth largest state by area, with more than 564.000 km 2 and 417 municipalities (IBGE 2019).
This state partially encompasses two freshwater ecoregions as proposed by Abell et al. (2008), the São Francisco (SFR, ecoregion 327) and Northeastern Mata Atlantica (NMA, ecoregion 328) ecoregions ( Figure 1). According to these authors, a freshwater ecoregion is defined as a large area encompassing one or more freshwater systems with a distinct assemblage of natural freshwater communities and species. Although political geographic boundaries are useless for biological organisms, national or regional species lists are important for monitoring and conservation planning efforts (Silveira et al. 2010, Hortal et al. 2015. In this sense, any conservation initiative starts from the identification of the species that will be protect by such initiative. However, that apparently simple and basic information is absent or incomplete for diverse regions of Brazil. For example, the procedure of compilation of fish species that occur in rivers that drain Bahia state to evaluation of conservation status took several weeks of hard work previously to 2013 workshop, and involved the participation of several experts.
Before that effort, the knowledge about the species that occur in Bahia rivers was dispersed in some studies which focused on description of new species (e.g., Garavello 1977, Malabarba et al. 2004, Costa 2007, Zanata & Serra 2010, or representing the fish species inventory of some basins or part of them (e.g., Sato & Godinho 1999, Rosa et al. 2003, Santos 2005, Sarmento-Soares et al. 2007, Barbosa & Soares 2009, Burger et al., 2011.
To make available the results of the list of threatened freshwater fishes of Bahia State elaborated during the aforementioned 2013 workshop, we report here the first checklist of freshwater fish species of the Bahia state. This list includes species from the SFR and NMA ecoregions described at present, as well the conservation status for those evaluate in 2013 Workshop. Without the pretense of being a definitive list, it is a starting point that should be broadened and updated in order to compile the scattered information available.

Study area
Freshwater fish species from stretches and tributaries in the SFR and NMA ecoregions of Bahia State ( Figure 1) were analyzed. The SFR ecoregion is equivalent to the São Francisco basin, the third largest Neotropical hydrographic basin which is enclosed in an area of more than 630,000 km 2 (Sato & Godinho 1999, Kohler 2003, Langeani et al. 2009). The São Francisco is the longest river running entirely in Brazil, corresponding to more than 7.5% of the Brazilian territory , Pompeu & Godinho 2006. With more than 2,500 km of extension , Langeani et al. 2009), the São Francisco river and its tributaries drain three biomes (Caatinga, Cerrado and, peripherally, Atlantic Forest) crossing six states (from its source to mouth: Minas Gerais, Goiás, Bahia, Pernambuco, Alagoas, and Sergipe) plus the Federal District (Paiva 1982, Langeani et al. 2009). From its headwaters in the Serra da Canastra, located in the central-western part of Minas Gerais State (at about 1,200-1,500 m above sea level), to its mouth, between Alagoas and Sergipe, the river drains more than 500 municipalities (Kohler 2003, Sato & Godinho, 2003. Although not entirely located in Bahia State, the São Francisco is the largest and one of the most important rivers of the state. The NMA, in turn, comprises all coastal drainages in eastern Brazil, from the Sergipe river in the north to the Itabapoana river in the south (Camelier & Zanata 2014a). To the west, the NMA ecoregion is limited by the watershed border with the São Francisco river basin, along the Serra do Espinhaço up to the north, and by the Paraíba do Sul river basin in the south (Hales & Petry 2013). This ecoregion includes more than 25 isolated basins (Camelier & Zanata 2014a), draining the eastern slopes of the Brazilian crystalline shield directly into the Atlantic Ocean. From north to south, the main drainages of the NMA in Bahia State are: Vaza-Barris, Real, Itapicuru, Inhambupe, Pojuca, Paraguaçu, Jequiriçá, Contas, Cachoeira, Almada, Una, Pardo, Jequitinhonha, Buranhém, Frades, Jucuruçu, Itanhém, Peruípe, andMucuri (Langeani et al. 2009, Camelier &Zanata 2014a).
These drainages, along with several other smaller isolated basins of the NMA, are separated by the scarped, mountainous landscapes of the eastern margin of the Brazilian shield (Ribeiro 2006). The NMA is mainly inserted in the Atlantic Forest biome, although the northern drainages from the upper Contas to the Vaza-Barris river basins are partially under the influence of the semiarid Caatinga (Rosa et al. 2003, Camelier & Zanata 2014a.

Species inventory and list compilation
The species inventory and information about their distributions were obtained by consulting different sources in the reliable specialized scientific literature (i.e. original descriptions, taxonomic reviews, phylogenetic studies, and species catalogues) and representative ichthyological collections such as Instituto Nacional da Mata Atlântica (formerly Museu de Biologia Professor Mello Leitão-MBML), Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul (MCP), Museu Nacional do Rio de Janeiro (MNRJ), Museu de Zoologia da Universidade de São Paulo (MZUSP), Museu de História Natural da Bahia (UFBA), and Universidade Federal do Rio Grande do Norte (UFRN). Data were obtained from these fish collections or by searches in the national system of information on ichthyological collections (e.g., SIBIP/NEODAT III 2019, CRIA 2019) and, eventually, checked by consulting specialists. Taxonomic classification and species naming were determined mainly according to Fricke et al. (2020); for the species of Characidae, according to Mirande (2010).
To elaborate the list supporting this study, only freshwater fish species formally described until December 2019 were considered. Despite the fact that freshwater species were defined as those known to spend a significant part of their life cycle in low salinity (<0.5 ppt) continental waters (Myers 1949;Berra 2001), in the present study only primary freshwater fishes were considered.
The International Union for Conservation of Nature (IUCN) criteria were used to asses the conservation status of the species (IUCN 2012). The conservation status of species already evaluated according to these criteria was updated to the state of Bahia, which represented the regional assessment. Since the regional workshop for the evaluation of endangered freshwater fish species in Bahia occurred in November 2013, species described after this period did not have their conservation status assessed. The only exception is Rhamdiopsis sp., an undescribed troglobitic species whose description process is well advanced (M. E. Bichuette pers. comm.). Subterranean ecosystems and their biota pose special problems for conservation due to their intrinsic fragility and the distinctive features of subterranean communities, such as a high degree of endemism and morphological, ecological and behavioral specialization (Trajano & Bichuette 2010). Therefore, the assessment of the conservation status of Rhamdiopsis sp. has become necessary.
Species whose known distribution is restricted to the stretches of the basins draining Bahia State were classified as endemic. It should be noted that endemic species from the ecoregions analyzed (SFR or NMA), which are known to occur in other states (e.g., Sergipe, Minas Gerais, Espírito Santo), were not classified as endemic. Non-native species recorded in basins of the Bahia State were included in the list, but their conservation status was not evaluated.

Ichthyofauna composition
A total of 281 native freshwater fish species was recorded along the drainages of Bahia State (Table 1), accounting for about 9% of all species (3,116) known to occur in Brazil (ICMBio 2014). Of the taxa listed in this study, one subfamily (Copionodontinae), nine genera (Copionodon, Glaphyropoma, Hirtella, Kalyptodoras, Mucurilebias, Myxiops, Ophthalmolebias, Prorivulus, and Pseudotatia), and 126 species are only known from river basins draining Bahia State. Most of the native species are from the NMA, with 187 species occurring in Bahia. In stretches of the SFR draining the state, 134 native species were listed (Table 1). Table 1. List of freshwater fish species of Bahia State and their conservation status according to state (SEMA 2017) and national assessments (MMA 2014), IUCN criteria and ecoregion (NMA, Northeastern Mata Atlantica; SFR, São Francisco), as well as their respective indication of origin (X, native species but not endemic to the Bahia part of the ecoregion; END, endemic to the Bahia part of the ecoregion; NNA, non-native species). Only 40 (14%) native species are shared between the two ecoregions. Eleven non-native species were listed in Bahia, which accounted for less than 5% of all species analyzed. Among the 30 families recorded (excluding those related only to non-native species), the most representative were Characidae and Rivulidae, with 53 and 48 species, respectively, followed by Loricariidae with 28 species (Figure 2). Many species were described in the last 20 years, 75 from the NMA and 41 from the SFR, corresponding to 27% and 15% of all species listed in this study, respectively ( Table 1).

ORDER/Family/Species
Most of the threatened species are in the NMA (23 species, 69.7%), while 10 (30.3%) endangered species are found in the SFR (Figure 3). Most of these belong to the family Rivulidae, with 14 species (42.4 % of threatened species), seven in each ecoregion. In addition, several small fish species of the Characidae, Heptapteridae, and Trichomycteridae families were also representative in the list of endangered species. These fishes are typical of first-and second-order streams, which may suffer more intensely from the effects of human activities (Oliveira & Bennemann 2005). Among tricomicterids and heptaperids, three troglobitic species (Glaphyropoma spinosum, Rhamdiopsis krugi, and Rhamdiopsis sp.) stand out among all others because of their low population density and restricted distribution in some caverns (Bockmann & Castro 2010, Bichuette et al. 2008, which are not protected in any conservation unit. Taken together, these factors can chronically devastate these populations and compromise species survival.

Species composition
In this study, 281 native freshwater fish species were recorded in Bahia State, distributed in coastal drainages of the NMA ecoregion and the São Francisco river basin draining the state. The composition of the Bahia State species partially agrees with the overall pattern of the Brazilian fish fauna, in which most species belong to Characidae, followed by Loricariidae (Bizerril 1994, Gonçalves & Braga 2012, Camelier & Zanata 2014a, Ferreira et al. 2014. Curiously, Bahia is one of the Brazilian states with the largest records of Rivulidae in its basins (see Frick & Eschmeyer 2020). Among the remaining families occurring in the state, more than half are represented by five or fewer species.
The number of Rivulidae species is higher in the SFR ecoregion, mainly due to the presence of several annual fish species of the genera Hypsolebias and Cynolebias that inhabit temporary pools in the tributaries at the right margin of the middle São Francisco river basin (Costa 2014. In the drainages of the NMA ecoregion, Rivulidae is mainly represented by the annual fish species of the genus Ophthalmolebias, most of them endemic to Bahia, presenting a narrow distribution, usually restricted to a single basin (Costa & Lima 2010). In this ecoregion, Rivulidae and Loricariidae have almost the same number of species, differing from the general pattern found in the other Brazilian coastal drainages cited above.
The river basins included in the NMA and SFR freshwater ecoregions which draining the state of Bahia exhibit a distinct composition, with only 40 native species shared between them. Most species from the NMA are characterized by a small size, possibly related to the large number of small streams of this ecoregion. According to several authors (e.g., Weitzman & Vari 1988, Castro 1999, Casatti et al. 2001, Abilhoa et al. 2011, the ichthyofauna of these freshwater ecosystems is mainly composed of small-sized species. In the São Francisco river basin, in addition to small fish species, larger species, most of them important for artisanal fisheries, are found, including migratory species such as Conorhynchos conirostris, Prochilodus argenteus, Pseudoplatystoma corruscans, and Salminus franciscanus (Sato & Godinho 2003, Godinho & Kynard 2006.

Assessment of conservation status
In this study, 214 freshwater fish species were evaluated. Most of them were classified as 'Least Concern' (LC), 45 as 'Data Deficient' (DD), and eight as 'Near Threatened' (NT), which are not considered threatened categories according to the IUCN criteria (IUCN 2012) (Table 1, Figure 3). Thirty-three freshwater fish species (26 of them endemic to Bahia) were included in the threatened categories: 11 as 'Vulnerable' (VU), 12 as 'Endangered' (EN), and 10 as 'Critically Endangered' (CR) (Table 1, Figure 3). The Bahia State Red list has been already published by the Secretaria do Meio Ambiente do Estado da Bahia (SEMA 2017), although it contains only the threatened species and their conservation status. However, the number of species gathered in the present study is likely underestimated due to a range of factors. Some undescribed species were not counted, the only exception being Rhamdiopsis sp. from the Chapada Diamantina region (SFR). Some nominal widespread species may represent species complexes that need revisionary studies to solve the confusing taxonomy and the definition of the new species described (e.g., Astyanax bimaculatus, A. fasciatus, Hoplias malabaricus, Geophagus brasiliensis, Rhamdia quelen). In addition, some sub-basins were not sampled (e.g., most tributaries of the middle São Francisco in southwestern Bahia and headwaters of various river basins of the NMA).
More than 20 years ago, Menezes (1996a, b) cited the lack of knowledge about the fish fauna of drainages in Brazil's Northeastern region. Although a series of studies increasing that knowledge were conducted at that time, the results were far from satisfactory and Northeast Brazil is still pointed out as a region of scarce available information about freshwater fish records in a global database compilation (Tedesco et al. 2017). Current evidence of the lack of knowledge about the ichthyofauna in this region is the large number of taxa considered "sp." or accompanied by the terms "cf." or "aff." in taxonomic inventories (e.g., Sarmento-Soares et al. 2009a, Cetra et al. 2010, Burger et al. 2011, Ramos et al. 2014. Although numerous freshwater fish species from the Bahia river basins have been described in the last two decades (e.g., Bertaco & Lucena 2006, Ribeiro & Lucena 2006, Lima & Britski 2007, Benine et al. 2007, Zanata & Camelier 2008, 2010, 2015, Bichuette et al. 2008, Sarmento-Soares et al. 2009b, Sarmento-Soares et al. 2011, Ferreira et al. 2014, Vari et al. 2010, Bichuette & Rizzato 2012, Oliveira et al. 2013, Sarmento-Soares & Martins-Pinheiro 2013, Camelier & Zanata 2014b, 2017, 2018, Mattos et al. 2015, Peixoto & Wosiacki 2016, Zanata & Pitanga 2016, Zawadzki et al., 2017Barreto et al. 2018, Mattos & Costa, 2018, Burger et al. 2019, Lucena & Lucena 2019, ichthyological explorations continue to reveal unknown species, especially in small tributaries and in upper drainage areas. The increase in the number of species recently described from the São Francisco river basin has already been documented in the literature (see Alves et al. 2011 andBarbosa et al. 2017).

Conservation concerns
Overall, the results of the state and national conservation status assessments were remarkably similar, with divergences only for two species: Acentronichthys leptos and Hypomasticus mormyrops. In Bahia State, both species were included in threatened categories (VU and EN, respectively) since they occur at few impacted localities with continuing decline in the habitat quality. However, these species were classified as LC in the national assessment (MMA 2014) since their total distribution was considered wider, including river basins outside Bahia where these species are more abundant and are not threatened (e.g., Paraíba do Sul, Doce, plus small drainages in the states of São Paulo and Rio de Janeiro).
The conservation status of some species which occur in Bahia State changed in the last years. Some examples are the catfish 'pacamã' Lophiosilurus alexandri and the killifish Hypsolebias adornatus, both endemic to the SFR ecoregion, which were classified before as LC (MMA 2004) are now VU in both lists (SEMA 2017, MMA 2014. Several subpopulations of L. alexandri were probably locally extinct, reducing their population size by at least 30% (ICMBio 2018). On the other hand, L. alexandri was introduced in the Doce river, where became an important resource for artisanal fishing (Alves et al. 2007).
Additionally, this species is cultivated in tanks as a commercial species for food near Colatina, Espírito Santo State (L. M. Sarmento-Soares pers. obs.). Nowadays, H. adornatus is also VU because one of its few known localities were destroyed, leading to local extinction. Moreover, this species is much appreciated as an aquarium fish, posing an additional and severe threat to this species. The category of three other annual killifishes, Hypsolebias fulminantis, H. ghisolfii, and Ophthalmolebias perpendicularis changed from VU (MMA 2004) to CR (MMA 2014). The first two, endemic to Bahia (SFR), are sympatric and were commonly found in temporary floodplain pools of Rio das Rãs, a tributary of the São Francisco basin (Costa 2007). However, their distribution is now restricted to a few localities as a consequence of the agricultural development and potteries established in the region. The case of O. perpendicularis is even more concerning since the species is currently classified as CR, the highest extinction risk category. In fact, this annual rivulid species may already be extinct since it was only known from the type locality in the Jequitinhonha river basin (NMA ecoregion), which was destroyed, and there has been no record of this species since 2000 (ICMBio 2018).
The large number of threatened freshwater fish species in the NMA ecoregion (23) is possibly due to the remarkable endemism of its ichthyofauna (Bizerril 1994, Ribeiro 2006, Camelier & Zanata 2014a) associated with the significant human occupation and alteration of the coastal region (Langeani et al. 2009). In the SFR ecoregion, most threatened species are annual killifishes, whose populations are disappearing due to the strong degradation and grounding of their habitats (see Costa 2002, ICMBio 2018. Eight species were classified as NT and may soon move to the list of endangered species if no conservation measures are adopted. In addition to the increasing human exploitation, the relatively small number of conservation units and protected areas in Bahia may be insufficient for the preservation of its fish fauna. Only 11.6% of the state area is protected as Conservation Units and less than 20% of these are in the higher protective level (Allen 2015). Additionally, we point out that most of these protect areas act as biodiversity islands, since they are surrounded by diverse monocultures, pastures and urban centers. One way to reduce these negative effect is the adoption of public polices that favor more environmentally appropriate agricultural practices in the buffer zones of Conservation Units, such as agroforestry systems (Sarmento-Soares & Martins-Pinheiro, 2017;Ewert et al. 2013).
The National Action Plans (Planos de Ação Nacional, PANs, in Portuguese) coordinated by the ICMBio, which have as main mission conserving Brazilian biodiversity, are public policies identifying and guiding priority actions to combat threats that endanger populations of species or environments (Polaz 2014). Therefore, the success of the PAN depends of both taxonomic information and data of the assessment of the conservation status of the species, such as provided in the present study. There are three PAN designed for freshwater fishes whose actions directly affect the conservation of the ichthyofauna in the state of Bahia: (1) Action Plan for the threatened species from the São Francisco watershed (Ordinance ICMBio nº 34, 27 May 2015), aiming mainly to improve the knowledge about threatened species and mitigate human impacting activities, to promote the conservation and recovery of aquatic fauna in the São Francisco river in five years (2015-2020); (2) Action Plan for the threatened fish species from the Atlantic Forest rivers (Ordinance ICMBio nº 370, 1 August 2019), objecting to increase the conservation status and popularization of fishes, rivers, and streams of the Atlantic Forest in five years (2019-2024); and (3) Action Plan for the threatened species of Rivulidae family, with the general objective of establishing mechanisms to protect the rivulids and canceling the loss of habitat of the focal species, in five years (2013)(2014)(2015)(2016)(2017)(2018); the second cycle of this PAN (2020-2025) was approved and it is in preparation, awaiting publication of the new ordinance.
Finally, it is expected that these joint actions (e.g., taxonomic studies, lists of species, conservation status of species, public policies) will contribute not only to the increase of the knowledge of the fish fauna but also to the conservation of these species and the environments inhabited by them.