Ichthyofauna of Mundaú river basin, Ceará State, Northeastern Brazil

: Mundaú river basin is located at Center-North Ceará State and occupies a total area of 2,227 km 2 , including Estuário do Rio Mundaú Environmental Protection Area. This study aimed to catalog the fishes of this basin. Collections were performed with active and passive gear in 35 sampling sites, between 2012 and 2014, in several habitats (main channels, streams, floodplains, permanent and temporary pools, ponds, and dams). A total of 2,545 specimens were collected, belonging to 55 species distributed in 10 orders, 31 families, and 50 genera; 30 of these are strictly freshwater species, and 25 estuarine-marine species. Three species ( Hemigrammus guyanensis Gery, 1995, H. rodwayi Durbin, 1909 and Poecilia sarrafae Bragança & Costa, 2011) represent new records for the Mid-Northeastern Caatinga ecoregion. Besides, two cynolebiid species, Hypsolebias sp. and Anablepsoides cearensis (Costa & Vono, 2009), were found and the latter, currently classified as critically endangered, had its occurrence area widened.

MNCE is largely inserted in the Brazilian semiarid, an area of Caatinga's phytophysionomy where rivers are mostly intermittent resulting in a simple hydrographical network (Rosa et al. 2003), except for headwaters and coastal areas in Alagoas, Pernambuco, Paraíba, and Rio Grande do Norte States, which are greatly nested within the Atlantic Forest (Rosa & Groth 2004, Paiva et al. 2014).Therefore, these semiarid river systems are constantly being modified through their damming as an attempt to assure the inland population a hydric demand during long drought periods.
Except Jaguaribe river basin and a small portion of Parnaíba river basin, Ceará hydrographic network is composed by small-sized coastal basins.Some of these basins may probably have an important role to the conservation of Caatinga's fishes, although they have been considered insufficiently known (MMA 2007).Among these, there is Mundaú river basin, located in Center-North Ceará State, whose freshwater ichthyofauna is virtually unknown.Soares-Filho et al. (2010) cataloged the estuarine porcion of this basin and reported 53 estuarine and marine fish species.The Estuário do Rio Mundaú Environmental Protection Area (EPA) is located at the lower extent of the basin, covering 1,596.37 hectares of Ceará West coast, and it is considered a priority area for fish conservation (SEMACE 2014).Because of the basin's importance for the Caatinga fish fauna knowledge, this study aimed to survey the fishes of Mundaú river basin.

Study area
Mundaú river basin (Figure 1) covers, approximately, an area of 2,227 km 2 (COGERH 2014), draining regional residual massifs, backland depressions, and seaside plains (IPECE 2012).The two main tributaries of Mundaú river basin, Cruxati in the west and Mundaú in the east, emerge from Uruburetama Massif at elevations up to 970 m, and are intermittent.
Along their courses, these rivers are fed by various first order waterbodies, like Sororô, Tabocas, Laginhas, and Torrados streams.Mundaú river main course runs 97.6 km north to south, and disembogues in the Atlantic Ocean, while Cruxati river runs 77.5 km from headwaters to Mundaú river's confluence (COGERH 2014).
The local climate is semiarid with mean annual precipitation of 1,110.6 mm, and 1,914.7 mm evaporation; mean annual temperatures between 26ºC and 28ºC, and highest precipitations occurring from January to June (FUNCEME 2015).

Sampling design
Acquisition of specimens was performed in 35 locations along the entire Mundaú river basin.For better coverage, collections were made at Cruxati and Mundaú rivers' main channels, as well as in streams, ponds, dams, and bogs (Table 1).Sampling took place during dry and wet seasons, between 2012 and 2014, covering localities from Mundaú river headwaters, 900 m higher than the estuary.Due to river intermittence, dry season samples were taken only in remaining pools at the main watercourse, while wet season sampling covered locations in the main flow and marginal environments.
The nomenclature followed the recommendation by Eschmeyer (2015), and species habitat definition followed Fishbase (2014).

Results
A total of 2,545 fish specimens were collected, belonging to 55 species, 50 genera, 31 families, and 10 orders (Table 2).Of those species, 30 (54.5%) are strictly freshwater, seven (12.7%) estuarine, and 14 (25.4%)marine ( Among freshwater fishes, Characiformes was the most representative order in number of species (53.3%), while among marine and estuarine fishes it was Perciformes (80%).The orders Siluriformes and Cyprinodontiformes represent 10.9% and 9.1% of total species, with six and five species, Table 2. List of fish species and information on physiology, habitat, abundance and voucher of the Mundaú river basin.Abbreviations: (E) Estuarine, (F) freshwater; (M) marine; (NR) new record for the MNCE; (CR) Critically endangered; (I)   respectively.The most diverse families were Characidae, with 10 species, representing 18.2% of total, followed by Cichlidae and Poeciliidae with three species each (5.5%) (Table 2).Of the five Cyprinodontiformes species listed, two belong to the family Cynolebiidae (Anablepsoides cearensis and Hypsolebias sp.).The non-annual killifish A. cearensis (Figure 2a and 2b) was the only threatened species in Mundaú river basin, listed as Critically Endangered (CR) in the Brazilian threatened fauna Red List (ICMBio 2014, Brasil 2014).This species was collected in two oxbow lakes (Figure 2d and 2e) and in a shallow perennial stream, located in an Arbustive Caatinga forest fragment (Figure 2 c), with similar features to the described type locality of the species (Costa & Vono 2009).

Discussion
The predominance of the orders Characiformes and Siluriformes in the freshwater ichthyofauna of Mundaú river basin follows the pattern found among freshwater fishes in Brazilian Northeast (Ramos et al. 2005, Nascimento et al. 2014, Ramos et al. 2014, Silva et al. 2014), in Brazil (Buckup et al. 2007), and in Neotropical region (Reis et al. 2003, Lévêque et al. 2008).However, when estuarine and marine species are also considered, the order Perciformes is the most abundant, corroborating with other MNCE species listings (Soares-Filho et al. 2010, Paiva et al. 2014).
Astynax aff.bimaculatus was recorded in 54% of sampling sites, being the most abundant species.It belongs to the Astyanax bimaculatus group composed by 22 valid species distributed along almost all drainages in South America, representing one of the most abundant morphotypes (Lucena & Soares 2016).Together with Poecilia vivipara, Serrapinus heterodon, S. piaba, and Steindachnerina notonota, they represented the most common species and could exhibit small sized body, generalist ecophysiological habits, and partitioned or all year reproduction.These features, likewise others related to anthropic disturbances, such hypoxia and eutrophic habitats, are usually present in the most frequent and abundant species in freshwater community studies in MNCE (Sánchez-Botero et al. 2014, Silva et al. 2014).However, most of the species were restricted to a few habitats, reflecting narrow ecological conditions for their occurrence.The estuarine-marine fishes were mainly juveniles of species previously recorded in Mundaú Estuary, including some important ones for artisanal fisheries (Soares-Filho et al. 2010).Of the 25 non-freshwater species registered in the basin in our study, six are not mentioned in Soares-Filho et al. (2010): Citharichthys sp.Hemicaranx sp., Genyatremus luteus, Haemulopsis corvinaeformis, Larimus breviceps, and Sciades herzbergii.The same authors also observed the goliath grouper Epinephelus itajara (Lichtenstein, 1822) at Mundaú Estuary, a critically endangered marine species (Brasil 2014).
The occurrence of cynolebiids at temporary pools in the main channel and floodplains in the medium and lower ranges of Mundaú river basin may reinforce the biological importance of this drainage as a priority area for Caatinga conservation, as suggested by Brasil (2007) and in the recent reevaluation (Brasil 2016).Anablepsoides cearensis was only known from the type locality, a shallow stream in São Gonçalo do Amarante, Ceará (Costa & Vono 2009).Thus, its distribution record was increased about 77 km west, to the lower portion of Mundaú river, in Itapipoca.Morphological differences between Hypsolebias sp. and its Caatinga congeners (Costa 2007) suggests that it may be a new species.The only species of the genus described for MNCE are: H. antenori (Tulipano, 1973), which occurs at the coastal basins east of Mundaú drainage, between Messejana municipality, in Ceará State, and Areia Branca municipality, in Rio Grande do Norte State (Costa 2007); H. longignatus Costa 2008 from Pacoti river basin, in Aquiraz municipality (Costa 2008), and H. martinsi from Icaraizinho river, in Amontada municipality (Britzke et al. 2016), Additional morphological and molecular studies should be done in order to determine its specific status.This record emphasizes the classification of MNCE as a freshwater ecoregion with a high percentage of endemic species (Albert et al. 2011).Among the species labeled as new occurrences for MNCE, P. sarrafae was considered as endemic to Parnaíba river basin (Bragança & Costa 2011, Ramos et al. 2014), and this is the first record outside Maranhão-Piauí ecoregion.Hemigrammus guyanensis was putatively endemic to Guiana Shield, while H. rodwayi and Nannostomus beckfordi are considered as native from Amazon-Orinoco-Guianas Core (Albert et al. 2011) occurring in the Guiana, Suriname, French Guiana, and Northern Brazil (Reis et al. 2003, Buckup et al. 2007).H. rodwayi is also found in several MNCE coastal rivers: Mamanguape (UFPB 5685) and Abiaí (UFPB 9384) river basins, in Paraíba State, and Doce (UFRN 2483) and Jundiaí drainages (UFRN 2595), in Rio Grande do Norte State (unpublished data).The occurrence of those Amazonian species in Brazilian Northeast might be an indicative of a past connection between the Atlantic and Amazon forests in more humid periods (Wang et al. 2004).Menezes et al. (2007) reported that Nannostomus beckfordi, recorded from Bahia and Alagoas states, was introduced in the Brazilian Northeast due to aquarism.However, the presence of this species in Mundaú river basin in Ceará State is the northern and westernmost record in MNCE, and it could be a relictual distribution and another evidence of the preterit connection between the Neotropical forested biomes.Currently, N. beckfordi is considered a poorly defined species complex, which needs a taxonomic review (Benzaquem et al. 2015).The native or introduced status of this taxon needs to be addressed once endemic undescribed species could be unprotected.
The introduction of Poecilia reticulata in Brazilian Northeast rivers can also be a result of aquarism.However, this species has been introduced in several countries for mosquito larvae control, such as Aedes aegypti (Lindholm et al. 2005).Meanwhile, larger species, such as tilapia Oreochromis niloticus, were introduced to fish farming in the reservoirs of the northeastern Brazil by the Departamento Nacional de Obras Contra Seca (DNOCS) in the 1970 (Paiva & Mesquita 2013).In addition to competing for resources with native species, tilapias are quite resistant, easily surviving in disturbed environments (Leão et al. 2011).
A total of 55 species were found in Mundaú river basin, of which only two are introduced.The high species richness, together with new records for MNCE, which includes two cynolebiids, one of them a critically endangered species (Anablepsoides cearensis), highlights the importance of preserving this basin, mainly the lowland stretches.However, some anthropic impacts were observed along Mundaú river basin waterbodies, mainly associated to riparian forest removal for agriculture and cattle raising in many stretches of the rivers and streams sampled; river sand extraction; damming; irregular occupation of river margins by human habitation; and domestic sewage discharge.The ichthyological survey of Mundaú river basin contributes to the knowledge of Caatinga fish fauna, and corroborates its importance as a priority area for the conservation of aquatic biota of this semiarid region.

Figure 1 .
Figure 1.Mundaú river basin location in Ceará State, northeastern Brazil, evidencing the sampling sites.Hot colors represent higher altitudes.

Figure 2 .
Figure 2. Anablepsoides cearensis, a critically endangered freshwater fish species collected in permanent pools in the lower portion of the Mundaú river basin.A = male, B = female, C, D, E = sampling sites.

Table 2 .
Continued... from small basins in Ceará State.Geographically, our record of Hypsolebias sp. is between the type locality of H. longignatus and H. martinsi, being the former eastern from Mundaú river basin and distant 140 km, while the latter is on the northwest and closer, about 25 km in the adjacent Aracatiaçu river basin.However, Hypsolebias sp.seems to belong to the H. antenori group, and thus very distinct from H. longignatus, which belongs to the H. flammeus group.The species collected in Mundaú river basin differs from H. martinsi by the presence of vertical bars in body, and from H. antenori by the virtual absence of round blotches on caudal peduncle. http://dx.doi.org/10.1590/1676-0611-BN-2016-0174both