Ichthyofauna of Mundaú river basin, Ceará State, Northeastern Brazil

Ictiofauna da bacia do rio Mundaú, Estado do Ceará, Nordeste do Brasil

Abstract

Mundaú river basin is located at Center-North Ceará State and occupies a total area of 2,227 km², 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.

Keywords:
intermittent river; semiarid; Mid-Northeastern ecoregion; freshwater neotropical fishes

Resumo

A bacia do Rio Mundaú está situada no centro-norte do Estado do Ceará, e drena uma área de 2.227 km² de Caatinga, incluindo a Área de Proteção Ambiental do Estuário do Rio Mundaú. Este estudo teve como objetivo realizar um inventário dos peixes desta bacia. As coletas foram realizadas com petrechos ativos e passivos, em 35 pontos amostrais entre 2012 e 2014 em diversos habitats (canal principal, córregos, alagados, poças permanentes e temporárias, lagoas e açudes) ao longo de toda a bacia. Um total de 2.545 indivíduos foram coletados, pertencentes a 55 espécies distribuídas em 10 ordens, 31 famílias e 50 gêneros; destas, 30 são estritamente de água doce e 25 estuarino-marinhas. Três espécies (Hemigrammus guyanensis Gery,1995, H. rodwayi Durbin, 1909 e Poecilia sarrafae Bragança & Costa, 2011) constituem novas ocorrências para a ecorregião do Nordeste Médio-Oriental. Além disso, foram registradas duas espécies de cinolebídeos, Hypsolebias sp. e Anablepsoides cearensis (Costa & Vono, 2009), a última classificada como criticamente ameaçada de extinção, teve sua área de ocorrência ampliada.

Palavras-chave:
rios intermitentes; semiárido; ecorregião Nordeste Médio-Oriental; peixes de água doce neotropical

Introduction

Freshwater ichthyofaunal studies in Brazil are mainly focused on South and Southeastern regions (Langeani et al. 2009). While these regions are well documented, the Northeastern region is in need of studies, especially the Mid-Northeastern Caatinga Ecoregion (MNCE) (Rosa et al. 2003; Ramos et al. 2005). This ecoregion includes coastal basins located between São Francisco and Parnaíba river basins, draining Alagoas, Pernambuco, Paraíba, Rio Grande do Norte, Ceará, and a small portion of Piauí States (Rosa et al. 2003). Albert et al. (2011) listed 88 freshwater fish species from MNCE; however, new species are being found and described (e. g. Parotocinclus seridoensis Ramos, Barro-Neto, Britski & Lima, 2013; Serrapinnus potiguarJerep & Malabarba, 2014; and Hypsolebias martinsiBritzke, Nielsen & Oliveira, 2016). The estimative of freshwater fish species number at Brazilian Northeast may be premature, given the lack of taxonomic revisions and few representative regional collections (Rosa et al. 2003; Langeani et al. 2009, Ramos et al. 2014).

Ichthyofaunistic inventories at MNCE basins are scarce (Langeani et al. 2009), and the existing ones usually deal with small portions of bigger basins (e.g.Silva et al. 2014), or reservoirs (e.g.Gurgel-Lourenço et al. 2013, Sánchez-Botero et al. 2014). Few coastal basins in this hydrographical region were fully cataloged, for example Gramame river basin, in Paraíba State, in which (Gomes-Filho & Rosa 2001) there were recorded 23 species; Curimataú river basin in Paraíba and Rio Grande do Norte States, 22 species (Ramos et al. 2005), and Pratagi river microbasin, also in Rio Grande do Norte State, 22 species (Paiva et al. 2014).

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.

Material and methods

1. Study area

Mundaú river basin (Figure 1) covers, approximately, an area of 2,227 km² (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).

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

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).

1.1. 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.

Table 1
Geographic coordinates, elevation, tributary and main habitat of the sampling sites along the Mundáu river basin.

Geographic Coordinates	Elevation (m)	Tributary	Habitat
3.62527° S 39.49782° W	108	Mundaú	Main channel
3.21225° S 39.45283° W	11	Mundaú	Estuary
3.46911° S 39.42811° W	51	Mundaú	Main channel
3.59491° S 39.43911° W	89	Mundaú	Main channel
3.60494° S 39.61399° W	913	Mundaú	Headwater
3.62936° S 39.55111° W	273	Mundaú	Main channel
3.46814° S 39.78777° W	56	Cruxati	Stream
3.44799° S 39.57688° W	80	Cruxati	Pond
3.42094° S 39.69766° W	62	Cruxati	Stream
3.41619° S 39.69288° W	70	Cruxati	Rock pool
3.40675° S 39.74111° W	44	Cruxati	Main channel
3.40438° S 39.73577° W	43	Cruxati	Stream
3.39431° S 39.73433° W	41	Cruxati	Main channel
3.37569° S 39.49455° W	34	Mundaú	Dam
3.61006° S 39.52488° W	145	Mundaú	Headwater stream
3.35383° S 39.73588° W	37	Cruxati	Pool on the main channel
3.34763° S 39.50277° W	23	Mundaú	Pool on the main channel
3.28102° S 39.64833° W	17	Cruxati	Pool on the main channel
3.24950° S 39.51011° W	6	Mundaú	Estuary
3.23722° S 39.50433° W	8	Mundaú	Estuary
3.21582° S 39.54688° W	10	Mundaú	Floodplain
3.20777° S 39.53649° W	9	Mundaú	Floodplain
3.20650° S 39.52169° W	8	Mundaú	Estuary
3.20456° S 39.53277° W	9	Cruxati	Dam
3.19706° S 39.53098° W	9	Mundaú	Estuary
3.19319° S 39.53528° W	8	Cruxati	Floodplain
3.19197° S 39.57933° W	13	Cruxati	Estuary
3.19114° S 39.56165° W	7	Mundaú	Pool on the main channel
3.18395° S 39.58353° W	21	Cruxati	Stream
3.18297° S 39.57402° W	14	Cruxati	Pond
3.17528° S 39.57939° W	33	Cruxati	Stream
3.16827° S 39.56391° W	29	Cruxati	Floodplains
3.16748° S 39.57683° W	26	Cruxati	Floodplains
3.49422° S 39.57544° W	102	Cruxati	Stream
3.20361° S 39.52817° W	7	Mundaú	Estuary

Fish were captured using seines (seine nets 20 x 2.5m, mesh size 10 mm and 4 x 2 m, mesh size 5 mm), castnets (2 m height, mesh size 15 mm), gillnets of various mesh sizes (15, 25, 35, 45 and 55 mm), and dip nets (mesh size 5 and 10 mm), and bottle traps. Fishes were anesthetized with 30 mL of a 10% clove oil solution (clove oil 10 mL; ethyl alcohol 90 mL) in 970 mL of water (Lucena et al. 2013), fixed in a 4% formaldehyde solution during a minimal eight-day period, and conserved in 70% ethanol solution. Fish surveys were conducted according to governmental laws (Permit n° 17632-2/ICMBio). Fishes were screened, identified, and deposited at the ichthyological collections of Universidade Federal do Rio Grande do Norte (UFRN) and Universidade Federal da Paraíba (UFPB). The fishes were identified to the lowest taxonomic level according to specialized sources, that is, group specific identification keys, systematic reviews, original descriptions (e.g. Araújo et al. 2004, Britski et al. 1984, Costa 2007, Marceniuk 2005, Kullander 1988, Ploeg 1991, Ramos 2012), and specialist support. Species classified as new occurrences were evaluated according to Reis et al. (2003), Rosa et al. (2003), and Buckup et al. (2007). 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 (Table 2). Astyanax aff. bimaculatus (Linnaeus, 1758) was widely distributed, being present in 19 of 35 sampling sites. Poecilia vivipara Bloch & Schneider, 1801, Awaous tajasica (Lichtenstein, 1822), and Dormitator maculatus (Bloch, 1792) were the only species present in both fresh Bragança & Costa, 2011 and brackish waters. Oreochromis niloticus (Linnaeus, 1758) and Poecilia reticulata Peters, 1859 are exotic introduced species. Poecilia sarrafae, Hemigrammus guyanensis Géry, 1959, and H. rodwayi Durbin, 1909 are new occurrences for MNCE, and Nannostomus beckfordi Günther, 1872 and Callichthys callichthys (Linnaeus, 1758) are new records for Ceará State.

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) introduced; ^(*) Photographed voucher.

ORDER/Family/Species	FISIOLOGY	MAIN CHANNEL	STREAM	FLOOD PLAIN	ROCK POOL	POND	DAM	TOTAL ABUNDANCE	VOUCHER
ELOPIFORMES (1)
Elopidae (1)
Elops saurus Linnaeus, 1766	M	6	0	0	0	0	0	6	UFRN 2612
CHARACIFORMES (16)
Curimatidae (1)
Steindachnerina notonota (Miranda Ribeiro, 1937)	F	122	22	20	0	8	25	197	UFRN 2642
Prochilodontidae (1)
Prochilodus brevis Steindachner, 1875	F	42	8	0	5	15	29	99	UFRN 3530
Anostomidae (1)
Leporinus piau Fowler, 1941	F	7	15	0	0	0	0	22	UFRN 1421
Erythrinidae (1)
Hoplias malabaricus (Bloch, 1794)	F	14	4	2	0	3	4	27	UFRN 2582
Lebiasinidae (1)
Nannostomus beckfordi Günther, 1872(NR)	F	24	19	15	0	3	44	105	UFRN 2591
Characidae (10)
Astyanax aff. bimaculatus (Linnaeus 1758)	F	204	36	4	23	8	24	299	UFRN 1420
Astyanax aff. fasciatus (Cuvier 1819)	F	114	15	0	0	20	0	149	UFRN 1432
Cheirodon jaguaribensis Fowler,1941	F	5	0	0	0	0	0	5	UFRN 2523
Compsura heterura (Eigenmann, 1915)	F	101	12	11	0	8	0	132	UFRN 1430
Hemigrammus guyanensis Géry, 1959(NR)	F	5	6	1	0	0	0	12	UFRN 2599
Hemigrammus rodwayi Durbin, 1909(NR)	F	41	30	4	0	3	0	78	UFRN 2562
Hyphessobrycon sp.	F	0	32	0	0	0	4	36	UFRN 2602
Phenacogaster calverti (Fowler, 1941)	F	114	8	12	0	8	11	153	UFRN 2557
Serrapinnus heterodon (Eigenmann 1915)	F	187	39	11	12	17	22	288	UFRN 1431
Serrapinnus piaba (Lütken, 1875)	F	132	18	11	7	12	11	191	UFRN 1429
Crenuchidae (1)
Characidium bimaculatum Fowler, 1941	F	10	5	0	0	0	0	15	UFRN 1439
SILURIFORMES (6)
Ariidae (2)
Sciades herzbergii (Bloch, 1794)	M	11	0	0	0	0	0	11	UFRN 3550
Auchenipteridae (1)
Trachelyopterus galeatus (Linnaeus, 1766)	F	4	0	0	0	0	0	4	UFRN 3531
Callichthyidae (1)
Callichthys callichthys (Linnaeus, 1758)	F	1	1	0	0	0	0	2	UFRN 2607
Loricariidae (2)
Hypostomus cf. pusarum (Starks, 1913)	F	9	0	0	0	0	4	13	UFRN 2584
Parotocinclus cearensis Garavello, 1977	F	4	0	0	0	0	0	4	UFRN 1422
BATRACHOIDIFORMES (1)
Batrachoididae (1)
Batrachoides surinamensis (Bloch & Schneider, 1801)	M	1	0	0	0	0	0	1	UFRN 3545
MUGILIFORMES (1)
Mugilidae (1)
Mugil curema Velenciennes, 1836	M	24	0	0	0	0	0	24	UFRN 2611
CYPRINODONTIFORMES (5)
Cynolebiidae (2)
Anablepsoides cearensis (Costa &Vono, 2009) (CR)	F	0	9	20	0	0	0	29	UFRN 3046*
Hypsolebias sp.	F	8	12	8	0	0	0	28	UFRN 1446
Poeciliidae (3)
Poecilia reticulata Peters,1859(I)	F	36	31	0	0	0	0	67	UFRN 2581
Poecilia sarrafae Bragança & Costa, 2011(NR)	F	0	20	26	0	0	0	46	UFRN 2574
Poecilia vivipara Bloch & Schneider, 1801	F	113	28	10	29	12	6	198	UFRN 1419
SYNBRANCHIFORMES (1)
Synbranchidae (1)
Synbranchus marmoratus Bloch, 1795	F	2	0	0	0	0	0	2	UFRN 3534
PERCIFORMES (20)
Centropomidae (1)
Centropomus undecimalis (Bloch, 1792)	M	5	0	0	0	0	0	5	UFRN 3546
Carangidae (2)
Hemicaranx sp.	M	4	0	0	0	0	0	4	UFRN 3541
Oligoplites saurus (Bloch & Schneider, 1801)	M	4	0	0	0	0	0	4	UFRN 3548
Lutjanidae (1)
Lutjanus sp.	M	3	0	0	0	0	0	3	UFRN 3538
Gerreidae (3)
Eugerres brasilianus (Cuvier, 1830)	M	4	0	0	0	0	0	4	UFRN 3549
Diapterus auratus Ranzani,1842	M	23	0	0	0	0	0	23	UFRN 3655
Eucinostomus argenteus Baird & Girard, 1855	M	8	0	0	0	0	0	8	UFRN 3654
Haemulidae (2)
Genyatremus luteus (Bloch, 1970)	M	5	0	0	0	0	0	5	UFRN 3535
Haemulopsis corvinaeformis (Steindachner 1868)	M	8	0	0	0	0	0	8	UFRN 3542
Sparidae (1)
Archosargus probatocephalus (Walbaum, 1792)	E	10	0	0	0	0	0	10	UFRN 4281
Sciaenidae (2)
Bairdiella ronchus (Cuvier, 1830)	M	5	0	0	0	0	0	5	UFRN 3537
Larimus breviceps Cuvier, 1830	M	11	0	0	0	0	0	11	UFRN 3540
Ephippidae (1)
Chaetodipterus faber (Broussonet, 1782)	M	15	0	0	0	0	0	15	UFRN 3547
Cichlidae (3)
Cichlasoma orientale Kullander,1983	F	41	8	5	0	6	8	68	UFRN 1426
Crenicichla menezesi Ploeg, 1991	F	11	12	0	0	0	6	29	UFRN 1442
Oreochromis niloticus (Linnaeus, 1758) (I)	F	23	3	0	0	8	12	46	UFRN 2588
Eleotridae (2)
Dormitator maculatus (Bloch,1792)	E	6	0	5	0	0	0	11	UFRN 2613
Eleotris pisonis (Gmelin,1789)	E	13	0	0	0	0	0	13	UFRN 2577
Gobiidae (2)
Awaous tajasica (Lichtenstein, 1822)	F	2	0	0	0	0	0	2	UFPB 10028
Gobionellus oceanicus (Pallas, 1770)	M	3	0	0	0	0	0	3	UFRN 3415
PLEURONECTIFORMES (3)
Paralichthyidae (1)
Citharichthys sp.	E	4	0	0	0	0	0	4	UFRN 3553
Achiridae (2)
Achirus achirus (Linnaeus, 1758)	E	3	0	0	0	0	0	3	UFRN 3552
Trinectes paulistanus (Miranda Ribeiro, 1915)	E	4	0	0	0	0	0	4	UFPB 10030
TETRAODONTIFORMES (1)
Tetraodontidae (2)
Lagocephalus laevigatus (Linaeus, 1766)	M	4	0	0	0	0	0	4	UFRN 3544
Sphoeroides testudineus (Linnaeus, 1758)	E	10	0	0	0	0	0	10	UFRN 3543
Total of species (n = 55) New record (n = 4)		1,570	393	165	76	131	210	2,545

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, 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).

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.

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) suggest that Hypsolebias sp. 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), both 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. 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.

Acknowledgements

We thank Conceição Teixeira, Miguel Pires, Elissângela Teixeira, Chagas Sousa, Evaldo Carlos, Tiago Sousa, André Pereira, Victor Távora, Frederico Garcia and Luana Magalhães for helping during fieldwork. Roberto Feitosa, Bianca Terra, Cynthia Ogawa, José Louvise and Márcio Silva for contributing with laboratory activities. Keilo Teixeira was funded by FUNCAP (Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico), and Project was partially funded by CAPES (AUXPE 23038.005584/2012-20).

References

• ALBERT, J.S., PETRY, P. & REIS, R.E. 2011. Major biogeographic and phylogenetic patterns. In Historical Biogeography of Neotropical Freshwater Fishes (J.S. Albert & R.E. Reis, eds). Berkeley University of California Press, p.21–58.
• ARAÚJO, M.E., TEIXEIRA, J.M.C. & OLIVEIRA, A.M.E. 2004. Peixes estuarinos marinhos do Nordeste do Brasil: guia ilustrado. Edições UFC, Fortaleza.
• BRAGANÇA, P.H.N. & COSTA, W.J.E.M. 2011. Poecilia sarrafae, a new poeciliid from the Parnaíba and Mearim river basins, northeastern Brazil (Cyprinodontiformes: Cyprinodontoidei). Ichthyol. Explor. Fresh. 21(4): 369-376.
• BENZAQUEM, D.C., OLIVEIRA, C., BATISTA, J.S., ZUANON, J. & PORTO, J.I.R. 2015. DNA Barcoding in Pencilfishes (Lebiasinidae: Nannostomus) Reveals Cryptic Diversity across the Brazilian Amazon. PLoS ONE 10(2): 1-14.
• BRASIL. 2007. Ministério do Meio Ambiente. Áreas Prioritárias para a Conservação, Uso Sustentável e Repartição de Benefícios da Biodiversidade Brasileira: Atualização – Portaria MMA N° 9, de 23 janeiro de 2007. Brasília: MMA. p.300.
• BRASIL. 2014. Lista Nacional Oficial de Espécies da Fauna Ameaçada de Extinção - Portaria N° 443, de 17 de dezembro de 2014. Ministério do Meio Ambiente. Diário Oficial da União, Brasília, Seção 1(245): 121-130.
• BRASIL. 2016. Ministérios do Meio Ambiente. Resultados da 2ª atualização das Áreas e Ações Prioritárias para Conservação, Uso Sustentável e Repartição dos Benefícios da Biodiversidade dos biomas Cerrado e Pantanal realizado em 2012, e da Caatinga, realizado em 2015. http://www.mma.gov.br/biodiversidade/biodiversidade-brasileira/%C3%A1reas-priorit%C3%A1rias/item/10724 (the last access in 13/09/2016).
  » http://www.mma.gov.br/biodiversidade/biodiversidade-brasileira/%C3%A1reas-priorit%C3%A1rias/item/10724
• BRITSKI, H.A., SATO, Y. & ROSA, A.B.S. 1984. Manual de Identificação de Peixes da Região de Três Marias: Com Chave de Identificação Para os Peixes da Bacia do São Francisco. Brasília: Câmara dos Deputados, Coordenação de Publicações - CODEVASF, Divisão de Piscicultura e Pesca.
• BRITZKE R., NIELSEN, D.T.B. & OLIVEIRA, C. 2016. Description of two new species of annual fishes of the Hypsolebias antenori species group (Cyprinodontiformes: Rivulidae), from Northeast Brazil. Zootaxa 4114(2):123-138.
• BUCKUP, P.A., MENEZES, N.A. & GHAZZI, M.S. 2007. Catálogo das Espécies de Peixes de Água Doce do Brasil. Rio de Janeiro, Museu Nacional, p. 1-195.
• COGERH. 2014. Companhia de Gestão dos Recursos Hídricos. Bacias hidrográficas do Litoral Características Gerais. http://portal.cogerh.com.br/downloads/category/83-pacto-das-aguas-plano-estrategico (the last access in 02/11/2014)
  » http://portal.cogerh.com.br/downloads/category/83-pacto-das-aguas-plano-estrategico
• COSTA, W.J.E.M. 2007. Taxonomic revision of the seasonal South American killifish genus Simpsonichthys (Teleostei: Cyprinodontiformes: Aplocheiloidei: Rivulidae). Zootaxa. (1669): 1-134.
• COSTA, W.J.E.M. 2008. Simpsonichthys longignatus, a new seasonal killifish of the S. flammeus group from the Pacoti river basin, northeastern Brazil (Cyprinodontiformes:Rivulidae). Ichthyol. Explor. Fresh. 19(2): 155-159.
• COSTA, W.J.E.M. & VONO, V. 2009. Rivulus cearensis, a new aplocheiloid killifish from northeastern Brazil (Cyprinodontiformes:Rivulidae). Ichthyol. Explor. Fresh. 20(1): 7-11.
• ESCHMEYER, W.N. 2015. Catalog of fishes: genera, species, references. http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp (the last access in 06/04/2015)
  » http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
• FISHBASE. http://www.fishbase.org/home.htm (the last access in 09/10/2014)
  » http://www.fishbase.org/home.htm
• FUNCEME. 2015. Fundação Cearense de Meteorologia e Recursos Hídricos. http://www.funceme.br/app/calendario/produto/municipios/maxima/diario?data=hoje (the last access in 24/03/2015)
  » http://www.funceme.br/app/calendario/produto/municipios/maxima/diario?data=hoje
• GOMES-FILHO, G. & ROSA R.S. 2001. Inventário da Ictiofauna da Bacia do Rio Gramame, Paraíba, Brasil. In A Bacia do Rio Gramame: Biodiversidade, Uso e Conservação (T. Watanabe, ed.). PRODEMA, João Pessoa, p.167–173.
• GURGEL-LOURENÇO, R.C., SOUSA, W.A., SÁNCHEZ-BOTERO, J.I. & GARCEZ, D.S. 2013. Ichthyofauna of two reservoirs in the middle Acaraú river. Check List 9(6): 1391-1395.
• IPECE. 2012. Instituto de Pesquisa e Estratégia Econômica do Ceará. http://www.ipece.ce.gov.br/publicacoes/perfil_basico/pbm-2013/Itapipoca.pdf (the last access in 01/01/2015)
  » http://www.ipece.ce.gov.br/publicacoes/perfil_basico/pbm-2013/Itapipoca.pdf
• JEREP, FC & MALABARBA, L.R. 2014. A new species of Serrapinnus Malabarba, 1998 (Characidae: Cheirodontinae) from Rio Grande do Norte State, northeastern Brazil. Neotrop. Ichthyol. 12(2): 301-308.
• KULLANDER, S.O. 1988. A revision of the South American cichlid genus Cichlasoma (Teleostei: Ciclidae). Swedish Museum of Natural History, Stockholm.
• LANGEANI, F., BUCKUP, P.A., MALABARBA, L.R., PY-DANIEL, L.H.R., LUCENA, C.A.S., ROSA, R.S., ZUANON, J.A.S., LUCENA, Z.M.S., BRITTO, M.R., OYAKAWA, O.T. & GOMES-FILHO, G. 2009. Peixes de água doce. In Estado da arte e perspectivas para a zoologia no Brasil (R.M. Rocha & W.A. Boeger, eds). Sociedade Brasileira de Zoologia, Volume I, Curitiba, p.211-230.
• LEÃO, T. C. C., ALMEIDA, W.R., DECHOUM, M.S., ZILER, S.R. 2011. Espécies exóticas invasoras no Nordeste do Brasil: contextualização, manejo e políticas públicas. Recife: Centro de Pesquisas Ambientais do Nordeste e Instituto Hórus de Desenvolvimento e Conservação Ambiental. 99 p.
• LÉVÊQUE, C., OBERDORFF, T., PAUGY, D., STIASSNY, M.L.J., & TEDESCO, P.A. 2008. Global diversity of fish (Pisces) in freshwater. Hydrobiologia. 595(1): 545-567.
• LINDHOLM, A.K., BREDEN, F., ALEXANDER, H.J., CHAN, W.K., THAKURTA, S.G., & BROOKS, R. 2005. Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Mol. Ecol. 14(12): 3671-3682.
• LUCENA, C.A.S. & SOARES, H.G. 2016. Review of species of the Astyanax bimaculatus “caudal peduncle spot” subgroup sensu Garutti & Langeani (Characiformes, Characidae) from the rio La Plata and rio São Francisco drainages and coastal systems of southern Brazil and Uruguay. Zootaxa 4072 (1): 101-125.
• LUCENA, C.A. S., CALEGARI, B.B., PEREIRA, E.H.L. & DALLEGRAVE, E. 2013. O uso de óleo de cravo na eutanásia de peixes. Boletim Sociedade Brasileira de Ictiologia 105: 20-24.
• MARCENIUK, A. P. Chave para identificação das espécies de bagres marinhos (siluriformes, ariidae) da costa brasileira. Boletim do Instituto de Pesca, São Paulo 31(2): 89 – 101.
• MENEZES, N.A., WEITZMAN, S.H., OYAKAWA, O.T., LIMA, F.C.T., CASTRO, R.M.C., & WEITZMAN, M.J. 2007. Peixes de água doce da Mata Atlântica: lista preliminar das espécies e comentários sobre conservação de peixes de água doce neotropicais. Museu de Zoologia da Universidade de São Paulo, São Paulo.
• NASCIMENTO, W.S., BARROS, N.H.C., ARAÚJO, A.S., GURGEL, L.L., CANAN, B., MOLINA, W.F., ROSA, R.S. & CHELLAPPA, S. 2014. Composição da ictiofauna das bacias hidrográficas do Rio Grande do Norte, Brasil. Bio. Amaz. 4(1): 126-131.
• PAIVA, M.P. & MESQUITA, P.E.C. 2013. Uma semente fecunda: Commissão Téchnica de Piscicultura do Nordeste (1932 – 1945). Revista do Instituto do Ceará. p.10-40.
• PAIVA, R.E.C., LIMA, S.M.Q., RAMOS, T.P.A. & MENDES L.F. 2014. Fish fauna of Pratagi river coastal microbasin, extreme north Atlantic Forest, Rio Grande do Norte State, northeastern Brazil. Check List 10(5): 968–975.
• PLOEG, A. 1991. Revision of the South American cichlid genus Crenicichla Heckel, 1840, with descriptions of fifteen new species and considerations on species groups, phylogeny and biogeography. Academisch Proefschrift, Universiteit van Amsterdam, Amsterdam.
• RAMOS, R.T.C., RAMOS, T.P.A., ROSA, R.S., BELTRÃO, G.B.M. & GROTH, F. 2005. Diversidade de Peixes (Ictiofauna) da bacia do rio Curimataú, Paraíba. In Análise das Variações da Biodiversidade do Bioma Caatinga: Suporte das Estratégias Regionais de Conservação (F.S. Araujo, M.J.N. Rodal & M.R.V. Barbosa, eds.), Ministério do Meio Ambiente, Brasília, p.291-318.
• RAMOS, T.P.A., R.T.C. RAMOS and S.A.Q.A. RAMOS. 2014. Ichthyofauna of the Parnaíba river Basin, Northeastern Brazil. Biota Neotrop. 14(1): 1-8. www.biotaneotropica.org.br/v14n1/en/abstract?inventory+bn01014012014 (the last access in 17/02/2016).
• RAMOS, T.P.A. 2012. Ictiofauna de água doce da bacia do rio Parnaíba. Tese de doutorado, Universidade Federal da Paraíba, João Pessoa.
• REIS, R.E., KULLANDER, S.O. & FERRARIS JR, C.J. 2003. Check list of the freshwater fishes of South Central and America, Porto Alegre.
• ROSA, R.S. & GROTH F. 2004. Ictiofauna dos Ecossistemas de Brejos de Altitude de Pernambuco e Paraíba. In Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação (K.C. Pôrto, J.J.P. Cabral & M. Tabarelli, orgs.). Série Biodiversidade, Ministério do Meio Ambiente, Brasília, p.201–210.
• ROSA, R.S., MENEZES, N.A., BRITSKI, H.A., COSTA, W.J.E. & GROTH F. 2003. Diversidade, padrões de distribuição e conservação dos peixes da caatinga. In Ecologia e Conservação da Caatinga (I.R. Leal, M. Tabarelli & J.M.C. Silva eds.). Editora Universitária da Universidade Federal de Pernambuco, Recife, p.135–180.
• SÁNCHEZ-BOTERO, J. I., REIS, V.C., CHAVES, F.D.N. & GARCEZ, D.S. 2014. Fish assemblage of the Santo Anastácio reservoir (Ceará State, Brazil). Boletim do Instituto de Pesca. 40(1): 1-15.
• SEMACE. 2014. Superintendência Estadual do Meio Ambiente - Área de Proteção Ambiental do Estuário do Rio Mundaú. http://www.semace.ce.gov.br/2010/12/area-de-protecao-ambiental-do-estuario-do-rio-mundau/ (the last access in 07/10/2014)
  » http://www.semace.ce.gov.br/2010/12/area-de-protecao-ambiental-do-estuario-do-rio-mundau/
• SILVA, M.J., RAMOS, T.P.A., DINIZ, V.D., RAMOS, R.T.C. & MEDEIROS, E.S.F. 2014. Ichthyofauna of Seridó/Borborema: a semi-arid region of Brazil. Biota Neotrop. 14(3): 1-6. http://dx.doi.org/10.1590/1676-06032014007713 (the last access in 17/02/2016)
  » http://dx.doi.org/10.1590/1676-06032014007713
• SOARES FILHO, A.A., SAMPAIO, C.M.S., FERREIRA, T.D., LOURENÇO, J.A., SOUSA, R.A.L. & IGARASHI M.A. 2010. Contribuição ao conhecimento da Ictiofauna estuarina no Estado do Ceará, Brasil. Revista da Gestão Costeira Integrada 8: 1-9.
• WANG, X., AUGUSTO, S.A., EDUARDS, R.L., CHENG, H., CRISTALLI, P.S., SMART., P.L., RICHARDS, D.A. & SHEN, C.C. 2004. Wet periods in northeastern Brazil over the past 210 kyr linked to distant climate anomalies. Nature 432: 740-743.

Publication Dates

• Publication in this collection
  2017

History

• Received
  18 Feb 2016
• Reviewed
  02 Nov 2016
• Accepted
  07 Dec 2016