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Papéis Avulsos de Zoologia

Print version ISSN 0031-1049On-line version ISSN 1807-0205

Pap. Avulsos Zool. vol.59  São Paulo  2019  Epub Nov 07, 2019

https://doi.org/10.11606/1807-0205/2019.59.50 

ARTICLE

Continental fishes from the Tambaba Environmentally Protected Area, Paraíba State, Brazil

Telton Pedro Anselmo Ramos1 
http://orcid.org/0000-0002-3808-8701

Yuri Gomes Ponce de Carvalho-Rocha2 
http://orcid.org/0000-0003-3123-0581

Leonardo Oliveira-Silva3 
http://orcid.org/0000-0002-4153-5648

Sílvia Yasmin Lustosa-Costa4 
http://orcid.org/0000-0003-2405-7039

Paula Honório Pires Ferreira5 
http://orcid.org/0000-0003-2528-660X

1Universidade Estadual da Paraíba (UEPB), Departamento de Biologia (DEPBIO), Laboratório de Ecologia Aquática. Campina Grande, PB, Brasil. E-mail: telton@gmail.com

2Universidade Federal da Paraíba (UFPB), Centro de Ciências Exatas e da Natureza (CCEN), Departamento de Sistemática e Ecologia (DSE), Laboratório de Sistemática e Morfologia de Peixes. João Pessoa, PB, Brasil. E-mail: yuri_gpcr@hotmail.com

3Universidade Federal da Bahia (UFBA), Instituto de Biologia (IBIO), Laboratório de Ictiologia. Salvador, BA, Brasil. E-mail: leonardoufcg.bio@hotmail.com (corresponding author)

4Universidade Federal do Rio Grande do Norte (UFRN), Centro de Biociências (CB), Departamento de Botânica e Zoologia (DBEZ), Laboratório de Ictiologia Sistemática e Evolutiva. Natal, RN, Brasil. E-mail: silviayasminlcosta@gmail.com

5Centro Universitário Maurício de Nassau (UNINASSAU). João Pessoa, PB, Brasil. E-mail: paulahonorio_bio@yahoo.com.br


Abstract

Tambaba environmentally protected area is situated on the south coast of Paraíba State, within the Atlantic forest biome of the northeastern region in Brazil. The Tambaba environmentally protected area consists of a series of independent drainages: Graú, Mucatú, and Bucatú river micro-basins, and Caboclo River sub-basin that belongs to Gurugi River micro-basin. Ichthyological samples were collected in five scientific expeditions between months of June and July in 2015. Twenty-nine sites from different habitats (e.g., spanning tributaries, streams, rivers, and estuaries) were accessed for sampling. A total of 44 species distributed within 38 genera, 25 families, and 17 orders were assigned to the Tambaba hydrographic region. Freshwater species comprised 36% (n = 16) and marine-estuarine species 64% (n = 28) of the total collected specimens. Two invasive species occur in the freshwater sites: Cichla monoculus and Poecilia reticulata. Cheirodon jaguaribensis, Cichlasoma orientale, and Crenicichla brasiliensis are endemic to the Brazilian Northeast region with the first species restricted to the Northeast Caatinga and Coastal drainages hydrographic ecoregion.

Key-Words. Atlantic forest ichthyofaunal; Endemism; Northeastern Caatinga, Coastal Drainages

INTRODUCTION

The Atlantic Florest originally extended from the Rio Grande do Norte State (Northeastern region of Brazil) to the Rio Grande do Sul (Southern region) in Brazil. Throughout its distribution exhibits several types and subtypes of tropical and subtropical forests, comprising the second largest forest in South America (Gouveia et al., 2017). Preservation and conservation of the Atlantic Forest rivers and ichthyofauna are imperative due to its high endemicity rate (e.g.,Gomiero & Braga, 2006; Oyakawa et al., 2006; Menezes et al., 2007; Miranda, 2012; Gouveia et al., 2017) and exclusive ecological characteristics (e.g.,Barbosa & Costa, 2012; Pereira et al., 2012). Menezes et al. (2007) listed 325 freshwater fish species for a portion of Atlantic forest in the Brazilian southeastern region. These authors called attention to the lack of taxonomic data related to the fish fauna for the Atlantic forest in the Brazilian northeast region; Abilhoa et al. (2011) recorded 269 freshwater species for streams in this region through data taken from the literature, and Camelier & Zanata (2014) recognized 169 native freshwater species for the northeastern Atlantic Forest ecoregion. Many species were recently described within this region (Barbosa & Costa, 2012; Pereira et al., 2012; Zanata & Pitanga, 2016; Craig et al., 2017; de Pinna et al., 2018; Burger et al., 2019) with achievements of several related studies on the systematics and biogeography of the continental ichthyofauna of the Forest Atlantic.

The Atlantic forest biome requires conservation efforts through the creation of conservation units (UCs) throughout its area of extension in relation to its high diversity and accelerated loss and fragmentation of the original habitat (Almeida, 2016). Despite having the largest number of environmentally protected areas among the South American regions and increased creation of reserves and natural parks in recent years, the conservation effort in the area is still insufficient (Tabarelli et al., 2005; Almeida, 2016). Tambaba environmentally protected area (APA) is situated on the south coast of Paraíba State in Northeast Brazil within the Atlantic forest biome. This conservation unit (UC) was regulated in 2002 through the State Act (№ 22.882) and assigned to the category of conservation unities for sustainable use in order to guarantee compatibility between the sustainable usage of the natural resources and nature conservation as defined in the principal action plan for effective protection of the local fauna and flora (Costa, 2002).

A complex of small littoral hydrographic basins covers the hydrography of the Tambaba Environmentally Protected Area, located in the Northeastern Caatinga and Coastal Drainages - NCCD ecoregion (sensuAbell et al., 2008). Several studies focused on assessing the ichthyofauna of hydrographic basins from the NCCD (e.g.,Rosa et al., 2003; Ramos et al., 2005; Paiva et al., 2014; Silva et al., 2014; Rodrigues-Filho et al., 2016; Teixeira et al., 2017; Gouveia et al., 2017; Oliveira-Silva et al., 2018; Ramos et al., 2018). However, with exception to Paiva et al. (2014) and Gouveia et al. (2017), the diversity of fishes within the Atlantic forest biome of this ecoregion was not yet investigated. Thus, the present study aimed to provide an inventory of the ichthyofauna from the river basins present in the Tambaba Environmentally Protected Area, contributing towards the taxonomic knowledge related to the fish fauna of the Atlantic Forest biome in the NCCD ecoregion.

MATERIAL AND METHODS

Study area

Tambaba Environmentally Protected Area is located in the micro-region of the south coast of Paraíba State, Brazil between 07°25’00”S and 07°16’30”S and 34°55’00”W and 34°47’30”W, incorporating the municipalities of Conde, Pitimbú, and Alhandra within the Mata Paraibana mesoregion (Almeida et al., 2008). It comprises 114,46 km² of total area extension, with its geographical limits defined by the local hydrographic basins (Fig. 1).

Figure 1 Map of Tambaba environmentally protected area (green area) in Paraíba State, Brazil, displaying the sampling sites (red dots) in Graú, Mucatú and Bucatú River basins, Caboclo River sub-basin and Gurugi River basin. 

Graú, Mucatú and Bucatú river micro-basins and the Caboclo River sub-basin with the latter belonging to the Gurugi River micro-basin are located in the Tambaba Environmentally Protected Area (AESA, 2004). Graú River basin has 18,304 km of extension and its main course discharges at the north of Bela beach between Pitimbu and Conde municipalities. Mucatú River micro-basin has 9,690 km of extension and releases in the estuary of Bela beach in Pitimbu municipality. Bucatu River micro-basin extends approximately 3,265 km and it comprises a small drainage system located on the coast of Tabatinga beach in Conde municipality. Caboclo River sub-basin, a tributary of Gurugi River basin, comprises 6,435 km of extension and discharges in the main course of Gurugi River that later discharges at Jacumã beach in Conde municipality.

Data collection

Five scientific expeditions were undertaken in the hydrographic basins in Tambaba Environmentally Protected Area in June (three) and July (two) 2015. Sampling took place at 29 sites covering streams, rivers and estuaries in the municipalities of Alhandra, Conde, and Pitimbu (Fig. 1, Table 1). Of these, 13 sampling sites are located at Graú River basin, seven to Mucatú River basin, five to Bucatú River basin and four to the Caboclo River sub-basin in the Gurugi River basin. Specimens from the fish collection of Universidade Federal da Paraíba (UFPB) were also examined.

Table 1 List of sampling sites in the Tambaba APA, Paraíba State, Brazil.  

ID Sampling sites Geographical Coordinates
1 Mucatú stream, Mucatú village, Pitimbu 07°23’19.1”S; 34°51’41.0”W
2 Stream in Mucatú village, Pitimbu 07°23’06.0”S; 34°51’52.1”W
3 Graú River, under bridge at PB-008 road, Pitimbu 07°21’04.2”S; 34°49’04.4”W
4 Andreza River, Andreza village, Pitimbu 07°20’38.2”S; 34°50’52.3”W
5 Tributary of Andreza River, Pitimbu 07°20’51.4”S; 34°50’44.5”W
6 Tributary of Graú River, PB-008, Pitimbu 07°22’19.9”S; 34°49’19.0”W
7 Riacho do Boi stream, tributary of Mucatú River, Pitimbu 07°24’37.2”S; 34°50’45.7”W
8 Riacho do Boi stream, tributary of Mucatú, Nova Vida village, Pitimbu 07°24’18.1”S; 34°50’16.0”W
9 Riacho do Boi stream, tributary of Mucatú River, Pitimbu 07°24’04.1”S; 34°49’58.6”W
10 Estuary of Graú River, Pitimbu 07°22’42.4”S; 34°48’16.3”W
11 Graú River mouth, Bela beach, Pitimbu 07°23’13.6”S; 34°48’13.7”W
12 Mucatú River, Pitimbu 07°23’36.1”S; 34°49’57.7”W
13 Graú River, Pitimbu 07°20’52.1”S; 34°48’47.7”W
14 Tributary of Graú River, between Mata do Chica and Igarapú villages, Alhandra 07°19’09.6”S; 34°53’21.5”W
15 Igarapú River, Alhandra 07°18’38.9”S; 34°54’14.2”W
16 Tributary of Graú River, Alhandra 07°20’03.0”S; 34°53’34.7”W
17 Tributary of Graú River. Alhandra 07°20’09.9”S; 34°52’29.4”W
18 Graú River, under bridge of Alhandra road - Jacumã, Alhandra 07°20’18.5”S; 34°51’53.4”W
19 Jangada stream, tributary of Graú River, Pitimbu 07°20’50.1”S; 34°51’18.9”W
20 Estuary of Mucatú River, Bela beach, Pitimbu 07°23’57.8”S; 34°48’21.0”W
21 Left side of source from Bucatú River, Conde 07°19’37.6”S; 34°49’22.3”W
22 Bucatú River, Conde 07°19’18.0”S; 34°48’46.2” W
23 Right side of source from Bucatú River, Conde 07°18’22.0”S; 34°49’09.9”W
24 Estuary of Bucatú River, under bridge of PB-008 road, Conde 07°18’48.1”S; 34°48’30.4”W
25 Estuary of Bucatú River, Tabatinga beach, Conde 07°18’43.5”S; 34°48’09.0”W
26 Tributary of Caboclo River, Conde 07°17’42.0”S; 34°50’14.9”W
27 Tributary of Caboclo River, Conde 07°18’13.8”S; 34°50’22.9”W
28 Caboclo River, tributary of Gurugi River, Conde 07°18’22.0”S; 34°50’34.5”W
29 Caboclo River, tributary of Gurugi River, Conde 07°17’44.9”S; 34°50’18.4”W

Specimens were collected using seine nets (4 m length, 5 mm mesh size; 10 m length, 5 mm mesh size; 20 m length, 12 mm mesh size), cast nets (20 mm mesh size), gillnets (10 m length, 20 mm mesh size) and dip nets (5 mm mesh size). Specimens were then anesthetized in eugenol solution diluted in alcohol and water, and then transferred to 10% formaldehyde for fixation. Later, scientific curatorial standards were undertaken such as specimen fixation in formaldehyde for a minimum of eight days, preservation in 75° GL ethyl alcohol solution, lot and specimen labeling, according to the methods of Malabarba & Reis (1987). Photographs of fresh specimens were taken whenever possible using a digital camera model Canon PowerShot SX60 HS. Sorting and taxonomic identification of specimens and subsequent labeling were performed at the Laboratório de Sistemática e Morfologia de Peixes of the Universidade Federal da Paraíba (LASEP/UFPB). Lots and specimens were registered and deposited at the UFPB Ichthyological Collection. Species identification was based on studies of Araújo et al. (2004), Britski et al. (1984), Figueiredo & Menezes (2000), Kullander (1988), Ploeg (1991), Ramos (2012) and Ramos et al. (2018). Taxonomic classification follows Fricke et al. (2019).

RESULTS

A total of 36 species were identified through examination of 1,124 specimens collected in the Tambaba APA (Figs. 2, 3, 4, and 5). In addition, eight species were identified based on the analysis of 54 specimens (23 lots) from the UFPB fish collection collected in the Graú River estuary in 2014. Thus, 44 species are recognized in the Tambaba APA hydrographic basins and are classified within 38 genera, 25 families, and 17 orders (Table 2). Of these, 36% (n = 16) are from freshwater and 64% (n = 28) are from estuarine-marine sites. Cichla monoculus Spix & Agassiz, 1831, the “tucunaré”, and Poecilia reticulata Peters, 1859 are invasive species in the freshwater sites. Cheirodon jaguaribensis Fowler, 1941, Cichlasoma orientale Kullander, 1983, and Crenicichla brasiliensis (Block, 1792) are endemic to the Brazilian northeast region, in which the first species is restricted to the NCCD hydrographic ecoregion.

Figure 2 Species from Tambaba APA hydrographic basins: (a) Atherinella brasiliensis, 98.2 mm SL; (b) Omobranchus punctatus, 39.4 mm SL; (c) Astyanax aff. bimaculatus, 42.1 mm SL; (d) Hemigrammus unilineatus, 29.5 mm SL; (e) Compsura heterura, 27.7 mm SL; (f) Cheirodon jaguaribensis, 32.3 mm SL; (g) Erythrinus erythrinus, 91.6 mm SL; (h) Hoplias aff. malabaricus, 59.3 mm SL; (i) Metynnis lippincottianus, 51.7 mm SL; (j) Crenicichla brasiliensis, 35.3 mm SL; (k) Cichlasoma orientale, 60.6 mm SL; (l) Cichla monoculus, 55.6 mm SL; (m) Geophagus brasiliensis, 54.8 mm SL; (n) Lycengraulis grossidens, 60.3 mm SL. 

Figure 3 Species of fish from Tambaba APA hydrographic basins: (a) Poecilia vivipara, 32.7 mm SL; (b) Dormitator maculatus, 67.3 mm SL; (c) Eleotris pisonis, 65.7 mm SL; (d) Awaous tajasica, 70.6 mm SL; (e) Bathygobius soporator, 71.9 mm SL; (f) Evorthodus lyricus, 90.9 mm SL; (g) Ctenogobius boleosoma, 16.6 mm SL; (h) Gymnotus carapo, 86.1 mm TL; (i) Sphyraena barracuda, 153.8 mm SL; (j) Mugil curema, 86.9 mm SL; (k) Centropomus undecimalis, 121.8 mm SL; (l) Gymnura micrura, 94.9 mm SL. 

Figure 4 Species of fish from Tambaba APA hydrographic basins: (a) Diapterus auratus, 57.4 mm SL; (b) Eucinostomus argenteus, 69.7 mm SL; (c) Eucinostomus gula, 61.4 mm SL; (d) Haemulon aurolineatum, 90.2 mm SL; (e) Lutjanus alexandrei, 55.6 mm SL; (f) Lutjanus jocu, 45.6 mm SL; (g) Abudefduf saxatil, 17.8 mm SL; (h) Trinectes inscriptus, 46.9 mm SL; (i) Citharichthys sp., 95.9 mm SL; (j) Citharichthys spilopterus, 103.1 mm SL; (k) Synbranchus aff. marmoratus, 315.3 mm TL. 

Figure 5 Species of fish from Tambaba APA hydrographic basins: (a) Sphoeroides spengleri, 90.3 mm SL; (b) Sphoeroides testudineus, 73.3 mm SL; (c) Syngnathus pelagicus, 153.8 mm SL. 

Table 2 List of species from Tambaba APA, Paraíba State, Brazil observed in the Graú, Mucatú, and Bucatú river basins, Caboclo River sub-basin and Gurugi River basin. DD = deficient data, LC = Last concern, NE = not evaluated, UFPB = Universidade Federal da Paraíba, UFRN = Universidade Federal do Rio Grande do Norte, NT = not threatened. 

ORDER/Family/species PHISIOLOGY STATUS VOUCHER
ATHERINIFORMES
Atherinopsidae
Atherinella brasiliensis (Quoy & Gaimard, 1825) Marine-estuarine LC UFPB 11559
BLENNIIFORMES
Blenniidae
Omobranchus punctatus (Valenciennes, 1836) Marine-estuarine LC UFPB 11569
CHARACIFORMES
Characidae
Astyanax aff. bimaculatus (Linnaeus 1758) Freshwater LC UFPB 10418
Cheirodon jaguaribensis Fowler, 1941 Freshwater DD UFPB 11617
Compsura heterura Eigenmann, 1915 Freshwater LC UFPB 9790
Hemigrammus unilineatus (Gill, 1858) Freshwater NE UFPB 10425
Erythrinidae
Erythrinus erythrinus (Bloch & Schneider, 1801) Freshwater LC UFPB 10431
Hoplias aff. malabaricus (Bloch, 1794) Freshwater LC UFPB 10417
Serrasalmidae
Metynnis lippincottianus (Cope, 1870) Freshwater LC UFPB 9906
CICHLIFORMES
Cichlidae
Crenicichla brasiliensis (Bloch, 1792) Freshwater LC UFPB 10649
Cichlasoma orientale Kullander, 1983 Freshwater LC UFPB 10686
Cichla monoculus Spix & Agassiz, 1831 Freshwater LC UFPB 10644
Geophagus brasiliensis (Quoy & Gaimard, 1824) Freshwater LC UFPB 10420
CLUPEIFORMES
Engraulidae
Lycengraulis grossidens (Spix & Agassiz, 1829) Marine-estuarine LC UFPB 9927
CYPRINODONTIFORMES
Poeciliidae
Poecilia reticulata Peters, 1859 Freshwater LC UFPB 10688
Poecilia vivipara Bloch & Schneider, 1801 Freshwater NE UFPB 10416
GOBIIFORMES
Eleotridae
Dormitator maculatus (Bloch, 1792) Marine-estuarine LC UFPB 10419
Eleotris pisonis (Gmelin, 1789) Marine-estuarine LC UFPB 10421
Gobiidae
Awaous tajasica (Lichtenstein, 1822) Marine-estuarine LC UFPB 10669
Bathygobius soporator (Valenciennes, 1837) Marine-estuarine LC UFPB 9904
Evorthodus lyricus (Girard, 1858) Marine-estuarine LC UFPB 9920
Ctenogobius boleosoma (Jordan & Gilbert, 1882) Marine-estuarine NE UFPB 9903
GYMNOTIFORMES
Gymnotidae
Gymnotus cf. darwini Campos-da-Paz & de Santana, 2019 Freshwater LC UFPB 10679
MUGILIFORMES
Mugilidae
Mugil curema Valenciennes, 1836 Marine-estuarine DD UFPB 11572
MYLIOBATIFORMES
Gymnuridae
Gymnura micrura (Bloch & Schneider, 1801) Marine-estuarine NT UFPB 11556
PERCIFORMES
Centropomidae
Centropomus undecimalis (Bloch, 1792) Marine-estuarine LC UFPB 11561
Gerreidae
Diapterus auratus Ranzani, 1842 Marine-estuarine LC UFPB 9919
Eucinostomus argenteus Baird & Girard, 1855 Marine-estuarine LC UFPB 11558
Eucinostomus gula (Quoy & Gaimard, 1824) Marine-estuarine LC UFPB 9902
Haemulidae
Haemulon aurolineatum Cuvier, 1830 Marine-estuarine LC UFPB 11568
Lutjanidae
Lutjanus alexandrei Moura & Lindeman, 2007 Marine-estuarine LC UFPB 11562
Lutjanus jocu (Bloch & Schneider, 1801) Marine-estuarine NT UFPB 9917
Pomacentridae
Abudefduf saxatilis (Linnaeus, 1758) Marine-estuarine LC UFPB 1566
Sphyraenidae
Sphyraena barracuda (Edwards, 1771) Marine-estuarine LC UFPB 11560
PLEURONECTIFORMES
Achiridae
Trinectes inscriptus (Gosse, 1851) Marine-estuarine LC UFPB 11571
Trinectes paulistanus (Miranda Ribeiro, 1915) Marine-estuarine LC UFPB 9922
Paralichthyidae
Citharichthys sp. Marine-estuarine NE UFPB 10671
Citharichthys spilopterus Günther, 1862 Marine-estuarine LC UFPB 9910
SILURIFORMES
Callichthyidae
Megalechis thoracata (Valenciennes, 1840) Freshwater NE UFPB 10654
SYNBRANCHIFORMES
Synbranchidae
Synbranchus aff. marmoratus Bloch, 1795 Freshwater NE UFPB 10658
SYNGNATHIFORMES
Syngnathidae
Microphis brachyurus (Bleeker, 1854) Marine-estuarine LC UFPB 9905
Syngnathus pelagicus Linnaeus, 1758 Marine-estuarine LC UFPB 9916
TETRAODONTIFORMES
Tetraodontidae
Sphoeroides spengleri (Bloch, 1785) Marine-estuarine LC UFPB 11557
Sphoeroides testudineus (Linnaeus, 1758) Marine-estuarine LC UFPB 9909

The most abundant freshwater species in the hydrographic basins in Tambaba Environmentally Protected Area are: Hemigrammus unilineatus (Gill, 1858) (32% of total collected specimens), Poecilia vivipara Bloch & Schneider, 1801 (27%) and Astyanax aff. bimaculatus (Linnaeus, 1758) (11%). Poecilia vivipara is a broadly distributed species that occurrs in 19 out of 29 sampling sites, and it is followed by Geophagus brasiliensis (Quoy & Gaimard, 1824) that occurs in 13 sampling sites and Astyanax bimaculatus and Hoplias aff. malabaricus (Bloch, 1794) in 12 sampling sites. Characiformes are the largest freshwater order with seven species (16% of total), with Characidae being the most speciose family represented by four autochthonous species. Cichliformes is the second largest freshwater order representing 9% of total collected species (n = 4), three autochthonous and one allochthonous species, all belonging to the family Cichlidae.

Atherinella brasiliensis (Quoy & Gaimard, 1825) (with 8%), Mugil curema Valenciennes, 1836 (3%), and Eucinostomus argenteus Baird & Girard, 1855 (3%) correspond to the most abundant estuarine-marine species. Perciformes is the largest marine-estuarine order, representing 20% (9 species) while Gobiiformes is the second largest order with 14% of total species (n = 6), of which Gobiidae is the most speciose family (n = 4) among the marine-estuarine representatives.

Other orders comprise Pleuronectiformes with 9%, Cyprinodontiformes, Tetraodontiformes and Syngnathiformes 5% each, Atheriniformes, Blenniiformes, Clupeiformes, Gymnotiformes, Myliobatiformes, Mugiliformes, Siluriformes and Synbranchiformes have one species each, representing 4% of the total species (Table 2).

Among the species recognized herein, none are currently classified as threatened species, according to the official list of threatened species of fishes and aquatic invertebrates from Brazil, Portaria MMA № 445, 17 December 2014, Ministério do Meio Ambiente (Brasil, 2014). Gymnura micrura (Bloch & Schneider, 1801), and Lutjanus jocu (Bloch & Schneider, 1801) are classified as Near Threatened (NT), and Cheirodon jaguaribensis, and Mugil curema are classified as Data Deficient (DD) (Brasil, 2014).

DISCUSSION

Freshwater fish species from Tambaba Environmentally Protected Area represent 16% (n = 15) of the 94 total species for the NCCD ecoregion (Oliveira-Silva et al., 2018). Studies that were previously carried out in the nearby areas such as Torelli et al. (1997) and Gomes-Filho & Rosa (2001) listed 22 and 21 freshwater species, respectively, in Gramame River basin within the NCCD ecoregion of the Atlantic forest biome. These authors recognized a higher number of freshwater species than those observed for Tambaba Environmentally Protected Area and this discrepancy is probably due to differences in the historical evolution factors of these drains or sampling efforts. Paiva et al. (2014) recognized 22 species of which 13 are freshwater species in the Pratagi River micro-basin in Rio Grande do Norte State, Brazil. Gouveia et al. (2017) registered 18 freshwater species, distributed within seven families and five orders in Guaribas Biological Reserve UC and surrounding areas from the Camaratuba River hydrographic basin. These studies are incongruent with the present analysis but it is noticed a similar number of species to that those registered for the coastal rivers of the Atlantic Forest in NCCD ecoregion.

Characiformes, Characidae is the most representative group among the freshwater fishes in the Tambaba APA. This result is congruent with previous studies on the freshwater ichthyofauna from the NCCD hydrographic basins (e.g.,Torelli et al., 1997; Ramos et al., 2005; Paiva et al., 2014; Silva et al., 2014; Rodrigues-Filho et al., 2016; Costa et al., 2017; Gouveia et al., 2017; Teixeira et al., 2017; Oliveira-Silva et al., 2018; Ramos et al., 2018). These results differ from the general pattern of dominance that is noticed for the NCCD ecoregion as provided in Lima et al. (2017); Siluriformes has the highest number of species (143 vs. 132 Characiformes). However, species of Characiformes dominate when each basin of the NCCD is evaluated individually as pointed out in Oliveira-Silva et al. (2018), and according to the authors the greatest number of Siluriformes for this ecoregion occurs due to the greater number of endemic species of this order for each individual basin that would explain the apparent dominance of Siluriformes when these numbers are put together.

The three most abundant freshwater species, Hemigrammus unilineatus, Astyanax bimaculatus (Characidae), and Poecilia vivipara (Poeciliidae), are small-sized autochthonous species. The first two species belong to the group commonly known as “piabas” (in Portuguese), which do not provide any commercial interest to most of the local population. Local fishermen often employ these species as bait for capturing larger species. The abundance of “piabas” is due to schooling behavior, which facilitates the collection of specimens in the field (Ramos, 2012). A small-sized species, Poecilia vivipara, popularly known as “guarú”, “guru” or “barrigudinho” also holds no commercial interest to local fishing communities. These three species combined correspond to 67% of the total captured specimens. Small-sized species are often used in the aquarium trade, as is the case for species from Characidae and Poeciliidae (Nelson, 2006; Magalhães & Jacobi, 2013), although this secondary activity was not observed within the Tambaba APA.

Hemigrammus unilineatus was recognized in coastal rivers from the Atlantic forest biome in the Brazilian northeast region (Buckup et al., 2007; Menezes et al., 2007; Langeani et al., 2009; Gouveia et al., 2017) even though the type-locality of this species is in Trinidad Island, West Indies (Reis et al., 2003). Historical relationships between the Atlantic and Amazonian forests explain the natural distribution of this species in the Brazilian northeast region (Wang et al., 2004; Menezes et al., 2007; Dagosta & de Pinna, 2017; Teixeira et al., 2017).

In the marine-estuarine ichthyofauna, Perciformes is one of the largest groups of the study area as previously observed in other Brazilian northeastern estuaries (e.g.,Teixeira & Falcão, 1992; Alves & Soares-Filho, 1996; Santos, 2000; Araújo et al., 2000; Paiva et al., 2008; Reis-Filho et al., 2010; Oliveira-Silva et al., 2008; Teixeira et al., 2017). Among the species recognized for this order, the occurrence of Centropomus undecimalis (known as “robalo-flexa” or “camorim”) must be highlighted due to its commercial importance such as it is noticed for most sea bass species in the artisanal, industrial and recreational fisheries (Fujimoto et al., 2009). This species occurs from North Carolina (U.S.A.) to Uruguay, including Gulf of Mexico and Caribbean Sea (Fricke et al., 2019).

Atherinella brasiliensis and Mugil curema, popularly known as “sauna” and “tainha” respectively, are the most abundant marine-estuarine species that also exhibit schooling behavior, which explains the large number of specimens collected. The former species is considered generalized, opportunistic omnivorous feeders in estuaries with tolerance to several distinct environmental conditions (Contente et al., 2011). The second species also tolerates environments with different levels of salinity since it is a migratory species inhabiting the ocean in adult stage and estuaries while juvenile that functioning as nursery areas (Carvalho et al., 2007). Abundance of these marine-estuarine species is also noticed in other estuarine areas from the Northeastern region of Brazil as seen in Reis-Filho et al. (2010), Costa & Camara (2012), Reis-Filho et al. (2012), and Campos et al. (2015). These species are of commercial importance to artisanal fisheries throughout the Brazilian coast (Soares-Filho et al., 2010).

The occurrence of Cichla monoculus, the “tucunaré”, is recorded in a single sampling site in Caboclo River, a tributary of Gurugi River in Conde municipality. The allochthonous species C. monoculus occurs originally along the riverbeds from the Rio Napo, Ucayali, Solimões-Amazonas, Araguari and Oiapoque (Reis et al., 2003). Species of Cichla have been largely introduced in the Brazilian hydrographic basins, especially in northeastern Brazil dams, through government fish breeding programmers and also in order to eliminate piranha species of Pygocentrus and Serrasalmus (Gurgel & Oliveira, 1987; Leão et al., 2011). They have also been introduced intensively by recreational fisheries and are possibly responsible for local extinctions of native species (Leão et al., 2011). Cichla comprises a genus of carnivorous species with very aggressive predation behavior (Leão et al., 2011), which might cause a reduction in the abundance and threat the diversity of native species from hydrographic basins in Tambaba Environmentally Protected Area.

Deforestation and civil construction areas are evident in the mangroves from the estuaries of Graú, Mucatú, and Bucatú Rivers. Mangroves correspond to merely 2.43 km² or 2.13% of the total area from Tambaba Environmentally Protected Area (Almeida et al., 2008), indicating a massive reduction of the native mangrove coverage when compared to other major hydrographic basins such as Mamanguape and Paraíba do Norte River basins, located in Paraíba State. Many marine fish species seasonally inhabit mangroves for feeding and reproduction while others utilize them permanently (Lowe-McConnell, 1999). Mangrove roots are often employed as nursery and refuge sites against predators for a variety of species for instance Lutjanus alexandrei Moura & Lindeman, 2007, L. jocu, Mugil curema, Sphoeroides testudineus (Linnaeus, 1758), and Sphyraena barracuda (Edwards, 1771) that are observed in Tambaba Environmentally Protected Area (Osório et al., 2011). Mangroves and estuaries from Tambaba APA (comprising the Mucatú, Bucatú, and Graú Rivers) require eminent conservation management due to its ecological role to the aquatic fauna as feeding, nursery, and home grounds (Thayer et al., 1987).

The Atlantic forest biome is one of the world biodiversity hotspots characterized by its high endemism and richness of species and habitats, although it is currently under risk of extinction (Myers et al., 2000). The ichthyofauna assessment of Tambaba Environmentally Protected Area demonstrates the diversity of species present within its coastal and hydrographic limits which is of major ecological and conservational value as it is situated within the Atlantic forest biome in the northeastern region of Brazil. This environmentally protected area is a national and international renowned region because its scenic nature landscapes. This region has been under considerable and fast-growing urban development for touristic purposes, especially in the hospitality industry. Besides that, the production of agricultural stocks such as banana, sugar cane and bamboo in the inner limits of Tambaba Environmentally Protected Area also contributes to environmental pressures, including intensive deforestation and deterioration (Almeida et al., 2008). Agricultural activities as well as livelihood in the region, including livestock, sediment extraction, and civil construction also entails anthropogenic impacts in the hydrographic basins and surrounding areas resulting in deforestation of the riparian forest in many rivers and streams. These latter two activities also contribute to the deposition of chemical waste in the river basins.

Forests with origin in river bases are considered permanently protected areas (APPs), according to the Brazilian Forest Code (Law № 12.651/2012). Thus, the conservation efforts of river sources as well as the riparian forest associated to it are essential for the natural maintenance of water springs. Restoration of the natural environments through environmental and conservation management is crucial in order to reach the natural stability from Tambaba Environmentally Protected Area as proposed in Meneses et al. (2005), Almeida et al. (2008), and Sobrinho Jr. & Araújo (2016). Finally, the results presented herein contribute to the taxonomic knowledge of the fish fauna from the Tambaba APA and more generally to the understanding of the ichthyological diversity of the NCCD ecoregion.

Acknowledgements

The authors thank Dr. Ricardo Rosa (UFPB) for supporting the access to data from the fish collection, Consultoria Ambiental Office 04 for the management plan in Tambaba Environmentally Protected Area, Ton Jones Anselmo for helping during field sampling, and Ana Carolina Figueiredo for borrowing a digital camera.

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Published with the financial support of the "Programa de Apoio às Publicações Científicas Periódicas da USP"

APPENDIX

Identification key to species from the Tambaba APA, Graú, Mucatú, and Bucatú river basins, Caboclo River sub-basin and Gurugi River basin in Paraíba State, Brazil

1. Gill slits ventrally located, dorsal and anal fins very reduced or absent ……................................ 2

1’. Gill slits laterally located, dorsal and/or anal fins well-developed ………..................................... 3

2. Five gill slits ventrally, body conspicuously depressed and disc shaped ………....... Gymnura micrura

2’. A single gill slit ventrally, body conspicuously eel-like ………................ Synbranchus marmoratus

3. Body lacking scales …….………………..................................................... Omobranchus punctatus

3’. Body with scales, bony plates or a series of articulated bony rings ………….................................. 4

4. Body covered by bony plates or series of articulated rings ……………….…………….................. 5

4’. Body covered by typical scales ……………….………………..................................................... 7

5. Body fusiform and covered by bony plates …………….................................... Megalechis thoracata

5’. Body tube-like and covered by series of articulated rings ……………….……............................... 6

6. 38-47 rays in dorsal fin, 24-30 rings in caudal region ……............................ Microphis brachyurus

6’. 27-28 rays in dorsal fin, 27-34 rings in caudal region ……………….…......... Syngnathus pelagicus

7. Fins with soft rays only ……………….………………................................................................ 8

7’. Fins with rigid (spines) and soft rays ……….………………..................................................... 23

8. Body markedly compressed and both eyes located on one side of the body ……………................. 9

8’. One eye on each side of the body ……………….………………..................................................... 12

9. Both eyes located on left side of body …………………………..................................................... 10

9’. Both eyes located on right side of body ……………….……………….......................................... 11

10. First dorsal-fin ray inserted above and adjacent to the anterior nostril on the blind side of the body ……………….………………..................................................... Citharichthys sp.

10’. First dorsal-fin ray inserted above and remote to the posterior nostril or equidistant to the two nostrils ……………….………………..................................................... Citharichthys spilopterus

11. Body brown and 10 to 11 transversal lines black in color present ……….... Trinectes paulistanus

11’. Body brown, transversal lines absent, light markings rounded, forming a mosaic …….. Trinectes inscriptus

12. Dorsal and pelvic fins absent, anal fin markedly elongate with more than 140 rays ......... Gymnotus carapo

12’. Dorsal and pelvic fins present, anal fin markedly small with less than 140 rays ……….............. 13

13. Premaxilla protruding, caudal fin not bifurcated ……………….………………............................ 14

13’. Premaxilla non-protruding, caudal fin bifurcated or not bifurcated …............................................. 16

14. Presence of a small and oval dark humeral spot ………......................................... Poecilia vivipara

14’. Absence of a small and oval dark humeral spot ……………….…………................................ 15

15. Lateral region of body with many colorful spots …………...................... Poecilia reticulata (male)

15’. Lateral region of body without colorful spots ………………............... Poecilia reticulata (female)

16. Lateral line and adipose fin absent ….......................................................... Lycengraulis grossidens

16’. Lateral line and adipose fin presents ……………….………………............................................ 17

17. Adipose fin absent and caudal fin rounded ……………….……………….................................... 18

17. Adipose fin present and caudal fin forked ……………….………………...................................... 19

18. Maxilla with conical teeth only ……………..................................................... Hoplias malabaricus

18’. Maxilla with conical and canine teeth …………............................................... Erythrinus erythrinus

19. Abdomen compressed, forming a keel prior to the pelvic fins ….................. Metynnis lippincottianus

19’. Abdomen rounded not forming a keel prior to the pelvic fins ……………….…......................... 20

20. Premaxilla with a single series of teeth ……………….…………...................... Compsura heterura

20’. Premaxilla with two series of teeth ……………….………......................................................... 21

21. Lateral line complete ……………….………................................................. Astyanax bimaculatus

21’. Lateral line incomplete ……………….………………................................................................ 22

22. Blackish marking on the caudal peduncle or under the median caudal rays present, dorsal and hyaline fins with black vertical bar absen………..................................................... Cheirodon jaguaribensis

22’. Blackish marking on the caudal peduncle absent, dorsal and anal fins with black vertical bar presents ……………….………………........................................................... Hemigrammus unilineatus

23. Pelvic fins absent ……………….………………......................................................................... 24

23’. Pelvic fins present ……………….………………....................................................................... 25

24. Dermal appendix present dorsal and laterally on body ………...................... Sphoeroides spengleri

24’. Dermal appendix absent ………………..................................................... Sphoeroides testudineus

25. Pelvic fins fused, forming a suction disk ……………….………………....................................... 26

25’. Pelvic fins not fused and not forming a suction disk ……………….………….......................... 29

26. Eight to nine rays in anal fin ……………..................................................... Bathygobius soporator

26’. More than 10 rays in anal fin ……………….………………..................................................... 27

27. Eleven rays in anal fin ……………….………………............................................. Awaous tajasica

27’. More than 11 rays in anal fin ……………….………………..................................................... 28

28. Dorsal fin with six spines and 14 rays ……………................................... Ctenogobius boleosoma

28’. Dorsal fin with six spines and 12 rays, anal fin with 13 rays ………................ Evorthodus lyricus

29. Lateral line absent ……………….…………...................……..................................................... 30

29’. Lateral line present ……………….…………….................…..................................................... 33

30. Caudal fin bifurcated ……………….…………...............……..................................................... 31

30’. Caudal fin rounded ……………….……..................…………..................................................... 32

31. Silver bar present horizontally, one spine and 17-19 rays in anal fin …........ Atherinella brasiliensis

31’. Silver horizontal bar absent, 2-3 spines and nine or 10 rays in anal fin ...................... Mugil curema

32. 29-31 rows of longitudinal scales on body ……………….………………...... Dormitator maculatus

32’. 57-64 rows of longitudinal scales on body ……………….……………….............. Eleotris pisonis

33. Lateral line discontinuous with upper (anterior) and lower (posterior) branches ……………... 34

33’. Lateral line continuous ……………….……………….............................................................. 37

34. Dorsal fin incised between anterior and posterior portions ……………….......... Cichla monoculus

34’. Dorsal fin without a fork between anterior and posterior portions ……………….…………….. 35

35. Upper branch of first gill slit with prominent lobe, black vertical bar over the eye present, reaching the corner of preopercle ……………….………………...................................... Geophagus brasiliensis

35’. Upper branch of first gill slit without prominent lobe, black vertical bar over the eye absent ....... 36

36. Body elongated and fusiform, posterior margin of preopercle serrated ........... Crenicichla brasiliensis

36’. Body tall and oval, posterior margin of preopercle straight …................... Cichlasoma orientale

37. Caudal fin truncate ……………….………………................................................................... 38

37’. Caudal fin bifurcated ……………….……………….............................................................. 39

38. Six scales between the dorsal fin origin and the lateral line ………………... Lutjanus alexandrei

38’. Nine to 10 scales between the dorsal fin origin and the lateral line ………............. Lutjanus jocu

39. Body elongate with two dorsal fins present ……………….………………................................ 40

39’. Body tall with one dorsal fin present ……………….………………......................................... 41

40. Mouth with large canine teeth, two spines and 8-9 rays in anal fin ……….. Sphyraena barracuda

40’. Mouth with villous teeth, three spines and 5-6 rays in anal fin ………. Centropomus undecimalis

41. Three spines in anal fin ……………….……………….............................................................. 42

41’. Two spines or spines absent in anal fin ……………….……………...................................…. 44

42. Margin of preopercle straight ……………….………………..................................................... 43

42’. Margin of preopercle with small dentations ……………….…....……………. Diapterus auratus

43. Premaxilla furrow discontinuous anteriorly by scales …………….....………. Eucinostomus gula

43’. Premaxilla furrow continuous not interrupted anteriorly by scales ….... Eucinostomus argenteus

44. Two spines in anal fin, dorsal-fin rays without scales ……………....………. Abudefduf saxatilis

44’. Anal fin without spines, dorsal-fin rays completely covered of scales .…. Haemulon aurolineatum

Received: April 19, 2019; Accepted: August 26, 2019

Edited by: Fernando César Paiva Dagosta

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