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Fishes from the Itapecuru River basin, state of Maranhao, northeast Brazil/Peixes da bacia do Rio Itapecuru, Estado do Maranhao, nordeste do Brasil.

1. Introduction

The Itapecuru River basin is a relatively large coastal drainage system in northeastern Brazil. It is situated in the mid-east of the state of Maranhao, between latitudes 2[degrees] 51 S and 6[degrees] 56 S, and longitudes 43[degrees] 02 W and 43[degrees] 58 W. It encompasses a total area of 52,972.1 [km.sup.2], corresponding to approximately 16% of the state. The Itapecuru River is limited to the southeast mainly by the Parnaiba basin, the Itapecuru mountains and the Azeitao plateau, to the southwest by the Mearim basin and to the northeast by the Munim basin. The Itapecuru River has three physically distinct areas. The upper Itapecuru, from its source to the east of the town of Colinas, is dominated by plains, plateaus and cuestas and has a strongly undulating relief rising to 350 m a.s.l. in the Itapecuru, Alpercatas, Croeira, and Boa Vista ranges. The middle Itapecuru from Colinas to Caxias is in an area of low plateaus with gently to strongly undulating relief and many plateaus, with a difference of 60 m altitude. The lower Itapecuru, from Caxias to its mouth in the Bay of Sao Jose, is characterized by gently undulating relief with low plateaus (Alcantara, 2004).

Little is known about the ichthyofauna of the Itapecuru, although the adjoining basins of the Parnaiba and Pindare-Mearim Rivers have been relatively well sampled. The first naturalists to set eyes on the Itapecuru were actually Spix and Martius, but they merely used the waterway to navigate from Caxias to the state capital, Sao Luiz in June, 1819 (Papavero, 1971). The first freshwater fish species described from northeast Brazil were based primarily on specimens collected in the Parnaiba River basin during the Thayer Expedition, headed by Louis Agassiz from the Museum of Comparative Zoology of Harvard University. The specimens were all collected by Orestes St. John, between October and December, 1865 at locations labeled as "Lagoa de Parnagua, Piaui", "Parnahyba River basin", "Puty River, Theresina" and "Gurgeia River, Piaui" (Higuchi, 1996). The species described from specimens collected during this field trip were described by Garman (1890a, b, 1913), Steindachner (1877, 1881), Eigenamnn and Eigenmann (1889), Eigenmann and Henn (1916) and Borodin (1931). Another large collection from the Parnaiba River basin was compiled by Steindachner in 1903 and resulted in a considerable amount of publications and species descriptions (Steindachner, 1906, 1907, 1908a, b, 1909, 1910). In 1903, Haseman, in a field trip to the area, was the first to collect specimens of fish in the Itapecuru near Caxias. His material was used by Steindachner (1915), who described Otocinclus hasemani, and by Nijssen (1971) who described Corydoras blichi vittatus.

The most comprehensive contribution to the scientific knowledge of the fish species of the Brazilian Northeast is the study of Fowler (1941), who analyzed material collected at several sites by Rodolpho von Ihering, one of the pioneers of pisciculture in Brazil. Von Ihering's collection contained 823 specimens representing approximately 104 species, 36 of which were described by Fowler (1941). Many specimens were from Ceara, Lago Papary in Rio Grande do Norte, the Jaguaribe and Sao Francisco rivers in Pernambuco, and Teresina in Piaui. Fowler's (1941) paper included his drawings and the vernacular names recorded by R. von Ihering. As noted by Rosa et al. (2003), Fowler's species names are often synonyms--e.g., Hassar woodi and Hassar iheringi, which are both synonymies of Hassar affinis Steindachner--while some descriptions are based exclusively on small juveniles (e.g., Ancistrus salgadae, with approximately 2 cm SL). A recent survey of the Mearim River in Maranhao recorded 60 species (Soares, 2005).

[FIGURE 1 OMITTED]

The aim of the present paper is to present and comment on an inventory of fish species from the Itapecuru basin in the Brazilian state of Maranhao.

2. Material and Methods

Specimens of fish were collected during eight field expeditions (each of approximately five days duration) to the lower, middle and upper section of the Itapecuru River (Figure 1). Three locations were sampled on the lower Itapecuru, one near the town of Rosario (02[degrees] 55' 60" S and 44[degrees] 14' 60" W), one at Itapecuru-Mirim (03[degrees] 31' 39" S and 44[degrees] 24' 19" W) and the third near Aldeias Altas (04[degrees] 44' 09" S and 43[degrees] 27' 54" W). On the middle section of the river, two sites were sampled near Caxias (05[degrees] 02' 44" S and 43[degrees] 24' 45" W and 05[degrees] 07' 33" S and 43[degrees] 33' 60" W), and one at 05[degrees] 26' 37" S and 43[degrees] 52' 03" W near the town of Governador Eugenio Barros. The upper stretch was sampled at 06[degrees] 22' 26" S and 44[degrees] 22' 60" W in the proximity of Mirador and near the town of Colinas town (06[degrees] 01' 60" S and 44[degrees] 18' 60" W). Additional sampling was conducted in tributaries, targeting mainly small-sized fishes.

Fish were captured using gillnets (15-35 mm meshes), cast nets (12-35 mm meshes), and hand nets (5 mm mesh). Specimens were transported on ice to the laboratory, where they were preserved in 10% formalin solution and finally conserved in 70% ethanol. The specimens were deposited under the numbers 104552-104603 in the fish collection of the Museu de Zoologia da Universidade de Sao Paulo, in Sao Paulo, and at the Universidade Estadual do Maranhao, CESC in Caxias.

The diversity of species was estimated using the Shannon-Wiener diversity index (H'), and the uniformity of the distribution of the species was assessed using the equitability index (Krebs, 1998a, b).

3. Results

A total of 1563 specimens were collected, representing 69 species, 65 genera, 29 families and 10 orders. Characiformes, with 24 species and Siluriformes with 25, were the richest species orders. Characidae, with 13 species, Loricariidae with seven, Cichlidae, Pimelodidae, and Auchenipteridae, all with five, were the richest species families (Table 1).

The maximum possible diversity for the 69 species collected from the Itapecuru River would be 6.108 bit per individual, although our results returned a diversity of 5.025 bits per individual with an equitability of 0.822, which indicates a high diversity, but with a certain degree of homogeneity among the species collected in the basin. Both diversity (H') and equitability (E) were highest on the mid Itapecuru in November, 2007 (H' = 4.334, E = 0.885), which is the dry season. The lowest values were recorded in the upper part of the river in the wet season, in March 2008 (H' = 3.226, E = 0.678). The largest number of specimens (644) and species (55) was collected in the lower Itapecuru, followed by the mid section, with 540 specimens and 36 species, and the upper river, with 411 specimens belonging to 29 species.

4. Discussion

The fish fauna in the Itapecuru River comprises 69 species, of which 20 or approximately 30%, are endemic to northeastern Brazil, known to occur from the Pindare-Mearim Rivers in Maranhao to the Jaguaribe River in Ceara (see Table 1). One species, Oreochromis niloticus, is an introduced African cichlid. A few species are known to be widespread, occurring in several South American river basins: Astyanax bimaculatus, Hoplias malabaricus, Apteronotus albifrons, Sternopygus macrurus, Arius rugispinis, Hexanematichthys couma, Ageneiosus inermis, Parauchenipterus galeatus, Pseudauchenipterus nodosus, Callichthys callichthys, Hemisorubim platyrhynchus, Pimelodus blochii, Pimelodus ornatus, Sorubim lima, Centropomus parallelus, Plagioscion squamosissimus, and Synbranchus marmoratus. Some of these species (e.g., Astyanax bimaculatus or Synbranchus marmoratus) may represent species complexes, rather than distinct taxa, and are in need of taxonomic revision. A number of other species are known to occur in the Amazon basin (in some cases ranging as far as the Orinoco and coastal rivers in Surinam and the Guyanas), a distribution pattern predicted by Agassiz and Agassiz (1975). This is the case of Poptella compressa, Pygocentrus nattereri, Serrasalmus rhombeus, Cynodon gibbus, Hemiodus argenteus, Aspredo aspredo, Ageneiosus ucayalensis, Hemiodontichthys acipenserinus, Loricariichthys acutus, Pterygoplichthys punctatus, Pseudoplatystoma punctifer, Strongylura marina, Anchovia surinamensis, Pterengraulis atherinoides, Anableps anableps, and Pachypops fourcroi. The present register of the latter three species are new records for northeastern Brazil (Casatti, 2002; Ghedotti, 2003; Kullander and Ferraris, 2003). Fifteen taxa could not be identified to the species level due to the poor taxonomic resolution. A few of these are new records for northeastern Brazil and may even represent undescribed species. Pseudopimelodus sp. is the first Pseudopimelodidae known to occur in the region (Shibatta, 2003), while the specimens of Serrapinnus sp., Aphyocharax sp., and Hypoptopoma sp. represent new records for these genera.

Several species (Apionichthys dumerili, Anableps anableps, Centropomus parallelus, Strongyrula marina, Anchovia surinamensis, Pterengraulis atherinoides, and Pseudauchenipterus nodosus) were only collected on the lower Itapecuru, indicating a preference for estuarine environments.

This is a first systematic inventory of the ichthyofauna of the Itapecuru River. Most of the coastal rivers of the Brazilian Northeast are still poorly known. Due to the predominance of Amazonian species in the Itapecuru basin, it might be predicted that the region's fish fauna becomes more species-rich towards the Amazon delta, i.e., present an east to west gradient of species richness.

Acknowledgements--This study was supported by the Banco do Nordeste do Brasil S/A (BNB/FUNDECI) and the Fundacao de Amparo a Pesquisa e ao Desenvolvimento Cientifico e Tecnologico do Maranhao (FAPEMA). We would like to thank the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renovaveis for authorization to collect specimens (IBAMA special license n. 02012.004159/2006), Whister Brito and students (Deborah Aragao, Ligia Silva, Francineto Reis, Katiana Santos, Cleydson Almeida, Samara Silva, Rosiane Santos and Suellen Santos) from the Genetics and Molecular Biology laboratory for collecting and identifying some specimens, and Janice Muriel Cunha for putting UEMA in contact with MZUSP.

References

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ALCANTARA, EH., 2004. Caracterizacao da bacia hidrografica do Rio Itapecuru, Maranhao. Caminhos de Geografia, vol. 7, no. 11, p. 97-113.

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CASATTI, L., 2002. Taxonomy of the South American genus Pachypops Gill, 1861 (Teleostei: Perciformes: Scianidae), with the description of a new species. Zootaxa, vol. 26, p. 1-20.

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FOWLER, HW., 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Academy of Natural Sciences Philadelphia, vol. 93, p. 123-199.

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ROSA, RS., MENEZES, NA., BRITSKI, HA., COSTA, WJEM. and GROTH, F., 2003. Diversidade, padroes de distribuicao e conservacao dos peixes da caatinga. In LEAL, IR., TABARELLI, M. and SILVA, JMC. (Eds.). Ecologia e conservacao da Caatinga. Recife: Editora Universitaria, UFPE. p. 135-181.

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--, 1906. Ueber zwei neue Corydoras--Arten aus dem Parnahyba und Parahimflusse im Staate Piauhy. Anzeiger Akademie der Wissenschaften in Wien, vol. 43, p. 478-480.

--, 1907. Uber eine neue Psilichthys-Art, Ps. cameroni aus dem Flusse Cubatao im Staate S. Catharina, Brasilien. Anzeiger Akademie der Wissenschaften in Wien, vol44, no. 6, p. 82-85.

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Barros, MC. (a) **, Fraga, EC. ** and Birindelli, JLO. (b)

(a) Laboratorio de Genetica e Biologia Molecular, Centro de Estudos Superiores de Caxias, Universidade Estadual do Maranhao--UEMA, Praca Duque de Caxias, s/n, CEP 65604-380, Caxias, MA, Brazil

(b) Museu de Zoologia, Universidade de Sao Paulo--USP, Av. Nazare, 481, CEP 04263-000, Sao Paulo, SP, Brazil

* e-mail: mbdene@yahoo.com.br, elmaryfraga@yahoo.com.br

Received December 14, 2009--Accepted May 26, 2010--Distributed May 31, 2011 (With 1 figure)
Table 1. List of species of fishes collected in the
Itapecuru River basin.

CHARACIFORMES
  Acestrorhynchidae   Acestrorhynchus cf. lacutris
  Anostomidae         Leporinus piau *
                      Schizodon dissimilis *
  Characidae          Aphyocharax sp.
                      Astyanax bimaculatus
                      Charax sp.
                      Hemigrammus sp.
                      Metynnis sp.
                      Myloplus sp.
                      Poptella compressa
                      Pygocentrus nattereri
                      Roeboides margaretae *
                      Roeboides sazimai *
                      Serrapinnus sp.
                      Serrasalmus rhombeus
                      Triportheus signatus *
  Crenuchidae         Characidium bimaculatum *
  Curimatidae         Curimata macrops *
                      Psetrogaster rhomboides *
                      Steindachnerina notonota *
  Cynodontidae        Cynodon gibbus
  Erythrinidae        Hoplias malabaricus
  Hemiodontidae       Hemiodus argenteus
  Prochilodontidae    Prochilodus lacustris *

GYMNOTIFORMES
  Apteronotidae       Apteronotus cf. albifrons
  Rhamphichtyidae     Rhamphichthys atlanticus *
  Sternopygidae       Sternopygus macrurus

SILURIFORMES
  Ariidae             Arius rugispinis
                      Hexanematichthys couma
  Aspredinidae        Aspredo aspredo
  Auchenipteridae     Ageneiosus inermis
                      Ageneiosus ucayalensis
                      Auchenipterus menezesi *
                      Parauchenipterus galeatus
                      Pseudauchenipterus nodosus
  Callichthyidae      Callichthys callichthys
                      Corydoras sp. *
  Doradidae           Hassar affinis *
                      Platydoras brachylechis *
  Heptapteridae       Pimelodella parnahybae *
  Loricariidae        Ancistrus sp.
                      Hemiodontichthys cf. acipenserinus
                      Hypoptopoma sp.
                      Hypostomus sp.
                      Loricaria sp.
                      Loricariichthys acutus
                      Pterygoplichthys cf. punctatus
  Pimelodidae         Hemisorubim platyrhynchus
                      Pimelodus blochii
                      Pimelodus ornatus
                      Pseudoplatystoma cf. punctifer
                      Sorubim lima
BELONIFORMES
  Belonidae           Strongylura marina

CLUPEIFORMES
  Engraulidae         Anchoviella iheringi
                      Anchovia surinamensis
                      Pterengraulis atherinoides

CYPRINODONTIFORMES
  Anablepidae         Anableps anableps

PERCIFORMES
  Centropomidae       Centropomus parallelus
  Cichlidae           Cichlasoma orientale *
                      Crenicichla sp. *
                      Crenicichla menezesi *
                      Geophagus parnaibae *
                      Satanoperca sp.
                      Oreochromis niloticus **
  Scianidae           Pachypops fourcroi
                      Plagioscion squamossisimus

PLEURONECTIFORMES
  Anchiridae          Apionichthys dumerili

SYNBRANCHIFORMES
  Synbranchidae       Synbranchus marmoratus

MUGILIFORMES
  Mugilidae           Mugil incilis

* Indicates species endemic to northeastern Brazil;
** indicates introduced species.
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Author:Barros, M.C.; Fraga, E.C.; Birindelli, J.L.O.
Publication:Brazilian Journal of Biology
Date:May 1, 2011
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