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Ichthyofauna of Trairí river basin, Rio Grande do Norte state, northeastern Brazil: a century after the study of the naturalist Edwin Starks in the Papari lagoon

Abstract

Fishes from the coastal basins of the Mid-Northeastern Caatinga ecoregion (MNCE) were first sampled by the Stanford expedition at the beginning of the 20th century, and published by Edwin C. Starks in 1913. This material included specimens from the Papary lake (= Papari lagoon) in the lower portion of the Trairí river basin, draining towards the eastern coast of Rio Grande do Norte State. In 1941, Henry Fowler provided a broad taxonomic study of the freshwater fishes from northeastern Brazil, including material from the Papari lagoon, besides describing four species assigned to this locality. However, these previous surveys focused only in the lower portion of the Trairí river basin and might be incomplete. Given this framework, the present study aimed at perform a wide ichthyofaunal inventory of Trairí river basin and compare with previously surveys performed in the regions. In 2013 and 2014, four expeditions along the whole basin, including the Papari lagoon itself, resulted in 28 species of fishes belonging to 17 families and seven orders. At Papari lagoon area 16 species were registered whereas 26 and 18 species were recorded by Starks and Fowler’s studies, respectively. Considering all records, 50 species were documented in the basin with 14 (28%) new records, including Serrapinnus potiguar, whose distribution was extended to the south. Two species described by Fowler, Pimelodella papariae and Pseudancistrus papariae, were not found in this study or in any fish collection, and are only known from their type-material. These two species can be naturally rare, locally extinct, or there were inaccuracies in their type-locality. However, species of these genera are only found in larger basins of the MNCE, which drains to the north, corroborating the latter assumption. Although not being a definitive list, the recent extensive fish surveys conducted in the MNCE’s coastal basins are helping to elucidate species’ geographic distribution and little knowing taxonomic issues.

Key-Words
Mid-Northeastern Caatinga Ecoregion; Freshwater fishes; Coastal basins; Semiarid

INTRODUCTION

The Mid-Northeastern Caatinga Ecoregion (MNCE), composed by coastal basins fully or partially inserted in the semiarid, was a knowledge gap in the diversity of freshwater fishes until recently (Lévêque et al., 2008Lévêque, 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.; Langeani et al., 2009Langeani, F.; Buckup, P.A.; Malabarba, L.R.; PY-Daniel, L.H.R.; Lucena, C.A.; 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: Rocha, R.M. & Boeger, W.A.P. (Orgs.). Estado da arte e perspectivas para a zoologia no Brasil. Curitiba, Editora da Universidade Federal do Paraná. p. 211-230.; Lima et al., 2017Lima, S.M.Q.; Ramos, T.P.A.; da Silva, M.J. & Rosa, R.S. 2017. Diversity, distribution, and conservation of the Caatinga fishes: advances and challenges. In: Silva, J.M.C.; Leal, I.R.; Tabarelli, M. (Orgs.). Caatinga the largest tropical dry forest region in South America. Springer. p. 97-131. Disponível em: https://link.springer.com/chapter/10.1007/978-3-319-68339-3_4.
https://link.springer.com/chapter/10.100...
). However, in the last decade many ichthyofaunal surveys and taxonomic studies were conducted in the ecoregion (Gurgel-Lourenço et al., 2013Gurgel-Lourenço, R.C.; Sousa, W.A.; Sánchez-Botero, J.I. & Garcez, D.S. 2013. Ichthyofauna of two reservoirs in the middle Acaraú River basin, Ceará, Northeastern Brazil. Check List, 9(6): 1391-1395.; Novaes et al., 2013Novaes, J.L.C.; Moreira, S.I.L.; Freire, C.E.C.; Sousa, M.M.O. & Costa, R.S. 2013. Fish assemblage in a semi-arid Neotropical reservoir: composition, structure and patterns of diversity and abundance. Brazilian Journal of Biology, 74(2): 290-301.; Paiva et al., 2014Paiva, R.E.C.; Lima, S.M.Q.; Ramos, T.P.A. & Figueiredo, L.M. 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.; Silva et al., 2014Silva, 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 Neotropica, 14(3): 1-6., 2017Silva, M.J.; Neves, C.P.; Ramos, T.P.A.; Pinto, M.P. & Lima, S.M.Q. 2017. Efetividade das unidades de conservação para a ictiofauna das bacias hidrográficas envolvidas na transposição do rio São Francisco. In: Mantovani, W.; Monteiro, R.F.; Anjos, L. dos & Cariello, M. (Orgs.). Pesquisas em unidades de conservação no domínio da Caatinga: subsídios à gestão. Fortaleza, Editora da Universidade Federal do Ceará. p. 181-205.; Botero et al., 2014Botero, J.I.S.; Garcez, D.S.; Cascon, P.; Lima, S.M.Q.; Brito, L.B.M. & Roberto, I.J. 2014. Anfíbios e peixes do Parque Nacional de Ubajara e entorno. Fortaleza, UFC/LABOMAR/NAVE.; Lira et al., 2015Lira, M.G.S.; Paiva, R.E.C.; Ramos, T.P.A. & Lima, S.M.Q. 2015. First record of Kryptolebias hermaphroditus Costa, 2011 (Cyprinodontiformes: Rivulidae) in the extreme north Atlantic Forest mangroves, Rio Grande do Norte state, Brazil. Check List, 11(3): 1656.; Ramos et al., 2013Ramos, T.P.A.; Barros-Neto, L.F.; Britski, H.A. & Lima, S.M.Q. 2013. Parotocinclus seridoensis, a new hypoptopomatine catfish (Siluriformes: Loricariidae) from the upper rio Piranhas-Açu basin, northeastern Brazil. Neotropical Ichthyology, 11(4): 787-796., 2016Ramos, T.P.A.; Lehmann A.P.; Barros-Neto, L.F. & Lima, S.M.Q. 2016. Redescription of the endangered hypoptopomatine catfish Parotocinclus spilurus (Fowler, 1941) (Siluriformes: Loricariidae) from the upper rio Jaguaribe basin, northeastern Brazil. Neotropical Ichthyology, 14(1): e150098., 2017Ramos, T.P.A; Zawadzki, C.H.; Ramos, R.T.C. & Britski, H.A. 2017. Redescription of Hypostomus johnii, a senior synonym of Hypostomus eptingi (Siluriformes: Loricariidae), Northeastern Brazil. Neotropical Ichthyology, 15(2): e160064.; Britzke et al., 2016Britzke, R.; Nielsen, D. & Oliveira, C. 2016. Description of two new species of annual fises of Hypsolebias antenori species group (Cyprinodontiformes: Rivulidae), from Northeast Brazil. Zootaxa, 4114(2): 123-138.; Rodrigues-Filho et al., 2016Rodrigues-Filho, C.A.S.; Gurgel-Lourenço, R.C.; Bezerra, L.A.V.; Sousa, W.A.; Garcez, D.S.; Lima, S.M.Q.; Ramos, T.P.A. & Sánchez-Botero, J.I. 2016. Ichthyofauna of the humid forest enclaves in the tablelands of Ibiapaba and Araripe, Northeastern Brazil. Biota Neotropica, 16(4): e20160273.; Teixeira et al., 2017Teixeira, F.K.; Ramos, T.P.A.; Paiva, R.E.C.; Távora, M.A.; Lima, S.M.Q. & Rezende, C.F. 2017. Ichthyofauna of Mundaú river basin, Ceará State, Northeastern, Brazil. Biota Neotropica, 17(1): e20160174.; Zawadzki et al., 2017Zawadzki, C.H.; Ramos, T.P.A. & Sabaj, M. 2017. Hypostomus sertanejo (Siluriformes: Loricariidae), new armoured catfish species from north‐eastern Brazil. Journal of Fish Biology, 91: 317-330.; Costa et al., 2017Costa, S.Y.L.; Viana, L.G.; Barbosa, J.E.L. & Ramos, T.P.A. 2017. Composition of the ichthyofauna in Brazilian semiarid reservoirs. Biota Neotropica, 17(3): 1-11.; Lima et al., 2017Lima, S.M.Q.; Ramos, T.P.A.; da Silva, M.J. & Rosa, R.S. 2017. Diversity, distribution, and conservation of the Caatinga fishes: advances and challenges. In: Silva, J.M.C.; Leal, I.R.; Tabarelli, M. (Orgs.). Caatinga the largest tropical dry forest region in South America. Springer. p. 97-131. Disponível em: https://link.springer.com/chapter/10.1007/978-3-319-68339-3_4.
https://link.springer.com/chapter/10.100...
). One of the first fish collections at the MNCE was undertaken by the Stanford Expedition in 1911 when a few drainages in Ceará and Rio Grande do Norte states were sampled (Starks, 1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.). Among the sampled locations was the Papary lake (or ‘Lago Papari’), located at the lower stretch of the Trairí river basin, draining to the eastern coast of Rio Grande do Norte State. Known since the 16th century, its native name means “fish jump”, emphasizing the abundance of fish (Ferreira, 2011Ferreira, F.R.F. 2011. De Papary à (Dio) Nísia: cidade e mulher. Imburana. Revista do núcleo Câmara Cascudo de estudos Norte-Rio-Grandenses, 2: 25-37.). In the vicinity of the lagoon, in Nísia Floresta Municipality, there was established a fishermen community which was mentioned by Edwin Chapin Starks (1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.) as responsible for the large fish collection at this locality.

Later, Fowler (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.) provided a taxonomic study on the fishes collected by Rodolpho von Ihering in many localities throughout northeastern Brazil in 1936 and 1937, including the Papari lagoon. In such study many species were described and four of them had their type-locality assigned to the Papari lagoon: Hypostomus papariae (Fowler), Pimelodella papariae (Fowler), Pseudancistrus papariae Fowler, and Psectrogaster saguiru Fowler (Fowler, 1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.). However, previous surveys focused only in the lower portion of the Trairí river basin and might have been incomplete. Besides that, our surveys provide fresh specimens from an historically important type-locality that might allow important material for future taxonomic reviews and molecular systematic studies. Thus, the main purpose of the present study is to provide a reliable ichthyofaunal inventory of the Trairí river basin and compare the results with those obtained by Starks (1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.) and Fowler (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.). Furthermore, some hypotheses concerning incongruences on the occurrence of some species described by Fowler were provided.

MATERIAL AND METHODS

Study area

The Trairí river basin has an approximate area of 2.900 km², of which 99.63% are inserted in Rio Grande do Norte State (RN) and a small fraction of its upper portion in Paraíba State (ANA/SGI, 2014Agência Nacional de Águas (ANA)/Superintendência de Gestão da Informação (SGI). 2014. Unidades Hidrográficas Estaduais. Available at: Available at: http://metadados.ana.gov.br/geonetwork/srv/pt/main.home . Access in: 15/09/2015.
http://metadados.ana.gov.br/geonetwork/s...
) (Fig. 1). It is located in the northeastern portion of the MNCE (Fig. 1), which is characterized by temporary rivers and lower species richness in comparison to the adjacent ecoregions, notwithstanding its high endemism (Albert et al., 2011Albert, J.S.; Petry, P. & Reis, R.E. 2011. Major biogeographic and phylogenetic patterns. In: Albert, J.S. & Reis, R.E. (Eds.). Historical biogeography of neotropical freshwater fishes. Berkeley, University of California Press. p. 21-58.). The main course of the Trairí river emerges at Serra do Doutor (in Campo Redondo and Coronel Ezequiel municipalities, in RN) and flows to Guaraíras lagoon between Tibau do Sul and Senador Georgino Avelino municipalities, also in RN (IBGE, 1990Instituto Brasileiro de Geografia e Estatística (IBGE). 1990. Divisão Regional do Brasil em Mesorregiões e Microrregiões Geográficas. Rio de Janeiro, Fundação Instituto Brasileiro de Geografia e Estatística - IBGE. v. 1.). About 88% of the basin lies within the Caatinga and the remaining in the Atlantic Forest (ANA/SGI, 2014Agência Nacional de Águas (ANA)/Superintendência de Gestão da Informação (SGI). 2014. Unidades Hidrográficas Estaduais. Available at: Available at: http://metadados.ana.gov.br/geonetwork/srv/pt/main.home . Access in: 15/09/2015.
http://metadados.ana.gov.br/geonetwork/s...
). Rains are more abundant in the coast, varying from 1,300 mm annually at the estuary to 500 mm in Santa Cruz municipality (“Agreste” portion of RN), and 700 mm close to the river’s headwaters (SERHID, 2001Secretaria de Recursos Hídricos do Estado do Rio Grande do Norte (SERHID). 2001. Plano estadual de recursos hídricos, Bacia 10 - Trairí. Available at: Available at: http://adcon.rn.gov.br/ACERVO/IGARN/DOC/DOC00000028905 . Access in: 11/05/2015.
http://adcon.rn.gov.br/ACERVO/IGARN/DOC/...
).

Figure 1
Map of sampling sites of the ichthyofaunal survey in Trairí river coastal basin, Rio Grande do Norte State, northeastern Brazil.

Sampling design

Four expeditions were conducted between October 2013 and August 2014 during dry and rainy seasons, consisting of 27 sampling locations (Fig. 1 and Table 1) from the upper stretch to the lower portion of Trairí river basin. The sampling sites marked with an asterisk in Table 1 were at the border of the Papari lagoon.

Table 1
Sampled locations and municipalities in Trairi river coastal basin. All sites are within Rio Grande do Norte state, Brazil. * Sampling sites at the Papari lagoon.

Samplings were done during the day and, occasionally at night, under collection permit 30532-1/2011 from Instituto Chico Mendes de Conservação da Biodiversidade/Sistema de Autorização e Informação em Biodiversidade - ICMBio/SISBIO) and applying the AquaRAP methodology (Rapid Assessment Protocol in Aquatic Systems) proposed by Alonso & Willink (2011Alonso, L.E. & Willink, P. 2011. History and overview of AquaRAP. In: Alonso, L.E.; Deichmann, J.L.; Mckenna, S.A.; Naskrecki, P. & Richards, S.J. (Eds.). Biodiversity exploration for conservation - the first 20 years of the Rapid Assessment Program. Arlington, Conservation International. p. 80-90.). Fishes were collected using active sampling gear, such as trawl (4.1 × 2.2 m and 5.0 mm), sieve (0.8 m × 0.5 mm), cast net (1.5 m × 12.0 mm), and gill nets as passive sampling gear to embody the highest number of microhabitats and reduce method selectivity (Uieda & Castro, 1999Uieda, V.S. & Castro, R.M.C. 1999. Coleta e fixação de peixes de riachos. In: Caramaschi, E.P.; Mazzoni, R.; Bizerril, C.R.S.F. & Peres-Neto, P.R. (Eds.). Oecologia Brasiliensis Ecologia de Peixes de Riachos. Rio de Janeiro, UFRJ/PPGE. p. 1-22. (Série Oecologia Brasiliensis, v. 6); Sabino, 1999Sabino, J. 1999. Comportamento de peixes em riachos: métodos de estudo para uma abordagem naturalística. In: Caramaschi, E.P.; Mazzoni, R.; Bizerril, C.R.S.F. & Peres-Neto, P.R. (Eds.). Oecologia Brasiliensis. Rio de Janeiro. p. 183-208.). Casting nets were also used in the middle of the Papari lagoon with the help of a local fisherman boat.

After collected, specimens were anesthetized in a 10% alcoholic eugenol solution (10 mL of clove oil; 90 mL of ethyl alcohol) (Lucena et al., 2013Lucena, 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.), then fixed in 10% formaldehyde and posteriorly transferred to a 70% ethanol solution (Malabarba & Reis, 1987Malabarba, L.R. & Reis, R.E. 1987. Peixes. In: Manual de técnicas para a preparação de coleções zoológicas, n. 36. Campinas, Sociedade Brasileira de Zoologia.). Specimens’ identification was done to the lower taxonomic level based on specialized literature (Britski et al., 1984Britski, 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, Codevasf, Divisão de Piscicultura e Pesca.; Kullander, 1983Kullander, S.O. 1983. A revision of the South American cichlid genus Cichlasoma (Teleostei: Cichlidae). Stockholm, Swedish Museum of Natural History.; Marceniuk, 2005Marceniuk, A.P. 2005. Chave para identificação das espécies de bagres marinhos (Siluriformes, Ariidae) da costa brasileira. Boletim do Instituto de Pesca, 31(2): 89-101.; Ploeg, 1991Ploeg, 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 (Pisces, Perciformes, Cichlidae). Amsterdam, Academisch Proefschrift, Universiteit van Amsterdam. 152p.; Figueiredo & Menezes, 1980Figueiredo, J.L. & Menezes N.A. 1980. Manual de peixes marinhos do Brasil, Vol. III. Teleostei. São Paulo, Museu de Zoologia/Universidade de São Paulo. 90p. and Carpenter, 2002Carpenter, K.E. 2002. The living marine resources of the Western Central Atlantic. Volume 3: Bony fishes part 2 (Opistognathidae to Molidae), sea turtles and marine mammals. Rome, Food and Agriculture Organization of the United Nations. (Species Identification Guide for Fishery Purposes and American Society of Ichthyologists and Herpetologists Special Publication, n. 5).), or specialists’ support. The systematic classification and nomenclature of valid species followed Eschmeyer et al. (2017Eschmeyer, W.N.; Fricke, R. & van Der Laan, R. 2017. Catalog of fishes: genera, species, references. Available at: Available at: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp . Access in: 08/07/2017.
http://researcharchive.calacademy.org/re...
). Specimens were deposited at the ichthyological collection of the Universidade Federal do Rio Grande do Norte (UFRN).

Recently collected data were compared to those recorded by Starks (1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.) and Fowler (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.) (Table 2). An updated identification of this material was checked in the online database from the Stanford University (SU) at California Academy of Science (http://researcharchive.calacademy.org/research/Ichthyology/collection/index.asp), and the Academy of Natural Science of Drexel University (ANSP). The species collected by Starks and Fowler refers only to the Papari lagoon, while those collected throughout this survey in the lagoon are marked with an asterisk (Table 2).

Table 2
Systematic list of fish species collected in Trairí river basin, Rio Grande do Norte. Material collected by Starks (1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.) and Fowler (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.) from Papari lagoon. FPE: peripheral freshwater; FPR: primary freshwater; FSE: secondary freshwater; MAR: marine. E: endemic species from the Mid-Northeastern Caatinga Ecoregion; EX: exotic species; *Species collected at the Papari lagoon during this study. (VU)Vulnerable species, and (SI)Species inquirenda. ANSP: The Academy of Natural Sciences of Drexel University; SU: Ichthyological collection of Stanford University at California Academy of Sciences; UFRN: Universidade Federal do Rio Grande do Norte.

Ecophysiological classification of salinity tolerance followed Myers (1949Myers, G.S. 1949. Salt-tolerance of fresh-water fish groups in relation to zoogeographical problems Bijdragen tot de Dierkunde, 28: 315-322.). The Brazilian list of endangered species (MMA, 2014) was used to discuss the conservation status of each species. Endemism of freshwater fishes, defined by occurrence in the MNCE, followed Rosa et al. (2003Rosa, R.S., Menezes, N.A., Britski, H.A., Costa, W.J.E.M. & Groth, F. 2003. Diversidade, padrões de distribuição e conservação dos peixes da Caatinga. In: Leal, I.R.; Tabareli, M. & Silva, J.M.C. (Eds.). Ecologia e Conservação da Caatinga. Recife, Editora da Universidade Federal de Pernambuco. p. 135-180.), Buckup et al. (2007Buckup, P.A.; Menezes, N.A. & Ghazzi, M.S. 2007. Catálogo das Espécies de Peixes de Água Doce do Brasil. Rio de Janeiro, Museu Nacional.), and Lima et al. (2017Lima, S.M.Q.; Ramos, T.P.A.; da Silva, M.J. & Rosa, R.S. 2017. Diversity, distribution, and conservation of the Caatinga fishes: advances and challenges. In: Silva, J.M.C.; Leal, I.R.; Tabarelli, M. (Orgs.). Caatinga the largest tropical dry forest region in South America. Springer. p. 97-131. Disponível em: https://link.springer.com/chapter/10.1007/978-3-319-68339-3_4.
https://link.springer.com/chapter/10.100...
). Lastly, the list of exotic species followed Leão et al. (2011Leão, T.C.C.; Almeida, W.R.; Dechoum, M.S. & Ziller, 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.).

RESULTS

A total of 28 species belonging to 25 genera, 17 families, and six orders were recorded in our surveys. Primary freshwater species were predominant (16 spp., 57.1%), followed by secondary (7 spp., 25%) and peripheral (5 spp., 17.9%) (Table 2). The order Characiformes was the most representative with six families, nine genera, and 12 species (42.8%), followed by Siluriformes with five families, five genera, and five species (17.8%), and Cichliformes with one family, four genera and four species (14.3%). The order Synbranchiformes was represented by a single species.

Sixteen species (57.1%) were collected in the Papari lagoon area, being nine primary freshwater (Astyanax aff. bimaculatus, Characidium bimaculatum, Erythrinus erythrinus, Hoplias malabaricus, Megalechis thoracata, Prochilodus brevis, Serrapinnus heterodon, S. piaba, and Steindachnerina notonota), four secondary (Cichlasoma orientale, Crenicichla brasiliensis, Poecilia vivipara and Oreochromis niloticus), and three peripheral (Bagre marinus, Centropomus undecimalis and Eleotris pisonis) (Table 2).

Of these 28 species herein registered (Table 2), 14 had already been recorded in previously studies (i.e.,Starks, 1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.; Fowler, 1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.). Therefore, 14 species (Astyanax aff. fasciatus, Bagre marinus, Characidium bimaculatum, Erythrinus erythrinus, Geophagus brasiliensis, Hemigrammus marginatus, Oreochromis niloticus, Plagioscion squamosissimus, Poecilia reticulata, P. vivipara, Rhamdia quelen, Serrapinnus heterodon, S. piaba and S. potiguar), most of which are freshwater, are new records for the basin, raising its richness to 50 species. Besides, three of them were introduced: the Nile tilapia (Oreochromis niloticus), the silver croaker (Plagioscion squamosissimus), and the guppy (Poecilia reticulata). No threatened species was recently collected; however, Starks recorded Megalops atlanticus Valenciennes, 1847, which is evaluated as ‘vulnerable’ (MMA, 2014Ministério do Meio Ambiente (MMA). 2014. Portaria № 445, de 17 de Dezembro de 2014. Lista Nacional Oficial de Espécies da Fauna Ameaçadas de Extinção - Peixes e Invertebrados Aquáticos. Diário Oficial da União, Brasília.).

DISCUSSION

Starks described the Papari lagoon as a large, shallow, and muddy estuarine water body with abundant superficial vegetation, which made it laborious to trawl fishes (Starks, 1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.). Being aided by local fishermen, he intensively sampled the lagoon during several days, collecting 26 species, most of which were estuarine (Table 2) (six primary freshwater fish species, three secondary, ten peripheral, and seven marine) (Starks, 1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.). In 1936, von Ihering collected 18 species at the same locality (Table 2) (13 primary freshwater, three secondary, and two marine), being eight previously recorded by Starks (Achirus achirus, Astyanax aff. bimaculatus, Cichlasoma orientale, Crenicichla brasiliensis, Hoplias malabaricus, Mugil liza, Steindachnerina notonota, and Synbranchus aff. bimaculatus), and ten were new records (Hypostomus papariae, Leporinus piau, Pimelodella papariae, Prochilodus brevis, Psectrogaster saguiru, Pseudancistrus papariae, Pygocentrus nattereri, Serrasalmus rhombeus, Triportheus signatus, and Trachelyopterus galeatus) (Fowler, 1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.). These studies together accounted for 36 fish species in the Papari lagoon (Table 2). The updated taxonomic list of the fish species herein provided allowed a comparison between these previous studies in the Papari lagoon.

Considering the records of Starks (1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.), Fowler (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.), and those of the recent surveys, 50 species were documented in the Trairí river basin. Among the 14 new records, it is remarkable the occurrence of Serrapinnus potiguar, which was only known from the Ceará-Mirim river basin (Jerep & Malabarba, 2014Jerep, F.C. & Malabarba, L.R. 2014. A new species of Serrapinnus Malabarba, 1998 (Characidae: Cheirodontinae) from Rio Grande do Norte State, northeastern Brazil. Neotropical Ichthyology, 12(2): 301-308.), located about 55 km to the north of Trairí river basin, expanding southward the distribution of this recently described species. However, since the Papari lagoon is situated at the estuarine portion of Trairí river basin and it is directly influenced by tides, as reported by Jenkins & Branner (1913Jenkins, O.P. & Branner, J.C. 1913. Geology of the Region about Natal, Rio Grande do Norte, Brazil. Proceedings of the American Philosophical Society, Philadelphia, 52(211): 431-466.), the records of Gymnotus carapo, Hypostomus papariae, Metynnis lippincottianus, Pimelodella papariae, Psectrogaster saguiru, Pseudancistrus papariae, Pygocentrus nattereri, and Serrasalmus rhombeus are dubious, and might have been captured upstream, as they are characterized as freshwater species and have low salinity tolerance (Myers, 1949Myers, G.S. 1949. Salt-tolerance of fresh-water fish groups in relation to zoogeographical problems Bijdragen tot de Dierkunde, 28: 315-322.).

Starks (1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.) and Fowler (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.) did not register any introduced species in the Papari lagoon, suggesting a scenario of environmental degradation over the last decades, since in recent samplings three introduced species were recorded: two from fish farming or aquaculture (Oreochromis niloticus and Plagioscion squamosissimus), and one from aquarium trade (Poecilia reticulata) (Leão et al., 2011Leão, T.C.C.; Almeida, W.R.; Dechoum, M.S. & Ziller, 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.). In addition to the introduction of exotic species of fish, the lagoon has been suffering from environmental impacts due to intense development of shrimp farming in Rio Grande do Norte State (Santos & Coelho, 2002Santos, M.C.F. & Coelho, P.A. 2002. Espécies exóticas de camarões Peneídeos (Penaeus monodon Fabricius, 1798 e Litopenaeus vannamei Boone, 1931) nos ambientes estuarino e marinho do Nordeste do Brasil. Boletim Técnico Científico do CEPENE, 10: 207-220.). Some stretches have been greatly modified at the lower portion of Trairí river basin as a result of the removal of riparian vegetation and riverbed sand for building shrimp farms, contributing for the lagoon’s silting. Besides, waste (antibiotics and organic matter) coming from those farms are dumped into the Papari lagoon without any prior treatment (Santos, 2005Santos, M.C.F. 2005. A prática da carcinicultura de Litopenaeus vannamei (Boone, 1931) (Crustacea, Decapoda, Penaeidae) e suas implicações no Nordeste do Brasil. Boletim Técnico Científico do CEPENE, 13: 129-142.). According to Santos (2005Santos, M.C.F. 2005. A prática da carcinicultura de Litopenaeus vannamei (Boone, 1931) (Crustacea, Decapoda, Penaeidae) e suas implicações no Nordeste do Brasil. Boletim Técnico Científico do CEPENE, 13: 129-142.), the small height of dikes has been contributing for the overflow of farms in the rainy seasons and for the invasion of the exotic shrimp species Litopenaeus vannamei (Boone) into the Papari-Guaraíras lagoon complex.

Fowler (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.) described many species from several type localities along the Brazilian northeast. At the Papari lagoon he described four species of which three are catfishes (Hypostomus papariae, Pimelodella papariae, and Pseudancistrus papariae) and one is a characin (Psectrogaster saguiru). However, except the latter, Fowler’s descriptions do not exhibit any diagnostic characters that allow their differentiation from congeners, including those of the same study. There have been some doubts regarding the taxonomic validity and geographic distribution of the species Pseudancistrus papariae and Pimelodella papariae once they have not been recorded in coastal basins that flow to the eastern coast of the MNCE and are only known from their type-series (Lima et al., 2017Lima, S.M.Q.; Ramos, T.P.A.; da Silva, M.J. & Rosa, R.S. 2017. Diversity, distribution, and conservation of the Caatinga fishes: advances and challenges. In: Silva, J.M.C.; Leal, I.R.; Tabarelli, M. (Orgs.). Caatinga the largest tropical dry forest region in South America. Springer. p. 97-131. Disponível em: https://link.springer.com/chapter/10.1007/978-3-319-68339-3_4.
https://link.springer.com/chapter/10.100...
).

Possible locality mislabeling or erroneous identifications of lots assigned to the Papari lagoon by Fowler (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.) are realistic possibilities, as already mentioned by Vari (1989Vari, R.P. 1989. Systematics of the neotropical characiform genus Psectrogaster Eigenmann and Eigenmann (Pisces: Characiformes). Smithsonian Contributions to Zoology, 481: 21-23.) and Ramos et al. (2017Ramos, T.P.A; Zawadzki, C.H.; Ramos, R.T.C. & Britski, H.A. 2017. Redescription of Hypostomus johnii, a senior synonym of Hypostomus eptingi (Siluriformes: Loricariidae), Northeastern Brazil. Neotropical Ichthyology, 15(2): e160064.). These authors noticed that the localities attributed to Psectrogaster saguiru (Lago Papary, Rio Grande do Norte) and Hypostomus eptingi (Fortaleza, Ceará) belong to the basins of the Jaguaribe and Parnaíba rivers, respectively. This could also have happened to further fishes of the Papari lagoon, based on the same kind of observation: the absence of some species (e.g., Pimelodella papariae and Pseudancistrus papariae) despite recent and previous surveys in the Trairí river basin, and the presence of some relatively large-sized species (e.g., Psectrogaster saguiru, Pygocentrus nattereri, Serrasalmus rhombeus, and Triportheus signatus) that are more common in the larger basins of the MNCE. These factors also contribute to questionings concerning the actual provenance of such species.

In northeastern Brazil, specimens of Pseudancistrus are only known from the two largest basins of the MNCE, which drain to the north, Jaguaribe and Piranhas-Açu rivers, and are usually identified as P. genisetiger (Lima et al., 2017Lima, S.M.Q.; Ramos, T.P.A.; da Silva, M.J. & Rosa, R.S. 2017. Diversity, distribution, and conservation of the Caatinga fishes: advances and challenges. In: Silva, J.M.C.; Leal, I.R.; Tabarelli, M. (Orgs.). Caatinga the largest tropical dry forest region in South America. Springer. p. 97-131. Disponível em: https://link.springer.com/chapter/10.1007/978-3-319-68339-3_4.
https://link.springer.com/chapter/10.100...
). Between 1936 and 1937, von Ihering and his team collected in many drainages in northeastern Brazil, including these MNCE’s large basins (Fowler, 1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.); therefore, the material assigned as Pseudancistrus papariae might have come from these drainages. Starks (1913Starks, E.C. 1913. The fishes of the Stanford Expedition to Brazil. Stanford, Leland Stanford Junior University Publications. 77p.) also did not record any specimen of this genus in Papari lagoon or in any sampling site. Due to the virtual absence of representatives of the genus in Trairí river basin and in other MNCE’s eastern coastal drainages, Lima et al. (2017Lima, S.M.Q.; Ramos, T.P.A.; da Silva, M.J. & Rosa, R.S. 2017. Diversity, distribution, and conservation of the Caatinga fishes: advances and challenges. In: Silva, J.M.C.; Leal, I.R.; Tabarelli, M. (Orgs.). Caatinga the largest tropical dry forest region in South America. Springer. p. 97-131. Disponível em: https://link.springer.com/chapter/10.1007/978-3-319-68339-3_4.
https://link.springer.com/chapter/10.100...
) suggested that it might have been some location mislabeling in the lots supposedly assigned to the Papari lagoon.

Fowler (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.) also described eight species currently allocated in the genus Pimelodella in northeastern Brazil, besides recognizing P. gracilis (Valenciennes). Six of those are from the MNCE (P. dorseyi, P. enochi, P. gracilis, P. papariae, P. witmeri, and P. wolfi); however, these descriptions do not establish a clear distinction among the proposed species, sometimes belonging to the same drainage (Slobodian, 2018Slobodian, V.B. 2018. Taxonomic revision of Pimelodella Eigenmann & Eigenmann, 1888 (Siluriformes: Heptapteridae): an integrative proposal to delimit species using a multidisciplinary strategy. (Doctoral Thesis). São Paulo, Museu de Zoologia, Universidade de São Paulo.). The same seems to apply to Fowler’s Hypostomus species, with H. papariae being difficult to be distinguished from H. pusarum Starks based on the original description. Meanwhile, H. papariae, Pimelodella papariae, and Pseudancistrus papariae were listed as species inquirendae by Lima et al. (2017Lima, S.M.Q.; Ramos, T.P.A.; da Silva, M.J. & Rosa, R.S. 2017. Diversity, distribution, and conservation of the Caatinga fishes: advances and challenges. In: Silva, J.M.C.; Leal, I.R.; Tabarelli, M. (Orgs.). Caatinga the largest tropical dry forest region in South America. Springer. p. 97-131. Disponível em: https://link.springer.com/chapter/10.1007/978-3-319-68339-3_4.
https://link.springer.com/chapter/10.100...
).

Taxonomic uncertainties caused by brief descriptions, locality mislabeling in Fowler’s study (1941Fowler, H.W. 1941. A collection of fresh-water fishes obtained in eastern Brazil by Dr. Rodolpho von Ihering. Proceedings of the Academy of Natural Sciences Philadelphia, 93: 123-336.), and complex nomenclature emphasize the need of taxonomic revisions of the genera Hypostomus, Pseudancistrus, and Pimelodella from northeastern Brazil basins. This is paramount to determine their taxonomic validity, including some species supposedly described from the Papari lagoon, in the Trairí river basin. Although not definitive, the extensive surveys of freshwater fish species from the MNCE’s coastal basins are providing more knowledge to solve the taxonomic problems. It also helps in gathering fresh material for morphological and molecular studies, as well as to assess the anthropogenic impacts, mainly in drainages with historical inventories and which are the type locality of some species.

ACKNOWLEDGEMENTS

The authors are thankful to Dr. Fernando Carvalho (UFMS) for identifying specimens of the genus Hemigrammus, and to Waldir Berbel-Filho, Janaína Gomes, and students who took the discipline of Ichthyology 2013.2 at UFRN for helping in fieldwork activities. TPAR received postdoctoral fellowship from FAPERN/CNPq (350674/2012-4), LSM and MGSL scientific initiation scholarship from PROPESQ, RECP Master’s scholarship from PRH-ANP (Programa de Recursos Humanos da Agência Nacional de Petróleo, Gás Natural e Biocombustíveis, proc. 486100097362013). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

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Edited by

Edited by: Fernando César Paiva Dagosta

Publication Dates

  • Publication in this collection
    25 Mar 2019
  • Date of issue
    2019

History

  • Received
    06 Mar 2018
  • Accepted
    09 Nov 2018
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