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

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., 2008;Langeani et al., 2009;Lima et al., 2017).However, in the last decade many ichthyofaunal surveys and taxonomic studies were conducted in the ecoregion (Gurgel-Lourenço et al., 2013;Novaes et al., 2013;Paiva et al., 2014;Silva et al., 2014Silva et al., , 2017;;Botero et al., 2014;Lira et al., 2015;Ramos et al., 2013Ramos et al., , 2016Ramos et al., , 2017;;Britzke et al., 2016;Rodrigues-Filho et al., 2016;Teixeira et al., 2017;Zawadzki et al., 2017;Costa et al., 2017;Lima et al., 2017).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, 1913).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 16 th century, its native name means "fish jump", emphasizing the abundance of fish (Ferreira, 2011).In the vicinity of the lagoon, in Nísia Floresta Municipality, there was established a fishermen community which was mentioned by Edwin Chapin Starks (1913) as responsible for the large fish collection at this locality.
Later, Fowler (1941) 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, 1941).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 (1913) and Fowler (1941).Furthermore, some hypotheses concerning incongruences on the occurrence of some species described by Fowler were provided.

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, 2014) (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., 2011).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, 1990).About 88% of the basin lies within the Caatinga and the remaining in the Atlantic Forest (ANA/ SGI, 2014).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, 2001).

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 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, 1999;Sabino, 1999).Casting nets were also used in the middle of the Papari lagoon with the help of a local fisherman boat.
Recently collected data were compared to those recorded by Starks (1913) and Fowler (1941) (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).
Ecophysiological classification of salinity tolerance followed Myers (1949).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. (2003), Buckup et al. (2007), and Lima et al. (2017).Lastly, the list of exotic species followed Leão et al. (2011).

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.

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, 1913).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, 1913).In 1936, von Ihering collected 18 species at the same locality (  (Fowler, 1941).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 (1913), Fowler (1941), 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, 2014), 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 (1913), the records of Gymnotus carapo, Hypostomus papariae, Metynnis lippincottianus, Pimelodella papariae, Psectrogaster saguiru, Pseudancistrus papariae, Pygocentrus nattereri, Serrasalmus rhombeus are dubious, and might have been captured upstream, as they are characterized as freshwater species and have low salinity tolerance (Myers, 1949).Starks (1913) and Fowler (1941) 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., 2011).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, 2002).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, 2005).According to Santos (2005), 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 (1941) 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., 2017).
Possible locality mislabeling or erroneous identifications of lots assigned to the Papari lagoon by Fowler (1941) are realistic possibilities, as already mentioned by Vari (1989) and Ramos et al. (2017).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 largesized 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., 2017).Between 1936 and1937, von Ihering and his team collected in many drainages in northeastern Brazil, including these MNCE's large basins (Fowler, 1941); therefore, the material assigned as Pseudancistrus papariae might have come from these drainages.Starks (1913) 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. (2017) suggested that it might have been some location mislabeling in the lots supposedly assigned to the Papari lagoon.
Fowler (1941) 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, 2018).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. (2017).
Taxonomic uncertainties caused by brief descriptions, locality mislabeling in Fowler's study (1941), 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 Medeiros, L.S. et al.: Ichthyofauna of Trairí river basin: a century after the study of the naturalist Edwin Starks Pap. Avulsos Zool., 2019;v.59: e20195901 6/8

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

Table 1 .
Table 1 were at the border of the Papari lagoon.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.Medeiros, L.S. et al.: Ichthyofauna of Trairí river basin: a century after the study of the naturalist Edwin Starks Pap.Avulsos Zool., 2019; v.59: e20195901 2/8

Table 2 .
Fowler (1941)st of fish species collected in Trairí river basin, Rio Grande do Norte.Material collected byStarks (1913)andFowler (1941)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)Vulnerablespecies, 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.