Redescription of the endangered hypoptopomatine catfish Parotocinclus spilurus ( Fowler , 1941 ) ( Siluriformes : Loricariidae ) from the upper rio Jaguaribe basin , northeastern Brazil

Parotocinclus spilurus (Fowler) was originally described as a species of Plecostomus based on six specimens collected in the rio Salgado, Icó Municipality, Ceará State, northeastern Brazil. Because the original description of P. spilurus is brief and uninformative, a detailed redescription of this endangered species based on the type series and on freshly collected topotypes was made. Data on osteology, intraspecific variation, sexual dimorphism and color pattern in life are presented for the first time, aiming at providing the necessary characters to differentiate the species from its congeners, as well as providing data on the distribution, habitat and conservation.


Introduction
A sample of 823 specimens, representing 104 species of freshwater fishes from northeastern Brazil, was collected by Rodolpho von Ihering (Fowler, 1941).In 1937, this valuable material was sent to the curator of fishes, Henry W. Fowler, at the Academy of Natural Sciences of Philadelphia (ANSP), who described 36 new species from the rio Parnaíba in Piauí State, rio São Francisco in Pernambuco State, rio Jaguaribe and other small coastal basins of Ceará, Rio Grande do Norte and Paraíba States (Fowler, 1941).However, that study, as others involving the freshwater fish fauna from northeastern Brazil, presents succinct descriptions, erroneous identification, and confused taxonomy, with some taxa probably being synonyms to species previously described (Rosa et al., 2003;Barros et al., 2011).Among those, is the original description of Plecostomus spilurus, based on six specimens collected in the rio Salgado, a tributary of the upper rio Jaguaribe basin, at Icó Municipality, Ceará State, with the holotype deposited under catalog number ANSP 69403 and five paratypes catalogued as ANSP 69404 to 69408.
Parotocinclus was raised to generic level by Eigenmann & Eigenmann (1890), and it was previously considered as a monotypic subgenus of Hisonotus Eigenmann & Eigenmann (Eigenmann & Eigenmann, 1889).Garavello (1977) revised Parotocinclus and placed Plecostomus spilurus in this genus.Although Garavello (1977) presented redescriptions of several Parotocinclus species known at that time, based on the type series.However, the morphological information is still brief for modern standard procedures and he did not present any osteological information, live color pattern, or habitat data.
During recent ichthyological surveys in the drainages involved in the project of the artificial watershed transposition of the rio São Francisco (Lima, 2005), including the rio Jaguaribe, rio Piranhas-Açu, rio Apodi-Mossoró and rio Paraíba do Norte basins, some species of Parotocinclus were collected.Thus, a detailed redescription of P. spilurus based on the type series and on freshly collected topotypes, including intraspecific variation, live color pattern, and osteologic information is provided, in order to make available details necessary to distinguish that species from congeners, sometimes occurring in sympatry, as well as new data on geographic distribution, habitat and conservation.

Parotocinclus spilurus
Plates lateral to anal-fin base 3 3-3 3 Plates between anal and caudal fins 11 9-11 10  Dorsal fin i,7; its origin in vertical line to pelvic-fin origin; when adpressed, extending to vertical through beyond anal-fin base.Dorsal-fin first unbranched ray flexible, followed by seven branched rays.Dorsal-fin spinelet present, trapezoid-shaped, wider than base of dorsal-fin unbranched ray.Dorsal-fin locking mechanism non-functional.Nuchal plate exposed, not covered by skin.Adipose fin rudimentary or vestigial.Pectoral fin i,6; pectoral-fin unbranched ray reaching nearly half length of unbranched pelvic-fin ray.Pelvic fin i,5; unbranched ray curved, covered with small odontodes; pelvic fin reaching beyond anus, ending in anal-fin origin.Anal-fin i,5; anal-fin base flanked by three plates.Caudal fin slightly notched, emarginated, with lower lobe slightly pointed and longer than the upper lobe; principal caudal-fin rays i,14,i.Lateral-line canal in median series complete, pore tube visible from parieto-supraoccipital to caudal peduncle.Body covered by dermal plates, except region between pectoral girdle and lower lip, central area of the pectoral girdle (medial area naked and exposed only laterally supporting odontodes), and areas around bases of paired fins and anus.Abdomen mostly covered by rounded dermal plates arranged in T-shape between pectoral girdle and anus (Fig. 5).Total vertebrae 26 (2 c&s).
Coloration. Background color in ethanol dark brown to yellowish brown.Specimens larger than 30 mm SL with yellowish gold rounded spots on dorsal and lateral portions of head and trunk, with lighter spot on pineal region.The spots are smaller in the anterior region of the body forming several series (5-7 series) longitudinal, and increase in size towards the caudal peduncle, converging to two or three series on lateral of trunk.Four inconspicuous dark bars on dorsum; upon pineal region features grayish yellow spot approximately on parieto-supraoccipital; ventral area of head and abdomen whitish yellow, with small sparse chromatophores on anterior portion of mouth, abdomen, pectoral fins and pre-anal region.Dorsal and caudal-fin rays with concentrated patch of dark chromatophores, forming irregular set of bands that alternates between dark brown and brownish yellow: four on dorsal fin and three to four on caudal fin, with chromatophores concentrated in conspicuous a spot on each caudal-fin lobe, especially in smaller individuals (Fig. 2).Pectoral, pelvic and anal fins with same color pattern, but slightly lighter.Live coloration with same pattern described above, with spotted pattern more evident (Fig. 4).
Sexual dimorphism.Males possess urogenital papilla positioned just behind anal opening and with developed dermal flap along posterodorsal margin of thickened first pelvic-fin ray.Adult males (>30 mm SL) have the odontodes of caudal peduncle dorsally or posterodorsally directed, and modified into cluster (Fig. 7), females lack this odontodes arrangement.Distribution.Parotocinclus spilurus is known from four localities in the rio Jaguaribe basin, in the Ceará State (Fig. 8).Individuals of P. spilurus were collected in the putative type locality of the species, in the rio Salgado, at Icó Municipality (Fig. 9), and were also found in three other sites: the rio Lima Campos in the Lima Campos Municipality, the riacho Machado in the Lavras da Mangabeira Municipality, all from rio Salgado sub-drainage; and the rio Jaguaribe itself in the Saboeiro Municipality, suggesting a restricted geographic distribution in the upper rio Jaguaribe basin.At Icó, the sampling site was under the BR 404 bridge at rio Salgado immediately upstream the urban area.Due to the ease of access, low environmental degradation and reduced metropolitan area this site may represent the type locality of P. spilurus.
Ecological notes.In the semi-arid Caatinga region, through which the rio Jaguaribe basin flows, the rivers may completely dry in some stretches and become restricted to small ponds, especially in periods of drought, due to the irregular rainfall regime (Rosa et al., 2003).Parotocinclus spilurus was usually found in moderate current flow in clear-water streams with small rocky bottoms and gravel substrates (Fig. 9).However, in recent collections P. spilurus was only found on rocky stretches below artificial dams that were releasing water, suggesting that the species may now be restricted to places where water availability is regulated by human action.The following species were also collected sympatrically in the rio Salgado: Astyanax aff.Remarks.Parotocinclus spilurus is endemic to the upper portion of the rio Jaguaribe basin in the State of Ceará.This basin is situated almost entirely within the boundaries of Ceará State, with a small portion extending to the south, into Pernambuco State, occupying part of Exú, Moreilândia and Serrita municipalities.In the last five years, several expeditions were carried out in the rio Jaguaribe basin, including one directed at capturing P. spilurus.As the result of over 40 sampling sites throughout the rio Jaguaribe basin, P. spilurus was only collected in four localities in a specific biotope of a restricted area in the upper portion of the drainage (about 16 km 2 in area of occupancy), suggesting that this species has a narrow distribution, further lending support to the belief that this area contains several restricted-range species (Nogueira et al., 2010).

Conservation status.
According to IUCN criteria (International Union for Conservation of Naturae (IUCN), 2001, 2010) P. spilurus was categorized as endangered (EN) in the recently published Brazil's official list of endangered species of fish and aquatic invertebrates (Brasil, 2014), representing one of the first freshwater fish species of the Mid-Northeastern Caatinga ecoregions to be recognized as imperiled.The region deserves more attention when considering that the rio Jaguaribe is one of the basins that will receive waters from the rio São Francisco transposition.

Discussion
Examination of a large number of specimens of Parotocinclus spilurus revealed a range of teeth number higher than presented in the original description (Fowler, 1941) and redescription (Garavello, 1977).According to Fowler (1941), P. spilurus has 8 to 9 teeth in the premaxilla and 10 to 12 in the dentary, while in the diagnosis presented by Garavello (1977) it has 13-18 premaxillary teeth, and 11-15 dentary teeth.In the present study, however, we observed 15 to 24 teeth in the premaxilla, and 17 to 28 in the dentary in the type series (including tooth scars count), meanwhile counts of the topotypes have 14 to 24 teeth in the premaxilla and 12 to 28 in the dentary.The recently collected material has shown the total number of teeth of P. spilurus, which is similar to the type series (including tooth scars), but distinct from counts made by Fowler (1941) and Garavello (1977).Thus, it is possible that these authors have counted only the remaining teeth, without considering the loss of teeth that can occur due to the age, preservation and handling of ichthyologic specimens.
Another noteworthy aspect is in the size of the adipose fin of P. spilurus illustrated in Fowler (1941: 149).In Fowler's drawing, the adipose fin appears as a small flap devoid of the spinelet, but no specimen of the type series or recently collected topotypes has the adipose fin in this stage of development, but instead have vestigial adipose fins (Figs.1-2).
Observation of the coloration of live specimens highlights phenotypic differences among Parotocinclus species from Mid-Northeastern Caatinga ecoregion, and provides support to specific epithets proposed by Fowler (1941).Live and recently preserved P. spilurus specimens have, besides the black spot in caudal peduncle and transverse dark bands, there are conspicuous dark spots in each caudal-fin lobe (Fig. 4), a character that also explains the etymology of the epithet referred by Fowler "with reference to the dark marks on the caudal" (Fowler, 1941).Another conspicuous difference between the color pattern described by Fowler (1941) and Garavello (1977) is the presence of rounded spots on the head and side of the body in individuals larger than 30 mm SL, evident both in live and recently collected specimens (Figs.2-4).In smaller specimens (< 30 mm SL), as the holotype (28.6 mm SL) the color pattern is as described by those authors, but above this size the rounded yellowish spots become more evident and the transverse bands inconspicuous (Fig. 3).Ontogenetic color variation is already known in some Siluriformes (Ferrer & Malabarba, 2013) and Loricariidae species (Zawadzki & Carvalho, 2014).Besides the color pattern, a few morphological variation could also be observed across the size range in P. spilurus specimens.These differences are mainly related to head shape, eye diameter and position and snout length (Fig. 3).Ontogenetic shape changes were already observed in loricariids, including hypoptopomatine catfishes (Aquino & Miquelarena, 2001;Rosa et al., 2014) and must be related to allometric development of bones, muscles and plates structures (Geerinckx et al., 2008(Geerinckx et al., , 2009)).
Most drainages in Ceará, Rio Grande do Norte and Paraíba States, and part of Piauí, Pernambuco and Alagoas Sates belong to the Mid-Northeastern Caatinga ecoregion, which comprises the small and medium-sized basins eastern to the rio Parnaíba (Maranhão-Piauí ecoregion) and northern to the rio São Francisco (São Francisco ecoregion) basins (Rosa et al., 2003;Abell et al., 2008;Albert et al., 2011), which have been subjected to several anthropic impacts due to water use conflicts (Rosa et al., 2003).These basins are mainly in the semi-arid region, subject to long periods of drought, and there is a predominance of temporary rivers.The major basins of the Mid-Northeastern Caatinga ecoregion will receive water from the ongoing inter-basin water transfer of the rio São Francisco, the largest perennial river in northeastern Brazil, which constitutes a distinct ecoregion (Rosa et al., 2003).
In some drainages of the Mid-Northeastern Caatinga ecoregion, as the Jaguaribe and Paraíba do Norte basins, at least three species of Parotocinclus occur in sympatry and sometimes in syntopy: P. spilurus, P. jumbo Britski & Garavello and P. cf. cearensis Garavello in the former, and P. spilosoma (Fowler) and the other previous mentioned species in the latter.Britski & Garavello (2002) suggested the presence of two additional Parotocinclus species in rio Salgado, besides P. spilurus, one of which is possibly young specimens of P. jumbo, but they could not determine the identity of the other species due to the poor condition of the material.These authors emphasized the need of well-preserved specimens from the rio Salgado to allow an accurate identification of this third species.According to the recently collected material from rio Salgado, comparative material and bibliographic information, the third species is P. cf. cearensis and the presence of P. jumbo is also corroborated (see Material examined below).Actually, P. jumbo and P. cf. cearensis seem to be the only species of Parotocinclus to have a broad geographic distribution in northeastern Brazil, and could in fact represent species complexes that may have dispersed through adjacent coastal basins in periods of lower sea levels during the Quaternary (Garavello, 1977).These two lineages (P.jumbo and P. cf. cearensis) are not closely related (Lehmann, 2006), and it is probably that the co-occurrence of Parotocinclus species in northeastern Brazil is due to secondary contact events.Rosa (2004) indicated that the rio Salgado is a high biological priority area for fish conservation in the semiarid Caatinga based on the occurrence of special biological phenomena, such as the presence of annual fish and /or cave species, the high phyletic diversity and occurrence of endemism.The restricted distribution of P. spilurus in the rio Jaguaribe basin, besides other species that may be endemic to that basin, such as Ancistrus salgadae Fowler, Hypostomus carvalhoi (Miranda Ribeiro), H. jaguribensis, Pseudancistrus genisetiger, Pimelodella witmeri, P. dorseyi, Squaliforma gomesi (Fowler) and Trachycorystes cratensis Miranda Ribeiro, although some of these species may not be valid (e.g. A. salgadae and H. carvalhoi), supports that drainage as an important area of endemism for fishes.
The geographically closest species to Parotocinclus spilurus are P. seridoensis Ramos, Barros-Neto, Britski & Lima, endemic to the upper rio Piranhas-Açu basin, P. haroldoi Garavello inhabiting the rio Parnaíba basin (Ramos et al., 2013).Despite being isolated in separate river basins, these species are similar in morphology and color pattern and apparently are closely related.They share the yellowish spots on the dorsal and lateral portions of the head; however, P. haroldoi has smaller spots, while P. seridoensis has large, faint rounded spots, usually uniform in size, and P. spilurus with conspicuous intermediate size spots.
Another character shared between P. spilurus and P. seridoensis is the sexual dimorphism related to the orientation of modified odontodes on the caudal peduncule in adult males.A similar modification is known in males of some Otocinclus species, and in both sexes of the monotypic genus Gymnotocinclus Carvalho, Lehmann & Reis (Carvalho et al., 2008).Ramos et al. (2013) mentioned characters, such as the adipose fin rudimentary or absent, which can represent synapomorphies for Parotocinclus spilurus and P. seridoensis, indicating a sister-species relationship.The authors also mentioned a possible vicariant process due to a tectonic activation in northeastern Brazil (Lima, 2000;Bezerra et al., 2006), in which the Chapada de Apodi acted as a watershed divisor between the rio Jaguaribe and rio Piranhas-Açu basins, which could be involved in the origin of these species.

Fig. 5 .
Fig. 5. Ventral view of abdominal region showing the lateral plates and preanal platelets arranged in T-shape in Parotocinclus spilurus.Abbreviations: LAPS, lateral abdominal plates series; MAPS, median abdominal plate series; PAR, pre-anal region.