Brycon hilarii Valenciennes 1850

Brycon hilarii (Valenciennes, 1850) (Figs. 57–61) Chalceus hilarii Valenciennes, in Cuvier & Valenciennes, 1850: 246 –248 (Type locality “Rio San Francisco”); Kner, 1860: 10 – 11 (in part; “Rio Cujaba”). ? Chalceus orbignyanus (not Valenciennes): Kner, 1860: 11 –12 (“ Rio Guaporé”). Salmo para-putanga Kner (ex Natterer), 1860: 4 (published as a synonym of Chalceus orbygnianus; not available). Brycon melanoxanthus Kner (ex Natterer), 1860: 4 (published as a synonym of Chalceus orbygnianus; not available). Megalobrycon erythropterus Cope, 1872: 263, pl.10, fig. 2 (Type locality: “Ambyiacu”). Brycon microlepis Perugia, 1897: 149 –150 (Type locality “Puerto 14 de Mayo, dipartimento di Bahia Negra, nel Chaco boreale”[Paraguay]); Boulenger, 1898b: 127 (same locality); Bertoni, 1914: 11 (Paraguay) (non vidi); Bertoni, 1939: 55 (Paraguay); Géry & Mahnert, 1992: 803 –806, figs. 6–7 (discussion, short description, literature compilation; Paraguay: “Arroyo Tagatya-mi, est de Puerto Max”; “Concepcion, gué de l’Arroyo Tagatya-mi”; “gué de l’Arroyo Tagatya-guazu”; “Concepcion, Laguna Negra, 15 km E. de Paso Bareto”; “Concepcion, Estância Primavera”; “en face de Puerto Iguazu”; Brazil: “Lagoa de Sinhá Mariana, 30 km en aval de Barão de Melgaço”; “Barão de Melgaço, rio Cuiabá”); Silimon et al., 1996: 12 (common name); Resende et al., 1998: 9 (diet, rio Paraguai basin, Brazil); Margarido & Galetti Jr., 1999: 357 – 358 (karyotype); Sabino & Sazima, 1999: 309 –312, figs.1–2 (feeding habits, Bonito, Mato Grosso do Sul, Brazil); Britski et al., 2007: 42 –43 fig. (description; Brazil, rio Paraguai basin, Pantanal, Brazil); Menezes et al., 2000: 292 (Upper rio Miranda, Mato Grosso do Sul, Brazil); Mateus & Estupiñan, 2002: 165 –170 (Rio Cuiabá, Mato Grosso; stock assessment); Wantzen et al., 2002: 242 –243, 246–247 (Lake Coqueiro, rio Cuiabá, Mato Grosso; seasonal shifts in stable carbon and nitrogen); Resende, 2003: 119 –120, 127, 147 (Rio Paraguai basin; fisheries); Lima, 2003: 176 (primary type material listed; as a synonym of Brycon. hilarii); Menni, 2004: 74 (listed, Argentina); Mateus et al., 2004: 219 (Rio Cuiabá basin, Mato Grosso; fisheries). Brycon orbygnyanus (not Valenciennes): Boulenger, 1897b: 4 (Bolivia: “Mission de San Francisco, Rio Pilcomayo; Caiza, Chaco Bolivien”); Ramlow, 1989: 10 (Paraguay: Depto. Amambay, Parque Nacional Cerro Corá; Depto. Central, Playa Carrasco). Brycon hilarii: Boulenger, 1900: 3 (“Carandasiñho, près de Corumbá”); Eigenmann & Ogle, 1900: 3 (Paraguay); Fowler, 1932: 346, 357–358 (Descalvados, Mato Grosso, Brazil); Bertoni, 1939: 55 (listed, Paraguay); Miranda-Ribeiro, 1940: 44 (Rio Miranda, Salobra, Mato Grosso [do Sul]); Aguirre, 1945: 38, fig. 15 (Rio Paraguai basin, Mato Grosso); Amaral Campos, 1950: 140 (part; Mato Grosso); Howes, 1982: 31 (Brazil, rio Paraguai, “Pan de ezucar”); Ferraz de Lima, 1987: 89 (fisheries, rio Cuiabá, Mato Grosso, Brazil); Sazima & Machado, 1990: 24 (predation by piranhas; Pantanal, Poconé, Mato Grosso, Brazil); Barrella et al., 1994: 14 –15, 19 (Rio Manso, upper rio Paraguai basin, Mato Grosso, Brazil; ecomorphology, abundance); Beaumord & Petrere Jr., 1994: 26, 32 (same as previous); Agostinho & Júlio Jr., 1999: 379 (Paraná, rio Paraná, downstream Itaipu dam, Brazil; common name); Lima, 2003: 176 (synonimic list, maximum length, distribution); Makrakis et al., 2007: 191 (Canal da Piracema, Itaipu dam rio Paraná); Graça & Pavanelli, 2007: 77 (upper rio Paraná, Paraná; short description, picture); Sanches & Galetti, 2007: 889 –895 (Rio Miranda, Mato Grosso do Sul: population structure analysed through RAPD markers); Reys et al., 2009: 136 –141 (frugivory and seed dispersal, rio Miranda basin, Mato Grosso do Sul); Lima & Ribeiro, 2011: 151, 158 (as an example of “foreland basin” distributional pattern); Bessa et al., 2011: 351 –354 (Rio Cuiabá and Rio Miranda basins, upper Paraguai basin, Brazil; aggressive mimicry by Salminus brasiliensis); Resende, 2011: 471, 483–485, 488 (Pantanal, Brazil; reproductive biology); Oliveira et al., 2011: 62–70 (Brazil, Mato Grosso, rio Cuiabá and Manso dam: larval development); Sanches & Galetti, 2012: 408-417 (Rio Miranda, Mato Grosso do Sul: population structure analysed through microsatellite loci). [not La Monte, 1935: 7; Amaral-Campos, 1950: 142; Marlier, 1968: 56; Braga, 1982: 175–180]. Brycon hilarlii (sic): Eigenmann & Kennedy, 1903: 523 –524 (Arroyo Trementina, Paraguay). Brycon erythropterus: Fowler, 1939: 263 (Contamana, Peru); Eigenmann & Allen, 1942: 254 (Rio Ucayali, Orellana; Lago Cashiboya; Rio Pachitea; Iquitos); Ortega & Vari, 1986: 7 (listed, Peru; common name); Howes, 1982: 25 –26 (literature compilation); Géry & Mahnert, 1984: 176 (comparison with B. melanopterus); Géry & Mahnert, 1992: 798, 800, 802–803, fig. 4 (diagnosis, Peru: Marañon, Ucayali; Bolivia: upper rio Madeira); Chang, 1998: 20, 22 (Zona Reservada Tambopata- Candamo, bacia do río Tambopata, Peru). [not Goulding et al., 1988: 124]. Brycon cf. whitei (not Myers & Weitzman): Saul, 1975: 103 (Río Aguarico, Napo, Ecuador; diet). Brycon erythropterum: Ortega, 1996: 464 (Río Manu, Parque Nacional Manu, depto. Madre de Dios and Cusco, Peru). Diagnosis. Brycon hilarii can be distinguished from all remaining cis-andean Brycon, except for B. orthotaenia, B. orbignyanus, B. whitei, and B. polylepis by possessing a broad caudal peduncle stripe extending into middle caudal-fin rays (vs. caudal peducle and caudal fin color pattern presenting a either a crescent-shaped blotch, an oblique stripe extending into the upper caudal-fin lobe, or no definite color pattern). It can be distinguished from Brycon polylepis by possessing wavy longitudinal stripes along the body, formed by pigmentation concentrated on upper and lower portions of scales (vs. narrow straight longitudinal stripes along the body, formed by pigmentation concentrated in the medio-distal portion of scales), and symphyseal teeth behind the main series of dentary teeth small, considerably smaller than symphyseal teeth belonging to the main series situated immediately in front of it (vs. symphyseal teeth behind the main series of dentary teeth well-developed, approximately as large as symphyseal teeth belonging to the main series situated immediately in front of it). It can additionaly be distinguished from Brycon orbignyanus and B. orthotaenia primarily by possessing higher scale counts (67–82, modally 74, vs. 52–63, modally 56, and 49–58, modally 52 lateral line scales in Brycon orbignyanus and B. orthotaenia, respectively; 12–17, modally 15, vs. 10–13, modally 12 and 9–12, modally 10 scales between lateral line and dorsal-fin basis in B. orbignyanus and B. orthotaenia, respectively; 20–28, modally 26, vs. 19–23, modally 20, and 18–21, modally 19 circumpeduncular scales in B. orbignyanus and B. orthotaenia, respectively). Brycon hilarii can be distinguished from B. whitei by presenting a midlateral dark stripe confined to the posterior half portion of body (vs. midlateral dark stripe generally extending anteriorly to supracleithrum area) and by lacking tiny stripes on caudal-fin rays (vs. tiny stripes present in B. whitei). See item “Comparisons” of Brycon amazonicus, for a discussion on the distinction between B. hilarii and the latter species in the Peruvian Amazon. Description. Morphometric data are presented in Table 16. Large-sized species, largest examined specimen 514.0 mm SL. Body moderately slender in specimens up to 240 mm SL, moderately high in larger specimens. Largest body height slightly ahead of dorsal-fin origin. Dorsal body profile slightly convex from upper lip margin to vertical through anterior naris, straight to slightly convex from latter point to basis of supraoccipital process, moderately to pronouncedly convex from latter point to dorsal-fin origin, straight along dorsal-fin basis, and straight to slightly convex from dorsal-fin basis to adipose-fin origin. Dorsal profile of caudal peduncle slightly concave. Ventral profile slightly convex from lower lip to pelvic-fin insertion, straight to slightly convex from this point to anal-fin origin and approximately straight along anal-fin base. Ventral profile of caudal peduncle slightly concave. Head profile slightly acute anteriorly, mouth terminal. Jaws approximately isognathous to slightly anisognathous, outer row of premaxillary teeth partially exposed when mouth is closed. Maxillary moderately long, extending posteriorly to anterior third of pupil. Adipose eyelid well developed. Premaxillary teeth in three rows; teeth of third row largest. Seven (2), 8 (12), 9 (12), 10 (17), 11 (16), 12 (5), or 13 (2) relatively small tri- to pentacuspidate teeth in outer series. Four (15), 5 (41), or 6 (11) tri- to pentacuspidate teeth in second, inner premaxillary row, plus 3 (17), 4 (45), or 5 (5) tricuspidate teeth between the first and third rows. Two teeth in third premaxillary row, medial teeth largest, symphyseal teeth smaller, slightly tilted towards each other, medial teeth penta- to hexacuspidate, symphyseal teeth tetracuspidate. Maxillary margins approximately parallel, straight in profile. Eleven to 21 maxillary teeth, slightly smaller than teeth of first premaxillary row, anterior teeth tri- to pentacuspidate, posterior teeth unicuspidate. Dentary with 7 (1), 8 (3), 9 (7), 10 (8), 11 (15), 12 (7), 13 (6), or 14 (1) teeth in main series. Anterior four dentary teeth assymetrical, considerably larger and bulkier than remaining teeth, penta- to hexacuspidate, each with central cusp distinctly larger than remaining cusps. Remaining dentary teeth progressivelly smaller, penta- to unicuspidate. Inner (lingual) series consisting of a small, single unicuspid symphyseal tooth, situated immediately posterior to symphyseal dentary teeth of main series, plus row of 10–18 small, aciculated, unicuspidate teeth, originating on lingual crest of dentary replacement trench at the level of fifth to tenth main series dentary teeth. Scales cycloid. Lateral line complete, from supracleithrum to caudal-fin base. Sixty-seven (2), 68(3), 69(3), 70(3), 71(7), 72(6), 73(8), 74(11), 75(9), 76(4), 77(3), 78(8), 79(2), 80(1), 81(5), or 82 (1) scales in lateral line series. Laterosensory tube simple in specimens smaller than 100 mm SL, ramified in specimens larger than 100 mm SL. Tubules ramification increasing in complexity along ontogeny, specimens up to 150 mm SL with tubules with two or three branches, three to four branches in specimens between 150–230 mm SL, and with more than 10 branches and developing a dendritic pattern of ramification, with tubules overlapping each other in larger (> 300 mm SL) specimens. Horizontal scale rows between dorsal-fin origin and lateral line 12(2), 13(13), 14(15), 15(31), 16(13), or 17(2). Horizontal scale rows between lateral line and pelvic-fin 6(3), 7(18), 8(44), or 9(9). Circumpeduncular scales 20 (1), 21 (5), 22(13), 23(5), 24(4), 25(10), 26(16), 27(12), or 28(9). Dorsal-fin rays ii, 9. Dorsal fin origin slightly ahead middle of SL. First dorsal-fin pterygiophore inserting behind neural spine of 13th (6) to 14th (2) vertebra. Anal-fin rays iii (not including first, small unbranched ray only visible in cs specimens), 19(3), 20(3), 21(7), 22(10), 23(16), 24(14), 25(11), 26(6), 27(2), or 28(2). First anal-fin pterygiophore inserting behind haemal spine of 25th (4) or 26th (4) vertebra. Anal-fin rays decreasing only slightly in size towards anal-fin end. Sheath of scales covering basis of anal-fin rays composed of four scale rows, lower scale row formed by 20–26 rectangular scales. Pectoral-fin rays i, 11 (2), 12 (8), 13 (49), 14 (12), or 15 (3). Pelvicfin rays i, 7. Main caudal-fin rays 10/9. Caudal fin slightly forked, distal margin slightly concave. Central caudalfin rays presenting in some specimens with a small, pointed middle projection extending beyond primary margin of fin. Laterosensory tube extending over interradial membrane between upper and lower caudal-fin lobes to the distal portion of fin. Laterosensory tube on caudal fin with dorsally and ventrally oriented side branches across its length. Four branchiostegal rays, three on anterior ceratohyal and one on posterior ceratohyal. First branchial arch with 12 (1), 13 (2), 14 (2), 15 (4), 16 (8), 17 (7), or 18 (2) lower, 1 at angle, and 14 (4), 15 (3), 16 (13), 17 (3), or 18 (3) upper gill rakers. Vertebrae 45 (5), 46 (7), 47 (4), 48 (2), or 49 (1). Supraneurals 10 (6) or 11 (2). Coloration in alcohol. Top of head, snout, supraorbital, and sixth infraorbital light- to dark-brown. Dorsal portion of body light-brown to dark-brown. Second, third, fourth, and fifth infraorbitals, and opercle silvery in specimens that retained guanine, light-brown in specimens that lost this pigment due to a long storage in formalin. Dentary, maxillary, gular area, and lower portion of body light-brown. Lateral portion of body light brown, with a silvery hue. Humeral blotch present, conspicuous, approximately rounded in shape, situated immediately above lateral line, its anterior margin at level of second to third, extending longitudinally to posterior margin of fifth to sixth lateral line scales, and vertically one and half scales high. Dark, wavy longitudinal stripes formed by dark pigment concentrated on upper and lower scale margins extending along trunk. Stripes more discernible dorsally. Series of irregular, narrow vertical stripes present in small (up to 120 mm SL) specimens. Caudal peduncle with broad median stripe, originating 8–12 scales from hypural joint and continuing posteriorly over 6 central principal caudal-fin rays to caudal-fin distal margin. Some specimens with dark stripe extending as a faint stripe anteriorly to the level of anal-fin origin. Remaining caudal-fin rays, and remaining fins, clear, pectoral fins darkened in some specimens. Coloration in life. Description based on photographs of freshly caught or living specimens from rio Formoso basin, Bonito, Mato Grosso do Sul, Nobres, rio Manso basin, and Nortelândia, rio Santana basin, Mato Grosso, Brazil, from the middle rio Paraná, Corrientes, Argentina, and from Parque Nacional Yanachaga-Chamilen, Río Pachitea drainage, Depto. Pasco, Peru. Overall coloration silvery, dorsum dark-grey, with a coppery hue. Specimens from the rio Paraná and rio Paraguai basins with yellow pigmentation along the lower portion of head and body. Top of head dark grey. Midlateral dark stripe commencing at vertical that passes through origin to middle portion of anal fin, extending through caudal peduncle into middle caudal-fin rays very conspicuous. Caudal-fin rays dorsal and ventral to middle dark stripe reddish to intense red. Anal, dorsal, pectoral, and pelvic fins reddish to intense red. Variation. Specimens from the La Plata system possess lower total vertebrae counts (45–47, modally 46, n = 14) when compared with specimens from the upper Amazon (47–49, modally 47–48, n = 5). Specimens from the La Plata system are also on average more high-bodied than specimens from the upper Amazon, as reflected in body depth (27.5–36.1 % SL, mean 32.0, vs. 25.6–33.1 % SL, mean 30.2, respectively) and head height (78.7–93.8 % HL, mean 84.9, vs. 72.0–84.6 % HL, mean 77.7, respectively). Color pattern in life also seems to differ, with specimens from the upper Amazon basin possessing fins with a less intense red pigmentation. Further studies including another type of data (e.g., molecular data) are necessary to confirm whether both populations are in fact conspecific or not. Sexual dimorphism. None of the examined specimens possess anal-fin hooks. Common names. Brazil: “piraputanga” (Silimon et al., 1996: 12; Britski et al., 2007: 42); “salmão-criolo” (Agostinho & Júlio Jr., 1999: 379); Argentina: “salmón de Río ”, “pirapitá amarillo” (F. Baena, pers. comm.); Peru: “Sábalo cola roja” (Ortega & Vari, 1986: 7, as Brycon erythropterum); “Rumi-uma” (Eigenmann & Allen, 1942: 254, as Brycon erythropterum). Distribution. Rio Paraguai and middle rio Paraná basins in Brazil and Paraguay, and upper Rio Amazonas basin in Peru, Ecuador, and Colombia (Fig. 62). Brycon hilarii is recorded for the rio Paraná below the now submerged Sete Quedas falls, the previous limit between the upper and lower portions of the rio Paraná. Photographs of specimens caught in the rio Paraná between Paso de la Patria and Itatí, Corrientes, provided by M. Ribeiro and F. Baena, and juveniles in the area of Rosario (province of Santa Fé, c. 32°57’S, 60°40’W), provided by F. Baena, testify the occurrence of Brycon hilarii also in Argentina, from where the species was in fact previously recorded by Menni (2004: 74, as B. microlepis) but not in other check-lists of the ichthyofauna of Argentina (López et al., 2003; Koerber, 2009). We have not examined specimens from Brycon hilarii from upper tributaries of the Amazon basin in Colombia, but a photograph of a specimen collected at the upper Río Putumayo provided by A. Linares confirm the occurrence of the species in that country. Although Géry & Mahnert (1992: 800) record Brycon hilarii from the upper rio Madeira system in Bolivia, we have only examined specimens of B. amazonicus from this latter area and consider that the eventual occurrence of the species at the upper Rio Madeira basin in Bolivia needs further corroboration. The species is being extensively stocked in eastern Brazil and accidental/intentional releases in the upper rio Paraná basin are reported (Graça & Pavanelli, 2007: 77). Ecological notes. Brycon hilarii is a relatively eurytopic species in the rio Paraguai basin in Brazil and Paraguay, occurring from the large rivers in the lowlands and associated floodplains to relatively small, fastflowing rivers in the headwaters. At the middle rio Paraná basin in Brazil and Argentina Brycon hilarii occurs syntopically with B. orbignyanus. The largest specimen recorded in the literature measured 670 mm TL (Mateus & Estupiñan, 2002: 166). Diet and feeding behavior in the rio Paraguai basin in Brazil were studied by Sabino & Sazima (1999) and Reys et al. (2009). As other Brycon species, B. hilarii is an omnivorous fish that ingests mainly vegetal matter (Reys et al., 2009). Seeds and fruits constitute an important portion of its diet (31% of the weight), and twelve fruit/seed species were either found in guts or observed to be eaten by Brycon hilarii in the rio Formoso (Reys et al., 2009). Reys et al. (2009) hypothesized that Brycon hilarii acted as a potential seed disperser for eight tree species that possessed relative small, hard seeds that were not found crushed in the fishes’ guts. Sabino & Sazima (1999: 310–312) observed schools of Brycon hilarii consisting in up to 30 specimens following capuchin monkeys (Cebus apella) to catch fruits (specifically, Guarea cf. guidonia, Meliaceae, and Zanthoxyllum riedelianum, Rutaceae) that have fallen into the water due to the activity of the monkeys. In the Pantanal area, Resende et al. (1998: 9) reported that Brycon hilarii (their B. microlepis) commonly ingesting flowers of Tabebuia impetiginosa (Bignoniaceae) and pods of Inga uruguensis (Fabaceae). Wantzen et al. (2002: 242, 246–247), noticed an increase in the presence of the isotope 13C in Brycon hilarii (their B. microlepis) during the flooding period, which was correlated to a increased ingestion of terrestrial invertebrates, attesting the importance of allochthnous resources for the species. Considering its importance to fisheries, it is remarkable the lack of studies on the reproduction of the species. As most of its congeners, Brycon hilarii undertake upstream migratory during the rainy season, and juveniles of the species are collected in the flooded areas of the Pantanal between December and March (F. A. Machado, pers. comm.). The population occurring in clear-water upper tributaries of the rio Miranda in Mato Grosso do Sul state is said to migrate downstream into the turbid, relatively warm rio Miranda to spawn (Resende, 2011). The species is one of most valued and important targets of both commercial and recreational fisheries of the rio Paraguai basin in Brazil (Ferraz de Lima, 1987; Resende, 2003; Mateus et al., 2004; Mateus et al., 2011). Analyses of microsatellites loci and RAPD markers in populations of B. hilarii from the rio Miranda by Sanches & Galetti (2007, 2012) indicated the presence of a considerable population variability and the presence of specimens distinct from the ones found at local populations in migratory schools, which indicate a considerable population structure, which is unexpected for a migratory species. Remarks. Valenciennes (in Cuvier & Valenciennes, 1850: 247–248) described Chalceus hilarii based on a specimen collected by Auguste de Saint-Hillaire at the “Rio San Francisco”, and also in “plusieurs autres … dans l’Amazone et dans d’autres rivières du Brésil”, collected by Castelnau. The species was primarily diagnosed from its congeners according to Valenciennes (in Cuvier & Valenciennes, 1850) by its small-sized scales—the specimen from the rio São Francisco possessing 80 lateral-line scales. Bertin (1948: 14–15) identified three syntypes for the species, the specimens MNHN A.8616 (Rio São Francisco; A. St. Hillaire) and MNHN A.9893-9894 (“Amazone”; Castelnau). Géry & Mahnert (1992: 815) selected the specimen MNHN A.8616 as the lectotype of the species, and noticed that the paralectotypes of the species were too poorly preserved to confirm their conspecificity with the lectotype. As noticed under the item “Remarks” of Brycon falcatus, the examination of the typical series of Chalceus hilarii showed that these specimens clearly are not conspecific with the lectotype but rather are referrable to B. falcatus. After its original descri