Hyphessobrycon flammeus Myers, 1924

Carvalho, Fernando R., de Jesus, Guilherme C. & Langeani, Francisco, 2014, Redescription of Hyphessobrycon flammeus Myers, 1924 (Ostariophysi: Characidae), a threatened species from Brazil, Neotropical Ichthyology 12 (2), pp. 247-256 : 248-254

Hyphessobrycon flammeus Myers, 1924

Figs. 1-5

Hyphessobrycon flammeus Myers, 1924: 330-331 . Type locality: Rio de Janeiro, Brazil. - Géry, 1977: 458 (classification in artificial group b); 463 (key for the species); 465 (image). -Weitzman & Vari, 1988: 447; 450 (listed as miniature species). -Weitzman et al., 1988: 419-420 (notes about geographic distribution and biogeography). - Mazzoni et al., 2000: 66 (citation for areas of occurrence - fluvial lowland and marsh). -Lima et al., 2003: 137 (check list for the genus). -Lima & Moreira, 2008: 72-73 (threatened species in Brazil, category EN - A2ace; B2ab(iii); historic and biology notes; additional notes about geographic distribution, biogeography and conservation strategies). -Oyakawa et al., 2009: 366 (listed as threatened for São Paulo State, category EN B2abiii; comments about distribution, ecological notes). - Marceniuk et al., 2011: 221; 223-225; 232; 235 (listed).

Diagnosis. Hyphessobrycon flammeus differs from its congeners (except H. bifasciatus , H. balbus Myers, H. chocoensis García-Alzate, Román-Valencia & Taphorn , H. columbianus Zarske & Géry , H. condotensis Regan, H. griemi Hoedeman , H. igneus Miquelarena, Menni, López & Casciotta, H. itaparicensis Lima & Costa, H. panamensis Durbin, H. savagei Bussing , H. sebastiani García-Alzate , Román-Valencia & Taphorn, H. tortuguerae Böhlke , and H. weitzmanorum Lima & Moreira ) by presenting two humeral spots vertically elongated and no caudal peduncle blotch. Hyphessobrycon flammeus differs from aforementioned species by presence of 5-8 maxillary teeth (vs. 1-3 in H. balbus , 1-2 in H. bifasciatus and H. igneus , 3 in H. condotensis and H. panamensis , 2-3 in H. griemi , 1-4 in H. savagei, 2 in H. chocoensis and H. sebastiani , 9-10 in H. tortuguerae), caudal fin hyaline (vs. caudal fin with black median stripe in H. weitzmanorum ), no longitudinal stripe dark and second humeral spot conspicuous as well as first humeral spot (vs. faint longitudinal stripe dark and second humeral spot less defined than first in H. weitzmanorum ).

Description. Morphometric data are summarized in Table 2 . Body compressed, moderately short, greatest body depth at vertical through dorsal-fin origin. Dorsal profile of head convex from tip of upper jaw to vertical through anterior nostril; slightly straight or concave from that point to tip of

supraoccipital spine. Dorsal profile of body slightly convex from posterior tip of supraoccipital spine to base of last dorsal-fin ray, and straight to adipose-fin origin; last dorsalfin ray at vertical through of anal-fin base. Ventral profile of body convex from tip of lower jaw to pelvic-fin origin, straight or slightly convex from that point to anal-fin origin, and straight and/or subtly rounded along anal-fin base. Dorsal and ventral profiles of caudal peduncle slightly straight.

Eyes relatively large compared with head, without distinct adipose eyelid. Lower jaw slightly longer than upper jaw, mouth slightly subterminal. Maxilla extending posteriorly surpassing anterior margin of orbit to vertical through crystalline lens anterior margin, slightly curved, aligned approximately at 45 degrees angle relative to longitudinal axis of body. Nostrils close to each other, anterior opening small and circular, posterior one twice in size and slightly reniform or elongate. Nostrils separated by skin flap. Nasal bone absent. Frontals separated anteriorly, with wide fontanel; parietal fontanel large, extending from epiphyseal bar to supraoccipital spine, slightly narrowed anteriorly. Infraorbital series with four or five elements (probably fifth and sixth, when present, fusioned). Laterosensorial canal of first infraorbital absent, from second to fourth canal close to inner margin of orbital rim. Third infraorbital largest, double size compared to other (in length and depth) and contacting laterosensory canal of preopercle ventrolaterally.

Premaxillary teeth in two rows: outer row with 1*(12) or 2(46) tricuspid teeth; inner row with 5*(57) or 6(1) pentacuspid teeth. Dentary with 4*(59) or 5(1) large, tri- to pentacuspid teeth, followed by 4(1), 5(14), 6(38), 7(6), or 8(1) small, conical or tricuspid, teeth abruptly smaller than anterior largest teeth. Dorsal border of maxilla relatively straight. Maxilla with 5*(35), 6(13), 7(10), 8(4), or 9(1) conical, tri- to pentacuspid teeth along anteroventral margin ( Fig. 3 ). Central median cusp of all teeth longer than remaining lateral cusps; cusp tips slightly curved inward on dentary teeth, and relatively straight on premaxillary teeth.

Scales cycloid, with few and relatively small radii (3- 7); circuli marked anteriorly and marginally (dorsal and ventral). Lateral line incomplete, extending to vertical through middle of pectoral fin; perforated scales 4*(23), 5*(24), or 6(9); longitudinal scales series including pored scales 26(8), 27(1), 28(17), 29(6), 30*(15), 31(4), 32(1), 33*(4), or 34(2); five*(52) or six*(6) scale rows between dorsal-fin origin and lateral line; five*(3) or six*(55) scale rows between lateral line and pelvic-fin origin. Predorsal scales 6(1), 7(1), 8*(27), 9*(14), or 10(15). Scale sheath along anal-fin base in single row of 4(13), 5*(25), 6(11), or 7(6) scales. Circumpeduncular scales 14*(47) or 15(6). Axillary scale absent.

Dorsal-fin rays ii,9*(62) or 10(3); first unbranched ray approximately one-half of second one or shorter.Dorsal-fin origin at midbody or posterior, at vertical through anterior third of pelvic fin base. Base of last dorsal-fin ray at vertical through distal tip of pelvic fin, anterior to origin of anal fin. Tip of longest ray of adpressed dorsal fin at vertical through base of first two branched anal-fin rays. First dorsal-fin pterygiophore inserting between neural spine of 10 th (1) and 11 th (3) precaudal vertebra. Adipose fin present. Pectoral fin with i,9*(2), 10*(40), or 11(11) rays, extending to pelvic fin origin. Pelvic fin with i,6*(43) or 7(22) rays; its origin anterior to vertical through dorsal-fin origin;tip of rays reaching anal-fin origin. Anal-fin rays iv,20(1), 21(3), 22*(11), 23(15), 24(21), or 25(8). Anal fin of males with small bony hooks. Caudal fin forked, lobes slightly rounded, similar in size, i,9/7,i (2), i,9/8,i*(41), or i,10/8,i (1) [one specimen with i,5/5,i, probably anomalous] rays. Caudal fin naked, scales restricted to its base. Dorsal procurrent caudal-fin rays 8(2) or 9(2) and ventral procurrent caudal-fin rays 7(1) or 8(3).

Branchiostegal rays 4. First gill arch with 6(3) or 7(1) gill rakers on epibranchial, 1(4) between epibranchial and ceratobranchial, 8(3) or 9(1) on ceratobranchial, and 2(4) on hypobranchial. Precaudal vertebrae 13(2) or 14(2) and caudal vertebrae 17(1), 18(2), or 19(1); total vertebrae 31(1) or 32(3). Supraneurals 4(2) or 5(2), filiform, some with dorsal portion expanded.

Color in alcohol. Overall body color yellowish to whitish. Dark chromatophores scattered on the lateral portion of head,

more densely concentrated from snout to the supraoccipital. Second and third infraorbitals and upper region of opercular apparatus denser chromatophores, and yellowish adjacent areas. Small chromatophores scattered on the jaws. Two conspicuous vertically elongated humeral spots, extending from the dorsal portion to the pectoral fin, positioned over three to four vertical series of scales above the lateral line and four to five below it, and vertically extending over two to four horizontal series of scales, more intense in the middle of the humeral spot; both spots are separated by two to three horizontal scales. Abdominal region yellowish, with few scattered chromatophores. Lateral side of the body scattered melanophores, dorsal portion with a reticulated pattern on the posterior margin of its scales. Midlateral body stripe absents. All fins hyaline or slightly dark (see more details for males in sexual dimorphism).

Color in life. Overall, body with an intense reddish color (hence the name flammeus , from latin, red - flame-colored). More intense concentration of erythrophores between verticals from the dorsal and/or pelvic-fin to anal-fin end. Distribution of melanophores on its head, flank and fins similar to the one described in alcohol coloration. Dorsal and dorsolateral regions of body rosaceous and orangish. Ventral area of its head up to its posterior humeral spot, including the abdominal region, slightly grayish to yellowish. Sometimes, the upper area of its head up to its first humeral spot with iridescent blue hues. All fins reddish, no pigmentation on the middle caudal-fin rays; caudal and anal fins with a more intense color. Males with black pelvic and anal fins tips and whitish dorsal fin (vs. absent in females) ( Fig. 4 ).

Sexual dimorphism. Males of Hyphessobrycon flammeus present bony hooks in the anal and pelvic fins ( Fig. 5 ) (vs. absent in females). Small, simple bony hooks in the anal fin, extending from the last unbranched ray to the last branched rays, i.e., in all fin rays ( Fig. 5a for the first bony hooks in the anal fin); pelvic fin with hooks in the first two or three branched rays ( Fig. 5b ). Distal portion of its anal fin slightly straight in males (vs. anteriorly falcate in females) ( Fig. 2 ). Males normally smaller than females, but present a bright reddish color, with black tips on pelvic and anal fins. Darkish dorsal fin in the middle portion and whitish on the tip in both males and females. Gill glands (Burns & Weitzman, 1996) were not found macroscopically on first gill arch on both sexes.

Distribution. Hyphessobrycon flammeus has occurrence in streams and coastal rivers of Rio de Janeiro State, in Guanabara bay basin, middle rio Paraíba do Sul basin and rio Guandu basin. In the upper rio Tietê drainage (upper rio Paraná basin, São Paulo State) it is found around of the metropolitan region of São Paulo city ( Fig. 6 ).

Ecological notes. Hyphessobrycon flammeus has been reported in small streams of slow flowing, dark-brown or clear water, shaded by small forest (Myers, 1944). Recently, it has been found in upper rio Tietê drainage, in small streams of clear water and sandy bottom, as well as in the marginal portions of rio Tietê (Lima & Moreira, 2008).

Life expectancy is around four years. In its natural habitat it forms relatively numerous schools with agonistic interaction among alpha males. The species prefer environments with vegetation and streams with slow flowing water, living in depths not superior to 50 cm, and water temperature from 22°C to 28°C. Its diet includes small insects, ‘worms’, and plants (Miranda et al., 2012). The c&s stomach contents of four specimens contained aquatic insects, mainly Chironomidae larvae, and fine organic matter.

During reproduction, the female deposits around 200 to 330 oocytes on rocks, plants, or submerged debris; after that, the male releases the sperm for fecundation. The eggs hatch in approximately 2-3 days (Miranda et al., 2012). Further ecological/biological information can be found in Myers (1924, 1945), Lima & Moreira (2008) and Oyakawa et al. (2009). On the Wide World Web, there is plenty of information shared among aquarists about behavior, reproduction, and many other biological characteristics of H. flammeus , including information on keeping and reproducing them in captivity.

Conservation remarks. Hyphessobrycon flammeus has been in the Brazilian list of threatened fish species since 2004 ( Diário Oficial da União, 2004), category EN-A2ace; B2ab(iii) (i.e., endangered species). However, after the last evaluation conducted by ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) (in 2012, unpublished data) the category EN will be maintained, but the criteria will be changed.

Notwithstanding its relative abundance in upper rio Tietê drainage streams, it is not common in the region of Rio de Janeiro State as referred in the material which was examined herein and mentioned by Lima & Moreira (2008). Therefore, in order to preserve its original population, it will continue as a threatened species, and public policies should prioritize its maintenance and conservation.

Popular names. Due to its popularity in the aquarium trade, Hyphessobrycon flammeus is known by many different names in the world, such as ‘engraçadinho’, ‘lambarizinho vermelho’, ‘Rio tetra’, ‘tetra-rio’, ‘tetra-rosa’, ‘tetra-vermelho’, and ‘vermelhinho’ ( Brazil), flame tetra ( USA and Philippines), ‘ognennaya tetra’ ( Russian Federation), ‘punatetra’ ( Finland), ‘red tetra’ ( USA), ‘rød Rio’ ( Denmark), ‘roter von Rio’ ( Germany) (Lima & Moreira, 2008; Froese & Pauly, 2013).

Phylogenetic reconstruction. Phylogenetic analysis, according to implied weighting procedures (Mirande, 2009, 2010), with consensus of “k” = 9.99804 (three trees) and “k” = 10.97824 (three trees) values, resulted in one tree with 2209 steps, consistency index (CI) of 0.17 and retention index (RI) of 0.66.

In this hypothesis, H. flammeus is the basal species of the clade 196 of Mirande (2010), i.e., ( H. flammeus (( Aphyocharacinae ( Aphyoditeinae , Cheirodontinae )) Stevardiinae )). Synapomorphies for this clade are: ch. 53:1 - length of supraoccipital spine extends only to anterior limit of neural complex; ch. 266:0 - two dorsal-fin rays articulating with first dorsal pterygiophore; ch. 363:1 - number of 2n chromosomes, 52 or more.Autapomorphies for H. flammeus are: ch. 33:1 - nasal bone absent; ch. 58:1 - bony lamellae bordering laterosensory canal of first infraorbital absent; ch. 99:0 - posterior extent of maxilla not reaching second infraorbital; ch. 168:2 - foramen in posterior region of metapterygoid in form of incomplete arch, bordered posteriorly by hyomandibula; ch. 201:1 - denticles on gill rakers absent; ch. 253:1 - position of ventral end of posttemporal posterior to lateral margin of epioccipital; ch. 305:0 - anterior ventral procurrent caudal-fin rays paired, only distally fused; ch. 332:1 - posterior attachment of A1 section of adductor mandibulae restricted or almost restricted to horizontal arm of preopercle; ch. 342:1 - second humeral spot present as a conspicuous vertical bar.

Examined material. Syntypes. USNM 92969 , 2 (2), 24.1-25.4 mm SL, Brazil , Rio de Janeiro State, vicinity of Rio de Janeiro, R. Brooca [probable], aquarium bred, no date. Non-types : All from Brazil. Rio de Janeiro State: Guanabara bay basin. MNRJ 8795 , 16 , 8.6-19.2 mm SL, floodplain near to Imbariê, Baixada Fluminense, L. Travassos, H. S. Lopes & H. Travassos,

04 Aug 1954. Middle rio Paraíba do Sul basin. MNRJ 19543, 20, 14.3-17.1 mm SL, 47 older road Rio-São Paulo, 15 Dec 1972. Rio Guandu basin: MZUSP 51020, 1(1), 17.8 mm SL, Itaguaí, ribeirão da Ponte do Teixeira, on road Itaguaí/Raiz da Serra, Km 5, 08 Sep 1969. ZUEC 4253, 7, 15.7-20.4 mm SL, Itaguaí, 15 Dec 1972. São Paulo State: rio Tietê drainage, upper rio Paraná basin. LBP 8890, 1(1), 21.0 mm SL, Salesópolis, rio Tietê, 10 Sep 2009. LBP 8905, 31 of 45 (31), 16.6-21.8 mm SL, Biritiba Mirim, rio Tietê, 10 Sep 2009. MCP 20235, 1, 19.5 mm SL, Mogi das Cruzes, Tietê, rio Taiaçupeba near electric plant of Tijuco Preto in Taiaçupeba, 12 Jan 1997. MCP 20237, 7 of 15, 13.2-20.9 mm SL, Biritiba Mirim, first stream in road from Biritiba Mirim to Casa Grande, 13 Jan 1997. MCP 20239, 3, 18.9-20.8 mm SL, Mogi das Cruzes, stream on road of Mogi das Cruzes to Salesópolis, ca. 8 km of Mogi das Cruzes, 13 Jan 1997. MCP 25545, 2, 15.5- 25.4 mm SL, Biritiba Mirim, Mogi das Cruzes, stream on road to Biritiba Mirim/Casa Grande, affluent of Ponte Nova Dam in the rio Tietê, 17 Dec 1999. MNRJ 39230, 1, 26.9 mm SL, Mogi das Cruzes, district of Natureza de Taiaçupeba, headwater of rio Grande, 07 Nov 2011. MNRJ 39235, 21, 14.2-29.4 mm SL, Mogi das Cruzes, stream tributary of rio Jundiaí together junction of road for fazenda rio Grande with municipal road TaiaçupebaBertioga , 07 Nov 2011. MNRJ 39240 , 31 , 11.8-23.6 mm SL, Mogi das Cruzes, headwaters of rio Jundiaí , fazenda do Sr. Celso Meida , 07 Nov 2011. MZUSP 86925 , 6 of 7 (6), 16.2-18.2 mm SL, Biritiba Mirim , in the area of VCN Mining , 21 Mar 2005. MZUSP 88175 , 1 (1), 12.6 mm SL, Embu , stream affluent of rio

Embu with empties in reservoir of Guarapiranga , 23 Aug 2005. MZUSP 88183 , 17 , 14.0- 24.4 mm SL, Itapecerica da Serra , stream affluent of rio Embu-Mirim , near deposit of construction material Lagoa , on road João Rodrigues de Morais , 23 Aug 2005. MZUSP 88190 , 1 (1), 13.5 mm SL, Itapecerica da Serra , stream affluent of rio Embu-Mirim , on road João Rodrigues de Morais , Lagoa neighborhood, 23 Aug 2005. MZUSP 88198 , 1 (1), 17.1 mm SL, Itapecerica da Serra , stream affluent of rio Embu-Mirim , Lagoa neighborhood, 23 Aug 2005. MZUSP 88207 , 19 (10, 1 c&s, 11.2- 19.6 mm SL), 9.6-19.6 mm SL, stream affluent of Guarapiranga dam, on road of Jaceguava , near soccer stadium, Casa Grande neighborhood, 24 Aug 2005. MZUSP 90285 , 28 , 12.7 -21.0 mm SL, São Paulo, Embu , stream affluent of rio Embu , 25 Mar 2006. MZUSP 90292 , 31 (10, 2 c&s, 17.5-26.1 mm SL), 17.5-26.1 mm SL, Embu , stream affluent of rio Embu-Mirim , near deposit of construction material Lagoa , on road João Rodrigues de Morais , 25 Mar 2006. MZUSP 90309 , 14 , 11.4-22.3 mm SL, São Paulo, stream affluent of Guarapiranga dam, on road of Jaceguava , near soccer stadium, 26 Mar 2006. MZUSP 95314 , 34 , 16.8-22.7 mm SL, Embu , ribeirão Embu (lowland), 29 Aug 2007. MZUSP 99700 , 54 , 14.6-28.7 mm SL, Embu , stream affluent of Ribeirão Embu- Mirim , stake 34101 of lot 5 Rodoanel Mário Covas (upstream), 21 May 2008. MZUSP 101342 , 2 , 20.4-20.7 mm SL, Itapecerica da Serra , ribeirão Itaquaxiara , affluent of rio Embu-Mirim , near road of Pedreira , Lagoa neiborhood, 18 Nov 2008. MZUSP 101345 , 46 , 14.8-21.9 mm SL, Embu , stream affluent of rio Embu-Mirim , stake 34101 of lot 5 Rodoanel Mário Covas , 02 Feb 2009. MZUSP 102799 , 3 , 19.9-21.7 mm SL, Biritiba Mirim , in the area of VCN Mining , 13 Mar 2009. MZUSP 102803 , 5 , 17.0- 17.8 mm SL, São Paulo, Biritiba Mirim , Tietê , rio Tietê , in the area of VCN Mining , 13 Mar 2009. MZUSP 109043 , 26 , 11.2-16.5 mm SL, Itapecerica da Serra , ribeirão Itaquaxiara , affluent of rio Embu-Mirim , near road of Pedreira , Lagoa neighborhood, 21 Aug 2009. MZUSP 109046 , 2 , 18.4 -23.0 mm SL, Itapecerica da Serra , ribeirão Itaquaxiara , affluent of rio Embu-Mirim , near road of Pedreira , Lagoa neighborhood, 06 Nov 2009. MZUSP 109052 , 46 , 9.9 -21.0 mm SL, Embu , stream affluent of ribeirão Embu-Mirim , stake 34101 of lot 5 Rodoanel Mário Covas (upstream), 06 Apr 2009. MZUSP 109053 , 29 , 12.8-22.9 mm SL, Embu , stream affluent of ribeirão Embu-Mirim , stake 34101 of lot 5 Rodoanel Mário Covas (upstream), 19 Dec 2008. MZUSP 109054 , 17 , 10.7-16.6 mm SL, Embu , stream affluent of ribeirão Embu-Mirim , stake 34101 of lote 5 Rodoanel Mário Covas (upstream), 15 Sep 2009. MZUSP 109055 , 16 , 17.8-24.5 mm SL, Embu , stream affluent of ribeirão Embu-Mirim , stake 34101 of lot 5 Rodoanel Mário Covas (upstream), 19 Marc 2009. MZUSP 111018 , 11 , 14.3- 20.5 mm SL, São Paulo, rio Embu-Guaçu , 04 Apr 2012. ZUEC 3560 , 9 , 12.1-18.3 mm SL, Mogi das Cruzes, Taiaçupeba , 18 Fev 1978. ZUEC 4439 , 10 , 13.7-20.2 mm SL, Mogi das Cruzes, rio Jundiaí , I. Sazima & M. Sazima, 21 Jul 1977. ZUEC 4624 , 10 , 10.8-22.2 mm SL, same locality as ZUEC 3560. Indeterminate locality: MHNG 857.64 , 1 , 27.7 mm SL, aquarium probably, no date. MHNG 2178.79 , 2 , 23.6-23.8 mm SL, aquarium, Zoology Museum Copenhagen, Apr 1970. MHNG 2178.077 , 2 , 22.5 -26.0 SL, aquarium, 1958. MHNG 2742.088 , 6 , 15.8-20.4 mm SL, aquarium specimens, 24 Fev 1961. MZUSP 87148 , 11 (6, 1 c&s, 18.2-20.0 mm SL), 16.5-20.0 mm SL, aquarium, no date .

Figures

Fig. 1. Hyphessobrycon flammeus, USNM 92969, syntype, 25.6 mm SL, vicinity of Rio de Janeiro, Rio de Janeiro State, Brazil. Scale bar = 2 mm. Photo by Sandra Raredon.

Fig. 2. Hyphessobrycon flammeus, LBP 8905, upper rio Tietê drainage, Biritiba Mirim, São Paulo State: (a) male, 19.1 mm SL (with a cyst nematode on upper lobe of caudal-fin), and (b) female, 20.1 mm SL. Scale bars = 2 mm.

Fig. 3. Hyphessobrycon flammeus, MZUSP 90292, 22.0 mm SL, scanning electronic micrograph of lower and upper jaws, left side. Scale bar = 0.3 mm.

Fig. 4. Hyphessobrycon flammeus, live specimens of (a) female and (b) male. Photos and copyrights by Peter Hoffmann and Martin Hoffmann..

Fig. 5. Hyphessobrycon flammeus, MZUSP 90292, 22.0 mm SL, bony hooks in (a) anterior portion of anal-fin rays and (b) in the two first branched pelvic-fin rays.

Fig. 6. Geographic distribution of Hyphessobrycon flammeus in the Rio de Janeiro and São Paulo States. Some symbols can represent more than one lot or locality.