Brachyhypopomus draco, Giora & Malabarba & Crampton, 2008

Giora, Julia, Malabarba, Luiz R. & Crampton, William, 2008, Brachyhypopomus draco, a new sexually dimorphic species of Neotropical electric fish from southern South America (Gymnotiformes: Hypopomidae), Neotropical Ichthyology 6 (2), pp. 159-168 : 161-165

Brachyhypopomus draco , new species

Figs. 1 , 2

Holotype. MCP 41540, 1 (male, 137.3 mm LEA), Brazil, Rio Grande do Sul, Parque Estadual de Itapuã, lagoa Verde (30°22’52.4"S, 51°01’25"W), 12 Jan 2004, D. Cognato, L. R. Malabarba, C. E. Machado & R. Q. Carvalho.

Paratypes. All from Brazil, Rio Grande do Sul. Laguna dos Patos drainage: MCP 41539, 1 (male, 147.1 mm LEA), collected with the holotype. UFRGS 8888 , 1 (male, 126.4 mm LEA), same locality of the holotype, 18 Jan 2006, J. Giora, A. P. Dufech & J. Ferrer. MNRJ 30916 , 2 (1 male, 151.8 mm LEA, 1 female, 128.4 mm LEA), same locality of the holotype, 9 Feb 2004, D. Cognato, M. Azevedo, A. Schaan & C. Hiroshi. MCP 41538, 2 (1 male, 88.4 mm LEA, 1 female, 91.7 mm LEA), same locality of the holotype, 30 Jun 2004, D. Cognato & A. Schaan. MNRJ 30917 , 1 (male, 150.2 mm LEA), MZUSP 94429 , 1 (male, 139.1 mm LEA), same locality of the holotype, 9 Sep 2004, D. Cognato, M. Schossler & A. Schaan. MCP 41537, 1 (female, 108.4 mm LEA), same locality of the holotype, 10 Oct 2003, D. Cognato & A. Schaan. MNRJ 30918 , 1 (male, 138.2 mm LEA), same locality of the holotype, 11 Nov 2003, D. Cognato, J. Giora, J. Anza & A. P. Dufech. UFRGS 732 , 1 (female, 78.0 mm LEA), Viamão, arroio Alexandrina (30°6’S, 50°57’W), 7 Sep 1980, L. R. Malabarba. UFRGS 820 , 1 (male, 93.7 mm LEA), Guaíba , açude near BR290 highway (30°07’S, 51°20’W), 4 Nov 1979, L. R. Malabarba, C. F. M. Souto & P. A. Buckup. UFRGS 822 , 1 (male, 92.5 mm LEA), Guaíba , açude in BR290 highway, near junction with BR116 highway (30°03’S, 51°21’W), 18 Jan 1980, P. A. Buckup & C. Souto. UFRGS 6526 , 1 (male, 102.2 mm LEA), UFRGS 6525 , 1 (male, 100.6 mm LEA), Eldorado do Sul , artificial canal near BR290 highway (30°2’55"S, 51°23’34"W), 10 Dec 2003, W. Crampton & L. R. Malabarba. UFRGS 4317 , 1 (male, 50.0 mm LEA), Viamão , arroio Itapuã (30°15’S, 51°02’W), 1 Mar 1988, F. Becker & L. R. Malabarba. Rio Tramandaí drainage: UFRGS 6486 , 1 (male, 85.3 mm LEA), UFRGS 6488 , 1 (male, 98.1 mm LEA), UFRGS 6489 , 1 (male, 100.8 mm LEA), UFRGS 6490 , 1 (female, 95.5 mm LEA), UFRGS 6491 , 1 (male, 80.9 mm LEA), Capão da Canoa , creek parallel to Estrada do Mar road (29°43’9"S, 50°56’0"W), 20 Nov 2003, L. R. Malabarba, J. Giora, J. Anza & D. Cognato. MNRJ 30915 , 2 (1 male, 69.9 mm LEA, 1 female, 85.2 mm LEA), Cidreira , lagoa Fortaleza (30°8’58"S, 50°14’30"W), 11 Jul 2003, L. R. Malabarba. UFRGS 6671 , 3 (2 males, 85.7-107.0 mm LEA, 1 female, 96.3 mm LEA), Terra de Areia , creek into rio Três Forquilhas , along the road RS486 (29°33’22"S, 50°4’19"W), 20 Nov 2003, L. R. Malabarba, J. Giora, J. Anza & D. Cognato. Rio Uruguay drainage: UFRGS 6748 , 1 (male, 90.8 mm LEA), Rosário do Sul , Sanga do Jacaré , BR290 (30°12’4"S, 55°3’17"W), 18 Jun 2004, D. Cognato, W. Crampton, J. Giora & D. Rocha. MZUSP 94428 , 8 (2 males, 95.6- 126.7 mm LEA, 6 females, 51.9-103.94 mm LEA), UFRGS 6753 , 1 (male, 88.3 mm LEA), Rosário do Sul , stream tributary of arroio Gueromana , BR290 (30°1’00"S, 55°23’18"W), 19 Jun 2004, D. Cognato, W. Crampton, J. Giora & D. Rocha. UFRGS 6785 , 4 (2 males, 79.3-105.1 mm LEA, 2 females, 84.5-85.3 mm LEA), UFRGS 6494 , 1 (male, 92.5 mm LEA), UFRGS 6497 , 1 (male, 90.1 mm LEA), Rosário do Sul , sanga do Jacaré , BR290 (30°12’42"S, 55°3’17"W), 26 Nov 2003, L. R. Malabarba, J. Giora, D. Cognato, G. Neves & J. Ferrer. UFRGS 6789 , 4 (2 males, 106.5-126.3 mm LEA, 2 females, 71.5-80.0 mm LEA), Rosário do Sul , stream tributary of arroio Gueromana , BR290 (30°1’0"S, 55°23’18"W), 26 Nov 2003, L. R. Malabarba, J. Giora, D. Cognato, G. Neves & J. Ferrer. UFRGS 6507 , 1 (male, 92.9 mm LEA), UFRGS 6509 , 1 (male, 92.5 mm LEA), UFRGS 6511 , 1 (male, 98.3 mm LEA), São Gabriel , stream tributary of arroio Piraí , BR290 (30°18’56"S, 54°24’22"W), 26 Nov 2003, L. R. Malabarba, J. Giora, D. Cognato, G. Neves & J. Ferrer .

Non-type material. The following specimens were used to record the distribution of the new species, but are not used in the species description and are not part of the type series. However, they do not differ in morphometric or meristic characteristics from the type specimens. Brazil, Rio Grande do Sul: MCP 20215, 5 , and MCP 20217, 3 , Eldorado do Sul ; MCP 20711, 1 , Osório ; UFRGS 7686 , 30 , Viamão , and UFRGS 7707 , 3 , Viamão ; UFRGS 8475 , 4 , Pantano Grande - Rio Pardo ; UFRGS 8938 , 1 , rio Tramandaí ; UFRGS 6780 , 11 , São Gabriel ; UFRGS 6750 , 14 , Rosário do Sul - Alegrete; UFRGS 8263 , 28 , Charqueadas. Paraguay : USNM 181483 , 5 , Pueblo Ybytymi, Departamiento Paraguarí ; ANSP 170412 , 1 , Deparatamiento Missiones ; ANSP 175180 , 1 , Departamiento Missiones. Uruguay: ZVC-P 2727, 1, Departamiento Artigas , lagoa Redonda.

Diagnosis. Brachyhypopomus draco can be distinguished from all described congeners by the extreme broadening of the distal portion of the caudal filament in males during the reproductive period to form a distinct paddle shaped structure (vs. moderately broadened distally in B. pinnicaudatus and B. brevirostris into paddle-shaped structures, and versus broadened along most of the length of the caudal filament in B. occidentalis , B. diazi , B. beebei , and B. janeiroensis ). Brachyhypopomus draco can be further diagnosed from other species of the genus by the following characters: caudal filament length 17.3-35.2% of LEA (vs. 36.5- 50.0% in B. jureiae ; 33.0-50.0% in B. janeiroensis , and 13.3- 20.0% in B. bombilla ); pectoral fin ray length 4.1-5.8% of LEA (vs. 6.7-7.9% in B. pinnicaudatus ); body depth 8.8-12.2% of LEA (vs. 12.1-16.2% in B. pinnicaudatus ); snout length 20.7- 30.0% of HL (vs. 31.7-32.2% in B. jureiae ); gape width 9.5- 16.5% of HL (vs. 17.8-23.1% in B. pinnicaudatus ); interorbital distance 22.7-35% of HL (vs. 14.9-20.5% in B. bombilla ); branchial aperture 16.5-26% of HL (vs. 24.9-31.0% in B. pinnicaudatus ); head width at operculum 48.4-65% of HL (vs. 60.0-73.0% in B. pinnicaudatus ); head width at eyes 31.3- 45.6% of HL (vs. 24.7-31.7% in B. bombilla ); number of anal fin rays 155-198 (vs. 188-211 in B. jureiae ; 251-295 in B. brevirostris ; 214-228 in B. beebei , and 200-240 in B. occidentalis ); upper jaw equal to lower jaw (vs. upper jaw slightly longer than lower jaw in B. bombilla , B. occidentalis , B. diazi , B. brevirostris and B. jureiae ).

Description. Morphometric and meristic data are presented in Table 1. Head conical, nearly triangular in lateral view, snout short, eyes small, mouth terminal with upper jaw equal to lower jaw, no teeth in both jaws. Body slender, slightly laterally compressed. Dorsal profile straight from snout to supraoccipital, slightly convex posteriorly to caudal filament. Ventral profile gently convex from lower jaw to anal-fin origin, slightly convex to nearly straight along anal-fin base. Highest body depth located posterior to anal-fin origin. Body depth increasing smoothly from head to body region near the 30th anal-fin ray, clearly gradually decreasing from that point to caudal filament. Caudal filament moderately short, slender and laterally compressed in females, juveniles and males in non-reproductive period; caudal filament paddle-shaped in sexually mature males (see sexual dimorphism, below). Cycloid scales covering uniformly the body, except head and fins. Scales smaller on all anterior quarter portion of body; posterior scales at dorsal and medial body regions two to four times larger in diameter than anterior ones; smallest scales covering region of anal-fin pterygiophores. First anterior perforated scale of lateral line above pectoral fin origin and lateral line extending to caudal filament tip, hardly discernible. Branchial aperture small and slightly anterior to pectoral fin origin. Anus with the presence of urogenital papilla in males and females, although less developed in juveniles. Pectoral fins rounded with pigmented rays and perpendicular insertion; pectoral-fin rays i-ii + 13-15 (15-17 total pectoral-fin rays, n = 47, median = 16). Anal fin relatively long with vii-xii + 148- 186 rays (155-198 total anal-fin rays, n = 41, mean = 181.3) which are pigmented. Anal-fin origin located posterior to posterior edge of pectoral fin. Precaudal vertebrae 21-23 (20-22 anterior, 1-2 transitional; n= 6).

Coloration in life. General body color brownish varying from dark brown to yellowish brown, dark brown near dorsal mid-

line and clearing ventrally. A highly variable number of dark brown bands, well delineated or not, nearly perpendicular or oblique to longitudinal body axis, running posterodorsally from base of anal-fin rays to nearby lateral line and occurring from head to tip of caudal filament. Anal and pectoral-fin rays speckled brown, with hyaline inter-radial membranes.Adults and juveniles exhibit the same coloration pattern.

Secondary sexual dimorphism. During reproductive period, established through monthly variation analysis of male and female gonads in a B. draco population, males undergo hypertrophy of the distal portion of caudal filament ( Fig. 2 ). This has been observed between August and December in a population studied from the type-locality (A. Schaan, J. Giora and C. Fialho, in preparation). Extremely vertical broadening and lateral compression give the caudal filament a paddle-like shape. After the reproductive period, this structure regresses until the caudal filament resembles those of females and juveniles. In addition, adult males are significantly larger than females.

Electric organ discharge. Brachyhypopomus draco generates a continuous train of pulse-type EODs. Adult specimens (with developing or fully developed gonads) (72.6-105 mm LEA) exhibited the following EOD parameters. The mean EOD repetition rate (per individual) during the day ranged from 15.7-24.6 Hz (mean among all specimens, 19.6 Hz, SD 2.5, n = 11 individuals fishes), with a standard deviation (SD) of 0.4- 1.2 Hz (mean 0.7, SD 0.3, n = 11), and coefficient of variance of 1.8-7.0 % (mean 3.9 %, SD 1.88, n = 11). The lowest and highest absolute pulse rates recorded from all diurnal recordings were 13.7 and 29.2 Hz respectively. During the hours of peak foraging activity, 1-3 hours after sunset, the mean EOD repetition rate (per individual) ranged from 34.2-45.8 Hz (mean among all specimens 38.6 Hz, SD 5.2, n = 6) with a standard deviation of 2.8-10.8 Hz (mean 2.9, SD 1.1, n = 6) and a coefficient of variation of 8.3-27.3 % (mean 20.7 %, n = 6). The lowest and highest absolute pulse rates recorded from all nocturnal recordings were 8.4 and 80.2 Hz respectively.

In sum, adult specimens of B. draco exhibited a distinct increase in pulse rate from the resting day-time state (mean 19.6 Hz) to the nocturnal active state (mean 38.6 Hz). The coefficient of variation of pulse rate during nocturnal activity (mean 20.7 %) was considerably higher than during the day (mean 3.9%) reflecting the greater variability in pulse rate during foraging. Disturbances such as minor vibrations provoked novelty responses, sudden increases in the resting pulse rate from the baseline rate ( Fig. 3). The approximately stable resting diurnal EOD punctuated by novelty responses results in a right-skewed distribution of inter-pulse intervals in a histogram ( Fig. 3). Some specimens of B. draco displayed spontaneous complete cessations of the EOD for periods of up to 1 minute. Normal EOD activity was resumed after these interruptions.

The EODs waveforms of adult specimens of B. draco comprised two components of alternating polarity (P1 and P2) sensu Crampton & Albert (2006), and varied in duration from 1.172 -1.992 ms (mean 1.578, SD 0.147, n = 23) ( Fig. 4). The Peak Power Frequency ( PPF) (see Fig. 4) of these EODs varied from 0.6958 -0.8942 kHz (mean 0.7707, SD 0.0534, n = 23) .

We did not encounter evidence for obvious sexual differences in the EOD waveforms of B. draco , despite evidence for this phenomenon in other species of Brachyhypopomus (e.g. B. occidentalis, Hagedorn, 1985 , Shumway & Zelick, 1988; B. pinnicaudatus Stoddard et al., 2003 ; B. brevirostris, Kawasaki & Heiligenberg, 1989 , Crampton, 1996). Where a sexual difference exists, this is manifest as an elongation of the second negative waveform phase, P2 and a corresponding reduction in the PPF of the EOD. We observed no consistent EOD waveform shape differences. Likewise, we observed no significant difference between the PPF of five sexually mature males (0.7504 -0.8942 kHz, mean 0.8178, SD 0.0675) and 2 sexually mature females (0.7385 -0.7949 kHz, mean 0.7667, SD 0.0399) (2-sample T-test, df = 5, n = 7, P = 0.38). The observation of a lower PPF in mature females than males contrasts with cases of sexual EOD differences in Brachyhypopomus , where sexually mature males invariably display lower PPFs. Nonetheless, we did note that the Spectral Power Densities of the two sexually mature females exhibited a more rapid decline from the PPF than in the five sexually mature males ( Fig. 4). Males and females with developing gonads also exhibited no obvious difference in waveform shape, and no significant difference in the PPF (males: 0.6958 -0.8362 Hz, mean 0.7518, SD 0.0460, n = 10; females: 0.7111 -0.8194 kHz, mean 0.7642, SD 0.0422, n = 6) (2-sample T-test, df = 14, n = 16, P = 0.59). All recorded specimens had been held in social isolation for several days before they were recorded. This is known to minimize the hormonally-induced modulation of the P2 phase in sexually mature males ( Stoddard et al., 2003). Further investigation is required to explore whether EOD differences emerge in males that are exposed to normal social stimuli (i.e. the presence of sexually mature conspecifics).

All recordings presented here were made during the southern summer (December) when ambient water temperature is typically in the range 24 – 30º C. During the winter, water temperatures in Rio Grande do Sul decline to as low as 10º C. We noted that these seasonal temperature changes have a significant impact on the waveform duration and shape of the EODs of B. draco . The PPF of the EOD declines substantially, and the P2 phase becomes diminished in relative amplitude. We will present detailed observations on this phenomenon elsewhere. Loureiro & Silva (2006) discuss the effect of temperature on the EODs of B. bombilla .

Distribution. Brachyhypopomus draco is widely known from central, southern and coastal regions of Rio Grande do Sul state, Brazil, and Uruguay. It is known from three drainages: laguna dos Patos, rio Uruguay and rio Tramandaí, and was also found at two localities in Paraguay (ANSP 170412; ANSP 175180; USNM 181483).

Habitat. Brachyhypopomus draco inhabits river edges, slowmoving creeks, lagoons and flooded areas with muddy or sandy bottom and abundant emergent or floating vegetation. The species was particularly abundant in the type locality, a lagoon (30°22’52.4"S, 51°01’25"W) inside a state preserved area, Parque Estadual de Itapuã in Rio Grande do Sul, Brazil. The lagoon is approximately 4 hectares in area and reaches 1 meter in depth. It has a muddy bottom, abundant macrophytes and vegetal material in various stages of decomposition, and is surrounded by psammophilous forest with strong vegetational influence from Atlantic forest formations ( Fig. 6 ). At the type locality, B. draco was found occurring together with an undescribed Gymnotus (Crampton et al., in prep.).At other collecting sites throughout Rio Grande do Sul state the species was collected along with the gymnotiforms Eigenmannia trilineata , B. bombilla and another undescribed Brachyhypopomus species (see Comparative Material).

Etymology. Name “draco”, from the Greek “drakon” meaning dragon, in reference to the shape of distal portion of caudal filament in mature males, similar to that illustrated in these imaginary creatures.

Figures

Fig. 1. Holotype (MCP 41540, male, 137.3 mm LEA, above) and paratype (MCP 41537, female, 108.4 mm LEA, below) of Brachyhypopomus draco, from Parque Estadual de Itapuã, Rio Grande do Sul, Brazil.

Fig. 2. Brachyhypopomus draco (holotype, MCP 41540, male, 137.3 mm LEA). Detailed images of head, above, and tail, below.

Fig. 6. Typical habitat of Brachyhypopomus draco; marshland in the Parque Estadual de Itapuã, Rio Grande do Sul, Brazil.