Gymnotus carapo Linnaeus 1758

Albert, James S., 2017, Revision of the polytypic electric fish Gymnotus carapo (Gymnotiformes, Teleostei), with descriptions of seven subspecies, Zootaxa 4318 (3), pp. 401-438 : 418-425

Gymnotus carapo Linnaeus 1758

Figure 3 , Tables 3 and 4

Gymnotus carapo ( Linnaeus 1758) : 246 (in part) (type locality: America). Gymnotus albus (Pallas 1769) : 35 (Suriname).

Gymnotus brachiurus (Bloch 1786) : 61, plate 157 (Brazil).

Gymnotus fasciatus (Pallas 1767) : 35 (Brazil: Roraima, Rio Branco). Gymnotus putaol (Lacépède 1800) : 145, 176 (Brazil).

Syntypes: NRM 64 (1), 262 mm; NRM 8224 (1), 331 mm; UUZM Linn. coll. 56 (1), 293 mm. Collected in the first half of the 18th Century near Paramaribo, Suriname (Lönnberg 1896:23; Fernholm & Wheeler 1983:216–217; Wheeler 1991:162–163, Figure 6 ).

Diagnosis: Gymnotus carapo differs from all members of the G. carapo clade except G. arapaima and G. interruptus in possessing 16–25 (mode=20) dark, obliquely-oriented pigment band-pairs, with irregular wavy margins, often broken into spots above lateral line on anterior half of body (shared only with G. inaequilabiatus , G. arapaima and G. diamantinensis ), without large pale blotches on head. Gymnotus carapo further differs from all members of the G. carapo clade by possessing the following unique combination of traits: 1, circular scales, about as long as wide above lateral line at midbody; 2, two laterosensory canal pores in posterodorsal corner of preopercle (in specimens 120–400 mm); 3, deep body (BD 42.7%–106.6% HL, mean 85.4% vs. 63.4%–133.3% TL, mean 86.5% in all other members of the G. carapo clade); 5, head length moderate to long (HL 10.2%–15.5% TL, mean 11.9% vs. 8.5%–14.3% TL, mean 11.2% in all other members of the G. carapo clade); 6, moderate size of scales over anal-fin pterygiophores (APS 6–10, mode 8 vs. 4–13, mode 8 in all other members of the G. carapo clade); 7, moderate number of lateral line scales to first ventral ramus (PLR 35–56, m median 47 vs. 27–65, median 45 in all other members of the G. carapo clade); moderate number of precaudal vertebrae (PCV 30–36, mode 34 vs. 31–40, mode 33 in all other members of the G. carapo clade); relatively few ventral lateral line rami (VLR 15–24, median 19 vs. 0–37, median 16 in all other members of the G. carapo clade); no dorsal lateral line rami.

Description: Shapes and pigment patterns specimens representing each of the G. carapo subspecies are presented in Figure 3 . Morphometric data in Table 3, and meristic data in Table 4. Large total length, to 360 mm. Sexual maturity at roughly 280 mm (males), 270 mm (females). Sexually monomorphic, including in breeding condition. Scales rounded to slightly ovoid, present on entire postcranial portion of body. Gape large in mature specimens, to or beyond posterior nares. Mouth superior with lower jaw longer than upper, rictus decurved. Chin fleshy and protuberant with fleshy pad of electrosensitive organs overlying tip of snout and oral jaws. Anterior narial pore partially to entirely included within gape in narial fold. Anterior nares large, subequal to eye diameter. Circumorbital series ovoid or tear-drop shaped. Ethmoid region broad between Anterior nares, with rounded anterior margin. Eye position lateral, lower margin of eye dorsal or horizontal to rictus. Premaxilla with 11–16 (mode 14) teeth disposed in single row along outer margin, arrow-head shaped Anteriorly, conical posteriorly. Curved median margin of premaxilla. Maxilla-palatine articulation near Anterior tip of endopterygoid. Maxilla vertical, rod-shaped, narrow distally with a straight ventral margin, length equal to roughly width of four–six dentary teeth. Dentary with one row of 16–19 (mode 17) teeth, two–four arrow-head shaped Anteriorly, all others conical posteriorly. Posterodorsal and posteroventral dentary processes abut at midlength. Dentary posteroventral process nearly as long as posterodorsal, narrow distally. Dentary ventral margin lamella narrow, depth less than posterior process. Dentary anteroventral margin rounded in lateral view, without a hook. Opercle dorsal margin straight to slightly convex. Dorsal opercular process lamellar or rugose, crest absent or small, posterior margin entirely smooth, without spines or processes. Ventral ridge field of opercle broad, dorsal ridge field long, more than one-half width of opercle. Preopercle with anteroventral notch, posterodorsal laterosensory ramus with two superficial pores, margin of medial shelf entire, median shelf large, more than one-half width of symplectic. Metapterygoid superior and inferior portions approximately equal in size, ascending process robust, long, base shorter than length, curved, tip simple. Interopercle dorsal margin ascending process broad. Subopercle dorsal margin concave. Retroarticular with an arched lamella posteriorly forming a small canal, posterior margin square. Anguloarticular process long, extending beyond ventral margin of dentary. Mandible long, extended, length greater than twice depth. Trigeminal nerve canals connected within the hyomandibula. Posterior lateral line fenestra contacting posterodorsal margin of hyomandibula. Cranial fontanels closed in juveniles and adults. Frontal shape narrow, width at fourth infraorbital less than that of parietal, Anterior margin of straight, continuous with margins of adjacent roofing bones, postorbital process broad, more than two times width of supraorbital canal. Lateral ethmoid absent. Parietal rectangular, length less than width. Parasphenoid anteroventral portion robust, extending ventral to lateral margin of parasphenoid, posterior processes narrow. Prootic foraminae separate for cranial nerves Vp and V2–3 +VII. Adductor mandibula muscle undivided at insertion, intermuscular bones absent. All basibranchials unossified. Gill rakers not contacting gill bar.

Pectoral fin of moderate size, with 13–17 rays, medial radial large. Mesocoracoid elongate, length more than four times width. Cleithrum narrow, ventral margin straight, anterior limb long, more than 1.8 times ascending limb, deeply incised on its anteroventral margin, without large facet for insertion of muscle from supracleithrum. Postcleithrum thin, discoid or sickle shaped. Body cavity of moderate length, with 30–36 (mode 34) precaudal vertebrae. Rib Five robust along its entire extent, less than three times width of rib Six. Hemal spines present. Displaced hemal spines absent. Length anal-fin pterygiophores equal to or longer than hemal spines. Anal fin of moderate length, with 173–315 (median 238) rays. Multiple branched anal-fin rays posterior to rays 10–17. Lateral line ventral rami 15–24, median 19 (left or right), lateral line dorsal rami absent in adults. Caudal appendage short, less one-half length of pectoral fin. Single hypaxial electric organ along entire ventral margin of body. Three or four (mode four) rows of electroplates near caudal insertion of anal fin.

Color in Alcohol: Bands irregular in shape, width and color, on specimens, individuals and regional subspecies. All specimens examined possess the following coloration: ground color tan ventrally grading to darker brown dorsally in adults (200–300 mm), pale yellow throughout in smaller specimens. Obliquely-oriented, chocolate-colored bands with wavy, irregular margins on lateral surface from nape and to tip of caudal appendage, occurring singly or as band-pairs, increasingly divided and irregular with size (16–28 mode 21). Band-interband contrast increases ventrally and caudally, fades with growth (juveniles> 150 mm with distinct margins, specimens 200– 200 mm faintly banded, and some specimens over 250 mm unbanded except very faintly in posterior one-third of body). Pale inter-bands roughly one-third width of dark bands at mid-body. Bands may be divided dorsally or ventrally to form X or inverted Y-shaped patterns. Head never banded, spotted, or blotched, dark brown grading to lighter brown dorsally to ventrally. Numerous chromophores speckled over branchiostegal membranes and ventral surface of head. Pectoral-fin rays brown, interradial membranes hyaline. Anterior 80% of anal fin membrane dark brown, gray or black, posterior 20% translucent. Specimens fixed in 10% formalin and preserved for 1–5 years in 70% ethanol maintain approximate colors of life, although darker pigments tend to pale with time.

Ecology: Gymnotus carapo occurs in floating macrophytes, shallow waters and seasonally flooded forests with little or no flow where they frequently exhibit aerial respiration using the vascularized posterior chamber of the gas bladder ( Liem et al. 1984). Gymnotus carapo breeds during the wet season ( Barbieri & Barbieri, 1982, 1985; Cognato & Fialho, 2006) and has been reported to mouth brood (Kirschbaum & Wieczorek 2002). Gymnotus carapo are known to undertake nesting and paternal care (Crampton & Hopkins 2003). In floodplains, juvenile specimens are found in patches of floating macrophytes along channel and lake margins. Juveniles feed primarily on small aquatic insects and crustaceans; especially chironomid larvae, Odonata and Coleoptera larvae and Choncostraca, whereas adults consume larger animals such as shrimps and fishes ( Ellis 1913, Saul 1975).

Within and among populations of G. carapo , head length is negatively correlated with body depth, such that individuals with a longer head tend to have a more-slender body in lateral profile. This pattern is similar to observed among members of the G. carapo clade as a whole, with long-headed species like G. arapaima having a more-slender body, and short-headed forms like Gymnotus CALA and G. ucamara having deeper bodies. This observation suggests the presence of an eco-morphological tradeoff between a long-headed, midwater piscivorous phenotype and a short-headed generalist, substrate-probing phenotype.

Karyotypes: Reported karyotypes of G. carapo vary substantially across its geographic range, from 2n=40 to 81, including: 2n=40 or 42 in G. c. orientalis from Pará State, Brazil ( Milhomem et al., 2007, 2008), 2n= 48 in G. c. madeirensis from the Rio Humaitá in the Madeira basin, Amazonas State, Brazil ( Milhomem et al., 2012a), 2n= 52 in G. c. australis from the Upper Paraná in São Paulo State, Brazil (G. “ inaequilabiatus ” of Milhomem et al., 2012; 2013), 2n= 54 in G. c. australis from the Pantanal of the Upper Paraguay basin, Paraguay ( Scacchetti et al., 2011), and 2n= 81 in G. c. australis from the Mojiguaçu River in São Paulo State, Brazil (Milhomem et al., 2012). These data suggest that G. carapo exhibits a polytypic karyotype (sensu Allendorf and Leary, 1988) across its range, although Milhomem et al. (2008) argue that sympatric 2n=40 and 2n=42 populations of G. c. orientalis from Pará represent cryptic species.

Reported karyotypes in other species of the G. carapo clade include: 2n= 34 in G. capanema from Pará State, Brazil, 2n=39 or 40 in G. pantanal from the Parana basin in southeastern Brazil, 2n= 40 in G. sylvius from the Upper Paraná and Ribeiro de Iguape in southeastern Brazil, 2n= 44 in G. arapaima from central Amazonas State, Brazil, 2n= 54 in G. mamiraua from central Amazonas State, Brazil, 2n= 54 in G. paraguensis from the Upper Paraná, São Paulo State, Brazil ( Milhomem et al., 2012a, b; 2013).

Clade Species / TL HL HL% PR %

Subspecies n min max mean n min max mean n min max mean n min max mean carapo G. carapo 158 110.0 419.0 211.9 158 13.4 56.2 25.4 158 10.2 15.5 11.9 111 31.0 40.1 35.4 carapo G. carapo Clađe 486 79.0 430.0 187.9 487 7.9 56.2 21.5 485 8.5 15.5 11.4 426 27.7 49.8 35.0 tigre G. tigre Clađe 36 130.0 645.0 293.6 36 13.5 58.2 31.2 35 8.9 13.3 10.7 36 34.0 39.9 37.4 ……continued on the next page. carapo G. carapo 144 31.4 49.0 41.3 107 55.0 66.9 62.2 145 29.1 44.8 37.9 152 42.7 106.6 85.4. carapo G. carapo Clađe 457 17.0 58.0 40.5 415 53.2 83.8 61.9 456 23.3 50.3 39.0 454 42.7 133.3 86.2. tigre G. tigre Clađe 36 37.2 49.4 42.9 35 57.7 63.1 61.2 35 31.1 50.8 43.3 35 67.7 100.6 86.4 ……continued on the next page Clade Species / TL BND AFR P1R

Subspecies n min max mean n min max mode n min max mode n min max mode. carapo G. carapo 158 110.0 419.0 211.9 88 16 25 20 58 173 315 238* 94 13 17 16*. carapo G. carapo Clađe 486 79.0 430.0 187.9 371 0 35 21 242 139 322 235* 307 11 22 16 *. tigre G. tigre Clađe 36 130.0 645.0 293.6 24 13 29 23 22 190 390 370* 32 15 21 17

……continued on the next page carapo G. carapo 62 5 8 6 55 3 4 4 22 6 10 8 43 30 36 34

carapo G. carapo Clađe 275 4 10 7 213 3 4 3 194 4 13 8 148 30 40 33

tigre G. tigre Clađe 32 5 13 9 24 3 6 4 32 9 16 12* 15 32 48 45* ……continued on the next page

Figures

FIGURE 3. Specimens illustrating variation in body shape and color pattern among seven subspecies of Gymnotus carapo A. G. c. australis, MLP 11222, 289 mm, Argentina, Misiones province, Río Iguazú basin, Arroyo Verde (25 ° 40 ’ 15 ” S, 053 ° 56 ’ 00.8 ” W); B. G. c. caatingaensis, AUM 20624, 225 mm. Brazil, Piauí, Río Gurgueia aff. Río Parnaíba (08 ° 32 ’ 24 ” S, 044 ° 25 ’ 48 ” W); C. G. c. carapo, UMMZ 190414, 146 mm. Suriname, Brokopondo, Marshal Kreek, aff. Suriname River (05 ° 14 ’ 24.9 ” N, 055 ° 05 ’ 58.6 ” W); D. G. c. madeirensis, UMSS 0 6964, 178 mm. Brazil, Amazonas, Río Beni (10 ° 51 ’ 44.302 ” S, 066 ° 04 ’ 50.300 ” W); E. G. c. occidentalis, UF 122820, 279 mm. Peru, Loreto, Iquitos (03 ° 43 ’ 51.73 ” S, 073 ° 15 ’ 3.83 ” W); F. G. c. orientalis, MCZ 45189, 165 mm. Brazil, Para, Parauapebas, Río Arari, Ilha de Marajó (01 ° 01 ’ S, 048 ° 58 ’ W); G. G. c. septentrionalis, ROM 83885, 233 mm. Guyana, Essequibo, Río Mazaruni (04 ° 55 ’ 33.208 ” N, 060 ° 36 ’ 53.784 ” W). Scale bars = 10 mm.

FIGURE 6. Principal components analysis of point-to-point linear measurements for five sympatric Gymnotus species from the southern humid Neotropics: G. c. australis (n = 25), G. chimarrao (n = 4), G. omarorum (n = 18), G. sylvius (n = 5) and Gymnotus CALA (n = 68). Head length (HL) and head depth (HD) load heavily on PC 1, while preorbital distance (PR) and postorbital distance (PO) load heavily on PC 2. Note the greater separation in PC space than is observed among G. carapo subspecies.