Paramormyrops sphekodes, SPHEKODES (SAUVAGE, 1879)

Rich, Madeline, Sullivan, John P. & Hopkins, Carl D., 2017, Rediscovery and description of Paramormyrops sphekodes (Sauvage, 1879) and a new cryptic Paramormyrops (Mormyridae: Osteoglossiformes) from the Ogooué River of Gabon using morphometrics, DNA sequencing and electrophysiology, Zoological Journal of the Linnean Society 180, pp. 613-646 : 626-628

PARAMORMYROPS SPHEKODES ( SAUVAGE, 1879)

Mormyrops sphekodes Sauvage, 1879: 101 . Lectotype: MNHN A 893 , paralectotype: MNHN 1998-1050 . Type locality: Ogooué River at Doumé, Gabon.

Mormyrops sphekodes – Sauvage, 1880: 55, Pl. 2, Fig. 4 . Mormyrus sphecodes – Günther, 1896: 280 Marcusenius sphecodes – Boulenger, 1898b: 793 Brienomyrus (Brienomyrus) sphecodes – Taverne, 1971: 106

Paramormyrops sphekodes – Hopkins et al., 2007: 292–293 [Note: Hopkins et al. (2007: 304; fig. 12.65) erroneously illustrated P. sphekodes using the paralectotype rather than the lectotype. Both specimens are now regarded as the same species (see comparison with existing types, in the following text).]

Redescription of Paramormyrops sphekodes

Because of the confusion surrounding the identity of P. sphekodes , its rarity in our collections from Gabon, and the existence of only two historic specimens from the type locality, we redescribe this species based on the lectotype, paralectotype, four topotypes and five additional specimens from near the type locality .

Lectotype: MNHN A. 893, 113.87 mm SL, male. Type location: Gabon, Ogooué-Lolo, Ogooué River at Doumé (modern GPS coordinates: 0.84137°S, 12.96548°E). A. Marche, late 1876–early 1877.

Paralectotype: MNHN 1998-1050 , 96.7 mm SL, female. Type location: Gabon, same location and date as lectotype .

Topotypes (4): Rapids in front of the village of Doumé on the Ogooué River (0.84137°S, 12.96548°E) : CUMV 96810 (1, specimen no. JPS-1118) 117.7 mm SL. J.P. Sullivan, 29 May 2011 ; MRAC B5-26 -P-2 (1, specimen no. JPS-1192) 113.5 mm SL. J.P. Sullivan, 17 September 2014 ; AMNH 264378 (1, specimen no. JPS- 1193) 94.5 mm SL. J.P. Sullivan, 17 September 2014 ; MNHN 2015-0257 (1, specimen no. JPS-1201) 111 mm SL. J.P. Sullivan, 17 September 2014 .

Other specimens (5): Five specimens included here are from a site close to the type locality. Sébé River, 45 km

south-east of Doumé, Ogooué-Lolo, Gabon (0.93442°S, 13.35777°E) J.P. Sullivan, 20 September 2014: MNHN 2015-0258 (1, specimen no. JPS-1214) male, 112.5 mm SL ; AMNH 264377 (1, specimen no. JPS-1216) male, 110 mm SL ; CUMV 98161 (1, specimen no. JPS-1219) female, 118.3 mm SL ; MRAC B5-26 -P-1 (1, specimen no. JPS-1230) male, 133 mm SL ; 22 September 2014; CUMV 98177 (1, specimen no. JPS-1238), male, 119.5 mm SL .

Diagnosis: Paramormyrops sphekodes is distinguished from all other Paramormyrops by this combination of characters: 5 teeth in upper-jaw, 6 in lower; 12 circumpeduncular scales; sharp head profile, V-shaped when viewed from above; snout angle 48–56° corresponding to an interorbital width 1–1.36 times the snout length; BD 15.4 – 17.31 % SL, BD at pectoral fin 84–94% BD at urogenital pore; eye diameter 13–16% HL measured from snout tip to posterior edge of bony operculum; snout length 24–27% HL; ratio of HL to depth (HLx/ HDx, measured from radiographs) 1.1–1.24; HL 21–23% SL; EOD waveform with two phases, head-positive then negative, EOD duration 1.635 ± 0.226 ms with a corresponding power spectrum peak at 1573 ± 531 Hz; electric organ composed of type NPp electrocytes, that is having N on- P enetrating stalks innervated on the p osterior face of the cell ( Hopkins, 1999) .

Comparison with other Paramormyrops: With five teeth in the upper jaw and six in the lower, P. sphekodes differs from P. hopkinsi , P. jacksoni and P. tavernei , which have seven or more teeth in the upper jaw and eight or more in the lower jaw. With 12 circumpeduncular scales, it differs from P. longicaudatus , the undescribed species coded in Sullivan et al. (2002) as P. sp. ‘OFF’, P. batesii and P. tavernei which all have 16 or more. With its relatively sharp V-shaped head profile, P. sphekodes differs from P. batesii , P. gabonensis , P. retrodorsalis , P. tavernei and P. kingsleyae which have distinctly blunt or U-shaped snouts. P. sphekodes has type NPp electrocytes in its electric organ, as do seven other Paramormyrops from Lower Guinea, while P. batesii and P. kingsleyae have electric organs composed of electrocytes with penetrating stalks innervated on the anterior face (Type Pa). These characters are summarized in the key and in Fig. 16 .

Paramormyrops sphekodes differs from P. curvifrons in head and snout shape. Head and shout are shorter, deeper and more rounded when viewed laterally in P. sphekodes compared to P. curvifrons . P. curvifrons also has a downward sloping forehead, protruding snout and enlarged chin. The ratio of HL to SL is 23.5–26.9 in P. curvifrons , higher than 21.5–23.4 in P. sphekodes ( Fig. 5A , Table 2), while the ratio of HD to HL (external measurement using callipers) is reduced in P. curvifrons compared to P. sphekodes ( Fig. 5C ). The ratio of pre-pectoral distance to pre-dorsal distance is greater in P. curvifrons compared to P. sphekodes ( Fig. 5B , Table 2), and P. curvifrons has a significantly narrower snout than P. sphekodes measured by either snout angle ( Fig. 5G ) or ratio IOW/SNL ( Fig. 5D , Table 2).

Paramormyrops sphekodes is most easily confused with the species referred to above as SN4, but SN4 may be recognized by its much longer duration EOD, and by subtle morphometric characters discussed above and illustrated in Figs 3 and 4 . Other distinguishing characters are presented below in the description of the new species.

Description: Based on the lectotype Fig. 1A (above) and 1B and 10 other specimens, Table 2. Figure 7 shows five specimens in photographs of live fish in the field.

A small-bodied Paramormyrops , the largest is a male, 133 mm SL, 153 mm TL. Body laterally compressed, maximum width at opercular bones. Viewed laterally, dorsal and ventral profile nearly parallel from behind the head to the first anal ray. Median BD 16.1% SL at pectoral fin, 17.6% SL at the urogenital pore. The ratio of these two BDs 84–89%, indicating that the depth changes little from anterior to posterior of the body anterior of the anal fin. Caudal peduncle length 17–20% SL, slightly wider at its origin than middle, depth 25–29% CPL. Lobes of caudal fin rounded.

Lateral head profile above eye usually gently convex to very slightly concave in some individuals ( Fig. 7 , #1214). Snout short and smoothly rounded ( Fig. 7 ). Forehead downward-sloping from halfway between opercular opening and snout tip. Tip of the snout one half eye diameter below the ventral margin of the eye. Viewed dorsally, head and snout V-shaped or sharp, median snout angle 53.6°, less sharp than P. curvifrons ( Fig. 5D ).

Mouth small, rictus directly beneath nares. Chin protrudes slightly below gular region, not extending beyond snout. Eye small, ED 11–14% HL, positioned mid-laterally. Eye socket forms pale ring around pigmented eye, with gold iris and dark centre. IOW 26.8–29.3% HL. Anterior naris about 1/3 distance from snout tip to eye, slightly below line drawn through centre of eye, posterior naris halfway between anterior naris and eye, at about level of eye’s lower margin. Opercular opening begins anterior to base of pectoral fin. POL 60–68% HL.

Pectoral-fin origin beneath posterior terminus of opercular opening, slightly below mid-horizontal line, length 12.4–17.0% SL, 11 rays. Pelvic-fin origin at 35.0– 38.8% SL, length 9.2–10.8% SL, positioned ventrally, 6 rays. Dorsal-fin origin at 64–65% SL; anterior margin gently convex, trailing margin concave in first third, remainder levels off at ½ DFH. Maximum height 62.3– 79.2% DFL, 20–23 total rays. Anal-fin origin slightly anterior to dorsal-fin origin: dorsal-fin origin above seventh (fifth branched) anal-fin ray. Anal fin mirrors general shape of dorsal fin, maximum height 45.2–65.0% AFL. In males, anterior AFR thickened and stiff with a noticeable notch at the base of the anal fin, spanning anterior half of anal-fin base. End of anal-fin base terminus directly beneath end of dorsal-fin base, rays 24–28. Lobes of caudal fin rounded, equal, slightly wider than caudal peduncle, deeply cleft, scaled at their bases.

Scales fine, cycloid, absent from head. Pierced lateral line scales, 63–68 based on recent specimens (lectotype = 72, significantly fewer than Sauvage’s description of 85 which must have been total scales rather than pierced scales). Our counts of lateral line scales on the lectotype are unreliable because of damage to the specimen, other counts and measurements for the lectotype are indicated separately from other specimens in Table 2. Scales between lateral line and anterior base of dorsal fin 9–11, 10–15 scale rows between pelvic fin and lateral line. Circumpeduncular scales 12. Vertebrae: 43–45 total, 18–19 precaudal, 24–26 caudal. Teeth bicuspid, 5 in upper, 6 in lower jaw.

Coloration: All fins with lightly pigmented rays, membranes hyaline. Dark band absent between dorsal and anal fins. Body darker dorsally, lighter ventrally. When alive, tan-brown body with yellow-olive or golden accents on top of head, back, and belly. Mouth, chin, and gular region unpigmented, whitish. Many small unpigmented spots and pores over electroreceptors (mormyromast and ampullary organs) visible on top of head and back, with fewer, large white spots (knollenorgans) on head. Preserved specimens uniform greyish-brown.

Electric organ discharge: Short biphasic pulses – head positive first then head negative – average duration, 0.851 ± 0.352 ms ( Fig. 8A, C , Table 3). First positive peak, P1, width W1 0.519 ± 0.194 ms (range: 0.320 –0.940 ms) – 1.6 times longer than width W2. First-time derivative of EOD rises smoothly from baseline with a single peak before P1 ( Fig. 8B ). Power spectrum of EOD peaks at 1910 ± 540 Hz (n = 9, Table 3, Fig. 10 D, E ). Other quantitative measurements of EODs are summarized in Table 3 using reference landmarks illustrated for the biphasic EOD in Fig. 8A and its power spectrum in Fig. 8D .

Several other species of Paramormyrops with biphasic EODs possess electric organs composed of electrocytes with N on- P enetrating stalks that are innervated on the p osterior faces of each cell (Type NPp Bennett, 1971; Bass, 1986; Sullivan et al., 2000; Gallant et al., 2011). Other species in this and other genera produce triphasic EODs (three peaks), beginning with a small head-negative phase P0, in advance of the larger head-positive phase P1, and the final head-negative phase P2. In all species with triphasic EODs, the electric organs are composed of electrocytes with P enetrating stalks innervated on the a nterior face of each cell (Type Pa in Alves-Gomes & Hopkins 1997). Inspection of the EODs of all P. sphekodes reveals that the P0 peak is absent, even when the discharge trace is expanded 20 times by amplification ( Fig. 8A , thin trace), suggesting that the electric organ is composed of Type NPp electrocytes. This is confirmed by dissection and histology shown in Fig. 9 .

Like many other mormyrids, P. sphekodes exhibits a sex difference in EOD waveform duration. One male recorded near the end of the rainy season in May 2011 had the longest EODs in all our EOD recordings (1.60 ms), but other, smaller males recorded early in the rainy season of September 2014 had EODs more similar to those of females. The averages of male and female EOD durations do not differ significantly (Student’s t = 1.439, d.f. = 7, P = 0.19, Table 3). In all adult males with SL> 115 mm, we note that the ratio of the width of the second peak, W2, to total duration, DT, is greater than for that for females (Student’s t = 2.99, P = 0.03). The ratio of W1 to DT is correspondingly less for males. The variation seen for male EODs might be a reflection of seasonal changes in male pulses which begin to elongate before or shortly after the onset of the rains when most mormyrids breed ( Hopkins, 1980, 1981; Hopkins & Bass, 1981; Bass & Hopkins, 1983, 1985).

Distribution. In spite of several previous collecting trips to the lower, middle and upper Ogooué River of Gabon in 1999, 2001 and 2002, our only collections of this species are from Doumé, the type locality (2011, 2014), and the Sébé River, about 45 km from Doumé (2014). Both sites are within the Ogooué-Lolo Province of Gabon ( Fig. 10 ) and both are large river habitats with rocky bottoms, sandy substrate, with rushing water and rapids ( Fig. 11 ); this species was absent from nearby streams and other smaller tributaries.

Etymology: The name sphekodes comes from the Greek, σφήκα, for wasp, which may refer to the fish’s elongate and slender body ( Harder, 2000); however, Sauvage (1879, 1880) gives no explanation for his name for this species.

The specimens referred to as ‘SN4’ above and in Sullivan et al. (2002, 2004) are here described as a new species.

Figures

Figure 1. (A) Paramormyrops sphekodes (Sauvage, 1877) MNHN A.893 photographed in 1984 by W. Harder at which time the lot contained two specimens, suspended vertically in a tall jar from a glass floater. The original MNHN catalogue shows two specimens accessioned in 1878 under this number. The larger specimen (SL = 113.8 mm) is currently catalogued as A 893; the smaller specimen (SL = 98.7 mm) was subsequently catalogued in 1998 as MNHN 1050-1998. Sauvage’s original description indicates multiple specimens with a largest of 140 mm total length, but he designated no holotype. We regard these specimens as syntypes prior to our designation of the larger as lectotype. (B) Radiograph of MNHN A893.

Figure 3. The Paramormyrops specimens with short EODs, and those called SN4 have overlapping meristics but differ in a number of morphometric ratios. Here, the short EOD specimens are shown as blue circles, while ‘*’ indicates the lectotype of P. sphekodes and ‘+’ indicates the paralectotype. The red circles show those with longer EODs referred to as SN4 specimens. The short EOD forms have elevated ratios of interorbital width to snout length and correspondingly blunter snout angles than the SN4 specimens. They also have slightly reduced caudal peduncle depth to length ratios. There is overlap in each ratio taken separately, but combined they provide a convenient morphological basis for diagnosis between these two EOD types. EOD traces are 10 ms long.

Figure 4. The short EOD and SN4 Paramormyrops differ in the ratio of head length (HL) to head depth (HD) when measurements are taken from radiographs. (A) HLx/HDx is plotted against standard length for 41 specimens including short EOD specimens (n = 9, blue circles), SN4 specimens (n = 30, red squares) and the two existing types (* = lectotype of P. sphekodes and ‘x’ = the paralectotype). Solid lines show linear regression lines showing that head shape changes little with overall size. The measurements of the lectotype (LT) of P. sphekodes (MNHN-A893) and paralectotype (PLT) (MNHN 1998-1050) identify the short EOD individuals as P. sphekodes. The specimens with SN4-type EODs belong to a new species (red * indicates the new species holotype). Specimen 1185 is shown in x-ray in C. (B) Non-overlapping histograms of HLx/ HDx allow for good diagnosis of the two EOD types even if no EOD is available, as with the two types of P. sphekodes. (C) Radiographs of two specimens (Specimen CUMV 98134 tag number JPS-1185, an SN4 fish and MNHN-A893) illustrate landmarks used for measuring HLx and HDx (see Material and Methods). Scale bars = 1 cm.

Figure 5. Morphometrics and ratios from the three species of Paramormyrops included in this study. (A–C) and (E–G) show measurement ratios useful in diagnosis of these three species. Snout angle measurements (see Material and Methods) are compared in (D) and (G). (D) plots snout angle against IOW/SNL. Holotypes or lectotypes are indicated by ‘*’ symbols and paratypes are indicated by ‘x’ symbols. (H) compares IOW/SNL for specimens of differing standard lengths. Superimposed on the data points in (A–C) and (E–G) are box plots showing range, 25% quartile, median and 75% quartile. Black bars above box plots span samples where means differ significantly (P ≤ 0.05) using Tukey–Kramer multiple comparison tests for differences in sample means. See Table 1 for abbreviations.

Figure 7. Five specimens of P. sphekodes from Ogooué basin of Gabon. From top to bottom: specimen tag number 1192, female, 113.5 mm; 1201, female, 111 mm from the Ogooué River at Doumé; 1214, male, 112.5 mm; 1230, male, 133 mm and 1238, male, 119 mm from the Sébé River nearby. Scale bars = 1 cm.

Figure 8. Electric organ discharges (EODs) from P. sphekodes. (A) Paramormyrops sphekodes specimen CUMV 98177 (tag JPS-1238), a male from type locality showing normalized voltage as a function of time, that is 1.0 V peak-to-peak. Head positivity is upwards on all traces. There are two peaks to the waveform: P1, which is head-positive, and P2, which is headnegative. EOD duration is measured between points marked by open circles – the first and last points exceed ±0.02 V. W1 and W2 are the widths of the first and second peaks. The thin line is a 20× vertical expansion of the waveform which rises gradually from the baseline with no indication of a head-negative pre-pulse, P0, that is present in some other species. The final overshoot, due to AC-coupling of the amplifier, is absent when making DC-coupled recordings. The dashed line indicates the zero baseline. (B) Time derivative, dV/dt, of EOD waveform in (A) has a single positive peak (arrow) in advance of peak P1 and there is no inflection point on the rising phase before P1. (C) EODs from nine specimens of P. sphekodes showing the stereotypy of the species waveform. After normalization to unity peak-to-peak height, all EODs are centred on the zero-crossing between P1 and P2 [zc in (A)]. Males are plotted in blue and females are plotted in red. (D) Power spectral density of EODs of P. sphekodes in (A) with its maximum power at 1125 Hz. Flow and Fhi are the frequencies where the spectral power drops 3 dB below the peak power of the FFT. The bandwidth of the power spectrum is Fhi–Flow. (E) Superimposed power spectra for the nine EODs shown in (C) with peak frequencies marked with ‘x’. Axes units are as in D.

Figure 10. Distribution map of West-Central Africa showing collection localities of specimens of P. sphekodes (blue), P. ntotom sp. nov. (red) and P. curvifrons (green). Stars mark collection locations of holotypes (or lectotype) and circles mark locations of other specimens.

Figure 11. (A, B) Collection localities near the rapids at Doumé (0.84245°S, +12.96249°E) on the Ogooué River of Gabon, where P. sphekodes is sympatric with P. ntotom sp. nov. (B) shows local villagers fishing with hoop nets at Doumé. (C, D) View of the Sébé River (0.93494°S, 13.35767°E) where the two species are also sympatric. Both habitats are moderate-sized rivers with gentle flow or rapids over rocky outcroppings, interspersed with sandy beaches, surrounded by dense rain forest. The Ogooué River is 75–100 m wide at Doumé, 3 m in depth, and the water had low conductivity (13.9 µs/cm) at pH 7.04 and 6.66 mg/L O2 (83.1% saturated) at 26.7 °C. The Sébé River is 55–75 m wide, approximately 3.1 m deep, 16.0 µs conductivity, 7.08 pH and 7.5 mg/L O2 (93.6% saturation) at 26.6°C).

Figure 16. Nine species of Paramormyrops from Lower Guinea showing, from left to right, head shape viewed from above, the outline of the body, and representative female and male EOD waveforms. Head shapes are camera lucida tracings of the holotypes for each species from the snout to end of opercular opening. The first six have sharp V-shaped head profiles and the last three have relatively blunt U-shaped heads. All but the last two have electric organs composed of Type NPp electrocytes (exhibiting Non-Penetrating stalks innervated on the posterior face). The last two have electric organs composed of Type Pa electrocytes (with Penetrating stalks innervated on the anterior face). All known mormyrids with Type Pa electrocytes have an initial, head-negative peak, P0, in the EOD waveform as illustrated here for P.kingsleyae. The P0 peak is absent in all species with Type NPp electrocytes. The EOD of P. batesii is unknown, but the electric organ is composed of Type Pa electrocytes.

Figure9. Histologyofpara-sagittalsectionofparalectotype of P. sphekodes specimen MNHN 1998-1050 (Female, 98.7 mm, SL) shows electrocytes of type NPp (Non-Penetrating stalks with posterior innervation). The specimen, collected from Doumé Falls by Alfred Marche in 1876–1877 and preserved in alcohol, was embedded in plastic, sectioned with a tungsten carbide knife at 7 µm and stained with toluidine blue. E = main body of the electrocyte; anterior = anterior face of electrocyte; post = posterior face of same electrocyte; c = collagen layer separating two electrocytes; S = stalk of electrocyte which is innervated by the axons from the electromotor nerve (not shown); s = stalklets, or small branches from a dividing stalk that eventually fuse with posterior face of the electrocyte. Stalks are innervated on the posterior side of the electrocyte and all branches of the stalk system remain posterior to the main body of the electrocyte without crossing to the opposite or anterior side.