Micrurus spixii Wagler, 1824

Nascimento, Lywouty R. S., Silva Jr, Nelson J., Feitosa, Darlan T. & Prudente, Ana L. C., 2019, Taxonomy of the Micrurus spixii species complex (Serpentes, Elapidae), Zootaxa 4668 (3), pp. 370-392 : 376-380

Micrurus spixii Wagler, 1824

Micrurus spixii Wagler 1824:48 .

Elaps spixii — Boulenger 1896:427 .

Elaps ehrhardti Müller 1926 , Zool., Anz. Manacapurú, Solimões, Brazil:198.

Micrurus spixii martiusi Schmidt 1953 , Fieldiana Zool. Santarém, Pará, Brazil:175.

Micrurus spixii spixii — Schmidt 1953:175 .

Micrurus spixii — Harvey et al. 2003:41 .

Micrurus spixii spixii — Campbell & Lamar 2004:227 .

Micrurus spixii martiusi — Campbell & Lamar 2004:229 .

Micrurus spixii martiusi— Silva Jr. et al. 2016a:133.

Micrurus martiusi— Wallach et al. 2014 :454.

Micrurus spixii —Wallach et al. 2014:454 .

Micrurus spixii spixii —Silva Jr. et al. 2016a:132 .

Micrurus spixii — Valencia et al. 2016:321 .

Holotype. Adult male, ZMH 209 /1, collected in the Spix and Martius expedition to Brazil, between 1817–20 at Solimões River, Amazonas, Brazil.

Diagnosis. Micrurus spixii can be distinguished from all congeners by unique combination of the following characters: black cephalic cap; black cephalic shields with white borders; gular scales black on posterior borders; black ring of the first triad connected to cephalic cap. Body triad 4–10, first triad incomplete (2/3+4 complete triads +2/3–2/3+10+1/3); ventrals 174–232 in males, 202–235 in females; subcaudals 16–28 in males, 17–29 in females; hemipenis slightly bilobed and capitate, with calcified spines arranged radially on the apex of the lobes; hemipenis with capitular crotch dividing the organ into hemipenial body and capitulum, and developed basal pocket; premaxilla located anteriorly to nasals; parietal narrow with posterior extremity pointed and angulated, exceeding prootics to the level of supratemporals; fangs long in relation to maxillary.

Comparisons. Micrurus spixii differs from M. obscurus by having black cephalic cap connected to first black body ring, hemipenis capitate, and fangs long in relation to maxillary and slightly inclined anteriorly (vs. black cephalic cap absent, black interorbital bar, first black ring separated from parietal and temporals by a narrow white ring, non-capitate hemipenis, and short fang in relation to the maxillary, inclined anteriorly); differs from M. brasiliensis , M. frontalis and M. ibiboboca by having black cephalic cap in contact with the first body ring, first triad incomplete and less than 10 complete body triads (vs. black cephalic cap absent or not connected to the first black body ring, white snout, first triad complete, more than 10 complete body triads); differs from M. diana by having first incomplete triad and body triads 4–10 (vs. first complete triad and body triads 9–15); differs from M. filiformis by having ventrals 174–232, subcaudals 17–26, body triads 4–10, first triads incomplete, and black cephalic cap (vs. ventrals 239–329, subcaudals 37–46, complete body triads 10-22 and black cephalic cap absent); differs from complex M. lemniscatus species by having black cephalic cap connected to first body ring, first body triad incomplete, white body rings extend beyond four dorsal rows (vs. tricolor head in M. l. diutius, M. l. carvalhoi and M. l. lemniscatus , and white body rings do not exceed four rows of dorsal scales); differs from M. hemprichii by having divided cloacal plate and red rings (vs. cloacal plate entire and yellow rings); differs from M. surinamensis by having hemipenis without spinulate calyces, black cephalic scales with light borders, first triad incomplete, and supralabials 3–4 in contact with orbit (vs. hemipenis with spinulate calyces, red cephalic scales with black edges, first triad complete, and only fourth supralabial in contact with orbit).

Redescription of the holotype ( Fig. 2A ). Adult male, ventrals 210, subcaudals 21, SVL 1167 mm, TL 63.1 mm, HE 32.5 mm. Black cephalic cap covering internasals, prefrontals, supraoculars, frontals and parietals; cephalic cap connected to medial black ring of first body triad; first six supralabials olive horn, being first fourth with posterior region black; seventh supralabial black, with anterior border buff; nasals, preoculars and postoculars buff with black spots; mental pale horn; first four infralabials olive horn, five to seven pale horn, with second, third and seventh pairs with posterior borders black; gulars olive horn with posterior border black; body with nine triads, first and last incomplete, separated by seven tawny olive rings (anterior and posterior red rings); first body triad incomplete (2/3), anterior pale horn ( ANTWH) ring (nine scales long), with posterior borders black; MIBL extending dorsally from parietal to second dorsal row, and ventrally to first and second preventrals and two gular rows; POSWH (eight scales long) with black posterior borders; POSBL (six scales long); after incomplete triad, follow seven incomplete triads, ANTRD and POSRD tawny olive rings (6–13 scales long), ANTWH and POSWH pale horn rings (6–7 scales long), and ANTBL, MIBL and POSBL black rings (4–5 scales long); last body triad incomplete (1/3), containing a single black ring; tail triad incomplete (2/3), with dark cream ANTRD ring, black ANTBL ring, pale horn ANTWH ring, black MIBL ring and pale horn POSWH; ventrally, pale horn and tawny olive rings without spots .

Meristic and morphometric variation (n = 208). Ventrals 174–232 in males (mean= 217; SD= 6.6; n = 131), 202–235 in females (mean= 220; SD= 6.1; n = 48); subcaudals 16–28 in males (mean= 23.1; SD= 2.16; n = 123), 17–29 in females (mean= 21.7; SD= 2.4; n = 52); width of head 10.1–39.0 mm in males (mean= 25.8; SD= 7.1; n = 127), 9.8–28.5 mm in females (mean= 21.7; SD= 2.4; n = 44); SVL 242–1490 mm in males (mean= 943.6; SD= 298.6; n = 133), 205–1083 mm in females (mean= 608.2; SD= 268.7; n = 58); TL 13.4–78.2 mm in males (mean= 57.3; SD= 16.3; n = 123), 12.8–65.0 mm in females (mean= 36.4; SD= 5.7; n = 52); body triads 5.3–11.0 in males (converted to 2/3+4+2/3–2/3+10+1/3; mean= 8.3; SD= 1.3; n = 138), 5.3–11.0 in females (converted to 2/3+4+2/3– 2/3+10+1/3; mean= 7.3; SD= 1; n = 62); ANTRD 2.9–84.4 in males (mean= 28.3; SD= 14.1; n = 123), 3.7–50.6 in females (mean= 18.0; SD= 9.9; n = 52); ANTBL 3.9–71.9 in males (mean= 19.75; SD= 8.2; n = 123), 2.7–31.1 in females (mean= 12.5; SD= 6.3; n = 52); ANTWH 3.1–41.1 in males (mean= 21.2; SD= 8.5; n = 123), 4.5–36.0 in females (mean= 14.4; SD= 7.24; n = 52); MIBL 3.9–33.0 in males (mean= 18.5; SD= 6.5; n = 123), 3.2–27.7 in female (mean= 12.1; SD= 5.7; n = 52); POSW length 3.1–41.1 in males (mean= 21.3; SD= 8.7; n = 123), 4.5–32.64 in females (mean= 14.43; SD= 7.11; n = 52); POSBL 3.9–81.8 in males (mean= 19.5; SD= 8.6; n = 123), 3.4–26.4 in females (mean= 12.0; SD= 5.7; n = 52); POSRD 5.1–67.6 in males (mean= 26.8; SD= 12.2; n = 123), 3.9–54.8 in females (mean= 16.9; SD= 9.7; n = 52).

Color pattern ( Figs. 1A , 8 ). In life (n = 18) ( Fig. 9 A–B), head with black cephalic cap covering internasals, prefrontals, supraoculars, frontal, and parietals; head scales black with anterior borders white; cephalic cap connected to first body triads; first seventh supralabials red with black posterior borders; nasals, preoculars and postoculars white, with black posterior borders; anterior temporal white with black posterior borders; mental red with black posterior border; infralabials red, first to second pair with black posterior borders (n = 8); chinshields red with black posterior borders; first triad incomplete formed by MIBL ring starting from posterior portion of parietals reaching 2–4 dorsal rows, followed by POSWH ring reaching 4–9 dorsal rows until connects to POSBL ring forming 2/3 of triad; incomplete body triad (1/3 or 2/3) in region before cloaca; tail with 1/3 of triads incomplete and one complete; dorsal scales of white and red rings with black posterior borders (2/3 of scales darkened and gradually become lighter towards anterior border); ventral scales with black rings narrower than dorsal region, and red and white rings without spots.

In preservative solution (n= 127) ( Fig. 8 C–F), red becomes light buff and white becomes pale buff. In melanic specimens (n= 17) ( Fig. 8B, D and F ), strong darkening occurs in keratinized portion of cephalic and corporeal scales; cephalic region intensely darker than the non-melanic individuals, without light borders; cephalic cap indistinct from first body ring.

Hemipenial morphology (n = 9) ( Figs. 4A–D and 6A ). Hemipenis short, slightly bilobed, capitate and ornamented with calcified spines; sulcus spermaticus deep, bifurcated at base of lobes, running centripetally along lobes and reaching apices; sulcus spermaticus bordered by diminutive spines; lobes short (less than 30% of hemipenial body), ornamented with small spines, arranged radially from distal extremity to rest of capitulum; intralobular region covered by short spines, irregularly arranged; capitular crotch evident on the proximal third, delimiting body in first third and capitulum in distal two thirds, capitular crotch narrower and deeper on the sulcate side, thicker and shallow on the asulcate side; capitulum ornamented by small spines, irregularly arranged, gradually decreasing in size and number towards apical region of lobes; spines larger and more numerous on the sulcate side; body covered by small spines, smaller and less number on the sulcate face; proximal region of hemipenis naked, except for presence of large basal pocket ornamented by small spines, delimited by central protuberance ornamented with small spines.

Skull morphology (n= 15) ( Fig. 7A ). The skull generally elongated anterior-posteriorly in relation to the other species compared; premaxillar wide (76.8% of total skull width), projected anteriorly, completely surpassing limits of nasal bones, not inserting beneath these; lateral processes of premaxillar (processus transversus) distally elongat- ed with pointed ends; parietal (67.7% maximum skull width; 43.9% skull length) with sharp proximal borders; external borders of parietal forming posterior part of ocular orbit; medial crest of parietal bifurcating on the proximal third, continuing toward orbital region; distal extremity of parietal sharp, exceeding limits of prootics and proximal region of supratemporals and supraoccipital; palatine with 7–8 teeth; pterygoid with 4–5 teeth; maxilla (19.3% of total skull length) with proximal region wider than distal, contacting ectopterygoid; dorsally maxilla contacting prefrontal at its middle third, proximal region reaching the height of septomaxillars; venom fangs long (81.7% of jaw length), curved posteriorly, inserted on the proximal ventral extremity of maxillary; dentary bone with 8–10 teeth; coronoid process of compound bone not extensive.

Distribution ( Fig. 9 ). Micrurus spixii occurs from the northeast of Bolivia (left bank of the river Mamoré River, in the vicinity of the city of Guayaramerín, Beni) following to the Brazil by the states of Rondônia, Mato Grosso (up until south bank of the Paraguai River, near the municipality of São José do Rio Claro), Amazonas (up until north bank of the Negro River, vicinity of the municipality of Novo Arião), Pará, Tocantins (left bank of the Tocantins River River, vicinity of the municipality of Tocantinópolis) and Maranhão (up until west of the Mearim River, near the municipality of Nova Vida).

Figures

FIGURE 1. Comparison of schematic representation of the color pattern in life of Micrurus spixii complex, M. s. spixii and M. s. martiusi (A—1= supralabial and infralabial red; 2= cephalic cap; 3= first body ring connected to cephalic cap) and M. s. obscurus and M. s. princeps (B—1= white snout and scales with black spots; 2= interocular black band; 3= red parietal region; 4= first narrow white body ring; 5= black body ring with anterior triangular portion).

FIGURE 2. General views of the holotypes of Micrurus spixii spixii (A—ZSM 209/0, SVL= 1167 mm) from Solimões River, state of Amazonas, Brazil; M. s. martiusi (B—MCZ 2612, SVL= 1213 mm) from municipality of Santarém, state of Pará, Brazil; M. s. obscurus (C—picture modified from the Jan & Sordelli 1872) from province of Iquitos, department of Loreto, Peru; and the lectotype of M. s princeps (D—BMNH 1946.1.20.44, SVL= 1241 mm) from province of Sara, department of Santa Cruz, Bolivia.

FIGURE 4. Intraspecific comparison of internal morphology between Micrurus spixii martiusi and M. s. spixii throughout the geographic distribution. Hemipenis morphology of M. s. martiusi (A—MPEG 20664) from municipality of Ourilândia do Norte, state of Pará, Brazil; M. s. spixii (B—MPEG 21029) from municipality of Juruti, state of Pará, Brazil; M. s. martiusi (C—MPEG 22274) from municipality of Coari, state of Amazonas, Brazil; M. s. spixii (D—MPEG 16480) from municipality of Porto Vellho, state of Acre, Brazil; and skulls of M. s. martiusi (E—MPEG 10115) from municipality of Viseu, state of Pará, Brazil; M. s. spixii (F—MPEG 20664), and M. s. martiusi (G—MPEG 8882) from municipality of Castanhal, state of Pará, Brazil. Scale bar= 5 mm.

FIGURE 6. Sulcate (left) and asulcate (right) views of the hemipenis of Micrurus spixii spixii (A—MPEG 20664) from municipality of Ourilândia do Norte, state of Pará, Brazil; and M. s. obscurus (B—MPEG 160) from Javari River, state of Amazonas, Brazil. Scale bar = 5 mm.

FIGURE 7. Dorsal, lateral, ventral views of the skull; and labial and lateral face of mandibles of Micrurus spixii spixii (A— MPEG 20664) from municipality of Ourilândia do Norte, state of Pará, Brazil; and M. s. obscurus (B—CEPB 5597) from municipality of Letícia, department of Amazonas, Colombia. Scale bar= 5 mm.

FIGURE 8. General view in life and after preservation for non-melanic and melanic specimens of Micrurus spixii. Live nonmelanic individual from municipality of Jaci Paraná, state of Rondônia, Brazil (A) and melanic individual from state of Rondônia, Brazil (B); preserved non-melanic specimen (C—MPEG 23389) from municipality of Juruti, state of Pará, Brazil; and melanic (D—MZUSP CCO-233) from municipality of Colíder, state of Mato Grosso, Brazil; and dorsal, ventral and lateral views of the head of preserved non-melanic (E—ZSM 203-1925) from municipality of Manacapurú, state of Amazonas, and melanic (F—ZSM 124-1915) from municipality of Campos do Ariramba, state of Pará, Brazil. Scale bar C–D= 30 mm, E–F= 15 mm. Photos by R. Gaiga (A) and T. Barros (B).

FIGURE 9. Geographic distribution of Micrurus spixii and M. obscurus. Legends: Black circle= Micrurus spixii; yellow circle= type-locality of M. spixii; black triangle= M. obscurus; and yellow triangle= type-locality of M. obscurus.