Micrurus paraensis

Feitosa, Darlan Tavares, Prudente, Ana Lúcia Da Costa & Lima, Ana Caroline De, 2007, Redescription and variation of Micrurus paraensis Cunha & Nascimento 1973 (Serpentes: Elapidae), Zootaxa 1470, pp. 35-45 : 36-44

Micrurus paraensis Cunha & Nascimento (1973)

Micrurus psiches [ psyches ] paraensis Cunha & Nascimento, 1973: 276. Type-locality: Icoaraci, Belém, Pará, Brasil.

Micrurus donosoi Hoge, Cordeiro & Romano, 1978: 71 . Type-locality: São Felix do Xingu, Pará, Brasil.

Micrurus psyches paraensis - Cunha & Nascimento, 1978: 164; Roze, 1982: 334; Campbell & Lamar, 1989: 140.

Micrurus paraensis - Hoge & Romano, 1981: 400; Cunha & Nascimento, 1982: 18; Nascimento et al. 1987: 57.

Micrurus psyches donosoi - Roze, 1982: 334; Campbell & Lamar, 1989: 140.

Micrurus paraensis debruini Abuys, 1987: 215 . Type-locality: Kwamalasamutu, Suriname.

Micrurus paraensis - Cunha & Nascimento, 1993: 116; Roze, 1994: 178; Roze, 1996: 207; Carvalho, 2002: 186; Campbell & Lamar, 2004: 185; Frota, 2004: 13.

Diagnosis. Micrurus paraensis can be distinguished from other species of Micrurus by the following combination of characters: black cap beginning on rostral, passing from the first to fourth supralabials, behind the eyes on postoculars and half of first temporal; white rings beginning on 5, 6 and 7th supralabials, sometimes beginning on half of fourth supralabial, through temporals towards parietals; black cap joined to first black body rings (nuchal collar) to end of parietals; black body rings range from 12 to 21, bordered by a short white rings (comprising one, half scale, with black posterior margin), 12–20 red rings range from, about 4 to 6 times longer than black rings; body rings do not form triads; 2–11 black tail rings alternated by 1–11 white rings; black tail rings with white spots on dorsal and ventral surfaces; and males have no supraanal tubercles.

Micrurus paraensis can be distinguished from the eastern Amazonian coralsnakes ( M. filiformis , M. hemprichii hemprichii , M. lemniscatus lemniscatus , M. spixii , M. surinamensis ) by the monadal color patterns, long tail, long and bifurcated hemipenis (vs. triad color patterns, short tail, short and bilobed hemipenis). In other Amazonian regions, M. paraensis can be distinguished from monadal color patterned species ( M albicinctus and M. langsdorffi ) by the tricolor pattern and lower number of black body rings. Bicolored patterns with higher number of black body rings (67 to 90 in males; 77 to 91 in females) on M. albicinctus , white spots on frontals and supraoculars, and white gular region with black spots. M. langsdorffi has a tricolor monadal patterns, higher number of black, white and red body rings (18 to 38 black, 38 to 57 white and 19 to 38 red in males; 29 to 47 black, 46 to 60 white and 20 to 46 red in females) with short red rings (3 to 4 dorsals and ventrals long).

Finally, it can be distinguished from the M. psyches group ( M. circinalis , M. mademi , M. psyches and M. remotus ) by the black body rings and the number of ventrals and subcaudals. M. psyches has black body rings ranging from 22 to 29 in males and 27 to 41 in females (if the black and the original red rings that are blackish are counted as black, the males have 44 to 57 and the females have 51 to 81), original red and black rings are 3 to 5 dorsals and ventrals long, and ventrals ranges from 188 to 196 in males and 203 to 212 in females. M. circinalis has black body rings ranging from 21 to 31, with short red rings (4 to 7 dorsals and ventrals long), and ventrals ranges from 174 to 193 in males and 192 to 209 in females. M. medemi has black body rings ranging from 15 to 25 (if the black and the original red rings that are blackish are counted as black, has 35 black body rings), and ventrals ranges from 193 to 198 in males and 211 to 218 in females. M. remotus has black body rings ranging from 25 to 29 in males and ranging from 29 to 40 in females, and ventrals ranges from 202 to 203 in males and 214 to 225 in females.

Description of Holotype. MPEG 0851; adult male; SVL 390 mm; TAL 85 mm (17.8 % of TL); and HL 12.5 mm (2.6 % of TL). Head indistinct from the body. Eyes small, pupil round. Body cylindrical. Snout rounded. Tail long. Dorsal scales smooth, in 15 rows, without reduction, no apical pits; 192 ventrals; 52 subcaudals; anal divided; 7 supralabials, 3 and 4th in contact with the orbit; 7 infralabials, 1 to 4th in contact with the first pair of genials; nasal half-divided; one preocular; two postoculars, the superior is higher; 1+1 temporal. White lateral ring beginning on parietals from inferior region of 4th supralabial; 5, 6 and 7th supralabials white, the 6th is higher and the posterior edge of 7th supralabial is black; little anterior part of temporal is black, the remainder of the anterior temporal and the posterior temporal is white; parietal totally black joining the black cap to the nuchal collar, this is interrupted by white spots on the right side of ventral surface; 1 to 3th infralabials black with white spots; 4 to 6th infralabials white, the 4th one is higher; the first pair of mentals is black with white spots, the second pair is white with black top. 15 black body rings (2 to 3 dorsals and ventrals long); 14 red body rings (7 to 14 dorsals long with black top); 9 black tail rings, the second black ring has a white spot on the ventral surface; 4th and 7th black rings with a spot on the ventral-lateral surface, alternating with by 8 short white rings; a ventral black spot between the 5 and 6th black body rings and two between 7th and 8th black body rings (Table 1).

Description. Rostral scale broader than high, with a triangular shape in frontal view and visible from above. Internasals shorter than prefrontals, which do not enter the orbit. Frontal longer than broad. Supraoculars aproximately as broad as the prefrontal. Parietals about two times longer than wide. Nasal half-divided. One preocular, longer than high. Two posoculars, the superior is higher. One anterior and one posterior temporal. Thirth and fourth supralabial in contact with the orbit. First pair of infralabials in contacts behind symphysial, and 1st to 4th pairs contact first pair of genials. Fourth infralabials in contact with second pair of genials. Two pairs of genials ( Figure 1 ). Dorsals scales in 15 rows, smooth, without reduction. Anal plate divided.

Color Pattern - Black cap beginning on rostral, passing from 1st to 4th supralabials, behind the eyes on postoculars and half of temporal anterior, a white ring beginning on 5th and 6th supralabials, sometimes beginning on half of 4th supralabial, passing by temporals towards parietals; middorsally, the black cap is joined to the first black body ring (nuchal collar) by the end of parietals ( Figure 1 ). First to third infralabials black; 4th to 5th and half of sixth infralabials white, mental white with black spots; 12 to 21 black body rings (3 to 4 dorsals long), 12 to 17 in males and 13 to 21 in females, short white rings formed by a half scale with black top; 12 to 20 red body rings (6 to 20 dorsals long, with top 2/3 of scale black), ranging from 12 to 17 in males and 12 to 20 in females; 2 to 11 black tail rings (ranging from 6 to 12 in males and 2 to 11 in females) alternating with 1 to 12 white rings (ranging from 6 to 12 in males and 1 to 11 in females); the black tail rings can present white spots on dorsal and ventral surface, the spots can sometimes form bands or rings. There is a tendency toward melanism on the dorsal surface. The ventral surface can be spotted ( Figure 2 ).

TABELE 1. Meristic and mophometric data (mm) for Micrurus paraensis holotype (0851) and paratypes (0909, 0 951, 0 973, 1424, 1496 and 2665) (Legend: - = no data).

Hemipenis. The hemipenis is up to 15 subcaudals long, and the bifurcation starts at around the 10th or 11th subcaudal. The base of the organ is naked up to the level of the 5th or 6th subcaudal where tiny spines appear on the sulcus ridge. Spinules and a few small spines begin at the 6th subcaudal and gradually increase in size until 9th subcaudal below the point where the sulcus bifurcates. The sulcus divides around the 8th or 9th subcaudals.

At the level, large calcified spines appear and continue on each fork of the hemipenis but gradually diminish in size again toward the apex. A large lateral naked fold runs from the base of the organ to the level of the 8th subcaudal ( Figure 3 ).

Variation and sexual dimorphism (N = 64) ( Tables 2 and 3 ). Micrurus paraensis presents significant sexual dimorphism in four morphometric characters (SVL (Snout-vent length); TAL (Tail length); TL (Total length); frontal width; distance between eyes) and six meristics (Ventral; Subcaudal; number of black and red body rings; number of white and black tail rings), as follows: largest male 463 mm SVL (= 362.5; SD = 64.2; N = 31) and 85 mm TAL (10 to 21% of TL); largest female 590 mm SVL (= 422.0; SD = 101.7; N = 22) and 77 mm TAL (9 to 18% of TL) (t = 3.7; df = 22; p> 0.01); frontal longer than wide, in male occupies 17 to 28 % of the HL and in females occupies 20 to 32 % the HL (t = -2.7; df = 56; p> 0.01); distance between eyes is 2.9 to 4.8 mm (= 4.0; SD = 0.4; N = 29) in males (43 to 73 % of the WH) and 3.2 to 5.8 mm (= 4.3; SD = 0.6; N = 22) in females (52 to 64 % of the WH) (t = -2.2; df = 56; p <0.05); ventrals 184 to 197 (= 191.3; SD = 3.6; N = 35) in males, and 186 to 217 (= 205.1; SD = 7.9; N = 27) in females (t = -7.9; df = 23; p> 0.01); subcaudals 36 to 54 (= 47.3; SD = 3.4; N = 35) in males, and 30 to 52 (= 38.0; SD = 6.6; N = 27) in females (t = 6.7; df = 23; p> 0.01); black body rings 12 to 18 (= 14.8; SD = 1.4; n = 35) in males; and 13 to 21 (= 17.1; SD = 2.2; N = 26) in females (t = -4.7; df = 59; p> 0.01); red body rings 12 to 17 (= 14.0; SD = 1.3; N = 34) in males, and 12 to 20 (= 16; SD = 2.1; N = 24) in females (t = -4.1; df = 58; p> 0.01); black tail rings 5 to 12 (= 8.2; SD = 1.7; N = 34) in males, and 2 to 11 (= 6.4; SD = 1.9; N = 23) in females (t = 3.9; gl = 55; p = 0.01); white tail rings 5 to 12 (= 8.2; SD = 1.7; N = 34) in males, and 1 to 11 (= 6.0; SD = 2.0; N = 23) in females (t = 4.2; df = 55; p> 0.01).

Among the meristics characters, that showed differences were: 7 supralabials, (3 and 4th in contact with the eye) (N = 63) and 7 (3, 4 and 5th) (N = 01) and temporals 1+1/1+1 (N = 43), 1+2/1+2 (N = 09), 1+1/1+2 (N = 02), and 1+2/1+1 (N = 03).

Geographic range. Tropical rainforest in southern Suriname and Brazil. In Brazil, it is present in the states of Pará, western Maranhão, southwest Mato Grosso and Rondônia ( Figure 4 ).

Comments. The variation of color patterns and the existence of melanic populations caused some taxonomic problems related to the proper identification of M. paraensis . The material analyses permitted to identification of melanic populations along the geographic distribution of M. paraensis in the states of Pará at Carajás, Melgaço and Mato Grosso state, Brazil. According to Roze (1994), this color variation is very common among coralsnakes belonging to the psyches group. In M. paraensis this fact is not related to sex, geographic distribution or age of individuals. Roze (1994) used the term “amazonic melanism” to characterize the melanin for the species from the psyches group, other species of Micrurus and colubrids. The variation on the number of black body rings does not differ from variation presented by Cunha & Nascimento (1978; 1982; 1993), Campbell & Lamar (1989) and Roze (1996).

The variation of the distribution of black and white tail rings of M. paraensis , cannot be treated as a diagnostic character, as considered by Abuys (1987) to describe the subspecies M. paraensis debruini . This character utilized by the author seems to be very common in M. paraensis , being observed in individuals from Mato Grosso and Pará states in Brazil.

According to Roze (1996) sexual dimorphism on the number of ventrals and subcaudals is common among species of Micrurus . Cunha & Nascimento (1982) noted sexual dimorphism in the number of ventrals and subcaudals in M. paraensis . Aside from, the characters presented by Cunha & Nascimento (1982), sexual dimorphism was detected in six meristics and four morphometric characters ( Tables 2 and 3 ).

The variation presented by Cunha & Nascimento (1978; 1982; 1993), Campbell & Lamar (1989; 2004), Roze (1996) and Carvalho (2002) of the number of ventrals and subcaudals in M. paraensis were: males have 188 to 200 ventrals and 45 to 52 subcaudals; females have 194 to 213 ventrals and 30 to 47 subcaudals. Based on analyses of a larger number of specimens, these characters presented the following ranges of variation: males have 184 to 197 ventrals and 36 to 54 subcaudals; and females have 186 to 217 ventrals and 30 to 52 subcaudals.

In the hemipenis of species of Micrurus a large lateral naked fold is present, and the sulcus spermaticus is bifurcated ( Slowinski, 1995; Roze, 1996). Hemipenial characters were also used to define two monophyletic groups (Roze, 1989, 1996; Campbell & Lamar, 1989; Slowinski, 1995). Micrurus paraensis shares with M. albicinctus , M. averyi , M. langsdorffi , M. psyches and others species with a monadal color pattern, long tail, long and strongly bifurcated hemipenis, with lobes elongated terminally and a large lateral naked fold; this may be a monophyletic group. According to Roze (1994), the psyches group form a natural group that share color pattern in monads, cephalic black cap, absence of supra-anal tubercles on males and presence of an elongated hemipenis, strongly bifurcated, and they can be differentiated by the number of ventrals and subcaudals, number of black and white body and tail rings. In the hemipenis of M. paraensis , described here for the first time, it is possible to observe the presence of characters considered to be synapomorphies of the M. psyches group (elongated organ and strongly bifurcated with lobes terminally elongated, and a large lateral naked fold, beyond, large calcified spines). Therefore, a systematic analysis in a phylogenetic paradigm could express the inferences of these characters.

Figures

FIGURE 1. Head of Micrurus paraensis (UFMT 1593) from Vale de São Domingos, state of Mato Grosso, Brazil: Dorsal (a), ventral (b), and lateral (c) views. Scale bar 5 mm.

FIGURE 2. Micrurus paraensis (MPEG 20867, 340 mm SVL) from Melgaço, state of Pará, Brazil: Dorsal (a) and ventral (b) views.

FIGURE 3. Hemipenis of Micrurus paraensis (UFMT 1596, Vale de São Domingos, state of Mato Grosso, Brazil). Sulcate (a) and asulcate (b) sides. Scale bar 5 mm.

FIGURE 4. Distribution of Micrurus paraensis (Closed circle – Material examined, open circle – Abuys (1987), closed square – Hoge et al. (1978), open square – Type-locality; open triangle - Frota (2004 )). Material examined and literature records are cited in Appendix 1.

Tables

TABLE 2. Variation of meristic data in males (N = 35) and females (N = 27) of Micrurus paraensis. (Legend: * Sexual Dimorphism (p> 0.01 and p <0.05); BBR – Black body rings; RBR – Red body rings; BTR – Black tail rings; WTR – White tail rings; N - Number of individuals; - mid; SD - Standard Deviation).

	Males			Females
Character	N Range		SD	N Range		SD
BBR *	35 12–18	14.8	1.4	26 13–21	17.1	2.2
RBR *	34 12–17	14.0	1.3	26 12–20	16	2.1
BTR *	34 5–12	8.2	1.7	23 2.0–11	6.4	1.9
WTR*	34 5–12	8.2	1.7	23 1.0–11	6.0	2.0
Ventrals*	35 184–197	191.3	3.6	27 186–217	205.1	7.9
Subcaudals*	35 36–54	47.3	3.4	27 30–52	38.0	6.6

TABLE 3. Variation of morphometric characters in males (N = 35) and females (N = 27) of Micrurus paraensis (Measures in mm). (Legend: * Sexual Dimorphism (p> 0.01 and p <0.05); N - Number of individuals; - mid; SD - Standard Deviation).

	Males			Females
Character	N Range		SD	N Range		SD
Snout-vent length *	31 220–463	362.5	64.6	22 175–590	422.0	101.7
Tail length *	31 25–85	63.7	16.1	22 20–77	49.3	13.5
Head length	28 7.9–14.7	11.8	1.6	21 8.1–16.6	12.4	2.1
Greater height of the head	28 2.9–6.0	4.7	0.7	21 2.3–6.3	4.9	1.0
Greater width of the head	28 4.8–9.2	6.5	0.9	21 3.8–9.4	7.0	1.5
Rostral length	25 0.8–3.3	1.2	0.4	20 0.9–2.0	1.3	0.2
Rostral width	26 1.8–3.0	2.4	0.3	20 1.6–3.6	2.5	0.5
Frontal length *	29 2.1–3.5	2.8	0.3	21 2.3–4.1	3.1	0.5
Frontal width	29 1.3–2.6	2.1	0.3	21 1.5–2.8	2.1	0.3
Parietal length	30 1.5–4.8	3.3	0.8	21 1.7–5.1	3.7	0.7
Parietal width	30 1.7–3.4	2.2	0.4	21 1.3–3.3	2.3	0.4
Vertical Eye height	28 0.7–1.7	1.1	0.2	22 0.7–1.6	1.1	0.2
Internasal length	31 0.6–2.6	1.3	0.4	21 1.1–2.7	1.7	0.4
Internasal width	31 1.1–3.2	1.7	0.4	21 1.2–2.9	2.0	0.4
Prefrontal length	31 1.0–2.6	1.8	0.4	21 0.7–1.7	1.1	0.3
Prefrontal width	31 1.5–2.8	2.2	0.4	21 0.9–2.0	1.4	0.4
Anterior Genial length	29 1.5–2.9	2.2	0.3	21 1.4–3.0	2.3	0.4
Posterior Genial length	28 2.0–3.4	2.6	0.3	21 1.7–3.8	2.8	0.5
Distance between Eyes *	29 2.9–4.8	4.0	0.4	22 3.2–5.8	4.3	0.6
Distance between Nostril	28 2.0–3.5	2.9	0.4	21 0.5–4.1	3.0	0.7
Distance between eye-oral edge	28 0.4–4.7	1.3	0.6	22 0.8–2.2	1.3	0.3