Micrurus silviae Di-Bernardo, Borges-Martins & Silva, 2007, sp. nov.
Creators: name: Di-Bernardo, Marcos
name: Borges-Martins, Marcio
name: Silva, Nelson Jorge Da
Publisher: name: Zenodo
Year: 2007
Subjects: Biodiversity
Taxonomy
Animalia
Chordata
Reptilia
Squamata
Elapidae
Micrurus
Micrurus silviae

description: Micrurus silviae sp. nov.
(Figures 1 and 2)
Type Material — Holotype: CRUPF 1488, adult male, from Passo Fundo Municipality, Miranda Stream (within the drainage basin of the Companhia Riograndense de Saneamento—CORSAN dam), in the W-NW of Rio Grande do Sul; collected on 21 March 2005 by Vilson Luiz Mello de Paulo.
Paratypes: Rio Grande do Sul - IB 699 (M), Alegrete; MCN 4652 (M) and IB 52173 (M), Cacequí; IB 6072 (M), IB 16643 (M), IB18689 (M), and IB 23418 (F), Carazinho; IB 53080 (M), Catuípe; MCN 5155 (M), IB 11122 (M), IB 11256 (M), IB 11432 (M), IB 15758 (M), IB 16604 (M), IB 18570 (M) and IB 40194 (F), Cruz Alta; IB 7357 (M), Friedhemi; IB 7846 (F), IB 8088 (M), and IB 23621 (F), Ijuí; IB 11615 (M), Itapeví, Alegrete; ZUFSM 0 86 (M), ZUFSM 2173 (F), and ZUFSM 2341 (M), Manoel Viana; CRUPF 581 (M), Mato Castelhano; CRUPF 149 (M), Nicolau Vergueiro; CRUPF 194 (M), Passo Fundo; IB 13640 (M), Rosário do Sul; IB 16055 (M), Santa Bárbara do Sul; MCN 3892 (M), Santa Maria; MCP 15983, Santo Augusto (M); MCP 12164 (F), Sarandi; MCN 8187 (F), Tupanciretã.
Diagnosis — Micrurus silviae is diagnosable from all other South American triadal coralsnakes by the combination of the following fixed characters: a) snout and head mostly black colored with white bordered scales (anteriorly), including the rostral, internasals, nasals, prefrontals, preoculars, and postoculars; b) gular region white with few black markings; and c) middle black ring 1.5 or twice as long as the external ones. Additionally M. silviae is unique in possessing an anteromedial process in the frontal bones.
Description of holotype —Rostral wider than high, prefrontals slightly longer than the internasals. Frontal longer than its distance from the snout; parietals as long as their distance from the snout. Dorsals in 15-15- 15 rows; 1+2 temporals; 7 supralabials; 7 infralabials; no preocular; 2 postoculars; 226 ventrals, 5 preventrals, and 21 subcaudals (paired). Snout predominantly black with white bordered scales anteriorly. Top of the head black including the frontal, supraoculars and parietals. Anterior border of the parietals partially white, and anterior border of the supraoculars and frontal white. Anterior temporals red and heavily marked by black with a thin white border anteriorly; posterior temporals red marked with black posteriorly (inferior border of the posterior inferior temporal white). First six supralabials white with black markings along the posterior bor- der reaching the middle and superior part of the 2nd, 3rd, 4th, and 5th scales; 6th supralabials mostly white (anterior half) with red posterior border, and black middle superior border; 3rd and 4th infralabials in contact with the orbit. Gular region white (mostly immaculate) with black markings between the anterior and posterior genials, and the posterior tip of the second genials. First five infralabials white; 6th and 7th infralabials red and all infralabials black marked posteriorly. 1st and 2nd ventral scales divided. The neck is red with first two to three scales heavily marked by black and the remainder of red scales black-tipped. The supraoculars are black with anterior white border. The first triad is separated from the parietals by two dorsal scales. There are 14 (13+1) black body triads, with the middle black ring two times longer than the external ones. White rings are blacktipped and shorter than the external black rings. Red rings shorter than the whole triad and all scales (red) are weakly black-tipped. Ventrally all black and white rings are irregular not always completing the circle around the body. Overall length of the holotype is 1,113 mm with a head length of 31 mm, a SVL of 1,050 mm, and a TL of 63 mm. The TL/SVL ratio is 0.06 (Figures 1 and 2).
Variation —With the initial sample of 34 specimens males showed a range of 205 to 232 ventral scales, 18 to 26 subcaudal scales, and 10 to 15 triads (n = 27; Tables 1 and 2). Females showed a range of 211 to 234 ventral scales, 15 to 24 subcaudal scales, and 11 to 13 triads (n = 6; Tables 1 and 2). The first triad is separated from the parietal scales by two to five dorsal scales. The head (nasals, prefrontals, frontal, supraoculars and parietals) is black with thin white borders at the anterior suture of scales. Rarely there is a reduction of the black color at the parietals in the unique fashion observed in Micrurus altirostris. However, sometimes a reduction of black in the margins of the parietals and a varying degree of white in the snout is also observable. The temporal region has a variable degree of red and black. The red rings may attain the length of the whole triad and even be a 1/3 longer; black tips of scales may vary from moderate to absent. The position of the first triad (as separated from the parietals) is quite variable within a range of one and a half to six dorsal scales with one specimen with one and a half scales (holotype), six specimens with two scales (17.6%), nineteen with three scales (55.9%), five with four scales (14.7%), two with five scales (5.9%), and one with six scales (2.9%). This is another example of the extreme values as 91.2% of the specimens had between one and a half to four dorsal scales separating the first triad from the parietals. The gular region has no tendency to melanism. Maximum total lengths of specimens of M. silviae includes 1,506 mm (MCP 15983 M), 1,333 mm (UPF 194 M), 1,310 mm (IB 6072 M), and 1,294 mm (IB 13640 M).
Color in preservative —All scales of the red rings are faded giving a cream color that is also visible on the head (behind and around the parietals). The black color of head, snout and triad rings are black and somewhat faded as a brownish color in old specimens. The white color of triad rings and gular region are light cream.
The general morphological characters of head and body color, triad arrangement, and scale counts are also diagnosable (by the PAA criterion of Davis & Nixon 1992) by the following combination:
a) head color pattern —mostly black in M. silviae, including the snout and all the head scales. In M. altirostris the black color is almost restricted to the supraoculars and frontal with the snout with varying degrees of melanism with a tendency to complete black scales (also interpreted as black snout with varying degrees of white markings). In most specimens, the parietals are almost completely red with a posterior black margin. In M. baliocoryphus the black color is mostly in parietals, frontal, and supraoculars with a white snout lightly marked with black; sometimes a white cross band might be present between the parietals and frontal and supraoculars. In M. frontalis, M. pyrrhocryptus and M. tricolor the head and snout are black with thin white markings between scales; very often the white markings are more evident in the snout of M. frontalis;
b) gular region pattern —white in M. silviae (with very few black markings); black in the anterior part in M. altirostris with remaining posterior part red, which might also be interpreted as a red (including both pairs of gulars and 3rd to 7th infralabials) and white (anterior border of the 1st pair of gulars an 1st to 3rd infralabials) with intense melanism. In M. baliocoryphus the gular region is mostly red with anterior part white (first three infralabials and anterior pair of genials), and red with varying black markings in M. frontalis, M. pyrrhocryptus and M. tricolor;
c) number of triads —ranges from 11 to 16 in M. silviae, 12 to 20 in M. altirostris, 10 to 16 in M. baliocoryphus, 10 to 19 in M. frontalis, 6 to 14 in M. pyrrhocryptus, and 9 to 12 in M. tricolor; this is typical of several meristic characters that show considerable overlap among species (Table 1). For this character the most divergent species are M. altirostris and M. pyrrhocryptus (on both numerical extremes), but there is an obvious gradient among species when using means and extreme values. However, when using means and standard errors it is possible to separate the species that overlap with M. silviae and/or M. baliocoryphus (Figure 3). In M. silviae (range = 11–16 triads), 97.0% of the specimens (n=33) are within the range of 11–15 triads, with one specimen having 16 triads (3.0%). In M. altirostris (12–20 triads) 98.8% of the specimens (n=574) are within the range of 13–18 triads, with six specimens with 19 triads (1.0%), and one specimen with 20 triads (0.2%). In M. baliocoryphus (10–16 triads) 94.3% of the specimens (n=100) are within the range of 11 –15 triads, two specimens have 10 triads (1.9%), and four specimens with 16 triads (3.8%). In M. frontalis (10–19 triads) 98.8% of the specimens (n=565) are within the range of 11–17 triads, three specimens have three triads (0.5%), and three specimens with 18 triads (0.5%), and one specimen with 19 triads (0.2%). In M. pyrrhocryptus (6–14 triads) 96.6% of the specimens (n=225) are within the range of 7 and 11 triads, four specimens have 6 triads (1.7%), one specimen with 12 triads (0.4%), two specimens with 13 triads (0.9%), and one specimen with 14 triads (0.4%). In M. tricolor (9–12 triads) 95.0% of the specimens (n=19) are within 9 and 11 triads, and one specimen had 12 triads (5.0%). All species show a pattern of one complete tail triad and usually 1/3 and rarely 2/3 of an incomplete triad. The same assumptions of extreme values and standard errors are applicable to ventral and subcaudal scales (see below);
d) position of the first triad —in M. silviae the first body triad is separated from the parietals by two to six scales, in M. altirostris it ranges from one to three scales, in M. baliocoryphus it ranges from three to six scales, in M. frontalis it ranges from one to seven scales (fusion of the black color of head and first triad is often observable); in M. pyrrhocryptus it ranges from five to eight scales, and in M. tricolor it ranges from seven to eleven scales. This character is subject to some variation but is useful for distinguishing these last two species (as a group) from the first four (as a group);
e) pattern of triads —middle black ring one-and-one-half to twice as long as the external ones in M silviae with red and white dorsal scales usually black-tipped (weakly tipped on red rings) and white rings shorter than the external black rings; subequal black rings in M. altirostris (middle one can be a little longer), with white rings as long as the external black rings (sometimes a little shorter, and very short in some specimens from Uruguay) with dorsal scales black-tipped (a little less in the red rings); middle black ring 2 to 2.5 times longer than the external ones in M. baliocoryphus with white rings (immaculate in anterior 1/3 to 2/3 of body) as long as the external black rings (Table 2); subequal black and white rings in M. frontalis (sometimes the middle black ring may be slightly longer than the external ones) with varying degrees of black tipped scales; middle black ring 2 to 4 times longer and white rings shorter than the external black rings in M. pyrrhocryptus with all scales black tipped; and middle black ring 2 to 3 times longer than the external ones in M. tricolor with white rings (immaculate in anterior 1/3 to 2/3 of body) of the same length of the external black rings. The description of a red or white ring being immaculate means that they are without the heavy black markings on the tip of the dorsal scales, they are extremely variable among specimens of a given species, and they are sometimes restricted to the posterior 1/3 or 2/3 of body;
f) number of ventral scales —ventral scales range from 205 to 232 in males (x=220.52) and from 211 to 234 (x=221.43) in females of M. silviae; 173 to 242 in males (x=208.80) and from 185 to 223 in females (x=208.85) of M. altirostris; 172 to 232 in males (x=221.06) and from 208 to 233 in females (x=220.10) of M. baliocoryphus; 190 to 250 in males (x=225.07) and from 197 to 252 in females (x=225.93) of M. frontalis; 202 to 244 in males (x=228.33) and 213 to 251 in females (x=232.09) of M. pyrrhocryptus; and 214 to 234 in males (x=226.00) and 208 to 231 in females (x=221.12) of M. tricolor (Table 1). This character shows considerable variation among the six species with an overlap owing to extreme values, which can be better demonstrated with standard errors as some species are separable (i.e., low numbers in M. altirostris and high in M. pyrrhocryptus; Figure 4);
g) number of subcaudal scales —subcaudal scales range from 18 to 25 in males (x=22.30) and from 15 to 24 (x=18.71) in females of M. silviae; 12 to 28 in males (x=19.83) and from 11 to 25 in females (x=18.04) of M. altirostris; 14 to 31 in males (x=22.82) and from 14 to 23 in females (x=20.15) of M. baliocoryphus; 14 to 27 in males (x=21.94) and 14 to 28 in females (x=19.86) of M. frontalis; 16 to 30 in males (24.56) and 19 to 26 in females (x=21.97) of M. pyrrhocryptus; and 24 to 29 in males (x=26.42) and 20 to 26 in females (x=22.50) of M. tricolor (Table 1). This character shows the widest range of overlap among the six species but with standard errors both sexes for most species are separable (Figure 5).
Sexual dimorphism —to demonstrate sexual dimorphism the ratio of TL/SVL is usually adopted with varying degrees of success (Roze 1996; Silva & Sites 1999; Campbell & Lamar 2004). For this group of triadal coralsnakes there is also a considerable overlap of values. However, with standard errors both sexes are easily separated (Figure 6). It can be also highlighted with the data of ventral and subcaudal scales (see also Figures 4 and 5).
Hemipenial morphology —as in most of triadal coralsnakes the hemipenis of M. silviae is bilobed with uniform size spines and a bifurcated sulcus spermaticus (CRUPF 1488— holotype, right organ; Figure 7). In the sulcate and asulcate surfaces the spines are large and uniform from the tip to near the base. The lobes are moderately long and conical; viewing from the sulcate side, the tip of the right lobe is more acute than the left. Measuring from the division point of the sulcus spermaticus, the lobes are 10.0 mm long, representing 48.3% of the total length of the organ. Between the lobes (in the intersection of them) there is a poorly ornamented region, with few and small spines, better visible from the sulcate side. The fully everted organ is 20.7 mm long, reaching the level of the 7th subcaudal. The distance from the base of the organ to the division point of the sulcus is 13.6 mm; the division occurs at the level of the 4th subcaudal. The base of the organ is 5.3 mm long and naked.
Cranial osteology —the premaxilla presents the posterior extension of the palatine process in both sides, a character shared with M. altirostris, M. baliocoryphus, M. frontalis, M. pyrrhocryptus, and M. tricolor. The dorsomedial process of the prefrontals are narrow and do not contact at midline. Only M. frontalis and M. pyrrhocryptus seem to present this condition. The anteromedial process of the frontals is present in M. silviae and absent in all other species. The parietal is longer and wider (measured at its widest point) in M. silviae. There is a dorsal crest at the midline of the parietal bone that might present a flat triangular tabular process anteriorly. This process might be discrete and small (as in M. pyrrhocryptus), reach the anterior 1/3 (M. silviae), or be wider and reach 2/3 of the entire length of the parietal bone (M. altirostris, M. baliocoryphus, M. frontalis, and M. tricolor). In M. silviae the parietal bone also presents a similar process at the posterior end of the parietal which is also pointed (as in M. pyrrhocryptus and M. tricolor). The suture of prefrontals + frontals is anterior to the maxilla + pterygoid suture in M. silviae, M. baliocoryphus, M. frontalis, M. pyrrhocryptus, and M. tricolor, and posterior in M. altirostris. In M. silviae there are seven to eight palatine, four to seven pterygoid, and ten to twelve dentary teeth. There are no noticeable differences in shape and proportions of the remaining cranial bones (Figure 8). However, there is an ongoing osteological study within the triadal coralsnakes that might contribute to better understand the fixed and variable conditions of this set of characters.
Statistical summary of morphological variation — Tables 1 and 2 summarize the descriptive statistics for all meristic and morphometric data collected from the specimens used in this description and the comparative species. For all characters analyzed, it is possible to observe a large overlap of variation among species, as revealed by maximum and minimum values, but in general, the use of standard errors show statistical differences among the species. Wilk’s statistics was equal to 0.045 (F = 111.98, P <0.0000), indicating significant differences among species in the multivariate space of the characters analyzed. The first two canonical axes explain 95% of the variation among species, which 81% of this total amount being concentrated in the first canonical axis. This first axis is basically composed by number of triads (TRI) and length of middle black ring (MBL). The second axis is defined by ventrals (VE) and length of anterior black ring (ANTBL) (Table 3). The distribution of individuals in the bivariate space formed by the first two canonical axis reveal that M. altirostris and M. pyrrhocryptus appear in opposite regions of the space along the first axis. In the other hand, M. baliocoryphus, M. silviae, M. tricolor, are in a clear intermediate position between the two extremes (M. altirostris and M. pyrrhocryptus), whereas M. frontalis overlaps with M. silviae and M. altirostris and M. baliocoryphus. There is also an overlap of M. tricolor and M. pyrrhocryptus (Figure 9). These results of CVA are qualitatively similar when the sexes are analyzed separately (data not shown). Despite the overlap of M. silviae and M. baliocoryphus and M. tricolor and M. pyrrhocryptus on both canonical axes there are several fixed characters that separate these species. For M. silviae and M. baliocoryphus it includes: (a) length of middle black ring; (b) length of white rings; (c) absence or presence of melanism on anterior 1/3 to 2/3 of white rings; (d) color pattern of the gular region; (e) color pattern of the snout; (f) color pattern of the head; (g) cranial osteology features. For M. tricolor and M. pyrrhocryptus it includes: (a) length of middle black ring; (b) distance of first triad from parietal scales; (c) length of external black rings compared to the middle black ring; (d) cranial osteology features.The Hotelling’s T2-test indicated that all species differ significantly from each other considering the 12 variables used (p<0.0001) (Table 4). When using the Mann Whitney U-test for number of ventral, subcaudal scales and triads number separately many differences were significative even after the Bonferroni’s correction for multiple significance tests. However, for each of these three variables there were exceptions: (a) ventral scales—there were no significant differences between M. baliocoryphus and M. silviae (p=0.306), M. baliocoryphus and M. tricolor (p=0.142), M. frontalis and M. tricolor (p=0.600); and M. silviae and M. tricolor (p=0.057); (b) subcaudal scales—there were no significant differences between M. baliocoryphus and M. frontalis (p=0.070), M. baliocoryphus and M. silviae (p=0.400), M. frontalis and M. silviae (p=0.840), and M. pyrrhocryptus and M. tricolor (p=0.294); (c) number of triads—there were no significant differences between M. baliocoryphus and M. silviae (p=0.500), and M. baliocoryphus and M. frontalis (p=0.100) (Table 5).
Etymology —the specific name is a noun in genitive case, in honor of Silvia Di Bernardo a promising herpetologist that died suddenly in July 2002.
Geographic Distribution — Micrurus silviae is known from 17 localities in Western to Northern Rio Grande do Sul, Brazil. One specimen was photographed in one additional locality, the Municipality of São Francisco de Assis (not collected). It is possible that its range includes Misiones, part of NE-E Corrientes (Argentina) and SE-E of Departamento Itapua (Paraguay) (Figure 10).
TABLE 4. T2-test between species of coralsnakes. Above diagonal are the significance value levels. Below diagonal are T2-test values.
Legend: Species 1 – M. altirostris; Species 2 – M. baliocoryphus; Species 3 – M. frontalis; Species 4 – M. pyrrhocryptus; Species 5 – M. silviae; Species 6 – M. tricolor.
Legend: Species 1 – M. altirostris; Species 2 – M. baliocoryphus; Species 3 – M. frontalis; Species 4 – M. pyrrhocryptus; Species 5 – M. silviae; Species 6 – M. tricolor.
Micrurus silviae probably occurs in open habitats, as its distribution is associated to the grasslands areas of western and northern Rio Grande do Sul. The geographical range of known records agrees closely to the northern delineation of the Uruguayan Savannas ecoregion along its interfaces with the Paraná-Paraíba Interior Forests and Araucária Moist Forests (Olson et al., 2001; WWF, 2001). This region corresponds to the range of grasslands inter-laced with gallery woodlands (IBGE, 1986). Distribution occurs along different geomorphologic units, encompassing parts of the Peripheric Depression and the Brazilian Southern Plateau, extending from the western lower elevations in the Depression of the Ibicuí-Negro Rivers and the Uruguaiana Plateau to the northern Santo Angelo Plateau (IBGE, 1986). Altitudinal distribution accordingly ranges from about 100 to nearly 700 m (above sea level) in Mato Castelhano.
Other sympatric species —Within the same geographical region there are records of one monadal species (Micrurus corallinus) and two additional triadal species (Micrurus decoratus and Micrurus lemniscatus carvalhoi). Micrurus corallinus has a unique pattern of one black ring with two external white rings arranged in 15–27 body combinations; 194 to 198 ventral scales in males, and 210 to 224 in females; 43 to 47 subcaudal scales in males, and 27 to 32 in females (fide Campbell & Lamar, 2004). It is impossible to confuse the other species with Micrurus corallinus. Micrurus decoratus (record indicated by Lema & Azevedo, 1969) has a black snout, with color restricted to rostral, nasals, internasals, and anterior 1–2 supralabial scales, followed by a yellowish-white crossband that covers the posterior part of nasals, part of 1 to 3 supralabials, anterior part of preoculars, prefrontals, and anterior edge of frontal scale. This is followed by a black crossband that covers the posterior part of the third, fourth, and anterior part of the fifth supralabials, orbit region, and postoculars, supraoculars, most part of frontal, and anterior part of parietals. The rest of the dorsal region is red with a frequent irregular black pigmentation. The gular region is mostly red with 1 to 3 infralabials completely black. Body triads vary from 15 to 19. The middle black ring is 1.5 to 2 times longer than the external ones, and the yellowish-white rings are of the same length or a little longer than the external black rings. The yellowishwhite rings have a tendency to be immaculate in most specimens of this species. Ventral scales vary from 195 to 208 in males, and 209 to 218 in females; subcaudal scales vary from 19 to 22 in males, and 16 to 19 in females (fide Roze, 1996; Campbell & Lamar, 2004). Micrurus lemniscatus is a complex group of subspecies poorly defined with an enormous geographical range. This taxon is under investigation at present time (NJS pers. comm.). The form found in the study region is Micrurus lemniscatus carvalhoi (Silva & Silva, 1996; Silva & Sites, 1999; Di-Bernardo et al., 2001). This taxon has a black snout, including the rostral, anterior part of nasals, sometimes reaching the anterior border of internasals. There is a white crossband that covers part of nasals, anterior part of preoculars, first two and anterior part of third supralabials, most part of internasals, prefrontals, and anterior border of frontal. This is followed by a black crossband that covers the posterior bor- der of the third, fourth, fifth, and anterior part of sixth supralabials, orbit region, postoculars, most of temporals, supraoculars, most of frontal, and anterior part of parietals. The rest of the dorsal area is red. The gular region is red with mental and first 3 to 4 infralabials completely black. Ventral scales vary from 235 to 246 in males, and 242 to 268 in females; subcaudal scales vary from 29 to 36 in males, and 27 to 34 in females (fide Roze, 1996; Campbell & Lamar, 2004).
description: Published as part of Di-Bernardo, Marcos, Borges-Martins, Marcio & Silva, Nelson Jorge Da, 2007, A new species of coralsnake (Micrurus: Elapidae) from southern Brazil, pp. 1-26 in Zootaxa 1447 on pages 3-18, DOI: 10.5281/zenodo.176163