Apostolepis albicollaris Lema, 2002

Entiauspe-Neto, Omar M., Koch, Claudia, Guedes, Thaís B., Paredero, Rafael C. B., Tiutenko, Arthur & Loebmann, Daniel, 2022, Unveiling an enigma from the Cerrado: taxonomic revision of two sympatric species of Apostolepis Cope, 1862 (Dipsadidae: Xenodontinae: Elapomorphini) from central Brazil, European Journal of Taxonomy 817 (1), pp. 143-182 : 150-168

Apostolepis albicollaris Lema, 2002

Apostolepis albicollaris Lema, 2002: 228 . Holotype MCP 8355 (adult male; Fig. 1A ), from Distrito Federal, Brasília , Parque Zoológico do Distrito Federal (15.775247º S, 47.922950º W, 1171 m altitude), Distrito Federal, Brazil.

Apostolepis cerradoensis Lema, 2003: 123 . Holotype MCP 15219 (adult male; Fig. 1C ), from Usina Hidrelétrica de Serra da Mesa , Minaçu (13.510069º S, 48.209950º W, 351 m altitude), Goiás, Brazil. Syn. nov.

Heterochresonymy

Apostolepis dimidiata – Lema 1993:35. — Harvey 1999: 408 (in part, misidentification) (figs 1–4, 8).

Diagnosis

This species presents (1) 15/15/15 dorsal scales; (2) preocular present, contacting nasal; (3) loreal absent (rarely present); (4) temporals absent; (5) supralabials six (rarely four, five, seven), 2 nd –3 rd in contact with orbit; (6) infralabials six or seven (rarely eight), 1 st –4 th in contact with anterior chinshields; (7) ventrals 196–230 (196–208 in males; 206–230 in females); (8) subcaudals 24–33 (24–30 in males; 28–33 in females); (9) dorsal pattern uniform orange or red, with two large lateral black stripes (a vestigial vertebral stripe rarely present); (10) ventral pattern uniformly black, bicolor or white; (11) white nuchal collar present, 3–4 wide, black nape collar present (rarely absent), 1.5–3 scales wide; (12) caudal blotch 5–9 scales long on dorsum, incomplete (rarely complete) on venter, terminal scale black and white; (13) supralabial blotch elongated, three to five scales wide; (14) maximum SVL 451 mm, maximum TL 50 mm; (15) hemipenis slightly bilobed, semicapitate, semicalyculate, body covered by moderately sized hooked spines on sulcate side.

Type material

Holotype BRAZIL • adult ♀; Distrito Federal, Brasília, Parque Zoológico do Distrito Federal ; 15.775247º S, 47.922950º W; alt. 1171 m; MCP 8355 ( Fig. 1A ).

Paratypes (n = 2) BRAZIL • 1 adult ♀; Goiás, Ipameri ; 17.72197º S, 48.1597º W; alt. 64 m; IB1822 • 2 adult ♂♂; Goiás, Minaçu ; 13.5331º S, 48.22º W; alt. 351 m; UHESM 18484 , 20907 .

Description

Head slightly distinct from body, twice as long as wide, triangular in dorsal view, arched in lateral view ( Fig. 3 ); cervical constriction absent; snout conical, tapered in dorsal view, projected in lateral view; nasal undivided, longer than wider, in contact with preocular (rarely separated), rostral, first two supralabials and prefrontals; prefrontals paired, longer than wider, in contact with rostral, nasal, supraocular, and frontal; supraocular longer than wider; frontal hexagonal, longer than wider; internasals absent (rarely present); loreal absent (rarely present); preocular present, longer than high; eye small; interorbital distance as long as parietal distance; postocular single, as long as high; temporals absent; occipital present, in contact with parietal and sixth supralabial; supralabials six (rarely four, five, seven), first in contact with nasal and rostral, 2–3 in contact with orbit, 3–4 in contact with postocular, 5–6 in contact with parietal; infralabials six or seven (rarely eight), first pair in contact with symphisal and anterior chinshields, second, third, and fourth pairs in contact with anterior chinshields, third, fourth, fifth, sixth, and seventh pairs in contact with posterior chinshields; dorsal rows 15/15/15; short tail, terminal spine rounded.

Coloration in life

Live specimens have dorsal portion of head black, with snout blotch absent or thin and divided, white or cream colored, covering rostral and prefrontals; white nuchal collar present, 3–4 scales wide; black nape collar present, covering 1.5–3 scales, rarely absent; lateral head portion black, white supralabial blotch elongated, covering three to five scales, infralabials white; ventral portion of head white, with a complete gular black collar; background dorsal coloration red or orange, vertebral stripe vestigial or absent, two lateral black stripes ( Fig. 4A–F ); ventral coloration uniformly black, bicolor, or white; caudal blotch 5–9 scales wide on dorsum, incomplete (rarely complete) on venter, terminal spine black and white.

Coloration in preservative

Orange and red colorations turn gray or white in preservative ( Fig. 1 ).

Comparisons

Apostolepis albicollaris might be misidentified as another congener from the Cerrado, Apostolepis dimidiata ( Fig. 4G–H ). Both species share an uniformly red dorsal background coloration, with two lateral black stripes, a white or black venter, and have overlapping scale counts of supralabials, infralabials, and subcaudals. However, A. albicollaris can be distinguished from A. dimidiata (characters in parentheses) by having nuchal collars (absent), a small-sized semicapitate hemipenis (medium-sized capitate hemipenis), and lower ventral scale counts (220–244 total range, 226–240 in males, 220–244 in females). It should also be noted that A. dimidiata is not sympatric with A. albicollaris in most of its range, with the former species occurring in the Cerrado of southeastern and central-western Brazil, in the states of São Paulo, Paraná, Minas Gerais, and Mato Grosso do Sul, and in Paraguay, while the latter is restricted to Goiás, Distrito Federal, and Minas Gerais, in central Brazil; both species can be found in sympatry in a small stretch of Cerrado in western Minas Gerais, in the locality of Uberlândia.

Three other similar congeners occur in sympatry with A. albicollaris : Apostolepis assimilis (Reinhardt, 1861) , Apostolepis flavotorquata (Duméril, Bibrón & Duméril, 1854) , and Apostolepis sanctaeritae Werner, 1924 . Apostolepis assimilis can be diagnosed from A. albicollaris based on its dorsal pattern with two black stripes (uniformly red), a divided snout blotch (entire), elongated supralabial blotch, up to five scales wide (smaller, up to three scales wide). Apostolepis flavotorquata can be diagnosed from A. albicollaris based on its distinct dorsal pattern (uniformly red or with three black stripes), ventral coloration in life (yellow), and hemipenial morphology (organ long and simple, spinules restricted to proximal area, enlarged spines absent, asulcate surface calyculate) ( Lema & Renner 2005). Apostolepis sanctaeritae can readily be diagnosed from A. albicollaris based on its single nuchal collar (additional white nuchal collar), smaller black nuchal collar, covering 1.5–3 scales (4–7 scales), elongated white supralabial blotch (small, tear-shaped), and a divided, white snout blotch in life (single, orange).

An extralimital species, Apostolepis quirogai Giraudo & Scrocchi, 1998 , bears striking similarity to A. albicollaris ( Fig. 4I–J ). Both species share a uniformly red dorsal background coloration, with two lateral black stripes, wide white and black nuchal collars, and black ventral coloration. However, A. albicollaris can be distinguished from this species based on its lower ventral scale counts (269 in the single male, 276 in the single female), a divided snout blotch (entire), and a larger, elongated, supralabial blotch (smaller, covering up to three scales). Furthermore, A. quirogai occurs in Misiones, in northwestern Argentina, and northern Rio Grande do Sul, southern Brazil, in Alto Paraná Atlantic Rainforests, a very distinct environment from the Cerrado of Central Brazil in which A. albicollaris occurs.

From Apostolepis multicincta Harvey, 1999 and A. dorbignyi (Schlegel, 1837) , two extralimital species from the Argentine and Bolivian Chaco open areas, A. albicollaris can be distinguished based on its dorsal pattern with two lateral black stripes (uniformly red coloration in life), divided snout blotch (entire), and bicolored tail tip (uniformly white).

Furthermore, A. albicollaris can be distinguished from A. adhara França, Barbo, Silva-Jr, Silva & Zaher, 2018, A. ambiniger (Peters, 1869) , A. arenaria Rodrigues, 1993 , A. borelli Peracc, 1904 , A. breviceps Harvey, Gonzales & Scrocchi, 2001 , A. christineae Lema, 2002 , A. gaboi Rodrigues, 1993 , A. goiasensis Prado, 1942 , A. intermedia Koslowsky, 1898 , A. kikoi Santos, Entiauspe-Neto, Araújo, Souza, Lema, Strüssmann & Albuquerque, 2018 , A. lineata Cope, 1887 , A. longicaudata Gomes, 1921 , A. nelsonjorgei Lema & Renner, 2004 , A. niceforoi Amaral, 1935 , A. nigrolineata (Peters, 1869) , A. nigroterminata Boulenger, 1896 , A. phillipsi Harvey, 1999 , A. quirogai Giraudo & Scrocchi, 1998 , A. rondoni Amaral, 1925 , A. serrana Lema & Renner, 2006 , A. striata Lema, 2004 , A. tenuis Ruthven, 1927 , A. thalesdelemai Borges-Nojosa , Lima, Bezerra & James, 2017, A. underwoodi Lema & Campbell, 2017 , and A. vittata (Cope, 1887) based on a combination of its uniformly red dorsal pattern with two lateral black stripes (a different combination of none, three, five, seven, or eleven dorsal stripes, over red, yellow, brown, black or gray background coloration) with the presence of white and black nuchal collars (nuchal collars absent in A. ambiniger , A. breviceps , A. christineae , A. dimidiata , A. goiasensis , A. intermedia , A. lineata , A. longicaudata , A. niceforoi , A. serrana , A. striata , A. vittata , variable for A. nigrolineata and A. thalesdelemai ).

Hemipenis

Hemipenis slightly bilobed, semicapitate, semicalyculate ( Fig. 5 ). Lobes slightly differentiated, present on distal portion of an incomplete capitular ring; lobes rounded, present on distal portion next to incomplete capitulum; lobes and incomplete capitulum covered by papillate calyces on sulcate and lateral sides; incomplete capitulum inconspicuous on both asulcate and sulcate sides, slightly smaller than hemipenial body, and positioned above bifurcation of sulcus spermaticus. Bifurcation of sulcus spermaticus in middle of organ. Capitular groove slightly distinct on sulcate side. Sulcus spermaticus branching centrolineally, with wide invagination on apex and incomplete capitulum; margins of sulcus spermaticus thin and inconspicuous, bordered by expanded lips. Hemipenial body moderately long for Apostolepis , subcylindrical; on sulcate surface, hemipenial body covered by small to moderate-sized hooked spines; on asulcate surface, hemipenial body with large basal naked pocket, extended to medial and apical regions, covered by enlarged spines, with inconspicuous lamellae on its asulcate side apex; 1–5 rows of enlarged spines present on lateral portion of sulcate side and medial and apical region of asulcate side.

Sexual dimorphism and variation

Females of Apostolepis albicollaris have higher ventrals (t 13,9 = 44.98, P <0.0009, n = 22), and lower subcaudals (t 13,9 = -34.18, P <0.005, n = 22) than their male counterparts ( Fig. 6 ). These results are in agreement with the inferences on sexual dimorphism for A. albicollaris encountered by Nogueira et al. (2012), differing only in detecting sexual dimorphism in subcaudal counts, to which these authors mention a tendency for males to have higher subcaudal counts, but failed to detect statistical differences among sexes. No differences of SVL and TL were encountered, although this might also be attributed to a relatively small sample size between groups. In males, the TL is 9–11% (10 ± 0, n = 13) of total length, and SVL is 88–89% (88 ± 0, n = 13) of total length, while in females, the TL is 7–9% (8 ± 0, n = 9) of total length, and SVL is 90–91% (90 ± 0, n = 9) of total length. Males have 197–215 ventrals (204 ± 5.6, n = 10), and 29–32 subcaudals (31 ± 1.4, n = 10), while females have 206–230 ventrals (216 ± 9.4, n = 7), and 24–30 subcaudals (28 ± 2.2, n = 7); these values appear to be close to the ones reported for A. ambiniger ( Entiauspe-Neto et al. 2021b) .

Geographic distribution and natural history

Known from the states of Goiás, Distrito Federal, and Minas Gerais, central Brazil, in the Cerrado biome ( Fig. 7A ). The locality reported by Nogueira et al. (2019) in Uruaçu, at Poções municipality, Bahia state, is considered here as erroneous. The specimen on which this record is based (IBSP 26712) is reanalyzed herein, and redetermined as being from Cana Brava, on the outskirts of Minaçu municipality, Goiás. Apostolepis albicollaris occurs in open areas, with dense shrub vegetation. Nogueira et al. (2012) report predation on legless lizards, twilight activity, and reproduction data.

Conservation status

It is known from 37 records representing 17 localities (unique georeferenced coordinates) ( Fig. 7A ). Its extent of occurrence was calculated to be 62 434 517 km ² and its area of occupancy was calculated to be 64 000 km² (B2). The species occurs in less than 10 locations (a). It is under strong pressure by the continued decline in habitat quality by extensive and ongoing habitat loss and fragmentation (b(iii)) due to expansion of agriculture, pasturing, mining, and fire frequency ( Fig. 7 BC). Additionally, only a small part of the distribution of the species is located in just one Protected Area (Parque Nacional de Brasília, Fig. 7D ). We suggest the species is under threat and qualifies to be listed as Vulnerable (VU ab(iii)).

Molecular analyses and systematics

Interspecific uncorrected p -distances range from 1 to 7% for 12S ( Table2 ) and 0to 1% for CMOS ( Table 3 ). Apostolepis albicollaris has a remarkably small genetic difference regarding its putative sister-species, Apostolepis dimidiata , having p -distances of 1% for 12S and 0% for CMOS. Further studies with larger samples and more molecular markers are needed in order to evaluate the presence or absence of gene flux and monophyletic reciprocity among species. Notably, the small distances recovered for the CMOS gene indicate that this single-copy, intronless, slow evolving nuclear marker may contain little phylogenetic information for this group, although proven useful for higher level relationships in squamates ( Saint et al. 1998). Patristic distances among A. albicollaris and A. dimidiata were recovered as 0.055, and for other species of Apostolepis ranged from 0.053 to 0.090 (for A. flavotorquata and A. sanctaeritae , respectively). The mean interspecific patristic distance for Apostolepis is recovered as 0.061, and for the other Elapomorphini genus, Phalotris , as 0.116. The results can be seen in Supplementary Table 4.

The phylogenetic trees inferred under maximum likelihood and Bayesian inference recovered as monophyletic the sampled Elapomorphini terminals ( Apostolepis , Elapomorphus , Phalotris ), with a

final ML optimized likelihood of –InL = –12757.360116. All Elapomorphini terminals are recovered as a sister group to Echinantherini genera. Both trees largely agree with each other regarding internal nodes within our clade of interest ( Elapomorphini ), and are depicted with a maximum likelihood topology and node values for both bootstrap (maximum likelihood) and consensus support (Bayesian inference) ( Fig. 8 ).A clade composed of A. albicollaris and A. dimidiata is recovered as strongly supported, sister to A. flavotorquata , another red congener from the Cerrado. The Apostolepis assimilis species group (sensu Ferrarezzi 1993; Ferrarezzi et al. 2005), composed of A. assimilis , A. cearensis , and A. sanctaeritae , is also recovered as monophyletic. Regarding the intrageneric and intergeneric relationships of Apostolepis terminals, our topology agrees with the one presented by Zaher et al. (2019).

Snout osteology

Snout complex consists of premaxilla, nasals, septomaxillae, vomers, and prefrontals ( Figs 9–10 ).

Premaxilla single, thick, robust, and edentulous, 1.5 (MCP 15219) to 1.6 (MCP 8355) times as broad as high; posterodorsally oriented ascending process has two broad lateral wings and a triangular dorsal apex, contacting anterior end of nasals; transverse processes are posterolaterally oriented, define widest part of premaxilla and are partly visible (MCP 8355) or not (MCP 15219) in dorsal view, long, approaching but not contacting maxillae; posteriorly oriented vomerine processes are robust thumb-like and almost parallel (MCP 15219) or slightly laterally diverging (MCP 8355), with a blunt tip, dorsally contacting anteroventral part of septomaxilla, distinctly separated from anterior end of vomers; ventral surface of premaxilla pierced by a slit-like foramen in anterior region and may have further perforations or notches (MCP 15219).

Nasals paired, more or less rectangular in dorsal view, 1.8 (MCP 15219) to 2.2 (MCP 8355) times as long as broad, convex, in medial contact along a straight suture, with front edges forming a broad V-shaped anterior region, together framing ascending process of premaxilla; lateral edges slightly curved downwards; posteriorly each nasal shares a loose, slightly oblique suture with corresponding frontal, although right nasal of MCP 15219 has a deep, almost circular indentation posteromedially,

0.02

which means that this nasal is hardly in contact with frontal; posterolaterally a small contact region with prefrontal; posteroventral process of nasal contacts anteroventral process of frontal posteriorly and anterior tip of dorsally oriented process of parasphenoid rostrum ventrally; vertical lamina of nasals laterally contacting medial edge of septomaxillae.

Septomaxillae paired and 1.8 (MCP 15219) to 2 (MCP 8355) times as long as broad, separated from each other by vertical laminae of nasals; each with a broad ascending conchal process, freely extending laterally beyond lateral edge of nasal in dorsal view, but not reaching height of lateral nasal edge; anteromedial process of septomaxilla one-fifth (MCP 8355) to one-sixth (MCP 15219) of total length of septomaxilla, curved and oriented anterolaterally, each extending over half depth of premaxilla and contacting posterior lamina of lateral wing of premaxillary ascending process, not visible in dorsal view; posteromedial process long and thin, accounts for 43% (MCP 8355) to 45% (MCP 15219) of total length of septomaxilla, contacts vertical lamina of nasal medially, rounded posterior tip contacts anteroventral tip of frontal, just lateral to ventral contact region between nasal and frontal; septomaxillary body a complex structure partly made of only thin bone material with a rounded indentation in rear view; anterior region of septomaxillary body medially contacting dorsal surface of premaxillary vomerine process; posterior region of septomaxillary body and ventral surface of posteromedial process of septomaxilla contact anterior and dorsal region of vomer.

Vomers paired, complex structures, about 1.4 times as long as wide, medially in contact, and with anterior and posterior regions diverging; anteriorly and dorsally contacting septomaxilla, laterally contacting anterior region of palatine; body of vomer made of thin bone material and globular, with an anteriorly oriented opening; bifurcate vertical posteromedial laminae diverging dorsally and ventrally, framing but not contacting anterior region of choanal process of palatine.

Prefrontals paired, oriented vertically and slightly oblique, 1.7 (MCP 8355) to 1.9 (MCP 15219) times as high as wide, greatly separated from each other, forming anterior margin of orbit; in lateral view, anterior margin undulated (MCP 15219) or convex (MCP 8355); posterolateral margin slightly concave; anterodorsally a small contact region with posterolateral region of nasal; dorsal edge contacts anterolateral edge of frontal along a slightly oblique suture; ventral edge firmly contacts dorsal surfaces of maxilla and of maxillary process of palatine; in rear view, a large, slightly oval lacrimal foramen visible in ventromedial region.

Braincase osteology

Braincase composed of frontals, parietal, supraoccipital, prootics, exoccipitals, parabasisphenoid, and basioccipital ( Figs 9–10 ).

Frontals paired, about semicircular in dorsal view, about 1.8 (MCP 15219) to 2 (MCP 8355) times as long as wide, slightly convex, in medial contact with a straight suture; only a short part of lateral margin of each frontal, at region of greatest width of frontal, participates in formation of dorsal margin of orbit; anterior edge slightly oblique, forming a loose suture with posterior edge of nasal; anterolateral edge forming an oblique suture with prefrontal; posterior edge curved and framed by anterolateral processes of parietal; anteroventrally frontal contacts nasal and directly lateral to this contact zone has a bulge whose anterior surface contacts posterior end of posteromedial process of septomaxilla; laterally each frontal has a ventromedially oriented concave lamina, that contacts its counterpart medially along anterior third of its length; anteromedially, frontal exhibits a vertical lamina fused ventrally with lateral lamina to form a short tubular structure in anterior region of each frontal, with vertical laminae of both frontals in firm medial contact; posterior to tubular structure, lateral lamina of both frontals clearly separated, with their medial margins approximately parallel to each other; on ventral side of contact zone of vertical lamina of frontal a facet into which anterior part of dorsal process of parabasisphenoid penetrates, behind it dorsal process of parasphenoid protrudes into gap between both lateral laminae and contacts them with its lateral edges.

Parietal single, elongate, 1.4 (MCP 15219) to 1.8 (MCP 8355) times as long as wide, roughly rectangular in dorsal view except for anterolateral processes; dorsal surface slightly convex, except for a slight depression longitudinally along its midline; anterolateral processes moderately long and robust, framing posterolateral borders of frontals and forming posterodorsal margins of orbits; anterior border strongly concave curved and posterior border almost straight in transverse direction; anterolateral processes diverge slightly laterally anteriorly; in dorsal view, parietal completely covers pterygoids (MCP 8355) or pterygoids partially visible laterally (MCP 15219); a weakly (MCP 15219) to moderately (MCP 8355) pronounced ridge extends dorsally on both sides of parietal from anterolateral process in posterior direction and almost reaches posterior margin of parietal, and even if both ridges slightly approach each other posteriorly, they remain clearly separated from each other; lateral to dorsal ridges, parietal slopes downwards forming a slightly concave surface in anterior region and a slightly convex surface in posterior region in lateral view; ventrally, parietal meets posterior half of parasphenoid rostrum and most of basisphenoid portion of parabasisphenoid; posterolaterally, parietal contacts anterior and dorsal margin of each prootic and forms anterior border of foramen for maxillary branch of trigeminal nerve at lateral suture with prootic; posterodorsal region of parietal forms an almost straight suture with supraoccipital.

Postorbitals absent.

Supraoccipital single, pentagonal, with straight anterior border and triangular posterior border, about twice as wide as long, slightly concave, and with anterior region slightly elevated; anteriorly it contacts parietal along a straight transverse suture, anterolaterally prootics with an slightly (MCP 15219) to strongly (MCP 8355) oblique suture, and posteriorly exoccipitals with an oblique suture; MCP 15219 has a short elongated notch anterodorsally right and left of midline, respectively, distinctly separated from supratemporals; internally, lateral borders of supraoccipital extend downwards to contribute to dorsomedial walls of otic capsules.

Prootics paired, ovaloid in lateral view, 1.2 (MCP 15219) to 1.45 (MCP 8355) times as high as long; each prootic contacts parietal anteriorly, supraoccipital dorsally, exoccipital posteriorly, parabasisphenoid complex anteroventrally, basioccipital posteroventrally, and anterior part of supratemporal on its dorsal surface; at suture with parietal, prootic forms posterior border of foramen for maxillary branch of trigeminal nerve and at suture with exoccipital it forms anterior margin of fenestra ovalis; slightly posterior and slightly below central part of prootic in lateral view a posterolaterally oriented foramen for mandibular branch of trigeminal nerve; two further foramina on lateral surface of prootic situated in between and ventral to both trigeminal nerve foramina; in dorsal view, prootic bears a depression in posterior region in which rests anterior tip of supratemporal; internally, prootic contributes to formation of anteroventral, anteromedial and anterolateral wall of otic capsule; few small foramina pierce medial laminae of each exoccipital.

Exoccipitals paired, irregularly shaped, and in medial contact along a straight suture; each has a moderately pronounced, dorsolateral ridge; anterodorsally, each exoccipital contacts supraoccipital with a straight, oblique suture, anterolaterally prootic, ventrally basioccipital and dorsolaterally, lateral to dorsal ridge, supratemporal; fenestra ovalis situated at suture between prootic and exoccipital, and exoccipital forms posterior margin of fenestra; posterior to fenestra ovalis halfway to foramen magnum a recess, bearing several foramina; internally, exoccipital contributes to formation of posteroventral, posteromedial and posterolateral wall of otic capsule; exoccipital most posteriorly projecting bone of skull roof and forms dorsal, lateral, and lateroventral border of foramen magnum, with exoccipital components of occipital condyle approaching but remaining slightly separated from each other, posterior process of basioccipital not excluded from participation in foramen magnum.

Parasphenoid and basisphenoid single and fused to form elongate parabasisphenoid, about 1.9 (MCP 15219) to 2.1 (MCP 8355) times as long as wide, and occupying most of skull floor; parabasisphenoid concave in parasphenoid region and convex in basisphenoid region; basisphenoid portion roughly rounded, parasphenoid rostrum lanceolate with a pointed anterior tip; anterior half of parasphenoid rostrum bears a dorsally oriented process, which protrudes into gap between vertical laminae of frontals, and contacts them with its lateral edges; anterior tip of parasphenoid rostrum does not surpass anterior border of frontals in ventral view; anteriormost part of dorsal process of parasphenoid rostrum contacts ventral surface of posteromedial region of nasals; parasphenoid rostrum distinctly separated from choanal process of palatine, from posterior ending of vomers, and from septomaxillae; dorsolaterally parabasisphenoid contacts frontals and parietal, and prootics posterior to it, and reaches greatest width at sutures between parietal and prootics; foramen located only on right side (both specimens) in posterolateral part of basisphenoid portion, at suture with prootic; in dorsal view (internally), parabasisphenoid pierced by some foramina in lateral region of bone.

Basioccipital single, about hexagonal, almost as wide as long, convex; contacts parabasisphenoid complex anteriorly with straight transverse suture, prootics anterolaterally with oblique sutures, and exoccipitals posterolaterally with oblique sutures; posterodorsally, basioccipital partly overlain by exoccipital components of occipital condyle; posterior end of basioccipital (part of occipital condyle), rectangular-shaped in ventral view and quadrant-shaped in posterior view; widest part of basioccipital at (MCP 15219) or slightly posterior (MCP 8355) to sutures with prootics and exoccipitals; ventral surface of basioccipital slightly elevated in anterior region; small foramen present medially in posterior region, at about where basioccipital part of occipital condyle begins.

Palatomaxillary arch osteology

Palatomaxillary arch composed of maxillae, ectopterygoids, palatines, and pterygoids ( Fig. 11 ).

Maxillae paired, elongate, account for about one-third of length of skull, about 4.5 (MCP8355) to 4.8 (MCP 15219) times as long as high, each extending from level of (MCP 8355) or shortly behind (MCP 15219) lateral process of premaxilla to posterior region of orbit, forming most of lower margin of orbit laterally; in lateral view, highest point at about mid-length of bone; anteriorly, maxillae slightly arched towards premaxilla; ventral surface of maxilla bears four tooth loci, with curved, and rear-facing anterior teeth approximately similar in size, followed posteriorly, after a small interspace, by a pair of larger and grooved fangs, situated below eye; posterior end of maxilla bears a tooth-like spur at lateral margin of ventral surface; maxilla contacts prefrontal on its dorsal surface at its highest point, anterior regions of lateral and medial processes of ectopterygoid posteriorly, and its short, knob-like palatine process contacts maxillary process of palatine (MCP 8355), or remains slightly separated from it (MCP 15219); a small, knob-like ectopterygoid process visible, but situated slightly anterior to contact zone with anterior tip of medial process of ectopterygoid.

Ectopterygoids paired, wishbone-shaped, deeply forked anteriorly, with a medial process 1.4 (MCP 8355) to 1.9 (MCP 15219) times as long as lateral process; in dorsal view, ectopterygoids either almost entirely visible (MCP 15219) or almost only lateral processes visible and rest of ectopterygoids covered by parietal (MCP 8355); anterior processes directed anterolaterally and frame posterior end of maxilla, forming a maxilo-ectopterygoid fenestra; ventral surface of flattened posterior process has facet, where it firmly contacts dorsal surface of anterolateral portion of pterygoid.

Pterygoids paired, either edentulous (MCP 15219) or with one small tooth in anterior region (MCP 8355), flattened, elongate and slender, 7.5 (MCP 15219) to 8.9 (MCP 8355) times as long as broad, corresponding to slightly less than half length of skull; not in contact with other skull bones except for firm contact with ectopterygoid; in dorsal view, pterygoids only partly (MCP 15219) visible or not visible at all (MCP 8355), completely covered by roofing skull bones; anteromedial tip of pterygoid approaching but not contacting palatine, either thumb-like (MCP 15219) or not pronounced (MCP 8355); in ventral view, lateral border of pterygoid slightly curved posterolaterally; medial borders of pterygoids nearly parallel to each other in anterior third, gradually diverging and tapering posterolaterally in posterior two-thirds, resulting in greatest distance between both pterygoids at their posterior tips; posterior end of pterygoid approaches ventromedial process of quadrate medially without touching it.

Palatines paired elongate and slender, about 6.2 (MCP 15219) to 6.3 (MCP 8355) times as long as wide, when not considering choanal and maxillary processes, and correspond to 25% (MCP 15219) to 27% (MCP 8355) of length of skull; medial edge slightly curved; ventral surface has three (MCP 8355), four (MCP 15219, left), or five (MCP 15219, right) tooth loci; teeth subequal, curved, and rear-facing; maxillary process of palatine contacts medioventral region of prefrontal on dorsal surface of its maxillary process, and palatine process of maxilla (MCP 8355), or remains slightly separated from it (MCP 15219); anterior portion of palatine, anterior to tooth line almost triangular and contacts ventrolateral part of vomer dorsally; dorsomedially, a long, thin choanal process rises and curves downwards in a semicircle, approaching but remaining separated from its counterpart medially; short, broad maxillary process situated on lateral surface of palatine at level of first tooth, directed anterolaterally; posterior part of palatine behind tooth line bifurcated, with equally long processes (MCP 15219) or slightly shorter ventrolateral process and slightly longer dorsomedial process (MCP 8355), both tapering towards posterior end.

Suspensorium and mandible osteology

Suspensorium composed of supratemporals and quadrates ( Fig. 10 ). Each mandible composed of dentary, splenial, angular, and compound bone ( Fig. 11 ).

Supratemporals laminar, elongate, more than five times as long as wide, slightly curved, and slightly oblique; in dorsal view, each supratemporal overlaps and firmly contacts more than posterior half of prootic and anterolateral part of exoccipital over well-defined facets; anteriorly approaching, but not reaching to parietal; posterolateral region approaches dorsomedial aspect of quadrate, without touching it; posterior end protrudes posteriorly slightly beyond dorsal region of quadrate, but ends before posterior end of exoccipital.

Quadrates flattened and broad dorsally, tapering dorsoventrally in lateral view, but gradually increasing in width in rear view; oriented obliquely, from anterodorsally to posteroventrally; posterodorsal part approaches posterolateral region of supratemporal medially; medial part has a short process, which corresponds to contact region with columella auris, but columella auris hardly visible; ventral part bifurcated, with medial branch broader than lateral branch and both together spanning glenoid cavity of retroarticular process of mandible; quadrate does not exceed posterior limit of skull roof.

Dentaries elongate and slender, making up about 43% (MCP 15219) to 47% (MCP 8355) of length of mandible, slightly curved anteromedially; dorsal surface bears six tooth loci; teeth subequal, curved and rear-facing; lateral face slightly convex with a mental foramen located at about level of third tooth, in anterior one-third of dentary; at (MCP 8355) or behind (MCP 15219) level of last tooth, dentary branches into a shorter dorsal process, which overlays anterior part of compound bone, and longer lanceolate ventral process; in medial view, gap between dorsal and ventral processes mainly filled by splenial; in ventral view, posteriormost part of ventral process contacts anteroventral part of angular; ventral process runs with its dorsal surface parallel and close along anterior part of medioventral region of compound bone without touching it; in medial view, dorsal process slightly bifurcated in its posteriormost region, distinctly behind last tooth, with a longer dorsolateral branch and a very short ventromedial branch.

Splenials elongate, triangular, tapered anteriorly, about 3.7 (MCP 8355) to 4 (MCP 15219) times as long as high, smallest bone of mandible, making up less than one-fifth of mandibular length; anterior mylohyoid foramen centrally positioned in posterior part of bone anterior to level of its greatest height; posterior edge of splenial firmly contacts anterior region of angular.

Angulars elongate, triangular, tapered posteriorly, almost 4.3 (MCP 8355) to 4.6 (MCP 15219) times as long as high, second smallest bone of mandible, making up a little less than one-third of mandibular length; each angular contacts splenial anteriorly, compound bone laterally and dorsally, posteriormost tip of medial process of dentary, and posteromedial surface of ventral process of dentary; posterior mylohyoid foramen centrally positioned in anterior third of bone.

Compound bones elongate and slender, about 7.3 (MCP 15219) to 8 (MCP 8355) times as long as high, largest bone of mandible, making up more than two-thirds of length of mandible; prearticular crest slightly higher than surangular crest and thus marginally visible in lateral view, the latter not visible in medial view; in lateral view, compound bone tapers anteriorly, loosely fitting between dorsal and ventral processes of dentary; an anterodorsally oriented foramen present in anterior region on lateral surface of compound bone; retroarticular process moderately long, slightly medially directed, and slightly extends (MCP 8355) or not (MCP 15219) beyond posterior end of exoccipital.

Osteological comparisons

The skull of A. albicollaris differs from that of A. assimilis ( Entiauspe-Neto et al. 2021a, characters in parentheses) in having robust thumb-like posterior processes (sharply pointed); weakly to moderately pronounced parietal ridges (well-pronounced); nasal and prefrontal in contact (not in contact); parabasisphenoid and basioccipital bones not fused (fused); anterior end of supratemporal overlaps more than posterior half of prootic and posterior end does not reach posterior end of exoccipital and is not most posteriorly protruding bone of skull roof (anterior end overlaying only posterior part of prootic and posterior end protrudes posteriorly beyond posterior end of exoccipital and is thus most posteriorly protruding bone of skull roof); 0‒1 pterygoid teeth (4); parabasisphenoid concave in parasphenoid region (straight); dentary with 6 tooth loci (7‒8).

The skull of A. albicollaris resembles that of A. ambiniger ( Entiauspe-Neto et al. 2021b, characters in parentheses) but differs from this species in having vomers medially in contact (not contacting each other medially); anterior border of parietal is strongly concave curved (anterior border is almost straight); exoccipital components of occipital condyle approaching but remaining slightly separated from each other, so that posterior process of basioccipital is not excluded from participation in foramen magnum (exoccipital components of occipital condyle are in close contact, excluding posterior process of basioccipital from participation in foramen magnum); prearticular crest is slightly higher than surangular crest of compound bone (prearticular and surangular crests are about similar in height).

It differs from that of A. cearensis ( Ferrarezzi et al. 2005, characters in parentheses) by having 0‒1 pterygoid teeth (2); prearticular crest is slightly higher than surangular crest of compound bone (same height as surangular crest); U-shaped fronto-parietal suture in dorsal view without parietal indentation between frontals (W-shaped suture, with an antero-median parietal indentation); dorsal laminae of nasal and frontals in contact (not in contact); dentary with 6 tooth loci (7‒8).

The skull of A. albicollaris differs from that of A. sanctaeritae ( Entiauspe-Neto et al. 2020a, characters in parentheses) by having dorsal laminae of nasal and frontal in contact (not in contact); nasal and prefrontal in contact (not in contact); 0‒1 pterygoid teeth (4‒5); weakly to moderately pronounced parietal ridges, both ridges slightly approach each other posteriorly, but remain clearly separated from each other (well-pronounced, both ridges merge in posterior fifth of parietal); dentary with 6 tooth loci (8‒9).

Figures

Fig. 1. Degrees of morphological variation in dorsal and ventral view, of Apostolepis Cope, 1862 from the Cerrado. A. Apostolepis albicollaris Lema, 2002, holotype from Brasília, Distrito Federal, Brazil (MCP 8355). B. Apostolepis albicollaris, specimen from Ipameri, Goiás, Brazil (IBSP 092627). C. Apostolepis cerradoensis Lema, 2003, holotype from Minaçu, Goiás, Brazil (MCP 15219). Notice the varying degrees of ventral melanism polymorphism, ranging from uniformly black, to black and cream, and uniformly cream. Photograph credits: Douglas Sebben (A, C), Rafael P. Benetti (B). Scale bars = 10 mm.

Fig. 3. Apostolepis albicollaris Lema, 2002, holotype (MCP 15219) from Minaçu, Goiás, Brazil. Head scalation. Drawings: Arthur Tiutenko.

Fig. 4. Similar red species of Apostolepis Cope, 1862. A–F. Apostolepis albicollaris Lema, 2002 in life, adult individuals from Brasília, Distrito Federal, Brazil. G–H. Apostolepis dimidiata (Jan, 1862) in life, adult individual from Laguna Blanca, San Pedro, Paraguay. I–J. Apostolepis quirogai Giraudo & Scrocchi, 1998 in life, adult individual from Misiones, Argentina. Photograph credits: Cyro de Sousa Bernardes (A, C–D), Luís Felipe Carvalho de Lima (E–F), Jean-Paul Brouard (G–H), Amado Martínez (I–J), and Gabriel Horta (B).

Fig. 5. Apostolepis albicollaris Lema, 2002, hemipenis. Sulcate and asulcate sides. Drawings: Arthur Tiutenko.

Fig. 6. Apostolepis albicollaris Lema, 2002, sexual dimorphism in morphometric (SVL, TL) and meristic (ventrals, subcaudals) characters. Outliers are indicated as circles, A. cerradoensis Lema, 2003 holotype indicated as red star.

Fig. 7. Geographic distribution of Apostolepis albicollaris Lema, 2002 in the Cerrado of Central Brazil. A. Total range, with minimum convex polygon representing extent of occurrence. B. Natural habitat remnants and land use and land cover changes (collection 4, MapBiomas 2021) within the range of A. albicollaris. C. Fire frequency between 2005 and 2015 (collection 1, MapBiomas 2021) within the range of A. albicollaris. D. Protected areas (ICMBio 2021) within the range of A. albicollaris.

Fig. 8. Consensus topology of Apostolepis Cope, 1862 BI and ML phylogenetic relationships, support given in Bootstrap (top,> 80) for maximum likelihood inference and Consensus Support (bottom,> 80) for Bayesian inference. Scale bar = molecular distance. Inset photograph: Apostolepis albicollaris Lema, 2002 by Luís Felipe Carvalho de Lima.

Fig. 9. Dorsal (A, D), lateral (B, E), and ventral (C, F) views of the skull based on μCT imagery. A–C. Apostolepis albicollaris Lema, 2002, holotype (MCP 8355). D–F. A. cerradoensis Lema, 2003, holotype (MCP 15219). Different skull elements are digitally colored and the mandible is removed for better visualization. Abbreviations: BO = basioccipital; BS = basisphenoid; ECP = ectopterygoid; EXO = exoccipital; F = frontal; MX = maxilla; NA = nasal; P = parietal; PAL = palatine; PFR = prefrontal; PMX = premaxilla; PRO = prootic; PT = pterygoid; Q = quadrate; SMX = septomaxilla; SO = supraoccipital; ST = supratemporal; V = vomer.

Fig. 10. Anterior (A, C) and posterior (B, D) views of the skull and lower jaw based on μCT imagery. A–B. Apostolepis albicollaris Lema, 2002, holotype (MCP 8355). C–D. A. cerradoensis Lema, 2003, holotype (MCP 15219). Different skull elements are digitally colored to improve visualization. Abbreviations: AN = angular; BO = basioccipital; BS = basisphenoid; CP = compound bone; D = dentary; EXO = exoccipital; F = frontal; MX = maxilla; NA = nasal; P = parietal; PAL = palatine; PFR = prefrontal; PMX = premaxilla; PRO = prootic; PT = pterygoid; Q = quadrate; SMX = septomaxilla; SO = supraoccipital; SP = splenial; ST = supratemporal.

Fig. 11. Lateral (A, E), medial (B, F), dorsal (C, G), and ventral (D, H) views of the lower jaw based on μCT imagery. A–D. Apostolepis albicollaris Lema, 2002, holotype (MCP 8355). E–H. A. cerradoensis Lema, 2003, holotype (MCP 15219). Different skull elements are digitally colored to improve visualization. Abbreviations: AN = angular; CP = compound bone; D = dentary; DPD = dorsal process of dentary; PCR = prearticular crest of compound bone; RP = retroarticular process of compound bone; SAC = surangular crest of compound bone; SP = splenial; VDP = ventral process of dentary.

Tables

Table 2. Pairwise genetic distances for the 12S gene among sequences of Apostolepis Cope, 1862 analyzed.

	1)	2)	3)	4)	5)	6)
1) A. albicollaris
2) A. rondoni	0.04
3) A. flavotorquata	0.06	0.06
4) A. dimidiata	0.01	0.04	0.06
5) A. assimilis	0.06	0.04	0.06	0.06
6) A. cearensis	0.05	0.03	0.05	0.05	0.03
7) A. sanctaeritae	0.07	0.04	0.06	0.07	0.03	0.03

Table 3. Pairwise genetic distances for the CMOS gene among sequences of Apostolepis Cope, 1862 analyzed.

	1)	2)	3)	4)	5)	6)
1) A. albicollaris
2) A. rondoni	0.01
3) A. flavotorquata	0.01	0
4) A. dimidiata	0	0	0
5) A. assimilis	0.01	0	0	0
6) A. cearensis	0.01	0	0	0	0
7) A. sanctaeritae	0.01	0.01	0.01	0	0	0