Bothrocophias tulitoi, Angarita-Sierra & Cubides-Cubillos & Hurtado-Gómez, 2022

Angarita-Sierra, Teddy, Cubides-Cubillos, Sergio Daniel & Hurtado-Gomez, Juan Pablo, 2022, Hidden in the highs: Two new species of the enigmatic toadheaded pitvipers of the genus Bothrocophias, Vertebrate Zoology 72, pp. 971-996 : 971

Bothrocophias tulitoi sp. nov.

Figs 1 , 2 , 3 , 4 , 5 , 6

Chresonymy.

Bothrocophias microphthalmus . (MLS 1632-34, 1636): Nicéforo-María (1975), Campbell and Lamar (1989): page 255, figure 230; Campbell and Lamar (2004): Volume 1, Plate 473; (MPUJ 1364): Angarita-Sierra et al (2013).

Holotype.

(Fig. 3 ) INSZ 073, an adult male from vereda Ciénaga La Valvanera, municipality of Garagoa, department of Boyacá, Colombia. Coordinates: N 5.106535941, W -73.25888414; elevation 1,894 m asl. The specimen was collected by staff of Corporación Autónoma Regional de Chivor (CORPOCHIVOR, Spanish acronym) on 17th October 2017.

Paratypes.

COLOMBIA (n =20; Fig. 4 ): Boyacá: municipality of Garagoa. Locality: unknown, IAvH-R 5742, 6392, 6396, coordinates N 5.08236, W -73.36334 (approximate to the town). Locality: vereda Ciénaga de la Valvanera, INSZ 128, 130, 134-38, 143-48, coordinates N 5.106535941, W -73.25888414. Municipality of Guateque. Locality: unknown, IAvH-R6391, coordinates N 5.006386111, W -73.47142222 (approximate to the town). Municipality of Miraflores. Locality: vereda El Tunjito, Finca San Antonio, IAvH-R6387, coordinates N 5.12216, W -73.21212. - Casanare: municipality of La Salina. Locality: unknown, MLS 1632-333, 1634, 1636, coordinates N 6.127602778, W -72.33372222 (approximate to the town). Municipality of Chámeza. Locality: vereda Centro-Norte, La Mosquera, MPUJ 1364, coordinates N 5.243917, W -72.89125; locality: vereda Centro Norte, Cerro Pan de Azúcar, IAvH-R7795, coordinates N 5.25, W -72.883333. Municipality of Yopal. Locality: corregimiento El Morro, vereda El Progreso, Highland Forest, IAvH-R8711, coordinates N 5.50775, W -72.428528. - Cundinamarca: municipality of Ubalá. Locality: unknown IAvH-R 5956, coordinates: N 4.743647222, W -73.53498889 (approximate to the town).

Diagnosis.

Bothrocophias tulitoi sp. nov. can be distinguished from all its congeners by the following combination of characters: (1) 150-172 ventral scales in females, 153-162 ventral scales in males; (2) internasal scales in contact or separated by a single small scale; (3) absence of canthorostral scales; (4) absence of lacunolabial scale; (5) one prelacunal scale; (6) hemipenial lobes subconical and ornamented toward the apex by large and dense calyces with spinulate edges; (7) bifurcation point of hemipenial lobes about 3-6 sudcaudal scales; (8) hemipenial body ornamented by numerous dense, large, and strongly calcified mesial spines arranged in oblique lines; (9) in sulcate view, lateral and mesial spines of the hemipenial body homogeneous in size; (10) body surface with less than 28 dark-brown bands dorsally and/or juxtaposed trapezoid-shaped blotches with paler centers; and (11) ventral surface of the tail uniformly bright reddish or orange-reddish speckles with black spots without a regular pattern (Figs 3 , 4 ).

Comparisons.

Bothrocophias tulitoi sp. nov. can be distinguished from all Bothrocophias species by having a creamy white or pale yellow ventral ground color with ventral scales heavily marked with black pigment towards the edges contacting the paraventral scales, and the presence of spots without a regular pattern on the mesial surface turning heavily mottled with dark brown pigment toward the tail (versus homogeneously dark brown to black in B. campbelli ; mottled heavily with dark brown pigment, with the pale interspaces between the ventrolateral blotches encroaching on the lateral edges of ventral scales in B. colombianus ; greyish brown medially, becoming paler laterally, with or without alternating dark brown spots in B. hyoprora ; yellow mottled with pale to dark brown, darker posteriorly in B. lojanus ; and pale pink to almost white in B. myersi ); ventral surface of the tail with bright reddish or orange-reddish speckles with black spots without a regular pattern, and heavily marked with dark pigment towards the base (versus proximally dark brown and distally yellow or yellow-green in B. andianus ; bright yellow to tan with diffuse grayish or brown pigment in B. campbelli ; cream or pale yellow with a sparse peppering of brown in B. colombianus ; and whitish with a moderate suffusion of grey in B. myersi ). Comparisons of meristic and hemipenial characters with all its congeners of toadheaded pitvipers are summarized in Table 4 .

Additionally, Bothrocophias tulitoi sp. nov. can be distinguished from Ecuadorian, Peruvian, and Bolivian populations of toadheaded pitvipers currently classified as B. microphthalmus by having ventral surface of tail with bright reddish or orange-reddish speckles with black spots without a regular pattern and heavily marked towards the base (versus heavily marked with black or dark brown pigment proximally, mottled medially with pale to dark brown, and pale diffuse mottling or pale with interspaces mottled distally in Bolivian and Peruvian populations). Comparisons of meristic and hemipenial characters with the Ecuadorian, Peruvian, and Bolivian populations of toadheaded pitvipers currently classified as B. microphthalmus are summarized in Table 5 . Specimens, taxonomic descriptions, and pictures of snakes classified as B. microphthalmus from the Amazonian slopes of Brazil ( Rondônia state) were not available for this study.

Description of holotype.

(Figs 3 - 5 ; Table 3 ) Male, small body size (SVL = 517 mm, TL = 96, ratio 18.5%), head and body strongly differentiated by nuchal constriction; head longer than wide (HW/HL 61.7%); snout prognathous and not upturned; absence of nasorostral and canthorostral scales; two internasal scales separated by a single small cone-shaped scale; rostral visible from dorsal view and in contact with internasals, as well as with the small cone-shaped scale; two canthal scales in broad contact with internasal scales and separating the first preocular and loreal scales in lateral view; four intercanthal scales; two supraocular scales wider than long (SW/SL = 60.9%); seven intersupraocular scales; 26 interrictal scales; two nasal scales: anterior nasal scale in broad contact with rostral, internasal, and first supralabial scale, and posterior nasal scale in contact with loreal, the first two prefoveal and subnasal scales; a single subnasal scale; two to three prefoveal scales on right and left lateral side of the head; a single prelacunal scale in broad contact with second supralabial and supralacunal scales and in narrow contact with prefoveal, sublacunal, and loreal scales; a single supralacunal scale in broad contact with first preocular scale and in narrow contact with loreal, canthal, and second preocular scales; a single sublacunal in broad contact with third supralabial and preocular scales and in narrow contact with prelacunal, surpralacunal, and second preocular scales; absence of a lacunolabial scale; a single subocular scale, five interoculolabial scales; two postocular scales; seven supralabial scales, third supralabial slightly higher and wider than fourth to seventh supralabial scales, and notably higher and wider than first and second supralabial scales; eight infralabial scales, first infralabial scales separated by mental scale and in broad contact with the first pair of gular scales, second and third infralabial scales in contact with first pair of gular scales; two pairs of gular scales; four preventral scales; dorsal scale rows 23-23-19; 153 ventral scales; anal scale single; 52 subcaudal scales; slender tail not prehensile.

Color of the holotype in life.

Ground color of the dorsal surface of the head is pale brown to brown with diffuse marks dark-brown or grey without a distinctive pattern. Ground color of the lateral surfaces of the head is scattered grey-brown from the snout to anterior edge of the eye; a conspicuous dark-brown postocular stripe running obliquely from the posterior edge of the eye to the angle formed by the quadrate and jaw bone joint encompasses the temporal scales, the last two supralabial scales, the last infralabial scale, and the mesial scales located between the preventral and infralabial scales; conspicuous tricolored ocelli in the third to fifth supralabial scales and third to seventh infralabial scales with center white or white-cream, followed by an internal edge dark-brown or black, and external broad circle or edge yellow or yellow-reddish. Ventral surfaces of the head are dark orange-gold and peppered with brown with conspicuous tricolored ocelli as described above in the first, third to seventh infralabial scales and first pair of gular scales. Ground color of the dorsal body surfaces is yellow-tan to brown mottling with dark brown-reddish pigment and weak orange speckles; 27 dark-brown bands and/or opposite or juxtaposed trapezoid-shaped blotches with pale center ornamented with or without brown spots. Ground color of body ventral surfaces is creamy white or yellow with ventral scales heavily marked with black pigment towards the edges contacting paraventral scales and spotted without a regular pattern on the mesial surface turning heavily mottled with dark brown pigment toward the tail; edges of the spots of the mesial surfaces yellow reddish turning dark brown toward the tail. Dorsal surfaces of the tail covered by nine broad dark brown bands separated by four narrow pale bands that fuse toward the distal end of the tail; tail ventral surface with bright reddish or orange-reddish speckles with black spots without a regular pattern, and heavily marked with dark pigment towards the base.

Color of the holotype in ethanol.

(Fig. 3 ) After five years in ethanol, the ground color of the dorsal surfaces of the head and body changed from pale brown or grey-brown to greyish blue. Dark brown and chocolate coloration was maintained, and surfaces with brown-reddish, yellow-reddish, or yellow coloration turned pale grey or creamish white.

Color pattern variation.

(Fig. 4 ) Adults of Bothrocophias tulitoi sp. nov. exhibit sexual dimorphism. The dorsal, lateral, and ventral surfaces of the head and body of males are melanized with conspicuously tricolored ocelli in the third to fifth supralabial scales, third to seventh infralabial scales, and first pair of gular scales, and the lateral and ventral surfaces of the head in females exhibit a homogenous creamish yellow coloration without ocelli in the labial or gular scales; some specimens exhibit weakly visible ocelli (e.g., INSZ148). Neonates and juveniles of both sexes can possess ocelli in some labials or gular scales, but only males retain them until adulthood. In addition, in neonates and juveniles, the dorsal body ground color is pale yellow, and the dorsal bands are conspicuous throughout the body (Fig. 4A ); in adults of both sexes, the dorsal ground color is yellow or tan to brown; the bands are inconspicuous in the first third of the body and become more conspicuous towards the medial and posterior body sections.

Meristic variation.

(Table 4 ) Female and male adults of Bothrocophias tulitoi sp. nov. exhibit sexual dimorphism in ventral scale counts (Table 4 ). The specimen IAVH 6396, exhibits an unusually low ventral scale count (150), which is an outlier among females in our sample. In four specimens (INSZ 134, 144-46), the supralacunal scale is fused with the third preocular scale and enters the eye orbit. On INSZ 073, the canthal scale separates the first preocular and loreal scale; in two specimens (MLS 1634, IAvH-R7795), infralabial counts are 10-11 scales; and in INSZ 130, the asymmetrical presence of a single and small canthorostral scale on one side of the head was observed. High counts of interoculolabial scales (range 9-12) were recorded in three neonates born in captivity (INSZ 128, 130, 136).

Hemipenial morphology.

(n =7, Fig. 5A-C ) Hemipenes in situ extend to the level of the 8th or 12th subcaudal scale, with the bilobation point ranging between the 3rd or 6th subcaudal scale. The everted organ is deeply bilobed; lobes are conical, bicalyculate and non-capitate; lobe crotch nude; sulcus spermaticus centrolineal and bifurcate, the branches run to the lobe tips, with the bifurcation always below the bilobation point and proximal to the midpoint of the hemipenial body; intrasulcar area densely covered with spines that increase in size distally; towards the distal half each lobe is densely ornamented with calyces; sulcus spermaticus walls robust and well defined. In sulcate view, hemipenial body covered with small spines proximally; ornamented medially by numerous dense, large, and strongly calcified mesial spines arranged in oblique rows, with lateral and mesial spines of the hemipenial body homogenous in size; and distally, the spines in each lobe replaced by dense small calyces arranged in a low-cut front centered in the sulcus spermaticus with two curved edges extending on the side, calyces are spinulated proximally but not distally. In lateral view, hemipenial body nude proximally; lobes ornamented medially by dense, large, and strongly calcified lateral spines equal in size and replaced distally by dense calyces. In asulcate view, hemipenial body nude proximally; hemipenial body ornamented medially by numerous dense, large, and strongly calcified mesial spines arranged in oblique rows which increase in size distally; and in each lobe, the spines replaced by dense calyces through an oblique cut.

Etymology.

We dedicate this species to the late Colombian educator Tulio Manuel Angarita Serrano (1941-2021, father of the first author), known as Tulito (employing the diminutive Spanish suffix “ito”) by his colleagues, friends, and relatives. The specific epithet Bothrocophias tulitoi represents the Latin translation of the nickname from the Spanish name Tulito. Professor Angarita-Serrano was a pioneer of the modern Colombian education model that helped catalyze the development of the theoretical and practical tools needed to implement institutional educational projects in Colombian public and private schools (see Angarita-Serrano 1990; Angarita-Serrano 1994; Angarita-Serrano and Chaves 1995; Angarita-Serrano 1996; Angarita-Serrano, 2000). He was also known for being a big thinker, a passionate advocate for the rights to education and free thought, and the development of educational paradigms that have helped Colombians overcome the new social, socioeconomic, and environmental challenges of the third millennium.

Distribution and natural history.

(Fig. 8 ) The known localities of Bothrocophias tulitoi sp. nov. are distributed between 1,650 and 2,700 m a.s.l. in both the central mountains and eastern slopes of the Cordillera Oriental of Colombia in the municipalities Garagoa, Gauteque, and Miraflores ( Boyacá); Chámeza, La Salina, and Yopal (Casanare); and Medina and Ubalá (Cundinamarca). Bothrocophias tulitoi sp. nov. appears to be associated with cloud montane, high Andean Forest, and subparamos and is tolerant of disturbed or transformed habitats such as livestock pastures and agricultural fields. Little is known of the natural history of B. tulitoi sp. nov. An adult female from the municipality of Garagoa, Boyacá (INSZ 144), gave birth to 15 offspring (two males and 13 females, eight of which are part of the paratype series: INSZ 128, 130, 134-36, 143, 146, 148) after 11 days in captivity at the INS serpentarium.

Envenomation.

A total of 40 snakebite events over the last decade might have been caused by B. tulitoi sp. nov. Both mild and moderate envenomation have been noted in 50% of patients, and no severe cases nor fatalities were reported. Local symptoms reported included oedema (92.5%), pain (87.5%), erythema (47.5%), ecchymosis (20%), paresthesia (17.5%), phlyctens (15%), paresthesia (17.5%), and bruises (7.5%); systemic symptoms included sickness (45%), vomiting (15%), vertigo (12.5%), bradycardia (7.5%), gingivorrhea (7.5%), muscular weakness (5%), hematuria (5%), hypotension (5%), abdominal pain (5%), and altered vision (5%).

Figures

Figure 1. Maximum likelihood tree obtained in IQ-tree based on the concatenated alignment of the two mitochondrial fragments (1616 bp), depicting the phylogenetic relationships of the genus Bothrocophias. Outgroups were removed for clarity. Values above branches indicate Ultrafast Bootstrap support of the ML tree; values below branches indicate posterior probabilities of the Bayesian tree.

Figure 2. Multidimensional scaling test of the merisitic characters between Bothrocophias tulitoi sp. nov. (cyan squares) and Bothrocophias myrringae sp. nov. (magenta dots). Vectors (black arrows) denote the discrimination capacity of each merisitic variable. A Dorsal scale count after head. B Dorsal scale count midbody. C Dorsal scale count before cloaca. D Dorsal bands. E Ventral scale counts. F Preventral scale counts. G Subcaudal scale counts. H Subnasal scales. I Presence / absence of internasal scales separated by one small scale. J Prefoveal scales. K Subfoveal scale. L Posfoveal scale. M Prelacunal scales. N Presence or absence of lacunolabial scale. O Sublacunal scales. P Supralacunal scales. Q Interoculabial scales. R Intersupraocular scales. S Cantal scales. T Intercantal scales. U Interrictial scales. V Sinsfisial scales. W Supralabial scales. X Infralabial scales. Y Preocular scale.

Figure 3. Holotype Bothrocophias tulitoi sp. nov. in preservative (INSZ 073. Male). A Dorsal view of the body. B Ventral view of the body. C Dorsal view of the head. D - E Lateral views (right / left) of the head. F Ventral view of the head. Black bar length = 1 cm.

Figure 4. Color in life of Bothrocophias tulitoi sp. nov. A, C Lateral and dorsal view of a male neonate (paratype INSZ 0128). B, D Lateral and dorsal view of an adult female (paratype INSZ 0144). All specimens from vereda Cienaga La Valvanera, municipality of Garagoa, department of Boyaca, Colombia. Coordinates: N 5.106535941, W - 73.25888414.

Figure 5. Hemipenial architecture. A, B, C Sulcate, lateral, and asulcate views of the hemipenis of the holotype of Bothrocophias tulitoi sp. nov. (INSZ 073) from vereda Cienaga La Valvanera, municipality of Garagoa, department of Boyaca, Colombia. Coordinates: N 5.106535941, W - 73.25888414; elevation 1894 m. asl. D, E, F Sulcate, lateral, and asulcate views of the hemipenis of the holotype of Bothrocophias myrringae sp. nov. (INSZ 0268) from vereda Mundo Nuevo, municipality of La Calera, department of Cundinamarca, Colombia. Coordinates: N 4.660602778, W - 73.88491667; elevation 2,761 m asl.

Figure 6. Comparison of the head pholidosis among the holotypes of Bothrocophias microphthalmus, Bothrocophias tulitoi sp. nov. and Bothrocophias myrringae sp. nov. A, B, C Dorsal, lateral, and ventral view of the head of B. microphthalmus ANSP 11515. D, E, F Dorsal, lateral, and ventral view of the head of B. tulitoi sp. nov. INSZ 073. G, H, I Dorsal, lateral, and ventral view of the head of B. myrringae sp. nov. Scales: dark green = second / third supralabial scale. yellow = lacunolabial / prelacunal. Blue = internasal scales. Fuchsia = scale separating internasal scales.

Figure 8. Color in life of Bothrocophias myrringae sp. nov., and sexual dimorphism. A, B Lateral and dorsal view of the holotype INSZ 0268. C Male exhibiting melanic coloration on dorsal body and head surfaces, as well as conspicuous tricolored ocelli on the infralabial scales (paratype INSV-SR 009). D Female exhibiting creamish-yellow to tan coloration on the dorsal body and head surfaces, without tricolored ocelli on the infralabial scales. Both C and D specimens are from vereda de Coasavista, municipality of Fomeque, Cundinamarca, coordinates N 4.495001, W - 73.852056. Pictures by Ronald A. Diaz-Flores.