Bothriechis nigroadspersus (Steindachner, 1870)

Arteaga, Alejandro, Pyron, R. Alexander, Batista, Abel, Vieira, Jose, Meneses Pelayo, Elson, Smith, Eric N., Barrio Amoros, Cesar L., Koch, Claudia, Agne, Stefanie, Valencia, Jorge H., Bustamante, Lucas & Harris, Kyle J., 2024, Systematic revision of the Eyelash Palm-Pitviper Bothriechis schlegelii (Serpentes, Viperidae), with the description of five new species and revalidation of three, Evolutionary Systematics 8 (1), pp. 15-64 : 15

Bothriechis nigroadspersus (Steindachner, 1870)

Figs 4 , 5 , 8

Bothrops nigroadspersus Steindachner, 1870: 348. Holotype NMW 18811 (Fig. 4 ), an adult female from Central America.

Teleuraspis nigroadspersus Garman, 1884: 108.

Referred specimens.

All labeled Bothriechis nigroadspersus in Suppl. material 1.

Proposed standard English names.

Central American Eyelash-Pitviper

Spanish names.

Bocaracá, toboba de pestañas, víbora de pestañas, oropel (yellow morph).

Diagnosis.

Bothriechis nigroadspersus is diagnosed based on the following combination of characters: (1) two raised and spinelike supraciliary scales; (2) anterior dorsal head scales keeled; (3) gular scales much smaller than chinshields; (4) 7-24 interoculolabials; (5) 2-6 canthals which may be nearly flat or with raised triangular projections; (6) loreal not in contact with preocular; (7) yellow morph present and common in some areas; (8) dorsal bands absent; (9) opposing kidney shaped dorsal marks present in the majority of individuals; (10) black speckles on dorsal scales usually absent; (11) black speckling on ventral surfaces usually absent or brown and faint; (12) ventral surfaces entirely white in some individuals; (13) iris pale straw yellow to golden with black reticulations or spots; (14) 21-25 dorsal scale rows at mid-body; (15) 153-169 ventrals in males, 148-167 in females; (16) maximum total length in males 626 mm, in females 916 mm.

Comparisons.

Bothriechis nigroadspersus is compared to other species of the genus previously subsumed under B. schlegelii sensu lato (differences summarized in Table 2 ). It differs from all of them by having a higher number of ventral scales in both males and females (although there is overlap with some species), two raised and spinelike supraciliary scales (vs low and granular or broad and triangular in the other species), and by lacking dorsal bands. Instead, most individuals of B. nigroadspersus have either opposing kidney shaped reddish dorsal marks o are of the golden morph (=oropel) (Fig. 5 ). Bothriechis nigroadspersus differs from B. supraciliaris by having a higher number of ventral scales, no broad blotches or dorsal bands, and a different pattern on the dorsal aspect of the snout. Bothriechis nigroadspersus differs from B. torvus by having opposing kidney-shape dorsal marks, a higher number of ventrals, loreal not in contact with preocular, and comparatively smaller spines on the hemipenial body (Fig. 8 ).

Description of holotype.

An adult female, SVL 532 mm, tail length 96 mm (18.1% SVL); head length 34.4 mm (6.5% SVL) from tip of snout to angle of jaw; head width 28.5 mm (82.9% head length) taken at broadest point; rostral broader than high; nasal not entirely divided, but fused with first supralabial; loreal about 1/2 size of pit, in contact with nasal, canthals, 1 suprafoveal, 2 prefoveals, prelacunal, and supralacunal; prefoveals 4; subfoveals 3/3; postfoveals 0; prelacunal fused with second supralabial; sublacunals 1/1; supralacunal elongated and in contact with orbit; preoculars 1/1 (2/2 if supralacunal is considered a preocular); suboculars 1; postoculars 2; loreal pit large, directed anteriorly, located slightly below line drawn from center of eye to naris; supralabials 9 (including lacunolabial); infralabials 12, first pair meet posteriorly; mental broader than long; 1 pair of chin shields; 5 pairs of gulars between chin shields and preventrals; preventrals 3; anterior internasals 3; canthals 3/3; 2/2 moderately triangular but low supraciliary scales; supraoculars kidney-shaped, 2.2 × longer than wide; intersupraoculars 5; anterior dorsal head scales keeled; posterior head scales keeled; dorsal scale rows at mid-body 23; ventrals 160; cloacal plate entire; 55 undivided subcaudals; tail prehensile.

Hemipenial morphology.

(n = 2, Fig. 8 ) Everted and inflated, the organ is deeply bilobed, unicalyculate and slightly capitate; hemipenial lobes thick and cylindrical; in sulcate and asulcate views, lobe crotch ornamented with scattered spinules; sulcus spermaticus centrolineal, bifurcate and with walls weakly defined, bifurcation occurs below bilobation point and proximal to the base of the hemipenial body; sulcus spermaticus branch runs to lobe tips; distal one third of each hemipenal lobe ornamented with calyces with spinulate edges. In sulcate view, hemipenial body surface nude, but with a pair of enlarged and strongly calcified lateral spines (basal hooks), one on each side; each hemipenial lobe ornamented with 1-3 mesial spines and 5-7 lateral spines, all about a third of the size of the basal hooks; the spines in each lobe are replaced distally by calyces with spinulate edges. In lateral view, hemipenial body nude with the exception of two basal spines; lobes also largely nude but with 5-6 smaller spines that are replaced distally by calyces. In asulcate view, the hemipenial body is nude with the exception of the pair of large lateral spines and also a pair of smaller mesial spines; hemipenial lobes largely nude but ornamented with smaller spines that decrease in size towards the lobe crotch.

Natural history.

Bothriechis nigroadspersus is an arboreal snake that inhabits evergreen lowland/foothill forests, plantations, and rural gardens. In Panama ( Sorrell 2007, 2009) and Costa Rica ( Solórzano 2004) these vipers were found to be mostly active at night or at dusk and on the base of tree or on low shrubby vegetation, and Leenders (2019) and Witold Lapinski (pers. comm. to AA) reports that they have been found in the canopy at heights of 32-35 m in Costa Rica. Sorrell (2007, 2009) observed that some snakes reside in the same perch for up to 14 days, 70.2% of individuals relocated each night, and only 6.4% remained at the same daytime perch site for more than two days. According to Rand and Myers (1990), Seifert (1983), Savage (2002), and our own observations, B. nigroadspersus is primarily nocturnal. During the day, most individuals of B. nigroadspersus remain in hunting posture on or close to their night perches, but others hide inside bromeliads, or occasionally remain active and move at ground level or on vegetation. Sorrell (2009) showed that members of this species are primarily ambush predators, but they also forage actively in search for food. In a study by Antonio (1980), captive juveniles fed mostly on frogs and attracted them by means of moving their bright yellow tails as a lure. Campbell and Lamar (2004), Sorrell (2009), Barrio-Amorós (2015), Morgan and Barrio-Amorós (2015), and Entiauspe-Neto et al. (2021) provide details on the dietary preference of adults encountered in the wild. These authors found that this age category also feeds on frogs (primarily treefrogs and rainfrogs), but also on lizards (anoles, whiptails, and geckos), birds (including hummingbirds), and mammals (bats, mice, and mouse opossums). We report on additional specimens found feeding on bats: CH 5651 from Coclé, Panama is preserved with an Artibeus jamaicensis in its mouth. An uncollected specimen photographed by Philipp Hoenle in Chiapas, Mexico was feeding on an unidentified bat, as well as it was another uncollected individual found by Barrio-Amorós near Arenal, Costa Rica, on the ground on a dirt road feeding on a bat, with only one wing out of its mouth. Gerhardt et al. (1993), Laurencio (2005), and Chavarría and Barrio-Amorós (2014) provide accounts of predation on this viper by hawks ( Buteogallus urubitinga and Herpetotheres cachinnans ) and snakes ( Clelia clelia ). Solórzano (2004) suggests that in Costa Rica, breeding in Bothriechis nigroadspersus coincides with the rainy season. Blody (1983) observed that females become sexually mature at an age of less than three years and can produce more than one litter per year. Antonio (1980) described the courtship and copulatory behavior of captive B. nigroadspersus from Honduras and Gómez et al. (2015) recorded a case of a female from Costa Rica that produced a litter after presumably storing sperm for no less than ~35 months (slightly under three years). A specimen from Lago Yojoa, Honduras, kept at Centro El Ocotal, produced a litter of four eggs and one live young after being kept in a terrarium without a male for 18 years (Alejandro Velasquez pers. comm. to AB). Antonio (1980), Blody (1983), Gómez et al. (2015), and Murphy and Mitchell (1984) report a gestation period of 150-166 days (~5 months) and litters of 6-23 neonates that measure 16-22.5 cm in total length at birth. Campbell and Lamar (2004) report that captive B. nigroadspersus have lived up to 20 years.

Venom.

In a series of 477 snakebite cases in Costa Rica in 1979, 18.9% were caused by Bothriechis nigroadspersus ( Bolaños 1984). Mekbel and Céspedes (1963) report that four of a series of 27 autopsied snakebite cases in San José were caused by this species. Savage (2002) observed that between 90 and 100 bites by B. nigroadspersus are reported in Costa Rica in a typical year, with 3-6 resulting in deaths according to Seifert (1983). An average bite results in the injection of ~0.5 cc of venom. The venom is hemotoxic and strongly myonecrotic when compared to other Central American vipers (Gutiérrez and Chaves 1980). In humans, it causes intense localized pain, progressive hemorrhagic edema, and, in some cases, hemorrhagic blisters or hives, ecchymoses, and necrosis ( Lomonte et al. 2008; Pla et al. 2017). Prezotto-Neto et al. (2016) studied the composition of the venom of specimens of B. nigroadspersus from Costa Rica and found that its properties differ drastically from specimens of Bothriechis torvus from Vegachi, Antioquia. When compared to the latter, the venom of B. nigroadspersus was found to be more edematous, hemorrhagic, and lethal. LD50 estimated as 1.7-5.6 mg/kg in B. nigroadspersus vs 9.24 mg/kg in B. torvus ( Bolaños 1972; Gutiérrez and Chaves 1980; Lomonte et al. 2008, 2012; Prezotto-Neto et al. 2016).

Distribution.

Bothriechis nigroadspersus is known from at least 335 localities (listed in Suppl. material 3) throughout much of the Mesoamerican biome, from the isthmus of Tehuantepec in Mexico to extreme northwestern Colombia (Cerro Tacarcuna) along the Panamanian border. The species occurs over an estimated 352,139 km2 area and has been recorded at elevations 0-1,434 m above sea level (Fig. 3 ). Approximately 1.0% of the predicted area of distribution of B. nigroadspersus overlaps with that of B. supraciliaris . Although sympatry has not been reported, we bring attention to a photographic record of an individual of B. nigroadspersus from the vicinity of San Pedro, Puntarenas province, just 4 km away from a record of B. supraciliaris (Photo by Ethyn Maki on iNaturalist; Suppl. material 3). An estimated 1.0% of the predicted area of distribution of B. nigroadspersus overlaps with that of B. torvus , and we found evidence of sympatry between the two species in Cordillera de Pirré, Darién province, Panama. MHCH 1664 is a B. nigroadspersus and MVUP 1384 is a B. torvus ; both from the same mountain range.

Etymology.

The specific epithet nigroadspersus comes from the Latin words nigrum (meaning “black”) and adspersus (meaning “sprinkled”). It refers to the minute black specks scattered throughout the dorsum of the holotype (Fig. 4 ).

Conservation status.

We consider Bothriechis nigroadspersus to be included in the Least Concern category following IUCN Red List criteria ( IUCN 2012) because the species is widely distributed (but see Discussion), present in dozens of protected areas, tolerates moderate habitat degradation, and is presumably not declining fast enough to qualify in a threatened category. In a rainforest locality in Panama, the occurrence rates of B. nigroadspersus have increased by a factor of ten in the period from 2006 to 2012 ( Zipkin et al. 2020). In another locality in Panama, the species was found to be extremely common in forest islands within a matrix of pastures ( Sorrell 2007). However, it is unsure whether such "forest islands" will sustain the species without the presence of a dense population nearby that may act as a source of individuals that can immigrate to the fragmented habitat ( Sorrell 2007).

Figures

Figure 3. Distribution of species of Bothriechis previously subsumed under B. schlegelii sensu lato. Each colored area is a geographic representation of the suitable environmental conditions for one of the clades recovered in the phylogeny of Fig. 2. Lime green shade in southeastern Panama represents overlap between between B. nigroadspersus and B. torvus.

Figure 4. Adult female holotype of Bothriechis nigroadspersus NMW 18811 in a. Dorsal and b. Ventral view. Photos by Alice Schumacher.

Figure 5. Photographs of some specimens of Bothriechis nigroadspersus in life. a. Adult female from a private collection in Costa Rica; b. MHCH 3269 adult from Guabito, Bocas del Toro province, Panama; c. Subadult from Parque Nacional Gandoca Manzanillo, Limon province, Costa Rica; d. Adult from a private collection in Costa Rica; e, f. Juveniles from Parque Nacional Gandoca Manzanillo, Limon province, Costa Rica; g. MHCH 3268 adult female from Porton, Chiriqui province, Panama; h. MHCH 3266 adult female from Chucanti Reserve, Darien province, Panama; i. Subadult from Parque Nacional Gandoca Manzanillo, Limon province, Costa Rica; j. Adult female from a private collection in Costa Rica; k. FP 001 from Cerro Gaital, Cocle province, Panama; l. MHCH 3267 juvenile male from Chucanti Reserve, Darien province, Panama. Photos by Jose Vieira.

Figure 8. Hemipenial architecture of Bothriechis nigroadspersus in sulcate, lateral, and asulcate views. a. UTA R- 32143 from Limon province, Costa Rica; b. UTA R- 12957 from Aldea Vista Hermosa, Izabal department, Guatemala. Photos by Eric N. Smith.