Bothrops nigroadspersus Teleuraspis nigroadspersus Systematic revision of the Eyelash Palm-Pitviper Bothriechis schlegelii (Serpentes, Viperidae), with the description of five new species and revalidation of three 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. Evolutionary Systematics 2024 2024-02-08 8 1 15 64 FF4665A6-39F0-5CFB-9335-4EAB607B67BA (Steindachner, 1870) Steindachner 1870 Viperidae Bothriechis treatment-meta Animalia Bothriechis nigroadspersus Squamata 0 15 species nigroadspersus   Figs 4 , 5 , 8   Bothrops nigroadspersusSteindachner, 1870: 348. Holotype NMW 18811 (Fig. 4), an adult female from Central America.  Teleuraspis nigroadspersusGarman, 1884: 108.  Referred specimens. All labeled  Bothriechis nigroadspersusin Suppl. material 1.  Proposed standard English names. Central American Eyelash-Pitviper  Spanish names.  Bocaraca, toboba de pestanas, viborade pestanas, oropel (yellow morph).  Diagnosis.   Bothriechis nigroadspersusis 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 nigroadspersusis 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. nigroadspersushave either opposing kidney shaped reddish dorsal marks o are of the golden morph (=oropel) (Fig. 5).  Bothriechis nigroadspersusdiffers from  B. supraciliarisby 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 nigroadspersusdiffers from  B. torvusby 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).   Figure 8.Hemipenial architecture of  Bothriechis nigroadspersusin sulcate, lateral, and asulcate views. a.UTA R-32143 from Limonprovince, Costa Rica; b.UTA R-12957 from Aldea Vista Hermosa, Izabal department, Guatemala. Photos by Eric N. Smith.  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 xlonger 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 nigroadspersusis an arboreal snake that inhabits evergreen lowland/foothill forests, plantations, and rural gardens. In Panama ( Sorrell 2007, 2009) and Costa Rica (  Solorzano2004) 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. nigroadspersusis primarily nocturnal. During the day, most individuals of  B. nigroadspersusremain 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-Amoros(2015), Morgan and Barrio-Amoros(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 Cocle, Panama is preserved with an  Artibeus jamaicensisin 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-Amorosnear 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  Chavarriaand Barrio-Amoros(2014)provide accounts of predation on this viper by hawks (  Buteogallus urubitingaand  Herpetotheres cachinnans) and snakes (  Clelia clelia).  Solorzano(2004)suggests that in Costa Rica, breeding in  Bothriechis nigroadspersuscoincides 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. nigroadspersusfrom Honduras and  Gomezet 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),  Gomezet 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. nigroadspersushave 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(  Bolanos1984). Mekbel and Cespedes(1963)report that four of a series of 27 autopsied snakebite cases in San Josewere caused by this species. Savage (2002)observed that between 90 and 100 bites by  B. nigroadspersusare 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. nigroadspersusfrom Costa Rica and found that its properties differ drastically from specimens of  Bothriechis torvusfrom Vegachi, Antioquia. When compared to the latter, the venom of  B. nigroadspersuswas found to be more edematous, hemorrhagic, and lethal. LD50 estimated as 1.7-5.6 mg/kg in  B. nigroadspersusvs 9.24 mg/kg in  B. torvus(  Bolanos1972; Gutiérrez and Chaves 1980; Lomonte et al. 2008, 2012; Prezotto-Neto et al. 2016).  Distribution.   Bothriechis nigroadspersusis 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. nigroadspersusoverlaps with that of  B. supraciliaris. Although sympatry has not been reported, we bring attention to a photographic record of an individual of  B. nigroadspersusfrom 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. nigroadspersusoverlaps with that of  B. torvus, and we found evidence of sympatry between the two species in Cordillera de Pirre, Darienprovince, Panama. MHCH 1664 is a  B. nigroadspersusand MVUP 1384 is a  B. torvus; both from the same mountain range.  Etymology. The specific epithet nigroadspersuscomes 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 nigroadspersusto 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. nigroadspersushave 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).