A relict lineage and new species of green palm-pitviper (Squamata, Viperidae, Bothriechis) from the Chortis Highlands of Mesoamerica Author Townsend, Josiah H. Author Medina-Flores, Melissa Author Wilson, Larry David Author Jadin, Robert C. Author Austin, James D. text ZooKeys 2013 298 77 106 http://dx.doi.org/10.3897/zookeys.298.4834 journal article http://dx.doi.org/10.3897/zookeys.298.4834 1313-2970-298-77 Bothriechis guifarroi sp. n. Figs 2-3, 5-6 Bothrops nigroviridis (in part): Meyer 1969 : 420. Bothriechis marchi (in part): Campbell 1982 : 381. Bothrops marchii (in part): Wilson and Meyer 1985 : 120. Holotype. UTA R-60303 (Figs 2, 3), an adult male from La Liberacion (Fig. 4A, C), 15.5302°N , 87.2939°W (DD), 1,015 m elevation, Refugio de Vida Silvestre Texiguat , Departamento de Atlantida , Honduras, collected 25 July 2010 by the field team of E. Aguilar, A. Contreras, L. Gray, L.A. Herrera-B., M. Medina-Flores, A. Portillo, A. Stubbs, and J. H. Townsend. Original field number JHT 3243. Genbank accession numbers: 16S (KC847259), cyt b (KC847275). Paratypes (8): HONDURAS: Departamento de Atlantida : Refugio de Vida Silvestre Texiguat : adult female (USNM 579875) collected 19 June 2010, two adult females (USNM 579876-77) collected 29 July 2010, and two unsexed neonates collected 18 June 2010 (USNM 579873-74), all from Cerro El Chino (Fig. 4B), 15.5225°N , 87.2802°W (DD), 1,360-1,450 m elevation, southeast of La Liberacion . Two males (CM 156870 and MVZ 269305) collected 28 July 2010 from a ridge-top trail above La Liberacion , 15.5418°N , 87.2891°W (DD), 1,290 m elevation. One male (USNM 579878) collected 30 July 2010 from La Liberacion (Fig. 4A, C), 15.5302°N , 87.2939°W (DD), 1,015 m elevation. Referred specimens (4). HONDURAS: Departamento de Atlantida : AMNH 46949 from "Tela," collected sometime before April 1932; USNM 319942 from Quebrada de Oro, Parque Nacional Pico Bonito. Departamento de Yoro: Refugio de Vida Silvestre Texiguat : USNM 337488-89 from 2.5 airline km north-northeast of La Fortuna. See Remarks. Definition. Bothriechis guifarroi is distinguished from all nine congeners by the following combination of features: dorsal scales in 19-19-15 rows; ventrals in males 162-166 (163.8), in females 158-166 (164.0), 162-166 (164.0) in neonates; subcaudals in males 60-68 (63.0), in females 60-63 (61.0), 62-68 (65.0) in neonates; intersupraoculars (3-7); superciliary scales absent; prelacunal scale fused to second supralabial on both sides; two known color patterns in juveniles, one brown (with a pale paraventral stripe and a series of short darker dorsal blotches and a dark brown postocular stripe bordered by yellow on its lower edge) and the other green (with a series of pale blue blotches and a deep blue postocular stripe bordered by pale blue on its lower edge); dorsal coloration in adults green with pale blue trim on anterior edges of dorsal scales, and pale blue postocular stripe with green along the keels in center of stripe; and iris pale green, pale gray, or pale tan. Diagnosis . Bothriechis guifarroi can be distinguished from the other members of the genus Bothriechis as follows ( Bothriechis guifarroi features indicated first, those for species compared next): Bothriechis aurifer (distributed at moderate and intermediate elevations from extreme east-central Chiapas, Mexico, to east-central Guatemala) - adult color pattern (green vs. black-bordered yellow blotches on green background and prominent black postocular stripe) and juvenile color pattern (green with pale blue blotches or brown with pale paraventral stripe and dark dorsal blotches vs. pale lime green with black-bordered yellow blotches); Bothriechis bicolor (occurring marginally at low upward to intermediate elevations from southeastern Chiapas, Mexico, to south-central Guatemala) - number of dorsal scales at midbody (19 vs. 21) and condition of prelacunal and second supralabial scales (fused vs. separate); Bothriechis lateralis (moderate to marginally high elevations from northwestern Costa Rica to western Panama) - number of dorsal scale rows at midbody (19 vs. modal number of 23), adult color pattern (green vs. green with pale paravertebral bars and paraventral stripe), and juvenile color pattern (bi-morph pattern of green with blue dorsal blotching or brown with pale paraventral stripe and short unicolor dark blotches vs. uni-morph pattern of brown ground color with pale paraventral stripe and short bicolor dark and pale blotches); Bothriechis marchi (found marginally at low elevations up to intermediate elevations in northwestern Honduras and adjacent Guatemala) - condition of prelacunal and second supralabial scales (fused vs. separate), number of subcaudals in females (60-63 vs. 46-57); Bothriechis nigroviridis (moderate to intermediate elevations from north-central Costa Rica to west-central Panama) - adult color pattern (patternless green vs. green with very heavy black mottling), juvenile color pattern (green with pale blue blotches or brown with pale paraventral stripe and a series of short darker dorsal blotches vs. green with heavy black mottling), iris color (pale green, pale gray, or pale tan vs. almost black), numbers of ventral scales in both sexes (162-166 and 158-166 vs. 143-158 and 134-158), numbers of subcaudal in both sexes (60-68 and 60-63 vs. 49-56 and 44-58), and condition of prelacunal and second supralabial scales (fused vs. separate); Bothriechis rowleyi (moderate to intermediate elevations from extreme southeastern Oaxaca to northwestern Chiapas, Mexico) - condition of prelacunal and second supralabial scales (fused vs. almost always separate), iris color (pale green, pale gray, or pale tan vs. yellow), and juvenile color pattern (green with pale blue blotches or brown with pale paraventral stripe and a series of short darker dorsal blotches vs. pale yellowish green with brown or purple dorsal blotches); Bothriechis schlegelii (low to intermediate elevations from northwestern Chiapas, Mexico, southward through Central America and into northwestern South America as far as extreme western Venezuela and extreme northern Peru) - lack of superciliary scales in the former and their presence in the latter, number of supralabials (10-12, usually 10 vs. 7-10, usually 8), number of midbody dorsal scale rows (19 vs. 21-25, usually 23), and adult color pattern (green vs. extremely variable color and pattern involving ground color of yellow, pink, brown, gray, or green and dorsal blotching of a sizable array of colors, but sometimes absent; contrasting postocular stripe absent vs. present); Bothriechis supraciliaris (moderate to intermediate elevations from southwestern Costa Rica to west-central Panama) - lack of superciliary scales in the former and their presence in the latter, number of midbody dorsal scale rows (19 vs. 21-23, usually 23), number of ventral scales in both sexes (162-166 and 158-166 vs. 145-150 and 141-148), number of subcaudal scales in both sexes (60-68 and 60-63 vs. 48-54 and 45-52), and adult color pattern (green vs. extremely variable color and pattern involving ground color of shades of green, brown, or maroon and dorsal blotching of an array of colors contrasting with that of the ground color; contrasting postocular stripe absent vs. present); Bothriechis thalassinus (moderate to intermediate elevations from extreme eastern Guatemala and extreme northwestern El Salvador to western Honduras) - number of midbody dorsal scale rows (19 vs. 21-23, usually 21), and condition of prelacunal and second supralabial scales (fused vs. separate). Description of holotype. An adult male (Figs 2, 3) with hemipenes partially everted, left removed;rostral broader than high (4.38 x 3.26 mm); 2 internasals an teriorly ; 2/2 canthals; 4 posterior intercanthals; supraoculars slightly more than two times as long as broad; 5 intersupraoculars; many scales on head of large size, including large, flat frontal and parietal scales; interrictals 25; single loreal, longer than high, bounded by upper two preoculars, canthal above, prelacunal and prefoveals below, and nasal; prefoveals 3/3, subfoveals 1/1; prelacunal and second supralabial fused; preoculars 3/3, upper largest, middle large and in contact with supralacunal; suboculars 2/2; postoculars 2/2; supralabials 10/10; mental broader than long (4.39 x 3.29 mm); infralabials 11/11; chin shields contacting first four pairs of infralabials; gulars between chin shields and first preventral 6/4; dorsal scale rows 19-19-15; preventrals 2; ventrals 161; cloacal scute undivided; 65 undivided subcaudals; tail spine short and blunt. Figure 2. Photographs in life of the adult male holotype of Bothriechis guifarroi (UTA R-60303), with lateral and dorsal views of the head. Photographs by JHT. Figure 3. Dorsal, lateral, and ventral aspects of the head of the holotype of Bothriechis guifarroi (UTA R-60303). Photographs by RCJ. Figure 4. Habitat in the vicinity of the type locality of Bothriechis guifarroi ,La Liberacion , Refugio de Vida Silvestre Texiguat , Honduras; A riparian vegetation along the Rio Jilamito, 1,015 m elevation B small seepage pond near the top of Cerro El Chino, 1,380 m elevation C premontane rainforest with the clearing aroundLa Liberacion (1,030 m elevation) visible in the foreground. Photographs by JHT. Figure 5. Paratypes of Bothriechis guifarroi in life; A USNM 579874, green-phase juvenile B USNM 579873, brown-phase juvenile C close-up of head of USNM 579874 D close-up of head of USNM 579873 E USNM 579875, female paratype photographed in situ at Cerro El Chino, 1,420 m elevation. Photographs by JHT. Figure 6. Variation in dorsal head scales among paratypes of Bothriechis guifarroi ; A USNM 579877, adult female B MVZ 269305, adult male C USNM 579876, adult female D USNM 579875, adult female E USNM 579878, adult male F USNM 579873, neonate G USNM 579874, neonate. Photographs by JHT. Measurement of holotype. Total length 734 mm; tail length 136 mm, comprising 18.5% of total length; head 29.8 mm from front face of rostral to posterior end of mandible; head 19 mm at broadest point; neck 7 mm directly behind jaws. Hemipenis description of holotype. The partially everted left hemipenis of the holotype is described. Hemipenis at least 20 mm in total length and 13 mm in maximum width at level of crotch; on sulcate side base with several rows of small spines (<0.5 mm) followed by rows of larger spines and hooks extending for 5 mm, largest protruding ca. 3.5 mm; asulcate side with minutely spined base up to 7 mm before level of bilobation; numerous small mesial spines (<0.5 mm) arranged in rows present for 4 mm to the calyces, with peripheral section of each lobe containing nine spines and hooks (≥ 2 mm), five of which border lower rim of calyces; calyces follow spines and hooks distally; calyces scalloped, at least 10 rows at least 7 mm to apex of hemipenis on asulcate side; sulcus spermaticus deep and bifurcating ca. 4 mm before site of bilobation and extending upwards through spines and calyces likely to tip of each lobe; sulcus spermaticus bordered by two, occasionally three, columns of minute scales to the beginning of calyces, which form the border likely to the apex of the lobes. Although the majority of the hemipenial characters of this specimen are reported, the lack of a fully everted hemipenis leaves information on the total length and the nature of the calyces incomplete. Coloration of holotype in life. Middorsal scales of the holotype Yellowish Spectrum Green (Color 128), fading to Light Grass Green (Color 109) laterally and becoming Chartreuse (Color 89) ventrolaterally, with Medium Greenish Yellow (Color 88) ventral scales; dorsal body scales edged anteriorly in Light Caribbean Blue (Color 163), with up to approximately one-fourth of the anterior end of some scales edged in blue; skin concealed between dorsal scales Spectrum Violet (Color 186); postoccipital stripe Light Caribbean Blue (Color 163), with keel and adjacent portion of three scales that lie within the postoccipital stripe Light Emerald Green (Color 142); terminal portion of tail Plumbeous (Color 295); iris Pale Bluish Gray (Color 287) with fine black reticulations most heavily concentrated around the pupil. Color pattern of holotype in preservative. Scales on dorsal surfaces of the head and body blue-green, becoming more green laterally and yellow-green to yellow ventrally. Tail is mostly green with some grayish blue-green at the dorsal base. Pupil is cloudy and pale, surrounded by lime green iris heavily speckled with black. Variation in paratypes. We discuss scutellational variation in the three adult male paratypes first, the three adult females next, and finally the two unsexed neonates. Scutellation varies as follows (range followed by mean): ventrals (162-166 [164.3], 158-166 [161.7], 162 and 166); subcaudals (60-68 [64.0], 60-63 [61.0], 62 and 68); ventrals + subcaudals (222-233 [228.3], 221-226 [222.7], 228 and 230); cloacal scute entire in all specimens; dorsal scale row formula 19-19-15, with the reduction to 15 rows occurring at ventrals 114-162; supralabials (10-11 [10.2], 10-11 [10.2], 10-10 and 12-11); infralabials (10-12 [11.0], 10-13 [11.7], 11-11 and 12-11); preoculars 2-2 in all specimens, except 3-3 in CM 156870; postoculars 2-2 in all specimens, except 3-2 in MVZ 269305 and 4-4 in CM 156870; suboculars 2-3 [2.5], 2-3 [2.7], 2-2 and 3-4; relative tail length (0.184-0.223 [0.199], 0. 167-0.182 [0.176], 0.179 and 0.194). Two juvenile color patterns are present in this species (Fig. 5), one we refer to as a "green phase", the other as a "brown phase." Both juvenile phases have distinctively colored tail-tips, presumably used in caudal luring, and well-differentiated postocular stripes. The green phase (USNM 579874) has a Chartreuse (Color 89) dorsal ground color with Light Turquoise Green (Color 146) edging on the dorsal scales as well as on a series of irregular middorsal blotches, a Pale Green (Color 99) venter, and a Chartreuse (Color 89) head with a Jet Black (Color 300) postocular stripe, bordered above and below by Light Turquoise Green (Color 146); tip of tail Cobalt Blue (Color 180); the iris is Pale Neutral Gray (Color 296) with fine darker reticulations. The brown phase (USNM 579873) has a Robin Rufous (Color 29) ground color middorsally and anteriorly, becoming Salmon Color (Color 58) laterally and posteriorly, with a series of irregular Ferrunginous (Color 35) middorsal blotches, a Pale Buff (Color 1) ventral surface of head and venter becoming gradually darker (Pale Pinkish Buff [Color 3]) posteriorly, a Dark Salmon Color (Color 59) head with a Chestnut (Color 30) postocular stripe, bordered above and below by Light Buff (Color 2); tip of tail Sepia (Color 286); a Pale Buff (Color 1) paraventral stripe is present on the lower half of the first dorsal scale row and the lateral edge of the ventrals; dark speckling along lateral edge of the ventrals; the iris is Chamois (Color 84) with fine darker reticulations. The type series of Bothriechis guifarroi demonstrates considerable variation in the condition and shape of the scales on the dorsal surface of the head (Fig. 6), a characteristic often considered diagnostic among Bothriechis ( Campbell and Smith 2000 , McCranie 2011a ). Two adult females (USNM 579875 [Fig. 6C] and USNM 579877 [Fig. 6A]), one adult male (MVZ 269305 [Fig. 6B]), and one neonate (USNM 579873 [Fig. 6F]) all have multiple enlarged, unkeeled, plate-like scales present anterior to the posteriormost edge of the orbits; one adult female ([Fig. 6D]), one adult male ([Fig. 6E]), and one neonate (Fig. 6G) all have smaller keeled scales present anterior to the posteriormost edge of the orbits. As a result of demonstrating essentially the full range of dorsal head scale conditions in the type series, we do not consider this characteristic to be of value in diagnosing Bothriechis guifarroi from other congeners. Etymology. The specific name guifarroi is a patronym used to honor our colleague and friend, Honduran environmental leader Mario Guifarro of Olancho. Don Mario fearlessly led grassroots efforts to stop illegal logging in the indigenous Tawahka territory of eastern Honduras, despite repeated assassination attempts and threats on his own life and those of his compatriots. Don Mario was murdered on 15 September 2007, ironically Honduras' Independence Day, while leading a mission to demarcate the boundaries of the Tawahka-Asangni Biosphere and stave off further illegal deforestation. On 21 July 2008, the only witness to Mario's assassination, his son Shamir Guifarro Ramirez , was also murdered, along with Mario's father-in-law, Henry Arturo Chacon , and mother-in-law, Nelda Ochoa, after they were followed out of the city of Juticalpa by unknown assailants. Distribution. Populations genetically confirmed to represent Bothriechis guifarroi are found between 1,015-1,450 m elevation in the western portion of the Cordillera Nombre de Dios, Department of Atlantida , Honduras, within the boundaries of Refugio de Vida Silvestre Texiguat (Fig. 7). These localities lie within the Premontane Wet Forest and peripherally in the Lower Montane Wet Forest formations of Holdridge (1967 ; as applied by McCranie and Wilson 2002 ). Figure 7. Geographic distribution of selected Bothriechis species and populations discussed in the text; localities are based on data published herein and those of Campbell and Lamar (2004) , McCranie (2011a) , and Savage (2002) ; red diamond = type locality of Bothriechis guifarroi in Refugio de Vida Silvestre Texiguat ; black diamond = referred population of Bothriechis guifarroi from Parque Nacional Pico Bonito; circles = Bothriechis sp. inquirenda populations for the Sierra de Sulaco; squares = Bothriechis marchi ; triangles = Bothriechis thalassinus , inverted triangles = Bothriechis lateralis . Natural history. The holotype was found coiled at 2130h approximately 2.5 m above the ground among old leaf sheaths in the crown of a medium-sized understory palm in gallery forest alongside the Rio Jilamito (Fig. 4A). Anurans of the genera Duellmanohyla and Ptychohyla were abundant in the immediate vicinity of the holotype. Two adult males (CM 156870 and MVZ 269305) were collected along a ridge on the north side of La Liberacion on the night of 28 July 2010. CM 156870 was active on a small tree from 0.5-1.5 m above the ground; the second snake (MVZ 269305) was sitting coiled on the ground at the edge of the trail, and attempted to escape by crawling across the path when we approached. In the immediate vicinity of these snakes were numerous Craugastor rostralis active on the ground and Bolitoglossa sp. active on low vegetation. Two neonates were collected on the same night (2100-2200 h) on 18 June 2010, and an adult female (USNM 579875) was collected the next night, in an area of elfin forest at 1,380 m on the ridge called Cerro El Chino (Fig. 4B) above the remote ranch locality La Liberacion (at 1,030 m). The brown-phase neonate (USNM 579873) was found atop a large, similarly-colored dead palm frond, while the green-phase neonate (USNM 579874) was sitting in essentially the same ambush position as USNM 579873, but on top of a living green frond. Amphibian species collected in the immediate vicinity of Bothriechis guifarroi include Bolitoglossa sp., Nototriton sp., Craugastor rostralis , Plectrohyla chrysopleura , and Ptychohyla spinipollex . Twelve Bolitoglossa sp. were encountered the same night as the two neonates, all while active on or around dead and living palm fronds in the immediate vicinity of the neonates. Remarks. Townsend et al. (2012 : 107) included a photograph of the holotype of Bothriechis guifarroi as " Bothriechis marchi ." Bothriechis guifarroi is typically distinguished from Bothriechis marchi by having the prelacunal scale fused to the second supralabial; however, one male paratype of Bothriechis guifarroi (CM 156870) has the right prelacunal separated from the second supralabial (they are fused on the left side). Also, one specimen of Bothriechis marchi (MCZ R-33335) from the "mountains west of San Pedro Sula" also has fused prelacunals and second supralabials on both sides, and another specimen (MCZ R-32030) from "La Cumbre" has the left prelacunal separated from the second supralabial (with them fused on the right side). We tentatively refer four additional specimens to Bothriechis guifarroi : two from a locality on the leeward side of Refugio de Vida Silvestre Texiguat (USNM 337488-89, from 2.5 airline km NNE of La Fortuna, Dept. Yoro, 1,550 m elevation), one from the central portion of the Cordillera Nombre de Dios (USNM 319942, from Quebrada de Oro in Parque Nacional Pico Bonito, Dept. Atlantida , 1,090 m elevation), and one from "Tela" (AMNH 46949). All four specimens also have fused prelacunals and second supralabials on both sides. USNM 319942 was collected as a juvenile and raised in captivity ( Wilson and McCranie 1992 ; McCranie 2011a ), and exhibited a similar juvenile color pattern as USNM 579873 before undergoing an ontogenetic shift in coloration to the bright green pattern exhibited by the type series of Bothriechis guifarroi . Campbell and Lamar (2004 : plates 385-386) also provided illustrations of juvenile Bothriechis marchi s. l. that demonstrated two color morphs similar to those exhibited by Bothriechis guifarroi ; however these two individuals were captive born in the Houston Zoo and known only from "Honduras." AMNH 46949 was collected sometime during or before 1932 by Douglas March of the Lancetilla Serpentarium, just outside of the seaside city of Tela. While the "Tela" locality is considered erroneous ( Wilson and McCranie 1992 ), it is possible that AMNH 46949 was obtained from somewhere in the nearby western portion of the Cordillera Nombre de Dios. Given that at least some highland taxa found at both RVS Texiguat and Parque Nacional Pico Bonito are endemic sister species (e.g., Oedipina gephyra and Oedipina petiola ; McCranie and Townsend 2011 ), we refer USNM 319942 to Bothriechis guifarroi with the understanding that phylogenetic evaluation of the Pico Bonito population might eventually show those animals to represent a distinct taxon.