Bolitoglossa jugivagans, Hertz, Andreas, Lotzkat, Sebastian & Köhler, Gunther, 2013

Hertz, Andreas, Lotzkat, Sebastian & Köhler, Gunther, 2013, A new species of Bolitoglossa (Caudata, Plethodontidae) from the continental divide of western Panama, Zootaxa 3636 (3), pp. 463-475 : 465-471

Bolitoglossa jugivagans sp. nov.

Continental Divide Salamander Figures 4–7

Holotype. SMF 94467 (original field number AH 314), an adult female from the headwaters of Río Chiriquí Malí, approximately 5 km N of the La Fortuna dam reservoir (8.7890°N, 82.2154°W, 1060 m), Bosque Protector Palo Seco, Comarca Ngöbe-Buglé (formerly province of Bocas del Toro), Panama ( Fig. 1 ); collected by Andreas Hertz and Sebastian Lotzkat on 28 October 2009.

Diagnosis. We assign the new species to Bolitoglossa because it has fewer than 14 costal grooves and lacks a sublingual fold (Savage 2002), and to the subgenus Eladinea based on mtDNA sequence data. It differs from all described species by the following combination of characters: Bolitoglossa jugivagans is a small species with short legs and a long tail. The hands and feet are moderately webbed, with the two terminal phalanges of the longest digits free of webbing. The prehensile tail is considerably longer than the body. Both maxillary and vomerine tooth counts are comparatively high in relation to SVL.

Bolitoglossa jugivagans is well differentiated from all described species of the subgenus Eladinea by 16S mtDNA distances ( Fig. 2 ; Table 1 ). It is further distinguished morphologically by the following characters (condition for B. jugivagans in parentheses): It differs from B. biseriata Tanner, B. bramei Wake, Savage, and Hanken, B. colonnea (Dunn) , B. lignicolor , B. minutula Wake, Brame, and Duellman, B. schizodactyla Wake and Brame, and B. epimela Wake and Brame by its less extensively webbed hands and feet. All these species have fully webbed hands and feet, or at least less than two phalanges free of webbing (slightly more than two phalanges free of webbing). Bolitoglossa jugivagans is easily distinguishable by coloration (described below in coloration section) from the large, almost entirely black species B. anthracina Brame, Savage , Wake, and Hanken, B. compacta Wake, Brame, and Duellman, B. copia Wake, Hanken, and Ibañez, B. magnifica Hanken , Wake, and Savage, B. nigrescens (Taylor) , B. robusta (Cope) , and B. sombra Hanken , Wake, and Savage. It can be differentiated from other small salamanders with high tooth counts from the Talamancan Mountains as follows: Bolitoglossa pygmaea Bolaños and Wake is almost unpigmented and has a short tail that never exceeds SVL ( B. jugivagans has a normal reddishbrown pigmentation and the tail is much longer than SVL). Bolitoglossa gracilis Bolaños and Robinson is bright yellowish to golden tan with dark streaks and spots (reddish-brown with light streaks), has longer legs with a limb interval of 3 to 3.5 (4) and fewer vomerine teeth VT: 10–22 (27; see also Fig. 3 ). Bolitoglossa pesrubra Taylor , with which the new species shares high vomerine and maxillary tooth counts, has longer legs with a limb interval of 0 to 3 folds (4) and a shorter tail TL/SVL≈1 (TL/SVL=1.24). Bolitoglossa subpalmata (Boulenger) has fewer maxillary and vomerine teeth at the same size ( Fig. 3 ) and a limb interval of 1 to 3 (4). Bolitoglossa gomezi Wake, Savage, and Hanken has a shorter tail TL/SVL: 1.15–1.19 in females (1.24), limb interval of 1.5–3 (4), and fewer maxillary and vomerine teeth at a comparable SVL ( Fig. 3 ). Bolitoglossa kamuk Boza-Oviedo, Rovito, Chaves, García-Rodríguez, Artavia, Bolaños , and Wake has a dark ground coloration with golden flecking on the posterior part of the body and the tail (reddish-brown with light streaks), as well as fewer maxillary and vomerine teeth MT: 34 (51), VT: 13–16 (27), and a shorter tail TL/SVL≈1 (TL/SVL=1.24). Bolitoglossa splendida Boza-Oviedo, Rovito, Chaves, García-Rodríguez, Artavia, Bolaños , and Wake is peculiarly colored with a bright-red dorsal band and bright-yellow spots laterally and ventrolaterally on jet black ground coloration (reddish-brown with light streaks), has only 18 vomerine teeth at a SVL of 47.8 mm (27 at SVL= 31.2 mm), has more webbing on feet that extends to between first and second phalangeal articulations of longest digits (two terminal phalanges free on the longest digits), and a broader head HW/SVL=0.17 (HW/SVL=0.14).

Based on molecular data, Bolitoglossa jugivagans is most closely related to B. robinsoni and B. aureogularis . Both differ from B. jugivagans by the following morphological characters (condition for B. jugivagans in parentheses): Bolitoglossa robinsoni is a large and stout species with a broad head HW/SVL=0.16–0.17 (0.14) and a tail that is shorter than the standard length TL/SVL≤1 (TL/SVL=1.24). The second species B. aureogularis is superficially very similar to B. jugivagans , primarily in dorsal coloration. However, B. aureogularis has fewer maxillary and vomerine teeth at a comparable size ( Fig. 3 ) and much shorter legs with a limb interval of 6.5 in females and 5 in males (4 in the female holotype of B. jugivagans ). Bolitoglossa aureogularis differs most markedly from B. jugivagans in ventral coloration, having a bright yellow gular region and a prominent midventral dark stripe on dirty white ground (gular region mustard yellow; ventral coloration of body grey to brownish speckled with blue, no conspicuous dark midvental stripe).

Description of the holotype. This is a small and slender Bolitoglossa . The holotype is an adult female of 31.2 mm SVL; tail long and prehensile, TL/SVL is 1.24; head short (HL about 21 % of SVL) and narrow (HW slightly less than 14 % of SVL); hands and feet narrow (HAW = 7 %, HFW = 9 % of SVL), and limbs short (HLL about 20 % of SVL, limb interval 4 costal folds between adpressed limbs); webbing moderate with the two terminal phalanges free on the longest digits ( Fig. 4 ); order of increasing length of digits I-IV-II-III in hands, and I-V-II-IV- III in feet; subterminal pads present on longest digits; small eyes that do only slightly protrude beyond lateral margins of head in ventral view; labial protuberances weakly developed; teeth moderate in size and numerous (PMT 4, MT 51, VT 27), maxillary teeth extending to about level of center of eye; prevomer clearly projecting from level of palate, bearing vomerine teeth in long, slightly arched, irregular series extending laterally well beyond outer margin of choanae.

Measurements (in mm), tooth counts and limb interval of the holotype. SVL 31.2, TL 38.8, HW 4.3, SG 6.5, HD 2.5, EW 0.7, EL 1.5, ES 1.8, ED 1.3, IC 2.2, IO 1.6, SF 8.4, IN 1.0 SP 0.6, SW 3.6, SAV 28.7, AX 17.8, LI 4, FLL 4.8, HLL 6.2, HAW 2.2, FW 2.8, T3 1.3, T5 1.0, Numbers of teeth: PMT 4, MT 23/28, VT 12/15.

Coloration of the holotype in life ( Fig. 5 ). Dorsal ground color Chestnut (32), interspersed with Fuscous (21) and Salmon Color (106) broken longitudinal lines. A Salmon Color (106) dorsolateral line running from eye to groin separates the middorsal coloration from the lateral and ventral ground coloration; ventral ground coloration Sulfur Yellow (157) flecked with gray at night and Fuscous (21) at daytime. Ventral surfaces speckled with Sky Blue (66). Gular region, hands, and feet Sulfur Yellow (157) suffused with Fuscous (21) on limbs.

Coloration of the holotype in alcohol ( Fig. 6 ). After three years in ethanol (60 %), its coloration has not changed much. Yellowish colors have faded to cream-colored shades as well as the reddish tones in the brown dorsal coloration.

Osteology ( Fig. 7 ). The radiographs of the holotype show the typical osteological features of the genus Bolitoglossa : Head well ossified; vertebral column consists of one atlas, 14 trunk vertebrae, one sacral and two caudosacral vertebrae, and 35 caudal vertebrae; digits well developed on all limbs; slightly more than two distal phalanges of the longest fingers and toes free of webbing, phalangeal formulae of the hand 1–2–3–2, and the foot 1–2–3–3–2. Terminal phalanges of longer fingers and toes slightly expanded distally ( Fig. 4 ).

Habitat and natural history notes. Bolitoglossa jugivagans is only known from the type locality, the upper section of the valley of a feeder stream of Río Chiriquí Malí, on the Caribbean slope of the Cordillera Central, not far from the continental divide in the Fortuna depression of the Cordillera Central of western Panama ( Fig. 1 ). The site is easily reachable on a paved road that serves as a maintenance access way to the Trans-Panama Oil Pipeline. The riverbank next to the street is an old clearing, overgrown with grass, herbaceous plants, and bushes, while the opposite bank is predominantly covered by broadleaf, evergreen mature forest. Mean annual precipitation is approximately 3000 mm and mean annual temperature approximately 20.6° C, making the site assignable to the Premontane Wet Forest life zone according to the Holdridge (1967) classification.

The holotype was encountered on October 28, 2009 at 23:00 h active on the large leaf of an Araceae plant growing out of the long grass on the cleared side of the river. That day, it had been raining in the afternoon and evening; our pluviometer registered 44.5 mm of precipitation between 16:00 and 24:00 h. The automatically recorded temperature was 19.6° C between 18:00 and 23:00 h, and then gradually decreased to a minimum of 17.6° C at 06:00 h. Relative humidity was constantly high at close to 100%. Bolitoglossa jugivagans was the only salamander encountered at this site. Other amphibian species collected in the vicinity include Craugastor fitzingeri (Schmidt) , Diasporus sp., Duellmanohyla uranochroa (Cope) , Espadarana prosoblepon (Boettger) , Incilius coniferus (Cope) , Pristimantis cruentus (Peters) , P. pardalis (Barbour) , and Smilisca phaeota (Cope) . Additionally this site is the type locality of the recently described snake species Sibon noalamina Lotzkat, Hertz , and Köhler. Lotzkat et al. (2012) give additional information on the reptile fauna of the surroundings.

Etymology. The species name is a compound adjective derived from the locative of the Latin noun jugum meaning “mountain ridge” and the present participle of the Latin verb vagare meaning “to wander”. The species epithet signifies “wandering on the mountain ridge” referring to the type locality next to the continental divide of the Cordillera Central.

Figures

FIGURE 1. Map showing the type locality (red triangle) of Bolitoglossa jugivagans on the banks of a feeder river of Río Chiriquí Malí. Further important watercourses are shown in blue. The black line represents the provincial border between Chiriquí in the south and the Comarca Ngöbe-Buglé in the north (cf. inset), and at the same time the border between the protected areas Reserva Forestal La Fortuna (south) and Bosque Protector Palo Seco (north), as well as the drainage divide between river systems flowing into the Pacific Ocean (south), and those flowing into the Atlantic Ocean (north). The elevation of the high point west of the type locality is Cerro Guayabo (approx. 2000 m asl).

FIGURE 2. Results of the molecular analyses. (A) Phylogeny of 16 S mtDNA data for Bolitoglossa jugivagans compared to selected specimens of Bolitoglossa (Eladinea) labeled with museum catalogue numbers, constructed using Bayesian analysis. Scale bar refers to number of substitutions per site. Maximum likelihood bootstrap values are shown above branches, Bayesian posterior probabilities (multiplied by 100) below branches. Taxonomic identities according to Boza-Oviedo et al. (2012). (B) Parsimony network with a connection limit of 15 steps; each node represents a unique haplotype separated from the next by one substitution step. Small circles represent unsampled haplotypes, the rectangle the probably ancestral haplotype.

FIGURE 3. Tooth counts in relation to SVL of Bolitoglossa species resembling each other morphologically (males and females are shown together; see Material and Methods for source of data). (A) Maxillary teeth (MT) divided by snout-vent length (SVL). (B) Vomerine teeth (VT) divided by snout-vent length (SVL).

FIGURE 4. Dorsal view and x-ray images of hands and feet of Bolitoglossa jugivagans. (A) Right hand in dorsal view with corresponding x-ray image to the right. (B) Right foot in dorsal top view with corresponding x-ray image to the right. Scale bar = 2 mm.

FIGURE 5. Holotype of Bolitoglossa jugivagans in life. (A) Holotype at the moment of encounter at night. (B) Holotype the subsequent day. Note difference in lateral coloration.

FIGURE 6. Holotype after three years in 60 % ethanol; (A) Dorsal view; (B) ventral view. Scale bar = 2 cm.

FIGURE 7. X-ray images of the entire holotype; (A) Ventrolateral view; (B) Lateral view. Scale bar = 2 cm.

Tables

TABLE 1. Mean genetic distances in the 16 S rRNA gene between Bolitoglossa species used in the phylogenetic analysis. Numbers above diagonal are for Tamura- 3 - parameter-distances and numbers below are uncorrected p-distances.

Species		Bjug	Brob	Baureo	Bbra	Bgom	Bsubp	Bgraci	Bepim	Bligni
B. jugivagans	Bjug	-	0.042	0.039	0.062	0.075	0.067	0.088	0.068	0.103
B. robinsoni	Brob	0.040	-	0.008	0.065	0.067	0.058	0.080	0.068	0.106
B. aureogularis	Baureo	0.038	0.008	-	0.062	0.064	0.056	0.077	0.065	0.103
B. bramei	Bbra	0.059	0.062	0.059	-	0.046	0.035	0.039	0.063	0.107
B. gomezi	Bgom	0.071	0.063	0.061	0.045	-	0.042	0.060	0.065	0.105
B. subpalmata	Bsubp	0.063	0.056	0.053	0.034	0.040	-	0.034	0.065	0.111
B. gracilis	Bgraci	0.082	0.075	0.072	0.038	0.057	0.033	-	0.078	0.125
B. epimela	Bepim	0.065	0.065	0.062	0.060	0.062	0.062	0.074	-	0.120
B. lignicolor	Bligni	0.095	0.097	0.095	0.098	0.097	0.102	0.114	0.109	-