Bolitoglossa yariguiensis, Meza-Joya & Hernández-Jaimes & Ramos-Pallares, 2017

Meza-Joya, Fabio Leonardo, Hernández-Jaimes, Carlos & Ramos-Pallares, Eliana, 2017, A new species of Salamander (Caudata, Plethodontidae, Bolitoglossa) from Serranía de los Yariguíes, Colombia, Zootaxa 4294 (1), pp. 93-111 : 101-108

Bolitoglossa yariguiensis sp. nov.

( Figures 3–5 )

English name: Yariguíes salamander

Spanish name: Salamandra de los Yariguíes

Holotype. UIS-A 5280 (original field number H 176; Fig. 3 ), an adult female from Colombia, department of Santander, Serranía de los Yariguíes, municipality of San Vicente de Chucurí , vereda La Colorada (6.7931, - 73.4788, 1,385 m elevation), collected by F.L. Meza-Joya and C. Hernández-Jaimes on April 2013.

Paratypes. UIS-A 5265 (adult female) and UIS-A 5266 (adult male) with same data as the holotype, collected on March 2014 by F.L. Meza-Joya and C. Hernández-Jaimes. UIS-A 5278, UIS-A 5279, and UIS-A 5281 (adult females), with same data as the holotype, collected on June 2015 by F.L. Meza-Joya and C. Hernández-Jaimes. UIS-A 5282 (adult male) from 0.3 linear km away from the former sampling site, Serranía de los Yariguíes, municipality of San Vicente de Chucurí, vereda La Colorada (6.7910, -73.4807, 1,473 m elevation), collected on August 2015 by E. Meneses.

Diagnosis. Species assigned to genus Bolitoglossa , subgenus Eladinea , species group adspersa (sensu Parra- Olea et al. 2004). Bolitoglossa yariguiensis is unique among South American salamanders by the following combination of characters: relative small size for adult males (SL 37.8± 0.3 mm) and females (SL 44.9± 2.5 mm); snout short (SNL/HL 0.4±0.01), slightly rounded in lateral profile and truncate in dorsal view; protruding rounded eyes, visible from ventral view; head broad (HW/SL 0.16±0.01), head nearly as wide as long in females (HW/HL 0.96±0.1), but narrowest in males (HW/HL 0.86±0.05); neck clearly distinguished, bearing an evident gular fold; males with non-prominent oval mental gland, transversally oriented; few premaxillary teeth in males (2.5±0.7) and females (3.0±0.7), usually one or two piercing the upper lip in adult males; numerous vomerine teeth in males (28.5±0.7) and females (38±11.5); vomerine teeth usually forming a more numerous patch near internal nares, then extending near to parasphenoid patch of teeth; number of maxillary teeth in males (41.5±0.7) and females (47.4±7.1); nasolabial grooves slightly prominent; relatively well-developed labial protuberances, more conspicuous in males; generally strongly webbed hands and feet with longest digits with a triangular tip, other digits rounded on feet and poorly evident on hands (see variation); subterminal pad not evident on digits; digits in order of increasing length I<II=IV<III on hands and I<V<II<IV<III on feet; trunk relatively short in males (18.9± 0.2 mm) and females (23.2± 1.3 mm); tail relatively short (TL/SL 0.8±0.1); pectoral width from 4.8 to 4.9 mm in males (4.9± 0.1 mm) and from 6.3 to 6.6 mm in females (6.4± 0.2 mm); limb interval equals 2 in all males and ranges from 2 to 2.5 in females (LI 2.1± 0.2). This species differs genetically from its closest South American relatives by a genetic distance of more than 4% for 16S rRNA and 11% for cyt b mtDNA ( Tables 3 and 4).

Comparisons with other species. Bolitoglossa yariguiensis can be readily distinguished from other species in the adspersa species group by the following characteristics (features for contrasting species are in parentheses; measurements and counts are given as mean values): It differs from B. adspersa , B. chucantiensis , B. hiemalis , B. hypacra , B. savagei , B. tamaense , B. tatamae , and B. vallecula by lacking dermal subterminal pads on the ventral surface of the digits (present in all digits of these species, except in B. chucantiensis [present only on toes 2–3–4 and fingers 2–3] and B. tamaense [present only on toes 2–3–4]). This species has smaller body size than B. borburata (males SL 44.0 mm, females SL 54.8 mm), B. capitana (males SL 64.4 mm, females SL 84.9 mm), B. nicefori (males SL 46.8 mm, females SL 59.3 mm), B. phalarosoma (females SL 55.8 mm), B. guaramacalensis (males SL 48.3 mm, females SL 69.4 mm), B. lozanoi (males SL 51.6 mm, females SL 55.9 mm), B. palmata (females SL 50.8 mm), B. pandi (females SL 50.4 mm), and B. silverstonei (males SL 49.3 mm). This species also differs from B. altamazonica , B. caldwellae , B. chica , B. madeira , B. mucuyensis , B. orestes , B. ramosi , and B. walkeri by having extensive webbing on hands and feet with only the tip of the third digit pointed, with remaining digits rounded on feet and almost indistinct on hands.

Bolitoglossa yariguiensis can also be distinguished from similar species in body size and webbing extension as follows (see Table 2 for additional details): from B. biseriata by having more vomerine teeth (males 24, females 28), smaller body size in females (48.7 mm), and shorter trunk (males 21.9 mm, females 27.3 mm), head (males 8.4 mm, females 10.2 mm), and limb interval (males 4, females 3); from B. digitigrada by having larger forelimbs (males 7.6, females 8.3), hindlimbs (males 7.8, females 8.1), and tail (males 26.2, females 28.1), more vomerine (males 16, females 18) and maxillary (males 17, females 15) teeth; from B. medemi by having smaller body size in males (40.4 mm, slightly overlapping) and shorter limb interval (males 0.6, females 1.1); from B. equatoriana by having smaller body size in males (41.5 mm), and more vomerine (males 21, females 21) and maxillary teeth (males 25, females 25). The new species can be distinguished from B. sima by having shorter trunk (males 19.6, females 25.1 mm, slightly overlapping) and tail (males 32.6, females 42.6 mm), and larger hindlimbs (males 8.8 mm, females 9.9 mm); this species also has fewer vomerine (males 10, females 20) and maxillary teeth (males 31, females 35). The only male B. sima available for comparison is a small specimen representing the lower limit of the measured characters. Bolitoglossa yariguiensis differ from B. tapajonica by having more vomerine (males 18, females 16) and maxillary teeth (males 19, females 16), larger head (males 6.2 mm, females 5.5 mm) and snout (males 2.1 mm, females 2.2 mm), and shorter limb interval (males and females 4.0).

Two other closely related species ( B. paraensis and B. peruviana ; Fig. 2 ) known to occur in the Amazon Basin ( Brcko et al. 2013) are morphologically similar to B. yariguiensis , which can be distinguished from B. paraensis by having more vomerine (males 16, females 15) and maxillary (males 23, females 24) teeth, larger (males 5.4 mm, females 5.6 mm) and broader head (males 5.1 mm, females 5.4 mm), larger snout (males 2.3 mm, females 2.2 mm), and shorter limb interval (males and females 2.5). Females of B. peruviana have larger (8.2 mm) and narrower head (5.9 mm), shorter hindlimbs (7.6 mm), larger limb interval (3.8), and fewer vomerine (males 15.6, females 21.5) and maxillary teeth (males 19, females 27.7). Two other closely related species ( B. leandrae and B. guaneae ; Fig. 2 ) known to occur on the northeastern Andes in Colombia and Venezuela also bear morphological similarity to B. yariguiensis . The new species can be distinguished from B. leandrae ( Fig. 4 , Table 2) by having larger body size (males 30.3 mm, females 39.2 mm), tail (males 23.8 mm, females 28.3 mm), and hindlimbs (males 6.8 mm, females 8.2 mm); shorter trunk (males 21.8 mm, females 29.3 mm), head (males 7.7 mm, females 9.2 mm), and more maxillary (males 23, females 29) and vomerine teeth (males 19, females 20). Bolitoglossa yariguiensis is very similar to B. guaneae , but differs from it by the following features (although slightly overlapping mainly in females; Fig. 4 , Table 2): larger (males 6.4 mm, females 7.4 mm) and wider head (males 5.6 mm, females 6.9 mm, both overlapping), larger snout (males 2.4 mm, females 2.7 mm), and more maxillary (males 21.7, females 37.2) and vomerine teeth (males 19.9, females 24.4). As additional evidence, this new species is also readily distinguishable from all salamanders in the B. adspersa group by having more than 4% K2P pairwise genetic distance ( Table 3 and 4).

Description of the holotype. An adult female (SL 46.63 mm) with broad head (HW/SL 0.16); head as wide as long (HW/HL 0.98); neck clearly distinguished with evident gular fold; snout slightly rounded in profile and truncate in dorsal view; large well developed eyes, protruding from outline of head in ventral view; postorbital groove present; canthus rostralis small and rounded; numerous maxillary (54) and vomerine (52) teeth; few premaxillary teeth (4) not piercing upper lip; labial protuberances relatively well-developed; nasolabial grooves slightly prominent; extensive interdigital webbing on hands and feet, with only tip of third digit free, other digits poorly defined except near the distal tips; subterminal pad on digits absent; digits in order of increasing length I<II=IV<III on hands and I<V<II<IV<III feet; longest digits triangular and pointed (L3T and L3F), other digits rounded on feet and almost indistinct on hands; limbs relatively short (FL/SL 0.24, HLL/SL 0.22); tail not exceeding standard length (TL/SL 0.76), slightly rectangular and moderately constricted at base, rounded toward tip; trunk relatively short (24.56 mm); 13 costal grooves between limbs; limb interval equals 2 costal grooves.

Measurements (in mm) and counts of holotype. SL 46.63; HL 7.71; HW 7.34; HD 4.09; SGF 11.21; EYW 2.17; EYL 3.26; SNL 3.17; SP 1.25; LWS 4.49; SWS 3.58; EN 2.73; OD 2.18; CEL 4.74; IOD 3.33; NGGF 4.09; SA 15.12; AG 24.56; PW 6.51; FL 11.09; HLL 10.37; HDW 3.02; FW 3.86; L3F 2.92; L3T 3.47; TL 35.37; TW 4.85; TD 4.41; VL 3.57; LI 3.5; MT 54; VT 52; PT 4.

Coloration of the holotype in life. The color pattern of the holotype specimen was recorded the day after capture (at 0 930 h), as follows: dorsum nearly uniform orange-brown, darker toward mid-dorsum; rostral surface of head dark-brown, forming light-brown inverted triangle behind eyes; labial region dark-brown with small, scattered, cream specks; dorsal surface of fore-limbs dark-brown; dorsal surface of proximal hindlimbs orangebrown, distal surface dark-brown; venter light-gray with scattered cream specks; dorsal and lateral surface of tail dark-brown, lighter toward base and tip; ventral surface of tail light-gray with larger, scattered, cream specks; body sides with dark-brown longitudinal stripe, wider on trunk ( Fig. 5 F).

Coloration of the holotype in preservative. The color pattern of the holotype specimen stored in ethanol (70%) was recorded after two years in storage. The specimen retains the original pattern of coloration, but the orange-brown dorsum turned golden-brown; the light-gray venter turned light-ochre, with a large abdominal black patch; ventral surface of tail turned dark-brown, darker toward the tip ( Fig. 3 A–C).

Color variation. We examined all specimens from the type series (two males and five females), which showed three additional variations of color pattern, relative to the holotype. Two males (UIS-A 5266 and UIS-A 5282) and two females (UIS-A 5278 and UIS-A 5279) have a nearly uniform dark-brown dorsum, lighter toward flanks; orange-brown inguinal patches and tail tips; ventral surfaces of these specimens vary from almost uniformly lightbrown (UIS-A 5266 and UIS-A 5278) to light-ochre (UIS-A 5279), with almost uniformly distributed spots (UIS- A 5266), scattered specks (UIS-A 5279), or without them (UIS-A 5 278). The venter of specimen UIS-A 5282 is golden-brown with a light-brown ventral stripe. One female (UIS-A 5265) has a yellow-ochre dorsum; rostral portion of the head dark-brown, forming a light-brown inverted triangle behind the eyes; dorsal surface of fore- and hindlimbs almost uniformly dark-brown; venter pale yellow. One female (UIS-A 5 281) has an almost uniformly light-brown dorsum; flanks light-gray; dorsal surface of fore- and hindlimbs light-gray; inguinal region orangebrown; tail tip light-ochre; venter light-ochre with a series of longitudinal, small, abdominal black patches, and scattered, cream spots ( Fig. 5 ).

Osteology. A single cleared and stained paratype (UIS-A 5265) showed the species to have the typical osteology of the genus Bolitoglossa and subgenus Eladinea . The skull is well formed in both number and degree of development of elements present; nasal region comprises premaxilla located on anterior border of upper jaw; paired maxilla on arch of upper jaw; nasals partly overlying dorsal surface of nasal capsule; small paired prefrontals situated on posterolateral portion of nasal capsule. Palatal region formed by paired anterior vomers, which lie on anterior roof of oral cavity and bear 30 bicuspid teeth. Parasphenoid lies posterior to anterior vomers, contacts ventral surface of posterior vomer, and bears parasphenoid teeth. Skull roof relatively smooth and lacking major ridges or crests, formed by two paired elements (frontal and parietal) entirely covering anterior and posterior roof of braincase, respectively. Temporal region encloses paired squamosal, covering dorsal surface of quadrate and laterally overlying otic process of palatoquadrate. Orbitosphenoid forms lateral side of braincase. Lower jaw consists of Meckel’s cartilage, replacing mentomeckelian bone, and two paired investing bones: dentary and prearticular. Posterior region of skull comprises occipital-otic complex, formed via fusion of three elements: prootic, opisthotic, and exoccipital. Cartilaginous hyoid apparatus formed by first basibranchial, from which ceratohyals, first and second ceratobranchials, and epibranchials extend posterolaterally. Fore- and hindlimbs well developed; phalangeal formula of hand is 1–2–3–2 and foot is 1–2–3–2–2, with terminal phalanges irregular in shape. Vertebral column consists of single cervical vertebra (atlas), 14 trunk, one sacral, two caudosacral, and 28 caudal vertebrae; ribs present on all trunk vertebrae except for terminal vertebra.

Measurement and webbing variation in the type series. The type series consists of seven adult specimens (five females and two males). This species is apparently sexually dimorphic in size (male SL 37.8± 0.3 mm; female SL 44.9± 2.5 mm). The SL ranges from 37.6 mm for the smallest male, to 46.8 mm for the largest female. Males have shorter heads than females (male SL/HL 5.3±0.3; female SL/HL 5.8±0.2), as well as narrower heads (male HD 3.1± 0.01 mm; female HD 3.9± 0.2 mm). Males also have narrower pectoral region than females (male PW 4.8± 0.1 mm; female PW 6.4± 0.2 mm). Despite these intraspecific variations, sexual dimorphism could not be thoroughly analyzed due to the low sample sizes for males and females. Males are easily recognizable by secondary sexual characters (presence of hedonic gland and 1–2 premaxillary teeth piercing the upper lip); both characteristics are absent in females. Two specimens (male UIS-A 5266, female UIS-A 5282) showed less webbed hands with all four fingers evident, the longest digit triangular at tip (as in the other specimens), others rounded.

Distribution, ecology, and natural history. Bolitoglossa yariguiensis is only known from a fragmented patch of Andean cloud forest on Serranía de los Yariguíes in the western slope of the Cordillera Oriental de Colombia, between 1,385 and 1,473 m elevation ( Fig. 1 ). The type locality consists of a forest patch with a dense canopy of trees up to 30 m high, dominated by trees of the genera Erythrina (Fabaceae) , Nectandra (Lauraceae) , and Cordia (Boraginaceae) , with abundant bromeliads and other epiphytes (e.g., Orchidaceae , Loranthaceae ; Fig. 6 ). All specimens of this species were found active at night (between 18:00 and 23:00 hours), on ferns, bromeliads, and low vegetation, between 20 and 80 cm height (51± 17 cm, n=6). The mean of the body temperature of the specimens collected was 18.8±0.3°C (n=6), the mean substrate temperature recorded was 18.1±0.3°C (n=6), the mean ambient temperature was 19.4±0.2°C (n=6), and the mean relative humidity was 79.6±2.5% (n=6). The small type series (7 specimens) were collected during multiple surveys to the study site, suggesting that B. yariguiensis is a rare species. Other amphibians found at the same collection site included Andinobates virolinenis (Dendrobatidae) , Espadarana andina (Centrolenidae) , Pristimantis gaigei , Pristimantis bacchus , Pristimantis bicolor , and Pristimantis miyatai (Craugastoridae) .

Etymology. The use of the Latin suffix – ensis (‘pertaining to or native of’) in the specific designation of yariguiensis denotes the fact that, so far, the species has only been found in the Serranía de los Yariguíes (Santander department, Colombia), itself named in honor of the former ancestral inhabitants, the Yariguíes indigenous tribe. This ethnic group was characterized as nomadic hunters and gathers with a Carib linguistic affiliation (Velázquez & Castillo 2006). They resisted the Spanish invasion for more than four centuries, but were exterminated in the mid-20th century as a result of governmental policies justified as “progress, civilization and development” ( Velásquez & Castillo 2006; Ortiz 2008).

Figures

FIGURE 1. Map of Serranía de los Yariguíes (Santander department, Colombia) showing the distribution of Bolitoglossa yariguiensis (white dot). Insert at left side shows the relative position of Serranía de los Yariguíes within South America and Colombia.

FIGURE 2. Maximum likelihood tree of Bolitoglossa (Eladinea) based on the concatenated sequences of 16 S rRNA and cyt b genes. The new sequences of the Bolitoglossa species included in this work are highlighted in different colors. Numbers on nodes represent bootstrap support and posterior probabilities, respectively. ML bootstrap support and Bayesian posterior probabilities are shown on the internodes.

FIGURE 3. Bolitoglossa yariguiensis holotype (UIS-A 5280). Ventral (A), lateral (B), and dorsal (C) views of the entire body. Ventral (D), lateral (E), and dorsal views (F) of head. Ventral views of right hand (G) and right foot (H).

FIGURE 4. Box plot showing morphological diagnostic features between B. yariguiensis and closely related species. Boxes represent the range of proportions (maximum and minimum values) and mean values of the data for males (empty circles) and females (filled squares). Data for B. leandrae was taken from the original description (Acevedo et al. 2013).

FIGURE 5. Color pattern variation in Bolitoglossa yariguiensis. Holotype UIS-A 5280, adult female (A, above) and paratype UIS-A 5279, adult female (A, below). Paratype UIS-A 5266, adult male (B). Paratype UIS-A 5281, adult female (C). Paratype UIS-A 5265, adult female (D).

FIGURE 6. General view of the type locality of Bolitoglossa yariguiensis (A) and the habitat corresponding to secondary Andean cloud forest where most of type specimens were found (B).