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Research Article
A new Bolitoglossa (Amphibia, Caudata, Plethodontidae) from the Cordillera Oriental of Colombia
expand article infoYeny Rocio López-Perilla‡§, Juan David Fernández-Roldán§, Fabio Leonardo Meza-Joya|, Guido Fabian Medina-Rangel§
‡ Fundación Natura, Bogotá, Colombia
§ Universidad Nacional de Colombia, Bogotá, Colombia
| Universidad Industrial de Santander, Santander, Colombia
¶ Massey University, Palmerston North, New Zealand

Corresponding author: Yeny Rocio López-Perilla ( yrlopezp@unal.edu.co )

Academic editor: Uri García-Vázquez
© 2023 Yeny Rocio López-Perilla, Juan David Fernández-Roldán, Fabio Leonardo Meza-Joya, Guido Fabian Medina-Rangel.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: López-Perilla YR, Fernández-Roldán JD, Meza-Joya FL, Medina-Rangel GF (2023) A new Bolitoglossa (Amphibia, Caudata, Plethodontidae) from the Cordillera Oriental of Colombia. ZooKeys 1158: 27-48. https://doi.org/10.3897/zookeys.1158.99077
ZooBank: urn:lsid:zoobank.org:pub:57A79842-A71A-4A25-917F-57A33D3334F5
Open Access

Abstract

A new salamander species of the genus Bolitoglossa is here described from the cloud forests of the western slopes of the Cordillera Oriental of Colombia, in the Cundinamarca department. The most salient characters of this new species are its numerous maxillary and vomerine teeth, its moderate webbing on hands and feet, its short and robust tail, and its chromatic variation. Based on molecular analyses this new species is assigned to the adspersa species group and its status established as the sister species of B. adspersa, with which it was previously confused. Lastly, the distribution, natural history, and conservation status of the new species are discussed.

Resumen

Describimos una nueva especie de salamandra del género Bolitoglossa proveniente de los bosques nublados de la vertiente occidental de la Cordillera Oriental de Colombia, en el departamento de Cundinamarca. Los caracteres más sobresalientes de esta nueva especie son sus numerosos dientes maxilares y vomerinos, su palmeadura moderada en pies y manos, su cola corta pero robusta, y su variación cromática. Basados en análisis moleculares asignamos esta nueva especie al grupo de especies adspersa y establecemos su estatus como especie hermana de B. adspersa, con la cual era previamente confundida. Finalmente, discutimos algunos aspectos de su distribución, historia natural y su estado de conservación.

Keywords

Biodiversity, coloration, phylogenetic systematics, salamanders, taxonomy

Palabras clave

Biodiversidad, coloración, salamandras, sistemática filogenética, taxonomía

Introduction

Bolitoglossa Duméril, Bibron & Duméril, 1854 is currently the largest and most diverse genus of salamanders (Amphibia: Caudata) with a total of 138 species recorded from northeastern Mexico to central Bolivia (Frost 2023). However, the actual diversity of Bolitoglossa in South America may be underestimated given the existence of cryptic forms (Jaramillo et al. 2020). Colombia currently has 24 species (Frost 2023), of which only seven have been described in this century, while the remainder are descriptions prior to 1973 (Frost 2023). As for the phylogenetic relationships for the species of the country, little is known; there are some works that include species distributed in the Colombian Amazon (Cusi et al. 2020; Jaramillo et al. 2020), as well as phylogenies presented in the most recent descriptions of species in the country (Acevedo et al. 2013; Meza-Joya et al. 2017).

The genus Bolitoglossa has its highest diversity in the Cordillera Oriental (Meza-Joya et al. 2017), where a total of 11 species have been described: B. adspersa (Peters, 1863), B. altamazonica (Cope, 1874), B. capitana Brame & Wake, 1963, B. guaneae Acosta-Galvis & Gutierrez, 2012, B. leandrae Acevedo, Wake, Márquez, Silva, Franco & Amézquita, 2013, B. lozanoi Acosta-Galvis & Restrepo, 2001, B. nicefori Brame & Wake, 1963, B. palmata (Werner, 1897), B. pandi Brame & Wake, 1963, B. tamaense Acevedo, Wake, Márquez, Silva, Franco & Amézquita, 2013, and B. yariguiensis Meza-Joya, Hernández-Jaimes & Ramos-Pallares, 2017.

These ‘mushroom-tongued’ or ‘tropical lungless’ salamanders, as they are commonly known, are characterized by lacking a sublingual fold; having a very long and rapidly projected tongue; a tendency towards tarsal reductions; extensive webbing associated with climbing behavior; and fully terrestrial to arboreal habits (Wake and Lynch 1976; Köhler 2011; Angarita-Sierra et al. 2020; Ponssa et al. 2022).These salamanders inhabit a variety of ecosystems, from lowland rainforests to highland areas, where they are particularly diverse in montane cloud forests and less so in paramo ecosystems (Köhler 2011).

In this paper, we describe a new species of Bolitoglossa using morphological and molecular data, associated with the existing remnants of Andean montane forests on the western flank of the Cordillera Oriental, and we compared it with other known species of the genus in Cundinamarca, Colombia.

Materials and methods

Specimen collection and fieldwork

The holotype and most of the paratypes were collected within vereda Roble Hueco, Bojacá municipality, Cundinamarca department, Colombia (4.6963, -74.3624, 2630 m a.s.l.; Fig. 1). Specimens were captured by hand using free searches over two 10-day field trips, kept in plastic bags until weighed and photographed, and then euthanized by applying 2% lidocaine gel. Tissue samples were obtained from the tail or liver of individuals and preserved in absolute ethanol. Specimens were then fixed in 10% formaldehyde and then stored in 70% ethanol. All specimens were deposited at Colección de Anfibios, Instituto de Recursos Biológicos Alexander von Humboldt, Villa de Leyva, Boyacá, Colombia (IAvH).

Figure 1. 

Map of Colombia showing the distribution records of Bolitoglossa muisca and other sympatric Bolitoglossa species in the Cordillera Oriental.

Morphology and taxonomy

Measurements and counts of morphological characters were taken using a Neiko digital caliper rounded to the nearest 0.1 mm under a Leica Stemi 2000 stereoscope, using the diagrams in Bingham et al. (2018) as a model. The following morphological traits were analyzed for all specimens: snout-vent length (SVL); head length (HL); head width (HW); tail length (TL); maxillary teeth (MT); vomerine teeth (VT); and additional measurements only for the description of the holotype: interorbital distance (IOD); eye diameter (EYD); snout length (SNL). Color descriptions are based on field notes and photographs of preserved specimens using the color catalogue of Köhler (2012). Format of diagnosis and description follows Meza-Joya et al. (2017). Species comparisons were made following Brame and Wake (1963) or their original descriptions for those species described after 1963, as well as by examining Bolitoglossa specimens housed at Colección de Anfibios, Instituto de Recursos Biológicos Alexander von Humboldt, Villa de Leyva, Boyacá, Colombia (IAvH), Laboratorio de Anfibios, Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá D.C., Colombia (ICN), Colección de Anfibios, Museo La Salle, Universidad de La Salle, Bogotá D.C., Colombia (MLS) and Colección Herpetológica of Universidad Industrial de Santander, Bucaramanga, Colombia (UIS).

Molecular and phylogenetic analyses

We extracted whole genomic DNA from liver or muscle tissue of specimens of Bolitoglossa preliminary identified as B. adspersa, using the DNeasy Blood & Tissue Kit (Qiagen, #69506). Extracted DNA samples were amplified by PCR for the partial non-coding 16S rRNA (16S ≈ 517 bp) and the protein-coding cytochrome b (cyt b ≈ 742 bp) mitochondrial genes, using the primers 16Sar-L and 16Sbr-H (Palumbi et al. 1991) and MVZ15 and MVZ16 (Moritz et al. 1992), respectively. Amplification protocols (reaction mix and thermocycler programs) are as described in Meza-Joya et al. (2017). The amplicons were cleaned and then sequenced at Macrogen Inc. (Seoul, Korea) by capillary electrophoresis using an ABI3730 genetic analyzer. The partial sequences obtained were visualized, cleaned, and assembled with Geneious v. 9.1.6 (Kearse et al. 2012); we only used sequences with a quality score higher than 90%. DNA sequences were deposited in GenBank (Appendix 1).

Homologous sequences from other Bolitoglossa in the adspersa group were downloaded from GenBank and compared with our molecular data. Representatives from other species groups within Eladinea (epimela, schizodactyla, and subpalmata) were used as outgroups (Appendix I). We also included partial sequences of the nuclear protein-coding recombination activating gene 1 (RAG1 ≈ 792 bp), a relatively well-sampled gene fragment, for other species of Bolitoglossa. We performed multiple alignments in MAFFT v. 7.304 (Katoh and Standley 2013) using the G-INS-i algorithm. Phylogenetic analyses were performed on the concatenated dataset. We inferred the best-fit partition scheme and the best-fit evolution models with PartitionFinder v. 2.1.1 (Lanfear et al. 2017) under the Bayesian Information Criterion (BIC). For this, we performed an exhaustive search of all possible partitioning schemes on our dataset, placing the 16S gene in a separate partition whereas protein-coding genes were further partitioned by codon position. We performed a maximum likelihood (ML) phylogenetic analysis on IQ-TREE 2.0 (Nguyen et al. 2015), running 10,000 ultrafast bootstrap pseudoreplicates for internal node support (Hoang et al. 2018). We also conducted a Bayesian Inference (BI) analysis with the software MrBayes 3.2.6 (Ronquist et al. 2012), using four chains on two runs for 10 million generations and a sampling frequency of 10,000 generations with a burn-in of 0.10. Stationarity was determined with the software Tracer 1.6 (Rambaut et al. 2018).

For species delimitation, we first calculated uncorrected pairwise genetic p-distances for the 16S and cyt b genes between the two distinct evolutionary lineages identified within B. adspersa, with 1,000 bootstrap replicates using MEGA X (Kumar et al. 2018). Then, we split genetic lineages into candidate species using the Automatic Barcode Gap Discovery (ABGD) method (Puillandre et al. 2012). This analysis was based on the 16S gene matrix, the best-represented gene in our dataset, using K2P distances, prior for maximum value of intraspecific divergence between 0.001 and 0.1, ten recursive steps, and a gap width of 1.5. We also used the tree-based method as implemented in the Species Delimitation plugin in Geneious (Masters et al. 2011), using the ML phylogeny as a guide tree to calculate the mean probability of the ratio of intra- to interspecific genetic distances for the initial two-species hypothesis within B. adspersa (Brame and Wake 1963).

Results

Molecular and phylogenetic analyses

The concatenated data matrix contains 2,070 bp for 67 terminals (excluding outgroups) from 26 described species of the Bolitoglossa adspersa group, as well as nine candidate species and the new species described herein: 64 samples for 16S (516 bp), 45 for cyt b (759 bp), and 26 for RAG1 (795 bp). The best partition scheme (LnL = -14128.62, BIC = 29,677.40) for our concatenated dataset includes five subsets, each with an evolution model: (16S, cyt b pos1: GTR+I+G) (cyt b pos2: HKY+I+G) (cyt b pos3: GTR+G) (RAG1 pos1, RAG1 pos2: K81+I) (RAG1 pos3: HKY+G). The resulting topologies from the ML and BI were congruent; thus, here we present only the ML tree (Fig. 2).

Figure 2. 

Maximum-likelihood tree of Bolitoglossa (Eladinea) adspersa group showing the phylogenetic position of Bolitoglossa muisca. Vertical bars indicate the two-species hypothesis within Bolitoglossa adspersa with the supported species partitions inferred using genetic data (p-distances, ABGD, and P ID). Support values for well-supported nodes correspond to ML ultrafast bootstrap (> 95) and Bayesian posterior probabilities (> 0.95), respectively. Photograph by JDF.

The inferred phylogenetic relationships were largely consistent with those from recent studies (Meza-Joya et al. 2017; Cusi et al. 2020; Jaramillo et al. 2020), with incongruences likely resulting from differences in taxon sampling. The Bolitoglossa adspersa species group was rendered as monophyletic with significant support (UFB = 99, PP = 1.0). All species included in our analyses were monophyletic with strong support, yet their relationships remained largely unresolved. As expected, samples from the new species were within the adspersa group, forming a well-supported clade (UFB = 100, PP = 1.0) sister to samples of B. adspersa from its type-locality, Bogotá, Cundinamarca department, Colombia, and surroundings, with significant support (UFB = 98, PP = 0.99). This clade was recovered as a sister to a clade grouping species from northeastern Colombia and Venezuela, but this relationship was poorly supported. GenBank sequences of a specimen from El Soche, Cundinamarca, Colombia, identified as Bolitoglossa sp. 1 (MVZ 167947, corrected here as MVZ 167997 based on the actual number on the MVZ catalog) by Parra-Olea et al. 2004, correspond with the new species described here. This specimen has long been recognized as different from adspersa (Hanken and Wake 1982; Parra-Olea et al. 2004).

With respect to species delimitation, all methods supported the two-species hypothesis within B. adspersa (Brame & Wake, 1963). Uncorrected pairwise p-distances between these two sister lineages were 2.1% (± 0.003%) for 16S and 7.0% for cyt b. The ABGD analysis resulted in five partitions separating the data into five (P ≤ 0.0028) or two putative species (P ≥ 0.0046), yet the new species described here was recovered as a candidate taxon in all partitions. Taxonomic distinctiveness for the new species was also supported under either relaxed or strict tree-based criteria (P ID Liberal = 1.00, CI = 0.86–1.00; P ID Strict = 0.79, CI = 0.62–0.97) with significant support: Rosenberg’s PAB statistics = 0.01 and PRD (randomly distinct) > 0.05. Furthermore, as it is shown below, morphological comparisons consistently support the recognition of this lineage as a new species.

Bolitoglossa muisca sp. nov.

https://zoobank.org/63BA9285-C4FE-45B0-B828-BDB37F4E06BF
Figs 2, 3, 4, 5, 6, 7, Tables 1, 2 Common English name: Muisca salamander Common Spanish name: Salamandra Muisca

Type material

Holotype. IAvH-Am-17413, an adult female from Finca La Esmeralda, vereda Roble Hueco, Bojacá municipality, Cundinamarca department, Colombia (4.6963, -74.3624, 2630 m a.s.l.), collected by Y.R. López-Perilla on 4 February 2021 (Fig. 1).

Paratypes (n = 8: 3 females, 5 males). IAvH-Am-17417 (adult male), IAvH-Am-17419 (adult female), IAvH-Am-17421 (adult male) and IAvH-Am-17422 (adult male) from Finca La Esmeralda, vereda Roble Hueco, Bojacá municipality, Cundinamarca department, Colombia (4.6963, -74.3624, 2630 m a.s.l.), collected by Y.R. López-Perilla in February 2021 (Fig. 5). IAvH-Am-17423 (adult male), IAvH-Am-17425 (adult male) and IAvH-Am-17428 (adult female) from Finca Peñas Blancas, vereda Roble Hueco, Bojacá municipality, Cundinamarca department, Colombia (4.6916, -74.3581, 2390 m a.s.l.), collected by Y.R. López-Perilla in February 2021. IAvH-Am-17429 (adult female) from vereda Cascajal, Soacha municipality, Cundinamarca department, Colombia (4.5954, -74.2922, 2700 m a.s.l.), collected by G.F. Medina-Rangel in September 2022.

Referred specimens

(n = 36: 7 females, 29 juveniles and subadults). ICN 3544–48, five adult females from Hacienda ‘El Soche’, Granada municipality, Cundinamarca department, Colombia (4.5153, -74.3240, 2600 m a.s.l.) obtained by Rurithza Velandia in December 1977; specimen ICN 3545 is cleared and stained; MVZ 167997, a juvenile obtained by Pere Alberch on 17 December 1978. ICN 58245–58268, a batch of 23 juvenile and subadult specimens from Hacienda ‘La Tribuna’, vereda Noruega Alta, Silvania municipality, Cundinamarca department, Colombia (4.4836, -74.3203, 2700 m a.s.l.) obtained by Cesar Monguí in September 2008. ICN 60319–20, two juveniles from vereda Roquemonte, San Antonio del Tequendama municipality, Cundinamarca department, Colombia (4.6056, -74.3008, 2600 m a.s.l.) obtained by J.D. Fernández in August 2013. ICN 60321–22, a juvenile and an adult female (respectively) also from vereda Roquemonte, San Antonio del Tequendama municipality, Cundinamarca department, Colombia (4.6056, -74.3008, 2600 m a.s.l.) obtained by J.D. Fernández in March 2017. ICN 60323–25, two juveniles and an adult female (respectively) from vereda Roquemonte, San Antonio del Tequendama municipality, Cundinamarca department, Colombia (4.6056, -74.3008, 2600 m a.s.l.), also obtained by J.D. Fernández in January 2018.

Diagnosis

Bolitoglossa muisca is a member the subgenus Eladinea and of the adspersa species group. The new species is characterized by the following morphological characters: a large-size body; a broad head; a rounded snout in dorsal and ventral views; a very thick postocular fold; a moderate subgular fold; smooth skin texture; moderately long limbs; moderate webbing on third finger and toe; and a short, robust tail.

Even though Bolitoglossa adspersa and B. muisca share their moderate webbing on hands and feet, we regard the former as having less webbing than the latter. Moreover, the tips of the fingers and toes are separated from the distal margin of the webbing, exposing their subcircular-shaped digits; unlike those of B. muisca (Fig. 4). The new species is slightly larger on average than B. adspersa (mean SVL 52.8±3.4 mm; range 33.0–72.1 mm; n = 22 vs. 45.0±3.4 mm; range 30.7–66.3 mm; n = 26), additionally, the tail of B. adspersa is thin and long in relation to the trunk but thick and short in relation to the trunk in B. muisca (Table 1). Bolitoglossa muisca differs from B. capitana by having moderately webbed hands and feet (vs. almost fully webbed hands and feet in B. capitana), by being overall smaller in size (mean SVL 52.8±3.4 mm; range 33.0–72.1 mm; n = 22 vs. 75.2±10.9 mm; range 59.2–85.5 mm; n = 5), by having fewer maxillary teeth (mean MT 24.4±3.0; range 14–36; n = 17 vs. 30.4±5.1; range 22–37; n = 5) by having fewer vomerine teeth (mean VT 35.1±4.0; range 24–53; n = 17 vs. 66.4±14.8; range 46–87; n = 5), and because the new species bears a faint, very small gular fold that is large, thick and notable in B. capitana (Cruz-Rodríguez et al. 2021: figs 13, 14). Bolitoglossa muisca differs from B. pandi because the tips of the third digit and toe of the latter are triangular and pointed in outline (vs. third digits and toes oval and webbed to a higher degree in B. muisca), by being a slightly larger species (mean SVL 52.8±3.4 mm; range 33.0–72.1 mm; n = 22 vs. 44.0±2.9 mm; range 35.9–52 mm; n = 12), and by having mostly smooth skin (vs. coarse skin in B. pandi); moreover, the tail of B. pandi tapers gradually and symmetrically from broad to slender antero-posteriorly, unlike that of the new species, which is slightly rectangular in outline, becoming abruptly wider than the base, and ending in a rounded tip (Table 1).

Table 1.
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Meristic data and morphological comparisons of Bolitoglossa adspersa, B. capitana, B. muisca, and B. pandi. For abbreviations see methods section.

Characters/Species B. adspersa B. capitana B. muisca B. pandi
VT 26.1±2.5 (18–38) [n = 17] 66.4±14.8 (46–87) [n = 5] 35.1±4 (24–53) [n = 17] 31.8±4 (21–42) [n = 12]
MT 17.6±1.5 (13–29) [n = 18] 30.4±5.1 (22–37) [n = 5] 24.4±3 (14–36) [n = 17] 18.3±2.2 (13–26) [n = 12]
SVL 45±3.4 (30.7–66.3) [n = 26] 75.2±10.9 (59.2–85.5) [n = 5] 52.8±3.4 (33–72.1) [n = 22] 44±2.9 (35.9–52) [n = 12]
TL 35±3.7 (21.2–54.2) [n = 26] 61.0±7.4 (53.2–70.8) [n = 4] 38.9±4.3 (11.6–55.5) [n = 22] 29.1±5.2 (15.4–42.8) [n = 11]
HW 6.6±0.4 (4.9–9.5) [n = 27] 10.9±1.5 (8.8–12.5) [n = 5] 7.9±0.4 (5.4–10.3) [n = 22] 6.6±0.5 (5.3–8.2) [n = 12]
HL 8.2±0.5 (5.8–10.2) [n = 27] 12.2 [n = 1] 9.1±0.7 (5.6–14.5) [n = 22] 7.47±0.6 (6.3–10.2) [n = 12]
TL/SVL 0.8±0.1 (0.6–1.1) [n = 11] 0.8±0.1 (0.7–1.1) [n = 4] 0.72±0.1 (0.2–0.9) [n = 22] 0.6±0.1 (0.34–1.1) [n = 11]
Webbing on third finger Moderate Extensive Moderate Moderate
Webbing on third toe Moderate Extensive Moderate Moderate
Postocular fold Thick Absent Very thick Absent
Subgular fold Very thick Thick Moderate Faint
Snout in dorsal and ventral view Truncated Truncated Rounded Truncated
Tail shape Tapered Tapered Stout Tapered

Description of the holotype

An adult female (SVL = 61.3 mm) with a broad head (HW/SVL = 0.16); head longer than wide (HW/HL = 0.90); neck with a small, faint gular fold; snout short and truncated in profile, and dorsal view, but less so in ventral view (SNL = 3.1 mm); large eyes that do not extend beyond the outline of the head in dorsal view and smaller than interorbital distance (EYD = 3.18 mm, IOD = 3.37 mm); with a thick post ocular fold that extends past the posterior commissure of the eye onto the anterior margin of the gular fold; canthus rostralis subtle, small, rounded in outline; 33 maxillary teeth, 16 to the right and 17 to the left; vomerine teeth 25, these are not arranged in a single row but grouped towards the margins of the parasphenoid bone; with three premaxillary teeth that pierce the upper lip in males; nasolabial grooves well developed; moderate interdigital webbing on hands but third finger extends slightly further than the other fingers; toes with less interdigital webbing than fingers, toes II–V with less membrane than toe I; with subterminal pads on digits, digits in order of increasing length I<II<IV>III; toes I<II<III<IV>V; longest digits of hand and feet are subcircular (L3T and L3F), limbs relatively long (FL/SVL = 0.23, HLL/SVL = 0.23); tail not exceeding standard length (TL/SVL 0.93), narrower than the body at the base (posterior to the vent), slightly rectangular in outline, becoming abruptly wider than the base and ending in a rounded tip, but this condition is artefactual because the tip of the tail is missing; a long trunk (52.5 mm); with 13 costal grooves (Fig. 3). See Table 2 for meristic data of all type specimens.

Figure 3. 

Holotype of Bolitoglossa muisca (IAvH-Am-17413) in A dorsal B ventral and C lateral views. Photographs by JDF. Scale bar: 10 mm.

Figure 4. 

Ventral views of the hands and feet of A Bolitoglossa muisca (IAvH-Am-17413) B Bolitoglossa adspersa (ICN 4885). Photographs by JDF. Scale bar: 10 mm.

Figure 5. 

Paratype of Bolitoglossa muisca (IAvH-Am-17419) in life. Photographs by JDF.

Table 2.
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Meristic data and measurements of the type series of Bolitoglossa muisca.

Characters/Type series IAvH-Am-17413 * IAvH-Am-17417 IAvH-Am-17419 IAvH-Am-17421 IAvH-Am-17422 IAvH-Am-17423 IAvH-Am-17425 IAvH-Am-17428 IAvH-Am-17429
Sex Female Male Female Male Male Female Male Female Female
SVL (mm) 61.3 50.6 60.3 58.1 57.4 72.1 54 51.5 65.9
TL (mm) 53.2 40.8 46.6 49.8 51.6 14.4+ 45.8 36.5 42.6
HW (mm) 9.6 7.7 9.2 7.7 8.7 9.8 8.5 8.2 10.3
HL (mm) 10.6 8.9 10.7 9.4 9.7 11.6 9 9.1 14.5
HW/SVL 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1
TL/SVL 0.8 0.8 0.7 0.8 0.9 -- 0.8 0.7 0.6
VT 25 23 26 18 23 36 22 32 36
MT 33 24 28 36 44 44 36 41 44

* Denotes de holotype. + regenerated tail. -- No data. For abbreviations see Materials and methods section.

Coloration of the holotype in life

The color pattern of the holotype is described based on a photograph taken the day after capture. The dorsal surfaces of the head, the body and the tail are Raw Umber (280), strongly speckled with Dark Salmon (59); white stipples on the lateral surface of the head; the flanks, dorsum, legs, and tail have an irregular thin white stripe; the iris is Light Sky Blue (191) with Pratt’s Rufous (72) reticulations. The throat and ventral surfaces are white with Raw Umber (280) speckles and reticulations; the ventral surfaces of the limbs and tails with some Light Orange Yellow (7) vermiculated; underside of hands and feet are Olive-Brown (278).

Coloration of the holotype in preservative

The color pattern of the holotype was recorded after approximately five months stored in 70% ethanol. The dorsal surfaces of the head, the body and the tail are Raw Umber (280), strongly speckled with Dark Salmon (59); the flanks, dorsum, legs, and tail have an irregular Smoke Gray (266) stripe; the iris is Amber (51) with Orange Rufous (56) reticulations. The throat and ventral surface are Smoke Gray (266) with Raw Umber (280) speckles and reticulations; hands and feet soles are Grayish Horn (268) ventrally (Fig. 3).

Color variation

The specimens IAvH-Am-17414–16 have the dorsal surfaces of the head, flanks, dorsum, front legs and vertebral band Orange-Rufous (56), strongly speckled with Raw Umber (280); paravertebral area, tail, and hind legs back Light-Yellow Ocher (13) with Raw Umber (280) dashes, and bordered with a wide Raw Umber (280) band; white stipples on the lateral surface of the head and back of the legs. The specimen IAvH-Am-17425 has the dorsal surfaces of the head, body, legs, and tail Dark Salmon (59), strongly speckled with Raw Umber (280), with greater concentration at the nape of the neck. Ventral markings or blotches on the ventral surfaces of the body and tail vary in shape and size; often with irregular margins but are consistently white or cream-colored independent of sex and age (Figs 5–7).

Figure 6. 

Chromatic variation of Bolitoglossa muisca in life. Notice some individuals bear white blotches on the ventral surfaces of the body and the tail. Photographs by YLP.

Figure 7. 

A non-captured individual of Bolitoglossa muisca from the surroundings of Reserva Chicaque, San Antonio del Tequendama, Cundinamarca, Colombia, photographed by JDF in October 2015. Notice the striking contrasting dark brown background coloration with ochre markings primarily on the dorsal surfaces of the body.

Etymology

Named after the native human inhabitants of the Altiplano Cundiboyacense and Sabana de Bogotá. The Muiscas regarded amphibians as sacred creatures associated with sex, fertility, and the arrival of the rainy season. The specific epithet is used as a noun in apposition.

Distribution

At present, Bolitoglossa muisca is known only from small cloud forest remnants on the western slopes of the Cordillera Oriental of Colombia in Bojacá, Granada, San Antonio del Tequendama, Silvania, and Soacha municipalities, Cundinamarca department. All specimens collected between 2390–2700 m a.s.l. (Fig. 2).

Natural history

Individuals from Bojacá municipality were regularly found at night on the base (on the mantillo) and leaves of Cyatheaceae ferns, which are dominant in the cloud forests of the Tequendama region of Cundinamarca department (Fig. 8). Most individuals from San Antonio del Tequendama municipality were found active at night perching on small branches of shrubs (Araceae and Melastomataceae), usually far away from rivers or streams. During the day, a few individuals were found inactive inside bromeliads below two meters height. When handled, these salamanders produced a sticky whiteish mucoserous substance; we consider this to be a defense mechanism against potential predators (Arrivillaga and Brown 2018). Two frog species (Pristimantis sp. and P. uisae) and a lizard (Anolis heterodermus) were found in sympatry with Bolitoglossa muisca; no other salamander species were found within our fieldwork area.

Figure 8. 

The Andean cloud forests of Bojacá, Cundinamarca, and the habitat of Bolitoglossa muisca. Photographs by YLP.

Other material examined

Countries are indicated in bold capitals, departments in regular capitals, municipalities, and localities in plain text. * Denotes specimens examined via photographs.

Bolitoglossa adspersa (n = 29). Colombia: Boyacá: Duitama, Páramo de la Rusia: ICN 4301, 4310; Toquilla, Páramo de Toquilla: ICN 9487. Cundinamarca: Bogotá, D.C., Páramo de Cruz Verde: IAvH-Am-8917, San Cristobal, Tánques de Vitelma, finca La Marranera: IAvH-Am-696, 2947, 2954, 2957-58, 2964, 2967, 2972, Usme, represa El Hato: ICN 37555; Cabrera: vereda de Hoyerías: IAvH-Am-13253 Fómeque, Laguna de Chingaza: ICN 4884, 4891; Guasca, Páramo de Guasca: ICN 4521, 4525, 4546; Fómeque, laguna Chingaza: ICN 4885; Fusagasugá, km 50 carretera Fusagasugá-La Florida: ICN 39096; Guatavita, vereda Montenquiva: IAvH-Am-13174–75, ICN 55420; Guayabetal: Páramo Atravezado: IAvH-Am-14808; Páramo de Palacio, P.N.N. Chingaza: IAvH-Am-3101, 3096, Quétame, km 22 carretera central Villavicencio-Alto del Tigre: ICN 7123; Ubaque, reserva ecológica Matarredonda: IAvH-Am-13254.

Bolitoglossa capitana (n = 4). Colombia: Cundinamarca: Albán, Granjas del Padre Luna: ICN 9221 & MLS 182–184*.

Bolitoglossa guaneae (n = 27). Colombia: Santander: Charalá, Virolín, Cañaverales, sector El Reloj: ICN 5197, 8555, 8557, 12770–72, 34230, Cuchilla del Fara: ICN 47980, Hacienda La Sierra: ICN 34229–30, km 56: ICN 19558, UIS-A 1369, UIS-A 2078, UIS-A 2082, UIS-A 2179, UIS-A 2317, UIS-A 2325–6, UIS-A 2891, UIS-A 2893, UIS-A 2895, UIS-A 2898–9, paratypes UIS-A 2203, UIS-A 2320, UIS-A 2324, UIS-A 2897.

Bolitoglossa muisca (n = 54). Colombia: Cundinamarca: Bojacá, vereda Roble Hueco, predio La Esmeralda: IAvH-Am-17413–22, Predio Peñas Blancas: IAvH-Am-17423–28; Granada, hacienda El Soche: ICN 3544–48, MVZ 167997*; San Antonio del Tequendama, vereda Roquemonte, cerca de entrada Parque Chicaque: ICN 60319–25; Silvania, vereda Noruega Alta, Hacienda La Tribuna: ICN 58245–58268; Soacha, vereda Cascajal: IAvH-Am-17429.

Bolitoglossa nicefori (n = 13). Colombia: Santander: Floridablanca, El Mortiño, quebrada Torrentosa: ICN 50000, 58227, 58231; Zapatoca, finca Los Puentes, quebrada Uchuvala: ICN 58223–24, 58226; Piedecuesta, vereda Los Monos: UIS-A 2987, UIS-A 2991; Los Santos, vereda El Carrizal, finca Utopía: UIS-A 5273–4; Guapotá, vereda Las Flores, finca La Chocolatera: UIS-A 5264; San Gil, vereda San José, finca La Esperanza: UIS-A 5270–1.

Bolitoglossa pandi (n = 20). Colombia: Cundinamarca: Pandi, vereda Buenos Aires Alta: ICN 45500, Supatá, vereda Las Lajas, reserva Cuzcungos: ICN 58492–05, Villeta, La Esmeralda: IAvH-Am-10303–08.

Discussion

Taxonomic background

Brame and Wake (1963: 44) examined a single specimen of Bolitoglossa from the Tequendama region of Cundinamarca (ICNB Tequendama), which was regarded as an undescribed species morphologically similar to B. adspersa. Despite finding diagnostic morphological differences between this specimen and those from B. adspersa, the limited sample size precluded any attempt by these authors to describe it as a new species. Our morphological and molecular results support Brame and Wake’s (1963) hypothesis. Through our conversations with Giovanni Chaves-Portilla we came across an unpublished manuscript written by the late David B. Wake and Arden H. Brame, dated sometime between the late 1980s and early 1990s (John D. Lynch pers. comm.), in which they proposed descriptions of three new Bolitoglossa from Colombia. One of these new species corresponds to Bolitoglossa muisca and is known from a site called Hacienda ‘El Soche’, Granada municipality, Cundinamarca department, Colombia, 2600 m a.s.l., i.e., from the same locality of MVZ 167997 (Fig. 1). Wake and Brame had planned to designate four types for this new species housed at Colección de Anfibios, Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá D.C., namely ICN 3544–46 and ICN 3550. We managed to examine these specimens and confirm them to be conspecific with Bolitoglossa muisca, but unfortunately these are not in the best condition and are therefore designated as referred material.

Phylogenetic status

Our taxonomic sampling indicates that Bolitoglossa muisca is sister to B. adspersa and both are reciprocally monophyletic (Fig. 1). These two species are close geographically and their genetic uncorrected p-distance for the 16S and cyt b (7.0%) fragments were relatively low (2.1 and 7%, respectively). Yet, lower distances between morphologically well-defined sister species of Bolitoglossa have been previously reported (Batista et al. 2014; Meza-Joya et al. 2017), with the smallest divergence reaching 0.5% for 16S (Parra-Olea et al. 2004). In addition, species delimitation analyses provided support to the distinctiveness of B. muisca as a new species.

Threats and conservation status

Deforestation, logging, and forest clearing are the main threats faced by the habitat of the new species in the remnant cloud forests of the Tequendama region in Cundinamarca department, Colombia. Nonetheless, the type locality of Bolitoglossa muisca is located within the regional protected area ‘Distrito de Manejo Integrado Cerro Manjui – Salto del Tequendama’, a conservation project led by Empresas Públicas de Medellín (EPM) and Fundación Natura that focuses on improving connectivity among cloud forests remnants of the Tequendama region. The calculated Extent of Occurrence (EOO) using the localities where the species is distributed is 102 km2 (estimate made with GeoCAT; Bachman et al. 2011). Bolitoglossa muisca is only known from an area of 102 km2 and only the type locality has a certain degree of protection. However, based on our results and field observation we consider that this species should be considered as Endangered (EN) using the IUCN criteria B1b(iii) of the IUCN, given its small known range (< 5000 km), and the current threats to its native habitat. The consequent loss of native vegetation may be causing the new species described here to be most likely threatened by habitat loss, and a monitoring program is warranted to better assess the current status of its few known populations (Liu et al. 2022).

Acknowledgements

For access to specimens and making available museum working space during our visits we thank Sandra Galeano (IAvH), John D. Lynch and Mauricio Rivera-Correa (ICN), and Fernando Sarmiento (MLS). Giovanni Chaves-Portilla provided clarification regarding the distribution patterns of various Bolitoglossa obtained during his fieldwork in western Cundinamarca and shared unpublished data with us. We thank Carlos Hernández for his invaluable laboratory assistance and Nelsy Pinto Sánchez, Martha Lucía Calderón, and Juan Carvajal Cogollo for kindly sharing their tissues and sequences with us. Sequencing was possible thanks to the funding provided by the Conservation Leadership Programme to FLMJ. We also thank Jorge Hernández, who kindly allowed us to use the equipment and space at his lab CINBIN. This project was funded by Empresas Públicas de Medellín (EPM) and Fundación Natura, Bogotá D.C., Colombia, via Acuerdo no. 894 of 2020; collection and research permits were granted by Autoridad Nacional de Licencias Ambientales de Colombia (ANLA), Resolución 0047-2015. The manuscript was greatly improved by comments and suggestions from Sean M. Rovito, Larry David Wilson, and Carlos Vásquez-Almazán.

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Appendix 1

Table A1.
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GenBank accession numbers of the Bolitoglossa and outgroup (*) sequences used in the phylogenetic analysis. Accession numbers in bold correspond to the new sequences presented in this paper. Subspecies and species group sensu Parra-Olea et al. (2004).

Species Subspecies Group 16S cyt b Rag–1 Voucher Locality
B. adspersa Eladinea adspersa OQ681031 OQ685920 – MLC348 Colombia: Cundinamarca, La Calera
B. adspersa Eladinea adspersa AF218492 AF212984 – MVZ 158485 Colombia: Cundinamarca, Ubaté
B. adspersa Eladinea adspersa OQ681032 – – N/A Colombia: Cundinamarca, Choachí
B. adspersa Eladinea adspersa OQ681033 – – DEQ4 Colombia: Santander, Sucre
B. altamazonica Eladinea adspersa MT301583 MT301731 MT301938 ORP 505 Peru: Loreto, near Nauta
B. altamazonica Eladinea adspersa MT301579 MT301799 MT301913 F 01 Peru: Loreto, near Nauta
B. awajun Eladinea adspersa MG944411 MG944420 MG944441 CRBIIAPAR1124 Peru: San Martín, San Martín, San Antonio, Cordillera Escalera
B. awajun Eladinea adspersa MG944412 MG944422 MG944442 CRBIIAPAR1125 Peru: San Martín, San Martín, San Antonio, Cordillera Escalera
B. biseriata Eladinea adspersa AY526118 AY526161 – S13236 Panamá: Kuna Yala, Nusagandi
B. biseriata Eladinea adspersa – AY526161 KC614436 MVZ 232943 Panamá: Kuna Yala, Nusagandi
B. caldwellae Eladinea adspersa AY526129 AY526168 – MPEG 12881 Brazil: Acre, Porto Walter
B. caldwellae Eladinea adspersa MT301584 – – CFBHT 54 Brazil: Acre, Serra do Divisor
B. chucantiensis Eladinea adspersa KM527324 – – SMF 97141 Panamá: Darién, Chepigana, Cerro Chucantí
B. equatoriana Eladinea adspersa MT301585 MT301789 – IIAP999 Peru: Loreto, Maynas, Curaray river
B. equatoriana Eladinea adspersa – DQ353842 KC614451 QCAZ 25448 Ecuador: Napo, Estación Biológica Jatun Sacha
B. guaneae Eladinea adspersa KU985264 KX458162 – UIS-A 5275 Colombia: Santander, Charalá, Virolín
B. guaneae Eladinea adspersa KU985265 KX458163 – UIS-A 5276 Colombia: Santander, Charalá, Virolín
B. hypacra Eladinea adspersa MT301588 – – SAS 446 Colombia: Antioquia, Paramo Frontino
B. hypacra Eladinea adspersa MT301589 – – SAS 447 Colombia: Antioquia, Paramo Frontino
B. leandrae Eladinea adspersa KC257102 – – MCNUP 63 Colombia: Norte de Santander, San Antonio
B. leandrae Eladinea adspersa MT301592 MT301732 MT301921 VVO 837 Colombia: Meta, Villavicencio
B. lozanoi Eladinea adspersa KU985266 KX458164 – H 3 Colombia: Santander, Floridablanca
B. lozanoi Eladinea adspersa KU985267 KX458165 – UIS-A 5269 Colombia: Santander, Girón
B. madeira Eladinea adspersa AY526128 AY526167 – LSUMZ-H 3086 Brazil: Amazonas, Ituxi river, Madeireira Scheffer
B. madeira Eladinea adspersa MT301594 MT301733 MT301895 MPEG 28601 Brazil: Acre: Fazenda Experimental Catuaba, Branco river
B. medemi Eladinea adspersa AY526123 AY526163 KC614437 S13237 Panamá: Kuna Yala, Nusagandi
B. medemi Eladinea adspersa KM527327 – – SMF 97131 Panamá: Darién, Serranía de San Blas
B. mucuyensis Eladinea adspersa JN635335 JQ665282 – CVULA 7100 Venezuela: Mérida, La Mucuy
B. mucuyensis Eladinea adspersa JN635336 – – CVULA 7101 Venezuela: Mérida, La Mucuy
B. nicefori Eladinea adspersa KX458176 KX458166 – UIS-A 5270 Colombia: Santander, San Gil
B. nicefori Eladinea adspersa KX458177 KX458167 – UIS-A 5271 Colombia: Santander, San Gil
B. orestes Eladinea adspersa JN635340 JQ665280 – CVULA 7109 Venezuela: Mérida, Sierra La Culata
B. orestes Eladinea adspersa JN635351 JQ665281 – MC00 Venezuela: Mérida, Sierra La Culata
B. palmata Eladinea adspersa AY526125 AY526164 – KU 217422 Ecuador: Napo, Cordillera de Guacamayos
B. palmata Eladinea adspersa MT301595 – MT301941 MZUTI 2220 Ecuador: Napo, Cordillera de los Guacamayos, La Virgen
B. paraensis Eladinea adspersa MT301596 – – CFBHT 20324 Brazil: Para, Moju, Moju river
B. paraensis Eladinea adspersa MT301597 MT301734 MT301892 MPEG 31672 Brazil: Para, Santa Izabel, Semente Etérea, Vila do Carapuru
B. peruviana Eladinea adspersa MG944408 MG944417 MG944436 CRBIIAP AR1118 Peru: Loreto, Alto Amazonas, Cordillera Escalera
B. peruviana Eladinea adspersa MT301600 MT301791 MT301900 CRBIIAP AR1038 Peru: Loreto, Alto Amazonas, Balsa Puerto, Shawi
B. muisca Eladinea adspersa AY526135 AY526173 – MVZ 167997 Colombia: Cundinamarca, El Soche
B. muisca Eladinea adspersa OQ681034 – – IAvH-Am-17414 Colombia: Cundinamarca, Bojacá
B. muisca Eladinea adspersa OQ681035 – – IAvH-Am-17417 Colombia: Cundinamarca, Bojacá
B. sima Eladinea adspersa AY526134 AY526172 – MVZ 2057 Colombia: Valle del Cauca
B. sp. ‘Chilma’ Eladinea adspersa – KC614431 KC614456 QCAZ 39981 Ecuador: Carchi, Chilma Bajo
B. sp. ‘Cisneros’ Eladinea adspersa MT301603 MT301735 MT301876 AFJ 006 Colombia: Valle del Cauca, Buenaventura, Cisneros, Los Turbos
B. sp. ‘Cisneros’ Eladinea adspersa MT301602 – – AFJ 010 Colombia: Valle del Cauca, Buenaventura, Cisneros, Los Turbos
B. sp. ‘Jingurudó’ Eladinea adspersa KM527329 – – MHCH 2663 Panamá: Darién, Chepigana, Serranía de Jingurudó
B. sp. ‘Llullapichi’ Eladinea adspersa MT301618 MT301741 MT301898 FGZC 4837 Peru, Huánuco, Panguana station, lower Llullapichis river
B. sp. ‘Llullapichi’ Eladinea adspersa MT301614 MT301739 MT301905 CORBIDI 14387 Peru: Huanuco, Puerto Inca, Llullapichis: Cordillera del Sira
B. sp. ‘Pensilvania’ Eladinea adspersa MT301607 MT301793 MT301917 GGD 640 Colombia: Caldas, Pensilvania, road to Arboleda
B. sp. ‘Pirinari’ Eladinea adspersa MT301700 – – MUBI 10081 Peru: Loreto, Parinari, Hamburgo, Samiria river
B. sp. ‘Pirinari’ Eladinea adspersa MT301701 MT301778 MT301885 MUBI 10099 Peru: Loreto, Parinari, Pithecia, Samiria river
B. sp. ‘Salamina’ Eladinea adspersa MT301606 MT301736 MT301875 GGD 111 Colombia: Caldas, Salamina, Tribunas farm
B. sp. ‘Sanare’ Eladinea adspersa MT301608 MT301737 MT301926 MOE 01 Venezuela: Lara, Sanare, El Blanquito, Yacambu National Park
B. sp. Eladinea adspersa MT301604 MT301792 – DQ 175 Venezuela
B. sp. Eladinea adspersa MT301605 – MT301871 DQ 177 Venezuela
B. tamaense Eladinea adspersa KC257098 – – MCNUP 56 Colombia: Norte de Santander, Los Remansos
B. tamaense Eladinea adspersa KC257099 – – MCNUP 57 Colombia: Norte de Santander, Los Remansos
B. tapajonica Eladinea adspersa MT301711 MT301802 MT301933 MPEG 31688 Brazil: Para, Juruti
B. tapajonica Eladinea adspersa MT301712 MT301786 MT301934 MPEG 31695 Brazil: Para, Lorena
B. taylori Eladinea adspersa KM527337 – – AB 171 Panamá: Darién, Pinogana, Serranía de Pirre
B. taylori Eladinea adspersa KM527335 – – AB 173 Panamá: Darién, Pinogana, Serranía de Pirre
B. vallecula Eladinea adspersa MT301713 MT301787 MT301874 AFJ 48 Colombia: Valle del Cauca, El Cairo, Cerro del Inglés
B. walkeri Eladinea adspersa MT301714 MT301788 MT301873 AFJ 02 Colombia: Valle del Cauca, Cali, San Antonio
B. walkeri Eladinea adspersa MT301715 – – AFJ 03 Colombia: Valle del Cauca, Cali, San Antonio
B. yariguiensis Eladinea adspersa KU985275 KX458173 – UIS-A 5280 Colombia: Santander, San Vicente de Chucurí
B. yariguiensis Eladinea adspersa KU985276 KX458174 – UIS-A 5281 Colombia: Santander, San Vicente de Chucurí
B. cerroensis* Eladinea epimela AF199233 AF199195 KC614459
B. epimela* Eladinea epimela AY526120 AF212097 –
B. minutula* Eladinea epimela AY526124 AF212098 KC614434
B. nigrescens* Eladinea schizodactyla JQ899164 JQ899194 –
B. robusta* Eladinea schizodactyla EU448109 EU448110 –
B. schizodactyla* Eladinea schizodactyla AY526133 AY526171 –
B. splendida* Eladinea subpalmata JQ899150 JQ899181 –
B. subpalmata* Eladinea subpalmata AF416697 AF212094 –
B. tica* Eladinea subpalmata JQ899162 JQ899192 –
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