Research Article |
Corresponding author: Adolfo Amézquita ( aamezquita@bioconservancy.org ) Corresponding author: Juan M. Daza ( jumadaza@gmail.com ) Academic editor: Anthony Herrel
© 2023 Adolfo Amézquita, Luis A. Mazariegos-H, Santiago Cañaveral, Catalina Orejuela, Leidy Alejandra Barragán-Contreras, Juan M. Daza.
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:
Amézquita A, Mazariegos-H LA, Cañaveral S, Orejuela C, Barragán-Contreras LA, Daza JM (2023) Species richness under a vertebral stripe: integrative taxonomy uncovers three additional species of Pholidobolus lizards (Sauria, Squamata, Gymnophthalmidae) from the north-western Colombian Andes. ZooKeys 1141: 119-148. https://doi.org/10.3897/zookeys.1141.94774
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The systematic study of biodiversity underlies appropriate inference in most other fields of biological research, yet it remains hampered by disagreements on both theoretical and empirical issues such as the species concept and the operational diagnosis of a species. Both become particularly challenging in those lineages where morphological traits are evolutionarily constrained by their adaptive value. For instance, cryptic organisms often conserve or converge in their external appearance, which hinders the recognition of species boundaries. An integrative approach has been adopted to study microgeographic variation in the leaf-litter lizard Pholidobolus vertebralis and test three predictions derived from the evolutionary species concept. Molecular data provided unambiguous evidence of divergence among the three recovered new clades and a common evolutionary history for each of them. The broadly sympatric clades were indeed diagnosable from externally visible traits, such as head scales, adult size, and sexually dimorphic ventral colouration. Also, they barely overlapped on the phenotypic space that summarised 39 morphometric and meristic traits. These clades are described as three species and an available name is suggested for a recovered fourth clade. The geographic distribution of the new and proximate species suggests a role for elevation on evolutionary divergence; it also raises interesting questions on the speciation pattern of an otherwise underestimated cryptic lineage.
Cryptic species, elevation, leaf-litter lizards, phenotypic space, tropical Andes
The external appearance of many animal species is known to reduce the probability of being detected against natural backgrounds, which arguably impedes eventual predation at its earliest stage: detection (
Lizards in many species bear a mid-dorsal vertebral stripe or line. It presumably contributes to conceal them against the leaf litter or vegetation, by mimicking the petiole and midrib of dead leaves, and thereby breaking their body silhouettes to the eyes of potential predators (
The neotropical lizards in the genus Pholidobolus (Gymnophthalmidae) are distributed throughout the mid to high elevation Andes, from northern Peru and throughout Ecuador up to Colombia (
To conduct phylogenetic and morphometric analyses, we collected specimens along the northern half of the Colombian Western Andes (Cordillera Occidental), and in the northern extreme of the Colombian Central Andes (Cordillera Central), at elevations between 1400–3100 m (Suppl. material
To build a phylogenetic hypothesis including the studied lizards, we extracted DNA from liver and muscle samples. Lizards were previously euthanised with an overdose of lidocaine and most of them were photographed, in dorsal and ventral views, against a standard white background. They were afterwards fixed in 10% formalin, and finally stored in 70% ethanol. We extracted DNA using either the Qiagen DNeasy or the GeneJET genomic DNA purification kits and following the standard manufacturer’s protocols for tissue samples. We assembled a molecular matrix including four genomic regions: three mitochondrial and one nuclear region. A fragment of the 12S ribosomal gene was amplified using the primers 12Sa and 12Sb (
We aligned each region using MAFFT under default parameters (
We examined and measured 101 individuals. To record meristic traits, we followed definitions for Pholidobolus lizards originally proposed by
To test whether the recovered lineages could be differentiated from the combined set of meristic and morphometric traits, we conducted discriminant analysis coupled to principal component analysis, DAPC (
Male ventral colouration differed at first sight among the clades. To visualise and validate photographic comparisons of the colour hues, we took ventral pictures of both males and females, and adjusted them for white balance using the plugin Auto White Balance Correction Master on the software FIJI (
The hemipenes of two of the three defined holotypes were extracted following
The reconstructed phylogenetic hypothesis (Fig.
Molecular phylogenetic hypothesis. Recovered relationship between species of the leaf-litter lizards in the genus Pholidobolus, including P. vertebralis near its type locality in Ecuador. The three recovered clades from the Colombian Western Andes are outlined in blue (clade A), orange (clade B) and yellow (clade D). A fourth clade of the Colombian Central Andes is outlined in green (clade C). Green dots indicate nodal support of at least 95%. See Methods for further details on the phylogenetic analysis and Suppl. material
The distribution of pairwise genetic distances was clearly discontinuous among the lineages with adjacent, parapatric or overlapping distribution in the north-western Colombian Andes: much shorter among individuals of the same recovered clade than among individuals of different clades (Fig.
Genetic distances. Average uncorrected genetic distances among the species of Pholidobolus with adjacent, parapatric or overlapping distributions in the north-western Colombian Andes. The species to which some of these individuals had been formerly added, P. vertebralis is added for comparison.
Species | Pa | Pc | Pm | Po | Pp | Pv |
---|---|---|---|---|---|---|
P. argosi sp. nov. | 0.066 | 0.066 | 0.065 | 0.060 | 0.047 | |
P. celsiae sp. nov. | 0.066 | 0.029 | 0.027 | 0.060 | 0.014 | |
P. marianus | 0.066 | 0.029 | 0.028 | 0.061 | 0.021 | |
P. odinsae sp. nov. | 0.065 | 0.027 | 0.028 | 0.058 | 0.017 | |
P. paramuno | 0.060 | 0.060 | 0.061 | 0.058 | 0.040 | |
P. vertebralis | 0.047 | 0.014 | 0.021 | 0.017 | 0.040 |
Within and among clades genetic distances. Distribution of uncorrected 16S genetic distances among individuals of leaf-litter lizards in the genus Pholidobolus. We include four species of the northern Colombian Andes, and P. vertebralis near its type locality in Ecuador. Pairwise distances among individuals of the same clade are indicated with the same colour; pairwise distances among individuals from different clades are represented by different colours. Dots denote each of the calculated distances, whose distribution is summarised by Kernel density smooths.
The three clades of the Colombian Western Andes (Clades A / B / D in Fig.
Key morphological features of the three new species on the holotypes. External morphological traits allowing unambiguous diagnosis of the three north-western Colombian clades of Pholidobolus lizards recovered in our phylogenetic analysis. Pholidobolus argosi sp. nov. lacks one supraocular (numbered) and the prefrontal (filled in red) scales, both of which are present in the other two species. Males of P. odinsae sp. nov. exhibit predominantly black and dark grey ventral colouration, which is red with black markings in males of the two other species, as further shown by the image segmentation analyses: the stacked areas denote the proportion of pixels with each summarised hue. Lastly, P. celsiae sp. nov. reaches larger adult body size than the other two species, as evidenced by blue (clade A in Fig.
Regarding the whole set of morphometric and meristic traits, the first cross-validation analysis indicated that seven principal components summarised enough variation as to attempt phenotypic discrimination and classification of individuals. The existence of near discrete clades was further supported by the scatter of individuals throughout the phenotypic space created by the two first discriminant axes (Fig.
Discriminant and classification analysis based on lizard morphology. Classification analysis of lizards in four species of Pholidobolus based on the whole set of meristic and morphometric traits A distribution of individuals (dots) of the recovered phylogenetic clades (colours) in the two-dimensional phenotypic space created by the discriminant analysis of principal components (DAPC) summarising all traits B actual (dot colour) and predicted (bar colour) membership of each lizard (museum identity) to the recovered clades; predicted membership is estimated from the DAPC and represents the probability of assignment of each lizard to one or more lineages (colours). See Methods for further detail on the underlying statistical analyses.
Regarding sexual dimorphism, males had wider heads than expected from their body size, though the pattern could not be corroborated in one clade due to the capture of a single female (Fig.
Sexual dimorphism in the lizard head width. Relationship between head width and body size across four species of Pholidobolus lizards. Males exhibit disproportionally wider heads compared to females. Only one female was available for P. celsiae sp. nov. Lines denote linear regression, and the coloured shadows indicate the 95% confidence interval of the line slope. Non-overlapping blue and red shadows represent significant differences in the slope of the head width to body size relationship, between males and females.
Variation in lizard ventral colouration. Among-species, among-sexes, and among-individuals variation in ventral colouration of three lizard species in the genus Pholidobolus. Pictures were taken immediately after euthanisation to reflect colour in life. To depict eventual covariation with body size, individuals are sorted from the smallest (extremes) to the largest (middle) one.
During this and parallel studies, all but one individual were captured at altitudes above 1500 m and up to 3100 m. They were thus absent in the lower elevation valley of the Cauca River, which separates the Western and Central Andean chains of Colombia. Among-clades differences in distribution were thus best described in terms of Andean chain and elevation. One clade (clade C in Fig.
Geographic and altitudinal distribution. Geographic (A) and altitudinal (B) distribution of five species of Pholidobolus lizards across the north of the Western and Central Colombian Andes. The cladogram summarises the recovered phylogenetic relationship among them (Fig.
Based on the collected samples and evidence, we recognise the existence of four phylogenetically independent lineages. A name is available for the specimens from the northern Central Andes (Cordillera Central) in Colombia (Clade C in Fig.
The specimens of the Colombian Western Andes (Cordillera Occidental) were grouped into three diagnosable (Fig.
Holotype. (Figs
Type series. Identity, sex and geographic location of type specimens of the three new species of Pholidobolus lizards described here.
Species | Voucher | Type | Field code | Sex | Locality | Elev (m) | GPS coordinates |
---|---|---|---|---|---|---|---|
P. argosi | MHUAR13905 | holotype | AA7058 | male | MPNR | 2500 | 5°29.92'N, 75°54.27'W |
P. argosi | MHUAR12011 | paratype | juvenile | Santa Rita | 2730 | 5°34.75'N, 75°57.68'W | |
P. argosi | MHUAR12012 | paratype | male | Santa Rita | 2730 | 5°34.75'N, 75°57.68'W | |
P. argosi | MHUAR13851 | paratype | AA7010 | male | MPNR | 2500 | 5°29.92'N, 75°54.27'W |
P. argosi | MHUAR13852 | paratype | AA7014 | male | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13853 | paratype | AA7017 | female | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13854 | paratype | AA7039 | male | MPNR | 2500 | 5°29.92'N, 75°54.27'W |
P. argosi | MHUAR13855 | paratype | AA7048 | male | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13856 | paratype | AA7049 | male | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13857 | paratype | AA7050 | male | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13858 | paratype | AA7051 | female | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13859 | paratype | AA7052 | female | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13860 | paratype | AA7053 | male | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13861 | paratype | AA7054 | female | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13862 | paratype | AA7055 | female | MPNR | 2740 | 5°29.54'N, 75°54.31'W |
P. argosi | MHUAR13863 | paratype | AA7059 | male | MPNR | 2500 | 5°29.92'N, 75°54.27'W |
P. argosi | MHUAR13864 | paratype | AA7066 | male | MPNR | 2840 | 5°28.76'N, 75°54.37'W |
P. argosi | MHUAR13865 | paratype | AA7067 | male | MPNR | 2840 | 5°28.76'N, 75°54.37'W |
P. argosi | MHUAR13866 | paratype | AA7068 | male | MPNR | 2840 | 5°28.76'N, 75°54.37'W |
P. argosi | MHUAR13867 | paratype | AA7179 | female | MPNR | 2500 | 5°29.92'N, 75°54.27'W |
P. argosi | MHUAR13868 | paratype | AA7180 | male | MPNR | 2490 | 5°29.39'N, 75°51.35'W |
P. argosi | MHUAR13869 | paratype | AA7181 | male | MPNR | 2840 | 5°28.76'N, 75°54.37'W |
P. celsiae | MHUAR13906 | holotype | AA7061 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13148 | paratype | juvenile | Mampay | 1720 | 5°21.51'N, 75°52.91'W | |
P. celsiae | MHUAR13520 | paratype | male | La Suiza | 1830 | 4°43.93'N, 75°35.09'W | |
P. celsiae | MHUAR13870 | paratype | AA7002 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13871 | paratype | AA7056 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13872 | paratype | AA7057 | female | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13873 | paratype | AA7069 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13874 | paratype | AA7070 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13875 | paratype | AA7071 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13876 | paratype | AA7072 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13877 | paratype | AA7073 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13878 | paratype | AA7074 | female | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13879 | paratype | AA7161 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. celsiae | MHUAR13880 | paratype | AA7172 | male | MPNR | 1900 | 5°28.01'N, 75°53.44'W |
P. odinsae | MHUAR13907 | holotype | AA7090 | male | MPNR | 2180 | 5°29.76'N, 75°53.35'W |
P. odinsae | MHUAR12574 | paratype | male | Santa Rita | 2150 | 5°35.52'N, 75°57.15'W | |
P. odinsae | MHUAR12584 | paratype | juvenile | Quebradona | 2240 | 5°45.38'N, 75°43.37'W | |
P. odinsae | MHUAR12986 | paratype | juvenile | La Isla | 1730 | 5°51.50'N, 76°9.73'W | |
P. odinsae | MHUAR13883 | paratype | AA7009 | male | MPNR | 1920 | 5°31.62'N, 75°51.75'W |
P. odinsae | MHUAR13884 | paratype | AA7011 | female | MPNR | 1920 | 5°31.62'N, 75°51.75'W |
P. odinsae | MHUAR13885 | paratype | AA7012 | female | MPNR | 1920 | 5°31.62'N, 75°51.75'W |
P. odinsae | MHUAR13886 | paratype | AA7013 | male | MPNR | 2300 | 5°31.13'N, 75°51.74'W |
P. odinsae | MHUAR13887 | paratype | AA7015 | male | MPNR | 1920 | 5°31.62'N, 75°51.75'W |
P. odinsae | MHUAR13888 | paratype | AA7016 | female | MPNR | 2210 | 5°29.62'N, 75°53.40'W |
P. odinsae | MHUAR13889 | paratype | AA7019 | juvenile | MPNR | 2300 | 5°31.13'N, 75°51.74'W |
P. odinsae | MHUAR13898 | paratype | AA7182 | female | MPNR | 2310 | 5°29.46'N, 75°53.33'W |
P. odinsae | MHUAR13899 | paratype | AA7183 | female | MPNR | 2310 | 5°29.46'N, 75°53.33'W |
P. odinsae | MHUAR13904 | paratype | AA7188 | male | MPNR | 2230 | 5°30.96'N, 75°50.63'W |
Paratypes. Fourteen males, six females, and one juvenile. Table
The species can be diagnosed combining the following characters: (1) two supraocular scales; (2) prefrontal scales absent; (3) 9–17 temporal scales; (4) dorsal scales keeled; (5) 28–32 transverse rows of dorsal scales; (6) 20–22 transverse rows of ventral scales; (7) 26–35 scales around mid-body; (8) 1–2 (usually 1) rows of lateral scales; (9) lateral and medial ventral scales equal in size; (10) 0–5 femoral pores; (11) no sexual dimorphism in number of femoral pores; (12) labial scales pale, often crossed dorsally by a longitudinal white stripe bordered with black; (13) ventral head colouration paler towards the anterior end; (14) cream or white vertebral stripe bordered by two black stripes, originating on the rostral scale, completely covering the dorsal region of the head and the vertebral region of the body, reaching only the anterior portion of the tail, with maximum width of four scales on the body; (15) lateral colour brown, orange towards the shoulders and anterior part of the tail, with some ocelli, usually less than seven between limbs insertions, each white in centre and surrounded by black scales, with a longitudinal white line in the head, pale and discontinuous towards the body; (16) venter pink to pale orange, with few black markings in females; vivid orange with much more and much larger black markings in adult males; (17) subcylindrical and bilobed hemipenial body with 6–8 and 7–9 rows of spinulated flounces in the lateral columns of the sulcate and asulcate sides, respectively; (18) lateral columns of spinulated flounces connecting in the proximal region of the asulcate side.
Pholidobolus vertebralis differs from P. argosi sp. nov. (character states in parenthesis) in having the lateral ventral scales smaller than the medial ventrals (lateral and medial ventral scales equal in size). The other species from the north-western and central Colombian Andes (Fig.
Meristic and morphometric traits. Summary of meristic and morphometric (in mm) traits in adult lizards of the four clades of Pholidobolus studied here. Mean ± sd (min – max).
Trait | P. argosi sp. nov. (n = 21) | P. celsiae sp. nov. (n = 11) | P. marianus comb. nov. (n = 24) | P. odinsae sp. nov. (n = 35) |
---|---|---|---|---|
Prefrontals | 0 ± 0 (0–0) | 2.0 ± 0.0 (2–2) | 2.0 ± 0.0 (2–2) | 2.0 ± 0.0 (2–2) |
Supraoculars | 2.0 ± 0.0 (2–2) | 3.0 ± 0.0 (3–3) | 3.4 ± 0.5 (3–4) | 3.0 ± 0.2 (3–4) |
Superciliaries | 3.9 ± 0.4 (3–5) | 3.9 ± 0.3 (3–4) | 3.7 ± 0.6 (3–5) | 4.0 ± 0.2 (3–5) |
Lower palpebrals | 3.9 ± 0.7 (2–5) | 4.4 ± 0.7 (3–5) | 5.4 ± 1.1 (4–7) | 3.9 ± 0.8 (2–5) |
Suboculars | 4.1 ± 0.6 (3–5) | 4.9 ± 0.9 (4–6) | 3.9 ± 0.8 (3–6) | 5.2 ± 1.1 (3–7) |
Postoculars | 2.0 ± 0.0 (2–2) | 2.1 ± 0.3 (2–3) | 2.9 ± 0.6 (2–4) | 2.2 ± 0.5 (2–4) |
Temporal | 12.5 ± 1.8 (9–17) | 21.8 ± 4.8 (14–28) | 13.8 ± 2.7 (10–19) | 19.9 ± 3.3 (11–26) |
Supralabials | 6.9 ± 0.4 (6–8) | 7.2 ± 0.4 (7–8) | 6.9 ± 0.5 (6–8) | 7.1 ± 0.4 (7–8) |
Infralabials | 5.6 ± 0.6 (5–7) | 4.6 ± 0.7 (4–6) | 4.9 ± 0.7 (3–6) | 4.8 ± 0.7 (4–6) |
Pregulars | 2.1 ± 0.2 (2–3) | 2.4 ± 0.5 (2–3) | 3.8 ± 0.9 (2–6) | 2.3 ± 0.6 (2–4) |
Gulars | 7.1 ± 0.4 (6–8) | 7.6 ± 0.5 (7–8) | 7.9 ± 1.3 (4–10) | 8.1 ± 0.6 (7–9) |
Collar scales | 10.3 ± 1.5 (7–13) | 11.2 ± 1.6 (9–14) | 10.3 ± 1.7 (6–13) | 10.9 ± 2.0 (6–17) |
Dorsal transverse | 30.1 ± 1.0 (28–32) | 29.5 ± 0.9 (28–31) | 30.3 ± 1.2 (28–32) | 29.9 ± 1.0 (28–32) |
Dorsal longitudinal | 18.8 ± 1.2 (17–21) | 24.9 ± 1.0 (23–26) | 22.3 ± 1.9 (19–26) | 22.5 ± 2.0 (20–26) |
Around mid-body | 31.3 ± 2.3 (26–35) | 39.6 ± 1.5 (37–43) | 35.9 ± 2.6 (30–42) | 38.4 ± 3.4 (31–45) |
Transversal ventral | 21.1 ± 0.7 (20–22) | 19.6 ± 1.0 (18–21) | 21.2 ± 1.2 (19–24) | 19.8 ± 1.2 (17–23) |
Head width | 8.70 ± 1.20 (6.6–11.3) | 11.89 ± 1.20 (7.4–14.6) | 7.53 ± 0.98 (5.9–9.7) | 8.02 ± 1.02 (6.0–10.0) |
Head length | 11.77 ± 1.79 (9.1–15.0) | 15.05 ± 2.46 (10.4–17.9) | 10.66 ± 1.56 (7.6–14.5) | 11.24 ± 1.39 (8.6–15.0) |
Head height | 6.13 ± 0.87 (5.0–7.7) | 8.44 ± 1.51 (5.2–9.7) | 5.32 ± 0.71 (3.9–7.1) | 5.41 ± 0.63 (4.2–6.7) |
Jaw length | 9.51 ± 1.42 (7.2–13.2) | 12.77 ± 1.56 (9.4–14.5) | 10.15 ± 1.88 (7.1–14.1) | 9.67 ± 1.50 (7.4–13.2) |
Longest finger | 5.25 ± 0.58 (4.1–6.4) | 5.80 ± 0.79 (4.7–6.8) | 4.75 ± 0.47 (4.0–5.6) | 4.72 ± 0.63 (3.9–6.3) |
Pelvis width | 6.57 ± 0.70 (4.8–7.6) | 8.60 ± 1.01 (6.2–9.6) | 6.57 ± 0.91 (4.2–7.9) | 6.67 ± 0.97 (4.9–8.9) |
Longest toe | 8.13 ± 0.77 (6.8–10.2) | 9.42 ± 0.90 (7.4–10.2) | 7.19 ± 0.65 (5.7–8.2) | 7.19 ± 1.06 (5.3–10.8) |
Tail width | 5.50 ± 0.59 (4.3–6.6) | 7.61 ± 1.42 (5.1–9.5) | 4.97 ± 0.60 (4.1–6.1) | 5.69 ± 0.97 (3.9–8.1) |
Snout-vent length | 50.85 ± 4.23 (42.6–57.9) | 62.38 ± 7.19 (45.0–68.6) | 46.97 ± 4.81 (35.6–55.8) | 48.36 ± 5.71 (35.4–60.3) |
Adult male; snout-vent length 57.5 mm; tail length 111.0 mm; other body measurements can be found in Table
Holotypes. Sex, body measurements (in mm), and voucher identity of the holotypes of the new lizard species describe herein.
Trait | P. argosi sp. nov. | P. celsiae sp. nov. | P. odinsae sp. nov. |
---|---|---|---|
Sex | male | male | male |
Snout-vent length | 57.5 | 68.2 | 54.2 |
Head length | 14.9 | 16.6 | 11.2 |
Head width | 11.3 | 14.6 | 8.8 |
Head height | 7.6 | 9.7 | 6.3 |
Jaw length | 10.5 | 12.8 | 10.9 |
Length of the longest finger | 6.4 | 6.1 | 4.9 |
Length of the longest toe | 8.8 | 10.0 | 7.4 |
Pelvis width | 7.6 | 9.6 | 6.3 |
Tail length | 111.0 | 79.0 | 50.0 |
Tail width | 6.4 | 9.5 | 5.0 |
Limbs pentadactyl with clawed fingers. Dorsal brachial and antebrachial scales lanceolate to polygonal, longer than wide, imbricate and smooth. Ventral brachial and antebrachial scales lanceolate to polygonal, almost as long as wide, juxtaposed, much smaller than the dorsal ones. Dorsal hand scales hexagonal, wider but shorter than the dorsal antebrachial scales. Finger length formula IV > III > II > V > I. Supradigital scales quadrangular, imbricate and wider than long. Palmar scales polygonal, juxtaposed, and small. Subdigital lamellae domelike with a quadrangular base, and often divided longitudinally, with six on finger I, 10 on II, 12 on III, 15 on IV, and 10 on V. Thigh scales on the dorsal, anterior and ventral surfaces lanceolate to rhomboidal, longer than wide, those in the dorsal surface smooth and the others smooth and imbricate. Thigh scales on the posterior surface of the legs rounded, smooth, juxtaposed and much smaller than those of the anterior and dorsal surfaces. Five femoral pores per leg; preanal pores absent. Anterior and ventral crus scales polygonal and smooth. Lateral and posterior crus scales rounded, small and subimbricate. Toe length formula IV > III > V > II > I. Supradigital scales quadrangular, imbricate and longer than wide. Plantar scales polygonal, juxtaposed and small. Subdigital lamellae domelike with a quadrangular base, and often divided longitudinally, with six on Toe I, 10 on II, 16 on III, 20 on IV, and 11 on V.
In life, dorsally brown, bisected by a mid-dorsal (i.e. vertebral) cream, pale brown, or white stripe, extending from the head to the base of the tail; vertebral stripe bordered with darker, usually black, stripes; on the head, the pale stripe extends from the first supralabial to the shoulder dorsally reaching the rostral scale, and laterally bordering the supraocular and parietal scales; sides of neck, flanks, and limbs predominantly brown, usually with less than ten white ocelli, bordered by a black stripe; white or cream lateral line from the supralabials to the shoulder; cream and interrupted lateral stripe, running between the insertions of fore and hind limbs, not extending towards the tail; scattered red scales, more common and grouped above the shoulder and along the lateral surface of the tail; throat pink to cream; chest, belly and base of the tail pink to pale orange, often with black blotches, apparently more common in adult males (Figs
The species epithet is dedicated to the Grupo Argos Foundation, for their commitment to sustainable development, and their voluntary actions directed to education and environmental restoration. Through its program “Sembrando Futuro”, they promote the conservation and recovery of water resources, depleted gallery forests, mangroves, and the habitat of the spectacled bear, an umbrella species for the conservation of entire Andean ecosystems.
The species is currently known from the hilltops of the western Andes, near the municipalities of Andes and Caramanta, within the department of Antioquia. Most specimens were seen amongst the leaf litter of elfin forests; some were collected on secondary forests at the edge of cloud forests. The observed specimens appeared clearly heliothermic: within minutes after the sun appeared, they came out of the leaf litter, remained exposed, and extended their ribs increasing the dorsal surface available for sunlight capture. Under sunny conditions, several individuals could be seen at once in at least two of the spots from where the species is known. Its distribution seems thus to be very patchy, known presently from fewer than five locations and in any case less than 500 km2 (Fig.
Holotype. Adult male, with genitalia in a separate microvial. Original label: AA_7061. Museum ID: MHUA-R13906. Type locality in Colombia, Risaralda: Municipality of Mistrató, 5°28.01'N, 75°53.44'W, secondary forest, under rocks, 7 October 2020. Collected by Ubiel Rendón and Luis A. Mazariegos-H.
Paratypes. Eleven males, two females, and one juvenile. Table
The species can be diagnosed combining the following characters: (1) three supraocular scales; (2) prefrontal scales present; (3) 14–28 temporal scales; (4) dorsal scales keeled; (5) 28–32 transverse rows of dorsal scales; (6) 18–21 transverse rows of ventral scales; (7) 36–44 scales around mid-body; (8) 1–3 rows of lateral scales; (9) lateral and medial ventral scales equal in size; (10) 5–6 femoral pores; (11) no sexual dimorphism in number of femoral pores; (12) labial scales pale, often with black markings; (13) ventral head colouration homogeneous in females; with irregular orange or black markings, and paler towards the anterior half in males; (14) white to cream vertebral stripe bordered by two black stripes, originating on the rostral scale, completely covering the dorsal region of the head and the vertebral region of the body, reaching only the anterior portion of the tail, with maximum width of two scales on the body; (15) lateral colour pattern brown and dark orange to red, with numerous ocelli, usually more than seven between the limbs insertions, white in centre and surrounded by black scales, with a longitudinal pale line laterally, continuous and white in the head, pale and discontinuous towards the body; (16) venter pink to pale orange, or brown, with darker marking towards the edge of scales in females; vivid orange to red, with scattered black markings towards the edge of scales in males; (17) subcylindrical and bilobed hemipenial body with 4–5 and 7–9 rows of spinulated flounces in the lateral columns of the sulcate and asulcate sides, respectively; (18) lateral columns of spinulated flounces connecting in the distal region of the asulcate side.
Pholidobolus vertebralis differs from P. celsiae sp. nov. (character states in parenthesis) in having the lateral ventral scales smaller than the medial ventrals (lateral and medial ventral scales equal in size). The other species from the north-western and central Colombian Andes (Fig.
Adult male; snout-vent length 68.2 mm; tail length 79.0 mm; other body measurements in Table
Limbs pentadactyl with clawed fingers. Dorsal brachial and antebrachial scales lanceolate to polygonal, almost as long as wide, imbricate and smooth. Ventral brachial and antebrachial scales lanceolate to polygonal, almost as long as wide, juxtaposed, much smaller than the dorsal ones. Dorsal hand scales hexagonal, wider but shorter than the dorsal antebrachial scales. Finger length formula IV = III > II > V > I. Supradigital scales quadrangular and imbricate. Palmar scales polygonal, juxtaposed and small. Subdigital lamellae domelike with a quadrangular base, and often divided longitudinally, with four on finger I, 8 on II, 12 on III, 13 on IV, and 7 on V. Thigh scales on the dorsal, anterior and ventral surfaces lanceolate to rhomboidal, longer than wide, those in the dorsal surface keeled and the others smooth and imbricate. Thigh scales on the posterior surface of the legs rounded, smooth, juxtaposed and much smaller than those of the anterior and dorsal surfaces. Five femoral pores per leg; preanal pores absent. Anterior and ventral crus scales polygonal and keeled. Lateral and posterior crus scales rounded, small and subimbricate. Toe length formula IV > III > II > IV > I. Supradigital scales quadrangular, imbricate and longer than wide. Plantar scales polygonal, juxtaposed and small. Subdigital lamellae domelike with a quadrangular base, and often divided longitudinally, with four on Toe I, 8 on II, 13 on III, 15 on IV, and 9 on V. Thigh scales on the dorsal, anterior and ventral surfaces lanceolate to rhomboidal, longer than wide, those in the dorsal surface keeled and the others smooth and imbricate. Thigh scales on the posterior surface of the legs rounded, smooth, juxtaposed and much smaller than those of the anterior and dorsal surfaces. Five femoral pores per leg; preanal pores absent. Anterior and ventral crus scales polygonal and keeled. Lateral and posterior crus scales rounded, small and subimbricate. Toe length formula IV > III > V > II > I. Supradigital scales quadrangular, imbricate and longer than wide. Plantar scales polygonal, juxtaposed and small. Subdigital lamellae domelike with a quadrangular base, and often divided longitudinally, with seven on I, nine on II, 13 on III, 18 on IV, and 10 on V.
In life, dorsally dark brown, bisected by a mid-dorsal (i.e. vertebral) cream, or white stripe, extending from the head to the base of the tail; vertebral stripe bordered with darker, usually black, stripes; on the head, the pale stripe extends from the first supralabial to the shoulder dorsally reaching the rostral scale, and laterally not in contact with the supraocular and parietal scales; sides of neck, flanks, and limbs predominantly brown; neck, flanks and tail base usually with more than 10 white ocelli, bordered by a black stripe; white or cream lateral line from the supralabials to the shoulder; cream and interrupted lateral stripe, running between the insertions of fore and hind limbs, not extending towards the tail; many red scales, more common in males and grouped above the shoulder and along the lateral surface of the tail; throat cream to pale brown in males, paler towards the anterior extreme; throat pink in females; chest, belly and base of the tail cream to pink in females, but orange in males, often with black blotches, apparently more common in adult males (Figs
The species epithet is dedicated to the Celsia Foundation, for their voluntary contribution to the restoration of cloud and dry forests in the tropical Andes, through their reforestation program Reverde-C, which already planted more than one million trees. In addition, their program for children education in rural areas, already benefited more than 16000 students in terms of school infrastructure, teacher training, and further logistic support during the Covid pandemic. We believe their commitment contributes to the well-being and education of direct neighbours and thereby stakeholders of Colombian protected nature.
The specimens were mostly collected in open areas with secondary vegetation, at the edge of a cloud forest. Groups of up to nine eggs were found together with adult individuals under a rock, suggesting communal nesting. Also, the observed specimens appeared clearly heliothermic: within minutes after the sun appeared, they came out of their refuges, remained exposed, and extended their ribs increasing the dorsal surface available for sun basking. The species is currently known from three localities, two of them within protected areas: the Mesenia-Paramillo Nature Reserve, and the Santuario de Flora y Fauna (SFF) Otún-Quimbaya. Further explorations are needed to ascertain the species distribution. In the meantime, we suggest listing the new species as Endangered EN B1ab(iii), B2ac(iii), under the IUCN criteria (
Holotype. (Figs
Paratypes. Six males, five females, and three juveniles. Table
The species can be diagnosed combining the following characters: (1) 3–4 (usually 3) supraocular scales; (2) prefrontal scales present; (3) 11–28 temporal scales; (4) dorsal scales keeled; (5) 28–32 transverse rows of dorsal scales; (6) 17–23 transverse rows of ventral scales; (7) 31–45 scales around mid-body; (8) 3–5 rows of lateral scales; (9) lateral and medial ventral scales equal in size; (10) 0–2 femoral pores; (11) no sexual dimorphism in number of femoral pores; (12) labial scales similar in colour to other head scales, crossed by a curved pale lip line, best described as two oblique white lines converging in the eye; (13) ventral head colouration homogeneous; (14) cream or white vertebral stripe bordered by two black stripes, originating on the rostral scale, completely covering the dorsal region of the head and the vertebral region of the body, reaching only the anterior portion of the tail, with maximum width of four scales on the body; (15) lateral colour pattern brown, with a complete longitudinal line laterally, white and continuous from the posteroventral edge of the ear until the insertion of the hind limbs; with very few ocelli usually above the insertion of the forelimbs and absent between the limbs insertions, small; ocelli white in centre and surrounded by black scales and, beyond that, sometimes a few reddish scales; (16) venter strongly dimorphic in colouration between the sexes, uniformly pink to pale orange in females, sometimes with very few black speckles but no markings; usually glossy black and sometimes medium grey in males; (17) hemipenial body with 7–8 and 11–12 rows of spinulated flounces in the lateral columns of the sulcate and asulcate sides, respectively; (18) lateral columns of spinulated flounces connecting in the medial region of the asulcate side.
Pholidobolus vertebralis differs from P. odinsae sp. nov. (character states in parenthesis) in having the lateral ventral scales smaller than the medial ventrals (lateral and medial ventral scales equal in size). The other species from the north-western and central Colombian Andes (Fig.
Adult male; snout-vent length 54.2 mm; tail length 50.0 mm; other body measurements in Table
Limbs pentadactyl with clawed fingers. Dorsal brachial and antebrachial scales lanceolate to polygonal, longer than wide, imbricate and smooth. Ventral brachial and antebrachial scales lanceolate to polygonal, almost as long as wide, juxtaposed, much smaller than the dorsal ones. Dorsal hand scales hexagonal, wider but shorter than the dorsal antebrachial scales. Finger length formula IV = III > II > V > I. Supradigital scales quadrangular, imbricate and longer than wide. Palmar scales polygonal, juxtaposed and small. Subdigital lamellae domelike with a quadrangular base, and often divided longitudinally, with six on finger I, 8 on II, 13 on III, 15 on IV, and 7 on V. Thigh scales on the dorsal, anterior and ventral surfaces lanceolate to rhomboidal, longer than wide, those in the dorsal surface smooth and the others smooth and imbricate. Thigh scales on the posterior surface of the legs rounded, smooth, juxtaposed and much smaller than those of the anterior and dorsal surfaces. Two femoral pores per leg; preanal pores absent. Anterior and ventral crus scales polygonal and smooth. Lateral and posterior crus scales rounded, small and subimbricate. Toe length formula IV > III > V > II > I. Supradigital scales quadrangular, imbricate and longer than wide. Plantar scales polygonal, juxtaposed and small. Subdigital lamellae domelike with a quadrangular base, and often divided longitudinally, with five on Toe I, 9 on II, 13 on III, 15 on IV, and 7 on V.
In life, dorsally brown or pale brown, bisected by a mid-dorsal (i.e. vertebral) white stripe, extending from the head to the mid tail; vertebral stripe bordered with darker, usually dark brown or black, stripes; on the head, the pale stripe extends from the first supralabial to the shoulder dorsally reaching the rostral scale, and laterally including the frontonasal, prefrontal, frontal, frontoparietal, interparietal, and postparietal scales; sides of neck, flanks, and limbs predominantly brown, usually with less than five, small and white ocelli, bordered by a black stripe, and predominantly on the shoulders; white or cream lateral line from the supralabials, passing through the shoulder and extending continuously up to the insertion of the limbs, but not towards the tail; very few scattered red scales, more common around the shoulder ocelli; throat cream to pink in females, but grey to black in males; chest, belly and base of the tail pink to orange in adult females, but grey to black in males, with bare or no patterning in all cases (Figs
The species epithet is dedicated to the company Odinsa, for their decisive involvement in the Cartama Conservation Project, in southwestern Antioquia, aimed at restoring ecosystem services by regenerating the Andean forest along the Quebrada San Antonio basin. Together with other stakeholders, the initiative planted more than 320000 native trees during 2019–2020 alone.
The species is currently known from forest edges, and open areas including pastures, crops, and around human buildings. Most specimens were seen and found amongst grass or leaf litter even hundreds of metres away from the nearest forests. They appeared clearly heliothermic: within minutes after the sun appeared, they came out of their refuges, remain exposed, and extended their ribs increasing the dorsal surface available for sun basking. Under sunny conditions, the species seems to be abundant at the known localities. Its distribution seems not to be patchy, and it is known from more than five locations. Although they encompass less than 500 km2 (Fig.
This study provides unambiguous phylogenetic, genetic, morphological, and geographic evidence of independent evolutionary history in four lineages of Pholidobolus lizards, formerly assigned to P. vertebralis. Based on the available evidence, their evolution would have occurred at mid and high elevation Andes, and led to the origin of several geographically proximate species yet occupying a small area each. The only exception would be P. vertebralis, whose status as a single species is thus challenged by at least two lines of evidence.
First, most Pholidobolus species occupy small areas. The genus currently comprises 13 species, 11 of which are considered endemic: five are known from a single locality and four others from areas below 7000 km2, mostly in Ecuador. To the best of our knowledge, the three new species described herein, and the single species resurrected, exhibit small distribution ranges. In contrast, P. vertebralis is the only taxon believed to occur throughout 110000 km2 and three countries: Ecuador, Colombia and Venezuela (
Second, the genus distribution appears to exclude low elevation areas. The available evidence supports that most Pholidobolus species occur above 1000 m elevation, sometimes on hilltops, but mostly confined to one side of the Andes or the other (
If our argument holds, we anticipate that new species will be recognised once enough molecular and morphological data are collected throughout the distribution of P. vertebralis sensu lato. We also suggest revising published decisions on the validity of species previously regarded as synonyms of P. vertebralis. For instance, the main argument to synonymise Prionodactylus [Pholidobolus] palmeri and P. marianus was that the holotype “falls within my concept of P. vertebralis” (
The findings and arguments exposed here have relevant implications not only for the systematics of the group, but also for the recognition of appropriate conservation units. One of the foremost tasks in conservation is the delineation of biologically meaningful units, which implies the recognition of ecologically discrete and evolutionarily significant lineages. Particularly in the tropics, the task is hampered by the paucity of information on the genotype, phenotype, and geographic distribution of most taxa, which is further aggravated by the contrast between the extremely high level of species richness and the meagre resources devoted to analysing it. During centuries, species recognition was mainly based on detailed written accounts of species external morphology. Now, much more consideration is needed to examine the extent of variation in external morphology that is merely attributable to phylogenetic signal. Morphology is often evolutionarily conserved, due to the adaptive value of the phenotype. Dorsal colouration is cryptic and arguably conserved in Pholidobolus species; ventral colouration instead probably plays a crucial role as mate recognition signal and could therefore bear important and overlooked information for species delimitation. The adoption of integrative approaches involving systematics and other branches of biology will probably contribute to untangling true diversity levels, by ascertaining the number and distribution of evolutionarily independent lineages. This information is badly needed to delimit biologically meaningful conservation units, which could allow sound, scientifically based, decisions on conservation actions and priorities.
We are deeply grateful to Osman López, Ubiel Rendón, and Jorge Jaramillo for invaluable help in collecting the lizards. Field work was supported by Bioconservancy.org, and molecular sequencing and analyses by the Colombian Institute for Science and Technology (Colciencias) as well as the Instituto de Biología, Universidad de Antioquia, Colombia.
Linked data table for primary biodiversity data
Data type: occurrences
Explanation note: Data types and sequenced specimens of Anadia, Macropholidus, and Pholidobolus lizards (Gymnophthalmidae) used to build the phylogenetic hypothesis in this study.
Detailed phylogenetic tree
Data type: phylogenetic
Explanation note: Phylogenetic hypothesis on the relationships between studied lizards. Each terminal represents an included individual.