Research Article |
Corresponding author: Santiago Ron ( santiago.r.ron@gmail.com ) Academic editor: Franco Andreone
© 2016 María Navarrete, Pablo Venegas, Santiago Ron.
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:
Navarrete MJ, Venegas PJ, Ron SR (2016) Two new species of frogs of the genus Pristimantis from Llanganates National Park in Ecuador with comments on the regional diversity of Ecuadorian Pristimantis (Anura, Craugastoridae). ZooKeys 593: 139-162. https://doi.org/10.3897/zookeys.593.8063
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We describe two new species of frogs of the genus Pristimantis from the eastern slopes of the Ecuadorian Andes, at Parque Nacional Llanganates. The new species are characterized by the spiny appearance typical of several species inhabiting montane forests. Pristimantis yanezi sp. n. is most similar to P. colonensis and P. incanus but differs from both in groin coloration and by having smaller tubercles on the upper eyelids, heels, and tarsus. Pristimantis llanganati sp. n. is most similar to P. eriphus and P. chloronotus. It can be distinguished from P. eriphus by the color pattern on the scapular region and by having smaller conical tubercles on the dorsum. Pristimantis chloronotus differs from P. llanganati sp. n. in having a pair of sinuous paravertebral folds. Both new species occur in a region with few amphibian collections and nothing is known about their abundance and ecology. Therefore, it is recommended to assign them to the Data Deficient Red List category. Updated figures of species richness of Pristimantis among biogeographic regions in Ecuador are also presented. Pristimantis reach their highest diversity in Montane Forests of the eastern versant of the Andes. Its species richness across regions cannot be explained by regional area, elevation, temperature, or precipitation. Political endemism in Pristimantis is higher than that of other terrestrial vertebrates.
Andes, Pristimantis llanganati sp. n., Pristimantis yanezi sp. n., species richness, systematics, taxonomy, Terrarana
With 484 species, Pristimantis is the most diverse genus of amphibians (
Pristimantis is notorious for its taxonomic problems (e.g.,
A region where amphibian inventories have been almost completely lacking is Llanganates National Park in the central Andes of Ecuador. With an area of 2197 km2, Llanganates is a mosaic of páramos and montane forests dominated by a complex topography that result in a great diversity of habitats (
The format for the descriptions follows
The most recent analysis of regional diversity of Pristimantis in Ecuador was published by
Species richness values by biogeographic region are based on the AmphibiaWebEcuador database (http://zoologia.puce.edu.ec/Vertebrados/anfibios;
English: Yánez Rain Frog. Spanish: Cutín de Yánez.
(2 specimens).
(1 specimen).
The new species is assigned to the genus Pristimantis. Although morphological synapomorphies are unknown for Pristimantis, the new species has the characteristic morphology of most Pristimantis including T-shaped terminal phalanges, toes without membranes, and Toe V longer than Toe III. Pristimantis yanezi is characterized by the following combination of characters: (1) Skin on dorsum smooth in the anterior half and shagreen or tuberculate in the posterior half, skin on venter areolate to weakly areolate; discoidal fold absent; dorsolateral folds absent; (2) tympanic membrane and tympanic annulus present, its upper and posterior margin covered by supratympanic fold; (3) snout short, rounded in dorsal and lateral view; (4) upper eyelid with one distinct conical tubercle surrounded by some low indistinct rounded tubercles; EW 92% of IOD; cranial crests absent; (5) dentigerous processes of vomers prominent, oblique, moderately separated, posteromedial to choanae; (6) vocals slits and nuptial pads absent; (7) Finger I shorter than Finger II; discs of digits expanded, truncate; (8) fingers without lateral fringes; (9) ulnar and carpal tubercles present, low and rounded; (10) heel bearing one low conical tubercle surrounded or not by few lower rounded tubercles; inner tarsal fold present, short; (11) inner metatarsal tubercle elliptical, prominent, 3X as large as outer metatarsal tubercle; outer metatarsal tubercle small, ovoid; low, numerous distinct supernumerary plantar tubercles; (12) toes without lateral fringes; basal toe webbing absent; Toe V slightly longer than Toe III (disc on Toe III reaches the middle of the penultimate subarticular tubercle on Toe IV, disc on Toe V does not reach the subarticular tubercle on Toe IV); toe discs about as large as those on fingers; (13) in life, dorsum yellowish brown to dark brown with scattered pale brown or orange blotches and black flecks, bearing a faint middorsal hourglass-shaped band; head bearing a dark brown interorbital bar and sides of head brown with darker vertical labial bars; flanks dark brown or olive brown with distinct dark brown to black flecks and diffuse dark brown diagonal stripes; groins cream or brownish cream; venter light cream to dirty cream with dark brown flecks and with or without dark brown mottling on the throat; iris reddish coppery; (14) SVL in adult female 36.9 mm (n = 1), in adult males 23.7–29.8 mm (n = 3).
In this section, coloration refers to live individuals unless otherwise noted. Pristimantis yanezi is similar to congeneric species characterized by a spiny appearance (i.e. presence of conical tubercles on dorsum, eyelids, heels and outer edge of tarsus). It differs from these species and from other Pristimantis by the combination of the following characters: iris reddish coopery, dorsum yellowish brown to brown bearing scattered pale brown to orange blotches; skin on flanks shagreen with small scattered tubercles and bearing distinctive brown to black flecks; upper eyelid, heel and outer edge of tarsus with small conical tubercles; venter and throat cream to dirty cream covered by brown flecks or brown mottling; groins cream or brownish cream; posterior surfaces of thighs and concealed surfaces of shanks brown or olive brown. Adult males of Pristimantis yanezi can be distinguished from P. chloronotus (
Coloration in life of new species and similar congeners. A Pristimantis llanganati sp. n.,
Adult male. Measurements (in mm): SVL 29.8; tibia length 17.0; foot length 14.8; head length 8.6; head width 11.5; eye diameter 3.7; tympanum diameter 1.1; interorbital distance 3.4; upper eyelid width 3.1; internarial distance 2.7; eye–nostril distance 3.3; tympanum–eye distance 1.5. Head wider than long, wide as body; head width 39% of SVL; head length 29% of SVL; snout rounded in dorsal view and in profile; eye–nostril distance 87% of eye diameter; nostrils narrow, higher than long, directed dorsolaterally; canthus rostralis distinct in lateral view, curved in dorsal view; loreal region concave; lips rounded; upper eyelid bearing one small but distinct conical tubercle surrounded by few indistinct smaller tubercles; upper eyelid width 92% of IOD; tympanic annulus distinct, with upper and posterior margins covered by supratympanic fold; tympanic membrane present, distinct; tympanum diameter 30% of eye diameter, tympanum–eye distance 134% of tympanum diameter; one enlarged conical postrictal tubercle surrounded by indistinct low tubercles. Choanae large, semicircular, not concealed by palatal shelf of maxilla; dentigerous processes of vomers prominent, oblique, moderately separated, positioned posteromedial to choanae; each vomer bearing several indistinct teeth; vocal slits absent; tongue two times wider than long, notched behind, free posteriorly along one third of its length.
Skin on dorsum smooth in the anterior half and shagreen in the posterior half; dorsolateral folds absent; skin on flanks with scattered tubercles; skin on throat, chest and belly weakly areolate, ventral surfaces of thighs areolate; discoidal fold absent; cloacal sheath short; skin in upper cloacal region shagreen, wrinkled ventrally, with several tubercles below the cloacal sheath. Ulnar tubercles present, indistinct; nuptial pads absent; palmar tubercles low, outer palmar tubercle bifid, approximately twice size of ovoid thenar tubercle; subarticular tubercles low, well defined, round in ventral and lateral view; supernumerary tubercles at base of fingers present, distinct; fingers lacking lateral fringes; Finger I shorter than Finger II; disc on Finger I rounded and on Finger II expanded, disc on Finger III and Finger IV broadly expanded and truncate; pads on fingers well defined, surrounded by circumferential grooves on all fingers (Fig.
Palmar and plantar surfaces of the new species. Photos of hand (A) and foot (B) of P. yanezi sp. n.,
Hindlimbs slender, tibia length 57% of SVL; foot length 50% of SVL; upper surfaces of hindlimbs smooth; posterior surfaces of thighs smooth, ventral surfaces of thighs areolate; heel bearing one low conical tubercle surrounded by some low rounded tubercles; outer surface of tarsus bearing low but distinct sub-conical tubercles; short inner tarsal fold present; inner metatarsal tubercle prominent, elliptical, rounded, much bigger than oval, ill-defined outer metatarsal tubercle; plantar surface with some supernumerary tubercles; subarticular tubercles well defined, round in ventral and lateral view; toes lacking lateral fringes; webbing between toes absent; discs nearly as large as those on fingers, most prominent on Toe IV and V; discs on toes expanded, elliptical; all Toes having pads surrounded by circumferential grooves, less distinct on Toe I; relative lengths of toes: 1 < 2 < 3 < 5 < 4 (Fig.
Color of holotype in life (based on digital photographs) (Fig.
Color of holotype in ethanol 70% (Fig.
In this section, coloration refers to preserved individuals. In the type series, adult males (23.7–29.8 mm) are smaller than the single known female (SVL = 36.9 mm). See Table
Preserved individuals of Pristimantis yanezi sp. n. showing dorsal and ventral variation. A dorsal view B ventral view. From left to right:
Measurements (in mm) and proportions of type series of Pristimantis yanezi sp. n. Ranges followed by means and one standard deviation in parentheses. All specimens are adults.
Characters | Females (n = 1) | Males (n = 3) |
---|---|---|
SVL | 36.9 | 23.7–29.8 (27.1 ± 3.1) |
TL | 18.5 | 13.5–17 (15.6 ± 1.8) |
FL | 17.3 | 12.5–14.8 (13.7 ± 1.2) |
HL | 10.4 | 7.6–8.6 (8.3 ± 0.5) |
HW | 14.2 | 9.4–11.5 (10.55 ± 1.1) |
ED | 4.6 | 3.2–3.7 (3.5 ± 0.3) |
TY | 1.4 | 0.9–1.3 (1.1 ± 0.2) |
IOD | 3.3 | 2.8–3.4 (3.0 ± 0.3) |
EW | 3.8 | 2.6–3.1 (2.9 ± 0.3) |
IND | 3 | 2.2–2.3 (2.4 ± 0.3) |
E–N | 3.9 | 2.2–3.3 (2.9 ± 0.6) |
TL/SVL | 0.5 | 0.6 |
FL/SVL | 0.5 | 0.9 |
HL/SVL | 0.3 | 0.3 |
HW/SVL | 0.4 | 0.4 |
HW/HL | 1.4 | 1.2–1.3 (1.3 ± 0.1) |
E–N/ED | 0.9 | 0.7–0.9 (0.8 ± 0.1) |
EW/IOD | 1.2 | 0.9–1.0 (1.0 ± 0.1) |
TY/ED | 0.3 | 0.3 |
Coloration in life (based on digital photographs of adult female
Pristimantis yanezi is known from two localities (elevation range is 2095–2280 m) from Provincia del Tungurahua and Provincia del Pastaza, Parque Nacional Llanganates. Airline distance between localities is 32 km. Ecosystem type is Evergreen Montane Forest of the Eastern Andean Cordillera (as defined by
The holotype and the paratopotypes were collected at night, on vegetation on recently logged forest. The paratype was collected at night, on a branch (1 cm diameter) 2 m above the ground. A deforestation map by Ministerio de Ambiente (2013) shows continuous forest at the known localities. Because we lack population data and most of the Llanganates region lacks amphibian inventories, we assign P. yanezi to the Data Deficient Red List category (based on
The specific name yanezi is a noun in the genitive case and is a patronym for Mario Yánez who provided useful insights for the description of the new species. Moreover, during his career, Mario Yánez has contributed significantly to the study of Ecuadorian amphibians, especially those of the genus Pristimantis. He is director of Museo Ecuatoriano de Ciencias Naturales (
Most species groups within Pristimantis have been defined exclusively on morphological grounds (e.g.,
English: Llanganates Rain Frog. Spanish: Cutín de los Llanganates.
(3 specimens).
(2 specimens). Ecuador, Provincia Napo,
The new species is assigned to the genus Pristimantis. Although morphological synapomorphies are unknown for Pristimantis, the new species has the characteristic morphology of most Pristimantis including T-shaped terminal phalanges, toes without membranes, and Toe V longer than Toe III. Pristimantis llanganati is characterized by the following combination of characters: (1) Skin on dorsum covered by minute conical tubercles, skin on venter areolate with scattered warts; discoidal fold absent; dorsolateral folds absent; (2) tympanic membrane and tympanic annulus present, covered by supratympanic fold on its upper and posterior margins; (3) snout short, rounded in dorsal and lateral view; (4) upper eyelid with a low conical tubercle and some low indistinct tubercles posteriorly; EW 82% of IOD; cranial crests absent; (5) dentigerous processes of vomers varying from low and indistinct to high and evident, oblique, moderately separated, posteromedial to choanae; (6) vocals slits present, nuptial pads absent; (7) Finger I shorter than Finger II; discs of digits broadly expanded, truncate; (8) fingers bearing narrow lateral fringes; (9) ulnar and tarsal tubercles present, conical and low; (10) heel with two or three low conical tubercles; inner tarsal fold present, long and ill defined; (11) inner metatarsal tubercle elliptical, low, 2X as large as outer metatarsal tubercle; outer metatarsal tubercle small, ovoid; supernumerary plantar tubercles low and indistinct; (12) toes bearing narrow lateral fringes; toe webbing absent; Toe V longer than Toe III (disc on Toe III reaches the proximal edge to the proximal subarticular tubercle on Toe IV, disc on Toe V extends to the proximal edge of distal subarticular tubercle on Toe IV); toe discs about as large as those on fingers; (13) in life, dorsum olive green with X-shaped or rhomboidal dark brown mark on scapular region, and scattered brown flecks or blotches; flanks, dorsal and posterior surfaces of thighs and ventral surfaces of shanks dirty white or white with dark brown diagonal stripes; groins white or tan with distinct black or dark brown diagonal stripes; venter dirty cream with brown mottling in the throat and chest and brown flecks in belly and ventral surfaces of thighs. Iris coppery with a reddish horizontal stripe; (14) SVL in one adult female 29.8 mm, in adult males 24.0–27.0 mm (n = 2).
(Fig.
Adult male. Measurements (in mm): SVL 27.0; tibia length 18.8; foot length 22.8; head length 7.9; head width 9.8; eye diameter 3.2; tympanum diameter 1.3; interorbital distance 3.4; upper eyelid width 2.7; internarial distance 2.3; eye–nostril distance 2.8; tympanum–eye distance 1.3. Slender body; head as wide as body, wider than long; head width 36% of SVL; head length 29% of SVL; snout short, rounded in dorsal and lateral view; eye–nostril distance 89% of eye diameter; nostrils narrow, higher than long, directed dorsolaterally; canthus rostralis curved in dorsal view, slightly curved in profile; loreal region concave; lips rounded; upper eyelid bearing one small conical tubercle on its center and some low rounded tubercles posteriorly; upper eyelid width 82% of IOD; tympanic annulus barely visible, with upper and posterior margins covered by supratympanic fold; tympanic membrane present, distinct; tympanum diameter 39% of eye diameter, tympanum–eye distance 102% of tympanum diameter; few indistinct postrictal tubercles present. Choanae small, semicircular, not concealed by palatal shelf of maxilla; dentigerous processes of vomers low, indistinct, oblique, moderately separated, posteromedial to choanae; right vomer bearing two teeth and left vomer one tooth; vocal slits present; tongue slightly wider than long, notched behind, free posteriorly along one third of its length.
Skin on dorsum covered by minute conical tubercles, head bearing two large tubercles, one between the orbits and the other half way between the interorbital line and the tip of the snout; dorsolateral folds absent; skin on flanks with minute conical tubercles; skin on throat and chest weakly areolate, belly areolate with scattered enlarged warts, and ventral surfaces of thighs weakly areolate; discoidal fold absent; cloacal sheath short; skin in cloacal region tuberculate with two enlarged tubercles, on each side, below the cloacal sheath. Ulnar tubercles present, subconical and low; elbow bearing one low subconical tubercle; nuptial pads absent; palmar tubercles low, weakly defined, outer palmar tubercle bifid, approximately twice the size of ovoid thenar tubercle; subarticular tubercles low, well defined, round in ventral and lateral view; supernumerary tubercles at base of fingers present, indistinct; fingers bearing narrow lateral fringes; Finger I shorter than Finger II; disc on Finger I rounded and on Finger II expanded, disc on Finger III and IV broadly expanded and truncate; pads on fingers well defined by circumferential grooves on all fingers (Fig.
Hindlimbs slender, tibia length 70% of SVL; foot length 84% of SVL; upper surfaces of hindlimbs with minute conical and subconical tubercles; posterior surfaces of thighs smooth, ventral surfaces weakly areolate; knee bearing low conical tubercles; heel bearing low conical tubercles; inner tarsal fold present, long and weakly defined; inner metatarsal tubercle low, elliptical, rounded, two times the size of smaller, oval, rounded outer metatarsal tubercle; plantar surface weakly tuberculate; subarticular tubercles well defined, round in ventral and lateral view; toes bearing narrow lateral fringes; basal webbing between toes absent; discs nearly as large as those on fingers, most prominent on Toe IV and V; discs on toes expanded, rounded; all toes having ventral pads well defined by circumferential grooves; relative lengths of toes: 1 < 2 < 3 < 5 < 4 (Fig.
Color of holotype in life is unknown. Color of holotype in ethanol 70% (Fig.
In this section, coloration refers to preserved individuals. In the type series, adult males (24.0–27.0 mm) (n = 2) are smaller than the single known female (SVL = 29.8 mm) (n = 1). See Table
Measurements (in mm) and proportions of the type series of Pristimantis llanganati sp. n. All specimens are adults, range and average (in parenthesis) show for two males.
Characters | Females (n = 1) | Males (n = 2) |
---|---|---|
SVL | 29.8 | 24.0–27.0 (25.0) |
TL | 16.3 | 13.2–18.8 (16.0) |
FL | 15.7 | 18.2–22 8 (20.5) |
HL | 8.2 | 7.2–7.9 (7.5) |
HW | 10.3 | 9.0–9.8 (9.4) |
ED | 3.5 | 2.9–3.2 (3.04) |
TY | 1.2 | 0.9–1.1 (1.0) |
IOD | 3.4 | 2.7–3.4(3.0) |
EW | 3.2 | 2.36–2.7 (2.5) |
IND | 2.3 | 2.2–2.3 (2.2) |
E–N | 3.1 | 2.4–2.8 (2.6) |
TL/SVL | 0.6 | 0.6–0.7 (0.6) |
FL/SVL | 0.5 | 0.8 |
HL/SVL | 0.3 | 0.3 |
HW/SVL | 0.4 | 0.4 |
HW/HL | 1.3 | 1.3 |
E–N/ED | 0.9 | 0.9 |
EW/IOD | 0.9 | 0.8 |
TY/ED | 0.3 | 0.3 |
Coloration in life (Fig.
Pristimantis llanganati is known from three localities (elevation range is 2253–2883 m) from Provincia del Napo, Parque Nacional Llanganates, along the Salcedo-Tena road. Maximum airline distance between localities is 6.5 km. Ecosystem type is Evergreen Montane Forest of the Eastern Andean Cordillera (as defined by
All specimens were collected at night on vegetation. Four of them were in a flooded area in forest border. Two were in primary forest. A deforestation map by Ministerio de Ambiente (2013) shows continuous forest at the known localities. Because we lack population data and most of the Llanganates region is unexplored, we assign P. llanganati to the Data Deficient Red List category (based on
Map showing known localities for Pristimantis llanganati sp. n. and P. yanezi sp. n. Circles are for Pristimantis llanganati sp. n. and triangles for P. yanezi sp. n. Localities are based on type specimens deposited at the
The species name llanganati is a noun that refers to the kichwa word “Llanganati” that means “beautiful hill”. This word also gives name to Llanganates National Park, the area where the species was discovered. Many areas in the park are difficult to access and are biologically unexplored. This inaccessibility has protected large areas of its páramos and montane forests, a valuable asset for the conservation and Andean biodiversity.
As in P. yanezi, P. llanganati is not assigned to a species group until genetic data allows determining its phylogenetic position.
Across biogeographic regions (Fig.
Relationship between Pristimantis species richness and geographic area for Ecuadorian Biogeographic Regions (as shown in Fig.
Relative to all Ecuadorian amphibians, Pristimantis represents a higher proportion of the amphibian fauna in Páramo (46.1%) and montane forests (43.7% in Western Montane, 43.6 in Eastern Montane; Fig.
During the last decades, the number of described species of Ecuadorian amphibians has been steadily increasing reaching 566 species by 2016 (
The proportion of Pristimantis species endemic to Ecuador (98 spp., 54% of all Pristimantis) compares with 41% country endemism across all amphibians (
Lack of correlation between species richness and area of the region seems to be a consequence of the extremely low species richness of the Dry Shrub and Deciduous Forest and the extremely high richness in montane forests, relative to their size. Precipitation, temperature, and elevation were not correlated either. These results differ from local and global analyses indicating that environmental variables are strongly correlated with amphibian species richness (Ron et al. 2011, Pyron and Wiens 2013). Lack of correlation could be a real pattern or an artifact of the large number of species that remain undescribed in the Andes.
In summary, Ecuadorian Pristimantis reach their highest diversity in Montane Forests of the eastern versant of the Andes. Relative to other amphibian groups, they are particularly diverse in the Páramo region. Its species richness across regions cannot be explained by regional area, elevation, temperature, or precipitation.
This investigation was supported by grants from the Secretaría Nacional de Educación Superior, Ciencia, Tecnología e Innovación del Ecuador SENESCYT, Arca de Noé Initiative, and Pontificia Universidad Católica del Ecuador. The Ecuadorian Ministerio de Ambiente provided research and collection permits. We thank to E. Tapia and F. Núñez for specimen collection and D. Paucar, and F. P. Ayala for assisting access to the collection. Edgar Lehr and Alessandro Catenazzi provided helpful comments to the manuscript.
List of specimens examined and associated collection data
Data type: Occurrence
Explanation note: All samples belong to genus Pristimantis. We present museum and field number, locality, and coordinates, for each individual.