Research Article |
Corresponding author: Mario H. Yánez-Muñoz ( m.yanez@mecn.gov.ec ) Corresponding author: Diego F. Cisneros-Heredia ( diegofrancisco.cisneros@gmail.com ) Academic editor: Angelica Crottini
© 2019 Mario H. Yánez-Muñoz, David Veintimilla-Yánez, Diego Batallas, Diego F. Cisneros-Heredia.
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:
Yánez-Muñoz MH, Veintimilla-Yánez D, Batallas D, Cisneros-Heredia DF (2019) A new giant Pristimantis (Anura, Craugastoridae) from the paramos of the Podocarpus National Park, southern Ecuador. ZooKeys 852: 137-156. https://doi.org/10.3897/zookeys.852.24557
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A new species of frog of the genus Pristimantis is described from the paramos of the Nudo de Cajanuma, Podocarpus National Park, on the border between the provinces of Loja and Zamora-Chinchipe, Ecuador. The new species is readily distinguished from all other species of Pristimantis by its large body size (snout-vent length: 50.0–50.5 mm in adult females, 34.7–42.5 mm in adult males), thick glandular skin, large warts on flanks, prominent glandular patches on head and legs, and dark brown dorsum. This new species is among the largest and stoutest Pristimantis frogs of the high Andes. It is only known from its type locality, where it occurs in paramo bambusoid meadows at elevations between 3300 and 3400 m. It is morphologically similar to Pristimantis erythros, P. farisorum, P. obmutescens, P. orcesi, P. racemus, P. simoterus, P. simoteriscus, and P. thymelensis. Notorious morphological characters present in this new species are thick glandular patches covering dorsum and limbs and porous skin texture, which are shared with P. erythros.
Describimos una nueva especie de rana del género Pristimantis de los páramos del Nudo de Cajanuma, Parque Nacional Podocarpus, en el límite entre las provincias de Loja y Zamora-Chinchipe. La nueva especie se diferencia de otras especies de Pristimantis por su gran tamaño corporal (longitud rostro-cloacal: 50,0–50,5 mm en hembras adultas, 34,7–42,5 mm en machos adultos), piel glandular y gruesa, verrugas grandes en los flancos del cuerpo, prominentes parches glandulares en la cabeza y patas, y dorso café oscuro. Esta nueva especie está entre las ranas Pristimantis más grandes y fornidas de los altos Andes. Solo se conoce de su localidad tipo, donde habita en herbazales bambusoides de páramo a elevaciones entre 3300 y 3400 m. Es morfológicamente similar a Pristimantis erythros, P. farisorum, P. obmutescens, P. orcesi, P. racemus, P. simoterus, P. simoteriscus, y P. thymelensis. Características morfológicas notorias en esta nueva especie son los parches glandulares gruesos que cubren el dorso y las patas y la textura de la piel porosa, las cuales son compartidas con P. erythros.
Amphibia, Andes, Cajanuma, Craugastoridae, Loja, new species, paramo, Pristimantis, taxonomy, Zamora-Chinchipe
Amphibia, Andes, Cajanuma, Craugastoridae, Loja, nueva especie, páramo, Pristimantis, taxonomía, Zamora-Chinchipe
Pristimantis (
The Podocarpus National Park is located on the southernmost portion of the Cordillera Oriental of the Andes, in the provinces of Loja and Zamora-Chinchipe, southern Ecuador. It protects about 1450 km2 from 900 to 3600 m elevation, including foothill, low montane, cloud, high montane forests and paramos (MAE 2017). Little information exists about the herpetofauna of the highlands of Podocarpus National Park. Between 2009 and 2010, herpetological surveys were conducted on the paramos of Cajanuma, western side of the Podocarpus National Park, from 3320 to 3365 m elevation, as part of a project to evaluate the impacts of climate change on the biodiversity of this ecosystem (
Field work was carried out between December 2009 and April 2010 in the paramos of the Nudo de Cajanuma (nudo is the local name for transverse mountain ranges), Podocarpus National Park, on the border between the provinces of Loja and Zamora-Chinchipe, Ecuador. Paramos are highland Neotropical ecosystems dominated by grasses and forbs and located between the forest upper limit and the permanent snow line in the Andes from Venezuela to northern Peru (
Herpetological surveys were conducted at the paramo of Cajanuma across an area located at the following coordinates: 79.16219444°–79.16111111°W, 4.10861111°–4.09466667°S, at 3320–3365 m elevation (
Description format, definitions and terminology follows standards proposed by
Examined specimens are deposited at: División de Herpetología, Instituto Nacional de Biodiversidad, Quito (
ECUADOR: Pristimantis erythros: Provincia del Azuay: Chanlud, 3449 m,
Vocalizations were recorded with an Olympus WS-750 digital recorder and a Senheiser K6-C unidirectional microphone. During the recordings, air temperature and relative humidity were measured with a Springfield environmental thermometer. Acoustic analyses were done with Adobe Audition 3.0 software package (Adobe Systems Inc., San Jose, California, USA), at a sampling frequency of 44.1 kHz and 16-bit resolution. Waveform and spectrogram were made using Raven Pro 1.4 software package (Cornell Lab of Ornithology, Ithaca, NY) and analysed with a Fast Fourier Transformation of 512 points. Terminology and definitions follow proposals by
Pristimantis
grp. orcesi: L
English: Giant paramo rainfrog. Spanish: Cutín Gigante de Páramo.
Adult female; ECUADOR; provincia de Loja, Parque Nacional Podocarpus, Cajanuma; 4.108346°S, 79.162046°W, 3313 m alt.; 27 January 2010; David Veintimilla-Yánez and Karen Salinas leg.;
Same collection data as for holotype;
A new species of Pristimantis diagnosed by the following combination of characters: (1) Skin on dorsum porous, thick and glandular, with large, flat, glandular warts on flanks; dorsolateral folds absent; thick glandular patch on supra/postympanic region, and on dorsal surfaces of humeral, femoral, tibial and tarsal regions; glandular folds in wrists; skin on venter areolate; discoidal fold weakly defined; (2) tympanic membrane and tympanic annulus prominent; tympanic annulus rounded, 36% of eye length, with posterior margin in contact with supratympatic glandular patch; (3) snout rounded in dorsal view; rounded to slightly protruding in lateral view; (4) upper eyelid without tubercles, IOD wider than upper eyelid; cranial crests absent; (5) dentigerous processes of vomers present, oblique, moderately separated, posteromedial to choanae, with 4 to 5 teeth; (6) males with cream-coloured nuptial pads on dorsum of Finger I and vocal slits; (7) Finger I shorter than Finger II; emarginated discs of fingers broadly expanded and elliptical; (8) fingers without lateral fringes; (9) ulnar tubercle present but low or poorly differentiated; (10) heels without tubercles, inner tarsal wart low and poorly differentiated; (11) inner metatarsal tubercle ovoid, about 5–6x the size of subconical, rounded outer metatarsal tubercle; supernumerary plantar tubercles present; (12) toes with narrow lateral fringes; basal toe webbing between toes II–V; Toe V longer than Toe III (disc of Toe III does not reach distal subarticular tubercle on Toe IV, disc on Toe V reaches middle of distal subarticular tubercle on Toe IV); toe discs elliptical, slightly narrower than those on fingers; (13) in life, dorsal surfaces dark brown, chocolate brown, or orange-brown, with or without dark irregular botches, distinctive head markings absent, ventral surfaces brown with irregular pale flecks and blotches, iris bronze with dense black reticulations; in preservative, brown surfaces turn grey; (14) SVL 50.0–50.5 mm in adult females (n = 2), 34.7–42.5 (38.5 ± 2.1 SD, n = 10) mm in adult males (Table
Measurements (in mm) of type series of Pristimantis andinogigas sp. nov. from Nudo de Cajanuma, Podocarpus National Park, Andes of southern Ecuador. For males, range is followed by means and one standard deviation in parentheses.
Characters | Females (n = 2) | Males (n = 17) |
Snout-vent length | 50.0–50.5 | 34.7–42.5 (38.5 ± 2.1) |
Head width | 19.3–20.1 | 13.3–15. 9 (14.6 ± 0.8) |
Head length | 16.0–17.4 | 11.2–13.9 (12.7 ± 0.72) |
Eye diameter | 5.6–6.0 | 4.9–5.6 (5.3 ± 0.2) |
Interorbital distance | 8.2–8.8 | 5.5–7.9 (6.1 ± 0.6) |
Internarial distance | 4.4–4.6 | 3.5–4.6 (4.0 ± 0.3) |
Eye-nostril distance | 4.9–5.3 | 3.8–4.9 (4.1 ± 0.3) |
Tympanum diameter | 2.1–2.7 | 1.5–2.1 (1.8 ± 0.2) |
Tibia length | 22.1–23.2 | 16.5–19.0 (17.9 ± 0.7) |
Hand length | 15.7–15.8 | 11.0–13.3 (12.0 ± 0.7) |
Foot length | 23.7–24.3 | 16.3–20.4 (18.2 ± 1.0) |
Pristimantis andinogigas sp. nov. is readily distinguished from all other species of Pristimantis by its large body size, thick and glandular skin, large warts on flanks, prominent macroglandular patches on head and legs, and dark brown dorsum. The only species showing a similar combination of characters is Pristimantis erythros Sánchez-Nivicela, Celi-Piedra, Posse-Sarmiento, Urgiles, Yánez-Muñoz & Cisneros-Heredía, 2019, which is readily differentiated from P. andinogigas sp. nov. by being smaller (38.8–42.6 mm in adult females), having a conspicuous red coloration, and lacking dentigerous processes of vomers. In addition, P. andinogigas sp. nov. resembles the following species by bearing large, flat, glandular warts on flanks, and expanded discs on fingers and toes: Pristimantis farisorum Mueses-Cisneros, Perdomo-Castillo, & Cepeda-Quilindo, 2013, P. obmutescens (Lynch, 1980), P. orcesi (Lynch, 1972), P. racemus (Lynch, 1980), P. simoterus (Lynch, 1980), P. simoteriscus (Lynch), and P. thymelensis (Lynch, 1972). Pristimantis andinogigas sp. nov. is larger than any of these seven species, and furthermore, they differ from P. andinogigas as follows (characters of P. andinogigas sp. nov. in parentheses): areolate or shagreen dorsal skin (porous), thin supratympanic folds (prominent supra/post-tympanic glandular patch), thin glandular patches on legs (thick), and smaller body size, with adult females having 38.4–42.3 mm SVL in P. farisorum, 28.5–38.4 mm SVL in P. obmutescens, 35.2–36.1 mm SVL in P. orcesi, 29.9–37.9 mm SVL in P. racemus, 32.4–37.1 mm SVL in P. simoterus, 25.7–31.4 mm SVL in P. simoteriscus, and 28.0–33.5 mm SVL in P. thymelensis (versus 50.0–50.5 mm SVL in adult females of P. andinogigas). In addition, P. farisorum has snout subacuminate in dorsal view (rounded), fingers with narrow lateral fringes (absent), dorsum dark brown to black with irregular and elongated orange marking (brown with or without lighter irregular blotches), and inhabits upper montane forests on the Nudo de Pasto, Andes of southern Colombia (
Pristimantis loujosti and P. pycnodermis also stand out from other species of the genus by their stout body and thick glandular skin on dorsal surfaces of body and limbs, but they differ from P. andinogigas sp. nov. as follows (characters of P. andinogigas sp. nov. in parentheses): Pristimantis loujosti Yánez-Muñoz, Cisneros-Heredia & Reyes-Puig, 2010 has smooth skin on head and granular skin on dorsum and flanks (porous, with large warts on flanks), thick supratympanic fold (prominent glandular supra/post-tympanic patch), thin glandular patches on legs (thick), subacuminate snout in dorsal view (rounded in dorsal view), fingers bear lateral fringes (absent), black spots on hidden surfaces of limbs (uniformly coloured), light iris with dark reticulation (bronze with dense black reticulations), and it inhabits on cloud forests on the Upper River Pastaza, Cordillera Oriental of the Andes of Ecuador (
Adult female (50.0 mm SVL, Fig.
Skin on dorsum thick and glandular, surface texture porous (Figs
Hind limbs robust (tibia length 46% of SVL; foot length 49% of SVL); heel without tubercles; inner edge of tarsus with one wart low and poorly differentiated; inner metatarsal tubercle ovoid, about 5x round outer metatarsal tubercle; subarticular tubercles rounded; plantar supernumerary tubercles low and inconspicuous, smaller than subarticular tubercles; toes with narrow lateral fringes; basal toe webbing between toes II–V; discs of toes expanded, elliptical, slightly narrower than those on fingers, most prominent on fingers II–V, while disc on Finger I slightly expanded; toes with ventral pads well-defined by circumferential grooves; toe lengths, when adpressed, IV > V > III > II > I; Toe V longer than Toe III; disc of Toe III not reaching distal subarticular tubercle on Toe IV, disc on Toe V reaches middle of distal subarticular tubercle on Toe IV (Fig.
Snout-vent length 50.0; head width 20.1; head length 16.0; eye-nostril distance 5.3; internarial distance 4.6; interorbital distance 8.8; tympanum diameter 2.1; eye diameter 6.0; tibia length 23.2; hand length 15.8; foot length 24.3.
Dorsum dark brown; ventral surfaces dark brown with irregular light-yellow flecks and blotches on throat, hands, feet, armpits, and lower venter; iris golden-bronze with dense black reticulations (Fig.
Same pattern as in life, but brown surfaces turned dark grey (Fig.
Males are smaller than females, measurements of the type series are provided in Table
The specific epithet is coined from the New Latin adjective andinus (pertaining to the Andes) and the Latin noun gigas (giant). The name alludes to the large and stout body of this new species in comparison with other species of Pristimantis from the high Andes.
Males call from grasses at night, in heterogeneous chorus with extensive call superposition. Paratype
Pristimantis andinogigas sp. nov. is only known from its type locality, the paramos of the Nudo de Cajanuma, at elevations between 3300 and 3400 m, on the Cordillera Oriental of the Andes of southern Ecuador (Fig.
The ecosystem at the type locality is Paramo Bambusoid Meadow (MAE et al. 2013). The most representative plant genera were Bomarea, Miconia, Blechnum, Disterigna, Epidendrum, Gaultheria and Puya; and the most abundant plant species were Escallonia myrtilloides, Puya nitida, Hypericum lancioides, Tillandsia aequatorialis, Neurolepis nana, Cortaderia bifida, C. jubata, Chusquea neurophylla, Calamagrostris macrophylla, Themistoclesia epiphytica, Senecio tephrosioides, Disterigma pentandrum, and D. empetrifolium, Rubus laegaardii (
Pristimantis andinogigas was found active at night (19h00–22h00) at 6–10° C air temperature and 85–98% relative humidity. All males and some subadults and juveniles were observed active on bamboos (Neurolepis spp.); while both adult females were found active on the floor. During the day, individuals were found hidden inside rosettes (Senecio spp. and Puya spp.) or at the base of bamboos. Pristimantis andinogigas was the most abundant species during surveys at the type locality, representing 47 out of 108 anuran records. It was found in sympatry with Pristimantis percultus, Pristimantis sp. cf. colodactylus, Pristimantis sp. cf. orestes, and Lynchus sp.
The type locality of P. andinogigas is officially protected as part of the Podocarpus National Park, a national protected area created in 1982. The area has little anthropogenic impact, and in general, paramos of the Nudo de Cajanuma and the nearby Nudo de Sabanilla are reported to have a relatively good conservation status (
Pristimantis andinogigas sp. nov. is morphologically similar to several species formerly associated under the P. orcesi species-group (i.e., Pristimantis erythros, P. farisorum, P. obmutescens, P. orcesi, P. racemus, P. simoterus, P. simoteriscus, and P. thymelensis). However, we refrain from assigning it to any species-group in the absence of data to conduct an integrative phylogenetic analysis. Morphological characters in Pristimantis are by themselves unreliable to assess phylogenetic affinities, and most of the species-groups within Pristimantis that were solely defined on morphology have resulted non-monophyletic (
Pristimantis andinogigas shows two notorious morphological characters that are not extended in the genus: glandular patches covering dorsal surfaces body and limbs, and porous dorsal skin texture. Similar glandular patches were first reported in P. pycnodermis by
Over the last decades, field studies in the Podocarpus National Park and nearby areas have revealed extraordinary flora and fauna diversity on the southernmost portion of the Cordillera Oriental of the Andes in Ecuador (
This work is part of Programa de Investigación Red Terrarana del Ecuador of Instituto Nacional de Biodiversidad INABIO, developed with the support of Universidad Nacional de Loja, Laboratorio de Zoología Terrestre and Museo de Zoología of Universidad San Francisco de Quito USFQ, and Museo de Zoología QCAZ. We thank Karen Salinas who was part of the team that surveyed the herpetological diversity at Cajanuma, to José Villa Esparza and Enrique Armijos, park rangers of the Podocarpus National Park, for their field support, and to Rudolf von May and Alessandro Catenazzi for their comments as reviewers. Research was conducted under authorization by Ministerio del Ambiente del Ecuador. For access to collection specimens and working space, we thank Juan C Sánchez-Nivicela (Universidad del Azuay), Carolina Reyes-Puig (Museo de Zoología, Universidad San Francisco de Quito), Santiago R Ron (Museo de Zoología, Pontificia Universidad Católica del Ecuador PUCE), John D Lynch (Instituto de Ciencias Naturales, Universidad de Colombia), and Raúl Sedano (Colección Herpetológica, Universidad del Valle del Cauca). Revision of type specimens of Colombian Pristimantis was possible thanks to the support of Heinz Schneider of Basel Botanical Garden, Lou Jost, Javier Robayo and Juan P Reyes-Puig of Ecominga Foundation. Work by David Veintimilla-Yánez was supported by Universidad Nacional de Loja, Centro de Estudios y Desarrollo de la Amazonía CEDAMAZ, and Ministerio del Ambiente de Loja. Work by Diego F Cisneros-Heredia was supported by Universidad San Francisco de Quito USFQ (projects HUBI ID 48 “Taxonomía, Biogeografía y Conservación de Anfibios y Reptiles”, ID 1057 “Impact of habitat changes on the biological diversity of the northern tropical Andes”, ID 7703 “Estrés fisiológico y molecular en anfibios de los altos Andes tropicales”, funded by a grant of the Colegio de Ciencias Biológicas y Ambientales COCIBA-USFQ, ID 12268 “Taxonomía y Conservación del género Pristimantis en los páramos, estribaciones y tierras bajas del Ecuador”, ID 13524 “Desarrollo de una plataforma de bioinspiración médica a partir de la biodiversidad”, funded by a grant of the Escuela de Medicina, Colegio de Ciencias de la Salud. COCSA-USFQ) and by Programa “Becas de Excelencia”, Secretaría de Educación Superior, Ciencia, Tecnología e Innovación (SENESCYT), Ecuador. For their constant encouragement, Mario Yánez-Muñoz expresses his deepest gratitude to Mauro Yánez, Alejandra Figueroa, Joaquín Yánez, and Julieta Yánez; David Veintimilla-Yánez to Carlos Veintimilla, Lucía Yánez, Nikolay Aguirre Mendoza, Max González, Walter Apolo, Katiusca Valarezo, Johana Muñoz, Ivonne González, Tatiana Ojeda Christian Aguirre, and Andreas Fries; and Diego F Cisneros-Heredia to María Elena Heredia, Laura Heredia, and Jonathan Guillemot.