Pristimantis gretathunbergae, Mebert & González-Pinzón & Miranda & Griffith & Vesely & Schmid & Batista, 2022

Mebert, Konrad, Gonzalez-Pinzon, Macario, Miranda, Madian, Griffith, Edgardo, Vesely, Milan, Schmid, P. Lennart & Batista, Abel, 2022, A new rainfrog of the genus Pristimantis (Anura, Brachycephaloidea) from central and eastern Panama, ZooKeys 1081, pp. 1-34 : 1

Pristimantis gretathunbergae sp. nov.

Holotype.

MHCH 3082 (original field number AB 1059), an adult male (Figs 4A , 5 ) collected by Abel Batista & Konrad Mebert on the top of Cerro Chucantí (8.804621°N, - 78.45950°W; near 1439 m a.s.l.), Maje Mountains, Río Congo Arriba, Distrito de Chepigana, Darién, Panama, on 03 December 2012 at 18:21 hrs.

Paratypes.

Seven males, three females. Male and female SMF 97521-22 (AB 1056-7) respectively, male MHCH 3081 (AB 1058) same collecting attributes as holotype (Fig. 4B, C, E-F ); male MHCH 3111 (MG 28), male collected by Macario Gonzalez on 27 June 2018 at 23:40 hrs; male MHCH 3112 (MG 31), male collected by Macario Gonzalez on 07 August 2018 at 21:15 hrs, all from around the top of Cerro Chucantí (8.80455°N, 78.45951°W; near 1439 m a.s.l.) Maje Mountains, Río Congo Arriba, Distrito de Chepigana, Darién, Panama. Males MHCH 3113-4 (MG 48-9), males, collected by Macario Gonzalez on 27 June 2018 at 23:40 hrs (8.80455°N, 78.45951°W; 1439 m a.s.l.); females MHCH 3115 and SMF 97517 (AB 654), from Ambroya (8.92111°N, - 78.62786°W; 851 m a.s.l.), Cerro la Javillosa Torti, Chepo, Panama, on 28 August 2012 at 19:40 hrs.

Diagnosis.

Pristimantis gretathunbergae sp. nov., a member of the Pristimantis ridens species group (sensu Reyes-Puig et al. 2020), is characterized by the following combination of characters: (1) dorsal skin surfaces slightly areolate, with dispersed tubercles; venter weakly areolate; discoidal fold present, dorsolateral folds absent; (2) tympanum concealed, indistinguishable or poorly distinguished; annulus and tympanic membrane barely visible in males, not visible in females; tympanic fold from the posterior edge of the eye to the arm insertion; (3) snout short, broadly rounded in dorsal view, moderate in length, rounded and slightly protruding in profile; (4) upper eyelid with a single conical to spine-like, some triangular tubercle, ED wider than IoD; cranial crests absent; (5) dentigerous processes of vomers present, prominent, oblique, each bearing from 5 to 10 teeth; (6) vocal slits and nuptial pads absent; (7) Finger I shorter than Finger II; discs on outer fingers truncate, more than twice width of digit proximal to disc; (8) fingers bearing narrow lateral fringes; (9) three to four low ulnar tubercles, barely visible in preservative; (10) heel bearing a conical tubercles, outer edge of tarsus with three to four low and small conical tubercles, inner edge of tarsus lacking tubercles; (11) inner metatarsal tubercle large and elliptical, 4-5 × size of outer, ovoid metatarsal tubercle; supernumerary plantar tubercles low; subarticular tubercles conical; (12) toes bearing narrow lateral fringes; webbing absent; Toe V much longer than Toe III; discs as large as those on outer fingers; (13) dorsal ground coloration usually shades of brown with individual tones of red or yellow with or without scattered orange flecks, and/or larger reddish or distinct brown blotches, or light dorsolateral band; (14) venter uniform dirty white (some specimens exhibit dark spotting) or patternless yellow to orange; (15) groin and inner thighs white, yellow or orange-red, some with flecks matching the dorsal ground color or red; (16) blackish iris, some individuals show very dark red iris and/or red-golden speckling; (17) prominent light upper lip in all females and in some males, while other males exhibit some blotches extending from the nose vertically across the lip, however, the upper border of the light-colored lip patches is still demarcated by the darker nose coloration, except in generally light-colored specimens; (18) SVL up to 36.7 mm in males, up to 46.3 mm in females.

Comparative diagnosis to sympatric rainfrogs.

Pristimantis gretathunbergae sp. nov. differs markedly from all other Pristimantis species in central and eastern Panama by its very dark to black, non-reticulated iris, respectively entire eyes (iris pale and/or with heavy pale flecking in other species). Some fine golden to dark red speckling or flecking might be visible in some P. gretathunbergae sp. nov. In sympatry, the new species is most similar to the equally large and bulky P. cruentus (Fig. 4C ) from which it can be distinguished as follows (characters of P. gretathunbergae sp. nov. in parentheses): P. cruentus has venter heavily mottled with dark pigment to almost uniform black (white, dirty white or yellow, see Suppl. material 2: Fig. S10 G-I, M), upper surfaces gray, brown, brownish black (reddish brown, light gray to yellow-brown); lips mottled or with patches, whereas specimens with light upper lip usually show an irregular border with the dark snout coloration (upper lip uniformly colored white or yellow, but some males have upper lips with dark patches, yet the light parts are still sharply and straight-bordered by the dark snout coloration above, whereas the colored demarcation in specimens of P. cruentus with a light upper lip is normally diffuse or irregularly shaped, see Suppl. material 2: Fig. S11 for a multi-specimen comparison); tympanic annulus partially evident in females (not visible); P. cruentus exhibits a variable number and shape of tubercles on the eyelid (usually only one single conical to spine-like tubercle over the eyelid (see Fig. 4 and Suppl. material 2: Fig. S10A, B). Pristimantis gretathunbergae sp. nov. differs from other coexisting species of the P. ridens species group in Panama by being larger in size, and by having white, cream, yellow, or orange-reddish coloration on inguinal area, often suffused with red pigment (Suppl. material 2: Fig. S10C-F, K, L). A more detailed comparison by sympatric species from Panama follows: P. caryophyllaceus , dorsum smooth (slightly areolate, scattered with tubercles), sharp and projecting snout (short, broadly rounded in dorsal view); P. cerasinus , P. ridens , and P. taeniatus have general dorsal color brown (reddish brown or yellow) and tympanic membrane distinct (tympanic membrane indistinct); P. gaigei is black with orange dorsolateral stripes (reddish brown or yellow); P. museosus and P. moro general dorsal color is green (reddish brown or yellow); P. pardalis has silvery white spots on side and anterior portion of thighs (anterior portion of thighs yellow, suffused with reddish color).

Comparative diagnosis to related, allopatric rainfrogs.

This comparison includes only members of the Pristimantis ridens species group sensu Reyes-Puig et al. (2020). Pristimantis gretathunbergae sp. nov. is genetically most closely related to the allopatric rainfrog Pristimantis erythropleura . Like P. gretathunbergae sp. nov., P. erythropleura inhabits cloud forests higher than 980 m in the western and partly central Cordilleras in the Department Antioquia, Caldas, Cauca, Chocó, Quindío, Risaralda, Tolima, and Valle del Cauca (e.g., Lynch 1992; Atehortua-Vallejo et al. 2020). It is also highly polymorphic and sexually dimorph (see 41 examples in Suppl. material 2: Fig. S12). According to data from Lynch (1992) some P. erythropleura share a few characters with P. gretathunbergae sp. nov. by exhibiting: a dirty white venter, frequently also yellow to red flash colors on the concealed inner, some also outer, surface of the upper thigh and groin (however extended color variation is depicted in Suppl. material 2: Fig. S12), vocal slit absent and other characters shared within the P. ridens species group. But P. erythropleura differ in a few characters from P. gretathunbergae sp. nov. (character expression of P. gretathunbergae sp. nov. in parenthesis): body size regionally variable but always smaller, even in the population with the largest individuals from Calarca, Colombia, with SVL for males 21.2-25.4 mm, females 28.2-34.8 mm (substantially larger: SVL 26.9-36.7 mm males, 38.2-45.0 mm females), golden to red eyes, resp. iris, with some heavy reticulation (fully black eyes with golden or dark-red speckling/flecking in some individuals), subconical tubercle on upper eyelid (conical to spine-like single tubercle), glandular nuptial pad on thumb of males (lacking nuptial pads).

Two additional rainfrog taxa inhabit northwestern Colombia that are closely related to P. gretathunbergae sp. nov. First, Pristimantis penelopus , sister species to P. erythropleura , was originally known to inhabit montane areas higher than 1000 m a.s.l. in northwestern Colombia ( Lynch and Rueda-Almonacid 1999), but has also been found as low as 94 m a.s.l. ( Restrepo et al. 2017). The two confirmed samples of P. penelopus from the Cordillera Central exhibit a short 16S mtDNA genetic divergence of 4.8% to P. gretathunbergae (Table 1 ). Second, one sample in our analysis (SMF 97539), originally labeled as " P. cruentus ", clustered with the two Pristimantis penelopus -samples (16S mtDNA divergence <1%) but showed a large difference to P. gretathunbergae of 8.2%. It was collected in the Jingurudó (Pacific coastal) Mountain range, Comarca Emberá-Wounaan, Panama, and its external appearance resembles P. sanguineus from the Pacific versant of the Cordillera Occidental, Antioquia, and the coastal mountains of Choco ( Lynch 1998). Although, no sequence of P. sanguineus was available to verify its taxonomic allocation to specimen SMF 97539 from this little studied region (Pacific coastal border Panama-Colombia), morphological resemblance to former species and molecular proximity to P. penelopus are sufficient to provisionally label it as P. aff. sanguineus / Pristimantis penelopus pending further investigation.

Both, P. penelopus and P. sanguineus (examples in Suppl. material 2: Fig. S13), differ similarly from P. gretathunbergae sp. nov. (with the character expression of P. gretathunbergae sp. nov. in parenthesis), tympanum in P. penelopus and P. sanguineus more prominent (tympanum mostly concealed), upper eyelid with a subconical tubercle, with several non-pungent tubercles only in P. penelopus (triangular, conical to spine-like single tubercle); venter color cream to dull orange with brown spotting and/or more or less prominent dark reticulation in P. penelopus , brown stippling in P. sanguineus (uniformly dirty white to orange), groin and concealed surfaces of limbs black with light-colored spots (groin and inner thighs white, yellow or orange-red, some mixed with speckling of brown or yellow), iris copper or red with black reticulum (iris blackish, some golden or dark red speckling visible in some specimens), upper lips with marked labial bars (prominent light-uniformly colored upper lip in females and some males), smaller body size in P. penelopus / P. sanguineus with SVL in mm: 16.3/16.9-22.2/24.0 males, 31.2/29.1-37.835.2 females (SVL 26.9-36.7 in males, 38.2-46.3 females).

Further detailed comparisons to similar rainfrog species, e.g., P. viejas , P. latidiscus , P. laticlavius , P. cisnerosi , and P. paisa is provided in the Suppl. material 2. In addition, photo panels in the Suppl. material 2: Figs S12-S16 show color pattern variations of these related rainfrog taxa, as well as the two closest relatives of P. gretathunbergae sp. nov., P. erythropleura and P. penelopus . With regards to the blackish eyes, which is the most conspicuous character of P. gretathunbergae sp. nov., few other Pristimantis spp. from north-western South America exhibit very dark eyes (resp. iris), but none are related to the P. ridens group treated herein. Examples are P. farisorum , P. orcesi , P. parectatus , P. acerus , and P. piceus , which are primarily species of higher (> 2000 m a.s.l.) elevations of the Andean Mts., in which blackish iris coloration is only one morph and that tends to be more of a very dark grey, brown, or red, whereas other specimens of these species have lighter colored iris. One notable exception appears to be P. chalceus from the Chocoan lowlands and adjacent western Andean slopes up to 1970 m a.s.l. in western Colombia and Ecuador (e.g., Padial et al. 2014; Frenkel et al. 2021).

Description of the holotype

(Figs 4A , 5 ). Adult male (SVL 34.6 mm; head approximately as wide as long (HL/HW = 1.11); snout short, broadly rounded in dorsal view, moderate in length, rounded and slightly protruding in profile, eye to nostril distance 10% of SVL. Canthus rostralis and loreal region slightly concave, nares situated near tip of snout and slightly dorso-laterally directed, clearly visible in frontal and dorsal view, but not ventrally; interorbital area smooth, the upper eyelid is 1.4 of the IoD; a low and conical upper eyelid tubercle, rest of the head with scattered tubercles, but visible only in live specimens, without crests; tympanic annulus slightly visible, tympanum indistinguishable, tympanic annulus concealed by skin, tympanum of moderate size, ratio TY/EW 0.39, supratympanic fold present, from the outer edge of the eye to posterior the insertion point of the jaw, skin around the tympanum with scattered small tubercles; clearly visible choanae rounded and moderate in size, dentigerous processes of vomer in transverse row between choanae, separated by half of a vomer size, with five teeth on right side and seven on left side; vocal slits absent; tongue slightly longer than wide, 2/3 attached to mouth floor, shagreen in texture, with an evident papillae at the anterior 1/4 of the tongue; dorsal skin surface shagreen with scattered tubercles, ventral surface weakly areolate, without dorsolateral folds, discoidal fold present, extended from level of arm pit to the groin; cloaca partially smooth, granular in the lower part; hands moderate in size, 30% of SVL, four or five low and small ulnar tubercles; finger II longer than finger I, expanded disks on fingers II, III, & IV; relative lengths of adpressed fingers I <II <IV <III; finger II subequal in size to finger VI, finger II reaching the disc on finger IV when adpressed; finger III disc 2.4 × wider than distal end of adjacent phalanx; subarticular tubercles rounded, and elevated on lateral view, thenar tubercle long, oval and low; palmar and supernumerary present, slightly visible, no nuptial pads, narrow lateral fringes on fingers; hindlimbs of moderate length, TL 51% of SVL; relative lengths of adpressed toes I <II <III <V <IV; when adpressed, tip of toe I reach tubercle of toe II; disc of toe IV expanded, 1.9 × wider than distal end of adjacent phalanx; narrow lateral fringes on toes; between one and three non-protuberant subarticular tubercles present (one each on toes I and II, two on toes III and V, and three on toe IV); inner metatarsal tubercle elongated; outer metatarsal tubercles slightly pointed and smaller than inner; tarsal ridge absent, outer tarsal tubercles absent; hands and feet without webbing; finger and toe discs broadly expanded.

Measurements of the holotype.

SVL 34.6, HW 12.8, HL 14.2, InD 2.4, IoD 4.1, EW 5.4, ED 4.6, EN 3.6, TY 1.9, TL 17.7, FL 16.2, FAL 8.8, HAL 10.2, BW 8.7, 3FW 0.8, 3FD 1.5, 3TW 0.9, 3TD 1.4, 4TW 0.7, 4TD 1.3.

Coloration of holotype in life

(MHCH 3082; Fig. 4A ): Color codes of Köhler 2012 in parenthesis: In life, the dorsum is cream color (Light Yellow Ocher 13), with reddish (Chrome Orange 74) irregular big blotches, except in the flanks; inferior part of supratympanic fold suffused with brown color (Russet 44); thighs and anterior portion of tibia and foot with transverse bars. Groin is reddish (Scarlet 69) above and yellow (Orange Yellow 8) below. The margin of the upper lip is yellow (Sulphur Yellow 80). The iris is almost black (Black Carmine 61) with paler (Geranium 66) spots. The area between flanks and venter is suffused with cream color (Cream Yellow 82), the venter is dirty white.

Coloration in preservative

(Fig. 5 ): Dorsal ground color cream (Pale Pinkish Buff 3), suffused with minute dark pigments (Hair Brown 277), pale (Light Orange Yellow 7) groin, forelimbs, and hind limbs and with diffuse dark (Hair Brown 277) transverse bands; ventral areas cream (Cream Color 12); underparts of finger and toe disks diffused with dark (Hair Brown 277) pigments.

Variation

(Fig. 4 , Suppl. material 2: Figs S8-S11): Most specimens correspond with the general description of the holotype, but some specimens show variation, including pale brown (Clay Color 18, 20) dorsum, with or without reddish (Chrome Orange 74) irregularly distributed and sized large blotches on dorsum; a specimen from Cerro Chucantí photographed in 2016 had flanks with reddish color (Scarlet 69), in between the dorsal (Clay Color 20) and ventral (dirty white) color. Other specimens from Ambroya presented spots (GE) or bands on dorsum. One female had uniform yellow color (Orange Yellow 8) on venter. Morphometric variation is shown on Table 2 .

Etymology.

The specific name is a noun in the genitive case and is a patronym in honor for Greta Thunberg, a Swedish student, and her global climate activism. Greta initiated a "School Strike for Climate Action" outside the Swedish parliament to demand a radical response to the threat by the ongoing climate change. Then sixteen-year-old Thunberg’s example has inspired students worldwide to carry out similar strikes called Fridays For Future that started in August 2018. In December 2018 she addressed world leaders at the COP24 climate talks in Katowice, Poland, with sharp and unmasked words, and equally impressed a global audience in January 2020 with her unpolitical, direct speech down to the point on "Averting a Climate Apocalypse" at the WEF (World Economic Forum) in Davos, Switzerland. Just recently, she publicly slammed the world leaders at the 26th UN Climate Change Conference of the Parties (COP26) in Glasgow, November 2021, for not doing enough to meet the demands of the climate emergency. Greta Thunberg represents the authentic voice that exposes the motivations behind the diplomatic curtain of politicians and business stakeholders. Her voice is essential if we want to revert to and maintain a healthy environment on the planet we all share, and not least, learn to respect its magnificent mega-diversity of life that took millions of years to evolve.

Distribution.

Pristimantis gretathunbergae sp. nov. is endemic to Panama, but it could occur on near mountains along the border in Colombia. Its currently known distribution covers eastern Panama with records from the Darien Mountains within Embera Comarca and the Maje Mountains within Darien and Panama Provinces, including the type locality at Cerro Chucantí. The distribution continues west into Central Panama, including records from Piedras-Pacora Mountains, Panama Province, and Cerro Bruja, Colon Province, both within Chagres National Park. Farther west across the Panama Canal, P. gretathunbergae sp. nov. is present at Altos del Maria, region of Gaita Hills, Panama Oeste Province, and in the region of El Cope, Omar Torrijos National Park, Coclé Province.

Color pattern of specimens from Cerro Brewster, not included in the LDA (DFA) analysis, are consistent with the specimens from Maje Mountains in having a cream dorsum coloration, the margin of the upper lip in females yellow, an iris nearly black with pale dots or speckles, venter dirty white, and general stocky body and head. Due to the unique combination of characters of P. gretathunbergae sp. nov., in particular the blackish non-reticulated iris and light, unpatterned upper lip, that differs from any other related rainfrog in Panama and Colombia, we confidently allocate specimens available only as photo vouchers from Cerro Bruja, Colon Province, and Altos del Maria, Gaita Hills, Panama Oeste Province to the same species. The latter two localities substantially reduce the gap to El Cope, Cocle Province, the origin of the most western specimen of our Group 1. So far, we have not received photographic vouchers for the specimen from El Cope, but the low 16S-divergence of 2.3% clearly links it to the undescribed species from the Maje Mountains (see above).

Natural history.

Pristimantis gretathunbergae sp. nov. has been recorded at altitudes between 718-1439 m a.s.l. and occupies most frequently montane forest, a cloud forest consisting predominantly of trees covered with moss and a large variety of understory and midstory bromeliads ( Flores et al. 2018). At night, this species was observed between 0.5-3 m above the ground on tree bark and in the bromeliad foliage (Fig. 6 ). During daytime, individuals were found hiding between bromeliad leaves. At the top of Cerro Chucantí, males were calling (a sporadic “chack”) during the rainy season in December. Reproductive activities beginning with the rain period have also been observed at Altos del Maria, near Gaita Hills. Three females have been seen guarding clutch of eggs for at least four nights in bromeliads and moss-covered tree branches (Fig. 6 , Suppl. material 2: Fig. S8E). Diet is not known, but as in other Pristimantis , it likely consists of a variety of arthropods, mostly ants, orthopterans, and spiders ( Lynch and Duellman 1997; Garcia et al. 2015).

Conservation.

Habitats occupied by P. gretathunbergae sp. nov. are under latent threat. For example, anthropogenic pressure around Cerro Chucantí and the Maje Mountains most likely will lead to declines of populations through habitat destruction ( Batista et al. 2020). Similar scenarios are known and can be expected from the other known sites of P. gretathunbergae sp. nov., as they mostly represent restricted montane areas surrounded by agriculture and pastures, and only a few sites are within protected areas ( Chucantí Private Reserve, Chagres National Park, General de División Omar Torrijos Herera). Greta Thunberg’s Rainfrog is, thus far, known only from patches of primary forest and slightly disturbed areas. Unfortunately, in the areas surrounding P. gretathunbergae sp. nov. localities, population declines are related to the chytrid fungus ( Batrachochytrium dendrobatidis ) and pose an additional serious threat ( Rebollar et al. 2014; Voyles et al. 2018). Consequently, P. gretathunbergae sp. nov. should be listed as "Vulnerable (VU)" in the global Red List of the IUCN (2018) according to criteria B2ab(iii), because: i) its reduced area of occupancy is less than 2000 km2, ii) it is known from fewer than ten localities, iii) its range is severely fragmented with continuing decline in extent and/or quality of habitat. The Environmental Vulnerability Score (EVS) of this species is 18, placing it in the upper segment of the high vulnerability categories. This score is based on a contributory score of 6 for distribution limited to Central America in the vicinity of the type locality; 8 for ecological distribution, because it is known only from one forest type, and 4 for reproductive mode, because eggs are laid in moist arboreal situations, and tadpoles undergo direct development ( Johnson et al. 2015).

Figures

Figure 4. Coloration in life of specimens of Pristimantis gretathunbergae sp. nov. and P. cruentus from eastern Panama A holotype male (MHCH 3082), Cerro Chucanti B paratype female (SMF 97520), Cerro Chucanti C left, paratype female (MHCH 3081), right P. cruentus female (MHCH 3034) D female from Cerro Chucanti, not collected E female (MHCH 3115) La Javillosa F female, Cerro La Javillosa, Ambroya, Maje Mountain Range (SMF 97517) G female (MHCH 3079), Rio Tuquesa. Colored lines point to some diagnostic characters as follow: red: blackish iris; yellow: single spine-like tubercle; turquoise: light-colored upper lip; pink: cream, yellow to red groin (red groin also shown in Suppl. material 2: Fig. S 10).

Figure 5. Preserved holotype of Pristimantis gretathunbergae sp. nov. (MHCH 3082) A left hand in ventral view B left foot in ventral view C dorsal view D ventral view E ventral view of head F lateral view of head. Scale bars: 10 mm.

Figure 6. Habitat, mating, and parental care in females of Pristimantis gretathunbergae sp. nov. from Cerro Chucanti A Habitat on Cerro Chucanti at ca. 1300 m a. s. l. B understory bromeliad with a P. gretathunbergae sp. nov. in situ (blue line) and zoomed in on inset (MHCH 3115) C amplectant pair on axillary part of bromeliad leaf (not collected) D same female after amplexus guarding eggs E female of P. gretathunbergae taking care of its eggs with a male P. cruentus species holding on the female in reverse position (not collected) F female with eggs about to hatch, note the transparency of the egg membrane (not collected).