Centrolene charapita, Twomey, Evan, Delia, Jesse & Castroviejo-Fisher, Santiago, 2014

Twomey, Evan, Delia, Jesse & Castroviejo-Fisher, Santiago, 2014, A review of Northern Peruvian glassfrogs (Centrolenidae), with the description of four new remarkable species, Zootaxa 3851 (1), pp. 1-87 : 12-17

Centrolene charapita new species

Figures 4–6

Centrolene sp. 1 Castroviejo-Fisher, Guayasamin, Gonzalez-Voyer, and Vilà 2014

Holotype. MHNCP 13933, adult male in good state of preservation (left hind limb was cut below the knee and preserved in 96% ethanol for DNA analyses) from near the village of La Oliva past the village of Muyo (a larger village roughly 49 km N from Bagua), Amazonas, Peru (5°18'3.86"S, 78°23'44.57"W, 682 m), collected by M. Guerra Panaijo, E. Twomey, and S. Castroviejo-Fisher on 2 April 2010.

Paratopotype. MNCN 45392, same data as holotype.

Generic placement. The new species is placed in the genus Centrolene on the basis of our phylogenetic analyses that included complete or partial sequences of the mitochondrial genes 12S and 16S of the two known individuals of C. charapita ( Fig. 2b ). Additionally, the following phenotypic characters frequently observed in species of Centrolene are present in the new species (sensu Guayasamin et al. 2009): trilobed liver, covered by a transparent hepatic peritoneum; ventral parietal peritoneum white anteriorly and transparent/translucent posteriorly; bones green in life; dorsum lavender in preservative; dorsum of males with spicules during breeding season; nuptial pads conspicuous in males; enameled pericloacal warts. However, the value of these characters as synapomorphies for Centrolene needs to be tested.

Diagnosis. The following unique combination of characters distinguishes Centrolene charapita from other species of glassfrogs: (1) a dentigerous process on each vomer, each bearing a row of 4–6 small vomerine teeth; (2) snout truncate in dorsal view and truncate (slightly rounded) in profile; (3) tympanum covered by skin, not visible through skin; in preservative tympanic annulus not visible externally but appreciable under magnification in life; supratympanic fold absent; (4) dorsal skin texture complex, in life and preservative smooth with enameled microspicules and low enameled warts on ocelli, conspicuous enameled warts forming an irregular lateral band from snout to mid-part of body and extending into the dorsoposterior edge of the upper arm, skin of the venter and thighs coarsely areolate while all other ventral surfaces are smooth; (5) cloacal ornamentation conspicuous, formed by folded skin bearing four large enameled warts projected anteriorly (flaps,) surrounded by various lower warts with or without enameling; (6) parietal peritoneum anterior third white, posterior two-thirds transparent (state P2); pericardium, hepatic, renal, and gonadal peritonea transparent, visceral (stomach and intestines) peritoneum white; (7) liver with three lobules (state H0); (8) humeral spines not present; (9) webbing formula of fingers III 2 - 1 + IV; (10) webbing formula of toes I 1 /2 - 2- II 1 - 2 - III 1 - 2 IV 2 - 1 V; (11) scalloped enameled ulnar and tarsal folds, extending from fringe on postaxial edge of Finger IV to elbow and from fringe on postaxial edge of Toe V to ankle, respectively; (12) nuptial pad Type I, not pigmented, enameled glands present on webbing and fringes of finger and toes, prepollex and prepollical spine concealed by skin; (13) when appressed, Finger I of equal length with Finger II; (14) eye diameter 2.5 times the width of disc on Finger III; (15) coloration in life: dorsal and dorsolateral surfaces with yellow or pale green spots of different size (ocelli) bearing enameled warts and microspicules set in a dark green reticulum (darker around the ocelli), upper lip and tip of fingers and Toes I, II, and III white (enameled), ventral surfaces, flanks, upper arms, Fingers I and II, and Toes I and II not pigmented, bones green; (16) coloration in preservative: dorsal and dorsolateral surfaces with cream spots of different size (ocelli) bearing enameled warts and microspicules set in a lavender-greyish reticulum formed by minute melanophores that are darker around the ocelli, upper lip and tips of fingers and toes I, II, and III white (enameled), ventral surfaces, flanks, upper arms, Fingers I and II, and Toes I and II not pigmented; (17) iris in life off-white to light grey with yellow tones and black dots and reticulation with a black ring delimiting the iris, iris in preservative white with black dots and reticulation with a black ring delimiting the iris; (18) in life and preservative tip (discs) of fingers and toes white (enameled), Finger IV and Toes IV and V pigmented, Finger III and Toe III not pigmented but for a small group of melanophores towards the tip, Fingers and Toes I and II not pigmented; (19) large size adult males, SVL = 34.7–37.0 mm (N = 2), unknown in females.

Comparisons. Specimens of Centrolene charapita have a unique combination of characters that allows easy differentiation from all other known species of centrolenids. The presence of scalloped enameled ulnar and tarsal folds together with its large size (SVL> 34.0 mm) and a truncated snout in profile help diagnose this unique species. Specimens of Ce. daidaleum, Ce. paezorum , Ce. geckoideum, Ce. savagei , Ce. solitaria , Cochranella mache , Co. phryxa , Co. resplendens and V. uranoscopa have scalloped enameled ulnar and tarsal folds, weakly so in Ce. huilense , Ce. muelleri , and Nymphargus ocellatus ; however all the aforementioned species are smaller (adult males SVL <30.0 mm) and have a sloping snout in profile, except Ce. geckoideum , which has a truncated snout in profile but is much larger than the new species, up to 83.5 mm SVL in males and 72.0 mm SVL in females. Additionally, none of these species have the characteristic ocelli on dorsum and enameled warts on finger and toe webs and fringes of Ce. charapita (specimens of N. ocellatus have ocelli but no webs between Finger III–IV). Our analysis retrieved Ce. geckoideum as the sister species of Ce. charapita , but the following external characters are clearly diagnostic (character states of Ce. charapita in parenthesis): adult males with large and externally projecting conical humeral spines (humeral spines absent), forearms hyper-atrophied (normal), dorsal coloration dull green (dorsal coloration green with ocelli, Figs. 4 and 5 ), diameter of eye smaller than that of disc of Finger III (larger), adult males SVL> 50.0 mm (<40.0 mm).

Description of holotype. Adult male with SVL 37.0 mm. Head about 1/3 wider than body; head width 36% of SVL; head width 1.1 times head length. Snout truncate in dorsal view, in lateral view truncated (slightly rounded); eye-nostril distance/eye diameter 0.61 and eye-nostril distance/interorbital distance 0.88. Loreal region concave, nostrils round, flush with surrounding skin, slightly elevated; internarial region concave anterodorsally; canthus rostralis well defined. Eyes medium, directed anterolaterally, eyes angled 45.0° relative to midline (where anteriorfacing eyes would be 90° relative to midline); eye diameter 2.5 times wider than width of disc on Finger III; eye diameter 52% of head length and 1.44 times interorbital distance. Tympanum covered by skin, not visible through skin, tympanic annulus appreciable under magnification in life but not in preservative, supratympanic fold absent. A dentigerous process on each vomer present, each bearing a row of 4–6 vomerine small teeth (their size is so small that we could not determine the exact number); choanae large, drop-shaped, separated more widely than nostrils; tongue round, white in preservative, anterior 3/4 attached to floor of mouth; vocal slits present, extending from the sides of the base of tongue to the level of the mandibular joints. Forelimbs relatively robust, with forearm flattened and roughly 2 times as wide as arm; ulnar fold present, white (enameled) and scalloped; humeral spine absent. Relative length of fingers: I ~ II <IV <III; finger discs wide, rounded, just larger than toe discs, discs of Fingers I, II, III white (enameled), disc of Finger IV colored as dorsal skin; webbing absent between Fingers I and II, basal webbing between Fingers II and III, webbing between Fingers III and IV with formula III 2 - 1 + IV (see also Fig. 6 ). Prepollex concealed; subarticular tubercles round; supernumerary tubercles absent, palmar tubercle elliptical, thenar tubercle ovoid; nuptial pad present on medial side of Finger I, running from base of finger to about halfway up finger (Type I); enameled glands present on webbing and fringes of fingers. Hind limbs slender, tibia length 57% of SVL; tarsal fold white (enameled) and scalloped; discs of toes round, discs of Toes I, II, III white (enameled), disc of Toes IV and V colored as dorsal skin; inner metatarsal tubercle ovoid and slightly protruding; outer metatarsal tubercle not noted. Webbing formula of feet: I 1 /2 - 2- II 1 - 2 - III 1 - 2 IV 2 - 1 V. In preservative, dorsal and dorsolateral surfaces with cream spots of different size (ocelli) bearing enameled warts and microspicules set in a lavander-greyish reticulum formed by minute melanophores that are darker around the ocelli; dorsal skin texture complex, smooth with enameled microspicules and low enameled warts on the ocelli, conspicuous enameled warts forming an irregular lateral band from snout to mid-part of body and extending into the dorsoposterior edge of the upper arm, skin of the venter and thighs coarsely areolate while all other ventral skin is smooth. Cloacal opening at level of upper thighs, partially concealed by superior dermal fold, cloacal ornamentation conspicuous, formed by folded skin bearing four large enameled warts projected anteriorly (flaps) surrounded by various lower, enameled or not, warts.

Coloration in life of both types ( Fig. 4 ). Dorsal and dorsolateral surfaces with yellow or pale green spots of different size (ocelli), bearing enameled warts and microspicules, set in a dark green reticulum (darker around the ocelli). Upper lip and tips (discs) of fingers and toes I, II, and III white (enameled). Ventral surfaces, flanks, upper arms, Fingers I and II, and Toes I and II not pigmented. Iris delimited by a black ring, background coloration off white to light grey with yellow shades and black dots and reticulation. Parietal peritoneum anterior third white, posterior two-thirds transparent. Visceral peritoneum (stomach and intestines) white. Hepatic peritoneum transparent. Other peritonea not visible in life.

Coloration in preservative of both types ( Fig. 5 ). Dorsal and dorsolateral surfaces with cream spots of different size (ocelli), bearing enameled warts and microspicules, set in a lavender-greyish reticulum formed by minute melanophores that are darker around the ocelli. Upper lip and tips (discs) of fingers and toes I, II, and III white (enameled). Ventral surfaces, flanks, upper arms, Fingers I and II, and Toes I and II not pigmented. Finger III and Toe III not pigmented but for a small group of melanophores towards the tip. Finger IV and Toes IV and V pigmented as dorsum. Iris delimited by a black ring, background coloration white with black dots and reticulation. Parietal peritoneum anterior third white, posterior two thirds transparent, pericardium, hepatic, renal, and gonadal peritonea transparent, visceral (stomach and intestines) peritoneum white. Color of peritonea based on direct observations on the dissected holotype.

Measurements. Holotype measurements (in mm) with paratype measurements given in parentheses: SVL 37.0 (34.7); HL 11.9 (10.5); HW 13.3 (12.5); IND 2.8 (2.6); IOD 4.3 (3.8); ED 6.2 (6.5); EA 44.8° (not measured in paratype); EW 3.7 (3.3); END 4.4 (4.3); HaL 11.0 (11.0); 3DW 2.5 (2.3); TL 19.6 (19.0); SL 21.1 (20.1); FL 16.3 (15.5).

Variation. Except for the size there is no evident variation in the two individuals collected. Even the number and distribution of the large dorsal ocelli are virtually the same in both specimens.

Distribution and ecology. This species is known only from the type locality ( Fig. 7 ). Both specimens were found perched on vegetation along a relatively large secondary stream east of the Marañón River. This species likely occupies other streams in the mostly undisturbed forests of the surrounding mountains. The holotype was found perched on a branch approximately 2 m above the water. Its vocal sac was extended as typical of glassfrogs that have been recently calling. The paratype was found on the upper side of a Heliconia leaf ( Heliconiaceae ) approximately 5 m above the water. Other amphibians found in the same stream included Ameerega trivittata , Bolitoglossa altamazonica , Cochranella erminea , Hyloscirtus sp., Rulyrana mcdiarmidi , Pristimantis aff. acuminatus , Pristimantis sp., and Rhaebo glaberrimus . Advertisement call, fighting behavior, egg clutches, parental care, and tadpole are unknown for this species.

Etymology. As applied here, the specific epithet “ charapita ” derives from a type of small yellow chili pepper (aji charapita ) that is endemic to the Amazon lowlands and used in a variety of Amazonian dishes. These peppers resemble the yellowish ocelli characteristic of the dorsal coloration of this new species ( Fig. 8 ).

Remarks. Because we have only analyzed sequences of two genes (12S and 16S) and our results are not highly supported ( Fig. 2b ; JK = 72; GB = 3), the phylogenetic position of Centrolene charapita might change as more molecular and/or phenotypic data are analyzed, or if more species are included, particularly species in the Centrolene geckoideum group (containing Ce. acanthidiocephalum, Ce. geckoideum, Ce. medemi, Ce. paezorum , and Ce. petrophilum). If the current phylogenetic position is corroborated, Ce. charapita would be the only species of Centrolene known to occur below 800 m.

Figures

FIGURE 4. Type series of Centrolene charapita new species. a) holotype (MHNCP 13933, SVL 37.0 mm), b) ventral view of holotype, c) paratype (MNCN 45392 SVL 34.7 mm). Note yellow / pale green spots (ocelli) set in a dark green reticulum along the dorsum, giving the appearance of the aji charapita pepper from the Amazonian region of Peru.

FIGURE 5. Centrolene charapita new species holotype, in preservative (MHNCP 13933, SVL 37.0 mm), showing dorsal aspects and head shape.

FIGURE 6. Ventral surfaces of hand and foot in Centrolene charapita new species holotype, MHNCP 13933.

FIGURE 7. Distribution of Centrolene charapita new species (blue dot); type locality, La Oliva, Amazonas, 5 ° 18 ' 3.86 " S, 78 ° 23 ' 44.57 " W, 682 m; Ce. muelleri (red dots); (1) type locality, 14 km W of Venceremos, San Martín, approx. 5 ° 40 ' 58.96 " S, 77 ° 46 ' 45.74 " W, 2047 m; (2) 7.4 km SE from Puente Vilcaniza, Amazonas, 5 ° 48 ' 52.25 " S, 77 ° 50 ' 6.19 " W, 1858 m; (3) Gocta waterfall, Amazonas, 6 ° 1 ' 37.80 " S, 77 ° 53 ' 15.15 " W, 1830 m; Rulyrana saxiscandens (yellow dots); (1) Abra Tangarana, San Martín, 6 ° 16 ' 52.86 " S, 76 ° 43 ' 57.86 " W, 1047 m; (2) km. 26 on Tarapoto-Yurimaguas road, San Martín, 6 ° 24 ' 44.79 " S, 76 ° 19 ' 2.09 " W, 684 m; (3) San Jose, San Martín, 6 ° 25 ' 14.67 " S, 76 ° 17 ' 28.42 " W, 518 m; (4) type locality, Ahuashiyacu waterfalls, San Martín, 6 ° 27 ' 19.69 " S, 76 ° 18 ' 32.33 " W, 797 m; (5) 2.3 km E from Ahuashiyacu, San Martín, 6 ° 27 ' 30.28 " S, 76 ° 17 ' 14.35 " W, 988 m. Asterisks on map indicate type localities for each species.

FIGURE 8. Left: The yellow / pale green spots on the dorsum of Centrolene charapita new species resemble aji charapita peppers from the Amazonian region of Peru (photo courtesy of Tony Dunnell), from which it takes its name. Right: Juan Manuel Guayasamin (photo courtesy of Jessica Deichmann) with a specimen of Agalychnis callidryas in 2010. We named Cochranella guayasamini after him in recognition of his friendship and contributions to glassfrog systematics and natural history.

FIGURE 2 a. Phylogeny of Centrolenidae, Allophrynidae, and outgroups. Strict consensus tree of 52 most parsimonious trees (cost = 16898 steps). Values above and below branches indicate jackknife and Goodman-Bremer support, respectively. a) outgroups, Allophrynidae, Celsiella, and Hyalinobatrachium; b) Nymphargus and Centrolene; c) Vitreorana, Teratohyla, Chimerella, Espadarana, Cochranella, Sachatamia, and Rulyrana.

FIGURE 2 b. Phylogeny of Centrolenidae, Allophrynidae, and outgroups. Strict consensus tree of 52 most parsimonious trees (cost = 16898 steps). Values above and below branches indicate jackknife and Goodman-Bremer support, respectively. a) outgroups, Allophrynidae, Celsiella, and Hyalinobatrachium; b) Nymphargus and Centrolene; c) Vitreorana, Teratohyla, Chimerella, Espadarana, Cochranella, Sachatamia, and Rulyrana.