Chimerella corleone, 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 : 19-24

Chimerella corleone new species

Figures 10–12 , 16

Chimerella sp. Castroviejo-Fisher, Guayasamin, Gonzalez-Voyer, and Vilà 2014 Holotype. CORBIDI 10467, adult male collected from a stream near the village of San Jose in the Cainarachi valley near Tarapoto, Departamento San Martín, Peru. This stream crosses the Tarapoto-Yurimaguas road approximately 400 m before San Jose when traveling in the direction of Yurimaguas. The collection site is reached by climbing the stream approximately 0.5 km and is located at the top of a large waterfall (approximately 6°25'2.59"S, 76°17'21.33"W, 610 m). Collected by J. Delia on 26 May 2011.

Paratopotypes. CORBIDI 10469 (male), CORBIDI 10465 (female), CORBIDI 10466 (male), CORBIDI 10475 (male), same locality and collection data as holotype, with the exception that CORBIDI 10475 was collected on 31 May 2011.

Generic placement. The new species is placed in the genus Chimerella on the basis of our phylogenetic analyses that included complete or partial sequences of the mitochondrial genes 12S and 16S of four specimens of the type series of Ch. corleone ( Fig 2c ; JK = 99; GB = 15). This species shares the following phenotypic characteristics with Ch. mariaelenae , the only other member of the genus: humeral spine present in adult males, vomerine teeth absent, bones green, parietal peritoneum transparent (no bib-like patch visible), liver bulbous with rounded lobes, hepatic, cardiac, and visceral peritonea white, males vocalize from upper surfaces of leaves. However, the value of these characters as synapomorphies for Chimerella needs to be tested.

Diagnosis. The following combination of characters can distinguish Chimerella corleone from other species in the family: (1) dentigerous process of the vomer and vomerine teeth absent; (2) snout truncate in dorsal view, rounded in lateral view; (3) tympanum and tympanic annulus evident, with a slight dorsal inclination; (4) dorsal skin finely shagreened, ventral skin granular, (5) cloacal ornamentation consisting of two round, low, unpigmented tubercles lateral to cloaca on ventral side; (6) parietal peritoneum transparent with no bib-like patch visible; pericardial peritoneum pigmented (white); hepatic and visceral peritonea pigmented (white), urinary bladder unpigmented, (7) liver bulbous with two broadly rounded right/left lobes present on either side of the falciform ligament; (8) humeral spine present in adult males; (9) finger webbing absent between Fingers I and II, basal webbing between Fingers II and III, and between Fingers III and IV III 2 + - 2+ IV; (10) toe webbing I 1 + - 2 II 1 - 2 + III 1 + - 3- IV 3 - - 0+ V; (11) enameled fringe present on postaxial edge of Finger IV, metacarpal fold and enameled fringe on postaxial edge of toe V absent, ulnar fold present, white; tarsal fold present as a line of low white bumps on the lateral edge of tarsus; (12) nuptial pads present as small pad on medial side of Finger I, running from base of finger to about halfway up finger (Type I); prepollex not enlarged, concealed; prepollical spine not projecting (spine not exposed); (13) when appressed, Finger I longer than II; (14) diameter of eye diameter 2.1 times greater than width of disc on Finger III; (15) in life, dorsum green with scattered yellowish-green flecks; bones green; (16) coloration in preservative dull green with scattered pale yellow flecks; (17) iris coloration in life silvery white with dark grey reticulations; (18) distribution of melanophores on digits slightly variable, typically absent from digits except for one specimen (CORBIDI 10475) which has scattered melanophores along Finger III; melanophores present on foot and on Toes IV–V; in life hands and feet are light green, tips of fingers and toes pale orange; (19) males call from the upper sides of leaves and on branches (N = 6); advertisement call consisting of a high pitched, percussive pair of notes; call duration 0.39 s, note duration 0.013– 0.020 s, dominant frequency of first note 7629 Hz and second note 7425 Hz, which is the highest frequency known to the family; (20) clutches observed on the lower surface of leaves, along the margin, overhanging streams (N = 3); a single clutch had 18 dark grey eggs and were deposited in a viscous grey (“smoky”) jelly; (21) SVL in males 18.8–20.0 mm (N = 4); in females 21.0 mm (N = 1).

Comparisons. Of all the centrolenid species known to have a transparent parietal peritoneum (i.e., all Hyalinobatrachium , Chimerella mariaelenae , Vitreorana antisthenesi , V. eurygnatha , V. gorzulae , V. pa r v u l a, V. uranoscopa , Teratohyla amelie , and T. pulverata ), only Chimerella mariaelenae and Vitreorana gorzulae have humeral spines in adult males. Chimerella corleone can be readily differentiated from Ch. mariaelenae ( Fig. 16 ) by iris color (silvery white with dark grey reticulations in Ch. corleone vs. distinctly reddish with violet reticulations in most Ch. mariaelenae ), dorsal color (green with yellow flecks in Ch. corleone vs. green with blue flecks in Ch. mariaelenae ), and egg clutch color (animal pole of eggs pigmented, vegetal pole cream colored, with smoky egg jelly in Ch. corleone vs. unpigmented, white eggs in a clear jelly in Ch. mariaelenae ; see Fig. 16 and natural history section below). Vitreorana gorzulae has a “bib-like white patch” ( Duellman & Señaris 2003) (vs. patch absent in Ch. corleone ). In addition, V. gorzulae has a trilobate liver (vs. liver lacking distinct lobes, appearing bulbous in Ch. corleone ), dorsal color green with no flecks (vs. green with yellowish-green flecks in Ch. corleone ), a call consisting of a pulsed single note (vs. call consisting of two tonal percussive peeps), and unpigmented eggs (vs. pigmented eggs in Ch. corleone ).

Description of the holotype. Adult male with SVL 19.0 mm. Head about 1/3 wider than body; head width 40% of SVL; head width 1.2 times head length. Snout truncate in dorsal view, in lateral view rounded; eye-nostril distance/eye diameter 0.70, eye-nostril distance/interorbital distance 0.50. Loreal region slightly concave, nostrils flush with surrounding skin, round; internarial region concave anterodorsally; canthus rostralis well defined. Eyes medium, directed anterolaterally, eyes angled 47.6° relative to midline (where anterior-facing eyes would be 90° relative to midline); eye diameter 2.1 times wider than width of disc on finger III; eye diameter 38% of head length and 71% of interorbital distance. Tympanum fairly noticeable with both annulus and membrane visible, annulus unpigmented and slightly elevated, membrane colored as dorsum; supratympanic fold weakly defined leaving entire tympanum visible, tympanum with slight dorsal inclination. Dentigerous processes on vomers absent; choanae large, circular, separated more widely than nostrils; tongue round, white in preservative, anterior 3/4 attached to floor of mouth; vocal slits present but small, just visible as small holes lateral to the tongue. Forelimbs relatively robust, with forearm broadly flattened and roughly 2 times as wide as arm; ulnar fold present, white; humeral spine present as an elongated bump, weakly defined in preservative but prominent in life ( Fig. 10 ). Relative length of fingers: II <I <IV <III; finger discs wide, rounded, just larger than toe discs, disc on Finger III 48 % of eye diameter; webbing absent between fingers I and II, basal webbing between Fingers II and III, webbing between Fingers III and IV with formula III 2 + - 2+ IV ( Fig. 11 ). Prepollex concealed; subarticular tubercles round, faint; supernumerary tubercles not noted, palmar tubercle round and small, thenar tubercle ovoid; nuptial pads present as small pad on medial side of Finger I, running from base of finger to about halfway up finger (Type I). Hind limbs slender, tibia length 55% of SVL; tarsal fold present as a line of low white bumps on the lateral edge of tarsus; discs of toes medium, round, inner metatarsal tubercle ovoid and slightly protruding; outer metatarsal tubercle not noted. Webbing formula of feet: I 1 + - 2 II 1 - 2 + III 1 + - 3- IV 3 - - 0+ V. In preservative, dorsal skin densely covered with small round melanophores; dorsal skin finely shagreened on body, limbs, and head; skin on ventral side smooth, except on abdomen which is granular; cloacal opening at level of upper thighs, partially concealed by superior dermal fold, with two round, low, unpigmented tubercles lateral to cloaca present on ventral side, crenulated flaps absent.

Paratype CORBIDI 10466 was dissected and the internal organs appear as follows: liver with two indistinct, rounded lobes, completely covered in iridiphores (appearing white), corresponding to state H-1 sensu Cisneros- Heredia and McDiarmid (2007). Gall bladder white. For all other internal organs, the peritoneum is covered in iridophores (white) except for kidneys, which are uncovered (appearing tan in color), and gonads, which are partially covered in a white iridophore reticulum. However, in the holotype and two other paratypes that were dissected (CORBIDI 10469 and CORBIDI 10465), the liver is neither distinctly lobed nor bulbous. In both these specimens, the liver is clearly composed of two right/left lobes, but these lobes are broadly rounded and do not form free flaps ( Fig. 12 ).

Coloration in life. Dorsal surfaces green with circular greenish-yellow spots and dusted with minute dark melanophores ( Fig. 10 ). Distribution of melanophores on digits slightly variable, typically absent from digits except for one specimen. Fingers green and tips of toes light orange. Line of low white enameled bumps on the lateral edge of tarsus. Cloacal ornamentations not enameled. Iris coloration silvery white with dark grey reticulations, and with light brown spots spreading concentrically from the pupil, where they appear at higher density. Parietal peritoneum transparent; pericardium, hepatic peritonea and visceral peritonea white. Bones green.

Coloration in preservative. Body dark grayish-green with small pale yellow flecks on dorsum ( Fig. 10 ). Arms and thighs mostly white with narrow dorsal band of melanophores running along length. Forearms and lower legs colored as body. Iris and peritonea colored as in life.

Measurements. Holotype measurements (in mm) as follows: SVL 19.0, HL 6.1, HW 7.1, TD 0.5, IND 1.6, IOD 3.2, ED 2.3, EA 47.6°, END 1.9, HaL 5.7, 3DW 1.1, TL 9.9, SL 10.4, FL 7.9. For measurements of paratypes see Table 1 .

Variation. Slight variation in dorsal coloration has been noted in this species ( Fig. 10 ). Three out of five types are light green with small yellowish-green flecks, whereas two individuals (CORBIDI 10469 [male] and CORBIDI 10465 [female]) have a darker-green dorsum with larger, more prominent yellow flecks. Among males, humeral spine morphology is somewhat variable. In CORBIDI 10469 and CORBIDI 10475, the humeral spine is needlelike (as in drawing of Chimerella mariaelenae in Guayasamin et al. 2009: Fig.13 ). CORBIDI 10466 also has a needle-like bump but less protuberant than the two previously mentioned specimens. The holotype (CORBIDI 10467) has only a slight, elongated bump. The female (CORBIDI 10465) lacks any such bumps or spines.

Vocalizations. We obtained a recording of Chimerella corleone from a single male collected in amplexus (CORBIDI 10467; Fig. 13 ) at the type locality on 22:00, 26 May 2011. In captivity, the male was dislodged from the female’s back three times until we obtained a recording of a single call (at 1:00 on 28 May 2011). The male would initiate vocal activity ca. 10–30 minutes after being dislodged, giving a two note call that corresponded to the advertisement call given by other males in the field. Each time the female approached the male, he would change the call by adding an additional note (three notes). In the field we were able to instigate the three-note call by gently brushing vegetation near the calling male (CORBIDI 10466). In the field males called irregularly, with long periods between each call (5–15 minutes).

The advertisement call is a high pitched, percussive “peep-peep”, consisting of two short notes given in quick succession. The entire call (counting both notes together, plus the silence between) is 0.39 s in length. The individual notes are high-energy bursts of short duration (0.013– 0.020 s), spaced 0.271 s apart. Dominant frequency of first note 7629 Hz and second note 7425 Hz.

Distribution and ecology. Chimerella corleone is known only from the type locality ( Fig. 14 ) where all individuals were found on low herbaceous vegetation growing along vertical rock walls within waterfall spray zones ( Fig. 15 ). Males called from horizontal branches and the upper surfaces of broad-leaf herbs, from 2–4 m above the ground. Despite 12 nights working a large section of this stream, Ch. corleone was only found near waterfalls. In addition, ET and J. L. Brown had extensively searched the lower parts of this stream between the years of 2004–2006 and never encountered this species. In captivity, a pair deposited 18 pigmented eggs in a smoky, viscous jelly along the lower margins of a leaf placed in the tank, which contrasts that observed in Ch. mariaelenae ( Fig. 16 ). Two additional clutches at the waterfall corresponding to this species were found on the margins of the underside of a leaf, in a smoky jelly ca. 2 m above the surface of the water. The centrolenid diversity along this stream includes Cochranella guayasamini , Hyalinobatrachium carlesvilai , H. pellucidum , Rulyrana saxiscandens , and Teratohyla midas . In addition, a juvenile Cochranella resplendens has been found less than 1 km away and is likely to occur in this stream (J. L. Brown and ET, pers. obs.). Combat behavior, tadpoles, and parental care unknown for this species.

Etymology. The specific name is a patronym for the Corleone family depicted in Mario Puzo’s novel The Godfather and the trilogy of films directed by Francis Ford Coppola.

Remarks. Chimerella corleone represents the second species of this genus ( Fig. 2c ). The original arrangement of Chimerella ( Guayasamin et al. 2009) was a monotypic genus containing only Ch. mariaelenae , a species with a unique combination of characters within the Centrolenidae (transparent parietal peritoneum, white bulbous liver, and humeral spines in adult males). The fact that Ch. corleone possesses a similar combination of morphological characters as Ch. mariaelenae supports the hypothesis that the two are sister species. Chimerella mariaelenae has recently been registered from the Cordillera de Campanquis in northern Peru ( Catenazzi & Venegas 2012), and it appears to be morphologically identical to Ecuadorian populations. To date, this genus appears to be restricted to the eastern versant of the Andes, making it the only Andean glassfrog genus that is restricted to a single versant. The call of Ch. corelone has one of the highest frequencies registered for any glassfrog to date (7629 Hz, Fig. 13 ). Analyses of the call of Ch. mariaelenae would help determine whether the call of these two species provide synapomorphies for the genus.

Figures

FIGURE 10. Chimerella corleone new species in life. a) holotype, CORBIDI 10467, male (SVL 19.0 mm), b) ventral view of holotype, c) CORBIDI 10466, male (SVL 20.0 mm), d) ventral view of CORBIDI 10466, e) CORBIDI 10469, male (SVL 18.8 mm), f) CORBIDI 10465, female (SVL 21.0 mm).

FIGURE 11. Chimerella corleone new species holotype (CORBIDI 10467, SVL 19.0 mm) in preservative showing a) head, b) hand, and c) foot. The palmar surface of the hand is from paratype CORBIDI 10466.

FIGURE 12. Condition of the liver in Chimerella corleone new species. a) holotype CORBIDI 10467, and b) a female paratype CORBIDI 10465. Note that the liver is neither distinctly lobed nor bulbous. It is clearly composed of two lobes (right / left), but these lobes are broadly rounded and do not form free flaps.

FIGURE 13. Audiospectogram (upper panel) and oscillogram of the advertisement call of Chimerella corleone new species (CORBIDI 10467). This call was obtained in captivity by dislodging an amplectant pair and waiting for the male to resume calling.

FIGURE 14. Type locality of Chimerella corleone new species (blue dot) in San Jose, San Martín, 6 ° 25 ' 2.59 " S, 76 ° 17 ' 21.33 " W, 610 m. Rulyrana mcdiarmidi (purple dots), (1) 1 km S Conchay, Ecuador, approx. 3 ° 6 ' S, 78 ° 25 ' W, 1100 m; (2) type locality, 6 km S from Zamora, Ecuador, approx .. 4 ° 3 ' S 78 ° 56 ' W, 1150 m; (3) La Oliva, Amazonas, 5 ° 18 ' 3.86 " S, 78 ° 23 ' 44.57 " W, 682 m; (4) southwest Cordillera del Condor, Cajamarca, 5 ° 25 ' 16.5 " S, 78 ° 35 ' 23.2 " W, 1210 m; (5) Quebrada Goca, Amazonas, 5 ° 45 ' 50.78 " S, 77 ° 54 ' 46.52 " W, 1711 m; (6) 11.3 km WNW from Pedro Ruiz, Amazonas, 5 ° 54 ' 50.93 " S, 78 ° 4 ' 35.20 " W, 1077 m; (7) 4.7 km NW from Pedro Ruiz, Amazonas, 5 ° 55 ' 5.80 " S, 78 ° 0 ' 38.62 " W, 1238 m; (8) 0.45 km S from the town of Cocachimba, Amazonas, 6 ° 3 ' 44.28 " S, 77 ° 53 ' 36.47 " W, 1811 m. Teratohyla amelie (red dots), (1) type locality, Comunidad de Oglán, Cantón Arajuno, Ecuador, 1 ° 18 ' 65 " S, 77 ° 42 ' 41 " W, 600 m; (2) Huabico, Amazonas, 4 ° 57 ' 16.59 " S, 78 ° 12 ' 39.92 " W, 349 m; (3) Nuevo Jaen, San Martín, 7 ° 39 ' 16.20 " S, 76 ° 39 ' 24.60 " W, 591 m; (4) 10 km from Quincemil towards Pto. Maldonado, Cusco (13 ° 12 ' 3.6 " S, 70 ° 40 ' 28.9 " W, 572 m). Nymphargus chancas (yellow dots), (1) Yurilamas, San Martín, approx. 6 ° 14 ' S, 76 ° 32 ' " W, unknown elevation; (2) type locality, Abra Tangarana, San Martín, 6 ° 16 ' 52.86 " S, 76 ° 43 ' 57.86 " W, 1047 m; (3) 25 km SW from Tarapoto, San Martín, 6 ° 35 ' 38.10 " S, 76 ° 34 ' 17.24 " W, 1131 m; (4) 14 km SE from the town of Shamboyacu, San Martín, 7 ° 4 ' 8.9 '' S, 76 ° 0 ' 55.2 '' W, 1122 m. Asterisks on map indicate type localities for each species.

FIGURE 15. Type locality of Chimerella corleone new species. Males were calling from vegetation within spray zones and on the vertical faces of waterfalls. In addition to Ch. corleone, glassfrog diversity along this stream includes Cochranella guayasamini, Co. resplendens (a single specimen collected 0.6 km away), Hyalinobatrachium carlesvilai, H. pellucidum, Rulyrana saxiscandens, and Teratohyla midas.

FIGURE 16. Reproduction in glassfrogs of the genus Chimerella. a, b) Amplexus in Ch. corleone from San Jose, c) Ch. mariaelenae from Wawa Sumaco, Napo, Ecuador (this population was monitored by JD in 2007). Note difference in eye color and dorsal color between these species. d) egg clutch of Ch. corleone, note pigmented eggs in a smoky jelly, e) Ch. mariaelenae egg clutch, note unpigmented eggs in a clear jelly. Oviposition was confimed in captivity for both species, then compared to corresponding clutches in the field.

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 c. 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.

Tables

TABLE 1. Measurements of the type series of Chimerella corleone new species.

	CORBIDI 10465	CORBIDI 10466	CORBIDI 10467	CORBIDI 10469	CORBIDI 10475
SVL	21.0	20.0	19.0	18.8	18.9
HL	6.0	6.1	6.1	5.6	5.5
HW	7.9	7.4	7.1	6.9	7.4
TD	0.7	0.5	0.5	0.6	0.6
IND	1.8	1.6	1.9	1.5	1.7
IOD	3.4	2.9	3.2	3.3	3.5
ED	2.4	2.6	2.3	2.1	2.0
EA (degrees)	52.5	50.0	47.6	45.7	49.5
EW	3.2	2.9	3.2	3.0	3.0
END	1.8	1.8	1.6	1.8	1.7
HaL	5.5	5.9	5.7	6.5	5.7
3DW	0.9	0.8	1.1	0.9	1.2
TL	10.7	9.6	9.9	10.1	10.2
SL	11.5	10.3	10.4	10.2	10.5
FL	8.5	8.6	7.9	8.8	8.7
Sex	F	M	M	M	M