Rhaebo ecuadorensis, Mueses-Cisneros, Jonh Jairo, Cisneros-Heredia, Diego F. & Mcdiarmid, Roy W., 2012

Mueses-Cisneros, Jonh Jairo, Cisneros-Heredia, Diego F. & Mcdiarmid, Roy W., 2012, A new Amazonian species of Rhaebo (Anura: Bufonidae) with comments on Rhaebo glaberrimus (Günther, 1869) and Rhaebo guttatus (Schneider, 1799), Zootaxa 3447, pp. 22-40 : 24-29

Rhaebo ecuadorensis sp. nov.

( Figures 1 , 2 )

Bufo guttatus glaberrimus ― Rivero. 1961. Bull. Mus. Comp. Zool. 126: 21–22 (in part).

Bufo glaberrimus ― Duellman. 1978. Univ. Kans. Misc. Publ. No. 65:116–17; Schlüter. 1981. Stud. Neotrop. Fauna Environ. 16: 221; Lötters et al. 2000. Bonn. Zool. Beitr. 49:75–78; Cisneros-Heredia. 2003. Mem. I Cong. Ecología y Ambiente, Univ. San Francisco de Quito: 17; Schlüter et al. 2004. Salamandra. 40(2): 141–160; Pramuk. 2006. Zool. J. Linn. Soc. 146:407,443.

Rhaebo glaberrimus ― Frost et al. 2006. Bull. Am. Mus. Nat. Hist., 297: 365; Pramuk et al. 2007. Global Ecol. Biogeogr. 2007: App.S1. Aguilar et al. 2010. Rev. Peru. Biol. 17(1): 005–028.

Holotype: QCAZ 32715( Figure 1 ), an adult female collected at km 38 of the YPF-Maxus road, Parque Nacional Yasuní, Provincia de Orellana, Ecuador ( Figure 3 ), 00°40’16.7”S, 77°24’01.8”W, 250 m, on 12 June 2006 by Morley Read, Silvia Aldás Alarcón, and Aldo Sornoza.

Paratypes: ECUADOR: PROVINCIA DE SUCUMBÍOS: Reserva de Producción Faunística Cuyabeno, 00° 05' 02”S, 76° 12' 54” W, 280 m (DFCH-USFQ C320–21); PROVINCIA DE ORELLANA: Tiputini Biodiversity Station, Universidad San Francisco de Quito, 00°37’05” S, 76°10’19” W, 215–300 m (DFCH-USFQ T80–82); Estación Científica Yasuní, Pontificia Universidad Católica del Ecuador, 00°40’16.7”S, 77°24’01.8”W, 250 m ( QCAZ 23887); PROVINCIA DE MORONA SANTIAGO: Quebrada del Río Napinaza, 6.6 km N of Limón, on road to Macas, 02°55’05”S, 78°24’25.2”W, 1013 m, General Leonidas Plaza Gutiérrez, ( QCAZ 26558, 38113); PROVINCIA DE PASTAZA: Bobonaza, vía a Taculí, aprox. 01°29’53.2”S 77°52’45.5” W, 900 m ( QCAZ 38325); Conambo, aprox. 01°52’21”S 76° 53’53” W, 256–393 m (DHMECN 4667); Reserva de Bosque Tropical Hola Vida, camino a las cascadas, 01° 37' S, 77° 54' W, 831 m ( QCAZ 36767; Figure 3 ).

Referred specimens: (Juveniles). COLOMBIA: DEPARTAMENTO DE AMAZONAS: Leticia, aprox. 04°12’S 69°56’W (IAvH 4524); ECUADOR: PROVINCIA DE NAPO: Estrellayacu ( QCAZ 4497–8); Napo-Galeras, Río Pusuno, aprox 01°01’25”S 77°35’06”W, 1100 m, ( QCAZ 14055); Tena, junto al Río Misahuallí ( QCAZ 3895); PROVINCIA DE ORELLANA: Tiputini Biodiversity Station, Universidad San Francisco de Quito, 00°37’05” S, 76°10’19” W, 215–300 m (DFCH-USFQ T83–84); Coca, Puerto Francisco de Orellana ( QCAZ 12); Estación Científica Yasuní, Pontificia Universidad Católica del Ecuador, 00°40’16.7”S, 77°24’01.8”W, 250 m ( QCAZ 23896, 24577); Carretera NPF a Tivacuno, aprox. 0°42’26”S 76°28’19”W ( QCAZ 30900); Bloque Shiripuno, SW border of the buffer zone of the Parque Nacional Yasuní, aprox. 0°43’33”S 76°43’33”W, 220 m ( QCAZ 8973); Loreto, Ávila Viejo, aprox. 0°38’11”S 77°25’58”W, 748 m ( QCAZ 10722); PROVINCIA DE PASTAZA: Cononaco, Bataburo Lodge, al sur de la carretera desde Cononaco, 01° 12’S, 76°42’W, 220 m ( QCAZ 39417); Pablo López de Oglán, aprox. 1°18’00”S 77°42’24”W, 800 m (DHMECN 3067); Río Pucayacu, finca km 6 vía San Ramón–El Triunfo, Parroquia Teniente Hugo Ortiz, aprox. 01°22’22”S 77°51’36”W, 950 m ( QCAZ 33237); Plataforma K 10 de la empresa de explotación Petrolera AGIP en el bloque 10, Cerca a 10 de Agosto, 01°28’28”S, 77°31’54”W, 498 m ( QCAZ 39287; Figure 3 ).

Diagnosis. A bufonid of genus Rhaebo (diagnosed on the basis of their lack of cephalic crests (except for the low parietals crests), their yellowish-orange skin secretions, presence of an omosternum and hypertrophied testes), of large-sized (SVL 156.7 mm in adult female, 92.8–127.0 mm in adult males) lacking a preocular ridge ( Figure 1 ); having the cloacal opening near the middle level of thighs ( Figure 4 C), rounded to slightly oval parotoids, and dark to cream brown groin ( Figures 1 , 2 ).

Comparisons with other species: Rhaebo ecuadorensis is phenetically similar to R. glaberrimus and R. guttatus , and juveniles may be confused with R. blombergi (Myers and Funkhouser) . Rhaebo glaberrimus ( Figures 5 , 6 ) differs by having the cloacal opening situated towards the ventral level of the thighs ( Figures 4 A–B) [cloacal opening towards the middle level of thighs in R. ecuadorensis ], smaller body size (49.6–64.6 mm SVL in adult males) [large body size (92.8–127.0 mm in adult males) in R. ecuadorensis ], mainly smooth dorsal skin [dorsal skin warty, spiculae and coni in R. ecuadorensis ], enlarged parotoid glands [rounded parotoid glands in R. ecuadorensis ], and pink and yellow groin ( Figure 6 A) [groin without pink or yellow coloration in R. ecuadorensis ]. Rhaebo guttatus ( Figure 7 ) differs by having a preocular ridge ( Figure 8 ) [absent in R. ecuadorensis ], and ventral colouration pattern with rounded light spots on a dark background ( Figure 7 C) [ventral colouration without circular light spots in R. ecuadorensis ( Figure 2 )]. Juveniles of R. blombergi have more foot webbing that R. ecuadorensis , parotoids more rounded and snout truncated in lateral profile [weakly truncated to round in R. ecuadorensis ].

Further R. blombergi inhabits the Pacific lowlands and western Andean foothills from central Colombia (departments of Chocó, Valle del Cauca, Cauca, and Nariño) to northern Ecuador (provinces of Esmeraldas, Carchi, Imbabura and Pichincha, Mueses-Cisneros 2008), while R. ecuadorensis occurs on the Amazonian lowlands of Colombia, Ecuador, Peru, Bolivia and Brazil.

Description: Based on one adult female and six adult males; large-sized toad (female = 156.7 mm SVL, males = 92.8–127.0 mm, x = 105.6 ± 14.9 SVL); head narrower than body width, slightly wider than long. Head width slightly wider than at level of tympanum (female: HW/HL = 1.18; HW/SVL = 0.38; HL/SVL = 0.32; males: HW/ HL = 1.13–1.17, x = 1.15 ± 0.15; HW/SVL = 0.37–0.39, x = 0.38 ± 0.08; HL/SVL = 0.32–0.34, x = 0.33 ± 0.10). Head subacuminate in dorsal view; snout slightly rounded to truncate dorsally, weakly rounded to truncate in lateral view. Tip of snout without fleshy vertical ridge. Distance between nostril and tip of snout/distance between nostril and eye = 0.12 in female, 0.21–0.31 (x = 0.26 ± 0.38) in males. Nostrils open posterior to anterior rim of mouth, below canthus rostralis in slightly swollen area. Nostrils oblique, oval, directed laterally. Dorsal edge of nostril rounded, ventral edge straight to concave. Distance between nostrils/distance between nostril and eye = 1.10 in female, 1.15–1.22 (x = 1.18 ± 0.28) in males. Internarial area flat to weakly concave. Top of head from snout to anterior corners of eyelids flat. Interorbital and occipital region flat, with some low and slender tubercles near parotoids. Upper eyelid narrower than interorbital area, with low, slender tubercles. Upper eyelid width/IOD = 0.74 in female, 0.73–0.79 (x = 0.76 ± 0.24) in males. Inner and outer rim of upper eyelid not delineated by tubercles. Outer rim of upper eyelid not projecting beyond eye. Cephalic crests absent with exception of parietal crests, which are low in adult males, some pronounced in female holotype. Canthus rostralis straight, weakly fleshy in the males, fleshy in the holotype; projecting over loreal region. Loreal region weakly concave to flat, with some small, regularly distributed spiculae and coni, extending to the post-tympanic region. Lips not flared. Eyes with horizontally oval pupil. Preorbital ridge absent. Tympanum oval, 51.3% of eye length in the female, 44.2–53.0% (x = 48.3 ± 3.5) in the males; anterior 3/5 (or all) of tympanum visible. Supratympanic ridge present, fleshly. Parotoids large, distinct, rounded to slightly oval. Parotoid width 52.7% of parotoid length and 62.6% of interparotoid distance in the female, 53.1–61.9% (x = 56.1 ± 3.1) of parotoid length and 59.2–69.9% (x = 63.3 ± 3.7) of inter-parotoid distance in the males. Parotoids smooth, with nearly regularly distributed pores. Outer margin of parotoids without indentations. Inter-parotoidal region without evident crests (except in holotype). Skin of dorsum of body smooth, bearing some slender and low tubercles in sacral region and small rounded and prominent warts on postsacral region. Continuous lateral oblique row of round and oval, low and little evident o conspicuous warts, from parotoids to ½ of parotoid-groin distance. Ventral skin smooth, with some low tubercles mainly on throat and chest.

Forelimbs long, forearms somewhat robust in adult males, with warts, spiculae and coni on upper surface and flanks. Hand length 23.9% of SVL in the female, 24.8–29.2% (x = 26.6 ± 1.6) in males. Fingers without webs; with fleshy and bulbous tips. Finger I longer than II. Super-numerary palmar tubercles few, rounded and low. Subarticular tubercles rounded and evident. Palmar tubercle large, rounded, 1.2–1.5 times the size of rounded thenar tubercle. Ulnar tubercles and ulnar fold absent. Metacarpal fold absent ( Figure 9 D).

Hind limbs long. Thighs somewhat robust. Upper surface with some warts, spiculae and coni extending up the thighs. Inner tarsal fold evident and fleshy, 1/2– 2/3 of the tarsal length. Tubercles on outer edge of tarsus absent. Foot and tibia lengths 37.7% and 43.9% of SVL in the female, 35.9–41.8% (x = 38.8 ± 2.4) and 36.5–43.4% (x = 40.8 ± 2.6) of SVL in the males. Toes with fleshy, bulbous tips. Toes basally webbed. Foot-webbing formula I (1–1.5)–(1.5–2+) II (1–1.5)–(3–3+) III (1.5–2-)–(3½–3½) IV (3½–3½)–(1–2+) V. Supernumerary plantar tubercles low, round, scarce. Metatarsal inner tubercle elongate to oval, 1.2–1.3 times size of oval to round outer tubercle. Metatarsal fold absent ( Figure 9 ). Musculus adductor longus present. Omosternum present.

Tongue rounded, not notched posteriorly, 2/3 of its extension adherent to floor of mouth. Choanae rounded to oval, large, not concealed by palatal shelf of maxillary arch. Males with small, subgular vocal sac; vocal slits long, lateral and posterior to tongue. Nuptial pads dark brown or cream on fingers I and II. Cloacal opening towards the middle level of thighs ( Figure 4 C).

Colouration in life. (Based on DFC´s filed notes and color slides). Dorsal background colouration varying from pale to dark brown, orange-brown or olive-brown. Most specimens have low, dark brown to black warts scattered on dorsal surfaces. Parotoid glands slightly paler than dorsal colouration in most specimens. Background colouration on the sides of the head, tympanic area, arms, legs, flank, and groin dark brown to black (no flash colours in the groin) usually with pale low warts, especially on the posterior flanks and upper lip. Postrictal warts white to creamish. If legs are pale brown, they usually have dark spots sometimes forming indistinct bands. Background colour of the throat and chest varies from dark brown to black, marbled with cream or white; that on the venter varies from tan-cream to dark brown. White post-cloacal warts. Iris black with abundant bronze to golden punctuations especially concentrated around the golden circumpupillary ring ( Figure 2 ).

Colouration in preservative (70% ethanol). Dorsum light to dark brown. Parotoids yellowish-brown dorsally and dark brown to black laterally in most specimens (some juveniles have the same dorsal colouration throughout). Sides of head light brown. Body flanks dark brown; dorsal and flank colour sharply-separated. Arms and legs black or dark brown with or without dark to black warts; sometimes with indistinct dark bands. Throat and chest dark brown to grey, marbled with cream. Venter cream to dark brown or dark brown with some irregular creamish stain. ( Figure 1 ).

Measurements of female holotype (in mm). SVL: 156.7, HL: 50.3, HW: 59.6, IOD: 19.0, Upper eyelid width: 14.0, Internarial distance: 13.0, Parotoid length: 36.8, Parotoid width: 19.4, Inter-parotoid distance: 31.0, Tympanum diameter: 7.7, Eye diameter: 15.0, Eye-nostril distance: 11.8, Nostril-snout distance: 1.4, Tibia length: 68.8, Foot length: 59.1, Hand length: 37.5.

Measurements of the type series. The measurements of the type series are presented in Table 1 .

Natural history. Most specimens have been found on the leaf litter, especially after heavy rains. At the Tiputini Biodiversity Station, Province of Orellana, Ecuador, Rhaebo ecuadorensis was usually found in Lowland Evergreen Non-Flooded forests (= terra firme forests) amidst the leaf litter in the vicinities of small creeks during the late afternoon and early evening. QCAZ 32715 and QCAZ 23887 were collected on a paved road in an area of Terra firme forest. QCAZ 38325 was collected at the margin of a stream (about 3 m width). This specimen exuded a yellow excretion from the parotoid glands. QCAZ 36767 was collected on leaf litter. Other specimens have been found under trunks or among stones in the river banks.

Etymology. The specific name of this new species is proposed to honour the Republic of Ecuador, as a tribute to its people and natural diversity. Despite being one of the smallest countries on the continent of South America, Ecuador is one of the 10 megadiverse countries of the world. The examination of Ecuadorian material allowed us to determine the existence of this undescribed species of Rhaebo previously confused with R. glaberrimus and R. guttatus .

Conservation status. Unfortunately the information available on the current state of Rhaebo ecuadorensis populations, and the current state of their habitat is limited, so we suggest categorize Rhaebo ecuadorensis as Data Deficient (DD).

Distribution. Rhaebo ecuadoriensis is distributed across the Amazonian regions of southeastern Colombia, Ecuador, and northern Peru, at elevations between 215–1100 m a.s.l. ( Figure 3 ). Although we do not examine directly the specimens reported by Lötters et al. (2000), according to their comments and personal observations of JJM (see Remarks) we conclude that Rhaebo ecuadorensis also is distributed from Central Amazon of Brazil and Bolivia.

Remarks. Recently we found a specimen of Rhaebo (QCAZ 3812), collected in Taisha, Provincia de Morona Santiago, Ecuador, ca. 2°20'26”S 77°27'34"W ( Figure 3 ), phenetically similar to R. ecuadorensis . The specimen is an adult female with numerous eggs and well convoluted oviducts, of 94.0 mm SVL (versus 156.7mm in the holotype of R. ecuadorensis ). Externally we do not find marked differences other than SVL, to recognize this specimen as another different species, for this reason we refer this specimen to R. ecuadorensis , until more specimens are collected and studied.

Aguilar et al. (2010) reported " Rhaebo glaberrimus " from Peru, between 300-1400 m a.s.l.; however, although we did not examine directly specimens from Peruvian Amazon, we confirmed the report of Rhaebo ecuadorensis to Peru from the picture provided by Schlüter (1981) of a specimen of Panguana ( Figure 3 ), a tributary of the Rio Pachitea (at 9 °37'S 74°56'W, ca. 260 m a.s.l.), clearly without preocular ridge. Rodriguez & Duellman (1994) reported a photograph of " R. glaberrimus " of a specimen from Iquitos region, but the photo quality is not very good, and it is not possible to distinguish with certainty whether this specimen corresponds to R. ecuadorensis or to a juvenile of Rhaebo guttatus , therefore the identity of this specimen is in doubt and must be confirmed by direct examination.

Lötters et al. (2000) examined three specimens of Rhaebo ecuadorensis (as R. glaberrimus ) from Ecuador, adult specimens of Rhaebo guttatus from French Guyana and subadults from the Central Amazon of Brazil, and four specimens of Rhaebo guttatus from Bolivia. From his observations we can distinguish that one of the specimens of the Central Amazon of Brazil, and a specimen from Bolivia, do not present preocular ridge and ventrally differ from the general coloration of R. guttatus . JJM noted that the condition of the preocular ridge in Rhaebo guttatus , can be seen externally in juveniles from 25.5 mm SVL, so that the specimen reported by Lötters et al. (2000) from Brazilian Central Amazon (with 32.2 mm SVL) without preocular ridge may be referred to R. ecuadorensis . Meanwhile, the exemplar of Bolivia (CBF 3345), from Parque Nacional Noel Kempff, Provincia Velasco, Departamento Santa Cruz ( Figure 3 ), although it is a little smaller than the observed by JJM (20.0 mm SVL), can also be referred to Rhaebo ecuadorensis , confirming the presence of R. ecuadorensis in Brazil and Bolivia. Finally, JJM, in search of additional records of Rhaebo ecuadorensis in the Central Amazon of Brazil, examined photographs of two specimens deposited at Coleção de Vertebrados da Universidade Federal de Mato Grosso (UFMT), kindly provided by Dr. Robson Avila; however, both specimens [UFMT 5485 from Aripuanã municipality (59º 27'W, 10º 9'S), Northern Mato Grosso State, Brazil, and UFMT 5850 from Araputanga (15°08’S 58°54’W), western Mato Grosso State, Brazil] are Rhaebo guttatus .

Figures

FIGURE 1. Holotype of Rhaebo ecuadorensis sp. nov. Dorsal (A), ventral (B) and lateral (C) views, QCAZ 32715, adult female, 156.7 mm. SVL. Photos by Luis A. Coloma.

FIGURE 2. Rhaebo ecuadorensis sp. nov. in situ. (A) Dorsolateral view of Paratype, DHMECN 4667, adult male, 127.0 mm SVL. Photo by Mauricio Ortega; (B) dorsolateral and (C) ventral view of QCAZ 33237 from Pucayacu, Provincia de Pastaza, Ecuador (female juvenile 68.9 mm SVL); (D) dorsolateral and (E) ventral view of QCAZ 38113 from Napinaza, Provincia de Morona Santiago, Ecuador (adult male of 92.8 mm. SVL). Photos B – E by Luis A. Coloma.

FIGURE 3. Geographic distribution of Rhaebo ecuadorensis sp. nov. 1. Estación Biológica Tiputini; 2. Quebrada Napinaza; 3. Cuyabeno; 4. Type locality (white circle): Parque Nacional Yasuní; 5. Bobonaza; 6. Conambo; 7. El Porvenir; 8. Río Misahuallí; 9. Bloque Shiripuno; 10. Ávila Viejo; 11. Cononaco; 12. Pablo López de Oglán; 13. Río Pucayacu; 14. Diez de Agosto; 15. Leticia; 16. Pusuno; 17. Tivacuno; 18. Coca; 19. Puerto Bolivar; 20. Panguana; 21. Parque Nacional Noel Kempff; 22. Taisha. Squares represent literature records from Schlüter (1981) and Lötters et al. (2000).

FIGURE 4. Cloacal opening: Towards the ventral level of the thighs in Rhaebo glaberrimus (A – B), ICN 0 4969, adult male, 59.9 mm SVL. Photos by Jonh Jairo Mueses-Cisneros. Towards the middle level of the thighs in Rhaebo ecuadorensis (C), QCAZ 23887, adult female, 122.0 mm. SVL. Photo by Luis A. Coloma.

FIGURE 5. Holotype of Bufo glaberrimus. BM 1947.2. 20.56. Dorsal (A), ventral (B) and lateral (C) views. © The Natural History Museum, London (2010). All rights reserved. Photos by Martín Bustamante.

FIGURE 6. Rhaebo glaberrimus in situ. Dorsolateral (A-C) and ventral (D) views. A: adult male, 63.9 mm. SVL, ICN 4774. Photo by J. D. Lynch; B. adult, JJM 2229, from Villavicencio, Meta. Photo by J. J. Mueses-Cisneros, C-D: juvenile female, 31.9 mm. SVL, ICN 4775. Photos by J. D. Lynch.

FIGURE 7. Rhaebo guttatus in situ (A – B) from Ecuador. Photos by Martín Bustamante, and ventral view in preservative (C), ICN 51939, adult male, 126.6 mm SVL. Photo by Francisco López-López.

FIGURE 8. Preocular ridge (A) or bony projection of the posterior lateral edge of the nasal (B) in Rhaebo guttatus. A: photo by Martín Bustamante. B: ICN 54716, adult male, 122.2 mm SVL. Photo by J. J. Mueses-Cisneros.

FIGURE 9. Hands and feet in: Rhaebo ecuadorensis (A and D), holotype, QCAZ 32715, adult female, 156.7 mm. SVL; Rhaebo guttatus (B and E), QCAZ 26414, adult female, 174.3 mm SVL. Photos by Luis Coloma; and Rhaebo glaberrimus (C and F), ICN 0 4969, adult male, 59.9 mm SVL. Photos by J. J. Mueses-Cisneros.

Tables

TABLE 1. Measurement (in millimeters) of the type series of Rhaebo ecuadorensis sp. nov.

SEX SVL HL HW IOD	QCAZ 32715 Female 156.7 50.3 59.6 19.0	QCAZ 38325 Male 95.5 31.8 36.5 12.2	QCAZ 26558 Male 95.8 32.5 36.8 12.8	QCAZ 23887 Male 122.0 38.4 45.0 14.2	QCAZ 38113 Male 92.8 31.0 35.7 12.1	QCAZ 36767 Male 100.4 31.7 36.7 12.6	DHMECN 4667 Male 127.0 41.8 47.3 17.8
Upper eyelid width Eye-nostril distance Eye diameter Nostril-snout distance	14.0 11.8 15.0 1.4	9.5 7.1 12.6 1.8	9.8 6.4 9.5 1.9	10.6 9.1 11.5 2.1	9.6 6.6 10.0 1.4	9.5 7.1 11.1 2.2	12.9 8.8 12.4 2.2
Internarial distance Tympanum diameter	13.0 7.7	8.6 5.9	7.8 4.2	10.5 6.1	7.8 4.5	8.4 5.7	10.1 6.1
Parotoid length Parotoid width Inter-parotoid distance Tibia length	36.8 19.4 31.0 68.8	24.3 12.9 21.8 34.9	23.1 12.8 20.5 39.1	28.3 15.3 21.9 52.9	22.8 12.6 20.3 39.1	24.7 14.0 21.5 39.3	24.4 15.1 24.6 54.3
Foot length Hand length	59.1 37.5	34.3 23.7	39.7 26.4	47.0 30.6	38.8 27.1	36.7 26.2	49.1 33.7