Oreobates antrum

Vaz-Silva, Wilian, Maciel, Natan Medeiros, Andrade, Sheila Pereira De & Amaro, Renata Cecília, 2018, A new cryptic species of Oreobates (Anura: Craugastoridae) from the seasonally dry tropical forest of central Brazil, Zootaxa 4441 (1), pp. 89-108: 93-100

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Oreobates antrum

sp. nov.

Oreobates antrum  sp. nov.

( Fig. 2–3View FIGURE 2View FIGURE 3)

Oreobates remotus  (non Teixeira, Amaro, Recorder, Sena & Rodrigues 2010)—Andrade et al. 2012.

Holotype. MNRJAbout MNRJ 91628 ( Fig. 2 View Figure ), an adult male from São Domingos municipality, in the complex of caves belonging to farm “Baraunax”, an adjacent area to the municipality of Divinópolis de Goiás (13o22’17"S, 46o23’50”W, WGS 84, 638m a.s.l.), State of Goiás, Brazil, collected on 16 March 2011 by Sheila P. Andrade, Danusy L. Santos and Edmar P. Victor Jr..

Paratopotype s. ZUFG 5889, sex not determined, MNRJ 91629–91631, MNRJ 91633, MNRJ 91635, CEPB 9839, CEPB 9840, ZUFG 5888, ZUFG 11095, adult males; MNRJ 91632, MNRJ 91634, MNRJ 91636, CEPB 9841, ZUFG 5890, ZUFG 11096, adult females, collected along with the holotype. ZUFG 11097, adult male, collected on 14 April 2011 by Sheila P. Andrade, Danusy L. Santos and Edmar P. Victor Jr.. ZUFG 8710 and ZUFG 8730, sexes not determined, collected on 0 2 December 2013 by Cézar R. Filho and Edmar P. Victor Jr.

Diagnosis. Oreobates antrum  sp. nov. is characterized mainly by the following combination of characters: 1) small size (average of SVL 22.7 in males and 26.2 in females); 2) dorsal skin smooth to finely shagreened or with scattered little tubercles; 3) snout acuminate-triangular in dorsal view; 4) snout rounded in lateral view; 5) tympanic annulus and tympanic membrane length about 62% eye length; 6) cranial crests absent; 7) dentigerous processes of vomers oblique, positioned posterior to level of choanae; 8) first finger longer than second; 9) discs on Fingers III and IV broadly enlarged truncate; 10) advertisement call composed of a single note, no harmonics with dominant frequency ranged 2070 Hz to 3273 Hz; 11) in life, dorsum brown, with a W-shaped dark brown in occipital-scapula region.

Comparison with other Oreobates  species (features of other species between parenthesis). Oreobates antrum  sp. nov. differs from the other Oreobates  species mainly by having dorsal skin smooth to finely shagreened or with scattered little tubercles (vs. dorsal skin granular in O. amarakaeri  , O. barituensis  , O. choristolemma  , O. crepitans  , O. cruralis  , O. gemcare  , O. granulosus  , O. lehri  , O. madidi  , O. machiguenga  , O. pereger  , O. quixensis  , O. sanctacrucis  , O. sanderi  , O. saxatilis  , O. berdemenos  , O. zongonensis  , and O. yanucu  ) (see Harvey & Keck 1995, Reichle & Köhler 1997, Harvey & Sheehy 2005, Padial & De la Riva 2005, Vaira & Ferrari 2008, Padial et al. 2012, Köhler & Padial 2016). From O. quixensis  , O. saxatilis  , O. pereger  , O. zongoensis  , O. madidi  , O. sanderi  , O. ayacucho  , O. lehri  , and O. gemcare  it differs by having broadly enlarged truncate discs on Fingers III and IV (vs. not enlarged and rounded) (see Harvey & Keck 1995, Padial & De la Riva 2005, Padial et al. 2012). From O. pereger  , O. berdemenos  , and O. yanucu  by the presence of a complete discoidal fold (vs. weak or incomplete) (see Pereyra et al. 2014, Köhler & Padial 2016). From O. discoidalis  , O. granulosus  , O. heterodactylus  , O. choristolemma  , O. lundbergi  , O. sanderi  , O. ayacucho  , and O. barituensis  by absence of nuptial pads (vs. nuptial pads present) (see Pereyra et al. 2014). Oreobates antrum  sp. nov. is morphologically more similar to Oreobates remotus  and O. heterodactylus  from which it differs mainly by the small size (vs. SVL= 31.6 in males and SVL= 37.7 in females of O. remotus  and SVL= 24.6 in males and SVL= 30.8 in females of O. heterodactylus  (see Teixeira Jr. et al. 2012 and Padial & De la Riva 2005), snout acuminate-triangular in dorsal view (vs. subacuminated in O. remotus  ), and absence of nuptial pads (vs. nuptial pads present in O. heterodactylus  ) (see Padial & De La Riva 2005, Teixeira Jr. et al. 2012).

Additionally, Oreobates antrum  sp. nov. differs from all species of Oreobates  by the advertisement call attributes as call duration, number of notes per call, number of pulses per call, call repetition rate, pulse rate, dominant frequency, and call structure (see bellow).

Description of the holotype. Head slightly longer than wide; head width 35.7% SVL; snout acuminatetriangular in dorsal view ( Fig. 2A View Figure ) and rounded in lateral view ( Fig. 2B View Figure ); tip of snout extends beyond the border of lower lip in lateral view; nostrils oval, located near the tip of the snout, laterally directed; canthus rostralis weakly concave in dorsal view, nearly straight in profile; upper eyelid smooth; eyes lateral; vertical dark band below the eyes; cranial crests absent; supratympanic fold evident, marked by a dark band ( Fig. 2B View Figure ); tympanic membrane and annulus distinct; tympanic membrane rounded, its horizontal diameter about half of eye length (49%); choanae large, widely separated medially; tongue slightly longer than wide, posterior margin rounded, free posteriorly about two thirds of length; vomerine dentigerous process oblique, located posteriorly to choanae; vocal slits present.

Ulnar tubercle absent; thenar tubercle oval; palmar tubercle oval, about two-thirds larger than thenar tubercle; medium-sized, rounded and conical palmar supernumerary tubercles; subarticular tubercles of fingers conical, prominent. Fringes on the fingers absent; relative finger lengths: II <I <IV <III; tips of Fingers I and II rounded and of Fingers III and IV broadly enlarged, truncate ( Fig. 2C View Figure ). Tarsus lacking tubercles; inner metatarsal tubercle oval, twice as long as outer metatarsal tubercle (rounded); plantar supernumerary tubercles small, rounded and prominent; subarticular tubercles conical, prominent; fringes on toes absent; webbing absent; toes long and slender; toe tips rounded on toes I, II and V, and slightly truncated on toes III and IV; relative toe length: I <II <V <III <IV ( Fig. 2D View Figure ).

Skin of dorsum and dorsal surfaces of limbs smooth; head with interorbital bar; dorsum with a poorly defined

W-shaped marking on scapula; a poorly defined V-shaped on sacral vertebrae region; arms and hindlimbs with

transverse bars. Venter and ventral surfaces of limbs smooth; discoidal fold complete; small aggregations of melanophores on the gular and pectoral region.

Measurements of the holotype (mm). SVL = 20.6; HL = 7.4; HW = 6.8; EN = 2.8; EE = 4.1; ED = 3.0; TD = 1.5; INDAbout IND = 2.0; THLAbout THL = 10.8; TL = 11.0; FL = 9.9.

Color in life. Interorbital bar dark brown, broad, narrowly bordered by yellow or cream, with an irregular posterior medial projection expanded across head midline, and with irregular lateral borders. Canthal stripe dark brown, extending from tip of snout to anterior margin of eye, ventrally irregularly edged. Supratympanic area blackish brown, extending along supratympanic fold to post-tympanic region. Three diagonal labial bars dark brown, irregularly edged and discontinuous, extending to infralabial region, two below eye, and one slightly faded crossing loreal region and connecting to canthal stripe. Dorsal background coloration brown, with a W-shaped dark brown in occipital-scapula region, narrowly bordered by yellow or cream, connecting with a dark brown chevronshaped marks in middle of dorsum. Dorsolateral surface of body with an irregular dark brown bar from postscapular region to middle of flank. Arm light brown with irregular dark brown transversal marks; forearm light brown with transverse dark brown irregular bars and some flecks. Dorsal surfaces of legs light brown with transverse dark brown bars, hidden surfaces of thighs and shanks brown, slightly mottled with cream. Ventral background coloration whitish cream, inconspicuous white flecks distributed on throat, chest and venter. Iris bronze with black reticulations and a median, horizontal reddish brown streak.

Color in preservative. Background color light brown, pattern of dark coloration as described above, but turned in to brownish-gray. Venter whitish cream, throat and chest finely mottled in gray.

Variation. Upper eyelid with few small tubercles or smooth. Skin on dorsum varies in the amount of granules. Coloration is highly variable ( Fig. 3 View Figure ). Dorsally, the coloration varies from light brown to reddish-brown. Some specimens present light brown blotches between the eyes and nostrils ( CEPB 9840, MNRJAbout MNRJ 91630, MNRJAbout MNRJ 91631, MNRJAbout MNRJ 9633), and slightly faded diagonal labial bars ( MNRJAbout MNRJ 91630, MNRJAbout MNRJ 91633). Some specimens show a cream, brown, dark brown or black complete vertebral line, which can be continuous or discontinuous ( MNRJAbout MNRJ 91629, MNRJAbout MNRJ 91634). Some specimens show dark brown longitudinal stripes from the post-ocular to the sacral region ( CEPB 9839, MNRJAbout MNRJ 91628, MNRJAbout MNRJ 91629, MNRJAbout MNRJ 91631). Also, some specimens lack the dorsolateral bar that runs from the posterior part of the scapular region to the middle of the flanks ( CEPB 9841, MNRJAbout MNRJ 91630). Variation in size and proportions is presented on Table 1.

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Species Note Call Rate Call Duration (s) Pulse Pulse Rate Frequency range Dominant References

number (call/minute) number (pulse/second) (Hz) Frequency (Hz)

O. ibischi  1, 0.131 5.3 41, 2350 ( Reichle et al. 2001)

(0.117,0.193) (6,8) (36,43) (2000,2500)

1 19.7 ± 3.8 0.149 6 40.2 ± 1, 2588.7 ± 120.7 ( Márquez et al. 1995)

(10.5,23.1) (0.144,0.155) (38.5,41.5) (2463.5,2847.1)

1 20.75 0.161 ± 0.0043 6.26 ±1.3 39.7 ± 4.0 (1400,4000) 2609 ± 165 (Pađial et al. 2008)

(16.3,24.7) (0.089,0.264) (4,9) (30.9,51.5) (2254,2981)

O. heterodactylus  1 26.9 0.176 6.8 38.8, 3946 (Pađial & De La Riva 2005)

(24.9,29.33) (0.126,0.245) (5,9) (36.5,48.6) (2876,4134)

O. madidi  1,2 4.3 0.988 ± 0.050 29.6 ± 1.4 29.9 ± 0.4 (2200,2800) 2436 ± 65.1 (Pađial et al. 2008)

(0.926,1.075) (28,32) (29.3,30.3) (2411,2584)

O. quixensis  1, (0.120,0.170) (1,5), (710,1620) (950,1040) ( Heyer & Gascon 1995)

O. remotus  1 31.6 0.104 (2,3),, 3150 (Teixeira Jr. et al. 2012) (18,45) (0.089,0.142) (2866,3395)

O. sanctaecrucis  1 22 0.0 92 ± 0.002 11 120 (1400,2200) (1620,1920) ( Köhler 2000) (0.091,0.097)

Bioacoustics. The call of Oreobates antrum  sp. nov. ( Fig. 4 View Figure ) is composed of a single note containing 5–11 pulses (7.48 ± 1.66), no harmonics and an intermediate pulse rate (32.49–42.25 pulses per second). The amplitude increases to the end of the note but decreases quickly in the last few pulses. The call duration ranged from 0.186 to 0.302 s (0.198 ± 0.054) with a call repetition rate ranging from 12.27 to 17.14 calls per minute. Pulses do not have a tendency to be juxtaposed and are regularly spaced through the note, with pulse duration ranging from 0.004 to 0.011 s (0.007 ± 0.003 s) and interval of pulses vary between 0.010 and 0.056 s (0.22 ± 0.004 s). The dominant frequency was 2430 ± 344 Hz (2070–3273 Hz) ( Fig. 4 View Figure , Table 2).

The advertisement call of Oreobates antrum  sp. nov. is distinguished from O. crepitans  by the lower number of notes per call (a single note in O. antrum  sp. nov.; two notes in O. crepitans  ), and from O. remotus  by the higher number of pulses per note (5–11 in O. antrum  sp. nov.; 2–3 in O. remotus  ). It is distinguished from O. cruralis  and O. madidi  by the lower number of pulses per note (13–17 in O. cruralis  ; 28–32 in O. madidi  ). It is also distinguished from O. cruralis  by the lower dominant frequency (2070–3273 Hz in O. antrum  sp. nov.; 3390–3420 Hz in O. cruralis  ). It is distinguished from O. crepitans  and O. remotus  by the longer note (0.186– 0.302 s in O. antrum  sp. nov.; 0.03– 0.05 s in O. crepitans  ; 0.089– 0.142 s in O. remotus  ), and from O. berdemenos  , O. discoidalis  and O. madidi  by the shorter duration of the advertisement call (0.550– 0.720 s in O. berdemenos  ; 0.379– 0.632 s in O. discoidalis  ; 0.926– 1.075 s in O. madidi  ). The advertisement call of Oreobates antrum  sp. nov. differs from O. berdemenos  , O. discoidalis  , O. ibischi  , O. heterodactylus  , O. sanctaecrucis  and O. discoidalis  calls by the absence of harmonic structure. See quantitative comparisons and more details about advertisement calls of the Oreobates  species genus in Table 2.

Etymology. The specific name antrum  is a Latin adjective meaning “hollow, cave or cavity”. This name refers to the habitats where this species is found, caves of the calcareous rocky outcrops of the Cerrado associated to dry forests.

Natural history and distribution remarks. The new species is known only from the type-locality, in the municipality of São Domingos, in a contiguous area with municipality Divinópolis de Goiás, in northeastern State of Goiás, Central Brazil ( Fig. 5 View Figure ). Another population was registered by Andrade et al. (2012), near the typelocality, inside the cave "Revoltosos" (13o26’23"S, 46o25’52”W, WGS 84, 480 m a.s.l.). The sampled localities are very close to each other, not exceeding 8 km between the more distant areas. This area is inserted in the north area of the micro-region of Vão do Paranã, and it is listed as "Priority Area for Conservation, Sustainable Use and Distribution of Benefits of Brazilian Biodiversity” ( WWFAbout WWF – Brasil 2015), being considered a key ecological corridor for conservation of the Cerrado ( Felfili et al. 2007). The type locality is characterized by the presence fragments of deciduous forest and rocky outcrops mostly surrounded by pastures ( Fig. 6 View Figure ). It is worth mentioning that this locality lies within the influence of the Galheiros hydroelectric power plant.

The species is only found inside caves between 0–1.8 m height from the floor. Specimens can be observed throughout the year, but occur in higher abundance during the rainy season, from October to March. Males were observed vocalizing through November and December. The vocalization sites vary between 0–1.8 m above the floor. Males call very close to their neighbors, about one meter between them. The vocalizations could be heard starting around 20:00 h. Some specimens were found during the day, however the species appears to be preferably nocturnal. These populations are apparently stable, despite strong anthropogenic pressure in the region (Andrade et al. 2012).


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