Proceratophrys rotundipalpebra, Martins, Lucas Borges & Giaretta, Ariovaldo Antonio, 2013

Martins, Lucas Borges & Giaretta, Ariovaldo Antonio, 2013, Morphological and acoustic characterization of Proceratophrys goyana (Lissamphibia: Anura: Odontophrynidae), with the description of a sympatric and related new species, Zootaxa 3750 (4), pp. 301-320 : 308-311

Proceratophrys rotundipalpebra sp. nov.

Figures 5–7

Holotype. ZUEC 20470 (ex- AAG-UFU 1600), adult male, collected at Poço Encantado, Chapada dos Veadeiros, Municipality of Teresina de Goiás, State of Goiás, Brazil (13°52’22’’S – 47°15’43’’W, 820 m above sea level), on 16–17 November 2012 by L. B. Martins, T. R. C. Carvalho and B. F. V. Teixeira.

Paratypes. 26 adult males collected with the holotype (ZUEC 20471 [ex- AAG-UFU 1601], AAG-UFU 1598, 1599, 1602–1605) and in other two sites of the Chapada dos Veadeiros (Municipality of Alto Paraíso de Goiás, 14°10’25’’S – 47°35’27’’W, 1160 m a.s.l. and 14°09’50’’S – 47°47’23’’W, 1165 m a.s.l.): AAG-UFU 0 796, 0 799 (A. A. Giaretta and K. G. Facure cols., 13–19 Nov. 2011), ZUEC 20472-73 (ex- AAG-UFU 1570-71), 1559–1568, 1572–1576 (L. B. Martins, T. R. C. Carvalho and B. F. V. Teixeira cols., 10–15 Nov. 2012).

Diagnosis. In the genus Proceratophrys by lacking nuptial pads on thumb, body without enlarged glands, toes not webbed and ridged laterally, supernumerary tubercles present on hands and feet, dorsal surfaces of fingers and toes wrinkled, and by presenting a pair of symmetrical ridges on dorsum, extending from upper eyelids to sacral region. In the P. cristiceps group by lacking long palpebral appendages and postocular swellings. This species is characterized by: (i) male SVL = 30.4–39.3 mm; (ii) a symmetrical pair of dorsal ridges extending from the upper eyelids to sacral region; (iii) upper eyelids short and rounded; (iv) frontoparietal crests not well-developed; (v) overall color pattern stained by 3–4 tonalities of gray, without a clear background color; (vi) advertisement call emitted in a multi-note pattern, each noted pulsed, the first and last notes differing from each other and from those amidst the call in temporal features.

Comparison with other species. Proceratophrys rotundipalpebra sp. nov. can be distinguished from the other species of the P. cristiceps group, and from those not associated to any group, mainly by the following combination of characters (data for species in comparison in parenthesis): in size (male SVL = 30.4–39.3 mm in the new species), from P. caramaschii (SVL = 42.7–56.3 mm), P. cristiceps (SVL = 39.5–50.2 mm), P. redacta (26.9–29.7 mm), P. minuta (SVL = 20.0– 25.2 mm), P. rondonae (62.9 mm – only the holotype measured) and P. strussmannae (SVL = 41.1–47.3 mm); from P. minuta , P. rondonae and P. s c h i rc h i (upper eyelids with multiple short expansions/ appendages; symmetrical pair of dorsal ridges well-defined and continuous in the sacral region) by the upper eyelids short and rounded, and by the symmetrical pair of dorsal ridges not continuous in the sacral region; the presence of this last feature also distinguishes the new species from P. vielliardi (completely absent); from P. concavitympanum and P. strussmannae (tympanum visible as a depression in the skin) by the tympanum not visible externally; from P. moratoi , P. vielliardi (overall color mostly in tones of gray, with darker rounded blotches), P. aridus , P. caramaschii and P. cristiceps (several brown tones on a cream background) by the overall color pattern stained by 3–4 tonalities of gray, without a clear background color; from P. concavitympanum , P. cristiceps , P. cururu , P. huntingtoni and P. moratoi by the multi-note advertisement call pattern (single note); the new species also differs from P. aridus by the skin mostly covered by irregularly sized warts (small granules) and from P. caramaschii by the frontoparietal crests not developed (developed). From P. carranca the new species differs by the canthus rostralis highlighted by the presence of a well-defined canthal crest (canthus rostralis not evident) and by having a distinct interocular row of warts extending from the anterior half of each eyelid, somewhat interrupted medially (interocular crests absent).

Proceratophrys rotundipalpebra sp. nov. differed from P. goyana by the upper eyelids short and rounded (upper eyelids triangular, with a fleshy, slightly expanded tip), by the symmetrical pair of dorsal ridges not continuous in the sacral region (well-defined and continuous), by the frontoparietal crests not well-defined (frontoparietal crests visible as slight elevations, delimiting a shallow depression between them), and by the overall color pattern stained by 3–4 tonalities of gray, without a clear background color (overall color pattern browned, with symmetrical dorsal ridges bordered laterally by dark brown undulations.

The new species also differed from analyzed specimens of P. goyana in size, highlighted by the nonoverlapped lengths of hand, thigh, tibia and foot ( Table 1 ), and by the PCA performed with the raw morphometric data ( Table 2, Figure 8 a), where both species were separated almost without overlap along the first axis, that accounted for 83.56% of the variation. In the PCA performed with the residuals of morphometric data regressed against SVL ( Table 2, Figure 8 b), there was no clear separation between species, thus indicating that interspecific morphometric variation relied basically in body size ( Figure 8 a), not in body shape.

Description of holotype. SVL: 35.1 mm (other holotype dimensions in Table 1 ). General aspect of body ovoid, stout and warty. Head wider than long (Head length/width = 88%), its length 40% and width 45% SVL; snout outline nearly rounded in dorsal view, near vertical in profile. Nostrils elliptical, with prominent borders. Eyes anterolaterally directed. Preocular cutaneous crest not evident. Canthus rostralis highlighted by the presence of a well-defined canthal crest. Loreal region slightly concave. Region between eyes and nostrils concave. An enlarged tubercle posterior and ventral to mouth commissure. Oblique row of warts from below eye to mouth commissure. Upper eyelids short (28% head width) and rounded; warts covering upper eyelids somewhat arranged in rows, a distinct interocular row extending from the anterior half of each eyelid, somewhat interrupted medially; warts bordering eyelids more evident in the anterior and posterior edges. Frontoparietal crests not well-defined. Tympanum indistinct. A symmetrical pair of ridges on dorsum, initially converging from the upper eyelids to around the middle of dorsum, then diverging and converging again in the sacral region, forming a lozenge in the posterior half of dorsum, where warts are smaller and irregularly spaced from each other. Arms relatively short and stout; upper arm enclosed by a patagium; forearm with a well-defined ventrolateral series of enlarged tubercles, its length 24% SVL. Hands large (28% SVL), finger webbing and nuptial pads absent; outer metacarpal tubercle bifid, the lateral part slightly larger than the medial; inner metacarpal tubercle enlarged, oval; enlarged subarticular tubercles; other smaller, supernumerary tubercles scattered along the ventral surface of hand; sides of fingers ridged; tips of fingers keratinized; length of fingers: III>I>II>IV. Legs relatively short and stout; thigh length 39% SVL, tibia length 35% SVL; tarsus with a well-defined ventromedial series of enlarged tubercles. Feet large (43% SVL), toe webbing poorly developed; outer metatarsal tubercle barely distinct; inner metatarsal tubercle enlarged, strongly keratinized, spade-like, with a series of tubercles lying on its inner basis; enlarged subarticular tubercles; other smaller, supernumerary tubercles scattered along the ventral surface of foot; sides of toes ridged; tips of toes keratinized; length of toes: IV>III>II≈V>I. Skin shagreened, covered by warts variable in size (except ventral surfaces); no evident rows of warts on sides of body. A pair of enlarged tubercles below and lateral to cloacae. Vocal sac single, not expanded externally. Tongue cordiform, free posteriorly. Vomerine teeth lying in two patches between choanae. Vocal slits present.

Variables Raw measurements Residuals

PC 1 PC 2 PC 3 PC 1 PC 2 PC 3 Snout-vent length -0.977 -0.052 0.013

Head length -0.973 -0.052 -0.062 -0.693 -0.213 0.240 Head width -0.976 -0.089 -0.012 -0.817 -0.001 0.207 Eye diameter -0.684 0.532 -0.481 -0.237 -0.694 -0.351 Upper eyelid width -0.918 -0.076 -0.054 -0.403 0.267 -0.500 Internarial distance -0.615 0.681 0.375 -0.052 -0.753 -0.278 Eye-nostril distance -0.849 -0.023 0.214 -0.455 -0.155 0.125 Interorbital distance -0.869 -0.055 0.077 -0.177 0.224 -0.602 Hand length -0.979 -0.055 -0.032 -0.754 0.014 -0.235 Forearm length -0.958 -0.066 -0.005 -0.610 -0.123 0.292 Thigh length -0.978 -0.107 -0.007 -0.809 0.219 0.047 Tibia length -0.979 -0.129 0.006 -0.764 0.425 -0.049 Tarsus length -0.964 -0.064 0.040 -0.653 -0.208 0.348 Foot length -0.979 -0.049 -0.046 -0.796 -0.033 -0.271 Eigenvalues 11.698 0.811 0.436 4.853 1.530 1.272 Variance explained (%) 83.560 5.798 3.113 37.331 11.773 9.784 Cumulative var. expl . (%) 83.560 89.358 92.472 37.331 49.105 67.046 Color of holotype. In preservative (70% ethanol), sides and dorsum of head and trunk stained by 3–4 tonalities of gray (the lighter ones somewhat brownish), disposed in irregular blotches, without a clear background color. The region delimited by the pair of symmetrical ridges and the upper eyelids (posterior to the interocular crest) are homogeneously light gray, except for a small dark gray spot in the interocular region. Sides of the snout and dorsal surfaces of arms, legs, fingers and toes with alternated light and dark gray bars. Belly and ventral surfaces of arms and legs homogeneously beige. Throat blackened. In life, the color pattern was the same, but brownish tones were more evident.

Variation. The diagnostic morphological features are constant among all the type-series. The color pattern is basically the same in the preserved type-series, but the tonalities of gray are variable (there are lighter and darker specimens); in life (figure 5), browned colors may be added to or replace the grayish ones; the area delimited by the symmetrical dorsal ridges may be or not homogeneous in color; some specimens have small spots in the ventral region, specially near chest, that may be in similar color or darker than the background. The definition of the snout outline in dorsal view as rounded or nearly rounded sometimes is not very clear, and both states were considered present in the type-series; similarly, the degree of sloping of the snout in profile is somewhat variable, going from near vertical to clearly obtuse.

Natural history. Breeding sites of the new species ( Figure 4 ) were found within rocky grasslands (= campo rupestre)—an altitudinal physiognomy of the Cerrado biome mostly covered by herbaceous vegetation, but also with sparse shrubs and trees, where the soil is shallow and/or confined between rocks (Oliveira & Marquis 2002). It consisted of grassy areas with sandy soil, soaked by slow flowing rain water, or the margins of slow flowing, apparently seasonal, streamlets running along erosion trenches, with gravel/sandy bottom and sparse larger rocks. In Alto Paraíso de Goiás, the new species was more common in the latter habitat type, and rare in the former, where a related species, Odontophrynus salvatori Caramaschi (Odontophrynidae) , was abundant; at the type locality (Teresina de Goiás), the new species was found in both habitat types, and O. salvatori was not registered syntopically there. Proceratophrys goyana is sympatric to the new species, but they were not registered syntopically in the breeding sites (closest distance between both species habitats ≈ 4 km), with P. goyana apparently restricted to streamlets running over rocks. We visited the breeding sites of the new species only in the rainy season (November 2011 and 2012), when calling activity started at sunset, and was especially intense in rainy days.

Geographic distribution. Proceratophrys rotundipalpebra sp. nov. is presently known only from the Chapada dos Veadeiros region, Municipalities of Alto Paraíso de Goiás and Teresina de Goiás, State of Goiás, Brazil.

Etymology. The specific epithet, rotundipalpebra , used as a noun in apposition, is derived from two Latin words, rotunda, meaning rounded, and palpebra, meaning eyelid. It is a reference to the rounded upper eyelid of the new species, which helps to differentiate it from P. goyana .

Figures

FIGURE 4. Breeding sites of Proceratophrys goyana (A) and P. rotundipalpebra sp. nov. (B, C) at the Chapada dos Veadeiros region, State of Goiás, Brazil. A- Vale da Lua, Municipality of Alto Paraíso de Goiás; B- Poço Encantado, Municipality of Teresina de Goiás (type locality); C- Fazenda São Bento, Municipality of Alto Paraíso de Goiás.

FIGURE 5. Adult males of Proceratophrys rotundipalpebra sp. nov., in life. A—ZUEC 20470 (holotype), SVL = 35.1 mm; B—AAG-UFU 1563, SVL = 38.6 mm; C—AAG-UFU 1564, SVL = 34.9 mm; D—AAG-UFU 1565, SVL = 38.3 mm. Specimens from the Chapada dos Veadeiros region, Municipalities of Teresina de Goiás and Alto Paraíso de Goiás, State of Goiás, Brazil.

FIGURE 6. Dorsal and ventral views of the holotype of Proceratophrys rotundipalpebra sp. nov. (adult male, ZUEC 20470, SVL = 35.1 mm).

FIGURE 7. Dorsal view of head (A), ventral view of right hand (B), lateral view of head (C), and ventral view of right foot (D) of the holotype of Proceratophrys rotundipalpebra sp. nov., adult male, ZUEC 20470, SVL = 35.1 mm.

FIGURE 8. Scatterplot of the two first PCA factors derived from morphometric data of adult males of P. goyana (red squares) and P. rotundipalpebra sp. nov. (blue triangles). A—raw measurements (log- 10 transformed); B—linear regression residuals of raw measurements against SVL.