Proceratophrys minuta Napoli, Cruz, Abreu & Del-Grande, 2011, sp. nov.
Creators: name: Napoli, Marcelo Felgueiras
name: Cruz, Carlos Alberto Gonçalves
name: Abreu, Rafael Oliveira De
name: Del-Grande, Maria Lucia
Publisher: name: Zenodo
Year: 2011
Subjects: Biodiversity
Taxonomy
Animalia
Chordata
Amphibia
Anura
Cycloramphidae
Proceratophrys
Proceratophrys minuta

description: Proceratophrys minuta sp. nov.
Figures 1–4
Holotype. UFBA 6721, adult male, collected at the Riacho do Dandá (11°26'S, 40°33'W, ca. 800 m above sea level), Parque Estadual das Sete Passagens (an environmental State protected area), Municipality of Miguel Calmon, State of Bahia, Brazil, on 22 November 2006, by Rafael Oliveira de Abreu and Heverton Cardona.
Paratypes. Brazil, State of Bahia: Municipality of Miguel Calmon, Parque Estadual das Sete Passagens (11°26'S, 40°33'W, ca. 800 m a.s.l.)— MNRJ 75410 (ex-UFBA 6229, adult female), 75411 (ex-UFBA 6230, adult male), collected on 22–25 July 2006, by A. Xavier, M.B. Santos, and R. Burger; UFBA 6287, adult male, collected on 12–16 October 2006, by A.L. Xavier, D. Cruz, M. Camardelli, P.M. Fonseca, and R. O. Abreu; UFBA 6289 (adult male), 6290 (adult female), collected on 12–16 October 2006, by A.L. Xavier, D. Cruz, M. Camardelli, P.M. Fonseca, and R. O. Abreu; UFBA 6356–6358 (adult males), 6353–6355 (adult females), MNRJ 75417 (ex-UFBA 6351), UFBA 6349, 6350, 6352 (juveniles), collected on 23 July 2006, by A.L. Xavier, D. Cruz, M. Camardelli, P.M. Fonseca, and R. O. Abreu; MNRJ 75412–75416 (adult males, ex-UFBA 6718, 6722, 6723, 6726, 6728 [stained and cleared], respectively), UFBA 6716, 6720, 6725, 6727 (adult males), 6724 (adult female), 6717, 6719 (juveniles), collected on 18–23 November 2006, by A.L. Xavier, D. Cruz, M. Camardelli, P.M. Fonseca, R. O. Abreu, and W. Fahning; UFBA 7156, 7158 (adult males), 7155, 7157 (juveniles), collected on 20 January 2007, by A. Xavier, D. Cruz, R.A. Abreu, N. Menezes, and T. Jordão. Municipality of Palmeiras, Morro do Pai Inácio (12°27'49"S, 41°28'26"W, ca. 840 m a.s.l.)— UFBA 10755, adult male, collected on 0 1 May 2006, by M.L. Del- Grande; UFBA 10751–10754 (ex-UESB 387–390), adult males, collected on 28 September 2006, by M.L. Del- Grande.
Diagnosis. In the genus Proceratophrys by lacking nuptial pads on thumb, body without enlarged glands, fingers not webbed, supernumerary tubercles present on hands and feet, dorsal surfaces of fingers and toes wrinkled, and dorsum adorned with sinuous longitudinal ridges outlining a spear-shaped ornamentation like a hastate-shaped leaf, with flaring pointed lobes at eyes and spear point at urostile. Proceratophrys minuta is related to P. s c h i rc h i (Miranda-Ribeiro) by the presence of outer metacarpal tubercle single or partially grooved, and a short palpebral appendage with marginal tubercles, the largest tubercle in the middle more projected than lateral tubercles. The new species is diagnosed from its congeners by the following combination of characteristics: (1) small size (adult males SVL 20.4–25.2 mm, adult females 28.3–31.9 mm); (2) absence of rostral appendage; (3) a short palpebral appendage with marginal tubercles, the largest tubercle in the middle more projected than lateral tubercles; (4) snout rounded from above, vertical or slightly oblique in profile; (5) canthus rostralis well-marked, curved; (6) dorsum adorned with sinuous longitudinal ridges outlining a spear-shaped ornamentation like a hastateshaped leaf, with flaring pointed lobes at eyes and spear point at urostile; (7) dorsum with a pair of parallel thin rows of warts extending from interorbital to scapular region; (8) distinct row of warts transversally on head, interrupted at the center, and extending to the border of each eyelid; and (9) outer metacarpal tubercle single or partially grooved.
Comparisons with other species. Proceratophrys minuta is promptly diagnosed from all species of the P. bigibbosa group (P. avelinoi, P. bigibbosa, P. brauni, and P. p a l u s t r i s) by the absence of postocular swellings (present in those species), from all species of the P. b oi e i group (P. appendiculata, P. b oi ei, P. laticeps, P. melanopogon, P. moehringi, P. paviotii, P. phyllostomus, P. re n a l i s, P. sanctaritae, P. subguttata, and P. tupinamba) by the absence of a single long uni-cuspidate palpebral appendage (present in those species), and from P. rondonae by the smaller snout–vent length (P. m i n u t a males 20.0– 25.2 mm, females 28.3–31.9 mm; P. rondonae males 52.6–63.4 mm, females 37.7–72.8 mm); P. m i n u t a is promptly distinguished from all species of the P. cristiceps group (P. concavitympanum, P. cristiceps, P. cururu, P. goyana, P. m o r a t o i, P. strussmannae, and P. vielliardi) and from P. s c h i rc h i by the smaller snout vent–length 20.4–25.2 mm in males (P. cristiceps species group, SVL in males: P. concavitympanum 39.6–51.8 mm, P. cristiceps 40.6–49.1 mm, P. cururu 36.5–43.1 mm, P. goyana 28.0– 55.5 mm, P. m o r a t o i 26.4–30.0 mm, P. strussmannae 41.1–47.3 mm, and P. vielliardi 39.1–41.9 mm; P. schirchi 31.6–40.4 mm); P. m i n u t a is also diagnosed from all species of the P. cristiceps group by the outer metacarpal tubercle single or partially grooved and a short palpebral appendage with marginal tubercles, the largest tubercle in the middle more projected than lateral tubercles (outer metacarpal tubercle completely divided, and absence of palpebral appendages in those species); from P. m o r a t o i and P. vielliardi the new species also differs by the dorsum adorned with sinuous longitudinal ridges outlining a spear-shaped ornamentation like a hastate-shaped leaf, with flaring pointed lobes at eyes and spear point at urostile (absent in those species); P. m i n u t a is diagnosed from P. concavitympanum, P. cristiceps, P. cururu, P. goyana, P. strussmannae, and P. s c h i rc h i by dorsum with a pair of parallel thin rows of warts extending from interorbital to scapular region (thick rows of warts in those species); furthermore, P. minuta is diagnosed from P. s c h i rc h i by the absence of a rostral appendage (short rostral appendage present in that species).
Description of holotype. Head wider than long, head length 87% of head width; snout rounded in dorsal view, slightly oblique in profile (figs 1, 2A, B); nares elliptical, prominent, and external to the canthal crest, internarial distance 77% of eye to nostril distance; canthal crests well marked, curved, and prominent; no preocular crests; loreal region oblique; distinct row of spatulated warts from posterior corner of eye to angle of jaw; eye directed anterolateraly, small, 29% of head length; six short palpebral appendages, central appendage prominent; tympanum not distinct; row of warts transversally on head, interrupted at the center, extending to the border of each eyelid; a pair of parallel thin rows of warts extending from interorbital region to scapular region; vocal sac slightly expanded externally; tongue cordiform, free posteriorly; choanae large, well separated one from the other; vomerine teeth in two short transverse series lying between choanae; vocal slits large; no frontoparietal crest. Arms moderately robust (fig. 1); finger lengths I ≈ II <IV <III (figs 1, 2C); nuptial asperities absent; interdigital webbing absent; inner metacarpal tubercle large, elliptical; outer metacarpal tubercle twice the size of the inner, elliptical, and partially grooved; scarce small rounded supernumerary tubercles; subarticular tubercles large, nearly rounded, and grooved anteriorly and posteriorly. Legs moderately robust (fig. 1), thigh length longer than tibia length, the sum of thigh and tibia lengths 78% of snout–vent length; dorsal surface of tibia with three oblique parallel rows of enlarged warts; foot length 57% of snout–vent length; toes adorned with marginal spinulose tubercles (fig. 2D); toe lengths I <II <V <III <IV; webbing formula I 1–2 II 1–3 III 2–4 IV 4–2 V; inner metatarsal tubercle large, spatulated; outer metatarsal tubercle small, rounded; numerous small rounded supernumerary tubercles; subarticular tubercles large, nearly rounded, and grooved anteriorly and posteriorly. Dorsum adorned with sinuous longitudinal ridges outlining a spear-shaped ornamentation like a hastate-shaped leaf, with flaring pointed lobes at eyes and spear point at urostile (fig. 1). Dorsal surfaces and flanks with warts of different sizes and shapes, set in rows or scattered; ventral surfaces, except hands and feet, covered by numerous small, circular, uniform warts; skin and warts of dorsal and ventral surfaces covered by minuscule asperities.
Color in life. Based on color photographs of two paratypes: an adult male not identified among paratypes UFBA 6230, 6256–6258, and an adult female, UFBA 6290 (fig. 3A–D). Dorsal ground color faded tan brown, maculated with variegated browns, mainly with color tons of cream, reddish and grayish browns, looking like dead leaves. Longitudinal ridges of the spear-shaped ornamentation on dorsum dark brown to reddish brown, not contrasting with dorsal ground color. Warts on dorsum cream, reddish brown or dark brown; palpebral appendages reddish brown. Interior surface of the spear-shaped ornamentation on dorsum not contrasting with the rest of the dorsal surface in one specimen (fig. 3A), and grayish brown in the other, in which it contrasts from the general tan background color (fig. 3B, C). Upper eyelids light brown to grayish brown, connected by a light brown or reddish brown interorbital stripe. An oblique row of cream color warts is noticeable from the angle of jaw to the upper arm. Upper lip cream color. Canthus rostralis delimited from below by a dark brown irregular stripe, from anterior corner of eye to nostril. Lorus with grayish brown to dark brown background color, maculated by a dark brown band from the anterior corner of eye to upper lip, followed by two other dark brown bands, the latter from the posterior corner of eye to near the upper arm. Tip of snout dark brown. Two to three transverse dark brown bars on forearm, shank, and foot. Ventral ground color of throat, chest, belly, arms, legs, hands, and feet tan color, with warts and tubercles cream (fig. 3D). Pupil black; iris copper brown, its lower region gray color ornamented by black reticulations, marginally delimited by an irregular black aureole.
Color in preservative. Based on the type-series. Follows the color in life, but with less vivid colors (fig. 1). The background of dorsal surface varied from light brown to dark brown. Specimens with light brown background color (UFBA 6287, 6289, 6290, 6349–6352, 6354, 6355, 6723, 6725, 7157) evidenced a spear-shaped ornamentation on dorsum bordered along its external sides by a wave-shaped dark brown band, somewhat fragmented into three main dark brown triangular marks. Yet, in these specimens the dark brown stripes on arms and legs are well distinct from the background. These features are still noticeable, but less evident, in specimens of darker background color (UFBA 6357, 6358, 6716–6722, 6724, 6726, 6727), and not visible in specimens of darkest brown background color (UFBA 6353, 6356, 7156). Dorsal warts dark brown or cream color. Anterior and posterior surfaces of thigh with background color cream to homogeneous brown, immaculate or maculated by irregular dark brown marks and/or dark brown pin dots. Throat, chest, belly, ventral surfaces of arms and legs with cream background color, varying from almost immaculate (UFBA 6287, 6289, 6290, 6352, 6355, 6358, 6717, 6719–6721, 6723) to intensively scattered with dark brown pin dots (UFBA 6725, 6726, 6230). Palm of hand and sole of foot dark brown; subarticular and supernumerary tubercles cream color.
Measurements of holotype (mm). SVL 23.9; HL 9.6; HW 11.0; ED 2.8; UEW 3.3; IOD 2.7; IND 1.7; END 2.2; THL 9.8; TL 8.9; FL 13.7.
Variation. Specimens are congruent with respect to the morphologic characters. Descriptive statistics of measurement variables from adult males and females are in Table 1. Variations in color patterns were already described in color in life and color in preservative items.
Etymology. The specific name, a Latin adjective (minutus = small, minute), is an allusion to the small size of the new species.
Parque Estadual das Sete Passagens Morro do Pai Inácio
Males (n = 18) Females (n = 6) Males (n = 5)
Mean SD Min Max Mean SD Min Max Mean SD Min Max SVL 22.7 1.2 20.4 25.2 30.3 1.5 28.3 31.9 21.0 0.8 20.0 22.1 HL 9.6 0.4 9.0 10.4 12.1 0.6 11.5 13.0 8.2 0.6 7.4 9.1 HW 11.1 0.6 10.4 12.9 14.5 1.1 13.5 16.1 9.5 0.8 8.4 10.5 IND 1.7 0.3 1.4 2.5 2.3 0.2 2.0 2.5 1.6 0.2 1.5 1.9 END 2.1 0.2 1.5 2.5 2.7 0.3 2.5 3.1 1.8 0.1 1.7 1.9 ED 2.9 0.2 2.7 3.2 3.7 0.1 3.5 3.8 2.7 0.2 2.5 3.0 UEW 3.4 0.3 3.0 3.8 4.3 0.3 3.9 4.7 2.7 0.1 2.7 2.9 IOD 2.7 0.2 2.3 3.0 3.3 0.3 3.0 3.7 2.6 0.1 2.4 2.7 THL 9.9 0.5 8.8 10.5 12.9 0.7 12.0 13.7 8.8 1.0 7.4 10.0 TL 8.8 0.3 8.3 9.5 11.5 0.7 10.5 12.3 7.6 0.3 7.4 8.0 FL 14.0 0.4 13.2 15 18.1 0.9 17.0 19.2 11.6 0.4 11.1 12.1 HL/SVL 0.43 0.02 0.39 0.45 0.40 0.01 0.38 0.41 0.39 0.02 0.37 0.43 HW/SVL 0.49 0.02 0.46 0.52 0.48 0.02 0.46 0.51 0.45 0.03 0.42 0.49 HW/HL 1.16 0.04 1.10 1.24 1.20 0.04 1.14 1.27 1.15 0.02 1.13 1.18 THL/SVL 0.44 0.02 0.40 0.46 0.43 0.01 0.41 0.45 0.42 0.03 0.37 0.45 TL/SVL 0.39 0.02 0.36 0.42 0.38 0.01 0.36 0.39 0.36 0.01 0.35 0.37 FL/SVL 0.62 0.03 0.57 0.67 0.60 0.01 0.59 0.61 0.55 0.02 0.52 0.57 THL+TL/SVL 0.83 0.04 0.77 0.87 0.81 0.02 0.78 0.84 0.78 0.03 0.74 0.81 Natural History. All specimens of Proceratophrys minuta were captured inside gallery forests, always near (1–5 m distance) forest brooks of shallow waters (2–50 cm deep) with approximately 0.5–2 m wide. Advertisement calls of specimens from the Parque Estadual das Sete Passagens, Municipality of Miguel Calmon, State of Bahia, Brazil, were heard from these streams, from October to November 2008. Newly metamorphosed juveniles were recorded at the edge of a stream. Tadpoles were captured on 12–16 October 2006 by Rafael O. Abreu and Milena Camardelli, inside permanent forest streams of about 30 cm water depth, but also in temporary shallow streams (ca. 2–10 cm deep) of shaded areas in the Campo Rupestre (open habitat) that receive water from rivers and springs located in gallery forests. Adult specimens released distress calls when manipulated by the researchers. All paratypes from Morro do Pai Inácio, Municipality of Palmeiras, State of Bahia, Brazil, were emitting advertisement calls when they were captured, always positioned on the leaf litter, and never hidden under leaves or fallen logs. At this place, advertisement calls were always heard after nightfall, from September to October 2006. A detailed study of the spatial distribution of the anuran fauna of the Parque Estadual das Sete Passagens, including P. minuta, can be assessed in Xavier and Napoli (2011), referred in that publication as ‘ Proceratophrys sp. nov., allied to P. s c h i rc h i ’.
Tadpoles. Description of the tadpole of Proceratophrys minuta was based on nine specimens [UFBA 10756 (7), 10757 (1), 10758 (1)] in stages 31–38. Descriptive statistics is in Table 2. Total length 29.7–36.1 mm. Body wider than high, depressed, ovoid-elongated in lateral view, oval in dorsal view (fig. 3E). Body length 38.8–41.7% total length; body height 69.2–78.8% body width, and 45.7–57.4% body length. Snout rounded in lateral and dorsal views; snout slopes gradually toward the oral disc. Eye small, its diameter 9.0–10.3% body length, positioned dorsally, laterally directed; interorbital distance 36.1–44.4% body width; eye–snout distance 27.1–31.3% body length; eye–nostril distance 7.5–10.7% body length; nostril small, reniform, with small cutaneous extension on its inner margin, positioned dorsally midway between eyes and snout, but slightly nearer to eyes. Internarial distance 15.0–19.7% body width. Spiracle short, sinistral, inner wall free from body, positioned laterally on the beginning of the medium third of body, posterodorsally directed. Vent tube short, with dextral opening, fused to tail fin.
Tail length 58.3–61.2% total length; tail as high as the body height, slightly arched. Tip of tail rounded to slightly pointed. Dorsal fin starts on junction of body to tail, 1.3–1.7 times higher than the ventral fin, both highest at the second third of the tail; ventral fin slightly less arched than the dorsal fin. Oral disk emarginated, ventrally positioned, its width 30–38% body width, surrounded by a single row of conical or rounded marginal papillae, which are widely interrupted at the anterior labium. The marginal papillae are larger at the posterior labium, becoming smaller laterally towards the anterior labium. Tooth row formula 2(2)/3(1) with rows of teeth placed on ridges; rows A-1 and A-2 of equal length and P-3 shorter than the others. Labial teeth black, long, slightly curved towards oral opening. Upper and lower jaw sheaths wide, with serrated edges; upper sheath shaped as a shallow-M, lower sheath U-shaped.
Live tadpoles with dorsum densely covered by irregularly bordered golden blurs that reach the lower region of flanks, in which they became sparse, fragmented and shaped as small horizontal lines, which also occur in the venter and tail. Tail with 1–5 well marked broad and black irregular vertical bars, which are fragmented into smaller blotches towards fins and tail tip. The transparence of the skin confers to musculature a clear whitish-pink color. Venter transparent, oral region white, internal organs slightly visible. Iris orange-red, bordered internally and externally with the same golden color of dorsum, presenting a darken region that resembles a vertical bar. Limb bud with black marks. Dorsal surfaces of body, tail musculature, and dorsal fin at the end of tail with irregular areas of reddish-brown faded blurs.
Preserved tadpoles have translucent pale brown skin, clearer in tail. Dorsum with sparse dark-brown spots, the golden color became a clear bare visible brown. Black bars and blotches became dark brown. Intestine remains visible. Iris black. Tadpoles (UFBA 10750) in earlier (25–27) and later (40–41) stages are congruent with respect to general morphology and color of tadpoles in stages 31–38.
Out of 24 species of Proceratophrys, only 13 have their larvae formally described: P. boiei (Izecksohn et al. 1979), P. appendiculata (Peixoto & Cruz 1980), P. laticeps (Peixoto et al. 1981), P. s c h i rc h i (Peixoto et al. 1984, as P. precrenulata; see Caramaschi & Velosa 1997), P. moehringi (Weygoldt & Peixoto 1985), P. concavitympanum (Giaretta et al. 2000), P. palustris (Giaretta & Sazima 1993), P. moratoi (Rossa-Feres & Jim 1996), P. cururu (Eterovick & Sazima 1998), P. avelinoi (Sá & Langone 2002), P. cristiceps (Vieira et al. 2007), P. re n a l i s (Nascimento et al. 2010), and P. tupinamba (Fatorelli et al. 2010).
Live tadpoles of Proceratophrys minuta differ in color from that of P. avelinoi, P. cristiceps, P. concavitympanum, P. cururu, P. palustris, and P. m o r a to i mainly by the golden blurred dorsum and presence of black vertical bars in tail of the former (background color brown, maculated with dark brown or gray blotches in these species), and also from P. moehringi and P. re na li s (these two species differ from the six former species mainly by the presence of dark brown transverse bands on dorsal surfaces of the tail musculature). The overall color pattern of P. minuta tadpoles resembles that of P. schirchi, P. appendiculata and P. laticeps, but differs in the pattern of bars and blotches/spots on tail. In P. minuta, the tail musculature is often covered in its entire vertical range by transversal black bars, which sometimes reach the dorsal fin (transversal brown bars covering only dorsal region of tail musculature in P. schirchi, P. appendiculata, P. b o i e i, and P. laticeps); P. m in ut a tadpoles present only the first third of ventral fin transparent, ventral fin fully transparent and maculated by small golden blotches in P. schirchi (Peixoto et al. 1984); tadpoles of P. m i n u t a lack a small cream blotch in the middle of dorsum reported for P. appendiculata by Peixoto and Cruz (1980). The blurs that cover the dorsum and flanks of P. m i n u t a are golden colored, silver in P. boiei. Proceratophrys minuta lacks pale brown reticulations on caudal musculature and fins reported for P. moehringi by Weygoldt and Peixoto (1985). The golden blurred dorsum and the presence of black vertical bars on tail musculature of P. m i n ut a tadpoles differ them from that of P. renalis, which lack such patterns. Morphological features of tadpoles of Proceratophrys minuta are similar to that observed for the genus, with few subtle differences among species. Tadpoles of P. m in ut a differ from that of P. cururu by presenting the nostril nearer to eye than to tip of snout (closer to tip of snout in P. c u r ur u), and by the spiracle nearer to snout than to body-tail junction (closer to body-tail junction in P. cururu; Eterovick & Sazima 1998). The tip of tail is rounded in P. minuta, pointed in P. cururu, P. concavitympanum, P. cristiceps, P. laticeps, P. renalis, and P. tupinamba. The size of eyes in P. m i n u t a (eye diameter [ED] 9–10% body length [BL]) is similar to that of some species with palpebral appendages (P. laticeps and P. re n a l i s; ED up to 9.5% BL), P. schirchi (ED 10% BL), P. avelinoi (ED 9% BL), smaller than that of P. palustris (ED 11% BL) and species related to the P. cristiceps group (P. cristiceps, P. concavitympanum, and P. c u r u r u; ED larger than 12% BL), and larger than P. appendiculata, P. b o i e i, P. moehringi, and P. tupinamba (ED <9% BL). Second tooth row interrupted in P. minuta, continuous in P. appendiculata and P. tupinamba.
Geographic distribution. Proceratophrys minuta is known from two localities in the northern sector of the Espinhaço mountain range (fig. 5), both included in the Chapada Diamantina ecoregion (Velloso et al. 2002). The Chapada Diamantina ecoregion is comprised in the Caatinga Morphoclimatic Domain, characterized by vegetation morphologically and physiologically adapted to semiarid conditions (Ab’Sáber 1977). At both localities, elevations range from approximately 800 m to 1300 m. The topography is characterized by mountainous terrain, with deep valleys and steep cliffs, and is classified as extremely unstable with medium slopes ranging from 30o to 45o, except for the tops. According to the Köppen classification, the climate is of the semi-arid BSwh type, rainy in the summer and dry during winter. The rainy period is from October to April, and the wettest months are from November to January. Because of the high elevations, minimum temperatures reach less than 14o C in winter whereas in the surrounding areas are up to 20o C. Such characteristics are reflected in the vegetation cover, which consists of seasonal semi-deciduous forests and environments of campo rupestre (rocky mountain fields), which contrasts with lowland areas surrounding these mountains (up to ca. 500 m a.s.l.) that are characterized by shallow soils with caatinga vegetation (Ab’Sáber 2003). An extended description of the study area of the Parque Estadual das Sete Passagens can be assessed in Xavier and Napoli (2011).
Stages (Gosner 1960)
31 34 35 36 (n = 2) 38 (n = 4)
Mean SD Min Max Mean SD Min Max
description: Published as part of Napoli, Marcelo Felgueiras, Cruz, Carlos Alberto Gonçalves, Abreu, Rafael Oliveira De & Del-Grande, Maria Lucia, 2011, A new species of Proceratophrys Miranda-Ribeiro (Amphibia: Anura: Cycloramphidae) from the Chapada Diamantina, State of Bahia, northeastern Brazil, pp. 37-49 in Zootaxa 3133 on pages 39-47, DOI: 10.5281/zenodo.207360