A new species of Proceratophrys (Anura: Cycloramphidae) from western Brazil

A New Species of Proceratophrys (Anura: Cycloramphidae) from Midwestern Brazil Author(s): Robson W. Ávila , André Pansonato , and Christine Strüssmann Source: Journal of Herpetology, 46(4):466-472. 2012. Published By: The Society for the Study of Amphibians and Reptiles DOI: http://dx.doi.org/10.1670/11-038 URL: http://www.bioone.org/doi/full/10.1670/11-038

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Journal of Herpetology, Vol. 46, No. 4, 466–472, 2012 Copyright 2012 Society for the Study of Amphibians and Reptiles

A New Species of Proceratophrys (Anura: Cycloramphidae) from Midwestern Brazil ROBSON W. A´ VILA,1,2 ANDRE´ PANSONATO,3

AND

CHRISTINE STRU¨SSMANN4

1

´ ´ ˆ ´ ˆ Universidade Regional do Cariri, Centro de Ciencias Biologicas e da Saude, Departamento de Ciencias Biologicas, Campus do Pimenta, Rua Cel. Antonio Luiz, 1161, Bairro do Pimenta, CEP 63105-100, Crato, Ceara´, Brazil 3 ´ ´ ˜ o Colombo, 2265, Jardim Nazareth, CEP 15054-000, Pos-Gradua ca ¸ ˜ o em Biologia Animal, Universidade Estadual Paulista–UNESP. R. Cristova Sa˜o Jose´ do Rio Preto, Sa˜o Paulo, Brazil 4 ˆ Departamento de Ciencias Ba´sicas e Produca ¸ ˜ o Animal, Faculdade de Agronomia, Medicina Veterina´ria e Zootecnia, Universidade Federal de Mato Grosso (UFMT). Av. Fernando Correia da Costa, 2367, Boa Esperanca, ¸ CEP 78060-900, Cuiaba´, Mato Grosso, Brazil

ABSTRACT.—We describe adult morphology, advertisement call, and natural history aspects of a new frog species from riparian habitats alongside intermittent headwater streams in southwestern Cerrado, the second largest biome in Brazil. Presently known from three localities in Mato Grosso State, the new species belongs to the Proceratophrys cristiceps group. It is characterized mainly by small size (adult snout–vent length approximately 46 mm), snout rounded in dorsal view and obtuse in lateral view, absence of flared lips, dorsal skin granular, and absence of both postocular swellings and prominent palpebral appendages. The advertisement call of the new species consists of a single note with 19– 25 pulses. Calls are repeated at mean intervals of 0.7 sec. Mean dominant frequency is 1,250.2 Hz, with ascendant modulation.

The genus Proceratophrys Miranda-Ribeiro, 1920 presently comprises 25 species, distributed in Brazil, Argentina and ´ Paraguay (Cruz and Napoli, 2010; Avila et al., 2011; Martins and Giaretta, 2011). Three species groups have been recognized: the Proceratophrys boiei group (sensu Prado and Pombal, 2008), the Proceratophrys bigibbosa group (sensu Kwet and Faivovich, 2001), and the Proceratophrys cristiceps group (sensu Giaretta et al., 2000). Proceratophrys schirchi Miranda-Ribeiro, 1937 is not currently associated to any of these groups, although Amaro et al. (2009) suggested its relationship with the group of P. cristiceps. The P. cristiceps group is characterized by the absence of both postocular swellings and short palpebral appendages (sensu Giaretta et al., 2000). Seven species are currently recognized in this group: two from Amazonian sites of western Brazil (Proceratophrys concavitympanum Giaretta, Bernarde, and Kokubum 2000 and Proceratophrys strussmannae ´ Avila, Kawashita-Ribeiro, and Morais 2011), and the remaining five species distributed in the Cerrado domain of central and southeastern Brazil (P. cristiceps Mu¨ller, 1883, Proceratophrys goyana Miranda-Ribeiro, 1937, Proceratophrys cururu Eterovick and Sazima, 1998, Proceratophrys moratoi Jim and Caramaschi, 1980, and Proceratophrys vielliardi Martins and Giaretta, 2011). Proceratophrys cristiceps is also found in the Caatinga from northeastern Brazil (Giaretta et al., 2000; Vieira et al., 2008). Boulenger (1903) examined the specimens of amphibians and reptiles collected by M. A. Robert during the Percy Sladen expedition to central Brazil and incorrectly assigned specimens of Proceratophrys obtained at Chapada dos Guimara˜es, Mato Grosso State, to P. cristiceps. During herpetological field studies conducted in this and in other two localities in Mid-Southern Mato Grosso, we obtained specimens of Proceratophrys that we recognize as a previously undescribed taxon. Herein, we describe the new species that we assign to the P. cristiceps group. MATERIALS

AND

METHODS

´ Specimens examined are deposited at the ‘‘Coleca ¸ ˜ o Zoologica de Vertebrados da Universidade Federal de Mato Grosso,’’ 2

Corresponding Author. E-mail: [email protected]

DOI: 10.1670/11-038

Cuiaba´ , Brazil (UFMT), ‘‘Museu de Zoologia Ada˜ o Jose´ Cardoso,’’ Universidade Estadual de Campinas, Campinas, Brazil (ZUEC), and ‘‘Museu Nacional,’’ Rio de Janeiro, Brazil (MNRJ). Specimens used for comparisons are listed in Appendix 1. For comparisons, data from congeneric species appears in parentheses. Data for P. cururu appear in Eterovick and Sazima (1998); for P. moratoi in Jim and Caramaschi (1980), and Brasileiro et al. (2008), and for P. vielliardi are from Martins and Giaretta (2011). The following measurements (in millimeters) were taken with digital calipers, to the nearest 0.01 mm, according to Heyer et al. (1990) and Eterovick and Sazima (1998): ED (eye diameter); END (eye to nostril distance); F (foot length), FL (forearm length); H (hand length); HL (head length); HW (head width); ID (internarial distance); IML (inner metatarsal tubercle length); IND (internarial distance); SVL (snout–vent length); TD (tympanum diameter); TF (tarsus–foot length); TH (thigh length); TL (tibia length); UEW (upper eyelid width). Additionally, the following characters were included: NT (number of tubercles on the ventral surface of the left arm), NIT (number of tubercles on inner surface of left arm), and NTP (number of tubercles on upper eyelid). Webbing formula follows Savage and Heyer (1997). Advertisement calls of two adult males were recorded by Christine Stru¨ssmann with a Sony TCM 5000-EV cassette tape recorder, equipped with a Yoga EM-9600 external directional microphone. Air temperature was measured using a standard mercury thermometer of 0.18C. Tape recordings were digitized at 44.1 kHz, resolution of 16 bits (FFT 1024), with Cool Edit 96 (eSyntrillium) and Raven Pro 1.3. They are archived as .wav files in the ‘‘Banco de Registros Bioacusticos,’’ ´ housed at ´ ‘‘Laboratorio de Herpetologia do Instituto de Biociencias’’ ˆ of the ‘‘Universidade Federal de Mato Grosso’’ (IB-UFMT, Cuiaba´, Mato Grosso, Brazil), under accession numbers LH 18A-01 (unvouchered) and LH 18A-02 (voucher specimen UFMT 1747). Terminology for acoustic parameters follows Heyer et al. (1990) and Martins and Jim (2003). The following seven call variables were examined: note duration, internote intervals, mean rate of notes per minute, number of pulses, pulse duration, interpulse intervals, and dominant frequency.

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FIG. 1. Holotype of Proceratophrys huntingtoni sp. nov., adult male (UFMT 1745): (A) Dorsal view; (B) ventral view; (C) ventral view of right hand; (D) ventral view of left foot; (E) lateral view of the head. Scale = 10 mm. Color reproduction supported by the Thomas Beauvais Fund.

RESULTS Proceratophrys huntingtoni sp. nov. Orthochresonym: Proceratophrys cristiceps: Boulenger, 1903:69 Holotype.—UFMT 1745, an adult male collected on 29 August 2000 by Christine Stru¨ssmann during faunal monitoring activities at Manso Hydroelectric Power Plant, Municipality of Chapada dos Guimara˜es, Mato Grosso State, central Brazil. The specimen was calling from inside a grass tussock, near the headwaters of a small stream (14852 0 S; 55848 0 W), after heavy rain. Paratopotypes.—A total of seven paratopotypes: 2 adult females (UFMT 1748 and 11134), and 5 adult males (UFMT 1746, 1747,

1749, 11133, and 11135) collected on 29 August 2000 by Christine Stru¨ssmann. Paratypes.—A total of 14 specimens: 5 adult females (UFMT 6698, 6699, 6700, 6702, and 6704) and 5 adult males (UFMT 6695– 6697, 6701, and 6703) collected on 2–3 September 2006 by Marcos A. Carvalho at Fazenda Entre Rios (‘‘Jonas Pinheiro’’ small Hydroelectric Power Plant), municipality of Santo Antonio ˆ do Leverger, Mato Grosso State, Brazil; 3 adult males (UFMT 11129– 11131), and 1 adult female (UFMT 11132) collected on 27 November 2007 by Everaldo S. Moraes at Gruta da Cantina, municipality of Nobres, Mato Grosso State, Brazil; one adult male (UFMT 12635) collected on 20 July 2011 by Andre´ Pansonato and

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TABLE 1. Measurements (in millimeters) of male (including holotype) and female type specimens of Proceratophrys huntingtoni sp. nov. Means are 6 1 standard deviation, ranges are in parentheses. Character abbreviations are defined in the Material and Methods section. Character

SVL HL HW ED END TD TH TF F H IND TL FL IML UEW

Male (N = 14)

34.68 13.87 15.84. 4.33 3.08 2.01 13.46 18.03 14.36 9.31 2.41 13.36 8.16 2.76 4.10

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

2.07 1.10 0.88 0.47 0.34 0.34 1.18 1.23 0.97 0.56 0.30 0.86 0.42 0.31 0.30

Female (N = 8)

(31.75–38.67) (12.41–15.95) (14.25–16.97) (3.85–5.21) (2.53–3.54) (1.53–2.68) (11.24–15.87) (16.37–20.10) (12.83–15.86) (8.31–10.30) (1.74–3.17) (12.06–14.84) (7.45–8.73) (2.25–3.24) (3.61–4.86)

Christine Stru¨ssmann at Vale do Uatuma˜, municipality of Chapada dos Guimara˜es, Mato Grosso State, Brazil. Diagnosis.—The new species is characterized by: small size (31.75–38.67 mm SVL in males [N = 14]; 33.04–45.69 mm SVL in females [N = 8]), in comparison to congenerics; snout rounded in dorsal view, obtuse in lateral view, dorsal skin granular, foot length representing approximately 40% of SVL, absence of both postocular swellings and prominent palpebral appendages. These last two characteristics lead us to consider the new species as a member of the Proceratophrys cristiceps group (sensu Giaretta et al., 2000). Proceratophrys huntingtoni sp. nov. can be distinguished from the other species in the P. cristiceps group by the following characters: from P. cristiceps, by smaller SVL (vs. 40.62–49.09 mm in 5 males; 50.29–53.84 mm in 5 females), dorsal crests less defined beyond the sacral region (vs. more defined until the coccyx), and snout obtuse in lateral view (vs. vertical); from P. concavitympanum, by smaller SVL (vs. 45.76–49.23 mm in 3 males; 53.64–60.35 mm in 5 females), flared lips absent (vs. with flared lips), and inner metatarsal tubercle with dark brown color (vs. not colored); from P. cururu, by smaller SVL (vs. 36.5–43.1 mm in males; 47.0–53.9 mm in females); from P. goyana, by smaller SVL in males (vs. 43.41–46.3 mm; N = 2), snout obtuse in lateral view (vs. vertical), dorsal crests interrupted at the sacral region (vs. more defined extending to the coccyx), and canthal crests well defined (vs. not evident); from P. moratoi, by slightly larger SVL (vs. 24.7–30.9 mm in males; 32.1–41.6 mm in

41.06 16.51 18.34 4.83 3.94 2.15 14.84 21.64 16.88 10.91 2.99 15.18 9.12 3.37 4.63

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

5.16 (33.04–45.69) 1.95 (13.19–18.70) 2.56 (15.08–21.74) 0.42 (4.26–5.45) 0.74 (2.64–4.66) 0.40 (1.67–2.71) 1.68 (12.47–17.01) 3.11 (17.50–25.77) 2.45 (13.89–19.90) 1.56 (8.74–12.90) 0.82 (1.90–3.85) 1.48 (12.93–16.77) 0.84 (8.18–10.13) 0.50 (2.54–4.06) 0.56 (4.12–5.49)

females), snout obtuse in lateral view (vs. vertical), and longer legs (vs. mean TH 10.9 mm, range 10.2–11.6 mm; mean TL 9.9, range 9–10.7 mm); from P. strussmannae, by smaller SVL (vs. 41.1–47.3 mm in males; 52.7–59.8 mm in females); from P. vielliardi, by smaller SVL in males (vs. 39.1–41.9 mm in males), and presence of dorsal crests interrupted at the sacral region (vs. absent). Description of the Holotype.—Robust and stout body, head wider than long, head width representing 45.6% of SVL, snout rounded in dorsal view and obtuse in profile (Fig. 1A,E), eye diameter 20% larger than distance of eye to nostril, slightly smaller than upper eyelid length. Nostrils elliptical; canthal crests present on the canthus rostralis; 7 warts of equal size located at the margin of upper eyelid; a cutaneous dorsal crest from middle upper eyelid to sacral region, not reaching the coccyx; a row of three enlarged warts, initiating slightly above the corner of mouth, with the last at the level of mouth; a row of 8 tubercles on the lower jaw. Two rows of parallel warts (formed by 7 and 4 warts) extending from the end of hand to two-thirds of the length of the forearm. Fingers free, distally unexpanded, relative length 4 < 2 < 1 < 3; inner carpal tubercle oval in shape; outer carpal tubercle oblique, divided; subarticular and supernumerary finger tubercles enlarged, rounded (Fig. 1C). Toes with unexpanded tips, relative length 1 < 2 < 5 < 3 < 4; inner metatarsal tubercle piriform, with a dark brown color in the edge; outer metatarsal tubercle rounded, very small (Fig. 1D); a ridge of three warts in the tarsus, from beyond to the outer metatarsal tubercle; toes webbed

FIG. 2. Dorsal (A) and ventral (B) views of a live specimen (UFMT 12635) of Proceratophrys huntingtoni sp. nov. collected on 20 July 2011 at Vale do Uatuma˜, Chapada dos Guimara˜es, Mato Grosso, Brazil. Color reproduction supported by the Thomas Beauvais Fund.

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FIG. 3. Advertisement call of Proceratophrys huntingtoni sp. nov. (UFMT 1747), recorded in the municipality of Chapada dos Guimara˜es, Mato Grosso State, on 15 December 2000, 1830 h, air temperature 248C. (A) Oscillogram; (B) audio spectrogram.

basally, webbing formula: I 1-–2+ II 2+–3 III 3–2 ½ IV 3+–2 V. Foot length equals 23% of SVL. Dorsal skin basically granular, with scattered discrete warts; chest and belly covered with granulated skin. Dentigerous process of vomers oblique and barely separated, between choanae; vocal slits present, lateral to tongue. Tongue ovoid, covering the entire floor of mouth, notched posteriorly. Measurements of the Holotype (in Millimeters).—SVL 33.90; HL 13.46; HW 15.47; ED 3.70; END 2.96; TD 2.15; TH 13.55; TF 18.72; F 14.02; H 9.49; IND 2.45; TL 14.05; FL 8.25; IML 2.64; UEW 4.09. Coloration.—In life, five dark brown bands are present on each side of the face, each one separated by grayish-brown stripes. A dark brown stripe on canthus rostralis. There are 2–3 dark brown transverse stripes both on forearms, thighs and tibias. Dorsum predominantly light brown, with darker irregular patches in dorsolateral region and a clearer ‘‘X’’ on the back, from the supraocular region to the rump. Two triangular dark spots on interocular region. Irregular black reticulations all over the iris: over the golden middle section of its dorsal half, over the whitish middle section of its lower half, and over chestnut brown of anterior and posteriormost sections of the iris. Ventral color pattern not recorded in life.

Variation.—Sexual dimorphism is apparent, with females attaining greater SVL (Table 1). Adult males have a black pigmented vocal sac (Fig. 1B). Dorsal coloration is highly variable and there is a variation also in vermiculation pattern on belly. Four specimens (UFMT 6698, 6700, 6703, 6704) out of 22 have a light brown belly, without vermiculations. The coloration of a recently collected male specimen (UFMT 12635) was noted as follows: belly light vermiculations, chest and gular vermiculations, an evident patch in the innermost portion of the anterior ventral surface of the thighs. Little change in coloration is noted in relation to preserved specimens, with the exception of some apparent darkening of the brown markings (Fig. 2). Advertisement Call.—The advertisement call of P. huntingtoni is described based on 2 males recorded on 15 December 2000, respectively at 1815 h (unvouchered specimen) and 1830 h (UFMT 1747), at air temperature of 248C. Both calling males were found semiburied, inside a grass tussock, in a narrow gallery forest, at the margin of a small, intermittent oligotrophic headwater stream (14855 0 26 00 S; 55848 0 20 00 W) amid a matrix of open Cerrado vegetation (see below). The advertisement call of P. huntingtoni (Fig. 3) consists of a single note with 19–25 pulses (N = 103), and ascendant

TABLE 2. Measurements of acoustic parameters for two males of Proceratophrys huntingtoni sp. nov. Values are: mean 6 1 standard deviation, and ´ range, in parentheses. LH = Banco de Registros Bioacusticos, ´ Laboratorio de Herpetologia, IB-UFMT. LH 18A-01 (unvouchered) and LH 18A-02 (voucher specimen UFMT 1747). N = number of calls analyzed.

Note duration (sec) Internotes interval (sec) Dominant frequency (Hz) Number of pulses Pulse duration Interpulses interval (sec) Mean rate of notes/min

LH 18A–01 (N = 46)

LH 18A–02 (N = 57)

0.275 6 0.017 (0.2–0.32) 0.7 6 0.38 (0.37–2) 1284.9 6 23.6 (1263.8–1344.5) 22 6 1.3 (20–25) 0.007 6 0.001 (0.006–0.009) 0.005 (0.004–0.006) 64.25 6 11.9

0.271 6 0.01 (0.24–0.3) 0.7 6 0.35 (0.34–2.38) 1222.1 6 47.8 (1095–1316.7) 20.8 6 0.8 (19–23) 0.007 6 0.001 (0.005–0.009) 0.0045 (0.004–0.006) 65.15 6 6.26

Mean (N = 103)

0.27 0.7 1250.2 21.3 0.007 0.0046 64.63

6 6 6 6 6 6 6

0.01 (0.2–0.3) 0.36 (0.3–2.3) 49.9 (1095–1344.5) 1.2 (19–25) 0.001 (0.005–0.009) 0.0006 (0.004–0.006) 9.17

470

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FIG. 4. Known geographic distribution of Proceratophrys huntingtoni sp. nov. Circles: (1) Nobres municipality; (2) Santo Antonio ˆ do Leverger municipality. The star represents the type locality: Chapada dos Guimara˜es, Mato Grosso State, Brazil.

frequency modulation. Calls have a mean duration of 0.27 6 0.01 (range 0.2–0.3 sec) and are repeated at mean intervals of 0.7 sec. Notes were emitted at a rate of 64.6/min. Pulses have mean duration of 0.007 sec (except for the last pulse, which varies from 0.16–0.2 sec) and mean intervals of 0.005 sec. The mean dominant frequency was 1,250.2 Hz (Table 2). Natural History.—The new species inhabits narrow gallery forests alongside intermittent headwater streams amidst Cerrado. Males were heard calling near the margins of such intermittent streams both in relatively plain terrains and on the slopes of granitic (Santo Antonio ˆ do Leverger), limestone (Nobres), and sandstone formations (Chapada dos Guimara˜es). Males were ´ recorded in a small tributary of ‘‘Corrego Bananal,’’ which flows into the Casca River (which belongs to Manso River sub basin, and ultimately to the Cuiaba´ River Basin and Upper Paraguay River Basin). The small stream is situated at Fazenda Morro do Chape´u, Chapada dos Guimara˜es municipality, Mato Grosso State. Proceratophrys huntingtoni is a nocturnal, terrestrial species. The climate in the geographic range of the new species is generally hot and semihumid, with two well-marked seasons: the rainy season, from October to April, and the dry season, from May to September. Mean temperature in Chapada dos Guimara˜es region is 268C, and mean monthly relative air humidity varies from 60–83%, with a drop to approximately 30% in July and August (Alho, 2000). Total annual precipitation is 1,800 mm, on average (Brasil, 1992). Distribution and Conservation Concerns.—Proceratophrys huntingtoni is known from three municipalities in Mid-Southern Mato Grosso State, all of them in the Cerrado domain (Fig. 4). The Cerrado encompasses approximately 2 million km2, being the second largest vegetational domain in Brazil (Ratter et al., 1997). Despite their biological importance (Myers et al., 2000), natural areas of Cerrado are being greatly disturbed by the advance of the booming agricultural frontier, with more than 2 million ha of pristine habitats destroyed each year (Klink and Machado, 2005). Additionally, many huge areas of Brazilian Cerrado have been lost because of the establishment of hydroelectric impoundments (e.g., Manso powerplant, 427 km2, Mato Grosso State; Serra da Mesa, 1,780 km2, Goia´s State; see Alho, 2000, and Branda˜o and

Araujo, ´ 2008, respectively). Also, complexes of townhouses and other facilities are usually built near the margins of new reservoirs, as is the case at Manso Power Plant, increasing land division and habitat losses. Etymology.—The specific epithet honors Herbert Huntington Smith (1851–1919), an American naturalist and amateur conchologist, who signed himself ‘‘H. Huntington’’ in some of his chronicles. Smith traveled into southern Mato Grosso and collected zoological specimens in the small village of Chapada dos Guimara˜es between 1882 and 1885. Specimens of amphibians and reptiles obtained by Smith in Chapada were sent to the herpetologist Edward Drinker Cope, from the Academy of Natural Sciences (Philadelphia, PA), who described many new taxa based in that material (Cope, 1887). Interesting information on geology, landscapes, and biogeography of southern Mato Grosso were published in the book ‘‘Do Rio de Janeiro a Cuyaba´: notas de um naturalista’’ (Smith, 1922). Smith’s writings from the period spent in Chapada, however, were seemingly never published, as was his original intention. DISCUSSION Proceratophrys huntingtoni is the sixth species of the P. cristiceps group recorded for the Cerrado biome. In addition, at least one species in the same group, Proceratophrys concavitympanum, was originally described from Amazonian sites and lately recorded in forested habitats in central Cerrado (Pavan, 2007). In the remaining two species groups within the genus Proceratophrys, species in the P. boiei group (12 species in total) are mostly restricted to the Atlantic Forest, except for P. rondonae, described from Amazonian sites of the Guapore´ River drainage, in the Brazilian state of Rondonia ˆ (Prado and Pombal, 2008). Contrarily, in the P. bigibbosa species group (comprising four species), most species are restricted to subtropical regions of southern Brazil and Argentina (Kwet and Faivovich, 2001). Note duration of the advertisement call of P. huntingtoni is similar to that in P. moratoi and in P. concavitympanum (Brasileiro et al., 2008; Santana et al., 2010, respectively). However, it is strikingly different from note duration in other species of Proceratophrys also belonging to the P. cristiceps group (e.g., P. cristiceps, P. cururu and P. vielliardi; Table 3). It is very distinct, also, from note duration in species of the P. bigibbosa group: P. avelinoi (Kwet and Baldo, 2003), P. brauni (Kwet and Faivovich, 2001), and also in P. paviotti (Cruz et al., 2005) and P. sanctaritae (Cruz and Napoli, 2010), species in the P. boiei group. The dominant frequency of the advertisement call of P. huntingtoni is similar to that in P. moratoi (Brasileiro et al., 2008) and P. vielliardi (Martins and Giaretta, 2011), being lower than dominant frequency in P. avelinoi (Kwet and Baldo, 2003), and considerably higher than dominant frequency recorded for P. cristiceps (Nunes and Junca´, 2006), P. concavitympanum (Santana et al., 2010), P. cururu (Eterovick and Sazima, 1998), P. melanopogon (Mangia ˆ et al., 2010), P. sanctaritae (Cruz and Napoli, 2010), and P. paviotti (Cruz et al., 2005). The number of pulses in the call of P. huntingtoni is lower than in P. cristiceps (Nunes and Junca´, 2006), P. cururu (Eterovick and Sazima, 1998), and P. sanctaritae (Cruz and Napoli, 2010) and higher than in P. vielliardi (Martins and Giaretta, 2011). Note repetition rate is higher in the new species than in P. moratoi (Brasileiro et al., 2008) but lower than in P. vielliardi (Martins and Giaretta, 2011; Table 3). The ascendant frequency modulation found in the advertisement call of P. huntingtoni is known to occur in two other species: P. cururu, and P. paviotti (Eterovick

N

Note duration

35 0.59 6 0.83 (0.40–0.84)

P. vielliardi

8

P. paviotti P. sanctaritae

60

Proceratophrys boiei group P. melanopogon P. moehringi

P. brauni

1,179 6 66.66 (999.12–1,274.10) 450 (200–700)

1.350 (800–1,800)

0.387 6 0.028 (0.347–0.427) 660–1,280 0.4 (0.2–0.9) 1,130 (950–1,290)

0.79 (0.7–0.9)

1,600 (1,050–2,300)

1,133.8 6 93.3 (1,022.0–1,291.0)

1,342 6 73.7 (1,174–1,444)

59 0.245 6 0.02 (0.1–0.3)

600–1,000 1,250.2 6 49.9 (1,095–1,344.5)

Proceratophrys bigibbosa group P. avelinoi 1.6–1.9

57.46 6 6.02 (46–69)

Pulses

28.1462.12 (26–32) 46.70 6 6.40 (31–94)

26 (24–28)

37.5 6 9.4 (23–70)

6.4 6 0.9 (4.0–9.0)

20.5 6 2.5 (15–26)

21.3 6 1.2 (19–25)

45

948.17 6 66.66 (850.99–1,186.35) 30.85 6 4.81 (19–37)

103 0.27 6 0.01 (0.2–0.3)

1.2

13 0.37 6 0.06 (0.23–0.50)

940 6 0.2 (900–990)

Dominant frequency (Hz)

P. huntingtoni sp. nov. P. moratoi

P. concavitympanum P. cururu

Proceratophrys cristiceps group P. cristiceps 29 0.66 6 0.05 (0.52–0.79)

Taxa

TABLE 3. Advertisement calls described for the genus Proceratophrys.

118.8 6 69.7 (42.0–202.0)

32.3 6 6 (28.9–41.8)

64.63 6 9.17

Notes/minute

Nunes and Junca´, 2006 Santana et al., 2010

Reference

Mangia ˆ et al., 2010 Weygoldt and Peixoto, 1985 Ascendant Cruz et al., 2005 Cruz and Napoli, 2010

Kwet and Baldo, 2003 Kwet and Faivovich, 2001

Brasileiro et al., 2008 Martins and Giaretta, 2011

Ascendant Eterovick and Sazima, 1998 Ascendant

Not

Modulation frequency

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and Sazima, 1998; Cruz et al., 2005), being absent in P. cristiceps (Nunes and Junca´, 2006) (Table 3). With the addition of P. huntingtoni, the number of species in the P. cristiceps group raises to eight. Because of deficient information in the original description of many species in this group, a thorough revision of it, as previously made for the P. biggibosa and P. boiei groups by Prado and Pombal (2008), and by Kwet and Faivovich (2001), respectively, is badly needed. Proceratophrys goyana, for example, was described based only on two specimens from the state of Goia´s, and erroneously illustrated with a figure of P. cristiceps (see Miranda-Ribeiro, 1937). Acknowledgments.—Thanks are due to Marcos A. Carvalho, Jose´ P. Pombal Jr., and Luis F. Toledo for providing access to the ´ Coleca ¸ ˜ o Zoologica de Vertebrados da Universidade Federal de Mato Grosso, Museu Nacional do Rio de Janeiro, and Museu de Zoologia Ada˜o Jose´ Cardoso, of the Universidade Estadual de Campinas, respectively. Two anonymous reviewers and Erin Muths made valuable comments and suggestions to improve the quality of the paper.

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APPENDIX 1 Specimens Examined Proceratophrys concavitympanum.—UFMT 6808 (Colniza, Mato Grosso); UFMT 6996 and 7825 (Juı´na, Mato Grosso); UFMT 7906 (Paranaı´ta, Mato Grosso); ZUEC 11387, 11388 (Espiga˜o D’Oeste, Rondonia– ˆ holotype and paratype); ZUEC 14874, 14876, 16015 (Paranaı´ta, Mato Grosso), ZUEC 14950 (Jacareacanga, Para´). Proceratophrys cristiceps.—MNRJ 16472–16481. Proceratophrys bigibbosa.—ZUEC 10405–10406 (Sa˜o Francisco de Paula, Rio Grande do Sul). Proceratophrys goyana.—ZUEC 4110 (Picos, Piauı´); ZUEC 4125 (Santana do Cariri, Ceara´). Proceratophrys moratoi.—ZUEC 7031–7033 (Rubia˜o Jr., Botucatu, Sa˜o Paulo). Proceratophrys strussmannae.—UFMT 5859, 6659, 7869, 7872, 7874, 7876, 7878, 7880, 7882, 7885, 7886, 8319, 8320, 8377–8380 (Jauru and Vale de Sa˜o Domingos, Mato Grosso).