Phyllomedusa araguari, Giaretta, Ariovaldo A., De, Júlio C., Filho, Oliveira & De, Marcelo N., 2007

Giaretta, Ariovaldo A., De, Júlio C., Filho, Oliveira & De, Marcelo N., 2007, A new Phyllomedusa Wagler (Anura, Hylidae) with reticulated pattern on flanks from Southeastern Brazil, Zootaxa 1614, pp. 31-41 : 32-40

Phyllomedusa araguari sp. n.

( Figures 1 A–B, 2, and 3A–C right)

Holotype: ZUEC 12880 (formerly AAG-UFU 2598), an adult male from the Estação de Pesquisa e Desenvolvimento Ambiental Galheiro (± 19o12’S, 47o10’W; 900 m altitude), municipality of Perdizes, Minas Gerais, Brazil, collected by M. N. de C. Kokubum, J. C. de Oliveira Filho, and A. A. Giaretta, on December 5, 2003.

Paratopotypes: Two adult males. AAG-UFU 2576, November 22, 2003; AAG-UFU 2597, December 5, 2003; same collectors of the holotype.

Diagnosis: Phyllomedusa araguari sp. n. is like some other species in the P. hypochondrialis group by having a distinct reticulated pattern on flanks, as P. ayeaye ( Figures 1 D and 3B left), P. centralis , P. itacolomi , P. megacephala ( Figures 1 C and 3A left), and P. oreades ( Figure 3 C left). Phyllomedusa oreades Brandão 2002 topotypes and P. megacephala ( Miranda-Ribeiro 1926) are distinct from P. araguari sp. n. by lacking a reticulate pattern bordering the upper jaw and encircling the eyes. In P. ayeaye Lutz 1966 and P. itacolomi Caramaschi et al. 2006 the pattern on the hidden parts of legs tends to form large circles whereas in P. araguari sp. n. the legs are barred. Phyllomedusa araguari sp. n. emits short pulsed notes, whereas P. megacephala emits relatively longer notes (see call description below). Phyllomedusa araguari sp. n. is slightly smaller than P. c e n t r a l i s, P. megacephala , and P. itacolomi . From topotypic P. oreades , P. araguari sp. n. differs also by having a broader reticulated stripe on flanks, a better-defined reticulated pattern on the throat, belly, and ventral surfaces of hind limbs, and less protuberant nostrils. In life, P. araguari sp. n. has a white belly; this is in contrast to the pink venter of P. ayeaye , P. centralis and P. oreades , and with the yellow or orange venter of P. megacephala and P. itacolomi . In life, the mottled pattern of the concealed body parts of P. araguari sp. n. are orange, not salmon, as in P. centralis and the reticulation is dark blue, not black as in P. centralis , gray as in P. ayeaye , or deep purple as in P. itacolomi . The new species is a pond breeder, whereas P. c e n t r a l i s, P. megacephala ( Eterovick and Sazima, 2004; AAG, pers. obs.) and P. o re a d e s ( Brandão, 2002) breed in streams.

Phyllomedusa araguari sp. n. can be distinguished from the remainder species of the P. hypochondrialis group ( P. azurea , P. hypochondrialis , P. nordestina , P. rohdei , and P. palliata ) by having a reticulate pattern bordering the upper jaw and eyes and with orange cells with dark blue reticulations on flanks, additionally from P. rohdei and P. palliata by not having white stripes along the lateral part of body.

Description of the holotype: Description of the holotype: (ZUEC 12880, adult male, Figures 1 A, 2, and 3A and C right). Measurements in Table 1 . Proportions of body parts in relation to SVL (37.4 mm): HW – 31.8%, HL – 24.1%, ED – 11.2%, TD – 4.8%, FL – 32.9%, HAL – 27.5%, SL – 39.6%, TL – 41.4%. General aspect slender; snout round in dorsal view ( Figure 2 A) and vertical in lateral view ( Figure 2 B); loreal region slightly concave; nostrils and eyes laterofrontally positioned; tympanum nearly circular, annuli undefined at the superior border; parotoids undistinguished; no vocal slits or external vocal sac; tongue nearly circular, free posteriorly; choanae small, nearly circular; rudimentary vomerine teeth bordering choanae antero-medially; arm thin; forearm robust; no finger webbing; comparative finger length I<II<IV<III; finger tips not expanded; palmar callosities poorly developed ( Figure 2 C), inner and outer metacarpal tubercles undifferentiated; subarticular tubercles developed, barely distinct from adjacent supernumerary tubercles; nuptial asperity covering most of the dorsal face of finger I, except the tip; toe tips not expanded; comparative toe length II<I=III<V<IV; plantar callosities poorly developed ( Figure 2 D), inner and outer metatarsal tubercles undifferentiated; no toe webbing; dorsal skin smooth; ventral skin granulated on belly and throat; ventral surface of thigh granular anteriorly and smooth posteriorly.

Variation: Variation in size in Table 1 . The paratopotypes AAG-UFU 2576 and 2597 have a more rounded snout (less vertical) in lateral view than the holotype. The paratype AAG-UFU 2576 has a discrete thin white vertebral stripe from between nostrils to vent ( Figure 3 B right).

Coloration in life (N = 3 types, adult males, Figure 1 A–B): Dorsum and dorsal surfaces of forearm, shank, tarsus, and foot green or brownish green; flanks with dark blue reticulation encircling large vivid orange mottles from corner of mouth to groin; tympanic membrane green as the dorsum; dorsal surface of upper arms, fingers and toes reticulated as the flanks; hidden portions of shank, thigh, and tarsus with blue transversal stripes on a vivid orange background; border of maxillae and eyes circled by a fine light stripe with fine dark reticulations; throat and belly whitish; ventral surface of thighs discretely reticulated; iris silver with fine dark reticulation; pupil black.

Color in preservative (all three types): dorsal surfaces of body, forearms, tarsus and shank, bluish gray; blackish purple reticulations (cells) on flanks and irregular transverse bars (3–4, sometimes anostomosed) on hidden parts of thigh and ventral surface of shank; flank reticules increasing in size from the angle of mouth to groin; belly and chest discretely reticulated; lateral groin reticulations encircling large whitish mottles (vivid colors vanished). A thin light stripe with fine dark reticulations encircling the eyes and bordering the maxillae.

Tadpoles (N = 8, AAG-UFU 4200): Examined specimens at Gosner stage 25–33. Maximum observed total length– 45.7 mm (stage 33); body 31–32% of total length. Body ovoid in lateral and dorsal views, acuminated anteriorly. Labial tooth row formula– 2(2)/3(1), anterior gap broader than the posterior; third posterior tooth row 1/3 the length of the others. Oral apparatus– frontal. Medial marginal papillae gaps– one broad anterior and one short posterior (posterior gap absent in small (length <25 mm TL specimens). Submarginal papillae– present at latero-posterior borders. Disc emargination– no. Nares– small, closer the snout than to the eyes (dorsal view). Eye position– lateral. Spiracle– sinister, almost ventral, not forming a free tube. Upper jaw sheath– arc-shaped with a medial point, horny, serrated. Lower jaw sheath– V-shaped, horny, serrated. Dorsal fin– straight or slightly arched until the mid length of tail, greater height after the mid-length of tail; inserted at the body/tail junction. Ventral fin– deeper than the dorsal, slightly arched; great height just after the midlength of tail. Tail tip– acute flagella. Vent tube– dextral, without a free border. Body whitish; transparent or gray belly; tail translucent, with a large pale gray mottle across mid tail.

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Behavior and habitat: Males were found calling during the night along a narrow (0.5 m wide) deep (2 m) erosive trench (100 m) bordered by short (<1 m high) dense grass-like vegetation and sparse low (<2 m high) shrubs, including Velloziaceae . The tadpoles were found in deep (up to 2.5 m) pools along the trench. The water of these pools was colored muddy red and was permanently shaded by the marginal bank and bordering vegetation. One egg clutch (AAG-UFU 4201) was found in December (2003), it was wrapped in a leaf ( Melastomataceae ) hanging over a pond. It had 24 eggs with embryos (Gosner stage 21, 21.8 mm TL), and many small (2 mm) jelly spheres. Syntopic frogs shearing the same water body were Ameerega flavopicta (Lutz) and Leptodactylus cunicularius Sazima & Bokermann.

Advertisement call: Figure 4 A–D. Call (N = 1 male, 6 analyzed calls) composed of 5–9 notes (Mean = 7, SD = 1.7) emitted around one time per minute; call duration 980–2480 ms (Mean = 1900, SD = 570) with a time interval of 23100–47400 ms (Mean = 32100, SD = 11140). Note duration 30–50 ms (Mean = 40, SD = 6), duration of inter-note intervals 260–310 ms (Mean = 280, SD = 30). Notes with three to five pulses (Mean = 4.2, SD = 0.75), pulse duration 4–10 ms (Mean = 8, SD = 2); inter-pulse intervals 1–8 ms (Mean = 3, SD = 2). The dominant and fundamental are coincident, whit an energy maximum at 1722 Hz.

Phyllomedusa megacephala advertisement call: Figure 5 A–D. One male recorded (N = 10 analyzed calls). Call composed of 6–7 notes (Mean = 6.70, SD = 0.48) emitted around 13 times per minute; call duration 1370–1800 ms (Mean = 1610, SD = 150) with an interval of 1330–2740 ms (Mean = 1760, SD = 400). Note duration 90–140 ms (Mean = 110, SD = 20), duration of inter-note intervals 100–230 ms (Mean = 130, SD = 40). Notes with six to ten pulses, pulse duration 10–30 ms (Mean = 20, SD = 7); inter-pulse intervals 5– 40 ms (Mean = 10, SD = 10). The frequency raises from the beginning to the end of the call. The dominant and fundamental frequencies coincide, with an energy maximum at 1722 Hz.

Etymology: The specific epithet “ araguari ” is an indigenous Tupi word for the white-eyed parakeet ( Aratinga leucophthalmus ), it is also the name of the dammed river bordering the type locality of the new species and the name of a municipality at its margins. It is used as a noun in apposition. The new species is named after the formerly beautiful Araguari River, now severely damaged by the human activities. At the time of writing this paper two other dams were built at sites further downstream.

Distribution: Just known from the type locality.

Additional remarks. Phyllomedusa azurea is a ubiquitous species in the Brazilian Cerrados and is known to occur along the Araguari River in Uberlândia municipality (MG), about 150 km down the type locality of P. araguari sp. n.. We predict that both species may not overlap extensively in distribution since, similar to the other species of the P. hypochondrialis group with a reticulate pattern on flanks, the new species appears to be restricted to sites at relatively high elevations (> 900 m alt.) (Caramaschi et al., 2006).

The tadpole of Phyllomedusa ayeaye was originally studied by Lutz (1966) and, based on the same specimens, re-described by Cruz (1982). None of these works mentions a gap in the posterior row of papillae; in our sample (seven tadpoles; Gosner 25–41) of topotypes this gap is well defined. As observed in the new species, this feature appears to vary ontogenetically, being better noticed in larger (> 25 mm TL) and advanced (Gosner> 25) specimens.

The holotype of P. oreades is referred as having “vocal slits circular”, we have re-examined the holotype and five other adult male paratopotypes and did not found any sign of vocal slits. The holotype of P. oreades is also an exceptionally small male, with a shank length significantly (t = 3.20, p <0.05, df = 4) shorter than the mean of the other five male paratopotypes listed in Table 2 . Phyllomedusa oreades has been referred as occurring, in addition to the type locality (Serra da Mesa, Goiás), in localities around Brasília (DF) ( Figure 2 in Brandão, 2002). The large finger discs, broad reticulated pattern on flanks and reticulated border of maxillae of the individuals of this southern population renders their assignation to this species problematic. Actually, these last two features of the specimens from Brasília make them more similar to the new species described herein than to P. o re a d e s. Further studies and call analyses of specimens of P. oreades from the type locality, and of specimens from Brasília, are needed to elucidate this question.

The frog fauna of Galheiro shares identity with that of the Serra da Canastra ( Haddad et al., 1988; Oliveira Filho & Kokubum, 2003), which lays about 120 km to southeast. Recently Araújo et al. (2007) reported the presence of Pyllomedusa ayeaye there. We recommend studies on acoustics of the population of Serra da Canastra because to altitudinal restricted species, such as those of the P. hypochondrialis group with reticulated pattern on flanks, it is expected that the Rio Grande River may represent a major barrier to dispersion.

As the new species is a grass/shrub environment dweller, it probably is not threatened of extinction by local human activities such as damming, deforestation, and cattle farming. Potential threats appear to include fires, exotic grasses ( Melinis minutiflora Beauv ) over-shadowing trenches/ponds, and removal of natural vegetation for agriculture.

Figures

FIGURE 1. Three closely related species of Phyllomedusa from the state of Minas Gerais in life. A and B – Phyllomedusa araguari sp. n. (A – holotype ZUEC 1280; B – paratopotype AAG-UFU 2576); C – Phyllomedusa megacephala, Serra do Cipó; D – Phyllomedusa ayeaye topotype. C and D – unvouchered photos.

FIGURE 2. Phyllomedusa araguari sp. n. (holotype AAG-UFU 12880). A – Dorsal and B – lateral views of head; C – palmar and D – plantar views.

FIGURE 3. Dorsal views of three closely related species of Phyllomedusa illustrating their general aspect and patters on the hidden parts of legs. At right Phyllomedusa araguari sp. n. types (A and C – holotype ZUEC 12880 (former AAG- UFU 2598); B – paratopotype AAG-UFU 2576). Upper left – P. megacephala (ZUEC 2284), Serra do Cipó; Middle left – P. ayeaye (ZUEC 4160) topotype; Bottom left – P. o re a d e s (CHUNB 12515) topotype.

FIGURE 4. The advertisement call of Phyllomedusa araguari sp. n.. A – Spectrogram of an entire call with nine notes, B – Spectrogram, C – Oscillogram, and D – Power spectrum of the fifth note. AAG sound file PhyllomedaraguMG 1 bAAGm. Specimen recorded on December 0 5 2003, 21: 40 h; air temperature 23 C. Voucher paratopotype AAG-UFU 2597. Estação de Pesquisa e Desenvolvimento Ambiental Galheiro (CEMIG), municipality of Perdizes, Minas Gerais, Brazil.

FIGURE 5. The advertisement call of Phyllomedusa megacephala. A – Spectrogram of an entire call with seven notes, B – Spectrogram, C – Oscillogram, and D – Power spectrum of the fifth note; a denotes the background call of other frog species (Physalaemus cuvieri). AAG sound file PhyllomedmegacepMG 3 AAGb. Specimen recorded on December 0 4 2005, 18: 40 h; air 17.9, water 22.9 C. Voucher: AAG photo (Figure 1 C). Specimen from Serra do Cipó, Minas Gerais, Brazil.

Tables

TABLE 1. Measurements of the types of Phyllomedusa araguari sp. n.. Specimens from Estação de Pesquisa e Desenvolvimento Ambiental Galheiro, municipality of Perdizes, Minas Gerais, Brazil.

Specimens/ Feature	ZUEC 12880* AAG-UFU 2576	AAG-UFU 2597
Snout-vent length Head width	37.4 37.1 11.9 11.9	38.0 11.4
Head length	9.0 8.5	8.6
Eye diameter Tympanum diameter	4.2 4.5 1.8 1.6	4.1 1.9
Foot length	12.3 11.8	12.3
Hand length Shank length	10.3 9.6 14.8 13.7	0.0 15.1
Thigh length	15.5 13.4	16.0
Finger III disc diameter Toe IV disc diameter	0.9 1.0 1.0 1.1	0.9 1.0
Eye/nostril distance	2.1 2.2	2.1
* Holotype.

TABLE 2. Measurements of adult males types of Phyllomedusa oreades Brandão, 2002. Specimens from Serra da Mesa, state of Gois. Specimens deposited in CHUNB collection.

Specimens/ Feature	12510*	12513	12515	12514	12512	12516
Snout-vent length	34.2	35.8	37.3	36.3	37.3	35.3
Head width Head length	11.7 8.3	12.1 8.8	12.5 9.5	12.2 8.6	13.1 9.7	12.0 9.0
Eye diameter	4.3	4.7	4.4	4.4	4.8	4.2
Tympanum diameter Foot length	2.0 10.7	1.4 12.0	1.8 12.4	1.6 12.2	1.7 12.8	2.1 12.5
Hand length	8.7	10.1	10.0	10.0	10.6	9.9
Shank length Thigh length	12.2 12.1	14.1 14.8	15.7 16.3	14.4 14.6	15.5 16.5	14.3 14.9
Finger III disc diameter	0.9	1.1	1.1	1.1	1.0	0.9
Toe IV disc diameter Eye/nostril distance	1.0 2.3	1.1 2.3	1.2 2.5	1.1 2.5	1.1 2.3	0.9 2.3
*Holotype.