AnimaliaAnuraCraugastoridaeOliveiraElciomar Araújo DeRodriguesLuis ReginaldoKaeferIgor LuisPintoKarll CavalcanteHernández-RuzEmil JoséA new species of Pristimantis from eastern Brazilian Amazonia (Anura, Craugastoridae)Zookeys282017201768710112910.3897/zookeys.687.13221 Pristimantis latro http://zoobank.org/19BF72F8-BDA4-4C8C-965D-0D92B654B1DA sp. n.Figure 4Holotype.

LZATM – 467, adult female, collected on July 23, 2012 in the municipality of Anapu, Pará State, Brazil (3°9'28.15"S; 51°27'51.67"W) by Elciomar Araújo de Oliveira, Emil José Hernández Ruz and Joyce Celerino de Carvalho. Material stored in the collection of the Laboratório de Zoologia de Altamira (LZATM) of the Universidade Federal do Pará, Campus de Altamira, Brazil.

Paratopotypes. Two adult males: LZATM 739, LZATM 747 and nine adult females: LZATM 743, LZATM 749, LZATM 750, LZATM 740, LZATM 742, LZATM 754, LZATM 742, LZATM 748, LZATM 751, collected during field work by Claudia Liz Teles and Joyce Celerino de Carvalho. Material stored in the collection of the Laboratório de Zoologia de Altamira (LZATM) of the Universidade Federal do Pará, Campus de Altamira, Brazil.

Paratypes. Six males: LZATM 197, LZATM 0063, LZATM 1339, LZATM 818, LZATM 815, LZATM 816 and LZATM 1340. Eleven females: LZATM 386, LZATM 243, LZATM 360, LZATM 744, LZATM 281, LZATM 742, LZATM 748, LZATM 751, LZATM 230, LZATM 358 and LZATM 277 collected during field work by Claudia Liz Teles and Joyce Celerino de Carvalho. Material stored in the collection of the Laboratório de Zoologia de Altamira (LZATM) of the Universidade Federal do Pará, Campus de Altamira, Brazil. The collection locations of each specimen are listed in Appendix 1.

Holotype of Pristimantis sp. n. A ventral view B dorsal view C side view of the head D hand E and right foot (INPA-H 34576).

Allocation to genus and species group of the new species.

No morphological synapomorphy has yet been identified to support the genus Pristimantis (Hedges et al. 2008). The new taxon is therefore assigned to the genus Pristimantis based on (1) molecular phylogenetic relationships (Figure 2); and (2) its morphological characteristics, which fall into the range of other known Pristimantis species. The new taxon is assigned to the genus Pristimantis based on its geographic distribution and overall similarity to the majority of species of Pristimantis described. We assign the new species to the P. conspicillatus species group following Maciel et al. (2012) for having Finger I longer than Finger II, granular but nor aerolate belly, a tarsal fold, distinct tympanic membrane, and by its advertisement call composed of single pulsatile notes modulated in amplitude, as well as molecular phylogenetic relationships.

Diagnosis.

Pristimantis latro sp. n. is distinguished from other species of the group by the following combination of characters (summarized in Table 4): (1) dorsal skin weakly shagreened or smooth, dorsal tubercles present, dorsolateral folds absent, smooth skin on belly; (2) whitish or yellowish ventral coloration with black spots; (3) one subarticular tubercle on fingers I and II and two on Fingers III and IV; (4) supernumerary tubercles present at the base of fingers I, II, and III, and almost the same size of subarticular tubercles; (5) lateral fringes along fingers; (6) supernumerary tubercle present at the base of Toe IV; (7) basal webbing between toes and weak lateral fringes on toes; (8) twenty-one molecular autapomorphies for the gene fragment 16S mtDNA (Table 5); (9) call consisting of seven notes.

Comparison of diagnostic characters of some species of the Pristimantis conspicillatus group, including the new species: (1) belly texture (smooth or granular), (2) dorsal tubercles (present or absent); (3) fringe on finger (present or absent); (4) dorsolateral fold (present or absent); (5) fringe on toe (prominent, weak, absent); (6) basal membrane on toe (present or absent); (7) tarsal fold (prominent, weak or absent); (8) throat color pattern (stained, immaculate, variable or light); (9) supernumerary plant tubercle (present or absent); (10) External palmar tubercle (whole, split or semi-split).

Species12345678910
P. fenestratus*smoothpresentabsentweakpresentstainedabsent–-
P. fenestratus**smoothabsentpresentabsentweakpresentpresentvariablesplit
P. koehleri granular laterallyabsentabsentabsentweakabsentpresentlightpresentsplit
P. dundeei granularpresentabsentabsentprominentpresentpresentstainedsplit
P. samaipatae smoothabsentabsentabsentprominentabsentpresentstainedsplit
P. ventrigranulosus granularabsentweak or absentabsentweakpresentprominentweakly spottedabsentsingle
P. zeuctotylus smoothabsentabsentpresentabsentabsentabsentstainedpresentinteiro
P. chiastonotus smoothabsentabsentpresentabsentabsentabsentligthpresentsplit
Pristimantis latro sp. n. smooth present present present weak present weak stained present split

Diagnostic characters observed in the 16S mtDNA gene fragment from Pristimantis sp. n. and other species of the genus Pristimantis. The first column indicates the character position within the fragment. (-) indicates deletions.

Position (pb) P. latro sp. n. P. fenestratus (Borba 1) P. fenestratus (Borba 2) P. fenestratus (Bolivia) P. koehleri (Bolivia) P. chiastonotus (Brazil)
86GAAAAA
138AGGGGA
144TCCCCC
149ATTTTA
184TCCCCC
194C----A
197TAAAAC
202TAAAA-
208TCCCCC
229CTAAAT
230CTTTTT
237T----C
239TCCCCA
247CATTT-
269CTTTTT
273ACTTTA
289GAAAAA
293T-AAA-
330CTTTTT
401GAAAAA
455CTTTTA
Comparison with other species.

Due to difficulties in visiting museums to compare some of the species in the Pristimantis conspicillatus group with the species described in this work, data from the literature was used for this procedure. The consulted reference can be found, between brackets, at the end of each comparison. The character state of the compared species is between parentheses. Pristimantis latro sp. n. is distinguished from P. fenestratus by the absence of discoidal fold (present), the presence of supernumerary tubercles on hand (absent), length of notes in the male advertisement call ranging from 31 to 45.91 ms (50 to 91 ms) [Duellman and Lehr 2009; Padial and De La Riva 2009; Maciel et al. 2012]; from P. koehleri by smooth belly skin (finely granular), absence of discoidal fold (present), rostrum subacuminate in dorsal and protruding in lateral view (acuminate in dorsal view and subacuminate in lateral view), vocalization composed by seven notes (four, five, six, seven and eight notes) [Padial and De La Riva 2009]; from P. samaipatae by having whitish cream belly with black spots disposed randomly (immaculate), length of notes ranging from 31 to 45.91 ms (50 to 141 ms in P. samaipatae) [Köhler 2000; Padial and De La Riva 2009]; from P. dundeei by having smooth belly (areolate), presence of fringe in the fingers (absent), dorsolateral folds (absent), length of notes ranging from 31 to 45.91 ms (50 ms in P. dundeei) [Köhler 2000; Padial and De La Riva 2009]; from P. ventrigranulosus by having smooth belly skin (weakly areolate), dorsal tubercles (absent), presence of fringe in the fingers (weak or absent), dorsolateral fold present (absent), weak tarsal fold (prominent) [Maciel et al 2012]; from P. zeuctotylus by a divided palmar tubercle (entire), whitish cream-colored belly with black spots disposed randomly and dark brown dorsum (black belly and bronze dorsum) [Lynch and Hoogmoed 1977]; from P. chiastonotus for presenting basal webbing and fringe on the toes (absent), tarsal fold present (absent); snout subacuminate in dorsal view (acuminate), dorsal tubercles present (absent), vocalization composed by seven notes (one note) [Lynch and Hoogmoed 1977].

The comparisons were restricted to these species because they present the highest morphological and acoustic similarity with the new species. Another important factor is the geographical range of the new species, which becomes the only one in its group occurring in the eastern state of Pará, Brazil. The geographically-closest species are P. zeuctotylus and P. chiastonotus, north of Pará, whereas the most genetically-close are P. chiastonotus from the municipality of Monte Alegre in the state of Pará and the lineage of P. fenestratus from Borba 1 in the state of Amazonas.

Description of the holotype.

Adult female 40 mm SVL. Dorsal skin shagreened, absence of dorsal tubercles; smooth ventral skin, granular posterior surface of thighs; head longer (39% of the SVL) than wide; long snout, subacuminate in dorsal view and protruding in lateral view; concave canthus rostralis, flat loreal region; ovoid tongue covering the whole floor of the mouth; dentigerous process of vomer oblique and posterior to choanae; eye 78.9% of Distance from Eye to Nostril; elliptical pupil; absent supraocular tubercles; absent cranial crests; prominent supra tympanic fold, not contacting the eye; tympanic membrane 40% of ED, rounded, tympanic annulus prominent; relatively small hands, 26.25% of the SVL; relative length of fingers: II < IV < I < III; discs of Fingers III and IV are wider than fingers I and II; prominent, semi divided, heart-shaped external metacarpal tubercle; large internal palmar tubercle; one subarticular tubercle prominent on Fingers I and II, two prominent subarticular tubercles on fingers III and IV; supernumerary tubercles present at the base of fingers I, II and III; long legs, tibia 57% of the SVL; relative length of toes: I <II <V <III <IV; well developed and oval inner metatarsal tubercle; external metatarsal tubercle much smaller than the internal one; one subarticular tubercle on toes I and II; two subarticular tubercles on toes III and V; and three subarticular tubercles on toe IV; basal webbing and lateral fringes present on toes (weak); tarsal fold present.

Measurements of holotype (in mm). SVL: 40.0; HL: 15.6; HW: 14.5; SL: 7.9; DEN: 5.7; ID: 3.1; EL: 4.5; IoD: 3.9; EW: 3.6; TL: 1.8; AL: 8.9; HaL: 10.5; ThL: 20.5; TiL: 22.8; TaL: 11.9; FL: 18.9; LL: 30.3.

Color in life. Light brown dorsum with some black tubercles. Posterior and anterior limbs heavily barred dark brown. Weak labial bars. Black band extending from eye to tip of snout. Belly clear with some randomly scattered dark spots. Iris presents a yellowish coloration in the upper and lower part, whereas in the anterior and posterior region the color red is predominant.

Coloration in preservative. In alcohol, the coloration is predominantly brown in the dorsal region, whether male or female. The belly can be immaculate white or present dark spots arranged randomly. The dorsal band, present in some individuals, is white.

Variation (Figures 5 and 6). The males LZATM 197, LZATM 063 and LZATM 1339 have dorsal color light brown, while the males LZATM 818, LZATM 815, LZATM 816 and LZATM 1340 have dark brown dorsal and dorsolateral regions with more apparent brown bars. The ventral face of males may be immaculate white (LZATM 197, LZATM 816) or have black spots scattered around the belly and throat (LZATM 1339, LZA 063, LZATM 818, LZATM 815 and LZATM 1340). LZATM 1340 presents a heavily pigmented black throat, legs and arms with clear bars. Females have predominantly light brown dorsum, with weakly barred legs and arms of darker brown (LZATM 386, LZATM 467, LZATM 243, LZATM 360, LZATM 744, LZATM 281, LZATM 742, LZATM 748 and LZATM 751), while LZATM 230 and LZATM 358 have a darker coloration and a dorsal band from the face to the cloaca of yellow color (in life) and white (in alcohol). The latter individual has strongly barred legs and arms. Its belly is usually either immaculate white or with a few dark spots, but LZATM 277 has a belly and throat heavily black pigmented. The dorsal skin is smooth in most of the examined individuals, although some specimens present a weakly shagreened texture: LZATM 358, LZATM 816, LZATM 63, LZATM 1339, LZATM 1340 and LZATM 467.

Color variation in life of some individuals of Pristimantis latro sp. n. A holotype B, C paratypes of Anapu and D Altamira.

Dorsal and ventral morphological variation of the type series of Pristimantis latro sp. n. A Females in dorsal view B Females in ventral view C Males in dorsal view and D Male in ventral view.

Etymology.

The specific epithet “latro” (from the Latin latro = mercenary, robber) refers to the common name generally attributed to the species of Pristimantis – “Robber Frogs” – that exhibit a dark band on the snout, creating the illusion of a robber’s mask.

Distribution, ecology, and habitat.

Pristimantis latro sp. n. has been recorded in the municipalities of Anapu, Senador Jose Porfirio, Altamira, Medicilândia, Brasil Novo, Uruará and Flona Tapajós regions located in the interfluves Xingu / Tapajós and Xingu / Tocantins - Araguaia in Pará State, Brazil (Figure 7). It can be found in conserved areas of forests (Anapu, Flona do Tapajós) or with some environmental disturbance, e.g., forest fragments surrounded by pastures (Brasil Novo, Altamira and Vitória do Xingu). During the rainy/reproductive period, the males move up the vegetation to vocalize at a height of 1.5 m and in the dry period they can be found in the leaf litter.

Type locality of Pristimantis latro sp. n., municipality of Anapu, Pará, Brazil (star). The circles represent the other localities where the new species was found. The square and the diamond represent the localities of Pristimantis fenestratus used for the morphological and genetic comparisons. 1 Anapu (3°4'57.26"S; 51°22'25.67"W) 2 Senador José Porfírio (2°34'51.63"S; 51°56'13.47"W) 3 Altamira (3°13'24.85"S; 52°14'22.74"W) 4 Medicilândia (3°26'37.93"S; 52°53'35.26"W) 5 Flona do Tapajós (3°38'49.06"S; 55°11'46.00"W) 6 Borba (4°28'29.88"S; 59°42'12.06"W) and 7 La Paz, Bolivia (16°24'12.89"S; 68°6'10.20"W).

Appendix 1

Specimens examined. INPA-H (Instituto Nacional de Pesquisas da Amazônia – Herpetology); MPEG (Museu Paraense Emilio Goeldi); LZATM (Laboratório de Zoologia de Altamira); CTGANSISTA_D (Coleção de Tecidos de Genética Animal, Sisbiota Tapajós, margem direita).

Pristimantis fenestratus: INPA-H 34562, INPA-H 34565, INPA-H 34571, INPA-H 34573, INPA-H 34575, INPA-H 34577, INPA-H 34578, INPA-H 34579, INPA-H 34580, MPEG 7088, municipality of Borba, Amazonas, Brazil (type locality).

Pristimantis sp. n.: LZATM467, LZATM743, LZATM 739, LZATM749, LZATM747, LZATM750, LZATM740, LZATM742, LZATM754, LZATM742, LZATM748, LZATM751, MPEG 26050, MPEG 26059, MPEG 26052, MPEG 26063, MPEG 26065, municipality of Anapu, Pará, Brazil (type locality). LZATM 0063, LZATM139, LZATM155, LZATM213, LZATM265, LZATM270, LZATM277, LZATM280, LZATM281, LZATM386, LZATM 1344, LZATM 1112, MPEG 26055, MPEG 26053, MPEG 26054, MPEG 31415, MPEG 31416, MPEG 1113, municipality of Altamira, Pará, Brazil. LZATM137, LZATM138, LZATM197, LZATM 802, LZATM 876, LZATM 1340, municipality of Brazil Novo, Pará, Brazil. LZATM140, LZATM141, LZATM188, LZATM222, LZATM229, LZATM230, LZATM236, LZATM243, LZATM255, LZATM 818, LZATM 814, LZATM 816, LZATM 815, municipality of Medicilândia, Pará, Brazil. LZATM355, LZATM356, LZATM357, LZATM358, LZATM359, LZATM360, municipality of Uruará, Pará, Brazil. LZATM 753, LZATM 1125, LZATM 1140, municipality of Senador José Porfírio, Pará, Brazil. CTGANSISTA_D_1168, CTGANSISTA_D_1246, CTGANSISTA_D_1235, CTGANSISTA_D_1145, CTGANSISTA_D_1253, CTGANSISTA_D_1239, CTGANSISTA_D_1275, CTGANSISTA_D_1259, CTGANSISTA_D_1260, CTGANSISTA_D_1257, CTGANSISTA_D_1256, CTGANSISTA_D_1244, CTGANSISTA_D_1240 Flona Tapajós, Pará, Brazil.

Pristimantis zeuctotylus: LZATM1951, LZATM1054 and LZATM1057, municipality of Monte Alegre, Pará, Brazil.

Pristimantis chiastonotus: LZATM1050, LZATM1052, LZATM1055, and LZATM1056, municipality of Monte Alegre, Pará, Brazil.

Maximum Likelihood (ML) tree using the evolutionary model GTR + G, inferring phylogenetic relationships of Pristimantis sp. n. and other species of the P. conspicillatus group based on mitochondrial 16S mtDNA (490 bp). ML support values are shown before the “/”. Bayesian posterior probability support values (%) for major respective nodes are shown after the “/”. The horizontal bar below the tree represents the genetic distance between branches. The branch of the new species was collapsed (black triangle) to improve tree visualization.

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