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[left] Dendropsophus kamagarini [right] Dendropsophus kubricki Rivadeneira, Venegas & Ron, 2018
[lower] Dendropsophus parviceps (Boulenger, 1882)
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Abstract
The genus Dendropsophus is one of the most speciose among Neotropical anurans and its number of described species is increasing. Herein, molecular, morphological, and bioacoustic evidence are combined to assess species limits within D. parviceps, a widely distributed species in the Amazon Basin. Phylogenetic relationships were assessed using 3040 bp sequences of mitochondrial DNA, genes 12S, ND1, and CO1. The phylogeny shows three well-supported clades. Bioacoustic and morphological divergence is congruent with those clades demonstrating that Dendropsophus parviceps is a species complex. Dendropsophus parviceps sensu stricto occurs in the Amazon basin of Ecuador, northern Peru, southern Colombia and northwestern Brazil. It is sister to two previously undescribed species, Dendropsophus kubricki sp. n. from central Peru and Dendropsophus kamagarini sp. n. from southern Peru, northeastern Bolivia, and northwestern Brazil. Genetic distances (uncorrected p, gene 12S) between D. parviceps and the new species is 3 to 4%. Dendropsophus kamagarini sp. n. can be distinguished from D. parviceps by having a prominent conical tubercle on the distal edge of the upper eyelid (tubercle absent in D. parviceps). Dendropsophus kubricki sp. n. differs from D. parviceps by having scattered low tubercles on the upper eyelids (smooth in D. parviceps). Dendropsophus parviceps and both new species differ from all their congeners by their small size (adult maximum SVL = 28.39 mm in females, 22.73 mm in males) and by having a bright orange blotch on the hidden areas of the shanks and under arms. The advertisement call of the two new species has lower dominant frequency relative to D. parviceps. Probable speciation modes are discussed. Available evidence indicates that ecological speciation along an elevation gradient is unlikely in this species complex.
Keywords: Advertisement call, Amazon Basin, cryptic species, integrative taxonomy, morphology, phylogeny
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Figure 6. Dorsolateral and ventral views of Dendropsophus parviceps in life:
A, B Adult male, from type locality Sarayaku, Pastaza, Ecuador (QCAZ 52752) C, D Adult male, from Canelos, Pastaza, Ecuador (QCAZ 52816) E Adult male, from Yasuní, Orellana, Ecuador (QCAZ 51073) F Amplectant pair from Nuevo Rocafuerte, Río Napo, Orellana, Ecuador (QCAZ 44773–74) G, H Adult female, from Chiroisla, Río Napo, Orellana, Ecuador (QCAZ 44440). Photographs by S. Ron. |
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| Figure 1. Bayesian consensus phylogeny of Dendropsophus parviceps species complex based on 3040 bp of mtDNA. Node support is indicated with Bayesian posterior probabilities (pp) above branches and non-parametric bootstrap support below. Asteriks denote nodes with pp = 1 and bootstrap values = 100%. Outgroups, bootstrap values < 60%, and pp < 0.8 are not shown. Museum number and locality are provided for each sample. Abbreviations: BR = Brazil, PE = Peru, and EC = Ecuador. |
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Figure 9. Distribution of Dendropsophus parviceps species complex.
Dendropsophus parviceps (Northern Clade, blue crosses), D. kubricki sp. n. (Central Clade, green circles), D. kamagarini sp. n. (Southern Clade, orange rhombi). Stars = type locality, figures with a small black dot at the center = referred specimens, and hollow figures = unconfirmed records. |
Dendropsophus parviceps (Boulenger, 1882)
Hyla parviceps Boulenger, 1882: 393. Holotype BMNH 1947.2.13.51, an adult female from “Sarayacu”, Pastaza Province, Ecuador.
Hyla parviceps– Duellman and Crump 1974: 19; Duellman 1978: 156.
Dendropsophus parviceps– Faivovich et al. 2005: 93.
Diagnosis: Throughout the species account, coloration refers to preserved specimens unless otherwise noted. Dendropsophus parviceps is characterized by: (1) small size, mean SVL 16.4 mm in males (range 14.3–18.7; n = 65), 22.5 mm in females (range 20.3–24.4; n = 30); (2) throat sexually dimorphic, dark flecks posteriorly in males vs. white blotch with two or three longitudinal stripes or without stripes posteriorly in females (Fig. 8); (3) snout truncate in dorsal and lateral views, slightly inclined posteroventrally in lateral view; (4) nostrils slightly prominent; (5) tympanum visible, concealed posterodorsally, tympanic membrane differentiated and annulus evident; (6) conical tubercles on upper eyelid absent; (7) thoracic fold absent; (8) ulnar tubercles and outer tarsal tubercles indistinct; (9) axillary membrane present; (10) skin on dorsal surfaces smooth with scattered small tubercles; skin on chest areolate; skin on belly, posterior surfaces of thighs, and subcloacal area coarsely areolate; skin on throat and other surfaces smooth; (11) dark brown markings on dorsum (Fig. 8); (12) thenar tubercle is distinct; (13) hand webbing formula II11/2–2III2-–2-IV, feet webbing formula I1-−2-II1-−2-III1-–2IV2−1-V; (14) in life, dorsal surfaces brown, tan or grayish tan; (15) orange to amber blotch on the proximal ventral surface of shanks and under arms, from the axillae to near the elbow, in life (white to creamy white in preservative); (16) one suborbital white bar present both in life and preservative; (17) thighs are black to dark brown with two or three white spots on the anterodorsal surfaces both in life and preservative; (18) iris in life is creamy white to reddish brown with brow or dark brown reticulations.
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Distribution and ecology: Dendropsophus parviceps is known from 39 localities in the Ecuadorian Amazon basin (Napo, Orellana, Pastaza, Sucumbíos, and Tungurahua provinces; Fig. 9), few localities in the Peruvian Amazon basin at northwest Loreto (Andoas and San Jacinto; Fig. 9), the Colombian Amazon (Río Apaporis, Vaupés Department, and Ceilán, Caquetá Department; Cochran and Goin 1970; Fig. 9), and northern Brazil (“Taracuá” [= Taracuacá], Río Uaupés, Amazonas State; Melin 1941). Elevation range is 151 m (Andoas) to 1600 m above sea level (Río Verde). Our Colombian records are unverified and are based on Cochran and Goin (1970) who examined three specimens (MLS 54 and MCZ 28058–59) and explicitly mention the absence of tubercles on the upper eyelids. Moreover, the SVL for a gravid female from Ceilan (MLS 54, 21.8 mm) falls outside the known size range of D. kubricki sp. n. and D. kamagarini sp. n. (Table 3). Ecuadorian localities from Sucumbíos province are close to the Colombian border further suggesting the presence of D. parviceps in Colombia. In addition, there is an unconfirmed register of D. parviceps from Ramal do Purupuru, km 34 on the BR-319 highway (3.3535°S, 59.8557°W, 35 m, Amazonas State, Brazil; Fig. 9).
Dendropsophus parviceps inhabits Amazonian lower montane forest, Amazonian foothill forest, and Amazonian evergreen lowland rainforest (habitat types based on Ron et al. 2017). Dendropsophus parviceps is an opportunistic breeder and can be found in primary and secondary forest, temporary ponds, flooded areas, swamps, and artificial open areas. Calling activity starts at dusk (17–18h), but it is mainly nocturnal. According to Lynch (2005), D. parviceps is a canopy species that visits the lower forest strata for breeding.
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Figure 10. Dorsolateral and ventral views ofDendropsophus kamagarini sp. n. in life:
A, B Adult male, from La Habana, Tambopata, Peru (CORBIDI 5259) C, D Adult male, from Bahuaja, Puno, Peru (CORBIDI 13148) E–H Adult females, from Pagoreni norte, La Convención, Peru E, F not collected. Dorsolateral and ventral views of Dendropsophus kamagarini sp. n. in life: G, H (CORBIDI 10018) I, J Adult male, from Tahuamanu, Nicolás Suárez, Bolivia (11.4074°S, 69.0180°W, 260 m, not collected) K, L Adult male, from El Negro, Manuripi, Bolivia (12.3134°S, 68.6689°W, 187 m, not collected) N Adult male, from Rio Branco, Acre, Brazil (10.0387°S, 67.7957°W, 160 m, not collected) M Adult male, from Rio Madeira, Rondônia, Brazil (8.8482°S, 64.0689°W, 110 m, not collected). Photos A, B, E–H by V. Duran, C, D by P. J. Venegas I–L by A. Muñoz, N by P.R. Melo-Sampaio, and M by A.P. Lima. |
Dendropsophus kamagarini sp. n.
Etymology: The specific name kamagarini is a noun derived from the Matsigenka language, which means demon or devil (Snell et al. 2011). The Matsigenka language is spoken by the Matsigenka people who inhabit the highlands and lowlands of southeastern Peru, in the departments of Cusco and Madre de Dios. Judeo-Christian religions depict the demon as a human figure with horns. The species name is in allusion to the prominent horn-like tubercles on the upper eyelid of D. kamagarini.
Diagnosis: Throughout the species description, coloration refers to preserved specimens unless otherwise noted. The new species is assigned to the genus Dendropsophus based on our phylogenetic results (Fig. 1) and the overall similarity with D. parviceps and other species of the genus (Figs 10–11). Dendropsophus kamagarini is a medium-sized species, relative to other species in the D. parviceps group and is characterized by the following combination of traits: (1) size sexually dimorphic; mean SVL 19.9 mm in males (range 17.6–22.7; n = 35), 26.1 mm in females (range 24.0–28.1; n = 7); (2) throat brown mottled with white flecks posteriorly in males vs. white blotch with flecks or with stripes posteriorly in females (Fig. 11); (3) snout is short and truncate in dorsal and lateral views; (4) nostrils slightly protuberant; (5) tympanum visible, tympanic membrane non-differentiated, annulus distinct; (6) one prominent conical tubercle on the distal edge of the upper eyelid; (7) thoracic fold indistinct to barely evident; (8) ulnar tubercles and outer tarsal tubercles distinct; (9) axillary membrane present; (10) skin on dorsal surfaces smooth with scattered tubercles; skin on chest, belly, posterior surfaces of thighs, and subcloacal area coarsely areolate; skin on throat grooved with scattered tubercles; (11) dark brown markings on dorsum (Fig. 11); (12) thenar tubercle distinct; (13) hand webbing formula II1-–2+III1-–1-IV, feet webbing formula I11/2–2+II1-–1III1-–2-IV2–1V; (14) in life, dorsum tan, brown or reddish brown; (15) orange to amber blotch on the proximal ventral surface of shanks and under arms, from the axillae to near the elbow, in life (white to creamy white in preserved); (16) one suborbital white bar present both in life and preserved; (17) thighs black to dark brown with two or three spots on the anterodorsal surfaces both in life and preserved; (18) iris in life creamy white with brown to reddish brown reticulations and a cream ring around pupil.
Distribution and ecology: Dendropsophus kamagarini occurs in the Amazon basin of southeastern Peru (Cusco and Madre de Dios regions; Fig. 9), northwestern Brazil (Acre and Rondônia states; Fig. 9), and northeastern Bolivia, from the Andean slopes to lowland tropical rainforest (Fig. 9). Localities with known elevation range from 150 m (Acre) to 1696 m (Ochigoteni) above sea level.
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Figure 13. Dorsolateral and ventral views of Dendropsophus kubricki sp. n. in life:
A, B Holotype, adult male, from Río Tapiche, Requena, Peru (CORBIDI 15778) C, D Adult male from Río Tapiche, Requena, Peru (CORBIDI 15782) E Adult male from Jenaro Herrera, Requena, Peru (not collected) F Adults, pair in amplexus from Jenaro Herrera, Requena, Peru (not collected).Dorsolateral and ventral views of Dendropsophus kubricki sp. n. in life: G, H Adult female from Jenaro Herrera, Requena, Peru (not collected) I, J Adult female from Area de Conservación Municipal Chambira, Picota, Peru (CORBIDI 8864) K Adult female from Tarapoto, San Martín, Peru (6.4306°S, 76.2903°W, 600 m, not collected) L Adults, pair in amplexus from Area de Conservación Municipal Chambira, Picota, Peru (CORBIDI 8864–63). Photographs by P. J. Venegas. |
Dendropsophus kubricki sp. n.
Etymology: The specific name kubricki is a noun in the genitive case and is a patronym for Stanley Kubrick, an American filmmaker who is one of the most brilliant and influential film directors of all time. We dedicate this species to him for his legacy to film culture and science fiction.
Diagnosis: Throughout the species description, coloration refers to preserved specimens unless otherwise noted. The new species is assigned to the genus Dendropsophus based on our phylogenetic results (Fig. 1) and the overall similarity with D. parviceps and other species of the genus (Figs 13–14). Dendropsophus kubricki is a medium-sized species, relative to other species in the D. parviceps group and is characterized by the following combination of traits: (1) size sexually dimorphic; mean SVL 19.4 mm in males (range 18.3–20.1; n = 14), 26.0 mm in females (range 22.0–28.4; n = 8); (2) throat with white flecks posteriorly in males and white blotch with stripes posteriorly in females (Fig. 14); (3) snout truncate in dorsal view, rounded and inclined posteroventrally in lateral view; (4) nostrils slightly prominent; (5) tympanum distinct, rounded, concealed posterodorsally, tympanic membrane non-differentiated and annulus evident; (6) low tubercles on upper eyelid can be distinct or ill-defined; (7) thoracic fold slightly evident or indistinct; (8) ulnar tubercles and outer tarsal tubercles low; (9) axillary membrane present; (10) skin on dorsal surfaces smooth with scattered tubercles mainly on head; skin on throat areolate, skin on chest, belly, posterior surfaces of thighs, and subcloacal area coarsely areolate; (11) dark brown markings on dorsum consisting of chevrons and transverse blotches in variable arrangements (Fig. 14); (12) thenar tubercle distinct; (13) hand webbing formula II1-−2+III1-−1-IV, foot webbing formula I1-−2-II1-−2-III1-–2IV2−1-V; (14) in life, dorsal surfaces reddish brown, brown, or grayish tan; (15) orange to amber blotch on the proximal ventral surface of shanks and under arms, from the axillae to near elbow, in life (white to creamy white in preserved); (16) one suborbital white bar present both in life and preserved; (17) anterodorsal surfaces of thighs are black to dark brown with two or three white spots, both in life and preserved; (18) iris in life is reddish brown, brown or silver gray.
Distribution and ecology: Dendropsophus kubricki is distributed in the Amazon basin in northeastern and central Peru (Fig. 9), at elevations between 106 (Jenaro Herrera) and 725 m (Cordillera Azul). Dendropsophus kubricki was found in flooded forest. Specimens from Chambira were collected in a small pond in a Terra Firme forest. Males call at night while perching on leaves of bushes and trees. They were observed between 0.3 and 0.4 m above the water.
C. Daniel Rivadeneira, Pablo J. Venegas and Santiago R. Ron. 2018. Species Limits within the Widespread Amazonian treefrog
Dendropsophus parviceps with Descriptions of Two New Species (Anura, Hylidae).
ZooKeys. 726; 25-77. DOI:
10.3897/zookeys.726.13864
