Research Article |
Corresponding author: Jiří Moravec ( jiri.moravec@nm.cz ) Academic editor: Angelica Crottini
© 2020 Jiří Moravec, Edgar Lehr, Karel Kodejš.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Moravec J, Lehr E, Kodejš K (2020) A new species of Pristimantis (Amphibia, Anura, Strabomantidae) from the Pui Pui Protected Forest (central Peru), with comments on Pristimantis albertus Duellman & Hedges, 2007. ZooKeys 994: 125-148. https://doi.org/10.3897/zookeys.994.56277
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We describe a new Pristimantis species from the eastern Andes, Región Junín, Peru following an integrative taxonomic approach. The description is based on three adult males (snout-vent length 25.7–28.8 mm) collected in two montane forests between 1615 and 1800 m a.s.l. in the Pui Pui Protected Forest and its close surroundings. The new species is mainly characterised by absence of tympanum, presence of inner tarsal fold, broad horizontal red band across iris, ventre mottled black and cream and ventral surfaces of thighs salmon and grey mottled. Amongst the Amazonian and montane forest Pristimantis that have the ventre and groin contrastingly black and cream mottled, P. sinschi sp. nov. is morphologically most similar to P. lindae and P. ventrimarmoratus. However, DNA barcoding revealed a clear distinction between these three species and placed P. sinschi sp. nov. as sister taxon of P. lindae. We designate a lectotype for P. ventrimarmoratus and restrict the type locality of this species to “El Topo, R. Pastaza, [Provincia Tungurahua,] E. Ecuador, 4200 feet”. Pristimantis albertus and P. sagittulus are recorded for the first time in the Región Junín. Additional data on morphology and systematics are provided for P. albertus.
Andes, anuran diversity, montane rainforests, Pristimantis sinschi sp. nov., P. sagittulus, P. ventrimarmoratus
Faunal and taxonomic research provides the essential foundation and objectives for the effective conservation of biological diversity. The Pui Pui Protected Forest (PPPF) located in the eastern Andes of Peru (Provincias Chanchamayo, Jauja, Concepción and Satipo, Región Junín; Fig.
Herein, we describe a new species of Pristimantis Jiménez de la Espada, 1870 which phenotypically resembles P. diadematus (Jiménez de la Espada, 1875); P. divnae Lehr and von May, 2009; P. eurydactylus (Hedges & Schlüter, 1992); P. lindae (Duellman, 1978); P. orcus Lehr, Catenazzi & Rodríguez, 2009; and P. ventrimarmoratus (Boulenger, 1912). Furthermore, we provide the first records for Pristimantis albertus Duellman & Hedges, 2007 and P. sagittulus (Lehr, Duellman & Aguilar, 2004) for the Región Junín and additional data on systematics and morphology for P. albertus.
The format for the description follows
Comparisons of congeners focused on phenotypically-similar species from Ecuador and Peru and those with close phylogenetic relationships as recovered in our trees. Information on species for comparative diagnoses was obtained from
Proceeding from our previous study (
Names of taxa, museum numbers, field data and GenBank accession numbers of newly-genetically investigated material. For other abbreviations, see text. PPPF = Pui Pui Protected Forest.
Species | Museum number | Locality | Coordinates | Elevation (m) | Collectors; year | GenBank Accession number | |
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16S | 12S | ||||||
P. sinschi sp. nov. (holotype) |
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PPPF, Peru | 11°12'38.5"S, 74°57'28.9"W | 1800 | E. Lehr, J. Moravec; 2014 | MW075408 | MW075426 |
P. sinschi sp. nov. |
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PPPF, Peru | 11°12'38.5"S, 74°57'28.9"W | 1615 | E. Lehr, J. Moravec; 2014 | MW075407 | MW075425 |
P. albertus |
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PPPF, Peru | 11°07'37.2"S, 75°10'37.0"W | 1970 | E. Lehr, J. Moravec, J.C. Cusi, R. von May; 2013 | MW075393 | MW075414 |
P. albertus |
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PPPF, Peru | 11°07'37.2"S, 75°10'37.0"W | 1970 | E. Lehr, J. Moravec, J.C. Cusi, R. von May; 2013 | MW075394 | MW075415 |
P. cf. stictogaster |
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PPPF, Peru | 11°12'38.5"S, 74°57'28.9"W | 1700 | E. Lehr, J. Moravec; 2014 | MW075395 | MW075417 |
P. cf. stictogaster |
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PPPF, Peru | 11°12'38.5"S, 74°57'28.9"W | 1750 | E. Lehr, J. Moravec; 2014 | MW075396 | MW075419 |
P. cf. stictogaster |
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PPPF, Peru | 11°15'16.1"S, 74°53'30.7"W | 1615 | E. Lehr, R. von May; 2012 | – | MW075416 |
P. cf. stictogaster |
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PPPF, Peru | 11°15'16.1"S, 74°53'30.7"W | 1615 | E. Lehr, R. von May; 2012 | – | MW075418 |
P. cf. malkini |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2001 | MW075401 | MW075423 |
P. cf. malkini |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2001 | MW075399 | – |
P. cf. malkini |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2001 | MW075397 | – |
P. cf. malkini |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2001 | MW075402 | – |
P. cf. malkini |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2002 | MW075400 | MW075424 |
P. cf. malkini |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2002 | MW075398 | – |
P. diadematus |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2001 | MW075409 | MW075420 |
P. cf. lanthanites |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2001 | MW075405 | MW075421 |
P. cf. lanthanites |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2001 | MW075403 | – |
P. cf. lanthanites |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2001 | MW075404 | – |
P. cf. lanthanites |
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Tarapoto, Peru | 03°48'17"S, 73°24'19"W | 95 | J. Moravec; 2001 | MW075406 | – |
P. cf. olivaceus |
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Palmira, Bolivia | 10°35'S, 65°44'W | 150 | J. Moravec; 2007 | MW075410 | MW075422 |
P. reichlei |
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San Antonio, Bolivia | 11°29'S, 68°52'W | 250 | J. Moravec; 2007 | MW075411 | MW075427 |
P. reichlei |
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San Antonio, Bolivia | 11°29'S, 68°52'W | 250 | J. Moravec; 2007 | MW075413 | – |
P. reichlei |
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San Antonio, Bolivia | 11°29'S, 68°52'W | 250 | J. Moravec; 2007 | MW075412 | – |
The Bayesian phylogenetic tree of selected South American Pristimantis; for taxon sampling design, see Material and Methods. Nodes with less than 50% of the post burn-in tree samples were collapsed. Posterior probability values (pp) given only for main lineages. The new species, P. sinschi sp. nov., is a member of a monophyletic clade, yet unnamed species Group, comprising species from Peruvian Cordillera Oriental – P. lindae and P. rhabdocnemus. The PPPF representatives of P. danae species Group form two distinct genetic lineages, one conspecific with P. albertus and the second closer to P. stictogaster (labelled as P. cf. stictogaster). Species-group names follow
Genomic DNA was extracted from tissues stored in 96% ethanol. A fragment of the mitochondrial gene for 16S rRNA (16S), which is commonly used in the amphibian DNA barcoding (
In the case of Pristimantis ventrimarmoratus, only the 12S sequence was available in the GenBank database. Therefore, for the purpose of comparison, a fragment of 12S rRNA (12S) was sequenced for the holotype of the new species and 13 other selected specimens (Table
The Bayesian Inference (BI) was applied to construct a phylogenetic tree. First, the software PartitionFinder 2.1.1, using the PhyML algorithm (
The obtained phylogenetic tree (Fig.
Mean uncorrected genetic p-distance values of 16S rRNA barcode for species from the clade containing Pristimantis sinschi sp. nov. and for P. albertus–P. stictogaster clade within P. danae species Group.
Species | 1 | 2 | 3 | 4 | 5 | 6 | 7 | |
---|---|---|---|---|---|---|---|---|
1 | P. sinschi sp. nov. | 0.0000 | ||||||
2 | P. lindae | 0.0402 | 0.0000 | |||||
3 | P. rhabdocnemus | 0.0535 | 0.0713 | 0.0136 | ||||
4 | P. albertus GeneBank | 0.1721 | 0.1691 | 0.1808 | 0.0000 | |||
5 | P. albertus this study | 0.1721 | 0.1692 | 0.1809 | 0.0067 | 0.0000 | ||
6 | P. stictogaster | 0.1611 | 0.1514 | 0.1720 | 0.0468 | 0.0497 | 0.0000 | |
7 | P. cf. stictogaster | 0.1585 | 0.1571 | 0.1745 | 0.0444 | 0.0472 | 0.0283 | 0.0023 |
Morphologically-similar species P. ventrimarmoratus (individuals from Ecuador, GenBank accession numbers: JF906310.1, JF906311.1 and JF906312.1) clusters within the species-rich clade comprising species from the Andes and the Guiana Shield, as well as lowland species from the intervening Amazon, with P. altamazonicus (Barbour & Dunn, 1921) and P. brevicrus (Andersson, 1945) as closest relatives (recently revalidated P. brevicrus, see
The PPPF Pristimantis individuals, morphologically resembling P. albertus, belong to two separate lineages within the P. danae species Group. Specimens
Hylodes ventrimarmoratus Boulenger, 1912
(hoc loco): BMNH 1947.2.15.74
BMNH 1947.2.15.75 and BMNH 1947.2.15.76
“El Topo, R. Pastaza, [Provincia Tungurahua,] E. Ecuador, 4200 feet”
The fourth original syntype BMNH 1947.2.15.73 may be conspecific with Pristimantis sinschi sp. nov. but its accurate determination remains open.
Eleutherodactylus ventrivittatus Andersson, 1945; Type locality: “Ambitagua [= Abitagua], Rio Pastaza”, Provincia Tungurahua or Pastaza, Ecuador (according to
Pristimantis
sp. A –
Pristimantis
sp. nov. –
Two adult males:
We assign this species to Pristimantis, based on our molecular data (Fig.
A new species of Pristimantis not assigned to any species group having the following combination of characters: (1) Skin on dorsum shagreen with many small subconical tubercles and a narrow, hairline mid-dorsal fold, skin on ventre areolate; discoidal and thoracic folds present; dorsolateral folds absent; (2) tympanic membrane and tympanic annulus absent; (3) snout short, rounded in dorsal and lateral views; (4) upper eyelid without enlarged tubercles; EW slightly shorter than IOD; cranial crests absent; (5) dentigerous processes of vomers present; (6) males without vocal slits; nuptial pads absent; (7) Finger I shorter than Finger II; discs of digits broadly expanded, elliptical; (8) fingers with lateral fringes; (9) small conical ulnar and tarsal tubercles present; (10) heel without conical tubercles; short inner tarsal fold present; (11) inner metatarsal tubercle ovoid, 3 times as large as outer; outer metatarsal tubercle small, ovoid; low, numerous supernumerary plantar tubercles; (12) toes with lateral fringes; basal toe webbing absent; Toe V longer than Toe III; toe discs slightly smaller than those on fingers; (13) in life, dorsal ground colouration greenish-grey, reddish-brown or brown with or without a hairline mid-dorsal tan stripe; canthal stripe absent, supratympanic stripe greyish-brown; groin black with cream blotches, anterior surfaces of thighs and ventral surface of shanks black; ventral surfaces of thighs salmon and grey mottled; ventre black and cream mottled; iris pale bronze with fine black vermiculation and broad median red band through pupil and a narrow black vertical streak from pupil across lower half of iris; (14) SVL in adult males 25.7–28.8 mm (n = 3), females unknown.
Phylogenetically, Pristimantis sinschi and P. lindae from southern Peru (Región Cusco) are sister taxa. Both species have the dorsum shagreen with subconical tubercles, ventre areolate, dorsolateral folds absent, dentigerous processes of vomers, finger and toe discs expanded, fingers and toes with lateral fringes, tarsal folds, males with vocal slits and groin and ventre cream with black reticulations. However (characters for P. sinschi in parenthesis), P. lindae has a tympanum (absent), the single known male
Pristimantis sinschi is morphologically similar to five other Pristimantis (P. diadematus, P. divnae, P. eurydactylus, P. orcus and P. ventrimarmoratus) from the Amazonian lowlands and lower montane forests which have the ventre and groin contrastingly patterned in black and cream and an inner tarsal fold. However, P. sinschi is readily distinguished from its congeners (except for P. ventrimarmoratus) by lacking a tympanum and having the ventral surfaces of thighs orange brown and grey mottled. Characters for P. sinschi are in parenthesis in the following. Furthermore, P. diadematus has the ventral skin smooth (areolate), males with vocal slits (absent) and nuptial pads (absent) and the iris greenish-bronze with a median horizontal red streak or reddish-copper (pale bronze with fine black vermiculation and broad median horizontal red band) (
Head slightly narrower than body, slightly wider than long; head length 42% of SVL; head width 44% of SVL; cranial crests absent; snout moderately long, rounded in dorsal and lateral views (Fig.
Skin on dorsum and flanks shagreen with many small conical tubercles, dorsolateral folds absent, a narrow, hairline mid-dorsal fold present from snout towards cloacal sheath; skin on throat, chest and belly areolate; discoidal and thoracic folds present, weakly defined; cloacal sheath short.
Outer ulnar surface with four (left side) and three (right side) minute low tubercles; palmar tubercle partially divided distally; thenar tubercle ovoid; subarticular tubercles well defined, round in ventral view, conical in lateral view; supernumerary tubercles distinct, ovoid, subconical, approximately half the size of subarticular tubercles; fingers with narrow lateral fringes, much broader at base of fingers; Finger I shorter than Finger II; discs on digits of fingers broadly expanded (about 1.5 times width of digit proximal to disc), elliptical (Fig.
Hind limbs long, slender, tibia length 54% of SVL; foot length 51% of SVL; upper surfaces of hind limbs shagreen with many subconical tubercles; inner surface of thighs smooth, posterior and ventral surfaces of thighs areolate; heels without enlarged conical tubercles; outer surface of tarsus with scattered minute low tubercles; inner tarsal fold present, short and narrow, most distinct at its anterior third; inner metatarsal tubercle prominent, ovoid, three times the size of ovoid outer metatarsal tubercle; subarticular tubercles well defined, round in ventral view, conical in lateral view; plantar supernumerary tubercles distinct, about half the size of subarticular tubercles; toes with narrow lateral fringes; basal webbing absent; discs broadly expanded, elliptical, less expanded than those on fingers; relative length of toes: 1 < 2 < 3 < 5 < 4; disc on Toe III reaching distal subarticular tubercle on Toe IV, disc on Toe V extends distal subarticular tubercle on Toe IV (Fig.
In life (Fig.
In alcohol, general colouration pattern is as described for the holotype in life, except for brown which is pale brown, black which is dark brown, salmon which is cream and pale grey which is brown. Iris is pale grey.
Holotype measurements (in mm): SVL 25.7; TL 13.9; FL 13.0, HL 10.7; HW 11.2; ED 3.9; IOD 3.5; EW 3.0; IND 2.3; E-N 2.8.
All paratypes are similar to the holotype regarding morphology (see Table
Measurements (in mm) of male type specimens of Pristimantis sinschi sp. nov. For abbreviations, see Material and methods.
Character |
|
|
|
Ranges followed by means and SD in parenthesis |
---|---|---|---|---|
SVL | 25.7 | 25.8 | 28.8 | 25.7–28.8 (26.8 ± 1.8) |
TL | 13.9 | 14.2 | 15.6 | 13.9–15.6 (14.6 ± 0.9) |
FL | 13.0 | 13.0 | 14.6 | 13.0–14.6 (13.5 ± 0.9) |
HL | 10.7 | 10.7 | 11.5 | 10.7–11.5 (11.0 ± 0.5) |
HW | 11.2 | 11.4 | 11.8 | 11.2–11.8 (11.5 ± 0.3) |
ED | 3.9 | 3.5 | 3.8 | 3.5–3.9 (3.7 ± 0.2) |
IOD | 3.5 | 3.0 | 3.2 | 3.0–3.5 (3.2 ± 0.3) |
EW | 3.0 | 2.4 | 2.8 | 2.4–3.0 (3.1 ± 0.7) |
IND | 2.3 | 2.3 | 2.4 | 2.3–2.4 (2.3 ± 0.1) |
N–E | 2.8 | 2.6 | 2.8 | 2.6–2.8 (2.7 ± 0.1) |
Pristimantis sinschi is known from two localities in montane forest of the Pui Pui Protected Forest and its close surroundings in the eastern Andes between 1615 and 1800 m a.s.l. in the Región Junín (Figs
We dedicate this species to our colleague and friend Prof. Dr. Ulrich Sinsch in recognition of his important contributions to the South American and African herpetology. The specific epithet is used as a noun in apposition.
Collecting sites in montane forests of Pristimantis sinschi sp. nov. Type locality (A, B) in the close surrounding of the Pui Pui Protected Forest at 1800 m a.s.l. Second known locality (C) at the entrance of the Pui Pui Protected Forest at 1615 m a.s.l. Photos by J. Moravec (A, B) and E. Lehr (C).
Five males:
In general, the newly-collected and genetically-determined individuals of Pristimantis albertus correspond to the description of the type specimens. However, they differ in the following features: (1) discoidal fold is present, weakly defined (discoidal fold absent, according to
(Table
Measurements (in mm) of Pristimantis albertus. For abbreviations, see Material and methods.
Character |
|
|
|
|
|
|
|
|
---|---|---|---|---|---|---|---|---|
SEX | M | M | M | M | M | F | F | F |
SVL | 15.5 | 13.4 | 19.5 | 13.7 | 12.9 | 24.2 | 14.3 | 14.6 |
TL | 8.6 | 7.3 | 9.0 | 7.6 | 7.0 | 12.3 | 7.8 | 8.0 |
FL | 6.5 | 5.6 | 8.1 | 6.2 | 5.6 | 10.2 | 6.0 | 6.1 |
HL | 6.1 | 6.0 | 7.7 | 6.1 | 5.5 | 9.6 | 5.7 | 6.3 |
HW | 5.9 | 5.3 | 7.4 | 5.5 | 5.1 | 9.1 | 5.4 | 5.6 |
ED | 2.1 | 1.7 | 2.2 | 1.7 | 1.8 | 2.5 | 1.9 | 1.8 |
TY | 0.7 | 0.6 | 0.9 | 0.7 | 0.6 | 1.2 | 0.6 | 0.6 |
IOD | 1.9 | 2.1 | 2.3 | 1.8 | 1.8 | 2.8 | 1.8 | 2.0 |
EW | 1.2 | 1.2 | 1.7 | 1.3 | 1.0 | 1.6 | 1.0 | 1.1 |
IND | 1.9 | 1.8 | 2.3 | 1.9 | 1.7 | 2.9 | 1.9 | 1.8 |
(Fig.
Our record of Pristimantis albertus from the PPPF lies ca. 65 km straight SE of the species type locality and represents the first record of this species for the Region Junín (Fig.
One male:
Our record of Pristimantis sagittulus from the PPPF lies ca. 65 km straight SE of the species type locality (
Pristimantis aniptopalmatus (1): Peru, Junín, buffer zone of the Pui Pui Protected Forest, 1970 m a.s.l.,
Pristimantis ashaninka (5): Peru, Junín: border of the Pui Pui Protected Forest, 1700 m a.s.l.,
Pristimantis bipunctatus (1): Peru, Junín, buffer zone of the Pui Pui Protected Forest, 1970 m a.s.l.,
Pristimantis lindae (3): Peru, Cusco: Alto Shima, 1785 m a.s.l.,
With the description of Pristimantis sinschi, the number of species in this genus known from Peru rises to 140 (
The description of Pristimantis albertus was based on two adult females obtained by Hedges in 1987 from Rio San Alberto, 2.1 km E of Oxapampa (Provincia Pasco, Peru) at 1970 m a.s.l. (
With a long, acuminate snout and a broad, longitudinal, red stripe on the posterior surfaces of the thighs, Pristimantis sagittulus can easily be distinguished from all its congeners. Previously, the species was only known from its type locality at San Alberto, the Yanachaga-Chemillén National Park and adjacent localities at elevations of 1970–2479 m a.s.l. in the Region Pasco (
We are indebted to S. Ron, P. Székely and one anonymous reviewer for their valuable comments on this manuscript. For loan of material, we thank J. Córdova and C. Aguilar (