Research Article |
Corresponding author: Santiago R. Ron ( santiago.r.ron@gmail.com ) Academic editor: Alexander Haas
© 2021 Julio C. Carrión-Olmedo, Santiago R. Ron.
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:
Carrión-Olmedo JC, Ron SR (2021) A new species of the Pristimantis lacrimosus group (Anura, Strabomantidae) from the eastern slopes of the Ecuadorian Andes. Evolutionary Systematics 5: 151-175. https://doi.org/10.3897/evolsyst.5.62661
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With 566 species, the neotropical genus Pristimantis is the most speciose vertebrate genus. As a result of its striking diversity, taxonomic reviews remain a challenge. Herein, we present an updated phylogeny of the Pristimantis lacrimosus group and describe a new species from Llanganates and Sangay National Parks. We also report, for the first time, the phylogenetic position of Pristimantis degener, P. eugeniae, P. katoptroides, and P. petersi. Based on our phylogeny, we add two species to the Pristimantis lacrimosus group. Through the integration of molecular and bioacoustic evidence, we describe a new species which was hidden under “Pristimantis petersi”. Pristimantis petersioides sp. nov. is most closely related to Pristimantis petersi and an undescribed species from Peru. It can be distinguished from P. petersi by its advertisement call and large genetic differences (uncorrected p-genetic distances 7.9% to 8.4% for gene 16S). Moreover, the new species and P. petersi are not sister species. We suggest assigning the new species to the Endangered Red List category because it has a small distribution range with deforestation as result of agriculture and other anthropogenic influences.
Amphibia, Bioacoustics, Conservation, Diversity, National Parks, Phylogeny, Taxonomy
The genus Pristimantis Jiménez de la Espada, 1870 has bewildered scientists for its striking diversity. Comprising 566 Neotropical species it is the most speciose vertebrate genus (
The astounding species richness of Pristimantis has been attributed to terrestrial breeding – direct embryonic development without a tadpole stage (
The number of described species of Pristimantis is increasing rapidly as result of the use of DNA sequences allowing the discovery of a large number of cryptic species. DNA sequences helps to achieve better informed taxonomic decisions and speed up species discovery with more than 40 species of Pristimantis (e.g. Ortega et al. 2015;
Taxonomy within this group have been problematic and unstable because most species descriptions have been based on morphological traits (
One clade of Pristimantis containing undescribed species is the Pristimantis lacrimosus species group (
Despite these advances, there still are species of the Pristimantis lacrimosus group which have never been included in molecular phylogenies. One of them is Pristimantis petersi (Lynch & Duellman, 1980). Since its description, this species suffered several taxonomic changes.
Pristimantis petersi has been usually assigned to the P. lacrimosus species group.
Pristimantis petersi holotype (KU 143508) is from 16.5 km NNE of Santa Rosa, Napo Province, 1700 m. However, most specimens used in the species description by
The wide geographic distribution of Pristimantis petersi suggest that it may be a species complex. Recent reviews of Andean Pristimantis suggest that most species have highly restricted distributions. For example, in the subgenus Huicundomantis Páez & Ron, 2019 all species had distribution ranges below 5000 km2 and the seemingly large distribution of “P. phoxocephalus” and “P. riveti” were an artifact of the combined distribution of several cryptic species (
The existence of cryptic diversity within P. petersi is also suggested by reports of body size differences among populations of P. petersi (
Taxon names follow
We inferred the phylogenetic relationships of the new species and closely related taxa based on DNA sequences of one nuclear gene: Recombination activating gene 1 (RAG-1) and three mitochondrial genes: 12S rRNA (12S), 16S rRNA (16S), NADH dehydrogenase subunit 1 (ND1) and their flanking tRNAs. DNA was extracted from muscle or liver tissue preserved in 95% ethanol using standard Guanidine thiocyanate extraction protocols. We used polymerase chain reaction (PCR) to amplify DNA fragments. Primers used for amplification of 12S were t-Phe-frog and t-Val-frog (
We included 156 GenBank sequences of congeneric species. To find relevant sequences in GenBank, we made a 16S BLASTn search with the sequences of the new species (Table
Genbank accession numbers for DNA sequences used for phylogenetic analyses.
Species | Voucher | 12S | 16S | RAG1 | ND1 |
---|---|---|---|---|---|
Niceforonia elassodisca | QCAZ52495 | MW567328 | MW567375 | MW451754 | MW567403 |
Niceforonia nigrovittata | QCAZ59410 | NA | MW567340 | NA | NA |
Pristimantis acerus | KU 217786 | EF493678.1 | EF493678.1 | NA | NA |
P. actites | KU 217830 | NA | EF493696.1 | EF493432.1 | NA |
P. acuminatus | CORBIDI 4769 | MN128391 | NA | NA | NA |
QCAZ53263 | MN128394 | NA | NA | NA | |
CORBIDI 7469 | MN128392 | NA | NA | NA | |
CORBIDI 7579 | MN128393 | NA | NA | NA | |
P. aff. subsigillatus | QCAZ58017 | MW567302 | MW567373 | MW451755 | MW567411 |
P. altamazonicus | KU 215460 | EF493670.1 | EF493670.1 | NA | NA |
P. amaguanae | QCAZ39274 | MT636506 | MT636529 | MT635622 | MT635661 |
P. andinognomus | QCAZ16683 | NA | MW567356 | MW451748 | MW567390 |
P. angustilineatus | UVC 15828 | NA | JN371034.1 | NA | NA |
P. appendiculatus | KU177637 | EF493524.1 | EF493524.1 | NA | NA |
P. aureolineatus | QCAZ42286 | MT636509 | MT636530 | MT635626 | NA |
P. bambu | QCAZ46708 | NA | MW567357 | MW451727 | NA |
P. boulengeri | MHUAA 8951 | NA | KU724435.1 | NA | NA |
P. brevifrons | nrps 0059 | JN991498.1 | JN991433.1 | NA | NA |
P. bromeliaceus | QCAZ16699 | MT636505 | MT636527 | MT635618 | MT635659 |
QCAZ62940 | MT636512 | MT636523 | NA | MT635669 | |
P. calcarulatus | KU 177658 | EF493523.1 | EF493523.1 | NA | NA |
P. cedros | MZUTI 1713 | NA | KT210155.1 | NA | NA |
P. celator | QCAZ66230 | MW567326 | MW567368 | MW451723 | MW567406 |
P. cf. mendax | MTD 45080 | EU186659.1 | EU186659.1 | NA | NA |
P. conspicillatus | QCAZ28448 | MW567327 | MW567377 | MW451749 | NA |
QCAZ55439 | NA | MW567358 | MW451746 | MW567394 | |
P. crucifer | KU 177733 | EU186736.1 | EU186718.1 | NA | NA |
P. curtipes | QCAZ40722 | MW567323 | MW567363 | MW451750 | MW567416 |
P. degener | QCAZ40304 | MW567305 | MW567376 | MW451761 | MW567379 |
P. diadematus | KU 221999 | EU186668.1 | EU186668.1 | NA | NA |
QCAZ59442 | MW567325 | MW567354 | MW451735 | MW567419 | |
P. dissimulatus | KU179090 | EF493522.1 | EF493522.1 | NA | NA |
P. dorsopictus | MHUAA7638 | KP082864.1 | KP082874.1 | NA | NA |
P. ecuadorensis | CJ 5350 | KX785339 | KX785343 | NA | KX785347 |
CJ 5351 | KX785340 | KX785344 | NA | KX785348 | |
P. enigmaticus | QCAZ40918 | MT636513 | MT636520 | MT635636 | MT635670 |
P. eremitus | QCAZ40002 | NA | NA | MW451729 | MW567391 |
QCAZ49652 | NA | MW567366 | MW451732 | MW567409 | |
QCAZ43392 | NA | MW567333 | NA | NA | |
P. eugeniae | DHMECN8809 | MT853052 | MT853039 | NA | NA |
QCAZ52367 | MW567322 | MW567353 | MW451743 | MW567380 | |
P. galdi | QCAZ32368 | EU186670.1 | EU186670.1 | EU186746 | NA |
QCAZ58885 | MW567304 | MW567355 | MW451756 | MW567410 | |
QCAZ58886 | NA | MW567334 | MW451757 | NA | |
QCAZ58888 | NA | MW567335 | MW451739 | NA | |
P. glandulosus | KU 218002 | EF493676.1 | EF493676.1 | NA | NA |
P. imitatrix | KU 215476 | EF493824.1 | EF493667.1 | NA | NA |
P. inusitatus | KU 218015 | EF493677.1 | NA | NA | NA |
P. jaguensis | MHUAA 7249 | KP082862.1 | KP082870.1 | NA | NA |
P. katoptroides | QCAZ46360 | NA | MW567378 | MW451753 | MW567408 |
QCAZ58897 | NA | MW567330 | NA | NA | |
P. lacrimosus | QCAZ55238 | NA | MT636518 | MT635629 | MT635667 |
QCAZ59474 | NA | MT636517 | MT635633 | NA | |
QCAZ40261 | NA | MT636524 | MT635623 | MT635671 | |
QCAZ59469 | NA | MT636516 | MT635632 | NA | |
P. limoncochensis | QCAZ43794 | NA | MT636525 | MT635627 | MT635665 |
QCAZ52987 | MN128397 | NA | NA | NA | |
QCAZ56316 | MN128398 | NA | NA | NA | |
QCAZ37277 | MN128396 | NA | NA | NA | |
QCAZ19180 | MN128395 | MT636532 | MT635620 | NA | |
P. lymani | QCAZ46311 | NA | MW567365 | MW451752 | NA |
P. melanogaster | NA | EF493826.1 | EF493664.1 | NA | NA |
P. mindo | MZUTI 1382 | NA | KF801584.1 | NA | NA |
MZUTI 1381 | NA | KF801583.1 | NA | NA | |
QCAZ56512 | NA | MT636522 | MT635630 | MT635668 | |
MZUTI 1756 | NA | KF801581.1 | NA | NA | |
QCAZ42197 | MT636508 | MT636531 | MT635625 | MT635664 | |
P. moro | AJC 1860 | JN991520.1 | JN991454.1 | JQ025191.1 | NA |
AJC 1753 | JN991519.1 | JN991453.1 | JQ025192.1 | NA | |
P. muranunka | QCAZ54593 | NA | MW567358 | MW451762 | MW567393 |
P. nankints | QCAZ69137 | NA | MT636514 | MT635635 | NA |
P. nyctophylax | KU 177812 | EF493526.1 | EF493526.1 | NA | NA |
QCAZ32288 | NA | MT636519 | MT635621 | MT635660 | |
KU 218147 | EF493525.1 | EF493525.1 | NA | NA | |
QCAZ49637 | NA | MT636521 | MT635628 | MT635666 | |
P. olivaceus | CORBIDI 17473 | NA | KX155579 | NA | NA |
P. omeviridis | QCAZ55392 | MN128401 | NA | NA | NA |
FHGO 7192 | MN128399 | NA | NA | NA | |
QCAZ10564 | MN128400 | MK881398 | MK881312 | MT635658 | |
QCAZ19664 | NA | EU13057 | MT635619 | NA | |
P. orcesi | KU 218021 | EF493679.1 | EF493679.1 | NA | NA |
P. ornatissimus | MZUTI 4798 | KU720464 | KU720463 | NA | KU720480 |
MZUTI 4806 | KX785337 | KX785341 | NA | KX785345 | |
MZUTI 4807 | KX785338 | KX785342 | NA | KX785346 | |
P. pahuma | MZUTI 493 | NA | KT210158.1 | NA | NA |
P. petersi | QCAZ63455 | MW567303 | MW567369 | MW451725 | MW567405 |
QCAZ51390 | NA | MZ219640 | MZ219636 | MZ219631 | |
QCAZ15988 | NA | MZ219641 | MZ219635 | MZ219633 | |
QCAZ63456 | NA | MW567367 | MW451726 | MW567404 | |
P. petersioides sp. nov. | QCAZ58936 | NA | MW567331 | MW451740 | MW567401 |
QCAZ58937 | MW567306 | MW567336 | MW451758 | MW567381 | |
QCAZ58951 | MW567321 | MW567339 | MW451741 | MW567389 | |
QCAZ58939 | MW567307 | MW567337 | MW451759 | MW567386 | |
QCAZ59167 | MW567309 | MW567332 | MW451763 | MW567387 | |
QCAZ58944 | MW567308 | MW567338 | MW451760 | MW567395 | |
QCAZ59456 | MW567312 | MW567352 | MW451744 | MW567388 | |
QCAZ59466 | MW567314 | MW567343 | MW451745 | MW567383 | |
QCAZ59472 | MW567317 | MW567347 | MW451719 | MW567382 | |
QCAZ59479 | MW567318 | MW567348 | MW451724 | MW567384 | |
QCAZ59625 | MW567319 | MW567349 | MW451720 | MW567385 | |
QCAZ59470 | MW567316 | MW567345 | MW451737 | MW567397 | |
QCAZ59471 | MW567311 | MW567346 | MW451738 | MW567420 | |
QCAZ59468 | MW567315 | MW567344 | MW451742 | MW567402 | |
QCAZ59458 | MW567310 | MW567341 | MW451736 | MW567395 | |
QCAZ59461 | MW567313 | MW567342 | MW451718 | MW567398 | |
QCAZ49027 | NA | MZ219642 | MZ219638 | MZ219634 | |
P. platydactylus | MNCNDNA 5524 | FJ438811.1 | EU192255.1 | NA | NA |
P. pluvialis | CORBIDI 11862 | NA | KX155577 | NA | NA |
CORBIDI 16695 | NA | KX155578 | NA | NA | |
P. pulchridormientes | CORBIDI 15563 | NA | KX664106 | NA | NA |
CORBIDI 15566 | NA | KX664107 | NA | NA | |
P. pulvinatus | KU 181015 | EF186741.1 | EF186723.1 | NA | NA |
P. pycnodermis | KU 218028 | EF493680.1 | EF493680.1 | NA | NA |
P. quaquaversus | QCAZ25613 | MW567329 | MW567360 | MW451722 | MW567407 |
P. romeroae | QCAZ41121 | MT636507 | MT636528 | MT635624 | MT635662 |
P. rubicundus | QCAZ58932 | NA | MT372670 | MT372613 | NA |
KU 212220 | EF493681.1 | EF493681.1 | NA | NA | |
P. schultei | KU 291702 | EF493351.1 | EF493351.1 | NA | NA |
Pristimantis sp. | QCAZ63481 | NA | MW567350 | NA | MW567399 |
QCAZ63482 | NA | MW567351 | MW451721 | MW567400 | |
ROM 43978 | EU186678.1 | EU186678.1 | NA | NA | |
QCAZ60398 | NA | MT636515 | MT635634 | NA | |
QCAZ58956 | MT636511 | MT636526 | MT635631 | NA | |
CORBIDI 13805 | NA | MZ219639 | MZ219637 | MZ219632 | |
MECN 10117 | NA | KF801580.1 | NA | NA | |
P. subsigillatus | QCAZ45268 | NA | MW567370 | MW451730 | MW567412 |
QCAZ49370 | MW567320 | MW567371 | MW451731 | MW567413 | |
QCAZ51314 | NA | MW567361 | MW451734 | MW567392 | |
QCAZ50012 | NA | MW567372 | MW451733 | MW567414 | |
MHNC 12845 | MN128403 | NA | NA | NA | |
P. tantanti | CORBIDI 12987 | MN128402 | NA | NA | NA |
P. truebae | QCAZ13752 | NA | MW567362 | MW451747 | MW567417 |
QCAZ42714 | MW567324 | MW567364 | MW451751 | MW567418 | |
P. urani | MHUAA 7471 | NA | KU724442.1 | NA | NA |
P. w-nigrum | QCAZ45200 | MT636510 | MT372703 | MT372600 | MT372569 |
QCAZ46256 | NA | MT372704 | MT372603 | MT372571 | |
QCAZ41818 | NA | MT372691 | NA | MT635663 | |
QCAZ52365 | NA | MW567374 | MW451728 | MW567415 | |
P. zorro | MHUAA 8813 | NA | MT747833 | NA | NA |
MHUAA 8814 | NA | MT747834 | NA | NA | |
MHUAA 8816 | NA | MT747835 | NA | NA |
The phylogeny was inferred using Maximum Likelihood as optimality criterion. To choose the substitution models that best adjusted to our sequences, we used Model Finder under the command MFP+MERGE (
Diagnostic characters and comparisons are based on preserved specimens from Museo de Zoología at Pontificia Universidad Católica del Ecuador, Quito (
Adults were measured with digital calipers (to the nearest ± 0.01mm) for eleven morphological variables, following
To explore morphometric differentiation between species, we applied a Principal Components Analysis (PCA). To remove the effect of size covariation, we carried out linear regressions between the morphometric variables and SVL. The PCA was applied to the residuals of the regressions. Morphometric variables associated with eyes (i.e., eye diameter, interorbital distance, eyelid width, internarial distance and eye-nostril distance) had weak correlation with snout-vent length. Low correlation appears to be a result of the difficulty of defining the eye edge on preserved specimens. Therefore, were removed those variables from the analysis. Prior to the PCA, we ran a MANOVA on the residuals to test for morphometric sexual dimorphism independent of size differences . Because the MANOVA was non-significant, we pooled the measurements of both sexes on a single PCA.
To assess species limits between the new species and the closely related P. petersi, we analyzed calls from three males of the new species: QCAZ58940, SVL = 19.3 mm, from Refuge 1, Sardinayacu, Sangay National Park, Morona Santiago Province (2.0983°S, 78.1555°W, 1406 m) collected on 21 January 2015, air temperature 19 °C, recorded in situ by Daniel Rivadeneira, and QCAZ59466, SVL = 19.1 mm, from the ravines of Yurugyacu river, Zarentza community, Llanganates National Park, Pastaza Province, (1.3524°S, 78.0597°W, 1419 m) collected on February 24 2015 and recorded in captivity on 6 March 2015 by Santiago R. Ron and one male not collected from Sardinayacu, Sangay National Park, Morona Santiago Province, recorded by Diego Batallas. Advertisement calls of P. petersi were analyzed from two adult males (not collected) from near its type locality, Cocodrilos, Napo Province, (0.66812°S, 77.7975°W, 1725 m) recorded on 22 June 2016 by Santiago R. Ron. We did not have size data for the recorded individuals of P. petersi. However, we collected other adult males on the same night and chorus and used the size of those individuals to assess interpopulation size differences. For two of the recorded males of the new species, SVL was 19.1 and 19.3 mm; for Pristimantis petersi average SVL was 17.2 mm (16.5–17.8 mm; n = 3). Recordings were made in WAV format, with a sample rate of 44100 Hz and 16-bits. Call variables were measured with RAVEN PRO 1.5 (
Most of our recordings lacked temperature information. However, the variables that allowed us to differentiate the new species from the closely related P. petersi, where call duration and call frequency which are static and are not strongly influenced by ambient temperature (
For call measurements and terminology, we followed the call-centered approach by
The Maximum Likelihood tree (Fig.
Maximum likelihood tree of the Pristimantis lacrimosus group inferred from a partitioned analysis of 4026 aligned sites of DNA sequences of the mitochondrial genes 12S, 16S, and ND-1 and the nuclear gene RAG-1. Bold characters highlight individuals included for the first time in a phylogeny, red taxa highlight previously misidentified species. Pristimantis petersioides sp. nov. is highlighted in blue. SH-aLRT support (above branch) and ultrafast bootstrap support (below) are shown as percentages; asterisks denote 100% for both measures. Outgroups are not shown. Number for voucher museum specimens are shown to the left of the species name; locality is shown to the right and country abbreviation at the end, as follows: ECU Ecuador, PER Peru, COL Colombia, VEN Venezuela, GUY Guyana, PAN Panama.
The ML tree from mitochondrial DNA shows similar topology to the ML tree from all genes. The best-fit models of DNA evolution for each partition are available as Suppl. material
The mtDNA tree shows strong support for the Pristimantis lacrimosus group (bootstrap = 99), for Pristimantis petersi (bootstrap = 100) and for the new species (bootstrap = 99). The ML tree inferred from RAG1 shows lower support values but is congruent in showing a monophyletic Pristimantis lacrimosus group (bootstrap = 91) and in confirming a close relationship between P. petersi and the new species. The mtDNA and RAG1 phylogenies do not show strongly supported incongruences. Mitochondrial DNA and RAG1 phylogenetic trees are available as Suppl. material
The new species is the sister to P. petersi and an undescribed species from Cordillera Escalera, Peru. The uncorrected pairwise p-genetic distances for 16S between P. petersi and the new species range from 7.9% to 8.4%. The clade comprising these three species is sister to an undescribed species from Bombuscaro, Podocarpus National Park, Zamora Province, Ecuador. Samples of the new species separate in two sister clades, a northern clade in Zarentza, Pastaza Province and a southern clade from Sardinayacu and Bosque Protector Abanico, Morona Santiago Province; the uncorrected pairwise p-genetic distances between these clades range from 1.2% to 1.4%.
MANOVA results showed no sexual dimorphism (after removing size effects) on the new species and P. petersi. The PCA show broad overlap in morphometric space between both species (Fig.
Principal components 1 and 2 from analysis of five size-corrected morphological variables. See Table
Character loadings, eigenvalues, and percentage of explained variance for Principal Components (PC) I–II. The analysis was based on the residuals of morphometric variables of adult P. petersioides sp. nov. and P. petersi. Bold figures indicate highest loadings.
Variable | Character loading | |
---|---|---|
PC I | PC II | |
Tibia length | 0.7855 | -0.3038 |
Foot length | 0.7066 | 0.0834 |
Head length | 0.7873 | 0.2181 |
Head width | 0.8332 | 0.2434 |
Tympanum | -0.2087 | 0.9334 |
Eigenvalues | 4.9483 | 2.1547 |
% | 49.48 | 21.54 |
The differences in advertisement calls (see Comparisons with other Species section), the branch lengths in the phylogeny, and genetic distances indicate that the new species, in fact, represents a different species from P. petersi (see below). In the following section, we update the species content of the Pristimantis lacrimosus group and describe the new species.
We include all the descendants from the most recent common ancestor of P. eremitus and P. lacrimosus according to
According to our findings and those of
The Pristimantis lacrimosus group is distributed in Central America, the Guianan Shield, Pacific Basin of Ecuador, and the Amazon Basin. Its species richness peaks in the Ecuadorian Andes (n = 19) and Amazon basin of Ecuador and Peru (n = 14).
We refrain from assigning Pristimantis sneiderni (
Eleutherodactylus petersi Lynch & Duellman 1980 (in part)
Pristimantis petersi Batallas & Brito 2016
Pristimantis petersi
(Figs
Holotype of Pristimantis petersioides sp. nov. QCAZ58939, adult female, SVL = 22.02 mm. Sangay National Park, Sardinayacu, Ecuador. A lateral view of live individual, B dorsal view of live individual, C dorsal view of preserved individual, D ventral view of preserved individual. Photographs A, B by Juan Carlos Sánchez, C, D by Julio C. Carrión-Olmedo
(54: 39 adult males, 15 adult females). All individuals are adults unless otherwise noticed. All from Ecuador. Morona Santiago Province: Sangay National Park: QCAZ58871, female, QCAZ58944, male from Río Volcán (2.1008°S, 78.1559°W, 1345 m), collected by Daniel Rivadeneira, David Velalcázar, Javier Pinto, Francy Mora, Darwin Nuñez, Juan Sanchez, and Andrea Correa; QCAZ58936, 58939, QCAZ58941, females, QCAZ58940, 58942–43, males from Refuge 1 (2.0988°S, 78.1561°W, 1406 m), QCAZ58937–38, males from Chimerella lagoon (2.0885°S, 78.2069°W, 1650 m) collected by Daniel Rivadeneira, Francy Mora, Juan Sánchez and Andrea Correa; QCAZ58881, 58950, females, QCAZ58949 male from the proximities of Cormorant lagoon (2.0738°S, 78.2195°W, 1835 m) collected by Javier Pinto, David Velalcázar and Darwin Nuñez, QCAZ58880, 58951, males from El Enmascarado lagoon (2.0600°S, 78.2207°W, 1796 m) collected by Javier Pinto, David Velalcázar and Darwin Nuñez. in January 2015. QCAZ59166, female, QCAZ59167, 58945–48, males from Refuge 3 (2.0757°S, 78.2157°W, 1724 m), collected by Santiago Ron, Diego Paucar, Pablo Venegas, Pamela Baldeón, Marcel Caminer and Kunam Nucirquia; QCAZ59169–71, males from Cormorant lagoon (2.0738°S, 78.2195°W, 1835 m), collected by Santiago Ron, Diego Paucar, Pablo Venegas, Pamela Baldeón, Marcel Caminer and Kunam Nucirquia, in February 2015. Pastaza Province: QCAZ53227, female, from Anzu river (1.4177°S, 78.0485°W, 1272 m a.s.l), collected by Mauricio Ortega in May 2012. Llanganates National Park: QCAZ45846–50, 45892, 45898, males, from Challuwa Yacu river, Ankaku Reserve (1.2792°S, 78.0779°W, 2300 m) collected by Elicio Tapia and Silvia Aldás in October 2009; QCAZ66553, male, from Ankaku Reserve (1.2770°S, 78.0698°W, 2216 m) collected by Diego Almeida, Santiago Guamán, Darwin Nuñez, María Navarrete, Verónica Andrade, Angel Alvarado, Fernando Alvarado in January 2017, QCAZ59625, male, from Nuchimingue river (1.3626°S, 78.0582°W, 1350 m); QCAZ59456, male, from Yurugyacu river (1.3560°S, 78.0592°W, 1354 m); QCAZ59451, 59467–68, 59479, males, from Zarentza community (1.3556°S, 78.0597°W, 1363 m); QCAZ59458–59, females from near Yurugyacu river (1.3527°S, 78.0596°W, 1354 m); QCAZ59457, 59465 females, QCAZ59454–55, 59462–63, 59466, males from the ravines of Yurugyacu river (1.3523°S, 78.0597°W, 1419 m); QCAZ59470, 59472, females, QCAZ59471, 59473, males from Gustavo Ushpa house trail to Yurugyacu river (1.3430°S, 78.0574°W, 1221 m); QCAZ59461, female, from La paila waterfall (1.3397°S, 78.0594°W, 1360 m) collected by Daniel Rivadeneira, Francy Mora, Juan Carlos Sánchez, David Velalcázar, Darwin Nuñez and Javier Pinto in February 2015.
Napo Province: QCAZ46159, male, from Salcedo-Tena highway, km 60 (0.9847°S, 78.1928°W, 2253 m), collected by Elicio Tapia and Fernando Núñez in November 2009. Pastaza Province: QCAZ59452–53, 59460, 59464, juveniles from the ravines of Yurugyacu river (1.3523°S, 78.0597°W, 1419 m) collected by Daniel Rivadeneira, Francy Mora, Juan Carlos Sánchez, David Velalcázar, Darwin Nuñez and Javier Pinto in February 2015.
English: Sardinayacu’s Rain Frog. Spanish: Cutín de Sardinayacu
The assignment of the new species to the genus Pristimantis is based on the phylogeny (Fig.
Color comparisons are based on digital photos of live specimens, unless otherwise noted. Pristimantis petersioides sp. nov. is most similar to other species of the P. lacrimosus group, especially P. petersi (Lynch & Duellman, 1980), P. bromeliaceus (Lynch, 1979), P. lacrimosus (Jiménez de la Espada, 1875), P. schultei (Duellman, 1990), P. pastazensis (Andersson, 1945), and P. rhodostichus (Duellman & Pramuk, 1999) (Fig.
Quantitative and qualitative characteristics of the advertisement call of Pristimantis petersioides sp. nov. from two localities: Sardinayacu, Morona Santiago Province (2.0983°S, 78.1155°W, 1345 m) and Yurugyacu river, Llanganates National Park, Pastaza Province, Ecuador (1.3524°S, 78.0597°W, 1419 m) in comparison with Pristimantis petersi from Cocodrilos, Napo Province (0.6710°S, 77.7927°W, 1575 m). Mean is given with range in parentheses. Because the dominant frequency is on the first harmonic, it equals the fundamental frequency.
Pristimantis petersioides sp. nov. | Pristimantis petersioides sp. nov. | Pristimantis petersioides sp. nov. | Pristimantis petersi (not collected) | Pristimantis petersi (not collected) | |
QCAZ58940 | QCAZ59466 | (not collected) | |||
Calls analyzed | 47 | 37 | 13 | 4 | 9 |
Call duration (s) | 0.19 (0.11–0.32) | 0.32 (0.16–0.39) | 0.25 (0.19–0.34) | 0.46 (0.41–0.49) | 0.37(0.31–0.44) |
Call rate (calls/minute) | 11.26 (1.77–18.40) | 25.78 (4.52–35.14) | 22.64 (12–17.88) | 4.24 (1.86–6.62) | 9.04 (2.17–33.18) |
Call interval (s) | 6.21 (3.03–33.66) | 2.49 (1.37–13.09) | 2.44 (1.82–3.05) | 20.16 (8.59–31.73) | 11.13(1.41–27.20) |
Call rise time (s) | 0.03 (0.021–0.036) | 0.013 (0.011–0.019) | 0.008 (0.004–0.015) | 0.064(0.04–0.12) | 0.0107(0.07–0.18) |
Notes per call | 1 | 1 | 1 | 1 | 1 |
Fundamental frequency (Hz) | 4837.22 (4373.4–5092.6) | 4122 (3644.5–4382.8) | 4333.1 (4295.9–4392.8) | 3846.7(3820.3–3890.6) | 4076.8 (3914.1–4242.2) |
Dominant frequency (Hz) | 1st harmonic | 1st harmonic | 1st harmonic | 1st harmonic | 1st harmonic |
Qualitative morphological characters of species most similar to P. petersioides sp. nov.
Maximun size in females | Eyelid tubercle | Discoidal fold | Dorsal snout shape | Lateral snout shape | TY/ED | Knee tubercle | Heel tubercle | Dorsum | Data source | |
P. bromeliaceus | 27.2 mm | 2-3 non conical | prominent | subacuminate | pointed | 1/4 to 2/5 | small wart | conical | smooth | Lynch , 1979 |
P. lacrimosus | 32.5 mm | absent | evident | rounded | rounded | 3/10 | absent | absent | finely shagreen | Jiménez de la Espada, 1875 |
P. petersi | 21.1 mm | conical | absent | rounded | truncate | 3/5 to 1/2 | absent | absent | smooth | Herein |
P. petersioides sp. nov. | 24.8 mm | conical | ill-defined | rounded to truncate | truncate | 2/5 to 1/2 | absent | absent | smooth to shagreen | Herein |
P. rhodostichus | 29.5 mm | several low | prominent | long, acuminate | acutely rounded | 2/5 | absent | absent | finely shagreen | Duellman and Pramuk, 1999 |
P. schultei | 34.0 mm | several low | not evident | acuminate | inclined posteroventrally | 2/5 to 1/2 | absent | several low | shagreen | Duellman, 1990 |
Live specimens of Pristimantis petersioides sp. nov. and most similar species. A Pristimantis petersioides sp. nov., QCAZ58938, adult male (SVL 17.99 mm), B Pristimantis petersi, QCAZ63455, adult male (SVL 16.49 mm), C Pristimantis sp., QCAZ62940, adult male (SVL 23.45 mm), D Pristimantis bromeliaceus, QCAZ56454, adult male (SVL 21.93 mm) E Pristimantis schultei, QCAZ51551, adult male (SVL 24.60 mm). Photographs by Juan Carlos Sánchez A, by David Velalcázar B, by Valeria Chasiluisa C, by Jorge Brito D, by Diego Paucar E.
Adult female (QCAZ58939). Measurements (in mm): SVL 22.02; tibia length 12.07; foot length 10.72; head length 8.82; head width 9.09; eye diameter 2.96; tympanum diameter 1.35; interorbital distance 2.52; upper eyelid width 2.44; internarial distance 1.59; eye-nostril distance 2.59; tympanum-eye distance 0.71. Body slender; head slightly wider than long, wider than body; snout rounded to truncate with rostral papilla in dorsal view, truncate in lateral profile; canthus rostralis distinct, slightly curved in dorsal view; loreal region concave; interorbital space flat, no cranial crests; eye large, protuberant; upper eyelid about 97% of interorbital distance, bearing one subconical tubercle. Tympanic membrane and annulus distinct, rounded, with inconspicuous supratympanic fold, partially obscuring anterodorsal edge; horizontal diameter of tympanum about 13% of head length, separated from eye by a distance about one half tympanum length; choanae large, rounded, not concealed by palatal shelf of maxillary arc; dentigerous processes of vomers prominent, oblique, bearing a transverse row of five teeth; tongue big, elliptical, posterior border slightly notched, 40% of the anterior surface adherent to floor of mouth. Skin on dorsum smooth to shagreen; dorsolateral folds absent; skin on upper flanks bearing scattered low tubercles; skin on belly weakly areolate; skin on throat and chest smooth; discoidal fold ill-defined; skin in upper cloacal region shagreen. Forearms slender bearing low antebrachial tubercle and one subconical ulnar tubercle at the distal half of the forearm; fingers large and slender, all with broadly expanded pads, all fingers with discs; fingers bearing narrow lateral fringes; relative lengths of fingers I < II < IV < III; three subarticular tubercles on finger III (Fig.
Hindlimbs slender; tibia length about 55% of SVL; upper surfaces of hindlimbs smooth; foot length about 48% of SVL, posterior surfaces of thighs smooth, ventral surfaces of thighs slightly areolate; knee and heel lacking tubercles; outer surface of tarsus bearing three low, inconspicuous tubercles, equally distributed along tarsus; toes bearing narrow lateral fringes; webbing between toes absent; discs on toes broadly expanded as those on fingers, rounded; relative lengths of toes: I < II < III < V < IV; Toe V much longer than Toe III (disc on Toe III reaches proximal edge of penultimate subarticular tubercle on Toe IV, disc on Toe V exceeds the distal edge of penultimate subarticular tubercle on Toe IV), subarticular tubercles rounded, simple, elevated; plantar surface with low supernumerary tubercles, bearing four subarticular tubercles (Fig.
Color of holotype in preservative. (Fig.
Color of holotype in life. (Fig.
(Fig.
Morphometric variables of P. petersioides sp. nov. and P. petersi. Mean ± SD is given with range in parentheses. All measurements are in millimeters.
Variable | P. petersioides sp. nov. | P. petersi | ||
---|---|---|---|---|
male | female | male | female | |
n = 39 | n = 15 | n = 10 | n = 2 | |
Snout-vent length | 18.5 ± 1.5 (15.8–23.9) | 22.8 ± 1.4 (20.4–24.8) | 18.3 ± 1.7 (16.5 –22.7) | 20.1 ± 1.4 (19.1–21.1) |
Tibia length | 9.8 ± 0.8 (8.3–11.9) | 11.7 ± 1.0 (8.5–12.6) | 9.6 ± 0.6 (8.6–11.0) | 10.7 ± 1.6 (9.6–11.8) |
Foot length | 8.6 ± 0.9 (6,9–10.7) | 10.6 ± 0.7 (8.8–11.6) | 8.6 ± 0.7 (7.8–10.1) | 10.0 ± 0.3 (9.8–10.2) |
Head length | 6.5 ± 0.6 (5.3–7.8) | 8.0 ± 0.6 (7.2–9.1) | 6.1 ± 0.5 (5.5–7.1) | 7.1 ± 0.5 (6.8–7.5) |
Head width | 7.0 ± 0.6 (5.9–8.5) | 8.8 ± 0.5 (8.0–9.5) | 6.9 ± 0.5 (6.3–8.1) | 7.7 ± 0.4 (7.5–8.0) |
Eye diameter | 2.6 ± 0.2 (2.2–3.1) | 3.0 ± 0.3 (2.4–3.5) | 2.6 ± 0.2 (2.4–3.1) | 2.8 |
Tympanum diameter | 0.9 ± 0.1 (0.7–1.1) | 1.1 ± 0.2 (0.8–1.4) | 0.9 ± 0.1 (0.7–1.0) | 1.1 ± 0.1 (1.0–1.2) |
Interorbital distance | 2.2 ± 0.2 (1.9–2.6) | 2.6 ± 0.2 (2.4–3.0) | 2.2 ± 0.1 (2.0–2.5) | 2.6 ± 0.2 (2.4–2.7) |
Upper eyelid width | 2.2 ± 0.3 (1.6–2.6) | 2.6 ± 0.2 (2.3–3.0) | 2.1 ± 0.4 (1.7–2.9) | 2.27 |
Internarial distance | 1.4 ± 0.1 (1.2–1.7) | 1.7 ± 0.1 (1.5–2.0) | 1.5 ± 0.2 (1.3–1.7) | 1.6 ± 0.2 (1.4–1.7) |
eye–nostril distance | 1.9 ± 0.2 (1.6–2.5) | 2.5 ± 0.2 (2.2–2.8) | 2.1 ± 0.3 (1.8–2.9) | 2.3 ± 0.4 (2.0–2.6) |
Color variation in preserved individuals of Pristimantis petersioides sp. nov. A Dorsal view (left to right): QCAZ59461(SVL 22.95 mm), QCAZ59470 (SVL 22.94 mm), QCAZ58939 (SVL 22.02 mm), QCAZ58951 (SVL 19.75 mm), B Dorsal view (left to right): QCAZ59171 (SVL 19.50 mm), QCAZ59456 (SVL 19.05 mm), QCAZ59462 (SVL 19.00 mm), QCAZ59468 (SVL 18,35 mm), C Ventral view of specimens in (A), D Ventral view of specimens in (B). Photographs by Julio C. Carrión-Olmedo.
(Fig.
Variation in live adult individuals of Pristimantis petersioides sp. nov. A QCAZ59471 (SVL 17.45 mm), B QCAZ59455 (SVL 18.2 mm), C QCAZ58943 (SVL 17.73 mm), D QCAZ59456 (SVL 19.05 mm), E QCAZ58938 (SVL 17.99 mm), F QCAZ59458 (SVL 21.84 mm), G QCAZ58941 (SVL 20.42 mm), H QCAZ59466 (SVL 19.06 mm). Dorsolateral view on the left, ventral view on the right. Photographs A and H by Santiago R. Ron, B–G by Juan Carlos Sánchez.
Quantitative measurements of the advertisement call of Pristimantis petersioides sp. nov. (QCAZ58940) are shown in Table
Advertisement calls of Pristimantis petersioides sp. nov. and Pristimantis petersi. (A) oscillogram and spectrogram of a call series of Pristimantis petersioides sp. nov., (B) oscillogram (top), spectrogram (middle), and power spectrum (bottom) of a single call of Pristimantis petersioides sp. nov. and (C) oscillogram (top), spectrogram (middle), and power spectrum (bottom) of a single call of Pristimantis petersi.
Pristimantis petersioides sp. nov. is known from six localities in the eastern Andean slopes of central Ecuador between 1221–2300 m (Fig.
Records of Pristimantis petersioides sp. nov. (yellow) and P. petersi (red). Confirmed records are based on specimens deposited at the Museum of Zoology, Pontificia Universidad Católica del Ecuador. Unconfirmed records (diamonds) from
The specific epithet is a masculine noun in apposition. The suffix oides is derived from the Greek eidos meaning similar. The name makes reference to the similarity between the new species and its sister species, Pristimantis petersi.
Four out of six known localities are inside National Parks (Sardinayacu in Parque Nacional Sangay and Ankaku, Zarentza and Salcedo-Tena road in Parque Nacional Llanganates); nonetheless, based on a vegetation cover map (
In Sardinayacu, this species was one of the most common during surveys (24 individuals found in 9 days by 13 people) which suggest it can be locally abundant.
Pristimantis petersioides sp. nov. differs from P. sp. (
Pristimantis petersi was considered to have a wide distribution from the central Andes of Colombia in Caquetá, Huila, and Putumayo (
Our results and those of previous systematic reviews (show that eastern montane forests still harbor many undescribed species of Pristimantis. Similar findings have been previously reported by Ortega et al. (2015),
Similar to
Bioacoustic comparisons are of importance for taxonomy because advertisement calls mediate species recognition and mate choice (e.g.,
Laboratory and fieldwork was funded by a grant from SENESCYT (Arca de Noé Initiative; S. R. Ron and O. Torres-Carvajal principal investigators) and grants from Dirección General Académica of Pontificia Universidad Católica del Ecuador. We are thankful to the
Collection data for Museum specimens examined in the morphological comparisons
Data type: Collection data
Explanation note: All specimens are deposited at the amphibian collection of the Zoological Museum (QCAZ), Pontificia Universidad Católica del Ecuador in Quito, Ecuador.
Best-fit models of DNA evolution for partitions of the phylogenetic analyses
Data type: Phylogenetic
Explanation note: Models were chosen according to the BIC criterion.
Mitochondrial DNA and RAG1 phylogenetic trees
Data type: Phylogenetic
Explanation note: The Pristimantis lacrimosus species group is shown in green.