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Research Article
A new treefrog from Cordillera del Cóndor with comments on the biogeographic affinity between Cordillera del Cóndor and the Guianan Tepuis (Anura, Hylidae, Hyloscirtus)
expand article infoSantiago R. Ron‡, Marcel A. Caminer‡, Andrea Varela-Jaramillo‡, Diego Almeida-Reinoso‡
‡ Pontificia Universidad Católica del Ecuador, Quito, Ecuador

Corresponding author: Santiago R. Ron ( santiago.r.ron@gmail.com )

Academic editor: Angelica Crottini
© 2018 Santiago R. Ron, Marcel A. Caminer, Andrea Varela-Jaramillo, Diego Almeida-Reinoso.
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: Ron SR, Caminer MA, Varela-Jaramillo A, Almeida-Reinoso D (2018) A new treefrog from Cordillera del Cóndor with comments on the biogeographic affinity between Cordillera del Cóndor and the Guianan Tepuis (Anura, Hylidae, Hyloscirtus). ZooKeys 809: 97-124. https://doi.org/10.3897/zookeys.809.25207
ZooBank: urn:lsid:zoobank.org:pub:17A46360-8038-4385-A995-1168357B08A3
Open Access

Abstract

The Hyloscirtus larinopygion group is a clade of 16 species of large hylids that inhabit cascading Andean streams. They have brown coloration that, in most species, contrasts with bright marks. Herein morphological and genetic evidence is used to describe a new species of the group from Cordillera del Cóndor, a sub-Andean mountain chain that has phytogeographic affinities with the Guianan Tepuis. The new species is characterized by dark-brown coloration with contrasting bright orange flecks and by the presence of an enlarged and curved prepollex protruding as a spine. The new species is closely related to H. tapichalaca and an undescribed species from the southern Andes of Ecuador. The genetic distance between H. hillisi sp. n. and its closest relative, H. tapichalaca, is 2.9% (gene 16S mtDNA). Our phylogeny and a review of recently published phylogenies show that amphibians from Cordillera del Cóndor have close relationships with either Andean or Amazonian species. Amphibians do not show the Condor-Guianan Tepuis biogeographic link that has been documented in plants.

Keywords

Biodiversity, Colomascirtus , Ecuador, H. larinopygion group, Peru, prepollical spine, phylogeny

Introduction

Hyloscirtus Peters 1882, is a genus of 37 species of treefrogs distributed from Costa Rica to the Andes of Bolivia, Colombia, Ecuador, Peru, and Venezuela (AmphibiaWeb 2018; Frost 2018). They reproduce along streams and share, as a synapomorphy, the presence of wide lateral fringes on fingers and toes (Faivovich et al. 2005 but see Coloma et al. 2012). A well-supported clade within Hyloscirtus is the Hyloscirtus larinopygion species group (Almendáriz et al. 2014; Coloma et al. 2012; Duellman and Hillis 1990; Rivera-Correa et al. 2016). It is composed of 16 species characterized by large size (SVL < 60 mm) and gray or brown coloration that in many species contrast with bright marks. Species of this group were transferred to the genus Colomascirtus by Duellman et al. (2016). A recent phylogeny showed that the recognition of Colomascirtus rendered Hyloscirtus paraphyletic (Rojas-Runjaic et al. 2018). To maintain taxonomic stability, Colomascirtus was synonymized under Hyloscirtus by Rojas-Runjaic et al. (2018).

The Hyloscirtus larinopygion group is composed of two well-supported clades that replace each other latitudinally with a small area of sympatry in central Ecuador (Almendáriz et al. 2014a). The northern clade is distributed in the Andes of central and northern Ecuador and southern Colombia; the southern clade is distributed in the eastern Andean slopes of central and southern Ecuador and northern Peru (Rivera-Correa et al. 2016). The southern clade is composed of three species: H. condor Almendáriz et al. 2014a, H. tapichalaca (Kizirian et al. 2003), and an undescribed species previously reported as H. lindae (Almendáriz et al. 2014a). Hyloscirtus diabolus Rivera-Correa et al. 2016 is also a putative member of this clade (Rivera-Correa et al. 2016). The four species differ from species in the northern clade by having an enlarged prepollex with the shape of a spine that protrudes below the thumb (Almendáriz et al. 2014; Rivera-Correa et al. 2016). Recent fieldwork in Cordillera del Cóndor by a field team from the Museum of Zoology, Pontificia Universidad Católica del Ecuador, resulted in the discovery of an undescribed species of the southern clade which also shares a spine-shaped prepollex. Cordillera del Cóndor is a sub-Andean mountain chain with phytogeographic affinities to the Tepuis in the Guiana Region (e.g., Neill 2005). Herein we present morphological and genetic evidence to describe the new species and provide a new phylogeny for the genus Hyloscirtus. We also review recent amphibian phylogenies to explore the existence of biogeographic links between Cordillera del Cóndor and the Guianan Tepuis.

Materials and methods

DNA extraction, amplification, and sequencing

DNA was extracted from muscle or liver tissue preserved in 95% alcohol following standard phenol-chloroform extraction protocols (Sambrook et al. 1989). Standard polymerase chain reaction (PCR) was performed to amplify two mitochondrial genes (12S rRNA + tRNAVal and 16S rRNA), using primers listed in Goebel et al. (1999), Heinicke et al. (2007), Hedges et al. (2008), and Heinicke et al. (2009) under standard protocols. PCR products were sequenced in both directions by Macrogen (Macrogen Inc., Seoul, Korea).

Sequences were edited and assembled with Geneious 10.2.3 software (Gene Matters Corp, Kearse et al. 2012). The obtained sequences were compared with those available in GenBank (http://www.ncbi.nlm.nih.gov/genbank/) for the Hyloscirtus larinopygion and bogotensis groups (published by Almendáriz et al. 2014; Coloma et al. 2012; Darst and Cannatella 2004; Elmer and Cannatella 2008; Faivovich et al. 2004; Faivovich et al. 2005; Guayasamin et al. 2015; Rojas-Runjaic et al. 2018; Wiens et al. 2005; Wiens et al. 2006) (Table 1). For the outgroup we added sequences of Aplastodiscus weygoldti, Bokermannohyla circumdata, Boana crepitans, B. lundii, B. marianitae, B. riojana, Itapotihyla langsdorfii, Myersiohyla kanaima, and Pseudacris nigrita.

Table 1.
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Genbank accession numbers for DNA sequences included in the phylogenetic analysis.

Species Museum Number GenBank Accession Number Source
12S 16S
Hyloscirtus alytolylax QCAZ 24376 JX155799 JX155826 Coloma et al. 2012
QCAZ 24377 JX155798 JX155825 Coloma et al. 2012
H. armatus KU 173222 AY819423 – Wiens et al. 2005
AMNH 165163 AY549321 AY549321 Faivovich et al. 2004
H. callipeza UIS-A 5947 MG596780 MG596780 Rojas-Runjaic et al. 2018
H. charazani AMNH 165132 AY843618 AY843618 Faivovich et al. 2005
H. colymba SIU 6926 DQ380353 – Wiens et al. 2006
SIUC H-7079 AY843620 AY843620 Faivovich et al. 2005
H. condor MEPN 14754 KF756939 KF756939 Almendáriz et al. 2014a
MEPN 14758 KF756938 KF756938 Almendáriz et al. 2014a
H. criptico QCAZ 43421 JX155812 JX155839 Coloma et al. 2012
QCAZ 43422 JX155814 JX155841 Coloma et al. 2012
QCAZ 45466 JX155813 JX155840 Coloma et al. 2012
H. hillisi sp. n. QCAZ 68646 MH883792 MH883796 This study
QCAZ 68647 – MH883797 This study
QCAZ 68648 MH883793 MH883798 This study
QCAZ 68649 MH883794 MH883799 This study
QCAZ 68651 MH883795 MH883800 This study
H. jahni MHNLS 20318 MG596776 MG596776 Rojas-Runjaic et al. 2018
MHNLS 20319 MG596777 MG596777 Rojas-Runjaic et al. 2018
MHNLS 20324 MG596779 MG596779 Rojas-Runjaic et al. 2018
H. japreria MHNLS 18888 MG596766 MG596766 Rojas-Runjaic et al. 2018
MHNLS 19235 MG596769 MG596769 Rojas-Runjaic et al. 2018
UIS-A 5496 MG596770 MG596770 Rojas-Runjaic et al. 2018
H. larinopygion QCAZ 41826 JX155817 JX155844 Coloma et al. 2012
QCAZ 45462 JX155818 JX155845 Coloma et al. 2012
H. lascinius KU 181086 DQ380359 – Wiens et al. 2006
MHNLS 19163 MG596762 MG596762 Rojas-Runjaic et al. 2018
MHNLS 19164 MG596763 MG596763 Rojas-Runjaic et al. 2018
H. lindae QCAZ 41232 JX155821 JX155848 Coloma et al. 2012
QCAZ 45342 JX155824 JX155851 Coloma et al. 2012
QCAZ 45346 JX155822 JX155849 Coloma et al. 2012
QCAZ 45463 JX155823 JX155850 Coloma et al. 2012
H. mashpi MZUTI 614 KT279526 KT279511 Guayasamin et al. 2015
H. pacha KU 202760 AY326057 AY326057 Darst and Cannatella 2004
WED 53493 AY326057 AY326057 Darst and Cannatella 2004
H. palmeri MZUTI 608 KT279549 KT279520 Guayasamin et al. 2015
SIUC H-6924 AY843650 AY843650 Faivovich et al. 2005
H. pantostictus QCAZ 45435 JX155820 JX155847 Coloma et al. 2012
QCAZ 45438 JX155819 JX155846 Coloma et al. 2012
KU 202732 AY326052 – Darst and Cannatella 2004
H. phyllognathus QCAZ 23938 JX155800 JX155827 Coloma et al. 2012
QCAZ 32271 JX155802 JX155829 Coloma et al. 2012
QCAZ 41032 JX155801 JX155828 Coloma et al. 2012
KU 212119 DQ380369 – Wiens et al. 2006
MHNLS 20321 MG596772 MG596772 Rojas-Runjaic et al. 2018
MHNLS 20325 MG596774 MG596774 Rojas-Runjaic et al. 2018
QCAZ 42165 JX155806 JX155833 Coloma et al. 2012
QCAZ 43654 JX155807 JX155834 Coloma et al. 2012
H. psarolaimus QCAZ 27049 JX155808 JX155835 Coloma et al. 2012
QCAZ 46095 JX155809 JX155836 Coloma et al. 2012
H. ptychodactylus QCAZ 46030 JX155804 JX155831 Coloma et al. 2012
QCAZ 46031 JX155805 JX155832 Coloma et al. 2012
H. simmonsi KU 181167 DQ380376 – Wiens et al. 2006
H. staufferorum QCAZ 45962 JX155816 JX155843 Coloma et al. 2012
QCAZ 45967 JX155815 JX155842 Coloma et al. 2012
H. tapichalaca QCAZ 15083 JX155803 JX155830 Coloma et al. 2012
QCAZ 16704 AY563625 AY563625 Faivovich et al. 2004
H. tigrinus QCAZ 31550 JX155811 JX155838 Coloma et al. 2012
QCAZ 41351 JX155810 JX155837 Coloma et al. 2012
Hyloscirtus sp. MZUTI 3262 KT279503 KT279544 Guayasamin et al. 2015
KU 202728 DQ380361 – Wiens et al. 2006

Sequences were aligned using the Geneious extension MAFFT Multiple Alignment with the algorithm LINS-I (Katoh and Standley 2013). Alignments were imported into Mesquite (version 3.04; Maddison and Maddison 2018) for final visual adjustments. The final matrix included 2497 characters. The best partition strategy and best-fit model of nucleotide evolution for our data were obtained in PartitionFinder v.2.1.1 (Lanfear et al. 2012) under the corrected Akaike Information Criterion (AICc).

Phylogeny

Phylogenetic relationships were inferred using maximum-likelihood and Bayesian inference. Maximum likelihood analysis were conducted with GARLI 2.0 (Zwickl 2006) using default values, except for the number of generations without topology improvement required for termination (genthreshfortopoterm = 30000) and the maximum number of generations to run and maximum search time (stopgen and stoptime = 5000000). A total of 40 independent searches were run, 20 started from random trees (streefname = random) and 20 from stepwise addition trees (streefname = stepwise). Likelihood values of the 40 searches were within 0.1 likelihood units of each other indicating that all searches converged on similar optimal trees. Support was assessed using 200 bootstrap pseudoreplicates. Bayesian phylogenetic analyses were carried out in MrBayes 3.2.6 (Ronquist et al. 2012). We made four parallel runs of the Metropolis-coupled Monte Carlo Markov for 20 million generations. Each run had five chains, sampled every 1000 generations and with a temperature of 0.1. Convergence into a stationary distribution was measured with software Tracer version 1.4 (Rambaut and Drummond 2007). The search was finished when the average standard deviations of split frequencies was < 0.05 between runs and ESS values were > 200 for all parameters. The consensus tree was generated after discarding 10% of the initial generations as burn-in. Bayesian analyses were carried out at Cipres Science Gateway (available at https//www.phylo.org; Miller et al. 2010).

Pairwise genetic distances between-species (uncorrected-p) were calculated with MEGA 5 (Tamura et al. 2011) for genes 16S (886 bp) and 12S (773 bp). Genetic distances for gene 16S are the most widely used standard to identify candidate species (e.g., Coloma et al. 2012; Fouquet et al. 2007; Janzen and Hallwachs 2011; Vieites et al. 2009).

Morphology

Specimens of the new species were compared to published descriptions and alcohol-preserved specimens of the Hyloscirtus larinopygion group from Museo de Zoología at Pontificia Universidad Católica del Ecuador, Quito (QCAZ). Examined specimens are listed as Appendix 1. Webbing formulae of hand and foot follow Savage and Heyer (1967) as modified by Myers and Duellman (1982). Morphological measurements were taken with digital calipers (± 0.01 mm) from specimens fixed in 10% formalin and preserved in 70% ethanol according to the methodology described in Duellman (1970). Measurements are: SVL (snout-vent length); HL (head length); HW (head width); ED (eye diameter); TD (tympanum diameter); TL (tibia length); FEL (femur length); and FL (foot length). Sex was determined by direct examination of gonads.

We also compared qualitative morphological characters between the new species and its closest relatives. Six characters were evaluated: (1) dorsal coloration; (2) ventral coloration; (3) marks on flanks and hidden surfaces of thighs; (4) iris coloration; (5) prepollex condition; and (6) in life, webbing coloration. Life coloration was obtained from color photographs.

Results

Phylogeny and genetic distances

According to PartitionFinder, the best partition strategy consisted of two partitions under model GTR + I + G. Maximum likelihood and Bayesian inference analyses resulted in similar topologies. Four species groups within Hyloscirtus (H. jahni, H. bogotensis, H. armatus, and H. larinopygion group) were recovered with strong support (posterior probability, pp = 1.0 and bootstrap = 100) in both analysis (Figure 1). However, phylogenetic relationships among these groups were weakly supported (pp < 0.71 and bootstrap < 50), as previously reported (Almendáriz et al. 2014; Coloma et al. 2012; Guayasamin et al. 2015; Rojas-Runjaic et al. 2018). The only exception was the strong support found for the clade H. armatus group + H. larinopygion group found in the Bayessian analysis (pp = 0.99). The phylogeny shows Hyloscirtus hillisi sp. n. sister to Hyloscirtus sp. + H. tapichaca. Hyloscirtus sp. (KU 202728) is an undescribed species previously referred as “H. lindae” (Almendáriz et al. 2014; Duellman and Hillis 1990).Hyloscirtus condor is sister to a clade conformed by these three species. All together form a strongly supported clade distributed in the eastern slopes of the Andes of central and southern Ecuador and northern Peru (Southern Clade; Figs 1, 2). The Southern Clade is sister to a clade distributed to the north and confirmed by the remaining species of the Hyloscirtus larinopygion group (Northern Clade; Figs 1, 3). The Northern and Southern clades have a narrow zone of sympatry in central Ecuador (Figure 2).

Figure 1. 

Strict consensus tree of Hyloscirtus species inferred with Bayesian inference. Museum numbers are shown for each sample. Bayesian posterior probabilities (pp × 100) are shown above the branches and bootstrap values below. Values of 100% are represented by an asterisk. Missing values indicate weakly supported nodes (pp and bootstrap < 50). Outgroup species are not shown. For locality data see Table 1 and Appendix 1.

Figure 2. 

Records of the Southern Clade of the Hyloscirtus larinopygion group. Locality data were obtained from specimens deposited at Museo de Zoología, Pontificia Universidad Católica del Ecuador (QCAZ), Duellman and Hillis (1990), Almendáriz et al. (2014a), and Rivera-Correa et al. (2016). The arrow indicates the locality where the Northern and Southern clades are sympatric. See text for details.

Figure 3. 

Records of the Northern Clade of the Hyloscirtus larinopygion group. Locality data were obtained from specimens deposited at Museo de Zoología, Pontificia Universidad Católica del Ecuador (QCAZ) and Duellman and Hillis (1990). The arrow indicates the locality where the Northern and Southern clades are sympatric. See text for details.

Genetic distances between the new species and its closest relatives are characteristic of interspecific distances for the H. larinopygion group. For gene 12S, distances with H. tapichalaca are 0.031 to 0.038 and with H. sp. (KU 202728) are 0.031 to 0.033. These distances are higher than those observed for the same gene between H. pacha and H. staufferorum (0.014–0.018), H. princecharlesi and H. ptychodactylus (0.004–0.020) and H. criptico and H. psarolaimus (0.022–0.026; Almendáriz et al. 2014). Genetic distances for gene 16S range from 0.029 and 0.040 (Table 2). The genetic divergence between H. hillisi sp. n. and its closest relatives and its unique morphology indicates that it is a new species that we describe below.

Table 2.
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Pairwise genetic distances (uncorrected-p) between Hyloscirtus hillisi sp. n. and its closest relatives, based on sequences of 16S mtDNA. Mean and ± standard deviation are given with range in parentheses. Diagonal values are intraspecific distances.

H. hillisi sp. n. (n = 5) H. tapichalaca (n = 2) H. condor (n = 2)
H. hillisi sp. n. 0.001 ± 0.0007 (0–0.002) – –
H. tapichalaca 0.029 ± 0.0005 (0.029–0.030) 0.009 –
H. condor 0.04 ± 0.0005 (0.039–0.040) 0.041 ± 0.002 (0.039–0.043) 0

Hyloscirtus hillisi sp. n.

http://zoobank.org/95C54DD9-297E-471D-8E5F-2B96BE740147

Holotype

QCAZ 68649 (Figs 5–7), field no. SC 59176, adult female from Ecuador, Provincia Morona Santiago, Caverns-cascade trail, Reserva Biológica El Quimi, on the slopes of flat-topped mountain on the eastern side of the Río Quimi valley (3.5190S, 78.3788W), 2128 m above sea level, collected by Diego Almeida, Darwin Núñez, Kunam Nucirquia, Alex Achig, and Ricardo Gavilanes on 8 July 2017.

Paratopotypes

QCAZ 68646, 72549 subadult females, 68651–54, 72552, tadpoles, 69001, metamorphs, 72550, 72553, adult males, 2112–2134 m of elevation. Collected on 7–14 July 2017 and 12–19 April 2018 by Diego Almeida, Darwin Núñez, Kunam Nucirquia, Alex Achig, Ricardo Gavilanes, and María del Mar Moretta.

Paratypes

All specimens from Reserva Biológica el Quimi, eastern side of the Río Quimi valley, Provincia Morona Santiago, Ecuador. Base camp surroundings, near Río Cristalino (3.5183S, 78.3914W), 1992 m, QCAZ 68647, juvenile, 68648, 68650, metamorphs, 68655–56, 71182, tadpoles collected on 4, 8–9 July 2017; second plateau, near limestone cave (3.5189S, 78.3815W), 2121 m, QCAZ 72551, adult male, collected on 19 April 2018. Collected by Diego Almeida, Darwin Núñez, Kunam Nucirquia, Alex Achig, and Ricardo Gavilanes.

Diagnosis

The diagnosis and comparisons are based on one adult female, three adult males, and two subadult females. The new species is diagnosed by the following characters: mean SVL 70.3 mm in adult males (range 66.7–72.3; n = 3), 65.8 mm in one adult female; vomerine odontophores conic-shaped with a gap medially, each process with three to five prominent teeth; supracloacal flap ill-defined; supratympanic fold present; finger webbing formula: I basal II2-—3-III2½—2IV, toe webbing formula: I2-—2II1+—2+III1½—2½IV2½—1+V; forelimbs hypertrophied in males; enlarged and curved prepollex protruding as a spine in both sexes; fleshy calcar absent; dorsum, flanks, and dorsal areas of limbs dark grayish brown with tiny orange marks varying from abundant to sparse; venter dark grayish brown; iris bronze or yellowish with dark brown reticulation.

Comparisons

Hyloscirtus hillisi is most similar to H. condor, H. diabolus, and H. tapichalaca (Figure 4). They share the presence of an enlarged claw-like prepollex. Hyloscirtus condor differs in ventral coloration (light gray to light salmon in H. condor vs. dark brown in H. hillisi) and dorsal coloration (brown dorsum with diffuse yellow speckling in H. condor vs. dark brown dorsum with contrasting orange round marks in H. hillisi). Hyloscirtus diabolus differs from H. hillisi by having a red iris (bronze or yellowish with brown reticulations in H. hillisi) and a fleshy calcar (calcar absent in H. hillisi; Rivera-Correa et al. 2016). Hyloscirtus tapichalaca differs from H. hillisi by having a brown dorsum without orange marks (orange marks present in H. hillisi) and white disks on fingers and toes (disks are dark brown in H. hillisi). The remaining species of the H. larinopygion group lack the enlarged claw-like prepollex (Ardila-Robayo et al. 1993; Mueses-Cisneros and Anganoy-Criollo 2008; Mueses-Cisneros and Perdomo-Castillo 2011; Ruiz-Carranza and Lynch 1982; Rivera-Correa et al. 2016).

Figure 4. 

Live individuals of Hyloscirtus. A, B Hyloscirtus diabolus (CORBIDI 12885, adult male, holotype, SVL = 82.3 mm); C, D H. tapichalaca (QCAZ 63872, adult female, SVL = 76.19 mm); E, F H. condor (QCAZ 65237, adult male, SVL = 67.18 mm). Photographs: Karla García-Burneo, Diego Quirola, and Santiago Ron.

Description of the holotype

An adult female (Figs 5–7), 65.78 mm SVL. Head round in dorsal view, wider than long; snout nearly truncate in lateral and dorsal views; distance from nostril to eye shorter than diameter of eye; canthus rostralis rounded; loreal region slightly concave; internarial region nearly flat; top of head slightly concave; nostrils slightly protruding anterolaterally; lips rounded, not flared; interorbital area slightly convex; eye large, protuberant; diameter of eye 1.85 times diameter of tympanic annulus; supratympanic fold thick, curved, covering posterodorsal edge of tympanum, extending from eye to posterior end of mandible and to shoulder; tympanum rounded; tympanic annulus distinct, rounded, separated from eye by ca. 1.43 times its diameter.

Figure 5. 

Variation in life of Hyloscirtus hillisi sp. n. from Reserva Biológica El Quimi. AQCAZ 68649 (adult female, holotype, SVL = 65.78 mm) BQCAZ 68646 (subadult female, SVL = 48.55 mm) C not collected.

Figure 6. 

Variation of preserved specimens of Hyloscirtus hillisi sp. n. From left to right, first and second rows: QCAZ 68649 (holotype, adult female), QCAZ 68646 (subadult female); third and fourth rows: QCAZ 68647 (juvenile), QCAZ 69001, 68650, 68648 (metamorphs).

Figure 7. 

Ventral views of the left hand and foot of Hyloscirtus hillisi sp. n. Holotype (QCAZ 68649).

Forearms robust compared to upper arms but not hypertrophied; axillary membrane absent; ulnar tubercles absent; relative length of fingers I < II < IV < III; fingers bearing large, oval discs, wider than finger; subarticular tubercles prominent, round to ovoid, single; supernumerary tubercles present, small and rounded; thenar tubercle, elliptical; palmar tubercle round; prepollical tubercle large, elliptical; prepollex enlarged, claw shaped; webbing formula of fingers I basal II2-—3-III2½—2IV (Fig. 7).

Toes bearing discs broadly expanded, rounded and slightly smaller than those of fingers; relative length of toes I < II < III < V < IV; inner metatarsal tubercle large, oval; outer metatarsal tubercle absent; subarticular tubercles single, round, large, and protuberant; supernumerary tubercles present; toes webbing formula I2-—2II1+—2+III1½—2½IV2½—1+V (Fig. 7).

Skin on dorsum, flanks, dorsal surfaces of limbs, throat, chest, dorsal, and inner surfaces of thighs smooth; belly and ventral surfaces of thighs areolate, those of shanks smooth. Cloacal opening directed posteriorly at upper level of thighs, round tubercles below and of vent. Tongue slightly cordiform, widely attached to mouth floor; vomerine odontophores conic-shaped, separated medially, behind level of ovoid choana; each bearing 3–5 vomerine teeth. Additional measurements of the holotype are listed in Table 3.

Table 3.
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Descriptive statistics for measurements of Hyloscirtus hillisi sp. n. Abbreviations: SVL = snout-vent length; FL = foot length; HL = head length; HW = head width; ED = eye diameter; TD = tympanum diameter; TL = tibia length; FEL = femur length. All measurements in mm.

Adult female (holotype) Adult males (n = 3) Subadult females (n = 2) Juveniles (n = 1)
SVL 65.8 70.3 ± 3.1 (66.7–72.3) 48.6–56.8 40.2
FL 29.9 30.3 ± 0.1 (30.1–30.4) 21.4–27.6 17.6
HL 14.9 14.3 ± 2.7 (11.4–16.6) 11.9–12.9 9.4
HW 22.7 24.5 ± 0.9 (23.7–25.5) 18.4–20.5 13.1
ED 6.3 6.5 ± 0.1 (6.4–6.6) 5.1–5.2 5.4
TD 3.4 4.3 ± 0.2 (4.1–4.3) 2.9–3.2 2.1
TL 32.3 33.9 ± 0.6 (33.4–34.6) 25.6–28.1 21.2
FEL 35.2 35.9 ± 1.7 (34.3–37.7) 25.7–32.36 20.9

Color of holotype in preservative

(Figure 6). Dorsal surfaces of head, body, and limbs, including fingers, dark grayish-brown densely stippled with minute, cream flecks. Ventral surfaces of limbs and belly grayish-brown, ventral surfaces of discs, webbing, chest, and throat paler.

Color of holotype in life

(Figure 5A). Based on digital photographs. Dorsal surfaces same as above except that flecks are bright orange. Ventral surfaces are dark grayish-brown. Ventral pads of digital discs on fingers and toes are gray. Iris is yellowish-cream.

Variation

Dorsal and ventral variation of preserved individuals is depicted in Figure 6. Morphometric variation is shown in Table 3. In preservative, dorsum varies from dark grayish-brown (e.g., QCAZ 68646) in adults to pale grayish-brown (e.g., QCAZ 68647, 68650) or pale gray (e.g., QCAZ 68648) in juveniles and metamorphs. Scattered minutes cream flecks can be present on dorsal surfaces (e.g., QCAZ 68646, 68647). Specimen QCAZ 68647 (juvenile) has cream transverse bars on the dorsal surfaces of the limbs (two to four on the forearm and five to seven on the thigh, shank, and foot). Ventral surfaces vary from pale grayish-brown (e.g., QCAZ 68646) to pale brown or cream (e.g., QCAZ 68648, 68650). Coloration of webbing and discs vary from dark grayish-brown to pale grayish-brown or gray.

In life, (Figure 5), the adult specimens are very similar to the holotype except for the density of bright orange flecks (bright yellow in situ; Figure 11A) on the dorsal surfaces. Background dorsal coloration in juveniles and metamorphs (Figure 8) varies from mottled or uniformly brown (e.g., SC 59268, QCAZ 68650) to light brown (e.g., QCAZ 68648) with or without orange-brown transversal bars on the dorsal surfaces of the limbs. Ventral surfaces vary from dark grayish-brown to cream (e.g., SC 59268). Iris varies from bronze (e.g., SC 59268) to yellowish-cream (e.g., QCAZ 68648).

Figure 8. 

Color variation in life of juvenile and metamorphs of Hyloscirtus hillisi sp. n. A SC 59268 (SVL = 39.52 mm, not preserved) BQCAZ 68648 (SVL = 35.6 mm) CQCAZ 68650 (SVL = 40.73 mm).

Tadpole description

The following description is based on a tadpole of series QCAZ 68651 in Stage 25 (Gosner 1960). The specimen was collected in a slow-moving pool along the margins of a stream (Figure 9; 3.5187S, 78.3919W; 1991 m) at the type locality on 7 July 2017. All measurements are in mm. Total length 86.7; body length 29.1 (33.6% of total length). Body ovoid and depressed; width at the level of spiracle 19.2, height at same position 14.7; head width at level of the eyes 17.9; anterior margin of snout uniformly rounded in dorsal view and sloping at level of nares in lateral view; lateral-line system evident with supraorbital, infraorbital, mandibular, angular, postorbital, dorsal body, and ventral body lines. The arrangement of the lateral-line system is symmetrical; the supra and infra orbital lines begin at the tip of the snout and join behind the eye, continuing as a single longitudinal line extending along the anterior half of the tail. The dorsal lines extend along the posterior half of the dorsum until reaching the anterior edge of the tail, at the base of the upper fin. The angular line starts behind the orbit and extends longitudinally, contouring the spiracle, to the posterior end of the body, down towards the venter and ending at the base of the vent tube. The postorbital line starts behind the intersection of the supra and infraorbital lines and continues obliquely towards the venter, joining the anteroventral line. The mandibular line originates at the lateral border of the oral disc and runs obliquely until joining the anteroventral line. The posteroventral line forms a V whose vertex is directed towards the midposterior venter ending at the lateral edge of the venter, at the base of the spiracle. The nostrils are ovoid, not protruding and directed anterolaterally, 6.8 from tip of snout; internarial distance 8.6. Eyes positioned and directed dorsolaterally; eye length 2.8, eye width 2.5; interorbital distance 9.9. Spiracle sinistral, located at midbody and oriented posterodorsally, inner wall free from body; tube length 2.8, tube width 2.6; spiracular opening directed posterodorsally, diameter 1.6; distance from tip of snout to spiracular opening 22.5. Vent tube medial, opening directed posteriorly; tube length 3.8, tube width 2.6. Tail length 57.5; caudal musculature robust, narrowing gradually until tail terminus. At tail-body junction, tail muscle width 9.6, tail muscle height 11.7; maximum height of tail 17.7. Oral disc located anteroventrally; transverse width 11.6; bordered by two rows of small and rounded papillae; upper jaw sheath forming an arch, unpigmented, transverse width including lateral processes 4.0 (34.4% of transverse width of oral disc); oral apparatus well preserved, showing complete teeth rows. Labial tooth row formula 8(8)/11(1). Only A-8 and P-1 have gaps. Tadpoles were gregarious and fled to the bottom of the pool when disturbed.

Figure 9. 

Variation in life of tadpoles of Hyloscirtus hillisi sp. n. AQCAZ 68651 (photograph taken 5 days after capture on 19 July 2017) BQCAZ 71182 (photograph taken 16 days after capture, on 20 July 2017) CQCAZ 71182 (photograph taken 8 months and 4 days after capture on 08 March 2018). Note change in color between (B) and (C). Gosner Stage 25. Photographs by Gustavo Pazmiño.

Color in preservative of tadpoles

In dorsal view, the body is gray, lighter on the tip of snout and towards the base of the tail, grayish cream belly, mouth cream; tail musculature grayish cream with irregular gray spots, upper and lower fins transparent, light gray with irregular dark gray spots.

Color in life of tadpoles

In dorsal view, body brown, including head and snout; in lateral view body dark-brown. Small bronze dots concentrate in the anterior edge of the eye, become diffuse at level of the base of the spiracle. Venter cream, becoming darker medially as result of intestines being dimly visible; oral disc light brown becoming dark brown posteriorly. Iris bronze. Vent tube cream. Muscle tail light brown with gray irregular spots; lower fin transparent cream with a combination of brown and gray irregular spots; upper fin transparent light brown with light brown spots and few scattered dark gray spots. The brown coloration and the pattern of dark gray and brown spots in several individuals is maintained; however, an individual kept in captivity (QCAZ 71182) during 8 months presents an evident change in its coloration, becoming much clearer with a combination of light brown on the back and greenish brown on the flanks; muscles of tail light brown with gray spots; lower fin cream with brown spots, upper fin greenish cream becoming transparent in the distal third with dark brown spots. The differences in coloration after 8 months in captivity may be due to the effects of diet.

Tadpoles variation

Based on a series of five individuals in stage 25 and two in stages 37 and 40. Meristic variation of tadpoles in Stages 25–40 is shown in Table 4. Seven tadpoles in Stages 25–40 varied in total length, ranging from 57.4 to 101 mm; body length ranged from 20.4 to 34.2 mm; tail length ranged from 37.0 to 67.6 mm. Inter orbital distance from 6.27 to 10.43 mm. Labial tooth row formula varied from 8(8)/11(1) to 7(7)/12(1) (Figure 10).

Table 4.
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Measurements (in mm) of tadpoles of Hyloscirtus hillisi sp. n. Mean ± SD is given with range in parentheses. Abbreviations: TL (total length), BL (body length), TAL (tail length), TAL/TL (ratio tail length/total length), MHT (Maximum Height of Tail, including dorsal and ventral fins), IOD (inter orbital distance), WOD (transverse width of oral disc), WUJ (transverse width of upper jaw sheath, including lateral processes), WUJ/WOD (ratio width of upper jaw sheath/width of oral disc), TUW (tube transverse width), TUL (tube length spiracle).

Character Stage 25 (n = 5) Stage 37 (n = 1) Stage 40 (n = 1)
TL 79.2 ± 12.4 (57.4–86.7) 99.5 101
BL 26.1 ± 3.6 (20.4–29.1) 34.2 33.4
TAL 53 ± 9.02 (37–58) 65.3 67.6
TAL/TL 0.7 ± 0.04 (0.6–0.7) 0.7 0.7
MHT 15.4 ± 1.7 (13.7–17.7) 19 19.4
IOD 8.4 ± 1.5 (6.3–9.9) 10.2 10.4
WOD 9.3 ± 1.7 (7–11.6) 11.7 11.7
WUJ 3.9 ± 0.1 (3.8–4) 5.2 5.5
WUJ/WOD 2.8 ± 0.4 (2.3–3.3) 2.2 2.1
TUW 1.9 ± 0.5 (1.4–2.6) 2.7 3.6
TUL 2.4 ± 0.4 (1.7–2.8) 3.2 4.3
Figure 10. 

Oral disc of preserved tadpole of Hyloscirtus hillisi sp. n. QCAZ 68651, Gosner Stage 25. Photograph by Gustavo Pazmiño.

Etymology

The specific name is a noun in the genitive case and is a patronym for David Hillis, an evolutionary biologist who has made significant contributions to the study of the evolution of amphibians and reptiles. During the 1980s, David Hillis carried out fieldwork in Ecuador that resulted in the discovery of three undescribed species of the H. larinopygion group. In 1990, in collaboration with WE Duellman, he published the first phylogeny for the H. larinopygion group using allozyme data (Duellman and Hillis 1990). Currently he is professor at the University of Texas in Austin.

Distribution and natural history

Hyloscirtus hillisi is only known from two nearby sites (airline distance = 1.7 km) on the slopes of a flattop limestone mountain in the Río Quimi basin, Provincia Zamora Chinchipe, at elevations between 1991 and 2134 m (Figure 2). Biogeographic region is Eastern Montane Forest according to Ron et al. (2018) classification. Vegetation at the type locality (Figure 11B, C) was dominated by shrubs (1.5 m tall) with sparse trees (10–15 m tall). The ground had cushioned consistency and was covered by roots and bare soil. Mosses and ground-bromeliads were abundant. This type of ground cover is locally known as bamba. Two adults and one juvenile were found on shrubs next to small streams on the Río Cristalino basin, at an elevation of 2134 m. The tadpoles and juveniles were found in ponds on the margin of Río Cristalino, at an elevation of 1991 m (Figure 11D). Collections took place in July 2017 and April 2018. The site where the adults were collected is ~500 m from the border between Peru and Ecuador. Therefore, the occurrence of H. hillisi in Peru is almost certain.

Figure 11. 

Habitat of Hyloscirtus hillisi sp. n. A Hyloscirtus hillisi sp. n. in situB vegetation at the type locality, Reserva Biológica El Quimi, Ecuador C habitat where the adults were found D habitat where the tadpoles and metamorphs were found. Photographs by Diego Almeida.

Conservation status

Hyloscirtus hillisi is only known from two nearby sites in Cordillera del Cóndor. Population size is unknown, but the scant evidence suggests low abundances. In 2017, at the site where the tadpoles and juveniles were found, five hours of nocturnal search by five experienced herpetologists yielded no adults. At the site where the adults were found, ten hours of nocturnal search, for two nights, by two experienced herpetologists, yielded two adults and one subadult. Habitat destruction and fragmentation is evident at a distance of 3.5 km from one of the collection sites (according to Ministerio de Ambiente del Ecuador 2013 map). Cordillera del Cóndor is threatened by large and small-scale mining which has already affected amphibian populations (Valencia et al. 2017). Because of its small known distribution and nearby habitat destruction and mining activities, we suggest to assign H. hillisi to the Critically Endangered category under criteria B1a, b(iii), according to IUCN (2001) guidelines.

Discussion

Our phylogeny is consistent with previous phylogenies of Hyloscirtus (e.g., Almendáriz et al. 2014; Coloma et al. 2012; Faivovich et al. 2005; Rojas-Runjaic et al. 2018). The sister clade of the H. larinopygion group appears to be the H. armatus group (e.g., Rojas-Runjaic et al. 2018, Duellman et al. 2016, herein). A close relationship between the H. armatus group and H. larinopygion group is also supported by the shared presence of an enlarged prepollex protruding as a spine in the H. armatus group and in the Southern Clade of the H. larinopygion group. Under Duellman et al. (2016) topology, the absence of the spine in the Northern Clade would result from a secondary loss.

Hyloscirtus hillisi is the second species of the Hyloscirtus larinopygion group to be discovered in Cordillera del Cóndor, a sub-Andean mountain chain with unique geology. While the main Andes are composed of igneous and metamorphic rocks, Cordillera del Cóndor is composed predominantly by sedimentary rocks, specially limestone and sandstone (Neill 2005). Although much younger, Cordillera del Cóndor is geologically similar to the Tepuis in the Guianan region. Remarkably, surveys of the plant communities of Cordillera del Cóndor have recorded at least 10 genera that otherwise are endemic or nearly endemic to the Guianan Tepuis (Ulloa and Neill 2006).

The biogeographic affinity between the biotas of Cordillera del Cóndor and the Guianan Tepuis can be tested with phylogenies. Close relationships between biotas from El Cóndor and the Guianan Tepuis are expected under that biogeographic scenario. However, a review of recently published phylogenies is inconsistent with a Cóndor-Guianan link. Our phylogeny, for example, shows that both species of Hyloscirtus from el Cóndor are closely related to Andean species from southern Ecuador and northern Peru. Similar results are evident in Pristimantis muranunka (closely related to Pristimantis from the Andes of southern Ecuador; Brito et al. 2017), Pristimantis yantzaza (closely related to Pristimantis from the Andes and adjacent Amazonian lowlands of Peru and Ecuador; Valencia et al. 2017), Excidobates condor (closely related to Excidobates from Cordillera del Cóndor and adjacent Amazonian lowlands; Almendáriz et al. 2012), Centrolene condor (sister to a large clade of Centrolene with species from the Andes of Venezuela, Colombia, Ecuador and Peru; Castroviejo‐Fisher et al. 2014), and Chiasmocleis parkeri (closely related to Chiasmocleis from the Amazonian lowlands; Almendáriz et al. 2017). The combined evidence indicates that the biogeographic link between Cordillera del Cóndor and the Tepui region is not discernable in amphibians.

We suspect that the difference in biogeographic pattern observed between plants and amphibians may result from differences in the ecological factors that influence their geographic distribution. In plants, a key factor is soil type (e.g., Clark et al. 1999). The similarity in soil type between Cordillera del Cóndor and the Tepui region (Neill 2005) may explain the biogeographic connection observed in plants. In amphibians, in contrast, edaphic conditions appear to be of minor importance explaining the lack of biogeographic affinity between both regions.

As result of its historic inaccessibility, the organismal diversity of Cordillera del Cóndor is poorly known. During the last two decades, after armed conflicts between Ecuador and Peru ended, roads began to be built and biodiversity surveys became more frequent. These surveys have revealed a large number of unknown species of amphibians, several of which have been recently described (e.g., Almendáriz et al. 2014; Almendáriz et al. 2017; Almendáriz et al. 2012; Almendáriz et al. 2014; Brito et al. 2017; Brito et al. 2014; Terán-Valdez and Guayasamín 2010; Valencia et al. 2017). Additional expeditions to Cordillera del Cóndor are likely to result in more discoveries since it remains largely unexplored.

Acknowledgments

Field and laboratory work in Ecuador were funded by grants from Secretaría Nacional de Educación Superior, Ciencia, Tecnología e Innovación (SENESCYT, Arca de Noé Initiative; Omar Torres and SRR principal investigators) and PUCE-DGA (SRR principal investigator). Ana Carrillo and Claudia Terán carried out laboratory work. Fernando Rojas-Runjaic provided early access to unpublished sequences of Hyloscirtus. Gustavo Pazmiño and Valeria Chasiluisa helped making photographs of preserved specimens. Karla García-Burneo provided photographs of H. diabolus. For field assistance we thank María del Mar Moretta, Darwin Núñez, Kunam Nucirquia, Alex Achig, and Ricardo Gavilanes. Ministerio de Ambiente del Ecuador issued collecting permit 003-17-IC-FAU-DNB/MA. The park rangers fro Ministerio de Ambiente del Ecuador, Morona Santiago Province, provided field assistance.

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Appendix 1

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Examined specimens. All specimens were collected in Ecuador and are deposited at the Museum of Zoology, Pontificia Universidad Católica del Ecuador (QCAZ).

Species Museum Number Province Locality
Hyloscirtus condor QCAZ 65235 Zamora Chinchipe Reserva Biológica Cerro Plateado, 2200 m; 4.6045S, 78.8227W
H. condor QCAZ 65236 Zamora Chinchipe Reserva Biológica Cerro Plateado, 2243 m; 4.6044S, 78.8226W
H. condor QCAZ 65237 Zamora Chinchipe Reserva Biológica Cerro Plateado, 2219 m; 4.6044S, 78.8238W
H. condor QCAZ 65240 Zamora Chinchipe Reserva Biológica Cerro Plateado, 2320 m; 4.6050S, 78.8166W
H. condor QCAZ 65241 Zamora Chinchipe Reserva Biológica Cerro Plateado, 2320 m; 4.6050S, 78.8166W
H. criptico QCAZ 4161 Carchi 22 km E Maldonado, Maldonado-Tulcán Road, 2560 m; 0.8301N, 78.0456W
H. criptico QCAZ 4168 Carchi 22 km E Maldonado, Maldonado-Tulcán Road, 2560 m; 0.8301N, 78.0456W
H. criptico QCAZ 4169 Carchi 22 km E Maldonado, Maldonado-Tulcán Road, 2560 m; 0.8301N, 78.0456W
H. criptico QCAZ 4170 Carchi 22 km E Maldonado, Maldonado-Tulcán Road, 2560 m; 0.8301N, 78.0456W
H. criptico QCAZ 10487 Imbabura Cuellaje, 1813 m; 0.4N, 78.525W
H. criptico QCAZ 11989 Carchi 22 km E Maldonado, Maldonado-Tulcán Road, 2560 m; 0.8260N, 78.0420W
H. criptico QCAZ 41467 Imbabura Seis de Julio de Cuellaje, 2800 m; 0.3968N, 78.5273W
H. criptico QCAZ 42149 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 42150 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 42152 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 42153 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 42156 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 42157 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 42168 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 43421 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2560 m; 0.4747N, 78.5550W
H. criptico QCAZ 43422 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2560 m; 0.4747N, 78.5550W
H. criptico QCAZ 43500 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2794 m; 0.4732N, 78.5702W
H. criptico QCAZ 43503 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2830 m; 0.4758N, 78.5679W
H. criptico QCAZ 43516 Imbabura Cuellaje, San Antonio, 2760 m; 0.4724N, 78.5660W
H. criptico QCAZ 43517 Imbabura Cuellaje, San Antonio, 2760 m; 0.4724N, 78.5660W
H. criptico QCAZ 43518 Imbabura Cuellaje, San Antonio, 2765 m; 0.4724N, 78.5660W
H. criptico QCAZ 43528 Imbabura Cuellaje, San Antonio, 2885 m; 0.4724N, 78.5660W
H. criptico QCAZ 44894 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 44895 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 45466 Carchi Tulcán-Maldonado Road, Quebrada Centella, 2806 m; 0.8179N, 78.016W
H. criptico QCAZ 50320 Imbabura Seis de Julio de Cuellaje, 1858 m; 0.3968N, 78.5273W
H. criptico QCAZ 57951 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. criptico QCAZ 57952 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2720 m; 0.4775N, 78.5626W
H. larinopygion QCAZ 29211 Carchi 24 km Maldonado, Tulcán Road, 2664 m; 0.8231N, 78.0253W
H. larinopygion QCAZ 29212 Carchi 24 km Maldonado, Tulcán Road, 2664 m; 0.8231N, 78.0253W
H. larinopygion QCAZ 38418 Carchi Cerro Centella, Tulcán-Maldonado Road, 2788 m; 0.8143N, 78.0149W
H. larinopygion QCAZ 41826 Carchi Cañón de Morán, 2452 m; 0.7467N, 78.1038W
H. larinopygion QCAZ 45462 Carchi Tulcán-Tufiño-Maldonado Road, Quebrada Centella, 2806 m; 0.8179N, 78.0160W
H. larinopygion QCAZ 55574 Carchi Morán, 2800 m; 0.7729N, 78.0559W
H. larinopygion QCAZ 55575 Carchi Morán, 2800 m; 0.7729N, 78.0559W
H. lindae QCAZ 7593 Napo 10 Km E Oyacachi, 2510 m; 0.2322S, 78.0072W
H. lindae QCAZ 10483 Napo Oyacachi, 3217 m; 0.2128S, 78.0876W
H. lindae QCAZ 41232 Napo Pacto Sumaco, Parque Nacional Sumaco, 2479 m; 0.5696S, 77.5941W
H. lindae QCAZ 41294 Napo Pacto Sumaco, Pabayacu, 2775 m; 0.5639S, 77.6154W
H. lindae QCAZ 41295 Napo Pacto Sumaco, Pabayacu, 2775 m; 0.5639S, 77.6154W
H. lindae QCAZ 41296 Napo Pacto Sumaco, Pabayacu, 2775 m; 0.5639S, 77.6154W
H. lindae QCAZ 41297 Napo Pacto Sumaco, Pabayacu, 2775 m; 0.5639S, 77.6154W
H. lindae QCAZ 41298 Napo Pacto Sumaco, Pabayacu, 2775 m; 0.5639S, 77.6154W
H. lindae QCAZ 45342 Napo 11-12 km E Papallacta, 2700 m; 0.3884S, 78.0605W5W
H. lindae QCAZ 45345 Napo Papallacta, Papallacta-Cuyuja Road, 2600 m; 0.3884S, 78.0605W
H. lindae QCAZ 45346 Napo Papallacta, Papallacta-Cuyuja Road, 2600 m; 0.3884S, 78.0605W
H. lindae QCAZ 45463 Sucumbíos 11 km S Santa Bárbara, La Bonita Road, 2341 m; 0.6159N, 77.4879W
H. pacha QCAZ 10489 Morona Santiago Gualaceo-Limón Road, 2120 m; 3.0310S, 78.5270W
H. pacha QCAZ 48237 Morona Santiago Plan de Milagro, 8 km Plan de Milagro, 2152 m; 3.0011S, 78.5052W
H. pacha QCAZ 48238 Morona Santiago Plan de Milagro, 9 km Plan de Milagro, 2300 m; 3.0079S, 78.5253W
H. pacha QCAZ 48239 Morona Santiago Plan de Milagro, 9 km Cuenca Road, 2300 m; 3.0079S, 78.5253W
H. pacha QCAZ 48240 Morona Santiago Plan de Milagro, 9 km Cuenca Road, 2300 m; 3.0079S, 78.5253W
H. pacha QCAZ 48241 Morona Santiago Plan de Milagro, 9 km Plan de Milagro, 2300 m; 3.0079S, 78.5253W
H. pacha QCAZ 57944 Morona Santiago Limón Indanza, 2300 m; 3.0079S, 78.5253W
H. pantostictus QCAZ 731 Sucumbíos 3.5 km Santa Bárbara-La Bonita Road, 2690 m; 0.6490N, 77.5040W
H. pantostictus QCAZ 2721 Sucumbíos 6.1 km Santa Bárbara-La Bonita Road, 2760 m; 0.6410N, 77.4989W
H. pantostictus QCAZ 3753 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 4505 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 4506 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 6596 Sucumbíos Santa Bárbara, 2710 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 10661 Sucumbíos Santa Bárbara, 2700 m; 0.64373N, 77.5257W
H. pantostictus QCAZ 10671 Sucumbíos Santa Bárbara, 2700 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 11660 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 11661 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 11662 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 11663 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 11664 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 11665 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 11666 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 11667 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 12171 Sucumbíos Santa Bárbara, 2800 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 14084 Sucumbíos Santa Bárbara, 2710 m; 0.6415N, 77.5218W
H. pantostictus QCAZ 30529 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 30530 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 30531 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 42350 Sucumbíos Santa Bárbara, 2709 m; 0.6445N, 77.5228W
H. pantostictus QCAZ 45435 Sucumbíos Santa Bárbara, 2709 m; 0.6444N, 77.5522W
H. pantostictus QCAZ 45438 Sucumbíos Santa Bárbara, 2656 m; 0.6437N, 77.5257W
H. pantostictus QCAZ 45440 Sucumbíos Santa Bárbara, 2586 m; 0.6436N, 77.5323W
H. pantostictus QCAZ 45449 Sucumbíos Santa Bárbara, Quebrada Santa Bárbara, La Bonita, 2341 m; 0.6159N, 77.4879W
H. pantostictus QCAZ 46587 Sucumbíos 3 km Santa Bárbara, 2600 m; 0.6328N, 77.5231W
H. pantostictus QCAZ 46588 Sucumbíos 3 km Santa Bárbara, 2600 m; 0.6328N, 77.5231W
H. princecharlesi QCAZ 41465 Imbabura Seis de Julio de Cuellaje, 2800 m; 0.3968N, 78.5273W
H. princecharlesi QCAZ 41466 Imbabura Seis de Julio de Cuellaje, 2800 m; 0.3968N, 78.5273W
H. princecharlesi QCAZ 42165 Imbabura Cuellaje, San Antonio, 2720 m; 0.4775N, 78.5626W
H. princecharlesi QCAZ 43654 Imbabura Cuellaje, San Antonio, 2760 m; 0.4724N, 78.5660W
H. princecharlesi QCAZ 44893 Imbabura Cuellaje, San Antonio, Reserva Ecológica Cotacachi Cayapas, 2794 m; 0.4732N, 78.5702W
H. psarolaimus QCAZ 13252 Napo 11 km SE Papallacta, 2800 m; 0.3870S, 78.0600W
H. psarolaimus QCAZ 27049 Sucumbíos Santa Bárbara, 0.8 km Julio Andrade Road, 2600 m; 0.6422N, 77.5264W
H. psarolaimus QCAZ 31671 Morona Santiago San Vicente, Parque Nacional Sangay, 15 km Lagunas de Atillo, 2815 m; 2.2102S, 78.4487W
H. psarolaimus QCAZ 46095 Napo 60 km E Salcedo, 2748 m; 0.9709S, 78.2413W
H. psarolaimus QCAZ 46096 Napo 60 km E Salcedo, 2748 m; 0.9709S, 78.2413W
H. psarolaimus QCAZ 46097 Napo 60 km E Salcedo, 2748 m; 0.9709S, 78.2413W
H. psarolaimus QCAZ 46098 Napo 60 km E Salcedo, 2748 m; 0.9709S, 78.2413W
H. pantostictus QCAZ 46808 Sucumbíos Santa Bárbara, El Corazón, 2670 m; 0.6437N, 77.5321W
H. pantostictus QCAZ 46811 Sucumbíos Santa Bárbara, 2589 m; 0.6437N, 77.5321W
H. psarolaimus QCAZ 46890 Napo Salcedo-Tena Road, km 60, 2748 m; 0.9719S, 78.2413W
H. pantostictus QCAZ 46894 Sucumbíos Santa Bárbara, 2709 m; 0.6445N, 77.5522W
H. pantostictus QCAZ 46896 Sucumbíos Santa Bárbara, 2709 m; 0.6445N, 77.5522W
H. pantostictus QCAZ 46929 Sucumbíos Santa Bárbara, 2709 m; 0.6445N, 77.5228W
H. pantostictus QCAZ 50358 Sucumbíos Santa Bárbara, 2589 m; 0.6437N, 77.5321W
H. pantostictus QCAZ 50389 Sucumbíos Santa Bárbara, 2589 m; 0.6437N, 77.5321W
H. pantostictus QCAZ 50390 Sucumbíos Santa Bárbara, 2586 m; 0.6436N, 77.5323W
H. pantostictus QCAZ 50415 Sucumbíos Santa Bárbara, 2709 m; 0.6445N, 77.5228W
H. psarolaimus QCAZ 66563 Pastaza Reserva Comunitaria Ankaku, Parque Nacional Llanganates, 2165 m; 1.2752S, 78.0657W
H. psarolaimus QCAZ 66564 Pastaza Reserva Comunitaria Ankaku, Parque Nacional Llanganates, 2315 m; 1.2764S, 78.0759W
H. psarolaimus QCAZ 66565 Pastaza Reserva Comunitaria Ankaku, Parque Nacional Llanganates, 2334 m; 1.2771S, 78.0768W
H. psarolaimus QCAZ 66566 Pastaza Reserva Comunitaria Ankaku, Parque Nacional Llanganates, 2322 m; 1.2767S, 78.0763W
H. psarolaimus QCAZ 66568 Pastaza Reserva Comunitaria Ankaku, Parque Nacional Llanganates, 2216 m; 1.2770S, 78.0698W
H. ptychodactylus QCAZ 46030 Cotopaxi Pilaló, Quebrada 2, 2500 m; 0.9424S, 78.9956W
H. ptychodactylus QCAZ 46031 Cotopaxi Pilaló, Quebrada 2, 2500 m; 0.9424S, 78.9956W
H. staufferorum QCAZ 3701 Napo Volcán Sumaco, Lago Sumaco, 2463 m; 0.5689S, 77.5948W
H. staufferorum QCAZ 3704 Napo Codillera de Guacamayos, 31 km Baeza, Archidona Road, 2210 m; 0.6505S, 77.7907W
H. staufferorum QCAZ 3705 Napo Baeza, 2040 m; 0.4634S, 77.8915W
H. staufferorum QCAZ 3706 Napo Baeza, 2040 m; 0.4634S, 77.8915W
H. staufferorum QCAZ 11150 Napo 13.4 km S Río Cosanga, 2040 m; 0.6560S, 77.9129W
H. staufferorum QCAZ 36278 Napo Volcán Sumaco, Lago Sumaco, 2470 m; 0.5689S, 77.5948W
H. staufferorum QCAZ 36279 Napo Volcán Sumaco, Lago Sumaco, 2470 m; 0.5689S, 77.5948W
H. staufferorum QCAZ 45962 Pastaza Reserva Comunitaria Ankaku, Río Challuwa Yacu, Parque Nacional Llanganates, 2250 m; 1.2792S, 78.0779W
H. staufferorum QCAZ 45963 Pastaza Reserva Comunitaria Ankaku, Río Challuwa Yacu, Parque Nacional Llanganates, 2250 m; 1.2792S, 78.0779W
H. staufferorum QCAZ 45965 Pastaza Reserva Comunitaria Ankaku, Río Challuwa Yacu, Parque Nacional Llanganates, 2250 m; 1.2792S, 78.0779W
H. staufferorum QCAZ 45966 Pastaza Reserva Comunitaria Ankaku, Río Challuwa Yacu, Parque Nacional Llanganates, 2250 m; 1.2792S, 78.0779W
H. staufferorum QCAZ 45967 Pastaza Reserva Comunitaria Ankaku, Río Challuwa Yacu, Parque Nacional Llanganates, 2250 m; 1.2792S, 78.0779W
H. staufferorum QCAZ 56807 Pastaza Reserva Comunitaria Ankaku, Río Challuwa Yacu, Parque Nacional Llanganates, 2250 m; 1.2792S, 78.0779W
H. staufferorum QCAZ 64480 Pastaza Reserva Comunitaria Ankaku, Río Challuwa Yacu, Parque Nacional Llanganates, 2250 m; 1.2792S, 78.0779W
H. staufferorum QCAZ 66567 Pastaza Reserva Comunitaria Ankaku, Parque Nacional Llanganates, 2434 m; 1.2799S, 78.0826W
H. tapichalaca QCAZ 15083 Zamora Chinchipe Yangana-Valladolid Road, Reserva Tapichalaca, 2625 m; 4.4816S, 79.1491W
H. tapichalaca QCAZ 15084 Zamora Chinchipe Yangana-Valladolid Road, Reserva Tapichalaca, 2625 m; 4.4816S, 79.1491W
H. tapichalaca QCAZ 15085 Zamora Chinchipe Yangana-Valladolid Road, Reserva Tapichalaca, 2625 m; 4.4816S, 79.1491W
H. tapichalaca QCAZ 16704 Zamora Chinchipe Yangana-Valladolid Road, Reserva Tapichalaca, 2697 m; 4.4816S, 79.1491W
H. tapichalaca QCAZ 16705 Zamora Chinchipe Yangana-Valladolid Road, Reserva Tapichalaca, 2697 m; 4.4816S, 79.1491W
H. tapichalaca QCAZ 16706 Zamora Chinchipe Yangana-Valladolid Road, Reserva Tapichalaca, 2697 m; 4.4816S, 79.1491W
H. tapichalaca QCAZ 17776 Zamora Chinchipe Yangana-Valladolid Road, Reserva Tapichalaca, 2697 m; 4.4816S, 79.1491W
H. tapichalaca QCAZ 17777 Zamora Chinchipe Yangana-Valladolid Road, Reserva Tapichalaca, 2697 m; 4.4816S, 79.1491W
H. tapichalaca QCAZ 46887 Zamora Chinchipe Reserva Tapichalaca, 1637 m; 4.4730S, 79.1930W
H. tapichalaca QCAZ 63872 Zamora Chinchipe Parque Nacional Podocarpus, Tapichalaca, 2605 m; 4.4876S, 79.1479W
H. tigrinus QCAZ 31550 Sucumbíos Santa Bárbara, El Corazón, 2620 m; 0.6437N, 77.5321W
H. tigrinus QCAZ 40331 Sucumbíos Santa Bárbara, 2638 m; 0.6437N, 77.5321W
H. tigrinus QCAZ 41351 Sucumbíos 0.7 km SW Santa Bárbara, Quebrada El Corazón, 2638 m; 0.6437N, 77.5321W
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