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Taxonomy of Hypsiboas crepitans

Available at http://www.salamandra-journal.com© 2017 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany

SALAMANDRA 53(1) 99–113 15 February 2017 ISSN 0036–3375

Integrative taxonomy supports the existence of two distinct species within Hypsiboas crepitans (Anura: Hylidae)

Victor G. D. Orrico1, Ivan Nunes2,9, Camila Mattedi2, Antoine Fouquet3, Arthur W. Lemos2, Maurício Rivera-Correa4, Mariana L. Lyra5, Daniel Loebmann6, Bruno V. S. Pimenta7,

Ulisses Caramaschi2, Miguel T. Rodrigues8 & Célio F. B. Haddad5

1) Universidade Estadual de Santa Cruz, Departamento de Ciências Biológicas, Rodovia Jorge Amado, Km 16. CEP 45662-900 Ilhéus, BA, Brazil

2) Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Vertebrados. Quinta da Boa Vista, São Cristóvão. CEP 20940-040, Rio de Janeiro, RJ, Brazil

3) CNRS-Guyane, USR 3456 LEEISA – Laboratoire Ecologie, Evolution Interactions des Systèmes Amazoniens, Centre de recherche de Montabo 275 route de Montabo, BP 70620. 97334, Cayenne cedex, French Guiana

4) Pontifícia Universidade Católica do Rio Grande do Sul, Faculdade de Biociências, Laboratório de Sistemática de Vertebrados. Av. Ipiranga 6681. CEP 90619-900, Porto Alegre, RS, Brazil

5) Universidade Estadual Paulista (UNESP), Instituto de Biociências, Departamento de Zoologia and Centro de Aquicultura da UNESP – CAUNESP, campus Rio Claro, Av. 24A, N 1515. CEP 13506-900, Rio Claro, SP, Brazil

6) Universidade Federal do Rio Grande, Instituto de Ciências Biológicas, Laboratório de Vertebrados, Av. Itália Km 8, Carreiros. CEP 96.203-900, Rio Grande, RS, Brazil

7) Bicho do Mato Meio Ambiente Ltda. / Bicho do Mato Instituto de Pesquisa. Rua Perdigão Malheiros 222. CEP 30380-234, Belo Horizonte, MG, Brazil

8) Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461. CEP 05508-090, São Paulo, SP, Brazil

9) Present address: Universidade Estadual Paulista, Campus do Litoral Paulista, Instituto de Biociências, Laboratório de Herpetologia. Praça Infante Dom Henrique, s/n, Parque Bitarú. CEP 11.330-900, São Vicente, SP, Brazil

Corresponding author: Antoine Fouquet, e-mail: [email protected]

Manuscript received: 10 February 2016Accepted on 13 September 2016 by Jörn Köhler

Abstract. The Neotropical treefrog Hypsiboas crepitans (Wied, 1824) has an intriguing disjunct geographic distribution encompassing two large patches: the Atlantic Forest in southeastern South America and from the Guiana Shield to Cen-tral America in the north, that are separated by more than 1500 km. This distribution pattern led us to review the avail-able material and re-examine, under an integrative approach, the taxonomic status of these populations. We assessed data using three lines of evidence: morphology, morphometry, and mitochondrial DNA. All of them suggest that the popula-tions from the two geographical ranges are not conspecific. Given that the type material of H. crepitans is from the State of Bahia, Brazil, and that specimens from this area cluster with the southeastern group, we resurrect Hypsiboas xerophyllus (Duméril & Bibron, 1841) for the populations of the northwestern group. Hyla levaillantii Duméril & Bibron, 1841, Hyla doumercii Duméril & Bibron, 1841, Hyla fuentei Goin & Goin, 1968, and Hypsiboas indris Cope, 1867 are synonymized with H. xerophyllus.

Key words. Amphibia, Amazonia, Atlantic Forest, Hypsiboas faber species group, revalidation, South America, synonymy.

Introduction

The Hypsiboas faber species group was proposed by Faivo-vich et al. (2005) to accommodate a cluster of eight spe-cies: H. albomarginatus (Spix, 1824), H. crepitans (Wied, 1824), H. exastis (Caramaschi & Rodrigues, 2003), H. faber (Wied, 1821), H. lundii (Burmeister, 1856), H. pardalis (Spix, 1824), H. pugnax (Schmidt, 1857) and H. rosen

bergi (Boulenger, 1898). With the exception of H. albomarginatus (green, middle sized), all species are large, territorial tree frogs with a lichenous colour pattern, and rugose dorsal skin texture (Faivovich et al. 2005, Kluge 1979, Lynch & Suarez-Mayorga 2001).

One of the species of this group, Hypsiboas crepitans, exhibits an extensive and intriguing disjunct geographical distribution (Fig. 1). A southeastern group (hereafter SG)

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Victor G. D. Orrico et al.

of populations occurs along the Atlantic Forest and ad-jacent areas, including the State of Bahia in Brazil, from where the species was originally described (Wied 1824). The northwestern group (hereafter NG) of populations is distributed over the Guiana Shield, Caribbean (Tobago), Llanos, Andes, and Middle America (Panama), from sea level up to 2450 m a.s.l. (Duellman 1997, Frost 2014, Kluge 1979, Lehtinen 2014, Lynch & Suarez-Mayor-ga 2001). There is, thus, a > 1,500 km gap between the SG and the NG. This unusual disjunct distribution has raised doubts about the conspecificity of these groups of popu-lations (Casal & Juncá 2008, Duellman 1997, Kluge 1979, Lehtinen 2014, Lynch & Suarez-Mayorga 2001). Fouquet et al. (2007) found that the pairwise distance among 16S sequences of specimens from Alagoas, Brazil, and French Guiana was high enough to suggest the pres-ence of two distinct species. Lehtinen (2014) retrieved the same result comparing 16S sequences of specimens from Tobago and Brazil and suggested that the population stud-ied by Casal & Juncá (2008) from the State of Bahia “may represent a different, but currently undescribed, species”, not realizing that it could be the other way around given that this particular population is close to the type locality of H. crepitans (see below).

However, previous works on tadpoles and calls in both the NG and the SG provide only weak evidence support-ing the distinction. Tadpoles of the NG present a spiracle opening directed dorso-posteriorly, and antero-dorsal nos-trils (see Lynch 2006, figure 28), while tadpoles from the SG present a spiracle directed backwards, and dorsal nos-trils (Casal & Juncá 2008, figure 2). However, given the high plasticity of anuran larvae (e.g., Warketin 1999) we remain skeptical that these slight differences will be main-tained in larger samples. The basic structure of the calls of both groups is a periodic pulse train divided in one or some notes. The number of notes from the SG (2–5 notes: Casal & Juncá 2008, Martins et al. 2009) overlaps with the range of number of notes of NG from Panama (2–5 notes; Fouquette 1966, Duellman 1970, Kime et al. 2000) and from Colombia (1–2 notes; Bernal et al. 2004) (Table 1). The range of pulses per second from the SG (68–96; Casal & Juncá 2008, Martins et al. 2009) is slightly different from the value of NG recordings from Panamá (≈110; Duellman 1970). The dominant frequency range of SG recordings (0.53–1.3 kHz; Casal & Juncá 2008, Mar-tins et al. 2009) do not differ from the values recovered for the NG, although being individually lower than values found for NG specimens from Panama (0.96–2.55 kHz;

Figure 1. Map showing sampling localities of Hypsiboas crepitans (circles) and H. xerophyllus (triangles) specimens used in this study.

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Fouquette 1966, Duellman 1970, Kime et al. 2000), and higher than those found for Colombia (0.35 kHz; Bernal et al. 2004). Therefore, differences between the advertise-ment calls of specimens from the distinct groups are meag-er. However, Casal & Juncá (2008) used advertisement call data (dominant frequency mainly) to corroborate the hypothesis that more than one species is hidden under the name Hypsiboas crepitans. Therefore, although there is a suspicion that the two groups may represent distinct spe-cies, published data on advertisement calls and tadpoles are inconclusive in this respect.

The two groups of populations are separated by the Caatinga, Cerrado and Chaco biomes which are part of the “Dry Diagonal” of the Neotropics (Schmidt & Inger 1951, Werneck 2011), a group of “dry environments” pres-ently separating Atlantic and Amazonian Forests and to which some cladogenic events have been attributed (Cos-ta 2003). Successive fluctuations over time of these con-trasting habitats help to explain relationships and faunal exchanges between Amazonian and Atlantic Forests (see discussions in Fouquet et al. 2012, 2014). Most of the doc-umented dispersals of terrestrial anurans between these two biomes are rather ancient (Fouquet et al. 2012) and only a few examples of Atlantic Forest species like Rhinella hoogmoedi and Hypsiboas semilineatus are nested with relatively low genetic distances (1–3% on 16S) within oth-erwise Amazonian species (dos Santos et al. 2015, Fou-quet et al. 2016). However, no species of anuran restricted to forest habitats is known to be distributed in both biomes while it is the case in only a few open habitat species like Adenomera hylae dactyla (Fouquet et al. 2014).

Nevertheless, although Hypsiboas crepitans is predomi-nantly associated with forest and mesic habitats, many pop-ulations are found in dry or xeric environments. Lescure & Marty (2000) and Ouboter & Jairam (2012) reported that populations from French Guiana and Suriname, re-spectively, live in open environments such as in savannas and inselbergs surrounded by forest. In fact, the type local-ity of H. crepitans (Tamboril, Municipality of Condeúbas,

State of Bahia, Brazil, see Bokermann 1966) is situated in a transitional area between the rocky meadows of Serra do Espinhaço and the Caatinga where both open and forest vegetation are present. Therefore, the influence of the dry diagonal as a barrier for this species is not straightforward. Given these rather wide habitat requirements, a dispersal between Amazonia and the Atlantic Forest, recent enough to support a conspecific status of the two groups, cannot be excluded.

The goals of the present contribution are to review spec-imens assigned to Hypsiboas crepitans from both distribu-tion areas and perform analyses using an integrative ap-proach combining molecular (mtDNA), morphology and morphometry in order to evaluate the specific status of these populations.

If the existence of more than one species is supported, a number of synonyms are available for the NG and should therefore be examined. Additionally, Ouboter & Jairam (2012) also reported H. fuentei (Goin & Goin 1968), a spe-cies known only from three localities in northeast-central Suriname (Frost 2016), that are nested within the range of the NG. They also stated that they would “not be surprised, if H. fuentei proves to be a junior synonym of H. crepitans”. However, Hoogmoed (1979) suggested that because of the green colours of live specimens, H. fuentei seemed some-how related to H. punctatus or H. cinera scens – both today assigned to the H. punctatus species group. Neither Hoog-moed (1979) nor Ouboter & Jairam (2012) compared their specimens with the holotype of H. fuentei, solely with the description of Goin & Goin (1968). Although Faivo-vich et al. (2005) did not assign H. fuentei to any of their species groups, they state “the angulate dentigerous proc-ess of the vomer suggests that this species could be associ-ated with certain Gladiator Frogs... [that] have this charac-ter state. A study of the holotype … should clarify the mat-ter”. Given the confusion surrounding H. fuentei and the possible relation with H. crepitans, we include herein our own observations of the H. fuentei holotype and evaluate its taxonomic status.

Table 1. Advertisement call data for Hypsiboas crepitans distributional patches. See text for abbreviations.

OTU Call duration

(s)

Intercall interval

(s)

Number of notes per call

Number of pulses/

second

Note interval

(s)

Number of pulses/note

Pulse duration

(s)

Dominant frequency

(kHz)

Reference

NG – – 2–5 – – – – 2.55 Fouquette (1966)NG 2.5–5 – 3.3–4.4 110 – 3–5 0.009 0.965–1.288 Duellman (1970)NG – – 2–5 – – – – 2.15 Kime et al. (2000)NG 0.21–0.31 – 1–2 – – – – 0.35 Bernal et al. (2004)NG Summary 0.21–5 ? 1–5 110 ? 3–5 0.009 0.965–2.55 –

SG 0.51 0.87 1–5 72–96 0.04 3–33 0.010–0.014 0.8 Casal & Juncá (2008)SG 0.46 0.52 2 68–77 0.049 4–27 0.014–0.013 0.53–1.30 Martins et al. (2009)SG Summary 0.46–0.51 0.52–0.87 1–5 68–96 0.04–0.049 3–27 0.01–0.014 0.53–1.30 –

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Materials and methodsGeneral procedures

We examined specimens in zoological collections trying to assemble material from as many populations reported as H. crepitans as possible. Institutional abbreviations can be found in Sabaj Pérez (2010), with the addition of AL-MN (Adolpho Lutz Collection, housed at Museu Nacional, Rio de Janeiro, Brazil) and MTR (Miguel T. Rodrigues field numbers). Institutional abbreviations apply to both mor-phological and molecular (tissue) material. A number of specimens, published sequences, and tissues available were selected and gathered (see below). This material was either considered as NG or SG, allowing us to test the above-cit-ed hypothesis that the two distributional groups of popu-lations would represent two taxa with allopatric distribu-tion (Casal & Juncá 2008, Duellman 1997, Kluge 1979, Lynch & Suarez-Mayorga 2001). Specimens from NG are from Roraima state Brazil, Colombia, French Guiana and Venezuela, while specimens from SG are from sev-eral Brazilian localities (Supplementary document 1). Ad-ditional species for comparisons were chosen based on their availability according to the present taxonomy i.e., all the other species of the H. faber group, as defined by Faivovich et al. (2005). To discuss the taxonomic status of H. fuentei, we examined photos of the holotype and types of relevant material (H. crepitans lectotype and photos of the holo types of taxa currently considered synonyms).

Qualitative phenotypic data

We conducted the comparisons of adult specimens based on observations of collection material (Supplementary document 1) and on literature information (see below). Terminology of external morphology follows Duellman (1970). Standards for dorsal outline and profile of the snout follow Heyer et al. (1990). Fingers nomenclature follows Fabrezi & Alberch (1996). Webbing formula notation follows Savage & Heyer (1967), as modified by Myers & Duell man (1982). Types of vocal sac follow Liu (1935). Sex was determined by the presence of vocal sac, vocal slits, and developed projecting prepollex in adult males. Coloration always refers to preserved specimens, except when stated.

Quantitative phenotypic data

Sixteen morphometric variables were used and are given in millimeters throughout the text. Nine measurements fol-low Duellman (1970): SVL (snout–vent length), HL (head length), HW (head width), ED (eye diameter), UEW (up-per eyelid width), IOD (interorbital distance), IND (inter-narial distance), TD (tympanum diameter), and TL (tib-ia length). One measurement follows Heyer et al. (1990): THL (thigh length). Five measurements follow Napoli (2005): END (eye–nostril distance), NSD (nostril-tip of snout distance), FL (foot length, including tarsus), 4FD

(fourth finger disk diameter; using nomenclature of Fa-brezi & Alberch (1996)), and 4TD (fourth toe disk di-ameter). We included an additional measurement: FHL (forearm+hand length: straight line distance from elbow to the tip of the third finger). SVL, HL, HW, FHL, THL, TL, and FL were measured with a digital caliper to the nearest 0.05 mm. All other measurements were taken with an ocu-lar micrometer on a Zeiss stereomicroscope.

According to Bernal & Clavijo (2009), specimens preserved at different times can produce an artificial seg-regation among each time class when measured for mor-phometric analyses. The reason is the gradual modification of specimens along the years in preservative (see a brief historic account in Deichmann et al. 2009). Given that the measured specimens were collected in several differ-ent locations and times (see Supplementary document 1), the large amount of analyzed specimens and, the normal distribution of each measurement, we expect to minimize the possible problems regarding artefacts of preservation.

A total of 276 adult specimens were measured (NG: n = 98 males and 13 females; SG: n = 95 males and 70 females). Prior to analysis, all morphometric measures were log-transformed to conform to requirements of normality and homocedasticity (Zar 2009).

Principal Component Analysis (PCA) was used to ex-plore morphometric differences between groups. Eigen-vectors and associated eigenvalues were obtained from a variance-covariance matrix. Scores of individuals were then projected in the reduced space of the main compo-nents of larger contributions (Humphries et al. 1981). The first component (hereafter PC1) captures the largest pos-sible variation of the original data; the second component (hereafter PC2) is orthogonal to the first (independent) and provides the remaining of maximum variation (Peres-Ne-to & Bizerril 1994).

Molecular data procedures

Our survey of GenBank sequences (performed on the 27th of July 2012) showed that, with small additions from our own dataset, it was possible to assemble a nearly complete matrix using sequences of the 12S mitochondrial gene (hereafter 12S; 907 bp) and of the mitochondrial Cyto-chrome c oxidase subunit 1 (hereafter COI; 671 bp) for all species in the Hypsiboas faber group and for some close-ly related species according to Faivovich et al. (2005) to serve as outgroups. This includes both geographical groups of H. crepitans (see Supplementary document 2), however we were not able to gather sequences of both targeted gene fragments for all terminals. In order to reduce missing en-tries for outgroups, we used five chimerical sequences (see results). Chimerical sequences are solely of distinct indi-viduals assigned to a same species, and no chimerical se-quence was produced for ingroup terminals (Supplemen-tary document 2).

To amplify the 12S mtDNA, we used primers MVZ59 (5’–ATAGCACTGAAAAYGCTDAGATG–3’; Graybeal

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1997) and 12S F-H (5’–CTTGGCTCGTAGTTCCCT-GGCG–3’; Goebel et al. 1999) following the procedures of Faivovich et al. (2005). COI was amplified using primers dgHCO-2198 (5’-TAAACTTCAGGGTGACCAAARAAY-CA-3’) and dgLCO-1490 (5’-GGTCAACAAATCATAAA-GAYATYGG-3’) described in Meyer (2003) following his procedures. Fragments were sequenced in both directions and sequencing was performed by Macrogen Inc. (Seoul, South Korea). Data from complementary strands were compared to generate a consensus sequence for each DNA fragment using Sequencher 4.1 (Gene Code Corp, Ann Ar-bor, USA).

Alignments were conducted in the online version of MAFFT v6 (Katoh et al. 2002), aligning each fragment separately; both genes were aligned using MAFFT align-ment strategy L-INS-i. The final matrix comprises 68 ter-minals. The missing data are two 12S sequences of H. faber and 15 COI sequences of various representatives (two H. crepitans) of the H. faber species group. We collated 46 newly generated sequences of 12S and 45 of COI with 20 for 12S and eight for COI from GenBank. The final matrix can be found at BOLDSYSTEMS.

Genetic (uncorrected pairwise) distances were calculat-ed with MEGA 5.0 (Tamura et al. 2011) considering transi-tions and transversions. Pairwise distances were computed for a total of 907 bp for 12S and 671 bp for COI. As a first approximation, we considered genetic distances high (i.e., possibly not conspecific) when ≥ 3% for the 12S and ≥ 10% for COI. A threshold of 3% for 12S is common between dis-tinct amphibian species for which genetic distances were studied (e.g., Castroviejo-Fisher et al. 2012, Köhler et al. 2008, Ron et al. 2012). On the other hand, divergence values for COI have been studied for diverse animal groups and although thresholds vary among clades (e.g., Hebert et al. 2003), a minimum value of 10% is commonly found between amphibian species (e.g., Vences et al. 2005).

We used JModelTest 2.1.7 (Guindon & Gascuel 2003, Posada 2008) to select the best nucleotide substitution models according to the Akaike Information Criterion (AIC) for each of the four partitions we considered (12S and each codon position for COI). We used default settings (11 substitution schemes, ML optimization, NNI search). Selected models were GTR+I+G for 12S and TrNef+I, F81, and TrN+G for the first, second and third positions of the COI respectively.

The resulting models were employed in a Bayesian anal-ysis (BA) with MrBayes 3.2 (Ronquist et al. 2012). Instead of TrNef+I and TrN+G we used the closest models (GTR+I and GTR+G respectively) for BA. Gaps were treated as nu-cleotides of unknown origin in Bayesian inference analyses due to program constrains. The BA consisted of a 20×106 generations run and four Markov chains (one cold) sam-pled every 1,000 generations. A conservative burn-in (25%) was determined by examining stationarity of the likelihood scores (all parameters ESS were > 1,000) and convergence between the two runs using the deviation of split frequen-cies and mixing between chains. We considered relation-ships to be strongly supported when posterior probabilities

were equal to or higher than 0.95. Outgroup (root) was set as H. cinerascens + H. punctatus according to Faivovich et al. (2005).

ResultsMorphology

Specimens from the two groups can be distinguished based on adults colour patterns and general morphology. Howev-er, the two groups share the following characteristics: head in lateral view truncated, rounded, or acuminate; head in dorsal view rounded, truncated, or sub-elliptical; feet web-bing formulae I2[1] – 2[1]II1 – 2III1 – 2IV2 – 1V. The usu-al coloration of the body encompasses several patterns of marbled background with or without small spots (melano-phores) mostly resembling a bark-like pattern. The pattern on the posterior surface of thighs is different between both groups; specimens without blotches are found only in the NG, although some specimens may present some dark lines (Fig. 2C; Duellman 1970). Furthermore, the presence of a middorsal longitudinal stripe and the colour of the gular region differ between groups (see the comparisons section).

Morphometric analyses

PCA results are congruent with the hypothesis that the NG and the SG represent different species. Regarding the males (n = 193), PCA shows two major axes (PC1 57.3% of the total variation and PC2 22.4%). The standardized co-efficients and factor loadings of the Principal Component axes are presented in Supplementary document 3. The two axes show that the NG is completely separated from the SG, and the separation of these two groups is mostly due to both PC1 and PC2 (Fig. 3). When we look at the axes indi-vidually, PC1 is mostly influenced by FL, HW, THL, SVL, and IOD, in this order, and PC2 is mostly influenced by NSD, TD, END, 4FD, and 4TD, in this order (Supplemen-tary document 3).

Regarding the females (n = 83), PCA also display two major axes (PC1 accounted for 63.0% of the total variation and PC2 for 18.8%). The standardized coefficients and fac-tor loadings of the Principal Component axes are present-ed in Supplementary document 3. The two axes show that the NG is completely separated from the SG, and the sepa-ration of these two is mostly due to PC2 (Fig. 3). When we look to the axes individually, PC1 is mostly influenced by SVL, HW, HL, 4FD, and THL, in this order, and PC2 is mostly influenced by IOD, NSD, FL, 4FD, and UEW, in this order (Supplementary document 3).

Molecular analyses

The two groups of H. crepitans are reciprocally mono-phyletic and retrieved as strongly supported sister clades (Fig. 4). Genetic distances between them are high: 4% in

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12S and 13% in COI (Table 2). A phylogeographical struc-ture is also apparent within each of these two clades. The NG clade comprises two main lineages segregating east-ern populations in French Guiana and Guyana (east of Es-sequibo river) from western populations in Guyana (west of Essequibo river) and Roraima State (Fig. 4). However, genetic distance between them is low as well as support for the western lineage (< 0.5). The SG also comprises two main lineages segregating the northern part of the Atlantic Forest (AL, PE, BA) from the central part of the Atlantic Forest (BA, MG). Similarly, genetic distance between them is low (Table 2) as well as support for the central Atlantic Forest lineage (< 0.77).

Most of the nodes of the tree are strongly supported. However, the Hypsiboas faber species group was not re-trieved as monophyletic with the H. albopunctatus species group (Hypsiboas lanciformis and H. multifasciatus) being nested within it with uncertain relationship (Fig. 4). The basal divergence within the clade H. fa ber group + H. albopunctatus group separates H. albomarginatus from the rest. However, this relationship is also poorly supported. In fact, four major groups can be recognized in this clade,

the H. albopunctatus group (widespread in South Ameri-ca) and three strongly supported clades formed by the spe-cies of the Hypsiboas faber group. The first holds the two samples of H. albomarginatus (Atlantic Forest), the second samples of H. exastis, H. faber, H. lundii, and H. pardalis (hereafter the H. faber clade – Atlantic Forest, Cerrado), and the third H. crepitans, H. pugnax, and H. rosenbergi (hereafter the H. crepitans clade – from the Guiana Shield to Central America and the Atlantic Forest).

Observations on the holotype of Hyla fuentei

The holotype of Hyla fuentei (CM 44218; Fig. 5D) is a fe-male in good condition of preservation. The abdomen has a sagittal opening, possibly made for sex determination. The specimen presents two dorsal cuts in the skin: one over the frontoparietal fontanel and one from the right shoulder blade to the left hip. Colours have faded and no clear pat-tern can be seen.

Some specimens of the NG agree with the holotype of H. fuentei. Many specimens of the NG are dark green in

Figure 2. (A) Living specimen of Hypsiboas crepitans in diurnal coloration (photo by M. Solé) from the UESC campus in Ilhéus, Bahia, Brazil (specimen not collected). (B, C) Thigh patterns of two specimens of Hypsiboas crepitans (B = MNRJ32440 and C = MNRJ64374). (D) Living specimen of Hypsiboas xerophyllus in diurnal coloration (photo by A. FOUQUET) from Pacaraima, Roraima, Brazil. (E, F) Thigh patterns of two specimens of H. xerophyllus (E = MZUSP65854 and F = MZUSP68669). Scale bar = 1 cm.

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small melanophores on the dorsal surface, like the holo-type of H. fuentei. The nostril shape, the reduced webbing, and the absence of dermal ridges of the holotype conform to what is observed in specimens of the NG.

DiscussionTaxonomic conclusions

Although previous authors have used larval morphology and advertisement call data (Casal & Juncá 2008) to sug-gest that populations of Hypsiboas crepitans from the two geographical groups could represent two distinct species, published data on this subject remained ambiguous (see Introduction). Numerical parameters of advertisement call overlap (or nearly so, see Table 1), and call descriptions, especially for the populations of the NG, are too succinct and do not address intraspecific variation and other fac-tors known to influence amphibian calls (e.g., the social context; see Wells & Greer 1981). Larval morphology of Hypsiboas species presents high levels of intraspecific vari-ation and many closely related species have nearly indis-tinguishable larvae (see Kolenc et al. 2008, Orrico et al. 2007). However, since important character states are some-times overlooked in tadpole descriptions (see Kolenc et al. 2008), we cannot exclude that the larvae of the two dis-tributional groups are actually distinct. Additional studies are needed for a comprehensive comparison of larval mor-phology and bioacoustics of the two groups.

However, the molecular and morphological data pre-sented herein are concordant with the recognition of the populations from the two distributional groups as dis-tinct species. The SG is restricted to eastern Brazil, from the State of Paraíba to the northern State of Rio de Janeiro, including the State of Minas Gerais. The type locality of H. crepitans was originally designated as “Tamburil, Jiboya, Arrayal da Conquista”, State of Bahia, Brazil (Frost 2014). Bokermann (1966) restricted it to “Tamburil, [Municipal-ity of] Condeúbas, Bahia, Brazil”. Based on the aforemen-tioned characteristics, type series data, and type locality, the SG is considered to represent H. crepitans (Fig. 6).

The NG occurrence area comprises a region where five taxon names are available. Three names were proposed

Figure 3. Plots of individual scores resulted from Principal Com-ponent Analysis (PCA) of morphometric data from two groups of adult males (A) and adult females (B) of Hypsiboas crepitans (SG) and H. xerophyllus (NG) in the space of the first with the second canonical axes. Confidence ellipses (95%) for the scores of each group are shown.

Table 2. Mean intra (first column) and inter-specific uncorrected pairwise distances among species of the Hypsiboas faber group. Above the diagonal 12S (907 bp); below, COI (671 bp).

[COI/12S] 1 2 3 4 5 6 7 8 9

1 H. crepitans [0.01/0] – 0.04 0.07 0.06 0.07 0.09 0.07 0.08 0.092 H. xerophyllus [0.01/0] 0.13 – 0.06 0.05 0.07 0.08 0.07 0.07 0.083 H. rosenbergi [–/0.03] – – – 0.07 0.08 0.09 0.09 0.09 0.14 H. pugnax [–/0] – – – – 0.07 0.07 0.07 0.07 0.075 H. faber [0.06/0.02] 0.18 0.17 – – – 0.06 0.05 0.05 0.086 H. exastis [–/–] 0.17 0.2 – – 0.16 – 0.03 0.05 0.087 H. pardalis [0/0] 0.19 0.2 – – 0.15 0.11 – 0.04 0.088 H. lundii [0.01/0] 0.18 0.18 – – 0.16 0.15 0.15 – 0.089 H. albomarginatus [0.11/0.02] 0.17 0.17 – – 0.18 0.17 0.18 0.18 –

life also, but specimens from a given population can ex-hibit the dark green coloration while other present the pale coloration. Moreover, many specimens of the NG present

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by Duméril & Bibron (1841): Hyla doumercii Duméril & Bibron, 1841, from Suriname (holotype MNHN 766 [Fig. 5A], SVL 47.2 mm, adult male, vocal slits present, sup-plementary bone on Finger II =prepollical spine; A. Oh-ler, pers. comm.); Hyla levaillantii Duméril & Bibron, 1841, from Suriname (holotype MNHN 764 [Fig. 5B], SVL 48.1 mm, adult male, vocal slits present, prepollical spine on Finger II); Hyla xerophylla Duméril & Bibron, 1841, from “Cayenne”, French Guiana (holotype MNHN 752 [Fig. 5C], SVL 44.9 mm, probably an adult female, no male sexual secondary character, flat tubercle instead of prepol-lical spine). Article 24 of the International Code of Zoo-

logical Nomenclature (ICZN 1999) argues about the “Prec-edence between simultaneously published names, spellings or acts”. Following the rules of the Code, we cannot apply the Section 24.2 about the “Determination by First Revis-er” because this was already done (see Duellman 1970, Kluge 1979).

Although we cannot establish precedence, Article 24 of the Code still allows us to choose which of the names of Duméril & Bibron (1841) we will revalidate if applicable to a natural population. Thus, any of the three names de-scribed by Duméril & Bibron (1841) are available and can be applied to the NG. Herein, we decided to consider the

Figure 4. Phylogram (50% majority rule consensus with frequencies of all observed bipartitions) hypothesized from Bayesian analysis using 1578 bp of 12S and COI. Numbers above nodes are posterior probabilities (* indicates pp ≥ 0.99; pp < 0.5 are not indicated). Sam-ples are labeled according to collection numbers followed by origin (country in full or Brazilian state official acronym if from Brazil).

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Figure 5. Dorsal and ventral views of the holotypes of (A) Hyla doumercii [SVL = 47.2 mm, male], (B) H. levaillantii [SVL = 48.1 mm, male], (C) H. xerophyllus [SVL = 44.9 mm, likely a female], and (D) H. fuentei [SVL = 57.0 mm, female]. Figures are not to scale.

NG as Hypsiboas xerophyllus, resurrecting the name Hyla xerophylla Duméril & Bibron, 1841 from the synonymy of Hypsiboas crepitans (Wied, 1824) and transferring the species to the genus Hypsiboas based on phylogenetic re-lationships.

The two remaining names, Hypsiboas indris Cope, 1867 and Hyla fuentei Goin & Goin, 1968, are more recent and based on material from Suriname. Hyla fuentei holotype from “Suriname, Suriname District Powakka” (CM 44218 [Fig. 5D], SVL 57.0 mm, adult female; Goin & Goin 1968) presents a colour pattern in accordance with what was stat-ed by Goin & Goin (1968). The sagittal opening at the ab-domen seems to be made for information on ovaries and oocytes (see Goin & Goin 1968). In fact, all our obser-vations about the holotype agree well with Goin & Goin (1968). In addition, The holotype agreed with the NG pop-ulations and they exhibit a dark green coloration, while other present the pale coloration, a phenomenon proba-bly not uncommon in Hypsiboas, as also revealed in An-dean species of the H. pulchellus species group (Köhler et al. 2010). After the examination of the holotype of Hyla fuentei we considered this species as belonging to the NG and, thus, to be a junior synonym of the name applicable to this group (H. xerophyllus). We have not examined the holotype of Hypsiboas indris Cope, 1867. However, the dis-tribution of this taxa completely overlaps with the more in-clusive distribution of the NG. In the light of the present results – where the genetic diversity within each group is low (Table 3) – it seems very unlikely that it represents a different species from H. crepitans. Therefore, we provi-sionally transfer it from the synonymy of Hypsiboas crepitans to the synonymy of Hypsiboas xerophyllus.

Species account

Hypsiboas xerophyllus (Duméril & Bibron, 1841). New combination, revalidation

Hyla levaillantii Duméril & Bibron, 1841 – Erp. Gen. 8:550. New synonymy.Hyla doumercii Duméril & Bibron, 1841 – Erp. Gen. 8:551. New synonymy.Hyla fuentei Goin & Goin, 1968 – Copeia 1968:581. New synony-my.Hypsiboas indris Cope 1867 – J. Acad. Nat. Sci. Philadelphia, Ser. 2, 6: 201. New synonymy.

Holotype: MNHN 652, SVL 44.9 mm, probably female (no male secondary characters), “Cayenne” [= French Guiana] (Fig. 5C).

Diagnosis: Hypsiboas xerophyllus is a member of the H. faber species group (sensu Faivovich et al. 2005), character-ized by: SVL 42.9–63.8 mm in adult males, 40.9–71.8 mm in adult females; in dorsal view, head nearly rounded with rounded, truncated, or sub-elliptical snout; single, well de-veloped projecting prepollex in adult males; tympanum

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and tympanic annulus visible externally and in contact with the posterior margin of eye; well-developed supra-tympanic fold covering the upper edge of the tympanum; lower edge of the tympanum close to the mouth (at jaw articulation level); males with vocal slits under the tongue and parallel to the lower lip, vocal sac median, subgular (sensu Liu 1935); presence of two groups of vomerine teeth between choanae; dermal ridges (fimbriae) absent or ru-dimentary along arms and feet; skin smooth dorsally and granular ventrally; colour of gular region similar to belly colour in preserved males and females (cream); cloacal re-gion composed by a subcloacal fold, white tubercles around the cloacal opening, and a well-developed flap (horizontal,

above vent); flanks usually show parallel transverse thin bars; well-developed tubercles on the ventral surface of thighs; dorsal surface of thighs usually with parallel bars, if present, spaced and wider dorsally, thinner and lighter posteriorly; colour on dorsum ranging from pale gray to brown in preservative, with a X-shaped mark sometimes over the suprascapula.

Comparisons with other species: Hypsiboas xerophyllus is easily differentiated from H. crepitans, its sister taxon and morphologically most similar species, by the absence of a mid-dorsal longitudinal dark brown stripe (present, of dif-ferent widths, sometimes incomplete – i.e., not connect-ing snout and vent – in H. crepitans); immaculate cream gular region in both sexes (brown in males of H. crepitans); absence of, or barely visible, bifurcated vertical dark brown bars on ventroposterior surfaces of thighs (present in H. crepitans; Fig. 2).

From other species of the H. faber group, H. xerophyllus differs by having a smooth texture of skin on dorsal sur-faces, and low development of ulnar and outer tarsal der-mal ridges (skin texture lumpy, and well developed dermal ridges in H. pardalis, H. exastis, H. rosenbergi, and H. lundii). The absence of well-developed calcars distinguishes H. xerophyllus from H. pardalis, and H. exastis. The ab-sence of extensive hand webbing distinguishes H. xerophyllus from H. pardalis, H. exastis, and H. lundii. The su-pratympanic fold of H. albomarginatus is white (or whitish green in live specimens) while in H. xerophyllus it presents the same lichenous colour as the dorsum. The gular region is immaculate cream in H. xerophyllus while it has brown flecks in H. pugnax. In life, the iris coloration is whitish around the pupil and yellow-green on he outer edge in H. xerophyllus while it is golden yellow in H. pugnax.

Figure 6. Lectotype of Hypsiboas crepitans, AMNH 785, adult female, SVL ca. 69 mm, from Vitória da Conquista, State of Bahia, Brazil.

Table 3. Mean pairwise distances within species of the Hypsiboas faber group and within other groups (gr.) of Hypsiboas. 12S se-quences have 907 bp; COI, 671 bp.

12S COI

H. albomarginatus 0.02 0.11H. albopunctatus gr. 0.04 0.13H. crepitans 0.00 0.01H. exastis – –H. faber 0.02 0.06H. lundii 0.00 0.01H. pardalis 0.00 0.00H. pellucens gr. 0.01 0.11H. pugnax 0.00 –H. pulchellus gr. 0.08 –H. punctatus gr. 0.09 –H. rosenbergi 0.03 –H. xerophyllus 0.00 0.01

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Colour in preservative: Dorsal background light brown to cream with dark brown blotches; an interocular stripe and a X-shaped mark on the dorsum can be present. Flanks with well-defined dark brown transverse stripes. Chest and gular region beige, edge of lips green. Belly and ventral sur-faces green, sometimes orange. Fingers beige, dark green, or orange. Iris grey with green outer border.

Variation: Hypsiboas xerophyllus presents some variation in size, with females usually larger than males (Table 4). Adult males have hypertrophied forearms, enlarged and projecting prepollices, and vocal slits, all characteristics that are absent in females. In dorsal view, shape of head ranges from rounded to oval, and in lateral view from rounded to truncated. Specimens usually lack any colour pattern at inguinal region and posterior surface of thighs. In living specimens, the dorsal pattern can vary in colour (white, green, or brown), often depending on light inten-sity, and dorsal blotches can be present or absent.

Distribution: Eastern Panama, through northern Co-lombia, Venezuela, the Guiana Shield, including adjacent northwestern Brazil, below 2,450 m a.s.l. The species seems absent from most French Guiana, only occurring around inselbergs at isolated localities in the south and in dis-turbed forest along the lower course of the Maroni River (Apatou, Saint Laurent). The species has not been recorded in the states of Amapá (AF pers. obs., Dias-Lima 2005) and Pará, north of the Amazon River (Ávila-Pires et al. 2010). However, it occurs throughout most Guyana (Cole et al. 2013) and northern Suriname (Ouboter & Jairam 2012), although apparently absent from Kaieteur National Park (Kok & Kalamandeen 2008).

Natural history: According to Duellman (1970; as H. crepi tans), specimens from Panama do not exhibit the habit to build clay nests. However, Lynch & Rami-rez (2000) reported this behavior as usual in Colombian populations, and Lehtinen (2014) confirms this behav-ior for Trinidad populations. One of us (AF) observed building of clay nests in the state of Roraima in Brazil and in Suriname. Therefore, nest building behavior is likely facultative as already observed by Caldwell (1992) in other species of Hypsiboas. Males have been observed calling at night in small streams, ponds, and even flasks during the rainy and the dry season. The species seems to inhabit ecotonal forest and is often found in disturbed habitat.

Hypsiboas crepitans (Duméril & Bibron, 1841)

Lectotype: AMNH 785, SVL ca. 69 mm, adult female, from Tamburil, [Municipality of] Condeúba, Bahia, Bra-zil (Fig. 6).

Diagnosis: Hypsiboas crepitans is a member of the H. faber species group (sensu Faivovich et al. 2005), characterized by: SVL 48.1–72.0 mm in males and 42.3–70.6 mm in fe-males; interdigital membranae poorly developed; fimbrias absent in arms and tibia; Dorsal coloration brown, usually with an X-shape above the scapular region or a fragmented mid-dorsal line; dorsal skin smooth; flank and thigh with conspicuous transversal bars; absence of calcar flap or ap-pendage; presence of subcloacal dermal fold, surrounded by granules; upper cloacal flap poorly developed; absence of lichenous subcloacal plate.

Table 4. Descriptive statistics (in millimeters) for measurements of Hypsiboas crepitans and H. xerophyllus. The results are presented as mean ± standard deviation (range).

MeasuresHypsiboas crepitans H. xerophyllus

Males (n=95) Females (n=70) Males (n=98) Females (n=13)

SVL 58.1±7.6 (33.2–71.8) 55.4±4.59 (51.0–64.7) 50.6±3.86 (42.9–63.8) 57.7±7.91 (40.9–71.8)HL 19.2±2.2 (11.4–22.8) 18.4±2.23 (14.7–21.6) 16.6±1.5 (13.7–19.9) 19.1±2.21 (13.8–22.8)HW 20.3±2.5 (12.0–24.1) 18.9±1.32 (17.1–21.3) 17.7±1.25 (15.4–21.7) 20.0±2.51 (14.5–24.1)ED 6.1±0.7 (3.2–7.3) 2.2±0.15 (1.9–2.5) 5.4±0.54 (4.1–6.9) 3.7±0.43 (2.9–4.7)END 5.6±0.7 (3.5–6.8) 3.6±0.39 (2.8–4.3) 5.5±0.72 (4.3–9.8) 1.9±0.28 (1.3–2.6)TD 4.4±0.6 (2.1–5.5) 4.6±0.47 (4.0–5.5) 4.4±0.39 (3.4–5.3) 4.4±0.69 (2.7–6.3)UEW 4.6±0.7 (2.7–6.3) 5.6±0.47 (4.7–6.5) 4.4±0.63 (2.2–6.0) 6.0±0.67 (4.2–7.3)IOD 10.8±1.2 (7.0–12.8) 5.7±0.50 (5.0–6.6) 5.4±0.63 (4.0–7.0) 10.7±1.21 (7.7–12.8)IND 3.8±0.5 (1.7–4.8) 5.6±0.44 (5.0–6.1) 3.3±0.66 (1.8–4.6) 5.5±0.69 (4.2–6.8)NSD 1.9±0.3 (1.1–2.6) 4.5±0.50 (3.7–5.3) 2.5±0.63 (1.6–3.9) 4.4±0.63 (2.1–5.5)FAL 27.7±3.6 (15.4–34.4) 25.7±3.46 (16.8–30.3) 23.9±2.1 (12.0–29.6) 27.4±3.55 (19.2–34.4)4FD 2.6±0.4 (1.5–3.4) 2.7±0.38 (2.1–3.2) 2.4±0.25 (1.8–3.3) 2.6±0.38 (1.8–3.4)THL 32.4±4.2 (18.3–40.0) 30.6±1.91 (27.7–34.1) 28.3±1.92 (23.1–34.8) 31.9±4.19 (23.2–40.0)TL 31.7±4.1 (18.0–39.3) 30.4±1.85 (27.8–33.8) 28.0±1.99 (23.0–35.0) 31.5±4.13 (23.3–39.3)FL 40.8±5.2 (22.5–51.9) 38.6±2.40 (34.5–42.4) 35.5±2.61 (28.8–44.3) 40.4±5.14 (30.2–51.9)4TD 2.3±0.3 (1.2–3.0) 2.4±0.32 (2.0–3.0) 2.1±0.25 (1.5–2.9) 2.2±0.33 (1.6–2.9)

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Distribution: Central to eastern Brazil, from the Atlan-tic coast of the states of Rio de Janeiro to Paraíba (present study).

Phylogenetic relationships and biogeography

The Hypsiboas faber species group, as defined by Faivo-vich et al. (2005), has not been recovered as monophylet-ic in our results – the weak relationship between H. albomarginatus and the remaining species of the group has been already reported by previous authors (Kolenc et al. 2008, Wiens et al. 2006), and the nested position of the H. albo punctatus group within the H. faber group is strongly supported. However, we refrain to take any for-mal action regarding this matter as our molecular anal-yses were simply aimed at exploring genetic divergence within H. crepitans.

Faivovich et al. (2005) listed the H. faber group as an example of a clade having an Atlantic Forest (or at least an eastern Brazilian) origin with subsequent radiations into neighbouring regions. At that time the authors had only Atlantic Forest dwellers in their dataset (their sam-ple of H. crepitans was from State of Alagoas, Brazil) and probably assumed that H. albomarginatus would be sister to the remaining species of the group based on its unique colour. Our results suggest a more complex history of suc-cessive dispersals between Amazonia, Cerrados and the Atlantic Forest. However, the lack of support at the base of the clade prevents any further biogeographic analyses, and additional data are needed. Nevertheless, the H. faber clade is endemic to eastern Brazil while the H. crepitans clade is restricted to northern South America and Panama with the exception of H. crepitans. Such a pattern suggests that H. crepitans originates from a dispersal event from Amazonia to the Atlantic Forest probably via a northern route (Costa 2003). Given the genetic distances between H. crepitans and H. xerophyllus we hypothesize that this dispersal occurred before the Pleistocene and was probably favored by forest connection due to more humid climate. Such a route is supported by biogeographical analyses of different groups of organisms, as well as by climatic and floristic evidence (Batalha-Filho et al. 2013, Cabanne et al. 2008, Costa 2003, Melo Santos et al. 2007, Wang et al., 2004).

Hypsiboas pardalis and H. lundii were long consid-ered synonyms (Caramaschi & Napoli 2004) due to their morphological similarity. Although the relationship of H. exastis with H. pardalis and H. lundii was not unex-pected (see Caramaschi & Rodrigues 2003), we – unex-pectedly – found that H. lundii is instead sister to a clade composed of H. exastis + H. pardalis. Caramaschi & Ro-drigues (2003) related H. exastis to H. pardalis and H. lundii due to their similar skin texture and colour pattern; the lichenous aspect similar to tree bark were evidence that these species were more closely related to each other than to all other members of the Hyla boans species group, as defined at that time.

The IUCN distribution for Hypsiboas crepitans (La Marca et al. 2010) and H. xerophyllus needs to be re-eval-uated. Although Frost (2016) stated that the species oc-curs in the south of the Atlantic Forest, from São Paulo to Santa Catarina states, we were unable to find a speci-mens from this region (Fig. 1). We propose that the south-ern part of the IUCN distribution is based on misidenti-fied H. lundii or H. pardalis specimens and that the dis-tribution of H. crepitans (as re-defined here) is restricted to an area north of 22o southern latitude. Despite the fact that the respective ranges are now confined to a smaller portion of the formerly supposed range of H. crepitans, both species are still widespread and, given their habitat requirements, are likely relatively tolerant to human dis-turbance. Therefore, we suggest considering them as Least Concern (LC).

Acknowledgements

We are grateful toward S. Ron, P. J. R. Kok and an anonymous reviewer for valuable comments on a previous version. For their invaluable help and company in the field and for the gift of tis-sue samples, we thank P. Gaucher, M. Blanc, J. Cassimiro, C. M. Carvalho, F. Curcio, M. Dixo, A. Camacho, R. Da-masceno, D. Pavan, R. Recoder, M. Sena, S. M. Souza, M. Teixeira Jr., V. Verdade, H. de Niemeyer, and D. F. de Mo-raes Jr. Pictures of the holotype of Hypsiboas fuentei were kindly provided by S. Rogers and J. M. Padial. VGDO thanks Sao Paulo Research Foundation (FAPESP; grants #2007/57067-9, #2012/1200-5, BIOTA #2013/50297-0) and ANPCyT PICT 2202/2007 for financial support and C. S. Cassini for support and comments on a previous versions of this manuscript. AF benefited from an “Investissement d’Avenir” grant managed by Agence Nationale de la Recherche (CEBA, ref.ANR-10-LA-BX-25-01), France. IN thanks Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Conselho Nacional de Desenvolvimento Científico e Tec-nológico (CNPq) for support and fellowship, respectively. CM thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for fellowship. UC thank CNPq for finan-cial support. MLL thanks FAPESP (#2010/50124-0) and CNPq (#478670/2010-9; #564955/2010-8) for fellowship and financial support. CFBH and MTR thank FAPESP (Grant #2013/50741-7) and CNPq for financial support. This study was co-funded by NSF (DEB 1343578) and NASA. This research was supported by the Núcleo de Computação Científica (NCC/GridUNESP) from the Universidade Estadual Paulista ‘‘Júlio de Mesquita Fil-ho’’ (UNESP). The Centro de Estudos de Insetos Sociais (CEIS), UNESP, Rio Claro, Brazil, allowed the utilization of the facilities for molecular analyses.

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Supplementary material

Supplementary document 1. Examined specimensSupplementary document 2. Voucher information, localities, and GenBank accession numbers for the specimens analyzed for this study.Supplementary document 3. Standardized coefficients and factor loadings (r) from a Principal Component Analysis.

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Online Supplementary data – Taxonomy of Hypsiboas crepitans

Supplementary document 1. Examined specimens

Hypsiboas albomarginatusBrazil: Estado de Alagoas: MNRJ 9795 Fazenda Santa Justina, Pas-so de Camaragibe; MNRJ 9722–9723 Murici; MNRJ 36737, 9638, 36681–36684 São Miguel dos Campos; MNRJ 38631–38634 Rio Largo.

Brazil: Estado da Bahia: MNRJ 36959 Reserva Particular do Patrimônio Natural Cachoeira da Água Branca, Valença; MNRJ 27241 Mata da Cara Branca, Santa Cruz Cabrália; MNRJ 47823 Fei-ra de Santana; MNRJ 47961 Reserva Particular do Patrimônio Nat-ural Capitão, Itacaré; MNRJ 16939–16941 Fazenda Tiririca, Conde; MNRJ 37913 Entre Rios; MNRJ 40460 Fazenda São José, Mascote; MNRJ 69620–69621 Fazenda Pedra Branca, Itagibá; MNRJ 28877 Reserva Particular do Patrimônio Natural Estação de Vera Cruz, Porto Seguro; MNRJ 46488 Serra do Timorante, Valentim, Boa Nova; MNRJ 27238 Reserva Particular do Patrimônio Natural Ser-ra do Teimoso, Jussari.

Brazil: Estado do Espírito Santo: MNRJ 35468 Santa Teresa; MNRJ 79057, 60329–60331 Praia das Neves, Presidente Kennedy; MNRJ 68028 Costa Bela, Serra; MNRJ 84934–84936 Parque Es-tadual Fonte Grande, Vitória; MNRJ 27858–27860, 27933, 28419, 31375 Reserva Biológica de Duas Bocas, Cariacica; MNRJ 75675–75676 Barra do Riacho, Aracruz; MNRJ 50973–50977 Pedra do Garrafão, Mimoso do Sul; MNRJ 47790–47792 Guarapari; MNRJ 28327, 30877, 40067–40068 Reserva Biológica de Santa Lúcia, Santa Teresa; MNRJ 60306–60308 Mimoso do Sul; MNRJ 43402 Setiba, Guarapari; MNRJ 34137 Pedra Azul, Domingos Martins; MNRJ 29055–29056 Ponte da Chinchinha, Povoação, Linhares.

Brazil: Estado de Minas Gerais: MNRJ 37218–37223 Chia-dor; MNRJ 43625 Faria Lemos; MNRJ 63736, 78191–78192 Além Paraíba; MNRJ 56965–56966 Pádua; MNRJ 43333–43335 Faria Lemos.

Brazil: Estado do Paraná: MNRJ 33758 RPPN Salto Mor-ato, Guaraqueçaba; MNRJ 30382–30386 Estação II, Instituto Agronômico do Paraná, Morretes.

Brazil: Estado de Pernambuco: MNRJ 57828–57832, 57883–57886 Refúgio Ecológico Charles Darwin, Igarassu.

Brazil: Estado de Rio de Janeiro: MNRJ 2063 Jacarepaguá, Rio de Janeiro; MNRJ 42949, 42950–42951 Pedra de Guaratiba, Rio de Janeiro; 20016–20019, 20032–20033, 20054–20055 Ilha de Ma-rambaia, Mangaratiba; MNRJ 63934–63935 Vila Dois Rios, Ilha Grande, Angra dos Reis; MNRJ 16853, 16880, 81587–81590 Horto Florestal de Santa Cruz, Itaguaí; MNRJ 3122, 47489, 54008–54011, 61913–61914 Duque de Caxias; MNRJ 31984 Restinga Maricá, Maricá; MNRJ 48020 Manguinhos, Rio de Janeiro; MNRJ 16703 Araruama; MNRJ 21010, 21676 Fazenda Cachoeira, Morro Azul, Engenheiro Paulo de Frontin; MNRJ 48512–48513 Ilha Grande, Angra dos Reis; MNRJ 16080 Vale das Pedrinhas, Magé; MNRJ 75987 Lídice, Rio Claro; MNRJ 36583 Grussaí, Campos dos Goyt-acazes; MNRJ 79439 Ponta Negra, Maricá; MNRJ 38112, 43490, 43491–43495, 51229–51231 Tanguá; MNRJ 29473–29476, 74541–74543 Espraiado, Maricá; MNRJ 82169 Peró, Cabo Frio; MNRJ 72272–72274, 76539 Reserva Ecológica de Guapiaçu, Cachoeiras de Macacu; MNRJ 81093 Centro Marista São José das Paineiras, Mendes; MNRJ 40727–40728 Estrada Além Paraíba – Carmo, Carmo; MNRJ 84253 Restinga Massambaba, Arraial do Cabo; MNRJ 84227 Itaperuna; MNRJ 38200 Itapebussus, Rio das Os-tras; MNRJ 71683 Silva Jardim; MNRJ 45708, 53924 São Francis-co de Itabapoana; MNRJ 57807 Núcleo Experimental de Iguaba Grande–UFF, Iguaba Grande; MNRJ 82161–82167 Pontal do Ata-laia, Arraial do Cabo; MNRJ 47549, 54900–54901, 84022 São João da Barra; MNRJ 50331–50332, 50347–50348 Área da PCH Santa Fé, Três Rios; MNRJ 85218–85219 Ponte Preta, Magé; MNRJ 79608 Paracambi; MNRJ 30278, 16083–16084 Saquarema; MNRJ 57191–

57192 Reserva Biológica União, Casimiro de Abreu; MNRJ 65547–65556 Tinguá, Nova Iguaçu; MNRJ 74606 Parque Natural Mu-nicipal da Atalaia, Macaé; MNRJ 60815–60816 Itaperuna; MNRJ 74812–74813 Parque Natural Municipal da Prainha, Grumari, Rio de Janeiro; MNRJ 30676 Tarituba, Paraty; MNRJ 66646 Bom Jesus de Itabapoana; MNRJ 53964 Parque Nacional Restinga de Jurubat-iba, Macaé; MNRJ 77322–77327 Parque Natural Municipal Bosque da Barra, Rio de Janeiro; MNRJ 74800 Parque Natural Municipal da Prainha, Rio de Janeiro.

Brazil: Estado de Santa Catarina: MNRJ 74260–74262 Palhoça.Brazil: Estado de São Paulo: MNRJ 61941–61975, 81935 Praia de

Itaguaí, Ubatuba; MNRJ 34473 Picinguaba, Ubatuba; MNRJ 48009–48011 Pedro de Toledo; MNRJ 31345–31348 Praia de Barequeçaba, São Sebastião; MNRJ 47992 Eldorado Paulista; MNRJ 69327 Fa-zenda Jamapa, Jacupiranga; MNRJ 83272 Guarujá; MNRJ 43452 Parque Estadual Intervales, Ribeirão Grande; MNRJ 31302 Barra do Quilombo, Sete Barras; MNRJ 39922–39923 Estação Ecológica da Juréia, Iguape; MNRJ 31647, 80258–80264 Pariquera-Açu.

Brazil: Estado de Sergipe: MNRJ 16851, 47999 Fazenda Cruzei-ro, Cristinápolis; MNRJ 38108 São Cristóvão; MNRJ 17963, 17964–17965 Santa Luzia do Itanhy; MNRJ 49758–49759, 59720–59728 Fa-zenda CICP, Itaporanga d’Ajuda.

Hypsiboas crepitansBrazil: Estado de Alagoas: MZUSP 71001 UHE Xingó, Vila Resi-dencial, Piranhas; MZUSP 9264, 9265 Rio Largo, Fazenda Canoas; MZUSP 71002 UHE Xingó; MNRJ 9781 Fazenda São Bento, Água Branca; MNRJ 36705–36706, 9677–9678 São Miguel dos Campos; MNRJ 9673–9674 Fazenda do Prata, São José dos Campos; MNRJ 3536 Maceió.

Brazil: Estado da Bahia: MNRJ 62941, 62943–62946 km 8, Ro-dovia Jequié–Salvador, Salvador; MNRJ 70403 Salvador; MNRJ 16978–16980 Fazenda Tiririca, Conde; MNRJ 64329, 64347, 66953, 66957, 67140, 67141, 67143, 67145, 67147, 67156, 67157, 67158, 67929–67934, 85830–85833, 85840–85842, UFBA 6160 Fazenda Pe-dra Branca, Itagibá; MNRJ 59117 Parque Municipal da Lagoa Azul, São Desidério; MNRJ 59260, 59261, 59262, 59263, 59270, 59272, 59280, 59281, 59283, 64369–64370, 64373–64376, 64378, 67115, 67123, 78906–78908 Maracás; MNRJ 35361, 35363, 35364, 35366, 35368 Parque Estadual Serra do Conduru - Setor Norte, Itacaré; MNRJ 46508, 46526–46527 Boa Nova; MNRJ 26471 Mata da Cara Branca, Santa Cruz Cabrália; MNRJ 29185 Fazenda Pedra Formo-sa, Ibirapitanga; MNRJ 16936–16937, 25072, 36031–36032, 71174, UFBA 8563, 8564, 8565, 8566, 8567, 8568, 8569, 8979, 8980, 8987, 9001 9002 Caetité; MNRJ 47813, 80128–80129 Trancoso, Porto Seguro; MNRJ 78860, 78862, 85834–85835, 85836–85839, 85843–85844 Jequié; MNRJ 28930–28931 Fazenda Orion, Arataca; MNRJ 16993, 71175 CEPLAC, Ilhéus; MNRJ 27242–27244 Fazenda Vista Bela, Guaratinga; MNRJ 3777, 79070–79071 Januária; MNRJ 26476 Uruçuca; MNRJ 59135 Calumbi, Macaúbas; MNRJ 1192, UFBA 8191, 8194 Barreiras; MNRJ 71179 Alagoinhas; MNRJ 26472–26475 RPPN Serra do Teimoso, Jussari; MNRJ 70401, 70404, 70406, 79069 Salvador; UFBA 3945, 3946, 3947 Pratigi; UFBA 7330, 7331 Mucugê; UFBA 7710 Bom Jesus da Lapa; UFBA 8037, 8043 En-cruzilhada; UFBA 9756, 9757 Serra do Ramalho; MNRJ 12304 no locality provided.

Brazil: Estado do Espírito Santo: MBML 4461, 5755 Sítio do Am-arildo, Marechal Floriano; MNRJ 38951 Alto Nova Almeida, Mare-chal Floriano; MBML 2082, 2083, MZUSP 106506, 106507, 106508, 106511, 106512, 106513 Colatina; MBML 2873, 2874, 2875 Aparecid-inha, Santa Teresa; MBML 6811 Entorno da ESFA, Santa Teresa; MBML 673 Bairro Vila Nova, Santa Teresa; MBML 1768 Fazenda Recanto da Mata, Muniz Freire; MNRJ 51965 São Simão, Muniz

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Online Supplementary data – Victor G. D. Orrico et al.

Freire; MBML 773, 774, 776 Três Barras, Fundão; MBML 2123 Goi-apaba-Açu, Fundão; MBML 1844 Barra de São Francisco; MBML 7245 Cabeceira do Rio Mutum, São Roque do Canaã; MBML 5028 Anutiba, Pedra da Severina, Alegre; MZUSP 135137 Samarco, An-chieta; MZUSP 35647, MNRJ 34738, 36757 Baixo Guandu; MZUSP 106515, 106516, 106517 sem maiores procedências.

Brazil: Estado de Goiás: MNRJ 27833–27838 Mambaí; MNRJ 795, 2957 Ilha, Rio Paranã; MZUSP 141575, 141578, 141579, 141576, 141572, 141577, 141574, 141573 PCH Santa Edwiges; MZUSP 66392, 66393, 66410 Monte Alegre de Goiás, Rio Raiz; MNRJ 24785 Cat-alão; MNRJ 35734, 35735 Flores de Goiás.

Brazil: Estado de Minas Gerais: MNRJ 16931–16933, 21325, 21876–21884, 31712–31720, 32440–32445 Mocambinho, Manga; MNRJ 21589, 36350 Fazenda Curral Velho, Cristália; MNRJ 21590–21592, 21595, 70472–70474, 70783, 70785–70787 Peixe Cru, Turma-lina; MNRJ 21597–21599, 21610, 21668, 21669 Berilo; MNRJ 22469 Veredas, Botumirim; MNRJ 37892–37896 Córrego Santa Rita, Paraíso, Espera Feliz; MNRJ 38726, 71950–71951 Serra do Cipó, Santana do Riacho; MNRJ 43309–43313 Fazenda Cachoeira Ale-gre, Abre Campo; MNRJ 43628 Fazenda Todos os Santos, Faria Lemos; MNRJ 47775, 47781 Capitão Andrade; MNRJ 72661–72663 RPPN Santuário do Caraça, Catas Altas; MNRJ 55019–55020, 60348–60352 Fazenda do Engenho, Serra do Caraça, Catas Altas; MNRJ 60334 Paula Cândido; MNRJ 63268–63273 Estrada Gov-ernador Valadares–Mantena, km 15; MNRJ 21310 Minas Novas; MNRJ 15984 Grão Mogol.

Brazil: Estado da Paraíba: MZUSP 65355–65365 Fazenda Salga-do, Gurinhém; MNRJ 32839, 32840, 32841, 32842 Boqueirão.

Brazil: Estado de Pernambuco: MZUSP 51693–51697 Bom Conselho; MZUSP 63141–63147 Serra dos Cavalos, São Caetano; MZUSP 84571–84573 Engenho Sacramento; MZUSP 101821, 113839–113859, MNRJ 38625–38626 Caruaru; MNRJ 1614 Rio Bran-co; MNRJ 36259 Serra da Borborema.

Brazil: Estado de Sergipe: MNRJ 3802 Riachuelo; MNRJ 59739–59741 Fazenda Sabão, Indiaroba; MNRJ 16938 Fazenda Cruzeiro, Cristinápolis.

Hypsiboas exastisBrazil: Estado de Alagoas: ZUFRJ 10366, 10367, 10384, 13657 Que-brangulo.

Brazil: Estado da Bahia: UFBA 8327 Amargosa; UFBA 7367 Elí-sio Medrado; MNRJ 29784 (parátipo) Estação Ecológica Estadual Nova Esperança, Wenceslau Guimarães; MNRJ 29976 (parátipo), MZUSP 63538 (parátipo), 63540 (holótipo), 63541–63542 (paráti-pos) Fazenda Unacau, São José; MNRJ 35323–35328 Fazenda Capitão, Itacaré; MNRJ 44977 Fazenda Serra Verde, Jussari; MNRJ 44978 Rio Vermelho, Três Braços, Teolândia; MNRJ 55859 Amar-gosa.

Hypsiboas faberBrazil: Estado da Bahia: MNRJ 74672 Fazenda Serrinha, Itagibá; MNRJ 69504, Torrão, Prado; MNRJ 59288, 69534 Maracás; MNRJ 81446 Trancoso, Porto Seguro; MNRJ 82322 Itabuna; MNRJ 27239 Jussari; MNRJ 45001–45002 Teolândia; MNRJ 38922 Porto Seguro.

Brazil: Estado do Espírito Santo: MNRJ 40660 Sítio do Popota, São Lourenço, Santa Teresa; MNRJ 76930 Parque Estadual do For-no Grande, Castelo; MNRJ 50993 Pedra do Garrafão, Mimoso do Sul; MNRJ 30059–30060 Floresta Nacional do Rio Preto, Con-ceição da Barra; MNRJ 59431–59432 Domingos Martins.

Brazil: Estado da Paraíba: MNRJ 18053 Reserva Biológica Guaribas, Mamanguape.

Brazil: Estado do Paraná: MNRJ 31581 APA SEMA, Guar-aqueçaba.

Brazil: Estado do Rio de Janeiro: MNRJ 79365 Saquarema; MNRJ 18517 Pendotiba, Niterói; MNRJ 82170, 82173 APA Pau

Brazil, Búzios; MNRJ 53321 Fazenda Brasiléia, Natividade; MNRJ 36874 Quitandinha, Petrópolis; MNRJ 83041 Capela, Petrópolis; MNRJ 79454 Ponta Negra, Maricá; MNRJ 66597 Lídice, Rio Claro; MNRJ 82457 Pedreira Quatro Irmãos, Santo Antônio de Pádua; MNRJ 43615 Fazenda Vargem Alegre, Porciúncula; MNRJ 63719 Trajano de Moraes; MNRJ 48114 Ilha Grande, Angra dos Reis.

Brazil: Estado do Rio Grande do Sul: MNRJ 14818 Farroupilha.Brazil: Estado de Santa Catarina: MNRJ 37304–37305 Porto

Belo; MNRJ 74453–74454 Santo Amaro da Imperatriz.Brazil: Estado de Sergipe: MNRJ 17957 Mata do Castro, Santa

Luzia do Itanhy.Brazil: Estado de São Paulo: MNRJ 81145 Lageado, Botucatu.

Hypsiboas lundiiBrazil: Estado de São Paulo: MNRJ 23963–23970, 25773–25777, 65542–65545, 69001–69005, 69147–69148, 71162–71164, 85845–85846, 85847 Lageado, Botucatu; MNRJ 69014–69016 Chácara Furlan, Botucatu; MNRJ 23976 Rubião Júnior, Botucatu; MZUSP 37797 Corumbataí; MZUSP 126104 Garça; MZUSP 143906 Usina Ester, Engenho Coelho; MZUSP 145474 PCH Eleutério, Espírito Santo do Pinhal.

Brazil: Estado de Minas Gerais: MNRJ 15973, 25785–25786 Es-tação Biológica Vereda Grande, Presidente Olegário; MNRJ 57513–5714 Fazenda Cascata (sede), Patos de Minas; MNRJ 38850–38851, 38855, 38858, 57364–57369, 58116–58118 Fazenda Gameleira, João Pinheiro; MNRJ 57370 Fazenda Rio Verde, João Pinheiro; MNRJ 75277–75281 Capão da Água Limpa, João Pinheiro; MNRJ 22097–22099 Uberlândia; MNRJ 25781 Alegre, Grão Mogol; MNRJ 25782–25784 Fazenda Cabral, Cristália; MNRJ 27258 Córrego do Gigante, Turmalina; MNRJ 65780 Peixe-Cru, Turmalina; MNRJ 35563 AHE Queimado; MNRJ 39654 Usina Hidrelétrica de Mi-randa, Indianópolis; MNRJ 49474 Ribeirão das Moendas, Pains; MNRJ 60813–60814 Fazenda Índia, Brumadinho; MNRJ 75109 Ibituruna; MNRJ 78651–78654 Sete Lagoas; MZUSP 33999 Lagoa Santa (topótipo); MZUSP 96031 Belo Horizonte.

Brazil: Estado de Goiás: MNRJ 24785 Catalão; MNRJ 17422–17423, 26015–26016 EFLEX (Estação Florestal Experimental), Sil-vânia; MNRJ 58119–58121 Santo Antônio do Descoberto; MNRJ 17421, MZUSP 80932–80933, 102211 Chapada dos Veadeiros; MZUSP 141230, 141232–141235, 141243, 145680–145682 Luziânia; MZUSP 141584–141585 PCH Santa Edwiges I, Mambaí; MZUSP 74996, 75002, 141598, 141602–141605 PCH Santa Edwiges II, Buritinópolis; MNRJ 38349–38352 Unaí (MG) e Formoso (GO); MZUSP 71383, 71743–71744, 72039, 72041, 72043 Serra da Mesa; MZUSP 74994–74995, 74997–75001, 75004, 75006, 75010, 75016, 75018, 75028 UHE Corumbá, Caldas Novas.

Brazil: Estado de Mato Grosso: MZUSP 66785, 143737, 143744–143747 Alto Araguaia.

Brazil: Distrito Federal: MNRJ 25794 Mata do Gedige, Brasília.Brazil: Estado de Tocantins: MZUSP 111703 Paranã.

Hypsiboas pardalisBrazil: Estado da Bahia: MNRJ 46836 Guaratinga.

Brazil: Estado do Espírito Santo: MNRJ 26023, 26884, 30082–30083, MBML 4204, 514, MZUSP 34056, 96036–96037 Santa Ter-esa; MBML 2578, 2581, 3992, 4076, 4536, 4714 Nova Lombardia, Santa Teresa; MNRJ 26083, MBML 60, 1194, 1195, 1553, 4325 Es-tação Biológica de Santa Lúcia, Santa Teresa; MBML 383 Bairro do Eco, Santa Teresa; MBML 3943, 3944, 3945 Alto Rio Saltinho, Santa Teresa; MBML 2576 Sítio Pousada Canaã, Santa Teresa; MBML 1124 Vila Nova, Santa Teresa; MBML 3596 Associação do Banestes, Santa Teresa; MNRJ 27958, MBML 6400, 6401, 6487, 6488, 6495, 6497 Reserva Biológica de Duas Bocas, Cariacica; MBML 6403, 6404, 6405, 6490, 6502, 6525, 6501, 6511 Alto, Reserva Biológica de Duas Bocas, Cariacica; MBML 6115 Cariacica; MNRJ 76937,

III


76945, 77050, MBML 1617 Parque Estadual do Forno Grande, Castelo; MBML 56, 7264 Castelo; MNRJ 1452 FLONA Goytacaz-es, Linhares; MNRJ 30866 Fazenda Oliveira, Guaçuí; MNRJ 26034 Fazenda dos Japoneses, Vargem Alta; MNRJ 13263, MBML 4912, 4913 Parque Municipal Goiapaba-açu, Fundão; MNRJ 38946 Alto Nova Almeida, Marechal Floriano; MBML 4449, 5753, 5754, 5929 Sítio Amarildo, Marechal Floriano; MNRJ 25816 Afonso Claudio; MNRJ 84029–84031, 84036 Domingos Martins; MBML 6625 Pedra Azul, Domingos Martins; MBML 6300, 6302, 6984, 6985 RPPN Oiutrem, Matilde, Alfredo Chaves; MBML 2081 Povoação de Bau-nilha, Córrego Santinho, Colatina; MBML 242 Crubixá-Mirim, Santa Leopoldina; MBML 3592 Pousada Vila Suíça, Santa Leopol-dina; MZUSP 200, 269, 2155 Rio Doce; MZUSP 7794 Sooretama.

Brazil: Estado de Goiás: MNRJ 128 “Goyaz”.Brazil: Estado de Minas Gerais: MNRJ 21885–21886, MZUSP

65261, 65270 Fazenda Montes Claros, Reserva Ecológica de Carat-inga, Caratinga; MNRJ 78252, 78253 Sítio 2, Chiador; MNRJ 78254 Sítio 3, Chiador; MNRJ 60833–60835 Mata dos Pena, Eugenópolis; MNRJ 67937 Paula Cândido; MNRJ 78224 Sítio 6, Além Paraíba; MNRJ 78256 Sítio 8, Além Paraíba; MNRJ 78258 Sítio 9, Além Paraíba; MNRJ 83925–83929 Fazenda Cachoeirão, Além Paraíba; MNRJ 63738 Além Paraíba; MNRJ 80517 UHE Guilman-Amorim, Antônio Dias; MZUSP 142533 PCH Cachoeira Grande, Antônio Dias; MZUSP 143554–143556 PCH Cocais Grande, Antônio Dias; MNRJ 25746 Estação Biológica Mata do Sossego, Simonésia; MNRJ 26017, 27502, 27551 Fazenda Olinda, São José, Belmiro Bra-ga; MNRJ 25818 Água Limpa, Juiz de Fora; MNRJ 18512 Torrões, Juiz de Fora; MNRJ 41736 Lagoa do Maximus, próximo a Santa Rita de Ouro Preto, Ouro Preto; MNRJ 38114, 66650, 66653, 68126 Viçosa; MNRJ 66651 Muriaé; MNRJ 22341 Reserva Biológica de Mar de Espanha, Mar de Espanha; MNRJ 70595 Fazenda da Prata, Sapucaia; MNRJ 50373 Mata de Gruta, Santana do Deserto; MNRJ 66652, 66654 Eugenópolis; MNRJ 41557–41559 Fazenda Cachoeira Alegre, Abre Campo; MZUSP 133782–133783, 133787 PARNA do Caparaó; MZUSP 137934, 137938–137942 UHE Fumaça, Mariana.

Brazil: Estado do Rio de Janeiro: MNRJ 79610 Paracambi; MNRJ 16865 Teresópolis; MNRJ 40610–40611 Reserva Ecológica de Guapiaçu, Cachoeiras de Macacu; MNRJ 21674, 21888, 25747, 25749 Morro Azul, Engenheiro Paulo de Frontin; MNRJ 81156–81157 Tinguá, Nova Iguaçu; MNRJ 53603, 53608–53609, 65579–65580 Taquara, Duque de Caxias; MNRJ 75289, 77028, 77030, 77031 Visconde de Mauá, Resende; MNRJ 73239–73240 Fazenda Marimbondo, Resende; MNRJ 70444–70445 Fazenda Barreto, Nova Friburgo; MNRJ 75818–75819 Theodoro de Oliveira, Nova Friburgo; MNRJ 66676–66678 Fazenda João Fernando, RJ 151, Valença; MNRJ 32978 Capela, Petrópolis; MNRJ 42500, 49771 CEDEA, Rocio, Petrópolis; MNRJ 2004, 25740 Petrópolis; MNRJ 37251 23k 0716614 UTM 756614, Sapucaia, Três Rios ou Mar de Espanha; MNRJ 63938–63939 Fazenda Santa Bárbara, P.E. Três Picos, Cachoeiras de Macacu; MNRJ 63693–63695, 73282 Duas Barras; MNRJ 75536, 75542 Volta Redonda; MNRJ 53948–53949 Vale da Revolta, Teresópolis; MNRJ 25778, MZUSP 95829–95831 Teresópolis; MNRJ 73290 PNM Fazenda Atalaia, Macaé; MNRJ 49635, 51056, 51066 Comendador Levy Gasparian; MNRJ 34532 Rialto, Barra Mansa; MNRJ 34530 Floriano, entrada do km 290, Via Dutra, Barra Mansa; MNRJ 16078 Patronato, Três Rios; MNRJ 25744 Acampamento Batista Carioca, Areal, Três Rios; MNRJ 50366 Área da PCH Santa Fé, Três Rios; MNRJ 49633–49634 Fa-zenda Canaã, Três Rios; MNRJ 66601 Lídice, Rio Claro; MNRJ 60822 Itaperuna; MNRJ 63715 Trajano de Moraes; MNRJ 25741–25742 Paraty; MNRJ 30869 Fazenda Barra da Água Limpa, Bom Jesus do Itabapoana, MZUSP 96011–96013 Itatiaia; MZUSP 62955 Miguel Pereira.

Brazil: Estado de São Paulo: MNRJ 78302 Aparecida; MZUSP 136806–136807 Parque das Neblinas, Bertioga; MZUSP 136233–

136234 Praia de Boracéia, Bertioga; MZUSP 127594, 134652–134654 Juquitiba; MZUSP 136519–136521 Parque Estadual de Carlos Bo-telho, São Miguel Arcanjo; MZUSP 76305 São Miguel Arcanjo; MZUSP 4075, 4571, 137462 Boracéia, Salesópolis; MZUSP 37659 Boracéia; MZUSP 133697 E.E. de Bananal; MZUSP 123503, 136394 Piedade; MZUSP 225, 76519, 95840, 95937–95947 Campo Grande da Serra; MZUSP 93277 Fazenda Intervales; MZUSP 95982 Serra da Bocaina; MZUSP 34476 Ferraz de Vasconcelos; MZUSP 117483, 117484 Ribeirão Grande.

Hypsiboas pugnaxVenezuela: ZUEC 9376 Mantecal; MZUSP 55649–55650 Guárico El Corozo Ranch, 50km N de Calabozo; MZUSP 109423–109425 Guárico Espino.

Colombia: MZUSP 54450–54451 Meta: Villavicencio; MHUA 3623, 3627, 3630, 3634 Antioquia, Gomez Plata, Hacienda Vegas de La Clara U de A; MHUA 4496 Córdoba, Ayapel, Vinícolas ICA; MHUA 7284 Antioquia, Maceo, Hacienda Santa Barbara.

Trinidad: MZUSP 14150 Saint Benedict NR Saint Joseph Northern Range.

Hypsiboas rosenbergiEcuador: Bulin: AL 4563–4564.

Ecuador: Província de Esmeraldas: MZUSP 10554 San Javier; MZUSP 106961 Cachavi; MZUSP 109518–109539 Cachavi.

Ecuador: Província de Pichincha: MZUSP 55602–55603 Centro Científico Rio Palenque.

Panama: Província do Panamá: MZUSP 114546—Canal Zone 7 mi N Miraflores.

Hypsiboas xerophyllusBrazil: Roraima: MNRJ 25837–25839, 25840–25841, 25843–25844, 25881–25882, MZUSP 21785, 21786, 65854 Pacaraima; MZUSP 62467 Serra da Saracura; MZUSP 65656, 65657, 65658, 65659, 65683, 65684 Ilha de Maracá; MZUSP 65756 Marco de Fronteira BV8, Uiramutã; MZUSP 65930, 65942, 68588, 68589, 68590, 68619, 68620 Mucajaí; MZUSP 66027, 69779, 69780 Tepequem, Amajari; MZUSP 66030 Fazenda Salvamento; MZUSP 68666, 68667, 68668, 68669, 68670, 68671, MPEG 7761, 7762, 7763 Caracaraí; MZUSP 68757, MPEG 1037, 1069, 1070, 1073, 1074, 1075 Boa Vista; MZUSP 68876 Bonfim; MZUSP 117656 Uranduíque; MZUSP 121596 Fa-zenda São Marcos; MZUSP 140583, 140584, 140585, 140586, 140587 Serra do Tepequem; INPA 19130, 19131, 19133, 19134, 19135, 19136, 19137, 19165, 19166 PARNA do Viruá; MPEG 7715, 7899, 7928 Rio Ajarani, BR 210, Iracema.

Colombia: Meta: MZUSP 54450, 109427, 109428 Villavicencio; AL-MN 4765 “Palomina” (Possibly Palomino, Colombia); MZUSP 58685 Magdalena, Cañaveral, Parque Nacional Tayrona; MHUA–A 1911, 1915 Santander, Carmen de Chuqurí, Vereda La Bode-ga; MHUA-A 2067 Antioquia, Puerto Berrio, Hacienda la Suiza; MHUA-A 2406, 2596, 2653, 4818, 4840 Antioquia, Maceo, Vere-da Las Brisas; MHUA-A 5910 Caldas, Norcasia, Hacienda El Val-le; MHUA-A 6517 Antioquia, San Roque, Vereda La Providencia; MHUA-A 6541 Antioquia, Nariño, Vereda Puente Linda; MHUA-A 6663 Antioquia, San Francisco, Vereda La Lora; MHUA-A 6713 Tolima, Falan, Vereda La Roca; MHUA-A 6899 Caldas, Pensilva-nia, Vereda La Esperanza; MHUA-A 7019–21 Antioquia, Nariño, Vereda Puente Linda.

Panama: AL-MN 4770 San Pablo.Trinidad: MZUSP 14150 Saint Joseph.Venezuela: Guárico: MZUSP 55649 Calabozo; MZUSP 109423

Espino; Sucre: MZUSP 109426 Playa Colorada; Tabay: MZUSP 76444 Mérida; Aragua: AL-MN 1209 Maracay; ZUEC 9384 Santa Bárbara; Táchira: ZUEC 9135 Uribante; ZUEC 9413–9414, 9418 No further locality.

IV

Online Supplementary data – Victor G. D. Orrico et al.

Supplementary document 2. Voucher information, localities, and GenBank accession numbers for the specimens analyzed for this study. [a] Voucher information for 12S ; [b] Voucher information for COI.

Sample ID Locality Voucher 12S COI

H. crepitans Grão Mogol, Minas Gerais, Brazil CFBH 10243 KX697938 KX697985H. crepitans “Bahia”, Brazil CFBH 13275 KX697941 KX697988H. crepitans Campo Alegre, Alagoas, Brazil CFBH 16361 KX697945 KX697992H. crepitans Aurelino Leal, Bahia, Brazil CFBH 18728 KX697950 KX697997H. crepitans Caetité, Bahia, Brazil CFBH 21073 KX697948 KX697995H. crepitans Dom Basílio, Bahia, Brazil CFBH 21090 KX697949 KX697996H. crepitans Jaboticatubas, Minas Gerais, Brazil CFBH 24368 KX697953 KX698000H. crepitans Camamu, Bahia, Brazil CFBH 27826 KX697959 KX698006H. crepitans Itabuna, Bahia, Brazil CFBH 2885 KX697939 KX697986H. crepitans Piranhas, Alagoas, Brazil CFBH 2966 AY843621 – H. crepitans Mucugê, Bahia, Brazil JC 1273 KX697967 KX698013H. crepitans Jussari, Bahia, Brazil MRT 5785 KX697969 KX698015H. crepitans Januária, Minas Gerais, Brazil MTJ 384 KX697971 KX698017H. crepitans Buíque, Pernambuco, Brazil MTR 15366 KX697972 KX698018H. crepitans Miguel Calmon, Bahia, Brazil MTR 20070 KX697976 KX698022H. “xerophyllus” Haute Wanapi, French Guiana, France 552PG KX697932 KX697979H. “xerophyllus” Boa Vista, Roraima, Brazil CFBH 29144 KX697961 KX698008H. “xerophyllus” Mont Saint Marcel, French Guiana, France isolate BM095 KX697962 KX698011H. “xerophyllus” E.E.Maracá, Roraima, Brazil MTR 20407 KX697977 KX698023H. “xerophyllus” Pacaraima, Roraima, Brazil MTR 20730 KX697978 KX698024H. “xerophyllus” Kurupukari, Guyana ROM 20560 JN970517 JN970772H. “xerophyllus” Paramakatoi, Guyana ROM 28436 JN970518 JN970773H. “xerophyllus” Parish_Hill, Guyana ROM 44089 JN970519 JN970774H. “xerophyllus” “Igarapé Cocal”, Brazil USNM 302400 DQ380354 – H. albomarginatus Ilhéus, Bahia, Brazil MTR 16695 KX697975 KX698021H. albomarginatus_q [a] Caruaru, Pernambuco, Brazil;

[b] Juiz de Fora, Minas Gerais, Brazil[a]USNM 284519; [b]CF-BHT13378

AY549316 KX698009

H. cinerascens [a] Iwokrama, Guyana; [b] Unknown

[a]AMNH A-164105; [b] JF isolate 2371

AY549336 KX698010

H. ericae [a;b] Alto Paraiso de Goiás, Goiás, Brazil [a]CFBH 3599; [b]CFBH 6764 AY549332 KX698012H. exastis Arataca, Bahia, Brazil MTR 16289 KX697973 KX698019H. faber Uruçuca, Bahia, Brazil CFBH 13030 – KX697980H. faber São Carlos, São Paulo, Brazil isolate 118 – JQ627303H. faber San Vicente, Guarani, Argentina MACN 36999 AY549333 – H. faber San Vicente, Guarani, Argentina MACN 37000 AY549334 – H. faber Varzedo, Bahia, Brazil MTR 16691 KX697974 KX698020H. faber Salesópolis, São Paulo, Brazil USNM 303034 DQ380356 – H. lanciformis [a] Alpahuayo, Loreto, Peru;

[b] Shaime, Zamora-Chincipe, Ecuador[a] MJH 564; [b] isolate 18237 AY843636 JN970768

H. lundii Assis, São Paulo, Brazil CFBH 20059 KX697944 KX697991H. lundii Brasília, Distrito Federal, Brazil CFBH 22795 KX697956 KX698003H. lundii Belo Horizonte, Minas Gerais, Brazil CFBH 22814 KX697957 KX698004H. lundii Campo Limpo de Goiás, Goiás, Brazil CFBH 23593 KX697951 KX697998H. lundii Lagoa Santa, Minas Gerais, Brazil CFBH 24355 KX697952 KX697999H. lundii São Carlos, São Paulo, Brazil CFBH 26853 KX697954 KX698001H. lundii Rio Claro, São Paulo, Brazil CFBH 4000 AY843639 – H. lundii Costa Rica, Mato Grosso do Sul, Brazil CFBH 7280 KX697934 – H. lundii São Roque de Minas, Minas Gerais, Brazil CFBH 9154* KX697936 KX697983H. lundii Alto Paraíso, Goiás, Brazil CFBH 9324 KX697937 KX697984

V


Sample ID Locality Voucher 12S COI

H. lundii Paranã, Tocantins, Brazil MRT 4332 KX697968 KX698014H. lundii Petrolina de Goiás, Goiás, Brazil MRT 8417 KX697970 KX698016H. multifasciatus Demerara, Guyana AMNH A-141040 AY843648 AY843648H. pardalis Domingos Martins, Espírito Santo, Brazil CFBH 11334 KX697940 KX697987H. pardalis Petrópolis, Rio de Janeiro, Brazil CFBH 13962 KX697942 KX697989H. pardalis São Luis do Paraitinga, São Paulo, Brazil CFBH 16020 KX697935 KX697982H. pardalis Maringá, Rio de Janeiro, Brazil CFBH 17542 KX697946 KX697993H. pardalis Santa Leopoldina, Espírito Santo, Brazil CFBH 18002 KX697947 KX697994H. pardalis Teresópolis, Rio de Janeiro, Brazil CFBH 22027 KX697955 KX698002H. pardalis Mimoso do Sul, Espírito Santo, Brazil CFBH 25503 KX697958 KX698005H. pardalis Cachoeiras de Macacu, Rio de Janeiro, Brazil CFBH 27405 KX697960 KX698007H. pardalis São Luis do Paraitinga, São Paulo, Brazil CFBH 6499 KX697933 KX697981H. pardalis Itatiaia, Rio de Janeiro, Brazil CFBHT4595 KX697943 KX697990H. pardalis Salesópolis, São Paulo, Brazil USNM 303046 AY843651 – H. pellucens San Juan, Pichincha, Ecuador WED 53621 AY326058 AY326058H. pugnax Ayapel, Córdoba, Colombia MRC 510 KX697963 – H. pugnax Gómez Plata, Antioquia, Colombia MRC 513 KX697964 – H. pugnax Norcasia, Caldas, Colombia MRC 514 KX697965 – H. pulchellus Buenos Aires, Buenos Aires, Argentina MACN 37788 AY549352 – H. punctatus Resistencia, Chaco, Argentina MACN 37792 AY549353 – H. rosenbergi E Pedernales, Manabi, Ecuador KU 217629 AY819438 – H. rosenbergi Maceo, Antioquia, Colombia MRC 508 KX697966 – H. rufitelus [a;b] El Cope, Cocle, Panama [a] KRL 798; [b] USNM 572699 AY843662 FJ766740

Supplementary document 3. Standardized coefficients and factor loadings (r) from a Principal Component Analysis (CDA; Fig. 3) for 16 morphometric characters of two Operational Taxonomic Units (OTUs) of Hypsiboas crepitans. Cum. Prop. = cumulative proportion of eigenvalues.

MeasurementsMales Females

PC1 PC2 r (PC1) r(PC2) PC1 PC2 r (PC1) r(PC2)

SVL -0.051259 -0.019337 -0.903869 -0.340971 -0.056931 0.001937 -0.975977 0.033204HL -0.049143 -0.017838 -0.871643 -0.316396 -0.049324 0.002171 -0.946597 0.041662HW -0.049520 -0.017450 -0.910738 -0.320932 -0.052074 -0.002213 -0.967214 -0.041107NSD 0.033115 -0.092269 0.312513 -0.870765 -0.032079 0.042403 -0.470261 0.621610IND -0.055426 0.017232 -0.625668 0.194523 -0.037001 0.002607 -0.738501 0.052041UEW -0.034914 -0.040303 -0.494884 -0.571283 -0.047864 0.019396 -0.718680 0.291226ED -0.043462 -0.020399 -0.777362 -0.364856 -0.043967 -0.003470 -0.891364 -0.070353IOD -0.142854 0.058591 -0.896194 0.367574 -0.057721 -0.092086 -0.522806 -0.834058END -0.032284 -0.022338 -0.586094 -0.405529 -0.046775 0.006113 -0.882090 0.115281TD -0.027915 -0.031178 -0.513080 -0.573040 -0.054854 0.010522 -0.835374 0.160242FHL -0.052215 -0.018928 -0.855917 -0.310264 -0.054793 -0.003064 -0.919238 -0.0513964FD -0.041548 -0.029878 -0.693932 -0.499026 -0.053960 0.018977 -0.835099 0.2936864TD -0.039945 -0.031080 -0.648998 -0.504972 -0.052089 0.000047 -0.946296 0.000861THL -0.050017 -0.015955 -0.907767 -0.289567 -0.051758 0.000801 -0.943330 0.014607CL -0.047836 -0.015795 -0.891682 -0.294418 -0.050472 -0.000944 -0.946317 -0.017696FL -0.050864 -0.014523 -0.911669 -0.260300 -0.048540 0.026065 -0.758781 0.407444Eigenvalue 0.050425 0.019683 0.039746 0.011885Cum. Prop 57.2663 79.6201 63.0218 81.8662

integrative taxonomy supports the existence of two ... · 101 taxonomy of hypsiboas crepitans...

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