Abstract Abstract
Among Neotropical microhylids, the genus Chiasmocleis is exceptionally diverse. Most species of Chiasmocleis were described in recent years based on external morphology, but recent studies using molecular data did not support the monophyly of the species groups clustered based on feet webbing. Furthermore, a phylogeographic study of C. lacrimae estimated high genetic divergence and low gene flow among populations across small geographic ranges. Increasing the molecular and geographic sampling, and incorporating morphological data, we identified new cryptic species. Herein, we used novel genetic and morphological data to describe a new species of Chiasmocleis.
Keywords: Amphibians, Chiasmocleis quilombola sp. n., cryptic species, phylogenetics, systematics
Introduction
The diversity of evolutionary lineages with little phenotypic differences (i.e., cryptic species) might be better understood in the light of genetic delimitation of evolutionary units (Thomé et al. 2012, Hambäck et al. 2013). Recent molecular phylogenies of anuran, including work on species from the Brazilian Atlantic Forest, did not recovered as monophyletic the species groups clustered based mostly on morphology (Amaro et al. 2009, Canedo and Haddad 2012, Fouquet et al. 2012, Thomé et al. 2012).
Species are segments of population level evolutionary lineages and do not necessarily need to be phenetically distinguishable, diagnosable, monophyletic, intrinsically reproductively isolated, ecologically divergent, or anything else to be considered species, but they only have to be evolving separately from other lineages (de Queiroz 1998, de Queiroz 2007).
A recent molecular phylogeny (de Sá et al. 2012) recovered a polyphyletic Chiasmocleis and, to render the genus monophyletic, transferred one species to Elachistocleis and three species to Syncope. Recently, Peloso et al. (2014) placed Syncope in the synonymy of Chiasmocleis. Chiasmocleis is the most diverse genus of Neotropical microhylids, with 29 species distributed throughout Amazonia, Atlantic Forest, and open areas in South America, such as the Brazilian Cerrado and the Chaco of Bolivia and Paraguay (Cruz et al. 1997, de Sá et al. 2012, Peloso et al. 2014).
Tonini et al. (2013) in a phylogeographic analysis estimated high genetic divergence and low gene flow among populations of Chiasmocleis lacrimae (described as Chiasmocleis carvalhoi Cruz et al. 1997) in the Brazilian Atlantic Forest. Samples of two potential new species and of “Chiasmocleis capixaba” with less feet webbing were included as populations of Chiasmocleis lacrimae. Moreover, the study suggested that populations isolated-by-distance could represent recently diversified species, estimated to Miocene and Pliocene. Increasing the sampling along the distribution of Chiasmocleis lacrimae and Chiasmocleis capixaba and using additional molecular and morphological data, we were able to differentiate the phylogenetic structure and morphological differences associate to intraspecific and interspecific variation. We found that Chiasmocleis lacrimae and Chiasmocleis capixaba were not recovered as monophyletic, in fact populations corresponding to undescribed distinct evolutionary lineages. Although these undescribed lineages have similar body size and shape, and low nuclear divergence, they are exceptionally divergence in mitochondrial markers and are geographically structured.
Herein, we describe a new species of Chiasmocleis from the Atlantic Forest of southeastern Brazil and present a phylogenetic hypothesis for the species group.
Material and methods
Specimens and tissues used herein and comparative material are deposited in the following collections: 1) CFBH; 2) MNRJ; 3) Museu de Zoologia, Universidade de São Paulo, São Paulo, São Paulo State, Brazil; 4) MBML; 5) CTA and LGA; 6) RN and CTRN. Field numbers correspond to M. T. Rodrigues (MTR), Universidade de São Paulo, São Paulo, São Paulo State, Brazil; P. Rocha (PEU), Universidade Federal da Bahia, Salvador, Bahia State, Brazil; and J. F. R. Tonini (JFRT), vouchers are at UFES. Specimens examined and tissues samples are listed in Appendix 1 and 2, respectively, and sample localities are shown in Figure 1.
Figure 1.
Sample localities of A tissues and B specimens included in the present study. Sites with more than one color indicates syntopy. List of localities: 1 Porto Seguro, 2 Trancoso, 3 ReBio Córrego Veado, 4 FloNa do Rio Preto (type locality of Chiasmocleis quilombola sp. n.), 5 Parque Estadual de Itaúnas, 6 ReBio Sooretama, 7 Reserva Natural Vale, 8 Povoação, 9 FloNa dos Goytacazes, 10 Costa Bela, 11 ReBio Duas Bocas, 12 Guarapari, 13 Mata da Usina Paineiras, 14 Mimoso do Sul, 15 ReBio União, 16 Cachoeiras de Macacu, 17 Duque de Caxias, 18 Angra dos Reis, 19 Picinguaba, 20 Ilha de São Sebastião, 21 Bertioga, 22 Aracruz (type locality of Chiasmocleis capixaba), 23 Horto Florestal (type locality of Chiasmocleis lacrimae). Blue lines represent major coastal rivers, from North to South: Jequitinhonha, Mucuri, Doce, and Paraíba do Sul. BA = Bahia State, ES = Espírito Santo State, RJ = Rio de Janeiro State, SP = São Paulo State, and MG = Minas Gerais State.
The following measurements were adapted from Duellman (2001) and Peloso and Sturaro (2008); measurements were taken for 56 individuals with a digital caliper under a stereomicroscope to the nearest 0.1 mm: SVL; HDL; HDL4; HL; HW; ED; IOD; IND; END; THL; TBL; FAL; FL; 3FD; 4TD. Fingers and toes are numbered and abbreviated as follows: Fingers I–IV = FI–IV, Toes I–V = TI–V.
Molecular Analyses: Total genomic DNA was extracted from ethanol-preserved liver or muscle tissues using Qiagen DNeasy kit (Valencia, California, USA). We used four molecular markers (mtDNA: 12S, 16S, and NADH dehydrogenase subunit 2 [ND2]; nucDNA: brain-derived neurotrophic factor [BDNF]), amplified using previously published primer sets and PCR profiles (de Sá et al. 2012, Tonini et al. 2013). We performed a multiple loci alignment using an iterative procedure to compute a series of alignment/tree pairs in SATé-II (Liu et al. 2012), using default settings. GenBank accession numbers are given in Appendix 2.
The following outgroup were chosen based on published phylogenies including species of Chiasmocleis (de Sá et al. 2012): Chiasmocleis leucosticta, Chiasmocleis mantiqueira, Chiasmocleis crucis, Chiasmocleis schubarti, and Chiasmocleis cordeiroi. We selected a total of 100 samples (ingroup includes 69 samples) for a data set consisting of 2,473 base pairs. The best partition schemes and substitution models (Table 1) were chosen using PARTITION FINDER v1.1.1 (Lanfear et al. 2012) and used in phylogenetic analysis downstream.
Table 1.
Best partition scheme and substitution models selected using Partition Finder.
| Subset | Best Model | Subset partitions | Subset sites |
|---|---|---|---|
| 1 | HKY+I+G | 12S | 1–700 |
| 2 | HKY+G | 16S, ND2_1 | 701–1044, 1661–2473\3 |
| 3 | K80+I | BDNF | 1045–1660 |
| 4 | HKY+G | ND2_2 | 1662–2473\3 |
| 5 | GTR+G | ND2_3 | 1663–2473\3 |
We applied two approaches of phylogenetic estimation: 1) Maximum Likelihood (ML) and 2) Bayesian inference (BI) using the dataset containing the markers 12S, 16S, ND2, and BDNF. Maximum Likelihood in RAXML v7.2.8 (Stamatakis 2006) used a rapid-bootstrap with 1000 replications. Bayesian Inference in BEAST v1.7.4 (Drummond et al. 2012) used birth-death process as tree prior, linked tree models across partition, relaxed clock model with linked mitochondrial markers, but not the nuclear gene. The BI analysis ran for 50 million generations and the parameters were sampled every 5,000 generations producing a total of 10,000 trees. We discarded the first 1,000 trees as burnin in TREEANOTATOR. The output file was checked using TRACER v1.5 and values of Effective Sample Size >200 were considered suitable. Nodes having bootstrap values >70 in ML and posterior probabilities >0.95 in BI were considered as well supported. Analyses were performed through Cipres (Miller et al. 2010) and trees were visualized and edited using FIGTREE. Data available from the Dryad Digital Repository: http:// 10.5061/dryad.gm41t. Genetic distance (p-uncorrected) was calculated in MEGA5.0 (Tamura et al. 2011). A second species awaits description (Forlani et al. submitted) and it is referred throughout this manuscript as Chiasmocleis sp.
Results
The phylogenetic hypotheses generated through ML (Figure 2) and the BI (Figure 3) resulted in similar topology. The ML tree (Figure 2) supported two new species as sister group of Chiasmocleis capixaba, Chiasmocleis lacrimae correspond to a basal node; whereas in the BI tree (Figure 3) Chiasmocleis capixaba was estimated as sister to Chiasmocleis lacrimae, but the posterior probability of this node was lower than 0.95. Both the ML and BI trees showed clades of Chiasmocleis leucosticta, Chiasmocleis mantiqueira, Chiasmocleis crucis, Chiasmocleis schubarti, and Chiasmocleis cordeiroi, but not Chiasmocleis lacrimae and Chiasmocleis capixaba (Figure 2, 3). Populations of Chiasmocleis capixaba and Chiasmocleis lacrimae from the north of the Espírito Santo State, as well as populations of Chiasmocleis lacrimae from southern areas of the Bahia State, would represent two new cryptic lineages closely related to Chiasmocleis lacrimae and Chiasmocleis capixaba. In the ML analysis populations from southern Espírito Santo formed a clade that makes Chiasmocleis lacrimae polyphyletic (Figure 2), whereas in the BI these populations formed a clade including also populations of Chiasmocleis lacrimae from the states of São Paulo and Rio de Janeiro (Figure 3). However, given the lack of support for this node in both analyses, basing taxonomic change on the presumed polyphyly is not warranted at present.
Figure 2.
Maximum likelihood tree including 12S, 16S, ND2, and BDNF. Node numbers correspond to bootstrap, values >70 indicate good support. Although Chiasmocleis lacrimae may not represent a monophyletic species, bootstrap values are low to make further assumptions. Numbers after underscore symbol correspond to localities present in Figure 1. Scale bar represents number of substitutions/site.
Figure 3.
Phylogenetic hypothesis obtained through Bayesian Inference using 12S, 16S, ND2, and BDNF. Node numbers correspond to posterior probabilities, values >0.95 indicate good support. Numbers after underscore symbol correspond to localities present in Figure 1. Scale bar represents number of substitutions/site.
Therefore, our results show that the new species clusters within the genus Chiasmocleis.
Description of a new species
Chiasmocleis quilombola sp. n.
http://zoobank.org/81CD38A6-72C6-4CAF-A4AC-45C011459A0E
Figure 4.
Chiasmocleis quilombola sp. n. in vivo. A male (holotype: MZUSP147478) and B female (MZUSP147479, paratopotype). Not in scale.
Holotype.
MZUSP147478, adult male, collected at the Floresta Nacional do Rio Preto (Figure 4A), Municipality of Conceição da Barra, Espírito Santo State, Brazil (18°21'19"S, 39°50'39"W), collected on December 8-16, 2009, by L. P. Costa, J. F. R. Tonini, J. Dalapicolla, R. Duda, and C. M. Mattedi.
Paratopotypes.
Males: MZUSP147471–73, MZUSP147475–76, MZUSP147494; female: MZUSP147479 (Figure 4B), Municipality of Conceição da Barra, Espírito Santo State, Brazil (18°21'19"S, 39°50'39"W), collected on December 8-16, 2009, by L. P. Costa, J. F. R. Tonini, J. Dalapicolla, R. Duda, and C. M. Mattedi.
Diagnosis.
A small-sized species of Chiasmocleis (males SVL mean= 14 ± 1.4 mm; female SVL = 17.1 mm), diagnosed by the following combination of characters: (1) body slender; (2) snout rounded in lateral and dorsal views; (3) all fingers slightly fringed, not webbed, in males and female; (4) all toes fringed and slightly webbed in males and female; (5) dermal spines on fingers and toes of males can be present or absent, absent in female; (6) dermal spines on dorsal surface of males can be present or absent, absent in female; (7) dermal spines absent on ventral surface in males and female; (8) dermal spines on chin and snout of males can be present or absent, absent in female; (9) dermal spines over outer surfaces of legs and cloaca in males can be present or absent, absent in female; (10) female has para-cloacal glands; (11) incomplete occipital fold; (12) vocal slits present in males; (13) dorsal coloration brown; (14) medial ventral body surface light cream colored, whereas ventrolateral surfaces have a light brown and cream marbled pattern; (15) ventral surfaces of fore and hind limbs with a homogeneously and finely dark pattern over a cream background; (16) dorsal surface of fore and hind limbs light brown with a few cream spots or blotches, more distinct on the fore limbs; (17) male throat infuscate; (18) mid-dorsal and/or line on posterior surface of thighs may be present; and (19) tympanum indistinct.
Description of holotype.
Body small (SVL = 15.7 mm), slender, slightly ovoid (Figure 5); head triangular in shape, broader than long; snout short, tip of snout rounded (Figure 5A–B); nostrils located closer to the tip of snout than to eye, not protuberant, directed laterally (Figure 5C); inter-nostril distance smaller than eye–nostril distance and smaller than eye diameter; canthus rostralis slightly defined; loreal region slightly convex; lips not flared; eyes small, slightly protruding; inter-orbital area flat; incomplete occipital fold; tympanum indistinct; upper jaw projecting beyond lower one; tongue large, elongate, and laterally free; premaxillae, maxillae, and vomerine teeth absent; choanae small, rounded, widely separated, positioned anterolaterally to eye; vocal slit present.
Figure 5.
Holotype of Chiasmocleis quilombola sp. n. (MZUSP 147478). A Dorsal B ventral, and C lateral views D right hand and E right foot. White bars = 1 mm.
Arms slender, lacking tubercles on forearm. Hands not webbed (Figure 5D); fingers tips rounded, not expanded, and slightly fringed; fingers lacking dermal spines; finger lengths I<II<IV<III; thumb without nuptial asperities; subarticular tubercles well developed and rounded, proximal subarticular tubercles larger than others; supernumerary tubercles absent; thenar tubercle well developed, ovoid, and at the base of finger I; two palmar tubercles, a rounded inner tubercle and an elongated outer one (Figure 5D). Legs short, moderately robust; knee and heel lacking tubercles; tibial and tarsal ridges absent. Foot slightly webbed (Figure 5A–B, E); toes slightly fringed; toe tip rounded lacking disks; subarticular tubercles well developed, ovoid; supernumerary tubercles absent; an oval inner, but no outer, metatarsal tubercle. Toe lengths I<II<V<III<IV; toes lacking dermal spines; tibia length slightly shorter than thigh length; combined thigh and tibia lengths approximately 82.8% of snout-vent length; foot length approximately 43.9% of snout-vent length.
Skin smooth, dorsal surfaces of body lacking dermal spines. Throat black and few dermal spines found on chin and snout (Figure 5B). Cloaca lacks para-cloacal tubercles or glands.
Coloration in preservative.
Dorsum dark brown with a few small cream spots and blotches; dorsal surface of limbs dark brown with cream blotches and small spots, particularly on the proximal forelimb; palm of hands marbled brown and pale cream, foot dark brown; belly surface cream, dorsolateral and ventral surfaces with a marbled pale brown and cream pattern; throat dark brown to black. Ventral surface of thighs light brown with a finely reticulated dark pattern over a cream background cream with a few cream spots more evident close to the edges; ventral surfaces of tibia and tarsus finely marbled in light brown with cream, lighter than the dorsal surface. Absence of distinct lines on the body and limbs.
Measurements of holotype
(in mm). SVL 15.7; HDL 3.4; HDL4 2.3; HL 2.7; HW 4.5; ED 1.3; IOD 2.8; IND 1.1; END 1.2; THL 6.5; TBL 6.4; FL 6.9, FAL 3.2; 3FD 0.3; 4TD 0.4.
Variation in the type series.
Measurements data of the type series are given in Table 2 and information of the comparative material are provided in Appendix 1. Overall, the type series agrees with the holotype coloration; one specimen has a mid-dorsal line and a line on the posterior surface of the thighs and also more dermal spines (MZUSP147475). The incomplete occipital fold varied from indistinct to weakly visible laterally (= incomplete). The combined mean thigh and tibia length represents approximately 81% of mean snout-vent length in males, and 77.7% in females; foot length approximately 41.6% of snout-vent length in males and 39.7% in females.
Table 2.
Morphometric measurements (mm) of the type series of Chiasmocleis quilombola sp. n.
| Specimen | Type | Sex | SVL | HL | HW | ED | IOD | IND | END | THL | TBL | FL | 3FD | 4TD | FAL | HDL | HDL4 |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| MZUSP147471 | Paratype | Male | 14.4 | 2.8 | 3.8 | 1.0 | 2.6 | 1.1 | 1.5 | 6.1 | 6.3 | 6.2 | 0.3 | 0.3 | 3.0 | 2.8 | 1.8 |
| MZUSP147472 | Paratype | Male | 15.3 | 2.8 | 4.1 | 1.3 | 2.7 | 1.2 | 1.3 | 7.1 | 6.6 | 6.6 | 0.3 | 0.4 | 3.2 | 3.4 | 2.2 |
| MZUSP147473 | Paratype | Male | 16.1 | 3.2 | 3.9 | 1.1 | 2.2 | 1.1 | 1.3 | 6.0 | 6.0 | 6.4 | 0.2 | 0.2 | 3.2 | 3.3 | 2.1 |
| MZUSP147475 | Paratype | Male | 14.5 | 2.8 | 4.6 | 1.3 | 2.6 | 1.3 | 1.3 | 6.6 | 6.4 | 6.7 | 0.4 | 0.4 | 3.3 | 3.5 | 2.2 |
| MZUSP147476 | Paratype | Male | 16.1 | 2.7 | 4.4 | 1.2 | 2.7 | 1.3 | 1.4 | 6.7 | 6.3 | 6.1 | 0.3 | 0.5 | 3.0 | 3.3 | 1.8 |
| MZUSP147478 | Holotype | Male | 15.7 | 2.8 | 4.5 | 1.3 | 2.8 | 1.1 | 1.3 | 6.6 | 6.5 | 6.9 | 0.4 | 0.4 | 3.2 | 3.5 | 2.3 |
| MZUSP147494 | Paratype | Male | 16.6 | 3.1 | 4.6 | 1.4 | 2.6 | 1.2 | 1.4 | 7.0 | 6.9 | 7.6 | 0.3 | 0.4 | 3.3 | 3.8 | 2.4 |
| MZUSP147479 | Paratype | Female | 17.2 | 2.9 | 4.6 | 1.3 | 2.9 | 1.3 | 1.4 | 6.7 | 6.6 | 6.8 | 0.3 | 0.4 | 3.3 | 3.5 | 2.3 |
Abbreviations: SVL = snout-vent length; HDL = hand length; HDL4 = hand length from the base of the thenar tubercle to the tip of the fourth finger; HL = head length; HW = head width; ED = eye diameter; IOD = inter-orbital distance; IND = inter-nostril distance; END = eye-nostril distance; THL = thigh length; TBL = tibia length; FAL = forearm length; FL = foot length; 3FD = diameter of third finger disk; 4TD = diameter of fourth toe disk. For tissues numbers see Appendix 2.
Etymology.
The specific epithet quilombola refers to people who inhabit quilombo communities. Historically, quilombos were communities constituted by and used as refuges for escaped slaves between 1530 and 1815 during colonial Portuguese rule in Brazil. Nowadays in the north of Espírito Santo Estate quilombola communities still remain and maintain alive their traditions, such as quilombola food and craftwork. This species' name is indeclinable.
Distribution.
Chiasmocleis quilombola sp. n. is known from localities between the Doce River and the Mucuri River, e.g., Floresta Nacional do Rio Preto and Parque Estadual de Itaúnas, Municipality of Conceição da Barra; Reserva Biológica Córrego Veado, Municipality of Pinheiros; Reserva Natural, Reserva Biológica de Sooretama, and Cocoa plantations in Povoação, Municipality of Linhares (Appendix 2). The populations assigned to Chiasmocleis lacrimae and Chiasmocleis capixaba at northernmost of Espírito Santo State are allocated to the new taxon Chiasmocleis quilombola sp. n. (Figure 1).
Natural history.
Chiasmocleis quilombola sp. n. was collected in pitfall traps after heavy rains at Floresta Nacional do Rio Preto (Figure 6). The lines of pitfalls were installed at the vicinity of a permanent lagoon and a temporary swamp. The Floresta Nacional do Rio Preto has 2,830 ha and an elevation between five to 50 m above the sea level. The soil is typical of coastal areas, mostly sand. The area consists of secondary forested areas and plantations with few remnants of primary Atlantic Forest.
Figure 6.
Larissa Gaigher and Dr. Yuri Leite inspecting pitfall traps installed at the type locality of Chiasmocleis quilombola sp. n., Floresta Nacional do Rio Preto, Municipality of Conceição da Barra, Espírito Santo State, Brazil.
Discussion
Chiasmocleis quilombola sp. n. has been misidentified as Chiasmocleis lacrimae and Chiasmocleis capixaba due to an overlap in feet webbing and body size (e.g., Tonini et al. 2013, see below). Chiasmocleis quilombola sp. n. corresponds to clade N2, Chiasmocleis sp. to clade N1, Chiasmocleis capixaba to central clade, and Chiasmocleis lacrimae to southern clades of Tonini et al. (2013). Our morphological observations and comparisons with other species combined with molecular information support Chiasmocleis quilombola sp. n. and Chiasmocleis sp. as separate evolutionary lineages (see below and Figure 1, 2). Low levels of genetic divergence in the BDNF (Table 3) between Chiasmocleis quilombola sp. n. and closely related species is consistent with recent cladogenetic events and supports a previous study that estimated initial speciation within this clade (i.e., Chiasmocleis lacrimae, Chiasmocleis capixaba, Chiasmocleis quilombola sp. n., and Chiasmocleis sp.) during the Miocene/Pliocene (Tonini et al. 2013). Chiasmocleis quilombola sp. n. and Chiasmocleis sp. corresponds to an earlier lineage split dated to approximately the Pliocene/Pleistocene (Tonini et al. 2013).
Table 3.
Genetic distance (p-uncorrected) in the BDNF (upper-right) and in the ND2 (lower-left) among Chiasmocleis quilombola sp. n. and sister species. Values at the diagonal correspond to the genetic distance within species in the ND2.
| Species | Chiasmocleis capixaba | Chiasmocleis lacrimae | Chiasmocleis cordeiroi | Chiasmocleis crucis | Chiasmocleis quilombola sp. n. | Chiasmocleis schubarti | Chiasmocleis sp. |
|---|---|---|---|---|---|---|---|
| Chiasmocleis capixaba | 0.015 | 0.001 | 0.008 | 0.008 | 0.001 | 0.007 | 0.003 |
| Chiasmocleis lacrimae | 0.064 | 0.044 | 0.008 | 0.008 | 0.001 | 0.007 | 0.003 |
| Chiasmocleis cordeiroi | 0.211 | 0.227 | 0.013 | 0.005 | 0.008 | 0.004 | 0.007 |
| Chiasmocleis crucis | 0.182 | 0.198 | 0.108 | 0.015 | 0.008 | 0.005 | 0.007 |
| Chiasmocleis quilombola sp. n. | 0.071 | 0.082 | 0.217 | 0.209 | 0.006 | 0.007 | 0.004 |
| Chiasmocleis schubarti | 0.206 | 0.204 | 0.107 | 0.103 | 0.22 | 0.017 | 0.007 |
| Chiasmocleis sp. | 0.098 | 0.104 | 0.253 | 0.237 | 0.083 | 0.236 | 0.023 |
Chiasmocleis quilombola sp. n. is distinct from Chiasmocleis schubarti (species with which occurs in sympatry) in having smaller snout-vent length, feet slightly webbed, cream ventral surface, and marbled light brown and cream dorsolateral pattern instead of larger snout-vent length, absence of feet webbing and belly pattern roughly marbled in dark brown and light cream in Chiasmocleis schubarti (Cruz et al. 1997). Chiasmocleis quilombola sp. n. is most similar to Chiasmocleis lacrimae and Chiasmocleis capixaba, species with which it has been previously confused (e.g. Tonini et al. 2013). However, the new species is distinguished from closely relatives by the following set of characters: 1) a smaller body size, shorter head length, shorter thigh and tibia compared to Chiasmocleis lacrimae, Chiasmocleis capixaba, and Chiasmocleis sp. (Table 4), 2) smaller eye diameter, inter-orbital distance, inter-nostril distance, diameter of third finger disk, and diameter of fourth toe disk than Chiasmocleis capixaba, 3) smaller eye-nostril distance, feet length, hand length, and hand length to the tip of the fourth finger than Chiasmocleis lacrimae. Moreover, males of Chiasmocleis quilombola sp. n. have less webbing on the foot (more extensive web on the foot in Chiasmocleis capixaba, absent in Chiasmocleis sp., and ranging from little to absent in Chiasmocleis lacrimae; Cruz et al. 1997, Peloso et al. 2014, Forlani et al. submitted). The new species has slender arms, legs, finger, and toes (robust arms and legs in Chiasmocleis lacrimae; thick fingers and toes in Chiasmocleis capixaba), as well as smaller and less abundant dermal spines in males (spines larger and abundant in Chiasmocleis lacrimae; abundant in Chiasmocleis capixaba). Males of Chiasmocleis quilombola sp. n. posses less amount of fringes between fingers II and III and a slender third finger than males Chiasmocleis capixaba.
Table 4.
Differences between Chiasmocleis capixaba, Chiasmocleis lacrimae, Chiasmocleis quilombola sp. n., and Chiasmocleis sp.
| Species | Chiasmocleis capixaba | Chiasmocleis lacrimae | Chiasmocleis quilombola sp. n. | Chiasmocleis sp. |
|---|---|---|---|---|
| Chiasmocleis capixaba | SVL=15.1 (SD 0.6) HL=2.8 (SD 0.1) THL=6.2 (SD 0.3) TBL=6.1 (SD 0.3) |
Feet webbing | head length; thickness of limbs, fingers, and toes; dermal spines | Feet webbing; thickness of limbs; dermal spines |
| Chiasmocleis lacrimae | mtDNA (ND2: 6.4%, 16S: 1.3%, 12S: 1.8%) nuDNA (BNDF: haplotype sharing) | SVL=16.1 (SD 0.9) HL=3.3 (SD 0.2) THL=6.6 (SD 0.4) TBL=6.5 (SD 0.3) |
head and limb length; feet webbing; thickness of limbs; dermal spines | body size; thickness; dermal spines |
| Chiasmocleis quilombola sp. n. | mtDNA (ND2: 7.1%, 16S: 0.8%, 12S: 1.1%) nuDNA (BNDF: haplotype sharing) | mtDNA (ND2: 8.2%, 16S: 0.8%, 12S: 1.8%) nuDNA (BNDF: haplotype sharing) | SVL=14 (SD 1.4) HL=2.6 (SD 0.2) THL=5.8 (SD 0.7) TBL=5.6 (SD 0.6) |
Feet webbing; thickness of limbs |
| Chiasmocleis sp. | mtDNA (ND2: 9.8%, 16S: 2.2%, 12S: 1.2%) nuDNA (BNDF: no haplotype sharing) | mtDNA (ND2: 10%, 16S: 2.3%, 12S: 2.1%) nuDNA (BNDF: no haplotype sharing) | mtDNA (ND2: 8.3%, 16S: 1.6%, 12S: 2.1%) nuDNA (BNDF: haplotype sharing) | SVL=15.3 (SD 0.7) HL=3.4 (SD 0.1) THL=6 (SD 0.3) TBL=6.2 (SD 0.3) |
SVL snout-vent length; HL head length; THL tight length; TBL tibia length; SD standard deviation.
Chiasmocleis quilombola sp. n. are distinguished from other Chiasmocleis species by: 1) four externally evident fingers and five toes distinguishes it from Chiasmocleis antenori, Chiasmocleis carvalhoi, and Chiasmocleis tridactyla (digit reduction; Walker 1973, Nelson 1975, Duellman and Mendelson 1995); 2) a shorter snout-vent length differentiate it from Chiasmocleis alagoanus, Chiasmocleis albopunctata, Chiasmocleis anatipes, Chiasmocleis atlantica, Chiasmocleis avilapiresae, Chiasmocleis bassleri, Chiasmocleis centralis, Chiasmocleis cordeiroi, Chiasmocleis crucis, Chiasmocleis devriesi, Chiasmocleis hudsoni, Chiasmocleis leucosticta, Chiasmocleis magnova, Chiasmocleis mehelyi, Chiasmocleis papachibe, Chiasmocleis royi, Chiasmocleis sapiranga, Chiasmocleis shudikarensis, Chiasmocleis supercilialba, and Chiasmocleis ventrimaculata (larger snout-vent length; Dunn 1949, Bokermann 1952, Walker and Duellman 1974, Caramaschi and Pimenta 2003, Cruz et al. 1997, Cruz et al. 1999, Caramaschi and Cruz 1997, Cruz et al. 2007a, Moravec and Köhler 2007, Peloso and Sturaro 2008, Funk and Cannatella 2009, Morales and McDiarmid 2009, Peloso et al. 2014); 3) small feet webbing of males and females distinguish the new species from Chiasmocleis cordeiroi, Chiasmocleis leucosticta, Chiasmocleis mantiqueira, and Chiasmocleis sapiranga (more extensive webbed feet in males and females; Cruz et al. 1997, Cruz et al. 2007a, b); 4) a light cream belly pattern without dark spots distinguished it from Chiasmocleis alagoanus, C. atlantica, Chiasmocleis haddadi, Chiasmocleis leucosticta, and Chiasmocleis mantiqueira (belly pattern roughly marbled in dark brown and pale cream, Cruz et al.1997, Cruz et al.1999, Cruz et al. 2007b, Peloso et al. 2014); and 5) snout rounded and belly light cream colored differentiate it from Chiasmocleis gnoma (snout truncate and belly boldly marbled in brown and pale cream; Canedo et al. 2004).
Chiasmocleis quilombola sp. n. occurs in sympatry with Chiasmocleis schubarti at the Floresta Nacional do Rio Preto, Municipality of Conceição da Barra, and at the Reserva Biológica Córrego Veado, Municipality of Pinheiros; it also occurs with Chiasmocleis capixaba and Chiasmocleis schubarti at the Reserva Natural Vale, Reserva Biológica de Sooretama, and at Cocoa plantations in Povoação, sites in the Municipality of Linhares. The new species is allopatric to Chiasmocleis sp. and Chiasmocleis lacrimae (Figure 1). We did not have access to tissues samples of Chiasmocleis capixaba from Nova Viçosa, Bahia State (Van Sluys 1998), to include in the genetic analysis, thus the phylogenetic relationship of this population remains unclear.
Cryptic species have challenged our ability to assess current levels of biodiversity. Anuran taxonomy has used various data sources to describe the species diversity, e.g., advertisement calls, external morphology, osteology, tadpoles, ecology, molecular data, karyotypes (Duellman and Trueb 1986, Haas 2003). However, Chiasmocleis systematics has been based on external morphology from adults and behavioral information (Wogel et al. 2004, Hartmann et al. 2002, Nascimento and Skuk 2006, Oliveira Filho and Giaretta 2006, Langone et al. 2007, Peloso and Sturaro 2008, Rodrigues et al. 2008, Santana et al. 2012, but see Peloso et al. 2014). Sexual dimorphism in size, amount of webbing, and color pattern have been useful characters to diagnose species (Cruz et al. 1997). Recent molecular studies 1) demonstrated the non-monophyly of traditionally recognized species groups (de Sá et al. 2012, Peloso et al. 2014) and 2) reported high genetic divergences and low gene flow along small geographical scales, suggesting that some populations could represent new species (Tonini et al. 2013). Given the current overall biodiversity crisis and specifically the worldwide threats to amphibian biodiversity, molecular studies should move beyond the identification of genetic clades and should make every effort to formally describe those evolutionary lineages. Herein, we have taken this approach and described a new species based on a combination of morphological characters in a clade of cryptic species with shown high genetic diversity and low gene flow.
The new species occupy coastal areas North of Espírito Santo State, a region that is under strong human pressure. Therefore, marine and coastal communities are susceptible to impacts of proposed modifications in the landscape for the exploitation of mineral resources. In this context, Chiasmocleis quilombola sp. n. may face imminent threat of habitat loss, as consequence of the deforestation and intensive occupation of the space by human activities.
Supplementary Material
Acknowledgements
We are thankful to L. Costa, Y. Leite, and the Laboratório de Mastozoologia e Biogeografia team, for field assistance and tissues samples. L. Chagas and staffs of the Floresta Nacional do Rio Preto for valuable help during field surveys. M. T. Rodrigues, R. C. Amaro, C. F. B. Haddad, P. Rocha, M. Napoli, H. Zaher, M. Solé, V. Fagundes, J. L. Gasparini, J. P. Pombal Jr., and P. Passos for providing tissue samples and permission to examine specimens under their care. D. Baêta and A. C. Calijorne for hosting JFRT during visit to the Museu Nacional do Rio de Janeiro. R. Ferreira, J. L. Gasparini, M. Vences, R. A. Pyron, F. Andreone, and two anonymous referees for suggestions on the manuscript. JFRT acknowledge support by the Science without Borders program (CAPES/Brazil), The George Washington University, and award NSF-DEB 1144692 to R. O. de Sá.
Appendix 1
Table 5.
Examined material and measurements from males included in the morphological analyses.
| Chiasmocleis | Numbers | Locality | State | SVL | HL | HW | ED | IOD | IND | END | THL | TBL | FL | 3FD | 4TD | FAL | HDL | HDL4 |
| Chiasmocleis capixaba | MNRJ17514 | Aracruz | ES | 14.77 | 2.91 | 4.04 | 1.18 | 2.57 | 1.16 | 1.21 | 6.19 | 6.34 | 6.43 | 0.35 | 0.44 | 2.98 | 3.36 | 2.08 |
| Chiasmocleis capixaba | MNRJ17515 | Aracruz | ES | 13.98 | 2.84 | 4.44 | 1.28 | 2.71 | 1.21 | 1.39 | 6.17 | 6.13 | 6.58 | 0.29 | 0.46 | 3.07 | 3.28 | 1.94 |
| Chiasmocleis capixaba | MNRJ17516 | Aracruz | ES | 14.47 | 2.93 | 3.98 | 1.18 | 2.64 | 1.19 | 1.32 | 6.08 | 5.96 | 6.64 | 0.30 | 0.42 | 3.10 | 3.36 | 2.16 |
| Chiasmocleis capixaba | MNRJ17517 | Aracruz | ES | 14.70 | 3.00 | 4.10 | 1.36 | 2.61 | 1.29 | 1.26 | 6.23 | 6.10 | 6.74 | 0.33 | 0.51 | 3.15 | 3.55 | 2.32 |
| Chiasmocleis capixaba | MNRJ17518 | Aracruz | ES | 16.02 | 3.13 | 4.39 | 1.32 | 2.64 | 1.21 | 1.45 | 6.61 | 6.80 | 7.45 | 0.38 | 0.48 | 3.62 | 3.86 | 2.33 |
| Chiasmocleis capixaba | MNRJ17519 | Aracruz | ES | 15.40 | 2.99 | 3.95 | 1.36 | 2.63 | 1.23 | 1.56 | 6.05 | 6.31 | 6.28 | 0.33 | 0.45 | 3.38 | 3.17 | 2.09 |
| Chiasmocleis capixaba | MNRJ17520 | Aracruz | ES | 14.94 | 2.76 | 3.82 | 1.26 | 2.66 | 1.20 | 1.36 | 5.71 | 6.06 | 5.90 | 0.41 | 0.47 | 2.96 | 3.15 | 1.80 |
| Chiasmocleis capixaba | MNRJ17535 | Aracruz | ES | 15.23 | 2.96 | 3.83 | 0.97 | 2.39 | 1.18 | 1.07 | 6.18 | 5.76 | 5.97 | 0.38 | 0.42 | 2.76 | 3.05 | 2.13 |
| Chiasmocleis capixaba | MNRJ17536 | Aracruz | ES | 15.24 | 2.50 | 3.92 | 1.23 | 2.60 | 1.16 | 1.41 | 5.83 | 5.79 | 6.63 | 0.33 | 0.45 | 2.93 | 3.52 | 2.19 |
| Chiasmocleis capixaba | MNRJ17895 | Aracruz | ES | 15.46 | 2.89 | 4.32 | 1.12 | 2.56 | 1.22 | 1.21 | 6.62 | 6.30 | 6.46 | 0.33 | 0.47 | 3.25 | 3.34 | 2.15 |
| Chiasmocleis capixaba | MNRJ22962 | Reserva Natural Vale | ES | 14.83 | 3.02 | 4.44 | 1.26 | 2.67 | 1.18 | 1.38 | 6.29 | 6.08 | 6.37 | 0.36 | 0.44 | 3.12 | 3.34 | 2.08 |
| Chiasmocleis capixaba | MNRJ22966 | Reserva Natural Vale | ES | 15.05 | 2.99 | 4.41 | 1.37 | 2.71 | 1.19 | 1.43 | 6.71 | 6.20 | 6.25 | 0.36 | 0.52 | 3.18 | 3.15 | 1.72 |
| Chiasmocleis capixaba | MZUSP147468 | ReBio Duas Bocas | ES | 15.88 | 3.05 | 4.40 | 1.27 | 2.87 | 1.25 | 1.41 | 6.84 | 6.53 | 6.92 | 0.43 | 0.43 | 3.06 | 3.44 | 2.14 |
| Chiasmocleis capixaba | MZUSP147469 | ReBio Duas Bocas | ES | 16.23 | 3.02 | 4.61 | 1.05 | 2.99 | 1.31 | 1.68 | 6.80 | 6.71 | 7.05 | 0.48 | 0.48 | 3.28 | 3.29 | 2.30 |
| Chiasmocleis lacrimae | MNRJ17480 | Horto Florestal | RJ | 16.20 | 3.40 | 4.40 | 1.10 | 2.70 | 0.90 | 1.40 | 6.50 | 6.50 | 7.30 | 0.30 | 0.40 | 3.30 | 3.60 | 2.50 |
| Chiasmocleis lacrimae | MNRJ17481 | Horto Florestal | RJ | 15.60 | 3.30 | 4.10 | 1.10 | 2.60 | 1.00 | 1.40 | 6.20 | 6.30 | 7.20 | 0.40 | 0.40 | 3.50 | 3.60 | 2.60 |
| Chiasmocleis lacrimae | MNRJ17482 | Horto Florestal | RJ | 16.20 | 3.50 | 2.60 | 1.30 | 2.60 | 1.00 | 1.90 | 6.50 | 6.50 | 7.10 | 0.40 | 0.50 | 3.30 | 3.80 | 2.50 |
| Chiasmocleis lacrimae | MNRJ17484 | Horto Florestal | RJ | 19.15 | 3.57 | 4.82 | 1.35 | 2.84 | 1.44 | 1.69 | 7.45 | 7.35 | 8.23 | 0.34 | 0.36 | 3.56 | 4.23 | 2.69 |
| Chiasmocleis lacrimae | MNRJ17485 | Horto Florestal | RJ | 16.10 | 3.70 | 4.30 | 1.20 | 2.50 | 0.90 | 1.60 | 6.90 | 6.70 | 7.50 | 0.30 | 0.40 | 3.40 | 3.60 | 2.40 |
| Chiasmocleis lacrimae | MNRJ17486 | Horto Florestal | RJ | 15.07 | 3.00 | 4.33 | 1.22 | 2.52 | 1.22 | 1.50 | 6.30 | 6.22 | 6.68 | 0.30 | 0.43 | 3.19 | 3.44 | 2.24 |
| Chiasmocleis lacrimae | MNRJ17487 | Horto Florestal | RJ | 16.10 | 3.33 | 4.38 | 1.19 | 2.91 | 1.30 | 1.68 | 6.94 | 6.78 | 7.16 | 0.27 | 0.39 | 3.46 | 3.53 | 2.08 |
| Chiasmocleis lacrimae | MNRJ17488 | Horto Florestal | RJ | 15.90 | 3.20 | 3.80 | 1.10 | 2.50 | 0.90 | 1.30 | 5.80 | 6.20 | 6.60 | 0.30 | 0.40 | 3.00 | 3.30 | 2.20 |
| Chiasmocleis lacrimae | MNRJ17489 | Horto Florestal | RJ | 15.40 | 3.10 | 3.90 | 1.20 | 2.20 | 0.90 | 1.30 | 6.10 | 6.10 | 6.90 | 0.30 | 0.40 | 3.10 | 3.40 | 2.10 |
| Chiasmocleis lacrimae | MNRJ17490 | Horto Florestal | RJ | 16.10 | 3.30 | 4.00 | 1.10 | 2.50 | 0.90 | 1.40 | 6.70 | 7.10 | 7.70 | 0.40 | 0.40 | 3.50 | 4.20 | 2.70 |
| Chiasmocleis lacrimae | MNRJ17491 | Horto Florestal | RJ | 15.26 | 2.90 | 4.75 | 1.21 | 2.92 | 1.47 | 1.49 | 6.59 | 6.46 | 7.13 | 0.32 | 0.41 | 3.34 | 3.78 | 2.41 |
| Chiasmocleis lacrimae | MNRJ17492 | Horto Florestal | RJ | 15.50 | 3.90 | 4.60 | 1.30 | 2.50 | 1.20 | 1.50 | 6.10 | 6.30 | 6.50 | 0.40 | 0.40 | 3.10 | 3.70 | 2.50 |
| Chiasmocleis lacrimae | MNRJ17498 | Horto Florestal | RJ | 17.10 | 3.70 | 4.70 | 1.20 | 2.50 | 1.10 | 1.40 | 6.70 | 6.80 | 6.90 | 0.40 | 0.50 | 3.40 | 3.40 | 2.50 |
| Chiasmocleis lacrimae | MNRJ17505 | Horto Florestal | RJ | 16.80 | 3.42 | 4.62 | 1.41 | 2.84 | 1.32 | 1.71 | 7.19 | 6.88 | 7.43 | 0.33 | 0.38 | 3.50 | 3.87 | 2.42 |
| Chiasmocleis lacrimae | MNRJ17506 | Horto Florestal | RJ | 16.95 | 3.30 | 4.84 | 1.36 | 3.00 | 1.35 | 1.62 | 7.19 | 6.80 | 7.32 | 0.41 | 0.43 | 3.60 | 4.09 | 2.63 |
| Chiasmocleis lacrimae | MNRJ17507 | Horto Florestal | RJ | 15.16 | 3.14 | 4.43 | 1.29 | 2.71 | 1.24 | 1.45 | 6.06 | 6.13 | 6.28 | 0.34 | 0.41 | 3.12 | 3.51 | 2.22 |
| Chiasmocleis lacrimae | MNRJ17565 | Horto Florestal | RJ | 16.66 | 2.97 | 4.42 | 1.36 | 2.79 | 1.30 | 1.47 | 7.05 | 6.69 | 7.14 | 0.49 | 0.43 | 3.23 | 3.97 | 2.63 |
| Chiasmocleis lacrimae | MNRJ66497 | Mimoso do Sul | ES | 16.60 | 3.14 | 4.77 | 1.40 | 2.89 | 1.31 | 1.48 | 6.69 | 6.49 | 6.90 | 0.39 | 0.43 | 3.55 | 3.80 | 2.32 |
| Chiasmocleis quilombola sp. n. | MNRJ29057 | Povoação | ES | 12.72 | 2.70 | 3.89 | 1.05 | 2.42 | 1.08 | 1.20 | 5.35 | 5.05 | 5.24 | 0.30 | 0.39 | 2.65 | 2.79 | 1.79 |
| Chiasmocleis quilombola sp. n. | MNRJ29058 | Povoação | ES | 13.23 | 2.68 | 3.90 | 1.12 | 2.47 | 1.10 | 1.12 | 5.28 | 4.91 | 5.17 | 0.34 | 0.42 | 2.52 | 2.78 | 1.73 |
| Chiasmocleis quilombola sp. n. | MNRJ29059 | Povoação | ES | 13.56 | 2.53 | 3.63 | 1.15 | 2.37 | 1.08 | 1.12 | 5.36 | 5.25 | 5.33 | 0.29 | 0.39 | 2.80 | 3.00 | 1.89 |
| Chiasmocleis quilombola sp. n. | MNRJ29060 | Povoação | ES | 12.59 | 2.55 | 3.79 | 1.08 | 2.41 | 1.08 | 1.16 | 5.12 | 4.67 | 4.56 | 0.32 | 0.32 | 2.48 | 2.48 | 1.67 |
| Chiasmocleis quilombola sp. n. | MNRJ29073 | Povoação | ES | 13.76 | 2.53 | 3.94 | 1.25 | 2.43 | 1.18 | 1.29 | 5.67 | 5.63 | 5.88 | 0.41 | 0.41 | 2.88 | 3.07 | 1.85 |
| Chiasmocleis quilombola sp. n. | MNRJ29074 | Povoação | ES | 13.47 | 2.33 | 3.72 | 1.18 | 2.27 | 1.08 | 1.15 | 5.24 | 5.27 | 5.60 | 0.32 | 0.40 | 2.73 | 3.02 | 1.81 |
| Chiasmocleis quilombola sp. n. | MBML2858 | Povoação | ES | 13.47 | 2.54 | 3.94 | 0.88 | 2.04 | 0.82 | 1.03 | 5.11 | 5.39 | 5.50 | 0.33 | 0.43 | 2.61 | 2.91 | 1.72 |
| Chiasmocleis quilombola sp. n. | MBML2866 | Povoação | ES | 12.15 | 2.24 | 3.34 | 1.05 | 2.16 | 0.72 | 0.95 | 5.26 | 5.11 | 5.33 | 0.27 | 0.39 | 2.55 | 2.75 | 1.62 |
| Chiasmocleis quilombola sp. n. | MBML2863 | Povoação | ES | 12.30 | 2.34 | 3.75 | 0.82 | 2.00 | 0.83 | 0.93 | 5.22 | 5.32 | 5.42 | 0.31 | 0.48 | 2.50 | 2.63 | 1.59 |
| Chiasmocleis quilombola sp. n. | MZUSP147473 | Flona Rio Preto | ES | 16.07 | 3.18 | 3.87 | 1.09 | 2.18 | 1.09 | 1.33 | 6.01 | 6.00 | 6.41 | 0.24 | 0.23 | 3.15 | 3.30 | 2.07 |
| Chiasmocleis quilombola sp. n. | MZUSP147478 | Flona Rio Preto | ES | 15.71 | 2.75 | 4.52 | 1.30 | 2.80 | 1.13 | 1.25 | 6.55 | 6.47 | 6.91 | 0.35 | 0.44 | 3.21 | 3.45 | 2.33 |
| Chiasmocleis quilombola sp. n. | MZUSP147471 | Flona Rio Preto | ES | 14.43 | 2.75 | 3.83 | 1.03 | 2.57 | 1.11 | 1.51 | 6.07 | 6.27 | 6.23 | 0.25 | 0.26 | 2.99 | 2.84 | 1.83 |
| Chiasmocleis quilombola sp. n. | MZUSP147475 | Flona Rio Preto | ES | 14.48 | 2.79 | 4.55 | 1.28 | 2.55 | 1.28 | 1.25 | 6.63 | 6.41 | 6.73 | 0.36 | 0.36 | 3.26 | 3.48 | 2.16 |
| Chiasmocleis quilombola sp. n. | MZUSP147494 | Flona Rio Preto | ES | 16.55 | 3.14 | 4.63 | 1.36 | 2.55 | 1.24 | 1.36 | 7.02 | 6.89 | 7.59 | 0.25 | 0.37 | 3.33 | 3.80 | 2.40 |
| Chiasmocleis quilombola sp. n. | MZUSP147476 | Flona Rio Preto | ES | 16.09 | 2.70 | 4.36 | 1.24 | 2.65 | 1.31 | 1.36 | 6.73 | 6.26 | 6.11 | 0.32 | 0.47 | 2.95 | 3.33 | 1.83 |
| Chiasmocleis quilombola sp. n. | MZUSP147472 | Flona Rio Preto | ES | 15.28 | 2.80 | 4.08 | 1.33 | 2.67 | 1.24 | 1.33 | 7.08 | 6.55 | 6.60 | 0.34 | 0.41 | 3.20 | 3.40 | 2.22 |
| sp. | MTR13495 | Trancoso | BA | 15.92 | 3.39 | 4.07 | 1.06 | 2.65 | 0.94 | 1.43 | 6.37 | 6.16 | 6.77 | 0.27 | 0.42 | 3.60 | 3.45 | 2.06 |
| sp. | MTR13547 | Trancoso | BA | 13.80 | 3.53 | 4.09 | 0.97 | 2.36 | 1.00 | 1.35 | 5.59 | 5.68 | 5.72 | 0.27 | 0.35 | 2.95 | 3.18 | 2.27 |
| sp. | MTR13545 | Trancoso | BA | 15.07 | 3.51 | 4.24 | 1.10 | 2.43 | 1.03 | 1.35 | 5.91 | 6.41 | 6.78 | 0.29 | 0.38 | 2.95 | 3.40 | 2.35 |
| sp. | MTR13590 | Trancoso | BA | 15.48 | 3.48 | 3.99 | 1.17 | 2.51 | 0.80 | 1.32 | 6.01 | 6.22 | 6.69 | 0.30 | 0.45 | 3.11 | 3.73 | 2.41 |
| sp. | MTR13565 | Trancoso | BA | 16.27 | 3.78 | 4.31 | 0.95 | 2.59 | 1.04 | 1.61 | 5.64 | 6.33 | 6.56 | 0.33 | 0.46 | 3.20 | 3.68 | 2.67 |
| sp. | MTR13548 | Trancoso | BA | 15.36 | 3.34 | 4.57 | 1.06 | 2.52 | 1.12 | 1.09 | 6.44 | 6.62 | 6.72 | 0.30 | 0.40 | 3.19 | 3.64 | 2.36 |
| sp. | MTR13546 | Trancoso | BA | 15.53 | 3.10 | 4.40 | 1.24 | 2.30 | 0.91 | 1.46 | 6.02 | 5.96 | 6.56 | 0.31 | 0.40 | 2.90 | 3.30 | 2.14 |
| sp. | MTR13489 | Trancoso | BA | 15.34 | 3.53 | 4.05 | 1.16 | 2.35 | 1.00 | 1.36 | 6.67 | 6.54 | 6.73 | 0.27 | 0.44 | 3.40 | 3.46 | 2.40 |
Appendix 2
Table 6.
Samples included in the molecular analyses and genbank numbers. Numbers in bold were retrieved from previous studies.
| Chiasmocleis | Voucher | Tissue | Locality | State | 12S | 16S | ND2 | BDNF |
| Chiasmocleis capixaba | MZUSP147497 | CTA1861 | ReBio Duas Bocas | ES | KM111721 | KM111817 | JQ410706 | KM111908 |
| Chiasmocleis capixaba | MZUSP147498 | CTA1863 | ReBio Duas Bocas | ES | KM111722 | KM111818 | JQ410707 | KM111909 |
| Chiasmocleis capixaba | MZUSP147499 | CTA1864 | ReBio Duas Bocas | ES | KM111723 | KM111819 | JQ410708 | KM111910 |
| Chiasmocleis capixaba | MZUSP147468 | CTA1865 | ReBio Duas Bocas | ES | KM111724 | KM111820 | KM111992 | KM111911 |
| Chiasmocleis capixaba | MZUSP147482 | CTA1869 | ReBio Duas Bocas | ES | KM111725 | KM111821 | KM111993 | KM111912 |
| Chiasmocleis capixaba | MZUSP147469 | CTA1870 | ReBio Duas Bocas | ES | KM111726 | KM111822 | KM111994 | KM111913 |
| Chiasmocleis capixaba | MZUSP147500 | CTA1871 | ReBio Duas Bocas | ES | KM111727 | KM111823 | JQ410709 | KM111914 |
| Chiasmocleis capixaba | MZUSP147510 | CTA1872 | Serra | ES | KM111728 | KM111824 | JQ410685 | KM111915 |
| Chiasmocleis capixaba | MZUSP147512 | CTA1874 | Serra | ES | KM111729 | KM111825 | JQ410690 | KM111916 |
| Chiasmocleis capixaba | MZUSP147513 | CTA1875 | Serra | ES | KM111730 | KM111826 | JQ410691 | KM111917 |
| Chiasmocleis capixaba | JFT479 | CTA1876 | Serra | ES | KM111731 | KM111827 | JQ410692 | KM111918 |
| Chiasmocleis capixaba | MZUSP147514 | CTA1877 | Serra | ES | KM111732 | KM111828 | JQ410693 | KM111919 |
| Chiasmocleis capixaba | JFT483 | CTA1879 | Serra | ES | KM111733 | KM111829 | JQ410694 | KM111920 |
| Chiasmocleis capixaba | JFT499 | CTA1881 | Serra | ES | KM111734 | KM111830 | JQ410695 | KM111921 |
| Chiasmocleis capixaba | MZUSP147520 | CTA1893 | Serra | ES | KM111735 | KM111831 | JQ410700 | KM111922 |
| Chiasmocleis capixaba | MZUSP147521 | CTA1894 | Serra | ES | KM111736 | KM111832 | JQ410701 | KM111923 |
| Chiasmocleis capixaba | MZUSP147523 | CTA1896 | Serra | ES | KM111737 | KM111833 | JQ410702 | KM111924 |
| Chiasmocleis capixaba | MTR12276 | CTMZ6907 | FloNa dos Goytacazes | ES | KM111738 | KM111834 | - | KM111925 |
| Chiasmocleis capixaba | MTR12296 | CTMZ6908 | FloNa dos Goytacazes | ES | KM111739 | KM111835 | JQ410688 | KM111926 |
| Chiasmocleis capixaba | MTR12407 | CTMZ6912 | Reserva Natural Vale | ES | KM111740 | KM111836 | - | - |
| Chiasmocleis capixaba | MTR12484 | CTMZ6920 | Reserva Natural Vale | ES | KM111741 | KM111837 | - | KM111927 |
| Chiasmocleis capixaba | MTR12485 | CTMZ6921 | Reserva Natural Vale | ES | KM111742 | KM111838 | - | KM111928 |
| Chiasmocleis capixaba | - | CTMZ6939 | Guarapari | ES | KM111743 | KM111839 | - | KM111929 |
| Chiasmocleis capixaba | MTR12076 | MTR12076 | Reserva Natural Vale | ES | KM111744 | KM111840 | JQ410687 | KM111930 |
| Chiasmocleis capixaba | MTR12297 | MTR12297 | FloNa dos Goytacazes | ES | KM111745 | KM111841 | JQ410689 | KM111931 |
| Chiasmocleis cordeiroi | CFBH32057 | CFBH15784 | Ilhéus | BA | KM111759 | KM111852 | KM111995 | KM111939 |
| Chiasmocleis cordeiroi | MZUSP147496 | CTA1935 | Ituberá | BA | KM111760 | KM111853 | KM111996 | KM111940 |
| Chiasmocleis cordeiroi | MTR22122 | MTR22122 | EE Wenceslau Guimarães | BA | KM111761 | KM111854 | KM111997 | KM111941 |
| Chiasmocleis cordeiroi | MTR22123 | MTR22123 | EE Wenceslau Guimarães | BA | KM111762 | KM111855 | KM111998 | KM111942 |
| Chiasmocleis cordeiroi | PEU137 | PEU137 | Jaguaripe | BA | KM111763 | KM111856 | KM111999 | KM111943 |
| Chiasmocleis cordeiroi | PEU146 | PEU146 | Jaguaripe | BA | KM111764 | KM111857 | KM112000 | KM111944 |
| Chiasmocleis crucis | MTR6001 | CTMZ6898 | Serra do Teimoso | BA | KM111765 | KM111858 | KM112001 | KM111945 |
| Chiasmocleis crucis | - | CTMZ6900 | Ilhéus | BA | KM111766 | KM111859 | KM112002 | KM111946 |
| Chiasmocleis crucis | - | CTMZ6901 | Ilhéus | BA | KM111767 | KM111860 | KM112003 | KM111947 |
| Chiasmocleis crucis | MTR16070 | MTR16070 | Serra Bonita | BA | KM111768 | KM111861 | KM112004 | KM111948 |
| Chiasmocleis lacrimae | - | CFBH73 | Picinguaba | SP | KM111748 | KC180040 | JQ410715 | KC180202 |
| Chiasmocleis lacrimae | CFBH17495 | CFBH7361 | Ilha de São Sebastião | SP | KM111749 | KM111844 | - | |
| Chiasmocleis lacrimae | - | CFBH76 | Picinguaba | SP | KM111750 | KC180063 | JQ410714 | KC180163 |
| Chiasmocleis lacrimae | JFT981 | CTA1934 | Matada Usina Paineiras | ES | KM111751 | KM111845 | JQ410710 | KM111932 |
| Chiasmocleis lacrimae | - | CTMZ6946 | Bertioga | SP | KM111752 | KM111846 | - | KM111933 |
| Chiasmocleis lacrimae | RN7003 | CTRN173 | Angra dos Reis | RJ | KM111753 | KM111847 | - | - |
| Chiasmocleis lacrimae | RN7004 | CTRN174 | Angra dos Reis | RJ | KM111754 | KM111848 | - | KM111934 |
| Chiasmocleis lacrimae | RN7005 | CTRN175 | Angra dos Reis | RJ | KM111755 | KM111849 | - | KM111935 |
| Chiasmocleis lacrimae | MNRJ47477 | MNRJ47477 | ReBio União | RJ | KM111746 | KM111842 | - | - |
| Chiasmocleis lacrimae | MNRJ48415 | MNRJ48415 | ReBio União | RJ | KM111747 | KM111843 | - | - |
| Chiasmocleis lacrimae | MNRJ49302 | MNRJ49302 | Cachoeiras de Macacu | ES | KM111756 | KM111850 | JQ410712 | KM111936 |
| Chiasmocleis lacrimae | MNRJ60744 | MNRJ60744 | Duque de Caxias | RJ | KM111757 | - | JQ410713 | KM111937 |
| Chiasmocleis lacrimae | MNRJ66494 | MNRJ66494 | Mimoso do Sul | ES | KM111758 | KM111851 | JQ410711 | KM111938 |
| Chiasmocleis leucosticta | CFBH19029 | CFBH8594 | PE Ilha do Cardoso | SP | KM111769 | KM111862 | - | - |
| Chiasmocleis leucosticta | MZUSP136053 | CTMZ2485 | PE Carlos Botelho | SP | KM111770 | KM111863 | - | - |
| Chiasmocleis leucosticta | MZUSP136055 | CTMZ2493 | PE Carlos Botelho | SP | KM111771 | - | - | KM111949 |
| Chiasmocleis leucosticta | MZUSP136059 | CTMZ2497 | PE Carlos Botelho | SP | - | KM111864 | - | KM111950 |
| Chiasmocleis leucosticta | MTR7128 | CTMZ6943 | Fazenda Intervales | SP | - | - | KM112005 | KM111951 |
| Chiasmocleis leucosticta | - | CTMZ6944 | Piedade | SP | KM111772 | - | KM112006 | - |
| Chiasmocleis mantiqueira | - | CTMZ6891 | Serra do Brigadeiro | MG | KM111773 | KM111865 | - | KM111952 |
| Chiasmocleis mantiqueira | UFMG-A9643 | UFMG-T1802 | Ouro Branco | MG | KM111774 | KM111866 | KM112007 | - |
| Chiasmocleis mantiqueira | UFMG-A9659 | UFMG-T1804 | Ouro Branco | MG | KM111775 | KM111867 | - | KM111953 |
| Chiasmocleis mantiqueira | UFMG-A9651 | UFMG-T1810 | Ouro Branco | MG | KM111776 | KM111868 | - | KM111954 |
| Chiasmocleis mantiqueira | UFMG-A9656 | UFMG-T1815 | Ouro Branco | MG | KM111777 | KM111869 | - | KM111955 |
| Chiasmocleis quilombola sp. n. | - | CFBH1437 | ReBio Sooretama | ES | KM111778 | KC180044 | - | KC180193 |
| Chiasmocleis quilombola sp. n. | - | CFBH1438 | ReBio Sooretama | ES | KM111779 | KC179977 | - | KC180168 |
| Chiasmocleis quilombola sp. n. | CFBH19471 | CFBH9055 | Povoação | ES | KM111780 | KM111870 | KM112008 | KM111956 |
| Chiasmocleis quilombola sp. n. | CFBH18076 | CFBH9082 | Povoação | ES | KM111781 | KM111871 | KM112009 | KM111957 |
| Chiasmocleis quilombola sp. n. | CFBH18077 | CFBH9083 | Povoação | ES | KM111782 | KM111872 | KM112010 | KM111958 |
| Chiasmocleis quilombola sp. n. | JFT831 | CTA1906 | FloNa do Rio Preto | ES | KM111783 | KM111873 | JQ410669 | KM111959 |
| Chiasmocleis quilombola sp. n. | MZUSP147471 | CTA1907 | FloNa do Rio Preto | ES | KM111784 | KM111874 | JQ410670 | KM111960 |
| Chiasmocleis quilombola sp. n. | MZUSP147472 | CTA1908 | FloNa do Rio Preto | ES | KM111785 | KM111875 | JQ410671 | KM111961 |
| Chiasmocleis quilombola sp. n. | MZUSP147473 | CTA1909 | FloNa do Rio Preto | ES | KM111786 | KM111876 | JQ410672 | KM111962 |
| Chiasmocleis quilombola sp. n. | MZUSP147474 | CTA1918 | FloNa do Rio Preto | ES | KM111787 | KM111877 | JQ410673 | KM111963 |
| Chiasmocleis quilombola sp. n. | MZUSP147475 | CTA1919 | FloNa do Rio Preto | ES | KM111788 | KM111878 | JQ410674 | KM111964 |
| Chiasmocleis quilombola sp. n. | MZUSP147494 | CTA1923 | FloNa do Rio Preto | ES | KM111789 | KM111879 | JQ410677 | KM111965 |
| Chiasmocleis quilombola sp. n. | MZUSP147479 | CTA1929 | FloNa do Rio Preto | ES | KM111790 | KM111880 | JQ410679 | KM111966 |
| Chiasmocleis quilombola sp. n. | MZUSP147480 | CTA1931 | FloNa do Rio Preto | ES | KM111791 | KM111881 | JQ410680 | KM111967 |
| Chiasmocleis quilombola sp. n. | MZUSP147493 | CTA1933 | FloNa do Rio Preto | ES | KM111792 | KM111882 | JQ410681 | KM111968 |
| Chiasmocleis quilombola sp. n. | JFT990 | CTA1938 | PE de Itaúnas | ES | - | KM111883 | - | KM111969 |
| Chiasmocleis quilombola sp. n. | MTR12017 | CTMZ6903 | Reserva Natural Vale | ES | KM111793 | KM111884 | - | KM111970 |
| Chiasmocleis quilombola sp. n. | MTR12077 | CTMZ6905 | Reserva Natural Vale | ES | KM111794 | KM111885 | - | - |
| Chiasmocleis quilombola sp. n. | MTR12470 | CTMZ6916 | Reserva Natural Vale | ES | KM111795 | KM111886 | - | KM111971 |
| Chiasmocleis quilombola sp. n. | MTR12471 | CTMZ6917 | Reserva Natural Vale | ES | KM111796 | KM111887 | - | KM111972 |
| Chiasmocleis quilombola sp. n. | MTR21527 | LGA3267 | ReBio Córrego Veado | ES | KM111797 | KM111888 | JQ410668 | KM111973 |
| Chiasmocleis schubarti | CFBH9331 | CFBH2078 | ReBio Sooretama | ES | KM111798 | KC180071 | KM112011 | KC180122 |
| Chiasmocleis schubarti | CFBH18075 | CFBH9060 | Povoação | ES | KM111799 | KM111889 | KM112012 | KM111974 |
| Chiasmocleis schubarti | CFBH 22501 | CTA1860 | ReBio Duas Bocas | ES | KM111800 | KM111890 | KM112013 | KM111975 |
| Chiasmocleis schubarti | MZUSP147485 | CTA1887 | FloNa do Rio Preto | ES | KM111801 | KM111891 | KM112014 | KM111976 |
| Chiasmocleis schubarti | MZUSP147487 | CTA1924 | FloNa do Rio Preto | ES | KM111802 | KM111892 | KM112015 | KM111977 |
| Chiasmocleis schubarti | MTR12094 | CTMZ6906 | FloNa dos Goytacazes | ES | KM111803 | KM111893 | KM112016 | KM111978 |
| Chiasmocleis schubarti | LGA2630 | LGA2630 | ReBio Córrego Veado | ES | KM111804 | KM111894 | JQ410661 | KM111979 |
| Chiasmocleis schubarti | MTR12266 | MTR12266 | FloNa dos Goytacazes | ES | KM111805 | KM111895 | KM112017 | KM111980 |
| Chiasmocleis schubarti | MTR17524 | MTR17524 | PE do Rio Doce | MG | KM111806 | KM111896 | KM112018 | KM111981 |
| Chiasmocleis schubarti | MTR17571 | MTR17571 | PE do Rio Doce | MG | KM111807 | KM111897 | KM112019 | KM111982 |
| sp. | - | CFBH15818 | Porto Seguro | BA | - | KM111898 | - | KM111983 |
| sp. | MTR13466 | CTMZ6923 | Trancoso | BA | KM111808 | KM111899 | JQ410665 | KM111984 |
| sp. | MTR13489 | CTMZ6924 | Trancoso | BA | KM111809 | KM111900 | JQ410666 | KM111985 |
| sp. | MTR13495 | CTMZ6925 | Trancoso | BA | KM111810 | KM111901 | - | KM111986 |
| sp. | MTR13545 | CTMZ6927 | Trancoso | BA | KM111811 | KM111902 | - | KM111987 |
| sp. | MTR13547 | CTMZ6929 | Trancoso | BA | KM111812 | KM111903 | - | KM111988 |
| sp. | MTR13548 | CTMZ6930 | Trancoso | BA | KM111813 | KM111904 | - | KM111989 |
| sp. | MTR13565 | CTMZ6932 | Trancoso | BA | KM111814 | KM111905 | - | KM111990 |
| sp. | MTR13579 | CTMZ6933 | Trancoso | BA | KM111815 | KM111906 | - | KM111991 |
| sp. | MTR13589 | CTMZ6935 | Trancoso | BA | KM111816 | KM111907 | KM112020 | - |
Citation
Tonini JFR, Forlani MC, de Sá RO (2014) A new species of Chiasmocleis (Microhylidae, Gastrophryninae) from the Atlantic Forest of Espírito Santo State, Brazil. ZooKeys 428: 109–132. doi: 10.3897/zookeys.428.7352
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