Research Article |
Corresponding author: Erick Cristofore Guimarães ( erick.ictio@yahoo.com.br ) Academic editor: Javier Maldonado
© 2018 Erick Cristofore Guimarães, Pâmella Silva De Brito, Leonardo Manir Feitosa, Luís Fernando Carvalho-Costa, Felipe Polivanov Ottoni.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Guimarães EC, De Brito PS, Feitosa LM, Carvalho-Costa LF, Ottoni FP (2018) A new species of Hyphessobrycon Durbin from northeastern Brazil: evidence from morphological data and DNA barcoding (Characiformes, Characidae). ZooKeys 765: 79-101. https://doi.org/10.3897/zookeys.765.23157
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A new species of Hyphessobrycon is described for the upper Munim and Preguiças river basins, northeastern Brazil, supported by morphological and molecular species delimitation methods. This new species belongs to the Hyphessobryconsensu stricto group, as it has the three main diagnostic character states of this assemblage: presence of a dark brown or black blotch on the dorsal fin, absence of a black midlateral stripe on its flank and the position of Weberian apparatus upward horizontal through dorsal margin of operculum. Our phylogenetic analysis also supported the allocation of the new species in this group; however, it was not possible to recover the species sister-group. Pristella maxillaris and Moenkhausia hemigrammoides were recovered as the sister-clade of the Hyphessobryconsensu stricto group.
Uma nova espécie de Hyphessobrycon é aqui descrita para as bacias do alto Rio Munim e Preguiças, nordeste do Brasil, sustentada por métodos morfológicos e moleculares de delimitação de espécies. Essa nova espécie é membro do grupo Hyphessobryconsensu stricto, já que possui os três principais estados de caracteres diagnósticos desse agrupamento: presença de uma mancha marrom escura ou negra na nadadeira dorsal, ausência de uma faixa lateral no meio do flanco e a posição do aparelho de Weber localizado acima da horizontal da margem dorsal do opérculo. Nossa análise filogenética também apoia o posicionamento da nova espécie dentro desse grupo, entretanto não foi possível recuperar o grupo-irmão da espécie. Pristella maxillaris e Moenkhausia hemigrammoides foram recuperados com sendo o clado irmão do grupo Hyphessobryconsensu stricto.
Hyphessobrycon sensu stricto , integrative taxonomy, Pristellinae , rosy tetra clade
clado rosy tetra, Hyphessobrycon sensu stricto , taxonomia integrativa, Pristellinae
Hyphessobrycon Durbin, 1908 is one of the most species-rich genera of Characidae, currently comprising approximately 150 valid species (
Extensive data show that Hyphessobrycon is not a monophyletic group (
In addition, some artificial species groups of Hyphessobrycon were proposed based on the combination of character states (e.g.,
One of this species group was termed as “group F” by
After that,
One way to overcome the confusing taxonomy of problematic groups, to have accurate species identifications and species diversity estimates of groups is to use different operational criteria for species delimitation (
A new species of Hyphessobrycon, member of the Hyphessobryconsensu stricto Carvalho and Malabarba, 2015 is herein described from the Munim and Preguiças river basins, two coastal river basins of the Maranhão State, northeastern Brazil, based on both morphology and molecular data.
Measurements and counts were made according to
All specimens are from Brazil.
Hyphessobrycon amandae Géry & Uj, 1987: UFRJ 1557, 5 spcms, Goiás State, Jussara municipality. H. bentosi: CICCAA 00849, 2 spcms, aquarium trade. H. cf. bentosi: CICCAA 00701, 1 spcm, Pará State, Paragominas municipality. CICCAA 00702, 2 spcms, Pará State, Paragominas municipality. CICCAA 00703, 1 spcm (C&S), Pará State, Paragominas municipality. H. bifasciatus Ellis, 1911: UFRJ 0068, 6 spcms, Espírito Santo State, Marataízes and Guarapari municipality. H. copelandi: CICCAA 00722, 2 spcms, Pará State, Marabá municipality. H. diancistrus Weitzman, 1977: UFRJ 2166, 55 spcms, Tocantins State, Ilha do Bananal municipality. H. eques: CICCAA 00715, 4 spcms (C&S), Minas Gerais State, Tombos municipality. CICCAA 00710, 51 spcms, Minas Gerais State, Tombos municipality. H. griemi Hoedeman, 1957: UFRJ 4496, 7 spcms, Santa Catarina State, Esplanada municipality. H. haraldschultzi: CICCAA 00873, 20 spcms, Tocantins State, Ilha do Bananal municipality. H. itaparicensis Lima & Costa, 2001: CICCAA 00314, 6 spcms, Sergipe State, Areia Branca municipality. Pristella maxillaris (Ulrey, 1894): CICCAA 00850, 2 spcms, aquarium trade. H. micropterus: FMNH 57916, 1 spcm, Rio São Francisco at Lagoa do Porto (Photograph of a Holotype). CICCAA 00300, 24 spcms, Bahia; Barras municipality. CICCAA 00699, 8 spcms (C&S), Barras, Bahia municipality. H. reticulatus Ellis, 1911: UFRJ 0107, 4 spcms, Rio de Janeiro State, Desengano municipality. H. sergipanus Bragança, Ottoni & Rangel-Pereira, 2016: CICCAA 00296, 11 spcms, Sergipe State, Estância municipality. UFRJ 5582, 8 spcms, Mato Grosso State, Poconé municipality. UFRJ 3937, 4 spcms, Mato Grosso State, Cárceres municipality. H. stegemanni Géry, 1961: UFRJ 1988, 17 spcms, Tocantins State, Porto Nacional municipality. H. sweglesi: CICCAA 00852, 2 spcms, trade aquarium. H. wernerei: MUZUSP 42365, 1 spcm, Pará State, Santa Maria do Pará municipality. CICCAA 00751, 1 spcm, Pará State, Paragominas municipality.
DNA extraction was carried out with the Wizard Genomic DNA Purification kit (Promega) following manufacturer’s protocol. DNA quality was evaluated by agarose gel electrophoresis stained with GelRed (Biotium) and was quantified using Nanodrop 2000 (Thermo Fisher Scientific). DNA was stored at -20 °C until further procedures. Samples (N= 4; Table
Sampling sites, specimens and DNA sequence information included in the study.
Species | Locality | Basin/drainage | Country | GenBank/BoldSystems | Catalog number |
---|---|---|---|---|---|
Hyphessobrycon piorskii sp. n. | Anapurus, Maranhão | Munin | Brazil | MF765796 | CICCAA00725 |
Hyphessobrycon piorskii sp. n. | Anapurus, Maranhão | Munim | Brazil | MF765797 | CICCAA00726 |
Hyphessobrycon piorskii sp. n. | Barreirinhas, Maranhão | Preguiças | Brazil | MG791915 | CICCAA01650 |
Hyphessobrycon piorskii sp. n. | Anapurus, Maranhão | Munim | Brazil | MG791914 | CICCAA01651 |
Hyphessobrycon bentosi | Barcelos, Amazonas | Negro | Brazil | HYP097-13 | INPA37684-5939 |
Hyphessobrycon bentosi | Barcelos, Amazonas | Negro | Brazil | HYP098-13 | INPA37684-5940 |
Hyphessobrycon bentosi | Barcelos, Amazonas | Negro | Brazil | HYP099-13 | NPA37684-5942 |
Hyphessobrycon bentosi | Barcelos, Amazonas | Negro | Brazil | HYP100-13 | INPA37684-5943 |
Hyphessobrycon bentosi | Manaus, Amazonas | – | Brazil | HYP116-13 | INPA39527-BA1 |
Hyphessobrycon bentosi | Manaus, Amazonas | – | Brazil | HYP117-13 | INPA39527-BA2 |
Hyphessobrycon bentosi | Manaus, Amazonas | – | Brazil | HYP118-13 | INPA39527-BA3 |
Hyphessobrycon bentosi | Manaus, Amazonas | – | Brazil | HYP119-13 | INPA39527-BA4 |
Hyphessobrycon copelandi | Tabatinga, Amazonas | Solimões | Brazil | HYP094-13 | INPA37683-TU1 |
Hyphessobrycon copelandi | Tabatinga, Amazonas | Solimões | Brazil | HYP095-13 | INPA37683-TU1 |
Hyphessobrycon copelandi | Tabatinga, Amazonas | Solimões | Brazil | HYP096-13 | INPA37683-TU1 |
Hyphessobrycon eques | Santarém, Pará | Amazonas | Brazil | HYP070-13 | INPA37678-IC2 |
Hyphessobrycon eques | Parintins, Amazonas | Amazonas | Brazil | HYP072-13 | INPA37680-AL1 |
Hyphessobrycon erythrostigma | Tabatinga, Amazonas | Solimões | Brazil | HYP073-13 | INPA37681-AP1 |
Hyphessobrycon erythrostigma | Tabatinga, Amazonas | Solimões | Brazil | HYP074-13 | INPA37681-AP2 |
Hyphessobrycon epicharis | São Gabriel da Cachoeira, Amazonas | Negro | Brazil | HYP002-13 | INPA37665-JUF1 |
Hyphessobrycon epicharis | São Gabriel da Cachoeira, Amazonas | Negro | Brazil | HYP003-13 | INPA37665-JUF2 |
Hyphessobrycon megalopterus | – | – | – | FJ749058 | – |
Hyphessobrycon megalopterus | – | – | – | KU568879.1 | – |
Hyphessobrycon pyrrhonotus | Santa Isabel do rio Negro, Amazonas | Negro | Brazil | HYP039-13 | INPA37672-TRO1 |
Hyphessobrycon pyrrhonotus | Santa Isabel do rio Negro, Amazonas | Negro | Brazil | HYP040-13 | INPA37672-TRO10 |
Hyphessobrycon pyrrhonotus | Santa Isabel do rio Negro, Amazonas | Negro | Brazil | HYP042-13 | INPA37672-TRO2 |
Hyphessobrycon socolofi | Santa Isabel do rio Negro, Amazonas | Negro | Brazil | HYP020-13 | INPA37667-UR1 |
Hyphessobrycon socolofi | Santa Isabel do rio Negro, Amazonas | Negro | Brazil | HYP022-13 | INPA37667-UR7 |
Hyphessobrycon rosaceus | São Gabriel da Cachoeira, Amazonas | Negro | Brazil | HYP032-13 | INPA37669-MAC4 |
Hyphessobrycon rosaceus | Nova Airão, Amazonas | Negro | Brazil | HYP069-13 | INPA37677-FU1 |
Hyphessobrycon rosaceus | São Gabriel da Cachoeira, Amazonas | Negro | Brazil | HYP082-13 | INPA37682-ACA1 |
Hyphessobrycon sweglesi | São Gabriel da Cachoeira, Amazonas | Negro | Brazil | HYP024-13 | INPA37668-JAR1 |
Hyphessobrycon sweglesi | São Gabriel da Cachoeira, Amazonas | Negro | Brazil | HYP025-13 | INPA37668-JAR2 |
Hyphessobrycon sweglesi | São Gabriel da Cachoeira, Amazonas | Negro | Brazil | HYP028-13 | INPA37668-JAR5 |
Moenkhausia hemigrammoides | Rupununi Road-Guyana | – | Guyana | HYP101-13 | INPA38532-PR1 |
Pristella maxillaris | – | – | – | KU568982.1 | – |
Pristella maxillaris | – | – | – | KU568981.1 | – |
Hyphessobrycon flammeus | – | – | Brazil | FUPR988-09 | LBPV-40464 |
Hyphessobrycon anisitsi | – | – | Brazil | GBGCA516-10 | FJ749040 |
The unified species concept (
Two distinct operational criteria to delimit species, based on morphological and molecular data, were implemented here. The Population Aggregation Analysis (
Only morphological character states were used for this method. The morphological data was based on both examined material (see Comparative material examined) and the literature (e.g.,
Pairwise genetic distances between species were calculated using Kimura-2-parameters model (K2P) (
CICCAA 00695, 25.9 mm SL, Brazil, Maranhão State: stream at the Anapurus municipality, 03°40'14"S, 43°07'10"W, 05 Feb 2017, Guimarães E. C. and Brito P. S.
All from Brazil, Maranhão State: CICCAA 00430, 15,18.4–25.2 mm SL; CICCAA 00696, 15, 19.9–24.4mm SL, CICCAA 00697, 16 (C&S) 19.3–24.5 mm SL; CICCAA 00698, 6, 1 (C&S) 22.0–20.4 mm SL; CICCAA 00750, 9, 20.0–25.3mm SL;
(PAA). The new species Hyphessobrycon piorskii sp. n., promptly differs from most congeners except by species of Hyphessobryconsensu stricto by the presence of a dark brown or black blotch on dorsal fin (vs. absence), no midlateral stripe on the body (vs. presence) and Weberian apparatus upward horizontal through dorsal margin of operculum (vs. downward).
The new species herein described differs from all of its congeners from Hyphessobryconsensu stricto, with exception to H. bentosi and H. hasemani, by possessing an inconspicuous vertically elongated humeral spot [vs. approximately rounded humeral spot in H. copelandi, H. erythrostigma, H. jackrobertsi, H. minor, H. pando, H. paepkei, H. pyrrhonotus, H. roseus, H. socolofi, and H. sweglesi; humeral spot horizontally or posteriorly elongated in H. epicharis, H. khardinae, and H. werneri; conspicuous humeral spot in H. eques, H. haraldschultzi Travassos, 1960, H. micropterus, H. megalopterus, H. simulatus and H. takasei; and absence of humeral spot in H. compresus, H. dorsalis Zarske, 2014, H. georgettae, H. pulchripinnis, and H. rosaceus].
The new species differs from H. bentosi by the absence of an extended and pointed dorsal and anal-fin tips (Figures
Hyphessobrycon piorskii sp. n. ACICCAA 00698, paratype, 26.9 mm SL, Brazil: Maranhão State: Munim River basin; living specimen photographed immediately after collection BCICCAA 00089, paratype, 25.2 mm SL, Brazil: Maranhão State: Munim River basin; living specimen photographed immediately after collection (photographed by Felipe Ottoni).
Morphometric data of holotype and paratypes are presented in Table
Color in alcohol Figure
Dorsal fin ground coloration hyaline, with a conspicuous black or dark brown spot located on anterior portion of fin, reaching about sixth ray, approximately between half to two thirds of fin depth. Anal and caudal fins hyaline. Caudal fin with a darker, usually dark brown, posterior margin and on its base. Adipose fin hyaline to light brown, with dark brown or black chromatophores more concentrated on its dorsal portion, depending on the state of preservation of the specimen. Pectoral and pelvic fins hyaline; pelvic fin with variable amounts dark brown pigmentation remaining depending on the state of preservation of the specimen.
Color in life (Figure
Conspicuous black spot on dorsal-fin, with yellow or orange pigmentation on dorsal and ventral margins of spot; yellow or orange pigmentation lighter and less evident on dorsal margin, reaching half to two thirds of the spot length and extending to the tip of fin; yellow or orange pigmentation darker and more developed at ventral margin of the spot, reaching entire spot base length, not extended to dorsal fin-base. Rest of dorsal fin hyaline. Anal-fin base with red pigmentation, with different degrees of intensity, with milk white pigmentation on anterior tip of anal fin, which could be extended through entire anterior margin, reaching between second to fourth rays. Posterior margin of anal fin with an inconspicuous dark brown pigmentation. Adipose fin light brown to hyaline at base, with red to black pigmentation at tip. Pectoral and pelvic fins hyaline, with some sparser dark brown chromatophores, more concentrated at pelvic fin base. First ray of pelvic fin with a white pigmentation. Caudal fin with red pigmentation on almost fin, with an inconspicuous light brown, reddish brown or dark brown margin.
Sexual dimorphism. Mature males have hooks on anal-fin and pelvic-fin rays. Hooks absent on females. Anal-fin presenting hooks from 3rd, 4th or 5th rays through last ray. Number of hooks variable, increasing from the first ones to the last rays. Pelvic fin presenting 3rd and 4th rays with 5 smaller hooks (Figures
DNA-based identification. After trimming sequence ends with poor base call quality, the final alignment yielded 446 base pairs with 154 variable sites, and 22 haplotypes. The magnitude of sequence divergence clearly demonstrates the existence of a new species of Hyphessobrycon inhabiting the Munim and Preguiças river basins in Maranhão State. Average genetic distances were 14.2%, with the highest values between H. pyrrhonotus and H. epicharis (19.2%), while the lowest value (2.7%) was between H. epicharis and H. sweglesi (Table
Other evidence for the new species is that H. piorskii sp. n. formed a single and exclusive clade with maximum posterior probability support (posterior probability = 1) in the Bayesian phylogenetic tree (Figure
Kimura-2 parameters pairwise genetic distances among species. Species names in the upper columns are abbreviated as follows: H. piorskii (Hpio), H. flammeus (Hfla), H. anisitsi (Han), H. socolofi (Hsoc), H. copelandi (Hcop), H. bentosi (Hben), H. megalopterus (Hmeg), H. eques (Hequ), H. erythrostigma (Hery), H. pyrrhonotus (Hpyr), H. rosaceus (Hros), H. sweglesi (Hswe), H. epicharis (Hepi), M. hemigrammoides (Mhem), and P. maxillaris (Pmax).
Species | Hpio | Hfla | Hani | Hsoc | Hcop | Hben | Hmeg | Hequ | Hery | Hpyr | Hros | Hswe | Hepi | Mhem |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Hfla | 0.190 | - | ||||||||||||
Hani | 0.194 | 0.165 | - | |||||||||||
Hsoc | 0.199 | 0.193 | 0.168 | - | ||||||||||
Hcop | 0.158 | 0.206 | 0.162 | 0.216 | - | |||||||||
Hben | 0.207 | 0.204 | 0.173 | 0.008 | 0.221 | - | ||||||||
Hmeg | 0.195 | 0.209 | 0.180 | 0.087 | 0.213 | 0.086 | - | |||||||
Hequ | 0.161 | 0.205 | 0.186 | 0.190 | 0.102 | 0.194 | 0.199 | - | ||||||
Hery | 0.196 | 0.213 | 0.182 | 0.114 | 0.191 | 0.117 | 0.131 | 0.174 | - | |||||
Hpyr | 0.183 | 0.206 | 0.166 | 0.101 | 0.191 | 0.103 | 0.117 | 0.181 | 0.032 | - | ||||
Hros | 0.218 | 0.212 | 0.205 | 0.224 | 0.202 | 0.227 | 0.204 | 0.195 | 0.219 | 0.221 | - | |||
Hswe | 0.205 | 0.187 | 0.195 | 0.224 | 0.198 | 0.229 | 0.192 | 0.183 | 0.216 | 0.211 | 0.073 | - | ||
Hepi | 0.199 | 0.190 | 0.198 | 0.221 | 0.198 | 0.226 | 0.199 | 0.183 | 0.233 | 0.231 | 0.089 | 0.028 | - | |
Mhem | 0.185 | 0.204 | 0.178 | 0.214 | 0.216 | 0.219 | 0.234 | 0.205 | 0.233 | 0.222 | 0.200 | 0.204 | 0.208 | - |
Pmax | 0.223 | 0.212 | 0.197 | 0.203 | 0.219 | 0.207 | 0.218 | 0.200 | 0.230 | 0.239 | 0.202 | 0.187 | 0.181 | 0.169 |
Morphometric data (N = 95) for the holotype and paratypes of Hyphessobrycon piorskii sp. n. from the Munim River basin and Preguiças River basin. Abbreviations: SD: Standard deviation.
Holotype | Paratypes | Mean | SD | |
---|---|---|---|---|
Standard length | 25.9 | 18–29.4 | 20.8 | – |
Percentages of standard length | ||||
Depth at dorsal-fin origin (body depth) | 35.9 | 28.9–39.4 | 33.4 | 1.9 |
Snout to dorsal-fin origin | 49.8 | 44.2–56.5 | 52.5 | 2.1 |
Snout to pectoral-fin origin | 29.1 | 26.0–35.0 | 30.8 | 2.3 |
Snout to pelvic-fin origin | 47.5 | 39.1–52.2 | 47.5 | 1.9 |
Snout to anal-fin origin | 61.9 | 57.4–66.6 | 61.7 | 1.8 |
Caudal peduncle depth | 11.8 | 9.1–14.1 | 11.4 | 0.9 |
Caudal peduncle length | 12.2 | 8.1–13.6 | 10.2 | 1.1 |
Pectoral-fin length | 20.4 | 16.8–23.7 | 20.8 | 1.6 |
Pelvic-fin length | 18.1 | 13.3–20.4 | 17.1 | 1.5 |
Dorsal-fin base length | 15.5 | 12.9–18.3 | 15.7 | 1.2 |
Dorsal-fin height | 28.5 | 22.1–34.3 | 29.9 | 2.4 |
Anal-fin base length | 29.4 | 26.3–33.9 | 30.3 | 1.4 |
Eye to dorsal-fin origin | 35.2 | 33.6–39.4 | 36.4 | 1.4 |
Dorsal-fin origin to caudal-fin base | 50.7 | 44.9–57.3 | 51.4 | 2.3 |
Head length | 26.3 | 24.2–33.4 | 29.3 | 2.1 |
Percentages of head length | ||||
Horizontal eye diameter | 42.8 | 33.4–43.8 | 38.2 | 2.3 |
Snout length | 22.0 | 16.9–24.4 | 20.2 | 1.7 |
Least interorbital width | 25.7 | 16,4–27.0 | 20.4 | 2.2 |
Upper jaw length | 39.6 | 32.8–41.7 | 38.1 | 2.2 |
Hyphessobrycon piorskii sp. n. is presently known only from the upper Munim and Preguiças river basins, Maranhão State, northeastern Brazil (Figure
Hyphessobrycon piorskii sp.n. lives in shallow well-oxygenated streams with transparent waters flowing over different types of substrates (Figure
The name piorskii honors the ichthyologist Nivaldo Magalhães Piorski for his contributions to the ichthyologic knowledge of the Maranhão State.
Despite Hyphessobrycon, as defined today, being a non-monophyletic group (
Among the species considered by
Hyphessobrycon piorskii sp. n. exhibits all the diagnostic features that define Hyphessobryconsensu stricto (see introduction and diagnosis section). The new species differs from the other possible species of this assemblage, which also occur near Maranhão (e.g., lower Amazon River basin, Guamá River basin, and São Francisco River basin), such as H. bentosi, H. copelandi, H. eques, H. dorsalis, H. hasemani, H. haraldschultzi, H. micropterus, and H. werneri, by a set of features listed below.
Hyphessobrycon piorskii sp. n. possesses an inconspicuous vertically elongated humeral spot, distinguishing it from all the species cited above, except for H. bentosi and H. hasemani (see morphological diagnosis section). The shape of the dorsal-fin spot is also useful to distinguish H. piorskii sp. n. from H. eques, H. hasemani and H. micropterus, which possess dorsal fin spot vertically extended, reaching the tip of the fin, while in H. piorskii sp. n. the black spot of dorsal fin never reaches the tip of the fin. The new species also differs from H. eques by the color pattern of the anal fin: H. eques possess a conspicuous black anal-fin margin on preserved species, while H. piorskii sp. n. does not exhibit this feature at the anal fin.
The number of teeth cusps was also revealed to be a useful feature for species discrimination. Hyphessobrycon piorskii sp. n. possess all of its teeth with one to three cusps (never pentacuspid), while H. eques possess pentacuspid teeth on the maxillary and inner row of premaxillary, and H. copelandi and H. hasemani on the dentary and inner row of the premaxilla (see
The description of H. piorskii sp. n. was based on morphological and molecular species delimitation methods, using the congruence of multiple operational criteria for determining species boundaries. As mentioned earlier, evidence corroborated from multiple operational criteria is considered to produce stronger hypotheses of lineage divergence (
Our Bayesian tree also recovered H. piorskii sp. n. within the Hyphessobryconsensu stricto group with high support (posterior probability = 0.94), which fits the morphological evidence, since H. piorskii sp. n. exhibits the three main diagnostic character states of the group (see introduction and diagnosis section). Hyphessobrycon piorskii sp. n. was recovered as the sister-group of the clade including H. bentosi, H. socolofi, H. megalopterus, H. erythrostigma, and H. pyrrhonotus, however this relationship was supported by a lower support value (posterior probability value = 0.55). Only posterior probability values about or higher than 0.95 are considered as statistically significant (
We thank Wilson Costa for the loan and donation of material; Riccardo Mugnai for his assistance with osteological photographs; Ingo Schindler for providing useful literature; Vale S.A and Amplo Engenharia for the cession of part of the data analysed in this study; We also thank Pensoft and Clarisse Figueiredo for her English revisions; Elioenai Oliveira, Ivanilda Nascimento, Rozijane Fernandes, Valquíria Carneiro, Shyrley Viana, Marciara Lopes, Revangivaldo Sousa, Diego Campos, Pedro Bragança, Beldo Ferreira and Lucas Oliveira for collecting the examined material. This paper benefited from suggestions provided by Javier Maldonado and two reviewers: Jorge Enrique García Melo and Carlos García-Alzate. This study was supported by CNPq (National Council for Scientific and Technological Development – Ministry of Science, Technology Innovation and Communication) and FAPEMA (Foundation for Scientific Research and Development of Maranhão). We also thank FACEPE (Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco) for providing a scholarship to LMF. All material was collected with permits 51540-3/ from SISBIO (Brazilian Institute of Environment and Natural Resources).