Research Article |
Corresponding author: Wilson J. E. M. Costa ( wcosta@acd.ufrj.br ) Academic editor: Nicolas Hubert
© 2022 Wilson J. E. M. Costa, José Leonardo O. Mattos, Wagner M. S. Sampaio, Patrícia Giongo, Frederico B. de Almeida, Axel M. Katz.
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:
Costa WJEM, Mattos JLO, Sampaio WMS, Giongo P, de Almeida FB, Katz AM (2022) Phylogenetic relationships of a new catfish of the genus Trichomycterus (Siluriformes, Trichomycteridae) from the Brazilian Cerrado, and the role of Cenozoic events in the diversification of mountain catfishes. Zoosystematics and Evolution 98(1): 151-164. https://doi.org/10.3897/zse.98.83109
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The Brazilian Cerrado highlands shelter the headwaters of the three largest South American hydrographic basins, where a great species diversity is concentrated, but some biological groups are still insufficiently known. The focal taxa of this study are trichomycterid catfishes of the subgenus Cryptocambeva, genus Trichomycterus, endemic to mountain areas of south-eastern Brazil. The primary objective of this study is to test through a molecular phylogeny if a new species collected in streams of the upper Rio Paraná basin draining the Serra da Canastra is sister to T. macrotrichopterus, endemic to the upper Rio São Francisco at another facet of the Serra da Canastra, as suggested by morphological data. The analysis corroborated sister group relationships between these two species, besides supporting four main clades in Cryptocambeva, each of them endemic to distinct mountain regions. A time-calibrated analysis supported the divergence timing between the new species and T. macrotrichopterus at the Pliocene, which is chronologically compatible with the final period of intense fluvial configuration re-arrangement, when São Francisco headwater streams were captured by the Paraná basin. The new species herein described is similar to T. macrotrichopterus and distinguished from all other species of Cryptocambeva by having a long pectoral-fin filament. These two species are distinguished from each other by characteristics of the latero-sensory system, colour pattern and bone morphology.
molecular systematics, mountain biodiversity, osteology, paleo-drainages, Rio Paraná basin
Studies on the Cerrado biota have quickly increased since the 1980s (
The great trichomycterine species diversity concentrated in mountain ranges of south-eastern Brazil is probably a consequence of the past Cenozoic scenario, characterised by intense re-arrangements of the hydrographic systems due to generalised uplift during the Neogene (
The main focus of this study is an undescribed species of Trichomycterus, subgenus Cryptocambeva Costa, 2021, from the upper Rio Araguari drainage, upper Rio Paraná basin. Cryptocambeva comprises 16 species and is diagnosable by a unique morphology of the latero-posterior portion of the neurocranium and adjacent posterior region, including a relatively small posttemporo-supracleithrum separated by large interspaces from adjacent bones, and a narrow and long lateral extremity of the pterotic, with its tip extending beyond the lateral margin of the neurocranium (
The primary objectives of this study are to perform a multigene phylogenetic analysis to test the phylogenetic positioning of the new taxon and to provide a formal description to it. The secondary objective is to conduct a dating analysis in order to establish if the estimated divergence timing for Cryptocambeva lineages from south-eastern Brazil is compatible with the available model for the temporal drainage network evolution.
Material used in this study included specimens previously deposited in ichthyological collections: Instituto de Biologia, Universidade Federal do Rio de Janeiro (
Measurements were made using landmarks proposed by
DNA was extracted from muscle tissues of the caudal peduncle, using DNeasy Blood & Tissue Kit (Qiagen), according to manufacturer’s protocol. Amplification of DNA fragments was made using polymerase chain reaction (PCR) method, with primers RAG2 TRICHO F and RAG2 TRICHO R (
The new species and twelve species representing all lineages of Cryptocambeva were included as terminal taxa in the analyses, besides four trichomycterine out-groups: Trichomycterus albinotatus Costa, 1992, a member of the subgenus Humboldtglanis Costa, 2021 that is sister to Cryptocambeva (
Alignment was conducted in Clustal W (
The concatenated dataset was additionally analysed using Bayesian Inference (BI) with Mrbayes 3.2.5 (
Terminal taxa were the same as above, but including additional outgroups: the trichomycterines Scleronema minutum (Boulenger, 1891) and Ituglanis boitata Ferrer, Donin & Malabarba, 2015; Microcambeva ribeirae Costa, Lima & Bizerril, 2004, a member of the Microcambevinae that is sister to the Trichomycterinae (
Osteological structures included in the description are those that have informative variability to diagnose species of the eastern South American trichomycterine clade (e.g.
The phylogenetic analyses generated identical trees, which corroborated the new taxon as sister to T. macrotrichopterus with high support values (Fig.
Phylogenetic tree generated by Maximum Likelihood analysis for 13 species of Cryptocambeva and four trichomycterine outgroups (most external out-group, ‘Trichomycterus’ areolatus, not depicted in the figure), using a multigene data set (CYTB, ND4 and RAG2, total of 2545 bp); numbers above branches are: SH-aLRT support (%) / aBayes support / ultrafast bootstrap support (%); numbers below branches are posterior probabilities from the Bayesian Inference; asterisks indicate maximum support values; minus sign indicate support values below 0.8 for aBayes support and posterior probability, and below 50% for SH-aLRT support and ultrafast bootstrap support. CAN-clade means Canastra clade; ESP-clade, Espinhaço clade; NMM-clade, northern Mantiqueira-Mar clade, and SMM-clade, southern Mantiqueira-Mar clade.
Time-scaled maximum credibility tree obtained from the Bayesian analysis in Beast for 13 species of Cryptocambeva and 11 outgroups, using a multigene data set (CYTB, ND4 and RAG2, total of 2545 bp). Numbers above the branches indicates the average age of the nodes and bars represent the 95% highest posterior densities intervals for the ages. Red dots indicate the nodes with posterior probabilities values inferior to 80. The time scale is express in millions of years.
All from Brazil: Minas Gerais State: Araxá Municipality: Rio Araguari subdrainage, Rio Paranaíba drainage, Rio Paraná basin.
Trichomycterus araxa is distinguished from all other species of the subgenus Cryptocambeva by the presence of a black median longitudinal stripe on the caudal fin in juvenile specimens below about 40 mm SL (Fig.
General morphology
(Figs
Holotype | Paratypes (n = 10) | Mean | |
---|---|---|---|
Standard length (mm) | 53.6 | 43.3–64.0 | 53.5 |
Percent of standard length | |||
Body depth | 19.3 | 15.8–20.9 | 18.5 |
Caudal peduncle depth | 14.7 | 13.4–15.8 | 14.7 |
Body width | 11.7 | 10.4–13.2 | 12.3 |
Caudal peduncle width | 4.1 | 3.8–5.6 | 4.6 |
Pre-dorsal length | 64.2 | 63.2–67.5 | 65.3 |
Pre-pelvic length | 59.6 | 58.0–62.3 | 60.0 |
Dorsal-fin base length | 11.6 | 11.4–14.2 | 12.4 |
Anal-fin base length | 8.7 | 9.0–11.6 | 9.8 |
Caudal-fin length | 19.0 | 17.3–20.2 | 18.9 |
Pectoral-fin length | 15.0 | 12.3–14.6 | 13.3 |
Pelvic-fin length | 10.2 | 9.7–11.3 | 10.5 |
Head length | 20.2 | 19.4–21.6 | 20.1 |
Percent of head length | |||
Head depth | 54.9 | 51.0–67.9 | 56.2 |
Head width | 83.4 | 82.8–95.7 | 87.7 |
Snout length | 47.2 | 42.4–48.7 | 45.9 |
Interorbital length | 30.2 | 25.4–33.5 | 29.4 |
Preorbital length | 11.6 | 9.4–13.6 | 11.5 |
Eye diameter | 11.1 | 9.2–11.1 | 10.2 |
Dorsal and anal fins subtriangular, distal margin slightly convex; total dorsal-fin rays 10 or 11 (i–ii + II + 7), total anal-fin rays 9 (ii + II + 5); anal-fin origin at vertical through base of 5th branched dorsal-fin ray. Pectoral fin subtriangular in dorsal view, posterior margin slightly convex, first pectoral-fin ray terminating in long filament, reaching about 40–60% of pectoral-fin length in specimens above about 50 mm SL; total pectoral-fin rays 7 (I + 6). Pelvic fin subtruncate, its posterior extremity at vertical through middle of dorsal-fin base and posterior to urogenital aperture; pelvic-fin bases medially in contact; total pelvic-fin rays 5 (I + 4). Caudal fin subtruncate, posterior corners rounded; total principal caudal-fin rays 13 (I + 11 + I), total dorsal procurrent rays 20–23 (xix–xxii + I), total ventral procurrent rays 16 or 17 (xv–xvi + I).
Laterosensory system. Supraorbital sensory canal continuous, posteriorly connected to posterior section of infraorbital canal. Supraorbital pores 3, all paired: s1, adjacent to medial margin of anterior nostril; s3, adjacent and just posterior to medial margin of posterior nostril; s6, at transverse line through posterior half of orbit. Pores s6 nearer its symmetrical homologous pore than orbit. Infraorbital sensory canal arranged in 2 segments; anterior section isolated, with two pores: i1, at transverse line through anterior nostril, i3, at transverse line just anterior to posterior nostril; posterior segment posteriorly connected to postorbital canal, with 2 pores: i10, adjacent to ventral margin of orbit, i11, posterior to orbit. Postorbital canal with 2 pores: po1, at vertical line above posterior portion of interopercular patch of odontodes, po2, at vertical line above posterior portion of opercular patch of odontodes. Lateral line of body short, with 1 pore just posterior to head.
Osteology
(Fig.
Osteological features in Trichomycterus araxa sp. nov (A–C) and T. macrotrichopterus (D, E). A, D. Mesethmoidal region, middle and left portions, dorsal view; B, E. Left jaw suspensorium and opercular apparatus, lateral view; C. Parurohyal, ventral view. lee, lateral ethmoid expansion. Larger stippling represents cartilages.
Hyomandibula long, with well-developed anterior outgrowth; middle portion of dorsal margin of hyomandibula slightly concave. Opercle slender, with moderately deep odontode patch with 12–16 odontodes transversely arranged. Opercular odontodes pointed, anterior odontodes narrow and straight, posterior odontodes slightly broader, slightly curved. Dorsal process of opercle short. Opercular articular facet for hyomandibula with prominent rounded extension, articular facet for preopercle well developed, rounded. Interopercular patch of odontodes long, about four fifths of hyomandibula length, with 26–31 odontodes. Interopercular odontodes pointed, arranged in irregular longitudinal rows. Preopercle slender, narrowing anteriorly.
Parurohyal robust, lateral process subtriangular, latero-posteriorly directed, tip pointed; parurohyal head well-developed, with prominent anterolateral paired process; middle foramen oval circular; posterior process long, slightly shorter or equal to distance between anterior margin of parurohyal and anterior insertion of posterior process. Branchiostegal rays 8. Vertebrae 35. Ribs 12 or 13. Dorsal-fin origin at vertical through centrum of 19th vertebra; anal-fin origin at vertical through centrum of 22nd or 23rd vertebra. Two dorsal hypural plates, corresponding to hypurals 4 + 5 and 3, respectively; single ventral hypural plate corresponding to hypurals 1 and 2, and parhypural.
Colouration
(Figs
The name araxa is a reference to the occurrence of the new species in the region of Araxá, a historical Brazilian city founded in the 18th century, during the colonial period. The word araxa is possibly derived from the Tupi-Guarani to designate some native people formerly inhabiting the region.
Trichomycterus araxa occurs in the Rio Quebra Anzol drainage, which is part of the Rio Paranaíba drainage, a main tributary of the upper Rio Paraná basin, in altitudes about 940–1020 m asl (Fig.
Cryptocambeva occurs in a broad area of eastern South America, comprising different river basins and mountain ranges of south-eastern Brazil (Fig.
The phylogenetic analyses highly supported T. araxa as sister to T. macrotrichopterus (Fig.
Recent studies have shown a high concentration of closely related trichomycterine species in different South American regions, often exhibiting geographical distribution patters restricted to some neighbouring river drainages around mountain and high plateau areas (e.g.
The divergence timing between T. araxa from the upper Rio Araguari and its sister group, T. macrotrichopterus, from the upper section of the main canal of the Rio São Francisco, at the Pliocene (Fig.
We are grateful to Valter M. Azevedo-Santos, for discussion about fish distribution patterns in the upper Paraná basin and help during type material collection. The manuscript benefitted from reviews provided by Francisco Langeani and Paulo Brito. Thanks are also due to the Meio Ambiente team of the Companhia Brasileira de Metalurgia e Mineração, for allowing collections and use of specimens from the farms comprising the RPPN São Sebastião and Monte Alto, and to Aléssio Datovo and Michel Gianeti by the loan of specimens. This work was partly supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; grant 304755/2020-6 to WJEMC), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ; grant E-26/201.213/2021 to WJEMC, E-26/202.005/2020 to AMK, and E-26/202.327/2018 to JLM). This study was also supported by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Finance Code 001) through Programa de Pós-Graduação em: Biodiversidade e Biologia Evolutiva /
Tables S1, S2
Data type: pdf file
Explanation note: Table S1. Terminal taxa for molecular phylogeny and respective GenBank accession numbers. Table S2. Best-fitting models.