Iterative taxonomy reveals a new species of <i>Cambeva</i> (Siluriformes: Trichomycteridae) with intraspecific variation from the rio Piquiri and Ivaí basin, upper rio Paraná basin, Brazil

A new species of Cambeva occurring in the rio Piquiri and Ivaí, upper rio Paraná basin, Brazil, is described using the combination of morphological and molecular data. The new species is distinguished from most congeners by the presence of a notch in the posterior portion of the metapterygoid, number of branchiostegal rays, opercular and interopercular odontodes, and ribs. In addition, the results corroborated the existence of a single species with wide intraspecific variation in body coloration. The type-locality is within the area of influence of the Perobas Biological Reserve, a Conservation Unit in the Paraná State, composed of two Atlantic Forest physiognomic forms. Considering that the upper rio Paraná basin is an area of significant anthropic influence, it is crucial to describe and preserve species to understand their ichthyofauna.

Keywords:
COI; Conservation; Linnean shortfall; Ostariophysi; Trichomycterinae

Authorship

Isadora Carolina Martins

Conceptualization

Formal analysis

Investigation

Methodology

Writing-original draft

Writing-review and editing

Coleção Ictiológica, Nupélia, Departamento de Biologia, Centro de Ciências Biológicas, Universidade Estadual de Maringá, Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil. (ICM) icmartins@outlook.com.br (corresponding author), (RBR) reis.renanb@gmail.com, (WJG) weferson@nupelia.uem.br.Universidade Estadual de MaringáBrazilMaringá, PR, BrazilColeção Ictiológica, Nupélia, Departamento de Biologia, Centro de Ciências Biológicas, Universidade Estadual de Maringá, Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil. (ICM) icmartins@outlook.com.br (corresponding author), (RBR) reis.renanb@gmail.com, (WJG) weferson@nupelia.uem.br.

Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais, Departamento de Biologia, Centro de Ciências Biológicas, Universidade Estadual de Maringá. Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil. (BHMS) bhmstabile@gmail.com.Universidade Estadual de MaringáBrazilMaringá, PR, BrazilPrograma de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais, Departamento de Biologia, Centro de Ciências Biológicas, Universidade Estadual de Maringá. Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil. (BHMS) bhmstabile@gmail.com.

https://orcid.org/0000-0002-1104-2615

Renan Borges dos Reis

Conceptualization

Formal analysis

Investigation

Methodology

Writing-original draft

Writing-review and editing

https://orcid.org/0000-0002-3704-0749

Bruno Henrique Mioto Stabile

Conceptualization

Formal analysis

Investigation

Methodology

Writing-original draft

Writing-review and editing

https://orcid.org/0000-0002-3524-537X

Weferson Júnio da Graça

Conceptualization

Formal analysis

Investigation

Methodology

Writing-original draft

Writing-review and editing

Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia), Centro de Ciências Biológicas, Universidade Estadual de Maringá. Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil.Universidade Estadual de MaringáBrazilMaringá, PR, BrazilNúcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia), Centro de Ciências Biológicas, Universidade Estadual de Maringá. Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil.

Programa de Pós-Graduação em Biologia Comparada, Centro de Ciências Biológicas, Universidade Estadual de Maringá. Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil.Universidade Estadual de MaringáBrazilMaringá, PR, BrazilPrograma de Pós-Graduação em Biologia Comparada, Centro de Ciências Biológicas, Universidade Estadual de Maringá. Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil.

https://orcid.org/0000-0002-8925-5629

Edited-by

Carlos DoNascimiento

Correspondence

Isadora Carolina Martins icmartins@outlook.com.br

Competing Interests

The author declares no competing interests.

Ethical Statement

Not applicable.

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables

Figures (10)
Tables (2)

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FIGURE 1 |
Cambevaperobana, holotype: NUP 23907, 75.9 mm SL, Brazil, Paraná State, rio Mouro, tributary of rio Goioerê, rio Piquiri basin, upper rio Paraná.

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FIGURE 2 |
Dorsal view of neurocranium of Cambeva perobana paratypes. A. NUP 24271, 48.1 mm SL. B. NUP 24272, 50.5 mm SL. Abbreviations: af, anterior fontanel; an, antorbital; ap, autopalatine; ba, barbular bone; ep, epioccipital; fr, frontal; le, lateral ethmoid; i10 and i11, infraorbital sensory pores of the laterosensory system; me, mesethmoid; mx, maxilla; pf, posterior fontanel; pm, premaxilla; po1 and po2, postotic sensory pores 1 and 2; ps, posttemporo-supracleithrum; pt, pterotic; s1 s3, and s6, supraorbital sensory pores of the laterosensory system; sp + po + pn, sphenotic–prootic–pterosphenoid complex bone; su, parieto-supraoccipital; wc, Weberian capsule.

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FIGURE 3 |
A–B. Lateral view of left suspensory of Cambeva perobana. C–D. Medial view of lower jaw. A–C. Morphotype I, paratype, NUP 24271, 48.1 mm SL. B–C. Morphotype II, paratype, NUP 24272, 50.5 mm SL. Abbreviations: ar, anguloarticular; cp, coronoid process; de, dentary; hy, hyomandibula; iop, interopercle; mc, Meckel’s cartilage; mtg, metapterygoid; op, opercle; pop, preopercle; qu, quadrate. Arrow indicates a notch in the posterior portion of the metapterygoid.

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FIGURE 4 |
A–B. Ventral view of left hyoid arch of Cambeva perobana. C–D. Dorsal view of gill arches. A–C. Morphotype I, paratype, NUP 24271, 48.1 mm SL. B–D. Morphotype II, paratype,NUP 24272, 50.5 mm SL. Abbreviations: ac, anterior ceratohyal; bb2–4, basibranchials 2 to 4; br1–9, branchiostegal rays 1 to 9; cb1–5, ceratobranchials 1 to 5; eb1–5, epibranchials 1 to 5; hb1–3, hypobranchials 1 to 3; pb3, pharyngobranchial 3; pc, posterior ceratohyal; tp, tooth plate; vh, ventral hypohyal.

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FIGURE 5 |
Lateral view of morphotypes variation of Cambeva perobana, paratypes. Morphotype I: A. NUP 16086, 72.9 mm SL; B. NUP 17232, 27.4 mm SL; C. NUP 24167, 32.3 mm SL; specimen fixed in absolute alcohol 99.8% for molecular analysis. Morphotype II: D. NUP 24162, 73.7 mm SL; E. NUP 23908, 28.9 mm SL. Arrow indicates inconspicuous narrow dark-brown mid-lateral stripe. Scales bars = 10 mm.

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FIGURE 6 |
Paratype of Cambevaperobana immediately after capture, NUP 24166, 63.2 mm SL, Paraná State, Brazil, rio Mouro, tributary of rio Goioerê, rio Piquiri basin. Scales bar = 10 mm. Arrow indicates an inconspicuous narrow dark-brown mid-lateral stripe.

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FIGURE 7 |
A. Bayesian COI gene tree of Cambeva. B. Bayesian COI gene tree with species delimitation results. Vertical bars represent species delimitation from Assemble Species by Automatic Partition (ASAP), Generalized Mixed Yule Coalescent (GMYC), Bayesian implementation of Poisson Tree Process (bPTP) and its standard implementation (PTP). Circles represent posterior probability ≥ 0.95. Cambevaperobana is shown in red.

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FIGURE 8 |
Partial map of South America, highlighting Brazil and the state of Paraná, showing the geographic distribution of Cambevaperobana in the rio Piquiri and Ivaí basins. The yellow circles represent localities of paratypes, the gray circle represent locality of non-type material and the red star represents the type-locality.

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FIGURE 9 |
A–B. Type-locality of Cambevaperobana, rio Mouro, tributary of rio Concórdia, rio Piquiri basin, upper rio Paraná basin, Paraná State, Brazil. C–D. Microhabitat of C. perobana.

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FIGURE 10 |
Scatter plot of individual scores of samples of Cambeva perobana morphotypes from the Piquiri and Ivaí river basins, in the Principal Component Analysis (PCA).

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TABLE 1 |
Morphometric data for Cambevaperobana. Values of range (minimum-maximum), mean, and standard deviation (SD). Morphotype I (n = 25), Morphotype II (n = 15).

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TABLE 2 |
Loading results of measurements used in the PCA for Cambeva perobana.

FIGURE 1 | Cambevaperobana, holotype: NUP 23907, 75.9 mm SL, Brazil, Paraná State, rio Mouro, tributary of rio Goioerê, rio Piquiri basin, upper rio Paraná.

FIGURE 2 | Dorsal view of neurocranium of Cambeva perobana paratypes. A. NUP 24271, 48.1 mm SL. B. NUP 24272, 50.5 mm SL. Abbreviations: af, anterior fontanel; an, antorbital; ap, autopalatine; ba, barbular bone; ep, epioccipital; fr, frontal; le, lateral ethmoid; i10 and i11, infraorbital sensory pores of the laterosensory system; me, mesethmoid; mx, maxilla; pf, posterior fontanel; pm, premaxilla; po1 and po2, postotic sensory pores 1 and 2; ps, posttemporo-supracleithrum; pt, pterotic; s1 s3, and s6, supraorbital sensory pores of the laterosensory system; sp + po + pn, sphenotic–prootic–pterosphenoid complex bone; su, parieto-supraoccipital; wc, Weberian capsule.

FIGURE 3 | A–B. Lateral view of left suspensory of Cambeva perobana. C–D. Medial view of lower jaw. A–C. Morphotype I, paratype, NUP 24271, 48.1 mm SL. B–C. Morphotype II, paratype, NUP 24272, 50.5 mm SL. Abbreviations: ar, anguloarticular; cp, coronoid process; de, dentary; hy, hyomandibula; iop, interopercle; mc, Meckel’s cartilage; mtg, metapterygoid; op, opercle; pop, preopercle; qu, quadrate. Arrow indicates a notch in the posterior portion of the metapterygoid.

FIGURE 4 | A–B. Ventral view of left hyoid arch of Cambeva perobana. C–D. Dorsal view of gill arches. A–C. Morphotype I, paratype, NUP 24271, 48.1 mm SL. B–D. Morphotype II, paratype,NUP 24272, 50.5 mm SL. Abbreviations: ac, anterior ceratohyal; bb2–4, basibranchials 2 to 4; br1–9, branchiostegal rays 1 to 9; cb1–5, ceratobranchials 1 to 5; eb1–5, epibranchials 1 to 5; hb1–3, hypobranchials 1 to 3; pb3, pharyngobranchial 3; pc, posterior ceratohyal; tp, tooth plate; vh, ventral hypohyal.

FIGURE 5 | Lateral view of morphotypes variation of Cambeva perobana, paratypes. Morphotype I: A. NUP 16086, 72.9 mm SL; B. NUP 17232, 27.4 mm SL; C. NUP 24167, 32.3 mm SL; specimen fixed in absolute alcohol 99.8% for molecular analysis. Morphotype II: D. NUP 24162, 73.7 mm SL; E. NUP 23908, 28.9 mm SL. Arrow indicates inconspicuous narrow dark-brown mid-lateral stripe. Scales bars = 10 mm.

FIGURE 6 | Paratype of Cambevaperobana immediately after capture, NUP 24166, 63.2 mm SL, Paraná State, Brazil, rio Mouro, tributary of rio Goioerê, rio Piquiri basin. Scales bar = 10 mm. Arrow indicates an inconspicuous narrow dark-brown mid-lateral stripe.

FIGURE 7 | A. Bayesian COI gene tree of Cambeva. B. Bayesian COI gene tree with species delimitation results. Vertical bars represent species delimitation from Assemble Species by Automatic Partition (ASAP), Generalized Mixed Yule Coalescent (GMYC), Bayesian implementation of Poisson Tree Process (bPTP) and its standard implementation (PTP). Circles represent posterior probability ≥ 0.95. Cambevaperobana is shown in red.

FIGURE 8 | Partial map of South America, highlighting Brazil and the state of Paraná, showing the geographic distribution of Cambevaperobana in the rio Piquiri and Ivaí basins. The yellow circles represent localities of paratypes, the gray circle represent locality of non-type material and the red star represents the type-locality.

FIGURE 9 | A–B. Type-locality of Cambevaperobana, rio Mouro, tributary of rio Concórdia, rio Piquiri basin, upper rio Paraná basin, Paraná State, Brazil. C–D. Microhabitat of C. perobana.

FIGURE 10 | Scatter plot of individual scores of samples of Cambeva perobana morphotypes from the Piquiri and Ivaí river basins, in the Principal Component Analysis (PCA).

TABLE 1 | Morphometric data for Cambevaperobana. Values of range (minimum-maximum), mean, and standard deviation (SD). Morphotype I (n = 25), Morphotype II (n = 15).

	Morphotype I				Morphotype II
	Holotype	Min-Max	Mean	SD	Min-Max	Mean	SD
Standard length (mm)	75.9	27.60–79.50	58.30	–	29.09–74.78	51.42	–
Percent of standard length
Trunk	41.3	36.5–45.3	41.7	2.04	39.9–41.9	41.2	0.82
Preanal length	71.7	69.7–78.0	73.6	2.11	70.2–72.6	71.1	1.32
Prepelvic length	57.4	54.9–61.4	57.8	1.83	55.7–59.0	57.0	1.23
Pelvic-anal fins distance	14.7	7.7–17.3	14.3	2.09	13.1–15.5	14.4	1.62
Caudal-peduncle length	17.2	15.3–22.4	18.7	1.73	19.7–22.0	21.0	1.40
Scapular-girdle width	13.6	12.9–18.5	15.5	1.34	14.7–16.8	15.7	0.74
Pectoral-fin length	13.3	10.3–16.0	12.7	1.31	11.4–15.6	13.6	1.48
Pelvic-fin length	7.8	7.5–9.7	8.6	0.66	7.8–9.8	8.8	0.69
Anal-fin length	15.4	13.3–16.4	15.1	0.82	14.5–16.3	15.4	1.09
Head length	18.0	17.2–20.6	18.9	0.82	17.2–20.5	18.8	1.38
Predorsal length	66.1	63.3–69.8	66.5	1.82	63.4–66.9	65.0	1.74
Body length	80.9	79.6–86.1	83.2	1.92	84.1–86.0	84.9	1.99
Dorsal-fin length	16.4	13.1–18.5	16.6	1.21	16.1–18.4	17.2	1.43
Body depth	15.7	13.2–18.5	15.4	1.38	13.4–16.4	15.2	1.27
Dorsal-fin base length	11.0	8.2–12.5	10.6	1.09	9.9–12.1	10.9	0.84
Anal-fin base length	9.1	6.8–12.9	9.0	1.24	7.4–10.2	8.6	0.87
Caudal-peduncle depth	13.7	11.0–16.2	13.4	1.10	11.3–15.0	13.2	1.01
Percent of head length
Head width	74.2	73.8–89.3	81.7	4.69	76.4–88.0	81.1	5.43
Nasal-barbel length	44.8	36.9–74.3	50.8	9.93	50.4–64.0	56.0	4.87
Maxillary-barbel length	53.5	46.7–78.5	57.1	7.57	47.1–63.2	53.6	4.87
Rictal-barbel length	40.6	40.6–73.0	56.8	8.56	44.2–56.8	50.8	5.32
Snout length	44.0	34.9–52.4	42.3	3.54	40.3–44.7	42.4	2.20
Interorbital	20.1	20.1–29.9	25.1	2.53	21.5–25.3	23.6	1.76
Mouth width	41.7	34.9–53.0	45.4	4.49	34.4–52.9	45.8	4.90
Eye diameter	6.3	6.3–14.2	8.6	1.80	7.7–11.8	9.5	1.39
Supraorbital pores s6 distance	12.5	6.6–19.3	12.0	3.04	11.6–15.5	13.4	1.91

TABLE 2 | Loading results of measurements used in the PCA for Cambeva perobana.

Morphometric data	PC 1	PC 2	PC 3
Preanal lenght	0.029	-0.101	-0.02625
Prepelvic lenght	0.031	-0.073	-0.1071
Pelvic-anal distance	-0.251	-0.048	0.60038
Caudal-penduncle length	0.088	0.001	-0.16695
Scapular girdle width	0.069	0.026	0.042599
Pectoral-fin length	-0.061	-0.170	-0.0314
Pelvic-fin length	0.131	-0.095	-0.03154
Anal-fin length	0.034	-0.106	-0.06591
Head lenght	0.030	-0.052	-0.10419
Predorsal length	0.029	-0.074	-0.09848
Dorsal-fin lenght	0.021	0.062	0.08714
Body depth	-0.021	0.028	-0.07419
Dorsal-fin base length	0.083	0.023	0.17143
Anal-fin base length	0.150	-0.394	0.45076
Caudal-peduncle depth	0.028	0.022	-0.09493
Head width	0.015	0.026	-0.09189
Nasal-barbel length	-0.340	0.632	-0.14557
Maxillary-barbel length	-0.200	0.223	0.16384
Rictal-barbel length	-0.348	0.191	0.24651
Snout length	0.044	-0.103	-0.31877
Interorbital	-0.084	-0.080	-0.13356
Mouth width	-0.023	-0.126	-0.18196
Eye diameter	-0.004	-0.015	-0.01823
Supraorbital pores s6 distance	0.763	0.494	0.21447

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Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br

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Iterative taxonomy reveals a new species of <i>Cambeva</i> (Siluriformes: Trichomycteridae) with intraspecific variation from the rio Piquiri and Ivaí basin, upper rio Paraná basin, Brazil

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[1] Edited-by

Carlos DoNascimiento