Skip to main content

Advertisement

SpringerLink
Log in

Integrative taxonomy supports new candidate fish species in a poorly studied neotropical region: the Jequitinhonha River Basin

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Molecular identification through DNA barcoding has been proposed as a way to standardize a global biodiversity identification system using a partial sequence of the mitochondrial COI gene. We applied an integrative approach using DNA barcoding and traditional morphology-based bioassessment to identify fish from a neotropical region possessing low taxonomic knowledge: the Jequitinhonha River Basin (Southeastern Brazil). The Jequitinhonha River Basin (JRB) has a high rate of endemism and is considered an area of high priority for fish conservation, with estimates indicating the presence of around 110 native and non-indigenous species. DNA barcodes were obtained from 260 individuals belonging to 52 species distributed among 35 genera, 21 families and 6 orders, including threatened and rare species such as Rhamdia jequitinhonha and Steindachneridion amblyurum. The mean Kimura two-parameter genetic distances within species, genera and families were: 0.44, 12.16 and 20.58 %, respectively. Mean intraspecific genetic variation ranged from 0 to 11.43 %, and high values (>2 %) were recovered for five species. Species with a deep intraspecific distance, possibly flagging overlooked taxa, were detected within the genus Pimelodella. Fifteen species, only identified to the genus level, had unique BINs, with a nearest neighbor distance over 2 % and therefore, potential new candidate species supported by DNA barcoding. The integrative taxonomy approach using DNA barcoding and traditional taxonomy may be a remedy to taxonomy impediment, accelerating species identification by flagging potential new candidate species and to adequately conserve the megadiverse neotropical ichthyofauna.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abell R, Thieme ML, Revenga C, Bryer M, Kottelat M, Bogutskaya N, Coad B, Mandrak N, Balderas SC, Bussing W, Stiassny MLJ, Skelton P, Allen GR, Unmack P, Naseka A, Ng R, Sindorf N, Robertson J, Armijo E, Higgins JV, Heibel TJ, Wikramanayake E, Olson D, Lopez HL, Reis RE, Lundberg JG, Perez MHS, Petry P (2008) Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58:403–414

    Article  Google Scholar 

  • Albert JS, Reis RE (eds) (2011) Historical biogeography of Neotropical freshwater fishes. University of California Press, Berkeley

    Google Scholar 

  • Albert JS, Fernandes-Matioli FMC, Almeida-Toledo LF (1999) New species of Gymnotus (Gymnotiformes, Teleostei) from southeastern Brazil: toward the deconstruction of Gymnotus carapo. Copeia 2:410–421

    Article  Google Scholar 

  • Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asgharian H, Sahafi HH, Ardalan AA, Shekarriz S, Elahi E (2011) Cytochrome c oxidase subunit 1 Barcode data of fish of the nayband national park in the persian gulf and analysis using meta-data flag several cryptic species. Mol Ecol Resour 11:461–472

    Article  PubMed  Google Scholar 

  • Baldwin CC, Castillo CI, Weigt LA, Victor BC (2011) Seven new species within western Atlantic Starksia atlantica, S. lepicoelia, and S. sluiteri (Teleostei, Labrisomidae), with comments on congruence of DNA Barcodes and species. ZooKeys 79:21–72

    Article  PubMed  Google Scholar 

  • Becker RA, Sales NG, Santos GM, Santos GB, Carvalho DC (2015) DNA barcoding and morphological identification of neotropical ichthyoplankton from the Upper Paraná and São Francisco. J Fish Biol 87(1):159–168

    Article  CAS  PubMed  Google Scholar 

  • Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2006) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155

    Article  PubMed  Google Scholar 

  • Bizerril CRSF, Lima NRW (2005) Ictiofauna do curso inferior do Rio Jequitinhonha (BA/MG) Brasil. Acta Biol. Leopondensia 27:169–173

    Google Scholar 

  • Britski HA, Birindelli JLO (1837) Garavello JC (2012) A new species of Leporinus Agassiz, 1829 from the upper Rio Paraná basin (Characiformes, Anostomidae) with redescription of L. elongatus Valenciennes, 1850 and L. obtusidens (Valenciennes. Papéis Avulsos de Zoologia 52(37):441–475

    Google Scholar 

  • Britski HA, Sato Y, Rosa ABS (1988) Manual de identificação de peixes da região de Três Marias, 3º edn. CODEVASF, Brasília

    Google Scholar 

  • Brower AVZ (2006) Problems with DNA barcodes for species delimitation: ‘ten species’ of Astraptes fulgerator reassessed (Lepidoptera: Hesperiidae). Syst Biodivers 4:127–132

    Article  Google Scholar 

  • Bucklin A, Wiebe PH, Smolenack SB, Copley NJ, Beaudet JG, Bonner KG, Farber-Lorda J, Pierson JJ (2007) DNA Barcodes for species identification of euphausiids (Euphausiacea, Crustacea). J Plankton Res 29:483–493

    Article  CAS  Google Scholar 

  • Camelier P, Zanata AM (2014) Biogeography of freshwater fishes from the Northeastern Mata Atlântica freshwater ecoregion: distribution, endemism, and area relationships. Neotrop Ichthyol 12:683–698

    Article  Google Scholar 

  • Carvalho DC, Oliveira DAA, Pompeu PS, Leal CG, Oliveira C, Hanner R (2011) Deep Barcode divergence in Brazilian freshwater fishes: the case of the São Francisco River Basin. Mitochondrial DNA 22:1–7

    Google Scholar 

  • Carvalho DC, Palhares RM, Drummond MG, Frigo TB (2015) DNA Barcoding identification of commercialized seafood in South Brazil: a governmental regulatory forensic program. Food Control 50:784–788

    Article  CAS  Google Scholar 

  • Castro RMC, Vari RP (2004) Detritivores of the South American fish family Prochilodontidae (Teleostei: Ostariophysi: Characiformes): a phylogenetic and revisionary study. Smithsonian Contrib Zool 622

  • Collins RA, Cruickshank RH (2013) The seven deadly sins of DNA Barcoding. Mol Ecol Resour 13:969–975

    CAS  PubMed  Google Scholar 

  • Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415

    Article  Google Scholar 

  • Eigenmann CH (1917) The American Characidae. Memoirs of the Museum of Comparative Zoölogy. Harvard College. Cambridge. 43. Part 1

  • Eigenmann CH (1918) The American Characidae. Memoirs of the Museum of Comparative Zoölogy. Harvard College. Cambridge. 43. Part 2

  • Eigenmann CH (1921) The American Characidae. Memoirs of the Museum of Comparative Zoölogy. Harvard College. Cambridge. 43. Part 3

  • Eschmeyer WN (2016) Catalog of Fishes: World Wide Web electronic publication. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed 18 January 2016

  • Garavello JC (2005) Revision of genus Steindachneridion (Siluriformes: Pimelodidae). Neotrop Ichthyol 3(4):607–623

    Article  Google Scholar 

  • Géry J (1977) Characoids of the world. Tropical Fish Hobbyist Publications, Neptune, p 672

    Google Scholar 

  • Gomes LC, Pessali TC, Sales NG, Pompeu PS, Carvalho DC (2015) Integrative taxonomy detects cryptic and overlooked fish species in a neotropical river basin. Genetica 143(5):581–588

    Article  PubMed  Google Scholar 

  • Handfield D, Handfield L (2006) A new species of Plusia (Lepidoptera: Noctuidae) from North America. Can Entomol 138:853–859

    Article  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA Barcodes. Proc R Soc Lond B 270:313–321

    Article  CAS  Google Scholar 

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA Barcoding reveals cryptic species in the neotropical skipper butterfly Astrapes fulgerator. Proc Natl Acad Sci USA 101:14812–14817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubert N, Hanner R, Holm E, Mandrak NE, Taylor E, Burridge M, Watkinson D, Dumont P, Curry A, Bentzen P, Zhang JB, April J, Bernatchez L (2008) Identifying Canadian freshwater fishes through DNA Barcodes. PLoS ONE 3:2490

    Article  Google Scholar 

  • Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN (2007) Universal primer cocktails for fish DNABarcoding. Mol Ecol Notes 7:544–548

    Article  CAS  Google Scholar 

  • Keskin E, Atar H (2013) DNA Barcoding commercially important fish species of Turkey. Mol Ecol Resour 13:788–797

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kullander SO, Ferreira EJG (2006) A review of the South American cichlid genus Cichla, with descriptions of nine new species (Teleostei: Cichlidae). Ichthyol Explor Freshw 17(4):289–398

    Google Scholar 

  • Lara A, Ponce de León JL, Rodríguez R, Casane D, Côté G, Bernatchez L, García-Machado E (2010) DNA Barcoding of Cuban freshwater fishes: evidence for cryptic species and taxonomic conflicts. Mol Ecol Resour 10:421–430

    Article  CAS  PubMed  Google Scholar 

  • Mabragaña E, Astarloa JMD, Hanner R, Zhang J, Castro MG (2011) DNA Barcoding identifies argentine fishes from marine and brackish waters. PLoS ONE 6:1–11

    Article  Google Scholar 

  • Machado ABM, Drummond GM, Paglia AP (2008) Livro vermelho da fauna brasileira ameaçada de extinção. Belo Horizonte, Fundação Biodiversitas

    Google Scholar 

  • Martins FO, Rosa AC, Langeani F (2014) Microlepidogaster discus, a new species of Hypoptopomatinae (Siluriformes: Loricariidae) from the rio Jequitinhonha basin, southeastern Brazil. Zootaxa 3873(5):560–570

    Article  PubMed  Google Scholar 

  • Mejía O, Léon-Romero Y, Soto-Galera E (2012) DNA Barcoding of the ichthyofauna of Pánuco-Tamesí complex: evidence for taxonomic conflicts in some groups. Mitochondrial DNA 23:471–476

    Article  PubMed  Google Scholar 

  • Melo BF, Benine RC, Mariguela TC, Oliveira C (2011) A new species of Tetragonopterus Cuvier, 1816 (Characiformes: Characidae: Tetragonopterinae) from the rio Jari, Amapá, northern Brazil. Neotrop Ichthyol 9:49–56

    Article  Google Scholar 

  • Menezes NA, Géry J (1983) Seven new Acestrorhynchin Characid species (Osteichthyes, Ostariophysi, Characiformes) with comments on the systematics of the group. Revue suisse Zool 90(3):563–592

    Google Scholar 

  • Monaghan MT, Wild R, Elliot M, Fujisawa T, Balke M, Inward DJG, Lees DC, Ranaivosolo R, Eggleton P, Barraclough TG, Vogler AP (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Syst Biol 58:298–311

    Article  CAS  PubMed  Google Scholar 

  • Nwani CD, Becker S, Braid HE, Ude EF, Okogwu OI, Hanner R (2011) DNA Barcoding discriminates freshwater fishes from southeastern Nigeria and provides river system-level phylogeographic resolution within some species. Mitochondrial DNA 22:43–51

    Article  CAS  PubMed  Google Scholar 

  • Oliveira JC, Oyakawa OT (1999) Two new species of Hemipsilichthys (Teleostei: Loricariidae) from Serra do Espinhaço, Minas Gerais. Brazil Ichthyol Explor Freshw 10(1):73–80

    Google Scholar 

  • Oyakawa OT (1993) Cinco espécies novas de Harttia Steindachner, 1876 da região sudeste do Brasil, e comentários sobre o gênero (Teleostei, Siluriformes, Loricariidae). Comunn Mus Ciênc PUCRS, sér. zool 6:3–27

    Google Scholar 

  • Oyakawa OT, Mattox GMT (2009) Revision of the neotropical trahiras of the Hoplias lacerdae species-group (Ostariophysi: Characiformes: Erythrinidae) with descriptions of two new species. Neotrop Ichthyol 7(2):117–140

    Article  Google Scholar 

  • Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira EHL, Reis RE (2002) Revision of the loricariid genera Hemipsilichthys and Isbrueckerichthys (Teleostei: Siluriformes), with descriptions of five new species of Hemipsilichthys. Ichthyol Explor Freshw 13(2):97–146

    Google Scholar 

  • Pereira LHG, Maia GMG, Hanner R, Foresti F, Oliveira C (2011) DNA Barcodes discriminate fresh water fishes from the Paraíba do Sul River Basin, São Paulo, Brazil. Mitochondrial DNA 22:71–79

    Article  CAS  PubMed  Google Scholar 

  • Pereira LHG, Hanner R, Foresti F, Oliveira C (2013) Can DNA Barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genet 14:1–14

    Article  Google Scholar 

  • Prosdocimi F, Carvalho DC, Almeida R, Beheregaray L (2012) The complete mitochondrial genome of two recently derived species of the fish genus Nannoperca (Perciformes, Percichthyidae). Mol Biol Rep 39:2767–2772

    Article  CAS  PubMed  Google Scholar 

  • Ratnasingham S, Hebert PDN (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) System. PLoS ONE 8:1–16

    Article  Google Scholar 

  • Reis RE, Pereira EHL, Armbruster JW (2006) Delturinae, a new loricariid catfish subfamily (Teleostei, Siluriformes), with revisions of Delturus and Hemipsilichthys. Zool J Linnean Soc 147:277–299

    Article  Google Scholar 

  • Ribeiro AO, Caires RA, Mariguela TC, Pereira LHG, Hanner R, Oliveira C (2012) DNA Barcodes identify marine fishes of São Paulo State, Brazil. Mol Ecol Resour 12:1012–1020

    Article  CAS  PubMed  Google Scholar 

  • Riedel A, Sagata K, Suhardjono YR, Tänzler R, Balke M (2013) Integrative taxonomy on the fast track-towards more sustainability in biodiversity research. Front Zool 10:15

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosa RS, Lima FCT (2008) Os peixes ameaçados de extinção. In: Machado ABM, Drummond GM, Paglia AP (eds) Livro vermelho da fauna brasileira ameaçada de extinção. Ministério do Meio Ambiente/Fundação Biodiversitas, Brasília, pp 9–285

    Google Scholar 

  • Rosso JJ, Magragaña E, Gonzalez Castro M, Diaz de Astarloa M (2012) DNA Barcoding Neotropical fishes: recent advances from the Pampa Plain, Argentina. Mol Ecol Resour 12:999–1011

    Article  CAS  PubMed  Google Scholar 

  • Saadi A (1995) A geomorfologia da Serra do Espinhaço em Minas Gerais e de suas margens. Geonomos 3:41–63

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The Neighbor-Joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Silva GSC, Melo BF, Oliveira C, Benine RC (2013) Morphological and molecular evidence for two new species of Tetragonopterus (Characiformes: Characidae) from central Brazil. J Fish Biol 82:1613–1631

    Article  CAS  PubMed  Google Scholar 

  • Silvergripp AMC (1996) A systematic revision of the neotropical catfish genus Rhamdia (Teleostei, Pimelodidae). Department of Zoology, Swedish Museum of Natural History. Stockholm: 1–156

  • Smith MA, Woodley NE, Janzen DH, Hallwachs W, Hebert PDN (2006) DNA Barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proc Natl Acad Sci USA 103:3657–3662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Triques ML, Vono V (2004) Three new species of Trichomycterus (Teleostei: Siluriformes: Trichomycteridae) from the Rio Jequitinhonha basin, Minas Gerais, Brazil. Ichthyol Explor Freshw 15(2):81–92

    Google Scholar 

  • Ward RD (2009) DNA Barcode divergence among species and genera of birds and fishes. Mol Ecol Resour 9:1077–1085

    Article  CAS  PubMed  Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA Barcoding Australia’s fish species. Philos Trans R Soc B 360:1847–1857

    Article  CAS  Google Scholar 

  • Weigt LA, Baldwin CC, Driskell A, Smith DG, Ormos A (2012) Using DNA Barcoding to assess caribbean reef fish biodiversity: expanding taxonomic and geographic coverage. PLoS ONE 7:1–7

    Article  Google Scholar 

  • Zhang J, Hanner R (2011) DNA Barcoding is a useful tool for the identification of marine fishes from Japan. Biochem Syst Ecol 39:31–42

    Article  Google Scholar 

  • Zhang J, Hanner R (2012) Molecular approach to the identification of fish in the South China Sea. PLoS ONE 7:1–9

    CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Naiara G. Sales, Tobias A. Barroso, Iago S. Penido, Guilherme M. Santos, Gilberto N. Salvador and Amarildo A. Rodrigues for help in the fieldwork. Luisa M. Sarmento-Soares and Ronaldo F. M. Pinheiro for sharing data from Professor Mello Leitão Museum. DCC is grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for his productivity fellowship (308537/2014-9). This work was funded by the Brazilian Barcode of Life Network BrBol/CNPq (564953/2010-5), Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior (CAPES—PRÓ EQUIPAMENTOS grant number 783380/2013), Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (process numbers INCT 573899/2008-8 and 482852/2011-9) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais—FAPEMIG (process number INCT APQ-0084/08).

Author information

Authors and Affiliations

  1. Programa de Pós-graduação em Zoologia de Vertebrados, Laboratório de Genética da Conservação, PUC Minas, Rua Dom José Gaspar, 500, 30535-901, Belo Horizonte, Minas Gerais, Brazil

    Marina Lages Pugedo & Daniel Cardoso Carvalho

  2. Laboratório de Ictiologia, Museu de Ciências Naturais, PUC Minas, Belo Horizonte, Minas Gerais, Brazil

    Tiago Casarim Pessali

  3. Projeto Jequictio, Belo Horizonte, Minas Gerais, Brazil

    Francisco Ricardo de Andrade Neto

  4. Departamento de Biologia Animal e Vegetal, UEL, Londrina, Paraná, Brazil

    José Luís Olivan Birindelli

Authors
  1. Marina Lages Pugedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Francisco Ricardo de Andrade Neto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tiago Casarim Pessali
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José Luís Olivan Birindelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Daniel Cardoso Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel Cardoso Carvalho.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 106 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pugedo, M.L., de Andrade Neto, F.R., Pessali, T.C. et al. Integrative taxonomy supports new candidate fish species in a poorly studied neotropical region: the Jequitinhonha River Basin. Genetica 144, 341–349 (2016). https://doi.org/10.1007/s10709-016-9903-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-016-9903-4

Keywords

Search

Navigation