Skip to main content

Advertisement

SpringerLink
Log in

Integrative taxonomy detects cryptic and overlooked fish species in a neotropical river basin

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The great freshwater fish diversity found in the neotropical region makes management and conservation actions challenging. Due to shortage of taxonomists and insufficient infrastructure to deal with such great biodiversity (i.e. taxonomic impediment), proposed remedies to accelerate species identification and descriptions include techniques that combine DNA-based identification and concise morphological description. The building of a DNA barcode reference database correlating meristic and genetic data was developed for 75 % of the Mucuri River basin’s freshwater fish. We obtained a total of 141 DNA barcode sequences from 37 species belonging to 30 genera, 19 families, and 5 orders. Genetic distances within species, genera, and families were 0.74, 9.5, and 18.86 %, respectively. All species could be clearly identified by the DNA barcodes. Divergences between meristic morphological characteristics and DNA barcodes revealed two cryptic species among the Cyphocharax gilbert and Astyanax gr. bimaculatus specimens, and helped to identify two overlooked species within the Gymnotus and Astyanax taxa. Therefore, using a simplified model of neotropical biodiversity, we tested the efficiency of an integrative taxonomy approach for species discovery, identification of cryptic diversity, and accelerating biodiversity descriptions.

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
Fig. 2

Similar content being viewed by others

References

  • Agostinho AA, Thomaz SM, Gomes LC (2005) Conservação da biodiversidade em águas continentais do Brasil. Megadiversidade 1:70–78

    Google Scholar 

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

    Book  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 1999:410–421

    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  PubMed Central  CAS  PubMed  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. Mitochondr DNA 22:80–86

    Article  Google Scholar 

  • Castro RM, Vari RP (2004) Detritivores of the South American fish family Prochilodontidae (Teleostei: Ostariophysi: Characiformes): a phylogenetic and revisionary study. Smithsonian Contributions to Zoology, Washington

    Google Scholar 

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

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eigenmann CH (1921) The American characidae. Mem Mus Comp Zool 43:208–310

    Google Scholar 

  • Eschmeyer WN (2015) Catalog of fishes: world wide web electronic publication. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed 30 March 2015

  • Froese R, Paulay D (2010) FishBase: World Wide Web electronic publication. http://fishbase.org. Accessed 10 Dec 2014

  • Garutti V (1995) Revisão taxonômica dos Astyanax (Pisces, Characidae), com mancha umeral ovalada e mancha no pedúnculo caudal, estendendo-se à extremidade dos raios caudais medianos, das bacias do Paraná, São Francisco e Amazônica. Thesis, Universidade Estadual Paulista

  • Garutti V (1998) Descrição de uma espécie nova de Astyanax (Teleostei, Characidae) da bacia do Tocantins, Brasil. Iheringia, Sér Zool 85:115–122

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004a) 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004b) Identification of birds through DNA Barcodes. PLoS Biol 2:e312. doi:10.1371/journal.pbio.0020312

    Article  PubMed Central  PubMed  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:e2490. doi:10.1371/journal.pone.0002490

    Article  PubMed Central  PubMed  Google Scholar 

  • IGAM—Instituto Mineiro de Gestão das Águas. Bacias hidrográficas do Leste (2008) Bacia Hidrográfica do Rio Mucuri (MU1). www.igam.mg.gov.br/component/content/158?task=view. Accessed 2 August 2014

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York

    Google Scholar 

  • Kekkonen M, Hebert PDN (2014) DNA barcode-based delineation of putative species: efficient start for taxonomic workflows. Mol Ecol Resour 14:706–715

    Article  PubMed Central  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 

  • Marinho MM, Lima FC (2009) Astyanax ajuricaba: a new species from the Amazon basin in Brazil (Characiformes: Characidae). Neotrop Ichthyol 7:169–174

    Article  Google Scholar 

  • MMA—Ministério do Meio Ambiente (2006) Atlântico Leste In Caderno da região hidrográfica Atlântico Leste. Ministério do Meio Ambiente, Secretaria de Recursos Hídricos, Brasília

    Google Scholar 

  • Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B (2011) How many species are there on earth and in the ocean? PLoS Biol 9:e1001127. doi:10.1371/journal.pbio.1001127

    Article  PubMed Central  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. Mitochondr DNA 22:43–51

    Article  CAS  Google Scholar 

  • Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy . Front Zool 7(1):16. doi:10.1186/1742-9994-7-16

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pereira LHG, Hanner R, Foresti F, Oliveira C (2013) Can DNA Barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genet 14:14–20

    Article  Google Scholar 

  • Pompeu PS (2010) Os peixes do rio Mucuri. MG BIOTA 2:36–48

    Google Scholar 

  • Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol Ecol 21:1864–1877

    Article  CAS  PubMed  Google Scholar 

  • Ratnasingham S, Hebert PDN (2007) BOLD: the barcode of life data system (www.barcodinglife.org). Mol Ecol Notes 3:355–364

    Article  Google Scholar 

  • Ratnasingham S, Hebert PDN (2013) A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS One. doi:10.1371/journal.pone.0066213

    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. doi:10.1186/1742-9994-10-15

    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 

  • Taylor RW (1983) Descriptive taxonomy: past, present, and future. In: Highley E, Taylor RW (eds) Australian Systematic entomology: a bicentenary perspective. CSIRO, Melbourne

    Google Scholar 

  • Vari R (1992) Systematics of the neotropical characiform genus Cyphocharax Fowler (Pisces: Ostariophysi). Smithson Contrib Zool 529:1–137

    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 

  • Waugh J (2007) DNA barcoding in animal species: progress, potential and pitfalls. BioEssays 29:188–197

    Article  CAS  PubMed  Google Scholar 

  • Zanata AM, Camelier P (2009) Astyanax vermilion and Astyanax burgerai: new characid fishes (Ostariophysi: Characiformes) from Northeastern Bahia, Brazil. Neotrop Ichthyol 7:175–184

    Article  Google Scholar 

Download references

Acknowledgments

We thank Angelo Monteiro, Danilo Neto, Iago Penido and Ivo for helping with the fieldwork and laboratory analysis. 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, Pontifícia Universidade Católica de Minas Gerais, Rua Dom José Gaspar, 500,Coração Eucarístico, Belo Horizonte, MG, 30535-901, Brazil

    Laís Carvalho Gomes, Naiara Guimarães Sales & Daniel Cardoso Carvalho

  2. Museu de Ciências Naturais, Laboratório de Ictiologia, Pontifícia Universidade Católica de Minas Gerais, Rua Dom José Gaspar, 290,Coração Eucarístico, Belo Horizonte, MG, 30535-610, Brazil

    Tiago Casarim Pessali

  3. Laboratório de Ecologia de peixes, Departamento de Biologia, Universidade Federal de Lavras, Avenida Doutor Sylvio Menicucci, 1001, Kennedy, Lavras, MG, 37200-000, Brazil

    Paulo Santos Pompeu

Authors
  1. Laís Carvalho Gomes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tiago Casarim Pessali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naiara Guimarães Sales
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paulo Santos Pompeu
    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 (DOCX 142 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gomes, L.C., Pessali, T.C., Sales, N.G. et al. Integrative taxonomy detects cryptic and overlooked fish species in a neotropical river basin. Genetica 143, 581–588 (2015). https://doi.org/10.1007/s10709-015-9856-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-015-9856-z

Keywords

Search

Navigation