Barcoding Antarctic Fishes: Species Discrimination and Contribution to Elucidate Ontogenetic Changes in Nototheniidae

  • E. MabragañaEmail author
  • S. M. Delpiani
  • J. J. Rosso
  • M. González-Castro
  • M. Deli Antoni
  • R. Hanner
  • J. M. Díaz de Astarloa


Fish species richness in the Southern Ocean accounts for approximately 2 % of the world’s ocean species, with more than 370 species registered and several awaiting for formal description. Here we explore on the use of DNA barcoding to discriminate fishes from Antarctic Peninsula by compiling our results and placing them into a comparative framework with other previous studies to provide a comprehensive review of available barcodes for Antarctic fishes. A total of 275 specimens, belonging to 36 different putative species were barcoded. Nearly all species exhibit unique barcodes or clusters of closely related haplotypes, and only four species lacked genetic resolution using Barcode Index Numbers (BINs). Thus, ~90 % of the species barcoded in this study could be identified at species level with accuracy using BINs. However the use of nucleotic diagnostic character allowed us to discriminate the remaining species. Compiling our results with previous studies, about 80 species inhabiting the Antarctic Peninsula were already barcoded, representing approximately 60 % of the species occurring in the area. Finally, we highlighted ontogenetic morphological traits observed in some Notothenidae, which may lead to misidentification of juveniles. DNA Barcoding was a cornerstone element for obtaining a reliable identification of these specimens. These results are crucial for management and conservation purposes since an accurate species-level resolution of juveniles is necessary to determine nursery areas and to clarify species distributions.


DNA barcodes Fishes Antarctic Peninsula Barcode Index Number Species discrimination Ontogenetic variation 


  1. Acosta J, Canals M, Herranz P, Sanz J (1989) Informe de resultados “Antártida 8611”, investigación geológica-geofísica y sedimentológica en el arco de Escocia y península Antártica. In Resultados de la campaña “Antártida 8611”. Publ Espec Inst Esp Oceanogr 2:9–82Google Scholar
  2. Andriashev AP (1998) A review of recent studies of Southern Ocean Liparidae (Teleostei: Scorpaeniformes). Cybium 22(3):255–266Google Scholar
  3. Andriashev AP, Prirodina VP (1990) Review of the Antarctic species of the genus Careproctus (Liparididae) with notes on the carcinophilic species of the genus. Vopr Ikhtiol 30(5):709–719Google Scholar
  4. Andriashev AP, Stein DL (1998) Review of the Snailfish genus Careproctus (Liparidae, Scorpaeniformes) in Antarctic and adjacent waters. Contrib Sci (Los Ang) 470:1–63Google Scholar
  5. Aronson RB, Moody RM, Ivany LC, Blake DB, Werner JE, Glass A (2009) Climate change and trophic response of the Antarctic bottom fauna. PLoS ONE 4(2):e4385CrossRefPubMedPubMedCentralGoogle Scholar
  6. Balushkin AV (2012) Volodichthys gen. nov. new species of the primitive snailfish (Liparidae: Scorpaeniformes) of the southern hemishpere. Description of new species V. Solovjevae sp. nov. (Cooperation Sea, the Antarctic). J Ichthyol 52(1):1–10Google Scholar
  7. Balushkin AV, Prirodina VP (2010) A new species of Muraenolepididae (Gadiformes) Muraenolepis evseenkoi sp. nova from continental seas of Antarctica. J Ichthyol 50(7):495–502Google Scholar
  8. Barrera-Oro E (2002) The role of fish in the Antarctic marine food web: differences between inshore and offshore waters in the southern Scotia Arc and west Antarctic Peninsula. Antarct Sci 14:293–309CrossRefGoogle Scholar
  9. Becker S, Hanner R, Steinke D (2011) Five years of FISH-BOL: brief status report. Mitochondr DNA 22:3–9CrossRefGoogle Scholar
  10. Broughton RE, Milam JE, Roe BA (2001) The complete sequence of the zebrafish (Danio rerio) mitochondrial genome and evolutionary patterns in vertebrate mitochondrial DNA. Genome Res 11:1958–1967PubMedPubMedCentralGoogle Scholar
  11. Chernova NV (2006) New and rare snailfishes (Liparidae, Scorpaeniformes) with the description of four new species from the Southern Hemisphere and Tropical East Pacific. J Ichthyol 46(1):1–14CrossRefGoogle Scholar
  12. Clarke A, Barnes DKA, Hodgson DA (2005) How isolated is Antarctica? Trends Ecol Evol 20:1–3CrossRefPubMedGoogle Scholar
  13. Collins RA, Boykin LM, Cruickshank RH, Armstrong KF (2012) Barcoding’s next top model: an evaluation of nucleotide substitution models for specimen identification. Methods Ecol Evol 3:457–465CrossRefGoogle Scholar
  14. Constable A, Costa D, Murphy E, Hofmann E, Schofield O, Press A et al (2014) Assessing status and change in Southern Ocean ecosystems. In: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz C et al (eds) Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp 404–407Google Scholar
  15. Cook AJ, Fox AJ, Vaughan DG, Ferrigno JG (2005) Retreating glacier fronts on the Antarctic Peninsula over the past half century. Science 308:541–544Google Scholar
  16. Cook AJ, Vaughan DG (2010) Overview of areal changes of the ice shelves on the Antarctic Peninsula over the past 50 years. Cryosphere 4:77–98Google Scholar
  17. DeSalle R (2006) Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff. Conserv Biol 20:1545–1547CrossRefPubMedGoogle Scholar
  18. Dettai A, Lautredou AC, Bonillo C, Goimbault E, Busson F, Causse R et al (2011) The actinopterygian diversity of the CEAMARC cruises: barcoding and molecular taxonomy as a multi level tool for new findings. Deep Sea Res II 58:250–263CrossRefGoogle Scholar
  19. DeWitt HH, Heemstra PC, Gon O (1990) Nototheniidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 279–331Google Scholar
  20. Donnelly J, Torres JJ (2008) Pelagic fishes in the Marguerite Bay region of the West Antarctic Peninsula shelf. Deep-Sea Res II 55(3–4):523–539CrossRefGoogle Scholar
  21. Donnelly J, Torres JJ, Hopkins TL, Lancraft TM (1990) Proximate composition of Antarctic mesopelagic fishes. Mar Biol 106(1):13–23CrossRefGoogle Scholar
  22. Duhamel G (1992) Description d’espèces Nouvelles de Careproctus et Paraliparis et Donnés Nouvelles sur ces Genres et le Genre Edentoliparis du l’océan Austral (Cyclopteridae, Liparinae). Cybium 16(3):183–207Google Scholar
  23. Duhamel G, Hautecoeur M, Dettai A, Causse R, Pruvost P, Busson F et al (2010) Liparids from the Eastern sector of Southern Ocean and first information from molecular studies. Cybium 34:319–343Google Scholar
  24. Duhamel G, Hulley P-A, Causse R , Koubbi P, Vacchi, M, Pruvost P et al (2014) Biogeographic patterns of fish. In: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz C et al (eds) Biogeographic Atlas of the Southern Ocean, Chap 7. Scientific Committee on Antarctic Research, Cambridge, pp 328–362Google Scholar
  25. Eakin R (1990) Artedidraconidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 332–356Google Scholar
  26. Eakin RR, Eastman JT, Jones CD (2001) Mental barbell variation in Pogonophryne scotti Regan (Pisces: Perciformes: Artedidraconidae). Antarct Sci 13:363–370CrossRefGoogle Scholar
  27. Eakin RR, Eastman JT, Near TJ (2009) A new species and a molecular phylogenetic analysis of the Antarctic fish genus Pogonophryne (Notothenioidei: Artedidraconidae). Copeia 4:705–713Google Scholar
  28. Eastman JT (2005) The nature of the diversity of Antarctic fishes. Polar Biol 28:93–107CrossRefGoogle Scholar
  29. Eschmeyer WN (ed) (2015) Catalog of fishes. California Academy of Sciences. Accessed 03 Jan 2015
  30. Gon O (1990) Bathydraconidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 364–380Google Scholar
  31. Gon O, Heemstra PC (1990) Fishes of the Southern Ocean, 1st edn. JLB Smith Institute of Ichthyology, GrahamstownGoogle Scholar
  32. Gordon AL (1988) Spatial and temporal variability within the Southern Ocean. In: Saharge D (ed) Antarctic Ocean and resources variability. Springer, Berlin, pp 41–56CrossRefGoogle Scholar
  33. Heemstra PC, Duhamel G (1990) Congiopodidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 229–230Google Scholar
  34. Hubert N, Hanner R, Holm E, Mandrak NE, Taylor E, Burridge M et al (2008) Identifying Canadian freshwater fishes through DNA barcodes. PLoS ONE 3:1–8CrossRefGoogle Scholar
  35. Hüne M, González-Wevar C, Poulin E, Mansilla A, Fernández DA, Barrera-Oro E (2014) Low level of genetic divergence between Harpagifer fish species (Perciformes: Notothenioidei) suggests a Quaternary colonization of Patagonia from the Antarctic Peninsula Polar Biol. DOI  10.1007/s00300-014-1623-6
  36. Ivanova NV, de Waard JR, Hebert PDN (2006) An inexpensive, automation friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6:998–1002CrossRefGoogle Scholar
  37. Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN (2007) Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7:544–548CrossRefGoogle Scholar
  38. Iwami T, Kock KH (1990) Channichthyidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 381–389Google Scholar
  39. Jones CD, Anderson ME, Balushkin AV, Duhamel G, Eakin RR, Eastman JT, Kuhn KL, Lecointre G, Near TJ, North AW, Stein DL, Vacchi M, Detrich HW (2008) Diversity, relative abundance, new locality records and population structure of Antarctic demersal fishes from the northern Scotia Arc islands and Bouvetøya. Polar Biol 31:1481–1497Google Scholar
  40. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120Google Scholar
  41. Knebelsberger T, Landi M, Neumann H, Kloppmann M, Sell AF, Campbell PD et al (2014) A reliable DNA barcode reference library for the identification of the North European shelf fish fauna. Mol Ecol Res 14:1060–1071Google Scholar
  42. Kock KH (1992) Antarctic fish and fisheries. Cambridge University Press, CambridgeGoogle Scholar
  43. Kock KH (2005) Antarctic icefishes (Channichthyidae): a unique family of fishes. Rev Part I Polar Biol 28(11):862–895CrossRefGoogle Scholar
  44. Kock KH, Jones CD, Wilhelms S (2000) Biological characteristics of Antarctic fish stocks in the southern Scotia Arc region. CCAMLR Sci 7:1–41Google Scholar
  45. Koubbi P, Moteki M, Duhamel G, Goarant A, Hulley PA, O’Driscoll R, Ishimaru T, Pruvost P, Tavernier E, Hosie G (2011) Ecoregionalization of myctophid fish in the Indian sector of the Southern Ocean: results from generalized dissimilarity models. Deep Sea Res II 58:170–180Google Scholar
  46. La Mesa M, Vacchi M, Iwami T, Eastman JT (2002) Taxonomic studies of the Antarctic icefish genus Cryodraco Dollo, 1900 (Notothenioidei: Channichthyidae). Polar Biol 25:384–390Google Scholar
  47. Lautrédou A-C, Bonillo C, Denis G, Cruaud C, Ozouf-Costaz C, Lecointre G, Dettai A (2010) Molecular taxonomy and identification within the Antarctic genus Trematomus (Notothenioidei, Teleostei): how valuable is barcoding with COI? Polar Sci 4:333–352Google Scholar
  48. Lecointre G, Gallut C, Bonillo C, Couloux A, Ozouf-Costaz C, Dettai A (2011) The Antarctic Fish Genus Artedidraco is paraphyletic (Teleostei, Notothenioidei, Artedidraconidae). Polar Biol 34:1135–1145Google Scholar
  49. Mabragaña E, de Astarloa JMD, Hanner R, Zhang J, González Castro M (2011) DNA barcoding identifies Argentine fishes from marine and brackish waters. PLoS ONE 6:e28655Google Scholar
  50. Matallanas J (1999) New and rare snailfish genus Paraliparis from the Weddell Sea with the description of two new species. J Fish Biol 54:1017–1028Google Scholar
  51. Matallanas J (2009) Description of a new genus and species of zoarcid fish, Bellingshausenia olasoi, from the Antarctic Ocean. Polar Biol 32:873–878CrossRefGoogle Scholar
  52. Matallanas J (2010) Description of two new genera, Santelmoa and Bentartia and two new species of Zoarcidae (Teleostei, Perciformes) from the Southern Ocean. Polar Biol 33(5):659–672CrossRefGoogle Scholar
  53. Matallanas J (2011) Description of two new species of Ophthalmolycus (Teleostei: Zoarcidae) from the Southern Ocean and key to species of the genus. J Mar Biol Ass UK 91:561–567CrossRefGoogle Scholar
  54. Matallanas J, Pequeño G (2000) A new snailfish species, Paraliparis orcadensis sp. nov (Pisces: Scorpaeniformes) from the Scotia Sea (Southern Ocean). Polar Biol 23:298–300Google Scholar
  55. Matallanas J, Corbella C, Møller PR (2012) Description of two new species of Santelmoa (Teleostei, Zoarcidae) from the Southern Ocean. Polar Biol 35(9):1395–1405CrossRefGoogle Scholar
  56. Naish T, Powell R, Levy R, Wilson G, Scherer R, Talarico F et al (2009) Obliquity-paced Pliocene West Antarctic ice sheet oscillations. Nature 458:322–328CrossRefPubMedGoogle Scholar
  57. Neyelov AV, Prirodina VP (2006) Description of Harpagifer permitini sp. nova (Harpagiferidae) from the sublittoral zone of South Georgia and redescription of the littoral H. georgianus Nybelin. J Ichthyol 46(1):1–12Google Scholar
  58. Pegg GG, Sinclair B, Briskey L, Aspden WJ (2006) MtDNA barcode identification of fish larvae in the southern Great Barrier Reef. Australia Sci Mar 70:7–12CrossRefGoogle Scholar
  59. Piacentino GLM, Barrera-Oro E (2009) Phenotypic plasticity in the Antarctic fish Trematomus newnesi (Nototheniidae) from the South Shetland Islands. Polar Biol 32:1407–1413CrossRefGoogle Scholar
  60. Ratnasingham S, Hebert PDN (2007) BOLD: the Barcode of Life Data System. Mole Ecol Notes 7:355–364.
  61. Ratnasingham S, Hebert PDN (2013) DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8(8):e66213CrossRefPubMedPubMedCentralGoogle Scholar
  62. Rey O, Bonillo C, Gallut C, Cruaud C, Dettaï A, Ozouf-Costaz C, Lecointre G (2011) Naked dragonfishes Gymnodraco acuticeps and G. victori (Bathydraconidae, Notothenioidei) off Terre Adélie are a single species. Cybium 35(2):111–119Google Scholar
  63. Rock J, Costa FO, Walker DI, North AW, Hutchinson WF, Carvalho GR (2008) DNA barcodes of fish of the Scotia Sea, Antarctica indicate priority groups for taxonomic and systematics focus. Antarct Sci 20:253–262CrossRefGoogle Scholar
  64. Rosso JJ, Mabragaña E, Gonzalez Castro M, de Astarloa JMD (2012) DNA barcoding Neotropical fishes: recent advances from the Pampa Plain. Argentina Mol Ecol Resour 12:999–1011CrossRefPubMedGoogle Scholar
  65. Smith PJ, Steinke D, McVeagh SM, Stewart AL, Struthers CD, Roberts CD (2008) Molecular analysis of Southern Ocean skates (Bathyraja) reveals a new species of Antarctic skate. J Fish Biol 73:1170–1182CrossRefGoogle Scholar
  66. Smith PJ, Steinke D, McMillan PJ, Stewart AL, McVeagh SM, Diaz de Astarloa JM, Welsford D, Ward RD (2011) DNA barcoding highlights a cryptic species of grenadier (genus Macrourus) in the Southern Ocean. J Fish Biol 78:355–365Google Scholar
  67. Smith PJ, Steinke D, Dettai A, McMillan P, Welsford D, Stewart A, Ward RD (2012) DNA barcodes and species identifications in Ross Sea and Southern Ocean Fishes. Pol Biol 35(9):1297–1310Google Scholar
  68. Steig EJ, Schneider DP, Rutherford SD, Mann ME, Comiso JC, Shindell DT (2009) Warming of the Antarctic ice-sheet surface since the 1957 international geophysical year. Nature 457:459–462CrossRefPubMedGoogle Scholar
  69. Stein DL (2012) Snailfishes (family Liparidae) of the Ross Sea, Antarctica, and closely adjacent waters. Zootaxa 3285:1–120Google Scholar
  70. Steinke D, Hanner R (2010) The FISH-BOL collaborators’ protocol. Mitochon DNA 21:1–5Google Scholar
  71. Steinke D, Zemlak TS, Boutillier JA, Hebert PDN (2009) DNA barcoding of Pacific Canada’s fishes. Mar Biol 156:2641–2647CrossRefGoogle Scholar
  72. 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 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  73. Thatje S (2005) The future fate of the Antarctic marine biota? Trends Ecol Evol 20:418–419CrossRefPubMedGoogle Scholar
  74. Turner J, Bindschadler R, Convey P, Di Prisco G, Fahrbach E, Gutt L, Hodgson D, Mayewski P, Summerhayes C (2009) Antarctic climate change and the environment. Scientific Committee on Antarctic Research, CambridgeGoogle Scholar
  75. Valdez-Moreno M, Ivanova NV, Elías-Gutiérrez M, Contreras-Balderas S, Hebert PDN (2009) Probing diversity in freshwater fishes from Mexico and Guatemala with DNA barcodes. J Fish Biol 74:377–402CrossRefPubMedGoogle Scholar
  76. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos T R Soc B 360:1847–1857Google Scholar
  77. Ward RD, Holmes BH (2007) An analysis of nucleotide and amino acid variability in the barcode region of cytochrome c oxidase I (cox1) in fishes. Mol Ecol Notes 7:899–907CrossRefGoogle Scholar
  78. Ward RD, Holmes BH, White WT, Last PR (2008) DNA barcoding Australasian chondrichthyans: results and potential uses in conservation. Mar Freshw Res 59:57–71CrossRefGoogle Scholar
  79. Ward RD, Hanner R, Hebert PDN (2009) The campaign to DNA barcode all fishes, FISH-BOL. J Fish Biol 74:329–356CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • E. Mabragaña
    • 1
    Email author
  • S. M. Delpiani
    • 1
  • J. J. Rosso
    • 1
  • M. González-Castro
    • 1
  • M. Deli Antoni
    • 1
  • R. Hanner
    • 2
  • J. M. Díaz de Astarloa
    • 1
  1. 1.Laboratorio de Biotaxonomía Morfológica y Molecular de Peces, Instituto de Investigaciones Marinas y Costeras, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Universidad Nacional de Mar del PlataMar del PlataArgentina
  2. 2.Biodiversity Institute of Ontario, Department of Integrative BiologyUniversity of GuelphGuelphCanada

Personalised recommendations