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Misidentification of bluefin tuna larvae: a call for caution and taxonomic reform

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Abstract

The international effort to prevent the collapse of Atlantic bluefin tuna (BFT, Thunnus thynnus, Scombridae) stocks exemplifies the challenges associated with modern marine resource conservation. Rampant mismanagement, under-reporting and illegal, unreported and unregulated fishing led to decades of over-exploitation in the BFT fishery. Surveys of larval abundance in the Gulf of Mexico and the Mediterranean Sea have been used as a proxy for both spawning biomass and recruitment by researchers working to improve estimates of stock abundance. Recent genetic barcoding studies have revealed that species identification errors are common among larvae surveys that use morphology-based taxonomy alone. Misidentification of larvae can lead to uncertainty about the spatial distribution of a species, confusion over life history traits and population dynamics, and potentially disguise the collapse or recovery of localized spawning sites. In an effort to identify the source of these errors, we review several weaknesses in modern morphology-based taxonomy including demographic decline of expert taxonomists, flawed identification keys, reluctance of the taxonomic community to embrace advances in digital communications and a general scarcity of modern user-friendly materials. Recent advances in molecular techniques useful for specimen identification and population studies are discussed at length. We advocate a more constructive integration of morphology-based taxonomy and barcoding in order to add confidence to larval surveys and to strengthen associated fisheries management.

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References

  • Aguilar R, Lastra P, Madina M et al (2009) Bluefin tuna larval survey: 2008 Oceana-MarViva Mediterranean Project, pp 76

  • Akyuz EF, Artuz G (1957) Some observations on the biology of tuna (Thunnus thynnus) caught in Turkish waters. Proc Tech Pap Gen Fish Counc Mediterr Rome 4(14):93–99

    Google Scholar 

  • Albaina A, Iriondo M, Velado I et al (2013) Single nucleotide polymorphism discovery in albacore and Atlantic bluefin tuna provides insights into worldwide population structure. Anim Genet 44(6):678–692

    CAS  PubMed  Google Scholar 

  • Alemany F (1997) Ictioplancton del Mar Balear. PhD Thesis, University of Illes Balears, Palma de Mallorca, Spain

  • Alemany F (2008) Relevance of the Balearic Sea for the spawning of the bluefin tuna in the Mediterranean Sea. Spatial management to support recovery of the Atlantic bluefin tuna in the Mediterranean The case for implementing a bluefin tuna sanctuary (or permanent fishing closure) in the Balearic Sea. WWF, Rome, pp 6–38

    Google Scholar 

  • Alemany F, Deudero S, Morales-Nin B et al (2006) Influence of physical environmental factors on the composition and horizontal distribution of summer larval fish assemblages off Mallorca island (Balearic archipelago, western Mediterranean). J Plankton Res 28:473–487

    Google Scholar 

  • Alemany F, Quintanilla L, Velez-Belchi P et al (2010) Characterization of the spawning habitat of Atlantic bluefin tuna and related species in the Balearic Sea (western Mediterranean). Prog Oceanogr 86:21–38

    Google Scholar 

  • Alvarado Bremer JR, Naseri I, Ely B (1997) Orthodox and unorthodox phylogenetic relationships among tunas revealed by the nucleotide sequence analysis of the mitochondrial DNA control region. J Fish Biol 50(3):540–554

    Google Scholar 

  • Alvarado Bremer JR, Viñas J, Mejuto J, Ely B, Pla C (2005) Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Mol Phylogenet Evol 36:169–187

    CAS  PubMed  Google Scholar 

  • Amish SJ, Hohenlohe PA, Painter S, Leary RF, Muhlfeld C, Allendorf FW, Luikart G (2012) RAD sequencing yields a high success rate for westslope cutthroat and rainbow trout species-diagnostic SNP assays. Mol Ecol Resour 12(4):653–660

    CAS  PubMed  Google Scholar 

  • Aranda G, Abascal FJ, Varela JL, Medina A (2013) Spawning behaviour and post-spawning migration patterns of Atlantic bluefin tuna (Thunnus thynnus) ascertained from satellite archival tags. PLoS ONE 8(10):e76445

    CAS  PubMed Central  PubMed  Google Scholar 

  • Armstrong MJ, Connolly P, Nash RDM et al (2001) An application of the annual egg production method to estimate the spawning biomass of cod (Gadus morhua L.), plaice (Pleuronectes platessa L.) and sole (Solea solea L.) in the Irish Sea. ICES J Mar Sci 58(1):183–203

    Google Scholar 

  • Baglin RE (1976) A preliminary study of the gonadal development and fecundity of the western Atlantic bluefin tuna. ICCAT Col Vol Sci Pap 5:279–289

    Google Scholar 

  • Baldwin CC, Brito BJ, Smith DG, Weigt LA, Escobar-Briones E (2011) Identification of early life-history stages of Caribbean Apogon (Perciformes: Apogonidae) through DNA barcoding. Zootaxa 3133:1–36

    Google Scholar 

  • Boero F (2001) Light after dark: the partnership for enhancing expertise in taxonomy. Trends Ecol Evol 16:266

    PubMed  Google Scholar 

  • Boley RM, Heist EJ (2011) Larval surveys indicate low levels of endangered pallid sturgeon reproduction in the middle Mississippi River. Trans Am Fish Soc 140(6):1604–1612

    Google Scholar 

  • Catalán IA, Tejedor A, Alemany F, Reglero P (2011) Trophic ecology of Atlantic bluefin tuna Thunnus thynnus larvae. J Fish Biol 78:1545–1560

    PubMed  Google Scholar 

  • Chow S, Kishino H (1995) Phylogenetic relationships between tuna species of the genus Thunnus (Scombridae: Teleostei): inconsistent implications from morphology, nuclear and mitochondrial genomes. J Mol Evol 41(6):741–748

    CAS  PubMed  Google Scholar 

  • Chow S, Nohara K, Tanabe T et al (2003) Genetic and morphological identification of larval and small juvenile tunas (Pisces: Scombridae) caught by a mid-water trawl in the western Pacific. Bull Fish Res Agency Jpn 8:1–14

  • Chow S, Nakagawa T, Suzuki N, Takeyama H, Matsunaga T (2006) Phylogenetic relationships among Thunnus species inferred from rDNA ITS1 sequence. J Fish Biol 68:24–35

    CAS  Google Scholar 

  • Collette BB (1999) Mackerels, molecules, and morphology. In: Séret B, Sire JY (ed) Proceedings of the fifth Indo-Pacific fisheries conference (Proceedings of the Fifth Indo-Pacific Fisheries Conference, Noumea, 03 November–08 November, 1997) Société française d’ichtyologie, pp 149–164

  • Cuveliers EL, Volckaert FAM, Rijnsdorp AD, Larmuseau MHD, Maes GE (2011) Temporal genetic stability and high effective population size despite fisheries-induced life-history trait evolution in the North Sea sole. Mol Ecol 20(17):3555–3568

    CAS  PubMed  Google Scholar 

  • D’Alessandro EK, Sponaugle S, Serafy JE (2010) Larval ecology of a suite of snappers (family: Lutjanidae) in the Straits of Florida, western Atlantic Ocean. Mar Ecol Prog Ser 410:159–175

    Google Scholar 

  • Daniel LB III, Graves JE (1994) Morphometric and genetic identification of eggs of spring-spawning sciaenids in lower Chesapeake Bay. Fish B NOAA 92(2):254–261

    Google Scholar 

  • de la Gandara F, Mylonas CC, Coves D et al (2010) Seedling production of Atlantic bluefin tuna (ABFT) Thunnus thynnus The SELFDOTT project. In: Joint international symposium of Kinki University and Setouchi town on the 40th anniversary of Pacific bluefin tuna aquaculture, towards the sustainable aquaculture of bluefin tuna, October 15–16 2010. Amami, Japan, pp 45–52

  • Dicenta A (1975) Identificación de algunos huevos y larvas de túnidos en el Mediterráneo. Boletín Instituto Español de Oceanografía 198:1–22 (in Spanish)

    Google Scholar 

  • Drywa A, Poćwierz-Kotus A, Dobosz S, Kent MP, Lien S, Wenne R (2014) Identification of multiple diagnostic SNP loci for differentiation of three salmonid species using SNP-arrays. Mar Gen 15:5–6

    Google Scholar 

  • Duclerc J, Sacchi J, Piccinetti C, Piccinetti-Manfrin G, Dicenta A, Barrois J-M (1973) Nouvelles données sur la reproduction du thon rouge (Thunnus thynnus L.) et d´autres espèces de thonidés en Mediterranée. Revue Travaux Pêches maritimes 37(2):163–176 (in French)

    Google Scholar 

  • Durand JD, Diatta MA, Diop K, Trape S (2010) Multiplex 16S rRNA haplotype-specific PCR, a rapid and convenient method for fish species identification: an application to West African Clupeiform larvae. Mol Ecol Resour 10(3):568–572

    CAS  PubMed  Google Scholar 

  • Ehrenbaum E (1924) Scombriformes. In: Report on the Danish oceanographical expeditions 1908–1910 to the mediterranean and adjacent seas, vol 2. A. F. Høst, Copenhagen, pp 1–42

  • Fahay MP (1983) Guide to the early stages of marine fishes occurring in the western North Atlantic Ocean, Cape Hatteras to the southern Scotian Shelf. J Northwest Atl Fish Sci 4:423

    Google Scholar 

  • Fahay MP (2007) Early stages of fishes in the Western North Atlantic Ocean, vol 1, 1st edn. Northwest Atlantic Fisheries Organization, Dartmouth

    Google Scholar 

  • Fox CJ, Taylor MI, Pereyra R, Villasana MI, Rico C (2005) TaqMan DNA technology confirms likely overestimation of cod (Gadus morhua L.) egg abundance in the Irish Sea: implications for the assessment of the cod stock and mapping of spawning areas using egg-based methods. Mol Ecol 14(3):879–884

    CAS  PubMed  Google Scholar 

  • Fritzsche RA (1978) Development of fishes of the mid-Atlantic bight: an atlas of egg, larval and juvenile stages. Volume V Chaetodontidae through Ophidiidae. U.S. Fish Wildl. Serv. Biol. Serv. Prog. FWS/OBS-78/12, 340 pp

  • Froese R, Pauly D (ed) (2015) Fishbase World Wide Web electronic publication www.fishbase.org, version (02/2015)

  • Fromentin JM, Bonhommeau S, Arrizabalaga H, Kell LT (2014) The spectre of uncertainty in management of exploited fish stocks: the illustrative case of Atlantic bluefin tuna. Mar Policy 47:8–14

    Google Scholar 

  • Galuardi B, Royer F, Golet W, Logan J, Neilson J, Lutcavage M (2010) Complex migration routes of Atlantic bluefin tuna (Thunnus thynnus) question current population structure paradigm. Can J Fish Aquat Sci 67:966–976

    Google Scholar 

  • García A, de la Serna Ernst JM, López Jurado J, Alemany F, Rodríguez Marin E (2002) Bluefin tuna egg and larval survey in the Balearic Sea, June 2001 (TUNIBAL 06/01). ICCAT Col Vol Sci Pap 54:425–431

    Google Scholar 

  • García A, Alemany F, Velez-Belchí P et al (2005a) Characterization of the bluefin tuna spawning habitat off the Balearic Archipelago in relation to key hydrographic features and associated environmental conditions. ICCAT Col Vol Sci Pap 58:535–549

    Google Scholar 

  • García A, Alemany F, de la Serna JM et al (2005b) Preliminary results of the 2004 bluefin tuna larval surveys off different Mediterranean sites (Balearic Archipelago, Levantine Sea and the Sicilian Channel). ICCAT Col Vol Sci 58:1261–1270

    Google Scholar 

  • García A, Cortés D, Quintanilla J, Ramirez T, Quintanilla L, Rodríguez JM, Alemany F (2013a) Climate-induced environmental conditions influencing interannual variability of Mediterranean bluefin (Thunnus thynnus) larval growth. Fish Oceanogr 22(4):273–287

    Google Scholar 

  • García A, Laíz R, Quintanilla J, Corregidor F, Alemany F (2013b) Report on abundant bluefin larval concentrations Thunnus thynnus) found off the shelf/slope area in the Spanish Levantine coasts Signs of recovery? ICCAT Col Vol Sci Pap 69(1):292–296

    Google Scholar 

  • Gibbon VE, Penny CB, Štrkalj G, Ruff P (2009) Brief Communication: minimally invasive bone sampling method for DNA analysis. Am J Phys Anthropol 139:596–599

    PubMed  Google Scholar 

  • Giovanardi O, Romanelli M (2010) Preliminary note on tuna larvae in samples from the coasts of the southern-central Mediterranean Sea collected by the MV Arctic Sunrise in June/July 2008. ICCAT Col Vol Sci Pap 65:740–743

    Google Scholar 

  • Gleason LU, Burton RS (2012) High throughput molecular identification of fish eggs using multiplex suspension bead arrays. Mol Ecol Res 12(1):57–66

    CAS  Google Scholar 

  • Godfray HCJ (2002) Challenges for taxonomy. Nature 417:17–19

    CAS  PubMed  Google Scholar 

  • Grüss A, Robinson J, Heppell SS, Heppell SA, Semmens BX (2014) Conservation and fisheries effects of spawning aggregation marine protected areas: what we know, where we should go, and what we need to get there. ICES J Mar Sci. doi:10.1093/icesjms/fsu038

    Google Scholar 

  • Guerra-García JM, Espinosa F, García-Gómez JC (2008) Trends in Taxonomy today: an overview about the main topics in Taxonomy. Zoologica baetica 19:15–49

    Google Scholar 

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

    CAS  Google Scholar 

  • Heinisch G, Corriero A, Medina A et al (2008) Spatial–temporal pattern of bluefin tuna (Thunnus thynnus L. 1758) gonad maturation across the Mediterranean Sea. Mar Biol 154(4):623–630

    Google Scholar 

  • Hernandez FJ Jr, Powers SP, Graham WM (2010) Seasonal variability in ichthyoplankton abundance and assemblage composition in the northern Gulf of Mexico off Alabama. Fish B NOAA 108(2):193–207

    Google Scholar 

  • Hess JE, Campbell NR, Docker MF et al (2014) Use of genotyping by sequencing data to develop a high-throughput and multifunctional SNP panel for conservation applications in Pacific lamprey. Mol Ecol Resour. doi:10.1111/1755-0998.12283

    PubMed  Google Scholar 

  • Hobday AJ, Arrizabalaga H, Evans K, Nicol S, Young JW, Weng KC (2015) Impacts of climate change on marine top predators: advances and future challenges. Deep Sea Res Part II 113:1–8

    Google Scholar 

  • Hopkins GW, Freckleton RP (2002) Declines in the numbers of amateur and professional taxonomists: implications for conservation. Anim Conserv 5:245–249

    Google Scholar 

  • Houston RD, Taggart JB, Cézard T et al (2014) Development and validation of a high density SNP genotyping array for Atlantic salmon (Salmo salar). BMC Genom 15(1):90

    Google Scholar 

  • Hsieh CH, Reiss C, Watson W et al (2005) A comparison of long-term trends and variability in populations of larvae of exploited and unexploited fishes in the Southern California region: a community approach. Prog Oceanogr 67(1):160–185

    Google Scholar 

  • Hsieh CH, Reiss CS, Hunter JR, Beddington JR, May RM, Sugihara G (2006) Fishing elevates variability in the abundance of exploited species. Nature 443(7113):859–862

    CAS  PubMed  Google Scholar 

  • Hubert N, Delrieu-Trottin E, Irisson J-O, Meyer C, Planes S (2010) Identifying coral reef fish larvae through DNA barcoding: a test case with the families Acanthuridae and Holocentridae. Mol Phylogenet Evol 55:1195–1203

    CAS  PubMed  Google Scholar 

  • Hyde JR, Lynn E, Humphreys R Jr, Musyl M, West AP, Vetter R (2005) Shipboard identification of fish eggs and larvae by multiplex PCR, and description of fertilized eggs of blue marlin, shortbill spearfish, and wahoo. Mar Ecol Prog Ser 286:269–277

    CAS  Google Scholar 

  • ICCAT (2006) Recommendation by ICCAT to establish a multi-annual recovery plan for bluefin tuna in the eastern Atlantic and Mediterranean. ICCAT 06-05

  • ICCAT (2013) Report of the standing committee on research and statistics (SCRS) (Madrid, Spain, 30 September–4 October 2013), 344 pp

  • ICCAT (2014a) Report of the standing committee on research and statistics (SCRS) (Madrid, Spain, 29 September–3 October 2014), 348 pp

  • ICCAT (2014b) Recommendation by ICCAT amending the recommendation 13-07 by ICCAT to establish a multi-annual recovery plan for bluefin tuna in the eastern Atlantic and Mediterranean. ICCAT 14-04

  • Ingram GW Jr, Richards WJ, Lamkin JT, Muhling B (2010) Annual indices of Atlantic bluefin tuna (Thunnus thynnus) larvae in the Gulf of Mexico developed using delta-lognormal and multivariate models. Aquat Living Resour 23(01):35–47

    Google Scholar 

  • Ingram GW Jr, Alemany F, Álvarez D, García A (2013) Development of indices of larval bluefin tuna (Thunnus thynnus) in the western Mediterranean Sea. ICCAT Col Vol Sci Pap 69(2):1057–1076

    Google Scholar 

  • Isari S, Fragopoulu N, Somarakis S (2008) Interannual variability in horizontal patterns of larval fish assemblages in the northeastern Aegean Sea (eastern Mediterranean) during early summer. Estuar Coast Shelf Sci 79:607–619

    Google Scholar 

  • Jones PW, Martin FD, Hardy JD, Johnson GD, Fritzsche RA, Drewry GE (1978) Development of fishes of the mid-Atlantic Bight an atlas of egg, larval and juvenile stages, (Vol 5) US Department of the Interior: Fish and wildlife service, Washington, DC 340 pp

  • Kaji T, Tanaka M, Takahashi Y, Oka M, Ishibashi N (1996) Preliminary observations on development of Pacific bluefin tuna Thunnus thynnus (Scombridae) larvae reared in the laboratory, with special reference to the digestive system. Mar Freshw Res 47:261–269

    Google Scholar 

  • Karakulak S, Oray I, Corriero A, Deflorio M, Santamaria N, Desantis S, De Metrio G (2004) Evidence of a spawning area for the bluefin tuna (Thunnus thynnus L.) in the eastern Mediterranean. J Appl Ichthyol 20(4):318–320

    Google Scholar 

  • Kawakami T, Aoyama J, Tsukamoto K (2010) Morphology of pelagic fish eggs identified using mitochondrial DNA and their distribution in waters west of the Mariana Islands. Environ Biol Fish 87(3):221–235

    Google Scholar 

  • Kendall AW Jr, Matarese AC (1994) Status of early life history descriptions of marine teleosts. Fish B NOAA 92(4):725–736

    Google Scholar 

  • Kim JK, Watson W, Hyde J, Lo N, Kim JY, Kim S, Kim YS (2010) Molecular identification of Ammodytes (PISCES, Ammodytidae) larvae, with ontogenetic evidence on separating populations. Genes Genom 32(5):437–445

  • Ko HL, Wang YT, Chiu TS et al (2013) Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS ONE 8(1):e53451

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koched W, Hattour A, Alemany F, García A, Said K (2013) Spatial distribution of tuna larvae in the Gulf of Gabes (Eastern Mediterranean) in relation with environmental parameters. Mediterr Mar Sci 14:5–14

    Google Scholar 

  • Kohno H, Hoshino T, Yasuda F, Taki Y (1982) Larval melanophore patterns of Thunnus alalunga and T thynnus from the Mediterranean. JPN J Ichthyol 28:461–465

    Google Scholar 

  • Koutrakis ET, Kallianiotis AA, Tsikliras AC (2004) Temporal patterns of larval fish distribution and abundance in a coastal area of northern Greece. Sci Mar 68:585–595

  • Lafuente JG, García A, Mazzola S, Quintanilla L, Delgado J, Cuttita A, Patti B (2002) Hydrographic phenomena influencing early life stages of the Sicilian Channel anchovy. Fish Oceanogr 11(1):31–44

    Google Scholar 

  • Larson WA, Seeb LW, Everett MV, Waples RK, Templin WD, Seeb JE (2014) Genotyping by sequencing resolves shallow population structure to inform conservation of Chinook salmon (Oncorhynchus tshawytscha). Evol Appl 7(3):355–369

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lasker R (ed) 1985 An egg production method for estimating spawning biomass of pelagic fish: application to the northern anchovy, Engraulis mordax. US Department of Commerce, NOAA Technical Report, National Marine Fisheries Service, La Jolla, California, vol 36, pp 99

  • Li C, Waldbieser G, Bosworth B, Beck BH, Thongda W, Peatman E (2014) SNP discovery in wild and domesticated populations of blue catfish, Ictalurus furcatus, using genotyping-by-sequencing and subsequent SNP validation. Mol Ecol Resour 14(6):1261–1270

  • Lindeque PK, Parry HE, Harmer RA, Somerfield PJ, Atkinson A (2013) Next generation sequencing reveals the hidden diversity of zooplankton assemblages. PLoS ONE 8(11):e81327

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lindo-Atichati D, Bringas F, Goni G, Muhling B, Muller-Karger FE, Habtes S (2012) Varying mesoscale structures influence larval fish distribution in the northern Gulf of Mexico. Mar Ecol Prog Ser 463:245–257

    Google Scholar 

  • Lo NC, Dorval E, Funes-Rodríguez R, Hernández-Rivas ME, Huang Y, Fan Z (2010) Utilities of larval densities of Pacific mackerel (Scomber japonicus) off California, USA and west coast of Mexico from 1951 to 2008, as spawning biomass indices. Cienc Pesq 18(2):59–75

    Google Scholar 

  • Lockwood SJ, Nichols JH, Dawson WA (1981) The estimation of a mackerel (Scomber scombrus L) spawning stock size by plankton survey. J Plankton Res 3(2):217–233

    Google Scholar 

  • Lowenstein JH, Amato G, Kolokotronis SO (2009) The real maccoyii: identifying tuna sushi with DNA barcodes-contrasting characteristic attributes and genetic distances. PLoS ONE 4(11):e7866

    PubMed Central  PubMed  Google Scholar 

  • Lutcavage ME, Brill RW, Skomal GB, Chase BC, Howey PW (1999) Results of pop-up satellite tagging of spawning size class fish in the Gulf of Maine: do North Atlantic bluefin tuna spawn in the mid-Atlantic? Can J Fish Aquat Sci 56:173–177

    Google Scholar 

  • MacKenzie BR, Mariani P (2012) Spawning of bluefin tuna in the Black Sea: historical evidence, environmental constraints and population plasticity. PLoS ONE 7(7):e39998

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mariani P, MacKenzie BR, Iudicone D, Bozec A (2010) Modelling retention and dispersion mechanisms of bluefin tuna eggs and larvae in the northwest Mediterranean Sea. Prog Oceanogr 86:45–58

    Google Scholar 

  • Matarese AC, Spies IB, Busby MS, Orr JW (2011) Early larvae of Zesticelus profundorum (family Cottidae) identified using DNA barcoding. Ichthyol Res 58(2):170–174

    Google Scholar 

  • Matsumoto WM, Ahlstrom EH, Jones S (1972) On the clarification of larval tuna identification. Fsh B-NOAA 70:1–12

    Google Scholar 

  • McGowan MF, Richards WJ (1989) Bluefin tuna, Thunnus thynnus, larvae in the Gulf Stream off the southeastern United States: satellite and shipboard observations of their environment. Fish B NOAA 87:615–631

    Google Scholar 

  • Miyashita S, Sawada Y, Okada T, Murata O, Kumai H (2001) Morphological development and growth of laboratory-reared larval and juvenile Thunnus thynnus (Pisces: Scombridae). Fish B NOAA 99(4):601–616

    Google Scholar 

  • Moser HG, Charter RL, Watson W, Ambrose DA, Butler JL, Charter SR, Sandknop EM (2000) Abundance and distribution of rockfish (Sebastes) larvae in the Southern California Bight in relation to environmental conditions and fishery exploitation. Calif Coop Oceanic Fish Invest Rep 41:132–147

    Google Scholar 

  • Muhling BA, Lamkin JT, Quattro JM, Smith RH, Roberts MA, Roffer MA, Ramírez K (2011) Collection of larval bluefin tuna (Thunnus thynnus) outside documented western Atlantic spawning grounds. Bull Mar Sci 87(3):687–694

  • Muhling BA, Reglero P, Ciannelli L, Alvarez-Berastegui D, Alemany F, Lamkin JT, Roffer MA (2013) Comparison between environmental characteristics of larval bluefin tuna Thunnus thynnus habitat in the Gulf of Mexico and western Mediterranean Sea. Mar Ecol Prog Ser 486:257–276

    Google Scholar 

  • Neira FJ, Keane JP (2008) Ichthyoplankton-based spawning dynamics of blue mackerel (Scomber australasicus) in south-eastern Australia: links to the East Australian Current. Fish Oceanogr 17(4):281–298

    Google Scholar 

  • Nielsen EE, Hansen MM (2008) Waking the dead: the value of population genetic analyses of historical samples. Fish Fish 9:450–461

    Google Scholar 

  • Nishida T, Tsuji S, Segawa K (1998) Spatial data analyses of Atlantic bluefin tuna larval surveys in the 1994 ICCAT BYP. ICCAT Col Vol Sci Pap 48:107–110

  • Oray IK, Karakulak FS (2005) Further evidence of spawning of bluefin tuna (Thunnus thynnus L, 1758) and the tuna species (Auxis rochei Ris, 1810, Euthynnus alletteratus Raf, 1810) in the eastern Mediterranean Sea: preliminary results of TUNALEV larval survey in 2004. J Appl Ichtyol 21(3):236–240

    Google Scholar 

  • Özsoy E, Hecht A, Ünlüata Ü, et al (1993) A synthesis of the Levantine Basin circulation and hydrography, 1985–1990. Deep Sea Res Part II 40(6):1075–1119

  • Packer L, Gibbs J, Sheffield C, Hanner R (2009) DNA barcoding and the mediocrity of morphology. Mol Ecol Resour 9:42–50

    PubMed  Google Scholar 

  • Padoa E (1956) Scombriformes e Carangiformes In: Lo Bianco S (ed) Uova, larve e stadi giovanili di Teleostei. Fauna e Flora del Golfo di Napoli. Monografia 38, pp 471–576

  • Paine MA, McDowell JR, Graves JE (2007) Specific identification of western Atlantic Ocean scombrids using mitochondrial DNA cytochrome c oxidase subunit I (COI) gene region sequences. Bull Mar Sci 80:353–367

    Google Scholar 

  • Paine MA, McDowell JR, Graves JE (2008) Specific identification using COI sequence analysis of scombrid larvae collected off the Kona coast of Hawaii Island. Ichthyol Res 55(1):7–16

    Google Scholar 

  • Pegg GG, Sinclair B, Briskey L, Aspden WJ (2006) MtDNA barcode identification of fish larvae in the southern Great Barrier Reef, Australia. Sci Mar 70:7–12

  • Piccinetti C, Piccinetti Manfrin G (1993) Distribution des larves de thonidés en Mediterranée. ICCAT Col Vol Sci Pap 40:164–172 (in French)

    Google Scholar 

  • Piccinetti C, Piccinetti Manfrin G, Soro S (1997) Résultats d’une campagne de recherche sur les larves de thonidés en Mediterranée. ICCAT Col Vol Sci Pap 46:207–214 (in French)

    Google Scholar 

  • Poulsen NA, Hemmer-Hansen J, Loeschcke V, Carvalho GR, Nielsen EE (2011) Microgeographical population structure and adaptation in Atlantic cod Gadus morhua: spatio-temporal insights from gene-associated DNA markers. Mar Ecol Prog Ser 436:231–243

    Google Scholar 

  • Puncher GN, Arrizabalaga H, Alemany F, et al (2015) Molecular identification of Atlantic bluefin tuna (Thunnus thynnus, Scombridae) larvae and development of a genetic character-based identification key for Mediterranean scombrids. PLoS ONE (in press)

  • Ratnasingham S, Hebert PDN (2007) BOLD: The barcode of life data system (http://www.barcodinglife.org). Mol Ecol Notes 7:355–364

  • Reglero P, Urtizberea A, Torres AP, Alemany F, Fiksen Ø (2011) Cannibalism among size classes of larvae may be a substantial mortality component in tuna. Mar Ecol Prog Ser 433:205–219

    Google Scholar 

  • Reglero P, Ciannelli L, Alvarez-Berastegui D, Balbín R, López-Jurado JL, Alemany F (2012) Geographically and environmentally driven spawning distributions of tuna species in the western Mediterranean Sea. Mar Ecol Prog Ser 463:273–284

    Google Scholar 

  • Riccioni G, Landi M, Ferrara G et al (2010) Spatio-temporal population structuring and genetic diversity retention in depleted Atlantic bluefin tuna of the Mediterranean Sea. PNAS 107:2102–2107

    CAS  PubMed Central  PubMed  Google Scholar 

  • Riccioni G, Stagioni M, Landi M, Ferrara G, Barbujani G, Tinti F (2013) Genetic structure of bluefin tuna in the Mediterranean Sea correlates with environmental variables. PLoS ONE 8(11):e80105

    PubMed Central  PubMed  Google Scholar 

  • Richards WJ (1976) Spawning of bluefin tuna (Thunnus thynnus) in the Atlantic Ocean and adjacent seas. ICCAT Col Vol Sci Pap 5:267–278

    Google Scholar 

  • Richards WJ (ed) (2004) Early stages of Atlantic fishes: an identification guide for the western central north Atlantic, vol 1. CRC Press, Boca Roton, pp 2212–2213

    Google Scholar 

  • Richards WJ, Pothoff T (1974) Analysis of the taxonomic characters of young scombrid fishes, genus Thunnus. In: Blaxter JHS (ed) The early life history of fish. Springer, Berlin, pp 623–648

    Google Scholar 

  • Richards WJ, Potthoff T, Kim JM (1990) Problems identifying tuna larvae species (Pisces: Scombridae: Thunnus) from the Gulf of Mexico. Fish B NOAA 88:607–609

    Google Scholar 

  • Richardson DE, Vanwye JD, Exum AM, Cowen RK, Crawford DL (2006) High-throughput species identification: from DNA isolation to bioinformatics. Mol Ecol Notes 7(2):199–207

    CAS  Google Scholar 

  • Richardson DE, Llopiz JK, Guigand CM, Cowen RK (2010) Larval assemblages of large and medium-sized pelagic species in the Straits of Florida. Prog Oceanogr 86(1):8–20

    Google Scholar 

  • Robinson AR, Malanotte-Rizzoli P, Hecht A et al (1992) General circulation of the Eastern Mediterranean. Earth Sci Rev 32(4):285–309

    Google Scholar 

  • Sanzo L (1932) Uova e primi stadi larval de tonno (Orcynus thynnus Ltkn) Consiglio nazionale dell ricerche. Reale comitato talassografico italiano 189 (in Italian)

  • Sanzo L (1933) Uova e primi stadi larvali di alalonga (Orcynus germo LTKU). R. Com. Talas. Ital. Memoria 198:11 (in Italian)

    Google Scholar 

  • Scaccini A (1975) Uova e larve di tonno pescate nella Sicilia occidentale e loro allevamento. Ministero della marina mercantile, Direzione generale della pesca marittima Roma, Italy, Memoria 39:1–120 (In Italian)

    Google Scholar 

  • Scaccini A, Sara R, Piccinetti C, Manfrin G (1973) Donées préliminaires sur une campagne d’étude des œufs et larves de Thonidés. Rapp Comm Int Mer Médit 21(10):801–803 (in French)

    Google Scholar 

  • Scott GP, Turner SC (2003) Updated index of bluefin tuna (Thunnus thynnus) spawning biomass from Gulf of Mexico ichthyoplankton surveys. ICCAT Col Vol Sci Pap 55:1123–1126

  • Scott GP, Turner SC, Churchill GB, Richards WJ, Brothers EB (1993) Indices of larval bluefin tuna, Thunnus thynnus, abundance in the Gulf of Mexico; modelling variability in growth, mortality, and gear selectivity. Bull Mar Sci 53:912–929

    Google Scholar 

  • Seberg O, Humphries CJ, Knapp S et al (2003) Shortcuts in systematics? A commentary on DNA-based taxonomy. Trends Ecol Evol 18:63–65

    Google Scholar 

  • Seeb LW, Templin WD, Sato S, Abe S, Warheit K, Park JY, Seeb JE (2011) Single nucleotide polymorphisms across a species’ range: implications for conservation studies of Pacific salmon. Mol Ecol Resour 11:195–217

    PubMed  Google Scholar 

  • Shokralla S, Gibson JF, Nikbakht H, Janzen DH, Hallwachs W, Hajibabaei M (2014) Next-generation DNA barcoding: using next-generation sequencing to enhance and accelerate DNA barcode capture from single specimens. Mol Ecol Resour 14:892–901

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stein ED, Martinez MC, Stiles S, Miller PE, Zakharov EV (2014) Is DNA barcoding actually cheaper and faster than traditional morphological methods: results from a survey of freshwater bioassessment efforts in the United States? PLoS ONE 9(4):e95525

    PubMed Central  PubMed  Google Scholar 

  • Stevens MI, Porco D, D’Haese CA, Deharveng L (2011) Comment on “taxonomy and the DNA barcoding enterprise” by Ebach (2011). Zootaxa 2838:85–88

    Google Scholar 

  • Stratoudakis Y, Bernal M, Ganias K, Uriarte A (2006) The daily egg production method: recent advances, current applications and future challenges. Fish Fish 7(1):35–57

    Google Scholar 

  • Swartz ER, Mwale M, Hanner R (2008) A role for barcoding in the study of African fish diversity and conservation. S Afr J Sci 104(7–8):293–298

    Google Scholar 

  • Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2002) DNA points the way ahead in taxonomy. Nature 418:479

    CAS  PubMed  Google Scholar 

  • Tsuji S, Nishikawa Y, Segawa K, Hiroe Y (1997) Distribution and abundance of Thunnus larvae and their relation to the oceanographic condition in the Gulf of Mexico and the Mediterranean Sea during May through August of 1994. ICCAT Col Vol Sci Pap 46:161–176

  • Ueyanagi S (1966) On the red pigmentation of larval tuna and its usefulness in species identification. Rep Nankai Reg Fish Res Lab 24:41–48 (in Japanese)

    Google Scholar 

  • Ueyanagi S (1969) Observations on the distribution of tuna larvae in the Indo-Pacific Ocean with emphasis on the delineation of the spawning areas of albacore, Thunnus alalunga. Bull Far Seas Fish Res Lab 2:177–256

    Google Scholar 

  • Ueyanagi S, Watanabe H (1964) Methods of identification of larvae of tunas and billfishes (II) materials for tuna fisheries research council. Nankai Reg Fish Res Lab, Kohchi, pp 1–16

    Google Scholar 

  • Valdez-Moreno M, Vásquez-Yeomans L, Elías-Gutiérrez M, Ivanova NV, Hebert PDN (2010) Using DNA barcodes to connect adults and early life stages of marine fishes from the Yucatan Peninsula, Mexico: potential in fisheries management. Mar Fresh Res 61:655–671

    Google Scholar 

  • Vandersea MW, Litaker RW, Marancik KE et al (2008) Identification of larval sea basses (Centropristis spp.) using ribosomal DNA-specific molecular assays. Fish B NOAA 106:183–193

    Google Scholar 

  • Vecchione M, Mickevich MF, Fauchald K et al (2000) Importance of assessing taxonomic adequacy in determining fishing effects on marine biodiversity. ICES J Mar Sci: J Cons 57:677–681

    Google Scholar 

  • Victor BC, Hanner R, Shivji M, Hyde J, Caldow C (2009) Identification of the larval and juvenile stages of the Cubera Snapper, Lutjanus cyanopterus, using DNA barcoding. Zootaxa 2215:24–36

    Google Scholar 

  • Viñas J, Tudela S (2009) A validated methodology for genetic identification of tuna species (genus Thunnus). PLoS ONE 4(10):e7606

    PubMed Central  PubMed  Google Scholar 

  • Viñas J, Gordoa A, Fernández-Cebrián R, Pla C, Vahdet Ü, Araguas RM (2011) Facts and uncertainties about the genetic population structure of Atlantic bluefin tuna (Thunnus thynnus) in the Mediterranean Implications for fishery management. Rev Fish Biol Fish 21:527–541

    Google Scholar 

  • Vodianitskii VA, Kazanova II (1954) Diagnostic description of the eggs and larvae of the Black Sea fishes. Trudy VNIRO 28:240–327 (in Russian)

    Google Scholar 

  • Ward RD, Hanner R, Hebert PDN (2009) The campaign to DNA barcode all fishes, FISH-BOL. J Fish Biol 74:329–356

    CAS  PubMed  Google Scholar 

  • White WT, Last PR (2012) A review of the taxonomy of chondrichthyan fishes: a modern perspective. J Fish Biol 80(5):901–917

    CAS  PubMed  Google Scholar 

  • Willette DA, Allendorf FW, Barber PH et al (2014) So, you want to use next-generation sequencing in marine systems? Insight from the Pan-Pacific Advanced Studies Institute. Bull Mar Sci 90(1):79–122

    Google Scholar 

  • Wilson EO (2003) The encyclopedia of life. Trends Ecol Evol 18:77–80

    Google Scholar 

  • Worm B, Tittensor DP (2011) Range contraction in large pelagic predators. Proc Natl Acad Soc 108:11942–11947

    CAS  Google Scholar 

  • Yabe H, Ueyanagi S, Watanabe H (1966) Studies on the early life history of bluefin tuna Thunnus thynnus and on the larvae of the southern bluefin tuna T maccoyii. Rep Nankai Reg Fish Res Lab 23:95–129 (in Japanese)

    Google Scholar 

  • Yoder M, De Ley IT, Wm King I et al (2006) DESS: a versatile solution for preserving morphology and extractable DNA of nematodes. Nematology 8(3):367–376

    CAS  Google Scholar 

  • Zarrad R, Alemany F, Rodríguez JM, Jarboui O, Lopez-Jurado JL, Balbin R (2013) Influence of summer conditions on the larval fish assemblage in the eastern coast of Tunisia (Ionian Sea, Southern Mediterranean). J Sea Res 76:114–125

    Google Scholar 

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Acknowledgments

This work was co-funded by the MARES Joint Doctorate programme selected under Erasmus Mundus and coordinated by Ghent University (FPA 2011-0016). Many thanks to Antonio Di Natale, Jerry Scott, John Lamkin and Edorta Aranguena for helping to assemble the various tuna taxonomic keys. Thanks are also due to the IEO researchers in charge of the tuna rearing experiments at the IEO facilities in Mazarrón, F. de la Gándara, A. Ortega and P. Reglero, for providing the images of BFT larvae. Finally, we thank the three anonymous reviewers for their detailed and helpful suggestions.

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Authors and Affiliations

  1. Department of Biological, Geological and Environmental Sciences/Laboratory of Genetics and Genomics of Marine Resources and Environment (GenoDREAM), University of Bologna, Via S. Alberto 163, 48123, Ravenna, Italy

    Gregory Neils Puncher, Alessia Cariani & Fausto Tinti

  2. Department of Marine Biology, Ghent University, Ghent, Belgium

    Gregory Neils Puncher

  3. Instituto Español de Oceanografía, Centro Oceanográfico de Baleares, Palma, Spain

    Francisco Alemany

  4. AZTI Tecnalia, Marine Research Division, Herrera Kaia, Pasaia, Gipuzkoa, Spain

    Haritz Arrizabalaga

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  1. Gregory Neils Puncher
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  4. Alessia Cariani
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  5. Fausto Tinti
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Correspondence to Gregory Neils Puncher.

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Puncher, G.N., Alemany, F., Arrizabalaga, H. et al. Misidentification of bluefin tuna larvae: a call for caution and taxonomic reform. Rev Fish Biol Fisheries 25, 485–502 (2015). https://doi.org/10.1007/s11160-015-9390-1

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