The fishing and illegal trade of the angelshark: DNA barcoding against misleading identifications

Abstract Morphological identification in the field can be extremely difficult considering fragmentation of species for trade or high similarity between congeneric species. In this context, the shark group belonging to the genus Squatina is composed of three species distributed in the southern part of the western Atlantic. These three species are classified in the IUCN Red List as endangered, and they are currently protected under Brazilian law, which prohibits fishing and trade. Molecular genetic tools are now used for practical taxonomic identification, particularly in cases where morphological observation is prevented, e.g., during fish processing. Consequently, DNA barcoding was used in the present study to track potential crimes against the landing and trade of endangered species along the Sao Paulo coastline, in particular Squatina guggenheim (n = 75) and S. occulta (n = 5), as well as the Brazilian guitarfish Pseudobatos horkelii (n = 5). DNA barcoding revealed the continuous fishing and trafficking of these protected species, thus giving clear evidence that the current conservation models and methods of monitoring are not working.

[1]  R. Maggioni,et al.  Prospective molecular markers for the identification of illegally traded angelsharks (Squatina) and dolphin (Sotalia guianensis). , 2014, Genetics and molecular research : GMR.

[2]  G. Cliff,et al.  Molecular systematics and global phylogeography of angel sharks (genus Squatina). , 2010, Molecular phylogenetics and evolution.

[3]  A. Solé-Cava,et al.  Biochemical evidence for a third species of angel shark off the east coast of South America , 1987 .

[4]  Nicholas K. Dulvy,et al.  Why have global shark and ray landings declined: improved management or overfishing? , 2016 .

[5]  John A. Musick,et al.  Sharks and their Relatives: Ecology And Conservation , 1998 .

[6]  P. Hebert,et al.  bold: The Barcode of Life Data System (http://www.barcodinglife.org) , 2007, Molecular ecology notes.

[7]  G. Carvalho,et al.  Fish Product Mislabelling: Failings of Traceability in the Production Chain and Implications for Illegal, Unreported and Unregulated (IUU) Fishing , 2014, PloS one.

[8]  David L. Wheeler,et al.  GenBank , 2015, Nucleic Acids Res..

[9]  C. M. Vooren,et al.  Ações para a conservação de tubarões e raias no sul do Brasil , 2005 .

[10]  Dennis A. Benson,et al.  GenBank , 2016, Nucleic Acids Res..

[11]  Mudjekeewis D. Santos,et al.  Detection of mislabeled commercial fishery by-products in the Philippines using DNA barcodes and its implications to food traceability and safety , 2013 .

[12]  S. Weigmann,et al.  Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. , 2016, Journal of fish biology.

[13]  A. Solé-Cava,et al.  Isozymic differentiation of two sibling species of Squatina (chondrichthyes) in South Brazil. , 1983, Comparative biochemistry and physiology. B, Comparative biochemistry.

[14]  A. Hilsdorf,et al.  Genetic identification of Carcharhinus sharks from the southwest Atlantic Ocean (Chondrichthyes: Carcharhiniformes) , 2013 .

[15]  E. Harvey,et al.  Global patterns in the bycatch of sharks and rays , 2015 .

[16]  G. Naylor,et al.  A new species of guitarfish, Rhinobatos borneensis sp. nov. with a redefinition of the family-level classification in the order Rhinopristiformes (Chondrichthyes: Batoidea). , 2016, Zootaxa.

[17]  Sarah Valenti,et al.  You can swim but you can't hide: the global status and conservation of oceanic pelagic sharks and rays , 2008 .

[18]  E J Milner-Gulland,et al.  Global estimates of shark catches using trade records from commercial markets. , 2006, Ecology letters.

[19]  J. Felsenstein.  CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[20]  H. Schneider,et al.  Molecular Identification and Traceability of Illegal Trading in Lignobrycon myersi (Teleostei: Characiformes), a Threatened Brazilian Fish Species, Using DNA Barcode , 2016, TheScientificWorldJournal.

[21]  P. Borsa.  Comment on 'Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity by Weigmann (2016)'. , 2016, Journal of fish biology.

[22]  C. Oliveira,et al.  Illegal trade of the guitarfish Rhinobatos horkelii on the coasts of central and southern Brazil: genetic identification to aid conservation , 2012 .

[23]  Rob Ogden,et al.  Fisheries forensics: the use of DNA tools for improving compliance, traceability and enforcement in the fishing industry , 2008 .

[24]  J. Vitule,et al.  Shark mislabeling threatens biodiversity. , 2013, Science.

[25]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[26]  M. Kimura.  A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[27]  R. Ward,et al.  DNA barcoding Australia's fish species , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  D. Carvalho,et al.  DNA Barcoding identification of commercialized seafood in South Brazil: A governmental regulatory forensic program , 2015 .

[29]  Chaolun Allen Chen,et al.  DNA Barcoding of Shark Meats Identify Species Composition and CITES-Listed Species from the Markets in Taiwan , 2013, PloS one.

[30]  W. White.  Three new angel sharks (Chondrichthyes: Squatinidae) from the Indo-Australian region , 2008 .

[31]  Sudhir Kumar,et al.  MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. , 2016, Molecular biology and evolution.

[32]  J. Ragle,et al.  IUCN Red List of Threatened Species , 2010 .

[33]  R. Hanner,et al.  DNA barcodes identify marine fishes of São Paulo State, Brazil , 2012, Molecular ecology resources.

[34]  S. Cooke,et al.  Trends in shark bycatch research: current status and research needs , 2012, Reviews in Fish Biology and Fisheries.

[35]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[36]  L. Campagna.  Checklist of Living : Chondrichthyes , 2011 .

[37]  C. Bradshaw,et al.  Chapter 4. Susceptibility of sharks, rays and chimaeras to global extinction. , 2009, Advances in marine biology.

[38]  N. Saito.  The neighbor-joining method : A new method for reconstructing phylogenetic trees , 1987 .

[39]  John D. Stevens,et al.  The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems , 2000 .

[40]  M. Howlett,et al.  From Paper Trails to DNA Barcodes: Enhancing Traceability in Forest and Fishery Certification , 2012 .

[41]  F. Tuya,et al.  Population structure, distribution and habitat use of the Critically Endangered Angelshark, Squatina squatina, in the Canary Islands , 2017 .

[42]  Sarah Valenti,et al.  Extinction risk and conservation of the world’s sharks and rays , 2013, eLife.

[43]  王丽华,et al.  国际生命条形码计划—DNA Barcoding , 2009 .

[44]  Dos nuevas especies del género Squatina (Chondrichthyes: Squatinidae) del Golfo de México , 2014 .

[45]  F. Foresti,et al.  Genetic identification of lamniform and carcharhiniform sharks using multiplex-PCR , 2010, Conservation Genetics Resources.

[46]  Terence I. Walker,et al.  Can shark resources be harvested sustainably? A question revisited with a review of shark fisheries , 1998 .

[47]  A. E. Bester-van der Merwe,et al.  Species identification and comparative population genetics of four coastal houndsharks based on novel NGS‐mined microsatellites , 2017, Ecology and evolution.

[48]  P. Haye,et al.  Characterization of the pelagic shark‐fin trade in north‐central Chile by genetic identification and trader surveys , 2008 .