Abstract
Peru has globally important elasmobranch fisheries, and mobulids are no exception. However, little is known about Peru’s small-scale mobulid fisheries. Mismatches between fishing reports and studies regarding species occurrence suggest a problem in identification methodologies of mobulids at the species level. This is supported by evidence of external resemblance between species, landings of incomplete bodies, and the use of a single name for the five species known to occur in Peruvian waters (“Manta” for Mobula birostris, Mobula munkiana, Mobula mobular, Mobula tarapacana and Mobula thurstoni). Given the need for improved conservation and management measures of mobulids in Peru, we tested the applicability of DNA barcoding combined with morphological identification to better understand mobulid catches by small-scale fisheries in north Peru. A total of 137 samples of muscle tissue from mobulids captured during fishing activities were collected of which 99 amplified and analysed for Cytochrome C Oxidase Subunit I (COI). Samples of the five species known to occur in Peru were obtained, confirming captures of all of them by local fisheries. Morphological identification allowed us to correctly identify more than 94% of specimens to the species level even though most of them arrived butchered (e.g., only pectoral fins). Increased capacity building and training for morphological identification of mobulid species by field observers, authorities, and fishermen, combined with molecular tools, is highly recommended to avoid mistakes in landings reports and to correctly enforce conservation measures for these species.
Similar content being viewed by others
References
Alfaro-Cordova E, del Solar A, Alfaro-Shigueto J, Mangel JC, Diaz B, Carrillo O, Sarmiento D (2017) Captures of manta and devil rays by small-scale gillnet fisheries in northern Peru. Fish Res 195:28–36. https://doi.org/10.1016/j.fishres.2017.06.012
Asis AMJM, Lacsamana JKM, Santos MD (2016) Illegal trade of regulated and protected aquatic species in the Philippines detected by DNA barcoding. Mitochondrial DNA 27(1):659–666. https://doi.org/10.3109/19401736.2014.913138
Ayala L, Sánchez-Scaglioni R (2014) Captura, esfuerzo y captura incidental de la pesca con espinel en el centro de Perú. Rev Peru Biol 21(3):243–250
Biffi D, López-Mobilia A, Kelez S, Williams DA, Chumchal MM, Weinburgh M (2020) Mislabelling and high mercury content hampers the efforts of market-based seafood initiatives in Peru. Sci Rep. https://doi.org/10.1038/s41598-020-77338-x
Bineesh KK, Gopalakrishnan A, Akhilesh KV, Sajeela KA, Abdussamad EM, Pillai NGK, Basheer VS, Jena JK, Ward RD (2017) DNA barcoding reveals species composition of sharks and rays in the Indian commercial fishery. Mitochondrial DNA Part A: DNA Mapp, Seq, Anal 28(4):458–472. https://doi.org/10.3109/19401736.2015.1137900
Bucair N, Francini-Filho RB, Almerón-Souza F, Luiz OJ (2021) Underestimated threats to manta rays in Brazil: primacies to support conservation strategies. Global Ecol Conserv. https://doi.org/10.1016/j.gecco.2021.e01753
Bunholi IV, da Ferrette BLS, de Biasi JB, de Magalhães CO, Rotundo MM, Oliveira C, Foresti F, Mendonça FF (2018) The fishing and illegal trade of the angelshark: DNA barcoding against misleading identifications. Fish Res 206:193–197. https://doi.org/10.1016/j.fishres.2018.05.018
Cerutti-Pereyra F, Meekan MG, Wei NV, Shea OO, Bradshaw CJA, Austin CM (2012) Identification of rays through DNA barcoding: an application for ecologists. PLoS ONE. https://doi.org/10.1371/journal.pone.0036479
Cornejo R, Vélez-Zuazo X, González-Pestana A, Kouri C, Mucientes G (2015) An updated checklist of Chondrichthyes from the southeast Pacific off Peru. Check List 11(6):1809
Couturier LIE, Marshall AD, Jaine FRA, Kashiwagi T, Pierce SJ, Townsend KA, Weeks SJ, Bennett MB, Richardson AJ (2012) Biology, ecology and conservation of the Mobulidae. J Fish Biol 80(5):1075–1119. https://doi.org/10.1111/j.1095-8649.2012.03264.x
Croll DA, Dewar H, Dulvy NK, Fernando D, Francis MP, Galván-Magaña F, Hall M, Heinrichs S, Marshall A, Mccauley D, Newton KM, Notarbartolo-Di-Sciara G, O’Malley M, O’Sullivan J, Poortvliet M, Roman M, Stevens G, Tershy BR, White WT (2016) Vulnerabilities and fisheries impacts: the uncertain future of manta and devil rays. Aquat Conserv: Mar Freshw Ecosyst 26(3):562–575. https://doi.org/10.1002/aqc.2591
Dulvy NK, Pacoureau N, Rigby CL, Pollom RA, Jabado RW, Ebert DA, Finucci B, Pollock CM, Cheok J, Derrick DH, Herman KB, Sherman CS, VanderWright WJ, Lawson JM, Walls RHL, Carlson JK, Charvet P, Bineesh KK, Fernando D, Simpfendorfer CA (2021) Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Curr Biol. https://doi.org/10.1016/j.cub.2021.08.062
Dulvy NK, Pardo SA, Simpfendorfer CA, Carlson JK (2014) Diagnosing the dangerous demography of manta rays using life history theory. PeerJ 2:e400. https://doi.org/10.7717/peerj.400
FAO Fisheries Division, Statistics, and Information Branch. FishStatJ: Universal software for fishery statistical time series. Copyright 2020
Flounders, L. (2020). The impact of the IOTC fisheries on mobulid rays: status and interactions, data availability, and recommendations for management.
Giovos I, Aga Spyridopoulou RN, Doumpas N, Glaus K, Kleitou P, Kazlari Z, Katsada D, Loukovitis D, Mantzouni I, Papapetrou M, Papastamatiou YP, Moutopoulos DK (2021) Approaching the “real” state of elasmobranch fisheries and trade: a case study from the Mediterranean. Ocean Coast Manag. https://doi.org/10.1016/j.ocecoaman.2021.105743
Gonzalez-Pestana A, Velez-Zuazo X (2016) Situación de los batoideos en el Perú: Lo que sabemos y lo que no sabemos. V Congreso de Ciencias del Mar del Perú, Lambayeque
Guirkinger L, Rojas-Perea S, Ender I, Ramsden M, Lenton-Lyons C, Geldmann J (2021) Motivations for compliance in Peruvian manta ray fisheries. Marine Policy. https://doi.org/10.1016/j.marpol.2020.104315
Henderson AC (2020) A review of potential taxonomic barriers to the effective management of Gulf elasmobranch fisheries. Aquat Ecosyst Health Manage 23(2):210–219. https://doi.org/10.1080/14634988.2020.1800327
Hobbs CAD, Potts RWA, Bjerregaard Walsh M, Usher J, Griffiths AM (2019) Using DNA barcoding to investigate patterns of species utilisation in UK shark products reveals threatened species on sale. Sci Rep. https://doi.org/10.1038/s41598-018-38270-3
Instituto del Mar del Peru – IMARPE. (2021). Respuesta a la solicitud de acceso a la información pública: Estimados de desembarques de las especies de “mantas” registrado por la pesca artesanal a lo largo del litoral peruano, durante el periodo 2015–2020 Oficio Nº 570–2021 IMARPE/OGA. Inst. Mar Perú.
Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN (2007) Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7(4):544–548. https://doi.org/10.1111/j.1471-8286.2007.01748.x
John A, Arshaad WM, Sheikh HI (2018) DNA Barcoding and Molecular Phylogeny. In: Trivedi S, Rehman H, Saggu S, Panneerselvam C, Ghosh SK (eds) DNA Barcoding and Molecular Phylogeny. Springer International Publishing, Cham
Lewis SA, Setiasih N, Fahmi D, O’Malley MP, Campbell SJ, Yusuf M, Sianipar A (2015) Assessing Indonesian manta and devil ray populations through historical landings and fishing community interviews. PeerJ PrePrints. https://doi.org/10.7287/peerj.preprints.1334v1
Marín A, Serna J, Robles C, Ramírez B, Reyes-Flores LE, Zelada-Mázmela E, Sotil G, Alfaro R (2018) A glimpse into the genetic diversity of the Peruvian seafood sector: unveiling species substitution, mislabeling and trade of threatened species. PLoS ONE. https://doi.org/10.1371/journal.pone.0206596
Ministerio del Ambiente. (2021). Diagnóstico Situacional de las “Mobulas” en el Perú. Lima.
Pardo SA, Kindsvater HK, Cuevas-Zimbrón E, Sosa-Nishizaki O, Pérez-Jiménez JC, Dulvy NK (2016) Growth, productivity, and relative extinction risk of a data-sparse devil ray. Sci Rep. https://doi.org/10.1038/srep33745
Sembiring A, Pertiwi NPD, Mahardini A, Wulandari R, Kurniasih EM, Kuncoro AW, Cahyani NKD, Anggoro AW, Ulfa M, Madduppa H, Carpenter KE, Barber PH, Mahardika GN (2015) DNA barcoding reveals targeted fisheries for endangered sharks in Indonesia. Fish Res 164:130–134. https://doi.org/10.1016/j.fishres.2014.11.003
Smith WD, Bizzarro JJ, Richards VP, Nielsen J, Márquez-Farías F, Shivji MS (2009) Morphometric convergence and molecular divergence: the taxonomic status and evolutionary history of Gymnura crebripunctata and Gymnura marmorata in the eastern Pacific Ocean. J Fish Biol 75(4):761–783. https://doi.org/10.1111/j.1095-8649.2009.02300.x
Steinke Di, Bernard AM, Horn RL, Hilton P, Hanner R, Shivji MS (2017) DNA analysis of traded shark fins and mobulid gill plates reveals a high proportion of species of conservation concern. Sci Rep. https://doi.org/10.1038/s41598-017-10123-5
Stewart JD, Jaine FRA, Armstrong AJ, Armstrong AO, Bennett MB, Burgess KB, Couturier LIE, Croll DA, Cronin MR, Deakos MH, Dudgeon CL, Fernando D, Froman N, Germanov ES, Hall MA, Hinojosa-Alvarez S, Hosegood JE, Kashiwagi T, Laglbauer BJL, Stevens GMW (2018) Research priorities to support effective Manta and Devil Ray conservation. Front Marine Sci. https://doi.org/10.3389/fmars.2018.00314
Velez-Zuazo X, Alfaro-Shigueto J, Rosas-Puchuri U, Guidino C, Pasara-Polack A, Riveros JC, Mangel JC (2021) High incidence of mislabeling and a hint of fraud in the ceviche and sushi business. Food Control. https://doi.org/10.1016/j.foodcont.2021.108224
Velez-Zuazo X, Alfaro-Shigueto J, Mangel J, Papa R, Agnarsson I (2015) What barcode sequencing reveals about the shark fishery in Peru. Fish Res 161:34–41. https://doi.org/10.1016/j.fishres.2014.06.005
Wainwright BJ, Ip YCA, Neo ML, Chang JJM, Gan CZ, Clark-Shen N, Huang D, Rao M (2018) DNA barcoding of traded shark fins, meat and mobulid gill plates in Singapore uncovers numerous threatened species. Conserv Genet 19(6):1393–1399. https://doi.org/10.1007/s10592-018-1108-1
White WT, Giles J, Dharmadi, Potter IC (2006) Data on the bycatch fishery and reproductive biology of mobulid rays (Myliobatiformes) in Indonesia. Fish Res 82(1–3):65–73. https://doi.org/10.1016/j.fishres.2006.08.008
White WT, Last PR (2012) A review of the taxonomy of chondrichthyan fishes: a modern perspective. J Fish Biol 80(5):901–917. https://doi.org/10.1111/j.1095-8649.2011.03192.x
White WT, Corrigan S, Yang L, Henderson AC, Bazinet AL, Swofford DL, Naylor GJP (2018) Phylogeny of the manta and devilrays (Chondrichthyes: mobulidae), with an updated taxonomic arrangement for the family. Zool J Linn Soc. https://doi.org/10.1093/zoolinnean/zlx018
Willette DA, Simmonds SE, Cheng SH, Esteves S, Kane TL, Nuetzel H, Pilaud N, Rachmawati R, Barber PH (2017) Using DNA barcoding to track seafood mislabeling in Los Angeles restaurants. Conserv Biol 31(5):1076–1085. https://doi.org/10.1111/cobi.12888
Zeng Y, Wu Z, Zhang C, Meng Z, Jiang Z, Zhang J (2016) DNA barcoding of Mobulid Ray Gill Rakers for Implementing CITES on Elasmobranch in China. Sci Rep. https://doi.org/10.1038/srep37567
Acknowledgements
We would like to thank the members of the fishing communities who participated in this study, in particular F. Fiestas for all the support during sampling. We also thank ProDelphinus staff and members of the elasmobranch project: A. Gonzalez, F. Córdova, J. Coasaca, and N. Acuña for their support. This study was funded by the Rufford Small Grant (17953-1), a FINCyT/INNOVATE (Contract N° 369 PIBA 2014), Darwin Initiative and the Whitley Fund for Nature.
Funding
This study was funded by the Rufford Small Grant (17953–1), a FINCyT/INNOVATE (Contract N° 369 PIBA 2014), Darwin Initiative and the Whitley Fund for Nature.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. EA-C led on research design, data collection, processing and analysis, as well as manuscript preparation, OC and DS, assisted with sampling and data processing, RMC-A, JA-S and JCM, assisted with data analysis and manuscript preparation, and XV-Z assisted with research design and manuscript preparation.
Corresponding author
Ethics declarations
Competing interests
Financial interests: The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Alfaro-Cordova, E., Cañedo-Apolaya, R.M., Alfaro-Shigueto, J. et al. Is what you see what you get? Assessing external morphological identification of devil rays captured by small-scale fisheries in northern Peru using DNA barcoding. Conservation Genet Resour 15, 97–103 (2023). https://doi.org/10.1007/s12686-023-01306-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12686-023-01306-6