Elemental composition in the bones and gills of juvenile Atlantic Bluefin Tuna (Thunnus thynnus): can it be used to distinguish batches?
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Abstract
Atlantic Bluefin Tuna (Thunnus thynnus) aquaculture has developed rapidly in recent years, making it necessary to discriminate between specimens derived from aquaculture (captive-reared) and those derived from fisheries (wild-caught). In this study, a method based on the chemical composition of discard tissues (gills and bones) in 3 batches of juvenile T. thynnus (tank-cultured on land, cage-reared in the sea, and wild-caught) was assessed. The concentrations of 11 macro- and micro-elements (i.e., Ca, Fe, K, Mg, Na, P, S, Cu, Mn, Zn, and Sr) were determined and evaluated using an analysis of variance (ANOVA) and 2 multivariate tests, namely a principal component analysis (PCA) and discriminant canonical analysis (DCA). The best results were obtained from the gills and from the batch corresponding to the wild-caught specimens. However, the results were not robust enough to establish any specific pattern that would facilitate the identification of the origin of T. thynnus specimens.
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Aenglong C, Wang YM, Limpawattana M, Sukketsiri W, Tang QJ, Klaypradit W, Kerdpiboon S. 2022. Synthesis of soluble calcium compound from skipjack tuna bones using edible weak acids. LWT-Food Sci Technol.162:113460.
https://doi.org/10.1016/j.lwt.2022.113460 DOI: https://doi.org/10.1016/j.lwt.2022.113460
Aschner JL, Aschner M. 2005. Nutritional aspects of manganese homeostasis. Mol Asp Med. 26:353-362.
https://doi.org/10.1016/j.mam.2005.07.003 DOI: https://doi.org/10.1016/j.mam.2005.07.003
Balzarini M, Bruno C, Córdoba M, Teich I. 2015. Herramientas en el Análisis Estadístico Multivariado. 1st ed. Córdoba (Argentina): Escuela Virtual Internacional CAVILA, Facultad de Ciencias Agropecuarias, Universidad Nacional de Córdoba. 200 p.
Baudin JP, Adam C, Garnier-LaPlace J. 2000. Dietary uptake, retention and tissue distribution of 54Mn, 60Co and 137Cs in the rainbow trout (Oncorhynchus mykiss Walbaum). Water Res. 34:2869-2878.
https://doi.org/10.1016/S0043-1354(99)00365-6 DOI: https://doi.org/10.1016/S0043-1354(99)00365-6
Block BA, Teo SLH, Walli A, Boustany A, Stokesbury MJW, Farwell CJ, Weng KC, Dewar H, Williams TD. 2005. Electronic tagging and population structure of Atlantic bluefin tuna. Nature. 434:1121-1127.
https://doi.org/10.1038/nature03463 DOI: https://doi.org/10.1038/nature03463
Boustany A, Reeb CA, Block BA. 2008. Mitochondrial DNA and electronic tracking reveal population structure of Atlantic bluefin tuna (Thunnus thynnus). Mar Biol. 156 (1):13-24.
https://doi.org/10.1007/s00227-008-1058-0 DOI: https://doi.org/10.1007/s00227-008-1058-0
Brucka-Jastrzêbska E, Kawczuga D, Rajkowska M, Protasowicki M. 2009. Levels of microelements (Cu, Zn, Fe) and macroelements (Mg, Ca) in freshwater fish. J Elem. 14(3): 437-447.
https://doi.org/10.5601/jelem.2009.14.3.02 DOI: https://doi.org/10.5601/jelem.2009.14.3.02
Bury N, Grosell M. 2003. Iron acquisition by teleost fish. Comp. Biochem Physiol C Toxicol Pharmaco. 135(2):97-105.
https://doi.org/10.1016/s1532-0456(03)00021-8 DOI: https://doi.org/10.1016/S1532-0456(03)00021-8
Bury NR, Walker PA, Glover CN. 2003. Nutritive metal uptake in teleost fish. J Exp Biol. 206(1):11-23.
https://doi.org/10.1242/jeb.00068 DOI: https://doi.org/10.1242/jeb.00068
Bustamante P, Teyssie JL, Fowler S, Cotret O, Danis B, Miramand P, Warnau M. 2002. Biokinetics of zinc and cadmium accumulation and depuration at different stages in the life cycle of the cuttlefish Sepia officinalis. Mar Ecol Prog Ser. 231:167-77.
https://doi.org/10.3354/meps231167 DOI: https://doi.org/10.3354/meps231167
Bustamante P, Teyssie JL, Danis B, Fowler S, Miramand P, Cotret O, Warnau M. 2004. Uptake, transfer and distribution of silver and cobalt in tissues of the common cuttlefish Sepia officinalis at different stages of its life cycle. Mar Ecol Prog Ser. 269:185-95.
https://doi.org/10.3354/meps269185 DOI: https://doi.org/10.3354/meps269185
Bustamante P, Teyssie J, Fowler S, Wamau M. 2006. Assessment of the exposure pathway in the uptake and distribution of americium and cesium in cuttlefish (Sepia officinalis) at different stages of its life cycle. J Exp Mar Biol Ecol. 331(2):198-207.
https://doi.org/10.1016/j.jembe.2005.10.018 DOI: https://doi.org/10.1016/j.jembe.2005.10.018
Campobasso F, Fanizzi A, Bello G, Santamaria N, Corriero A. 2017. A ‘machine learning’ technique for discriminating captive-reared from wild Atlantic bluefin tuna, Thunnus thynnus (Osteichthyes: Scombridae), based on differential fin spine bone resorption. Fish Res. 194:42-49.
https://doi.org/10.1016/j.fishres.2017.05.008 DOI: https://doi.org/10.1016/j.fishres.2017.05.008
Cubadda F, Raggi A, Coni. 2006. Element fingerprinting of marine organisms by dynamic reaction cell inductively coupled plasma mass spectrometry. Anal Bioanal Chem. 384(4):887-896.
https://doi.org/10.1007/s00216-005-0256-6 DOI: https://doi.org/10.1007/s00216-005-0256-6
Dabrowska H, Meyer-Burgdorff KH, Gunther KD. 1991. Magnesium status in freshwater fish, common carp (Cyprinus carpio, L.) and the dietary protein-magnesium interaction. Fish Physiol Biochem. 9:165-172.
https://doi.org/10.1007/BF02265132 DOI: https://doi.org/10.1007/BF02265132
De la Gándara F, Ortega A, Buentello A. 2016. Tuna Aquaculture in Europe. In: Benetti DD, Partridge GJ, Buentello A (eds.), Advances in Tuna Aquaculture. From hatchery to market. London (UK): Academic Press. p. 115-157.
https://doi.org/10.1016/B978-0-12-411459-3.00005-9 DOI: https://doi.org/10.1016/B978-0-12-411459-3.00005-9
Evans DH, Claiborne JB. 2009. Osmotic and ionic regulation in fishes. In: Evans DH (ed.), Osmotic and Ionic regulation: Cells and Animals. Boca Raton (USA): CRC Press. p. 295-366.
https://doi.org/10.1201/9780849380525-8 DOI: https://doi.org/10.1201/9780849380525-8
Fromentin JM. 2010. Tagging bluefin tuna in the Mediterranean Sea: challenge or mission impossible? Collect Vol Sci Pap. (1021-5212) (ICCAT). 65(3):812-821.
Grosell M. 2012. Copper. In: Wood CM, Farrell AM, Brauner CJ (eds.), Fish Physiology: Homeostasis and Toxicology of Essential Metals. Cambridge (UK): Academic Press. p. 53-133. DOI: https://doi.org/10.1016/S1546-5098(11)31002-3
Hogstrand C. 2012. Zinc. In: Wood CM, Farrell AM, Brauner CJ (eds.), Fish Physiology: Homeostasis and Toxicology of Essential Metals. Cambridge (MA): Academic Press. p. 135-200. DOI: https://doi.org/10.1016/S1546-5098(11)31003-5
Jara Z, Chodyniecki A. 1999. Ichtopatologia. 1st ed. Wroclaw (Poland): Agriculture University of Wroclaw. 478 p.
Kim SK, Jung, WK. 2007. Fish and bone as a calcium source. In: Shahidi F (eds.), Maximising the Value of Marine By-Products. Sawston (UK): Woodhead Publishing. p.328-339.
https://doi.org/10.1533/9781845692087.2.328 DOI: https://doi.org/10.1533/9781845692087.2.328
Kormarnisky LA, Christopherson RJ, Basu TK. 2003. Sulfur: its clinical and toxicological aspects. Nutrition. 19(1):54-61.
https://doi.org/10.1016/S0899-9007(02)00833-X DOI: https://doi.org/10.1016/S0899-9007(02)00833-X
Lall SP. 2003. The minerals. In: Halver JE, Hardy RW (eds.), Fish Nutrition. London (UK): Academic Press. p. 259-308. DOI: https://doi.org/10.1016/B978-012319652-1/50006-9
Lall SP, Kaushik SJ. 2021. Nutrition and metabolism of minerals in fish. Animals. 11(9):1-41.
https://doi.org/10.3390/ani11092711 DOI: https://doi.org/10.3390/ani11092711
Lara Jacobo L, Díaz F, Denisse Re A, Galindo C, Sánchez-Lizarraga AL, Nuñez-Moreno LA, Moreno-Sierra D. 2016. Physiological responses of the red rocky crab Cancer antennarius exposed to different concentrations of copper sulfate. Rev Biol Mar Oceanogr. 51(2):327-336. DOI: https://doi.org/10.4067/S0718-19572016000200010
Limburg KE, Wuenschel MJ, Hüssy K, Heimbrand Y, Samson M. 2018. Making the otolith magnesium chemical calendar-clock tick: plausible mechanism and empirical evidence. Rev Fisheries Sci Aquaculture. 26(4):479-493.
https://doi.org/10.1080/23308249.2018.1458817 DOI: https://doi.org/10.1080/23308249.2018.1458817
López-Álvarez M, Souto-Montero P, Durán S, Pérez-Davila S, Vázquez JA, González P, Serra J. 2024. Valuable Ca/P sources obtained from tuna species’ by-products derived from industrial processing: physicochemical and features of skeleton fractions. Recycling. 9(6):109.
https://doi.org/10.3390/recycling9060109 DOI: https://doi.org/10.3390/recycling9060109
Milatou N, Dassenakis M, Megalofonou P. 2015. Do fattening process and biological parameters affect the accumulation of metals in Atlantic bluefin tuna? Food Addit Contam Part A. 32 (7):1129-1139.
https://doi.org/10.1080/19440049.2015.1038855 DOI: https://doi.org/10.1080/19440049.2015.1038855
Miller DW, Vetter RJ, Atchison GJ. 1980. Effect of temperature and dissolved oxygen on uptake and retention of 54Mn in fish. Health Phys. 38(2):221-225.
Murthy LM, Rao BM, Asha KK, Prasad MM. 2014. Extraction and quality evaluation of yellowfin tuna bonepowder. Fish Technol. 51(1):38-42.
https://doi.org/10.56093/ft.v51i1.36907
National Research Council. 2011. Nutrient Requirements of Fish and Shrimp. 1st ed. Washington DC (USA): The National Academies Press. 392 p.
[OJEU] Official Journal of the European Union. 2010. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Brussels (Belgium): OJEU. Directive, no. L 276/33. 47 p.
https://eur-lex.europa.eu/eli/dir/2010/63/oj/eng
[OJEU] Official Journal of the European Union. 2016. Regulation (UE) 2016/1627 of the European Parliament and the Council of 14 September 2016 on a multiannual recovery plan for eastern Atlantic and Mediterranean bluefin tuna and repealing Council Regulation (EC) No 302/2009. Brussels (Belgium): OJEU. Regulation, no. L252:1. 52 p.
Ortega A, De la Gándara F. 2017. Closing the life cycle of the Atlantic bluefin tuna Thunnus thynnus in captivity. Proc Aquac Eur. 17:857- 858
Percın F, Sogut O, Altınelataman C, Soylak M. 2011. Some trace elements in front and rear dorsal ordinary muscles of wild and farmed bluefin tuna (Thunnus thynnus L. 1758) in the Turkish part of the eastern Mediterranean Sea. Food Chem Toxicol. 49(4):1006-1010.
https://doi.org/10.1016/j.fct.2011.01.007 DOI: https://doi.org/10.1016/j.fct.2011.01.007
Peterson RA. 2000. A meta-analysis of variance accounted for and factor loadings in exploratory factor analysis. Mark Lett. 11(3):261-275.
https://doi.org/10.1023/A:1008191211004 DOI: https://doi.org/10.1023/A:1008191211004
Poulet N, Reyjol Y, Collier H, Lek S. 2005. Does fish scale morphology allow the identification of population Leuciscus burdigalensis in river Viaur (SW France)? Aquat Sci. 67(1):122-127.
https://doi.org/10.1007/s00027-004-0772-z DOI: https://doi.org/10.1007/s00027-004-0772-z
Riccioni G, Landi M, Ferrara G, Milano I, Cariani A, Zane L, Sella M, Barbujani G, Tinti F. 2010. Spatio-temporal population structuring and genetic diversity retention in depleted Atlantic bluefin tuna of the Mediterranean Sea. Proc Nat Acad Sci. 107(5):2102-2107.
https://doi.org/10.1073/pnas.0908281107 DOI: https://doi.org/10.1073/pnas.0908281107
Rjeibi M, Metian M, Hajji T, Guyot T, Ben Chaouacha-Chekir R, Bustamante P. 2015. Seasonal survey of contaminants (Cd and Hg) and micronutrients (Cu and Zn) in edible tissues of cephalopods from Tunisia: assessment of risk and nutritional benefits. J Food Sci. 80(1):T199-206.
https://doi.org/10.1111/1750-3841.12711 DOI: https://doi.org/10.1111/1750-3841.12711
Rodríguez-Ezpeleta N, Díaz-Arce N, Walter III JF, Richardson DE, Rooker JR, Nøttestad L, Hanke AR, Franks JS, Deguara S, Lauretta MV, et al. 2019. Determining natal origin for improved management of Atlantic bluefin tuna. Front Ecol Environ. 17(8):439-444.
https://doi.org/10.1002/fee.2090 DOI: https://doi.org/10.1002/fee.2090
Rooker JR, Alvarado-Bremer JR, Block BA, Dewar H, De Metrio G, Corriero A, Kraus RT, Princes ED, Rodríguez-Marín E, Secor DH. 2007. Life History and stock structure of Atlantic bluefin tuna (Thunnus thynnus). Rev Fish Sci. 15(4):265-310.
https://doi.org/10.1080/10641260701484135 DOI: https://doi.org/10.1080/10641260701484135
Rouleau C, Tjalve H, Gottofrey J, Pelletier E. 1995. Uptake, distribution, and elimination of 54Mn (II) in brown trout (Salmo trutta). Environ Toxicol Chem. 14(3):483-490.
https://doi.org/10.1002/etc.5620140318 DOI: https://doi.org/10.1002/etc.5620140318
Salvat-Leal I, Ortega A, Blanco E, García J, Romero D. 2023. Elemental composition in soft tissues as a model for identifying batches of juvenile Atlantic bluefin tuna (Thunnus thynnus). J Food Compost Anal. 118:105-176.
https://doi.org/10.1016/j.jfca.2023.105176 DOI: https://doi.org/10.1016/j.jfca.2023.105176
Sarà G, Sarà R. 2007. Feeding habits and trophic levels of bluefin tuna Thunnus thynnus of different size classes in the Mediterranean Sea. J Appl Ichthyol. 23(2):122-127.
https://doi.org/10.1111/j.1439-0426.2006.00829.x DOI: https://doi.org/10.1111/j.1439-0426.2006.00829.x
Shearer KD, Åsgård T. 1992. The effect of water-borne magnesium on the dietary magnesium requirement of rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem. 9(5-6):387-392.
https://doi.org/10.1007/BF02274219 DOI: https://doi.org/10.1007/BF02274219
Shrestha N. 2021. Factor analysis as a tool for survey. Am J Appl Math Stat. 9(1):4-11
https://doi.org/10.12691/ajams-9-1-2 DOI: https://doi.org/10.12691/ajams-9-1-2
Siccardi AJ, Padgett-Vasquez S, Garris HW, Nagy TR, D’Abramo LR, Watts SA. 2010. Dietary strontium increases bone mineral density in intact zebrafish (Danio rerio): A potential model system for bone research. Zebrafish. 7:267-273.
https://doi.org/10.1089/zeb.2010.0654 DOI: https://doi.org/10.1089/zeb.2010.0654
Sinopoli M, Pipitone C, Campagnuolo S, Campo D, Castriota L, Mostarda E, Andaloro F. 2004. Diet of young-of-the-year bluefin tuna, Thunnus thynnus (Linnaeus, 1758), in the southern Tyrrenian (Mediterranean) Sea. J Appl Ichthyol. 20(4):310-313.
https://doi.org/10.1111/j.1439-0426.2004.00554.x DOI: https://doi.org/10.1111/j.1439-0426.2004.00554.x
Sogut O, Percin F. 2011. Trace elements in the kidney tissue of Bluefin Tuna (Thunnus thynnus L. 1758) in Turkish seas. Afr J Biotech. 10(7):1252-1259.
Sturrock AM, Hunter E, Milton JA, EIMF, Johnson RC, Waring CP, Trueman CN. 2015. Quantifying physiological influences on otolith microchemistry. Met Ecol Evol. 6(7):806-816.
https://doi.org/10.1111/2041-210X.12381 DOI: https://doi.org/10.1111/2041-210X.12381
Talib A, Hariati AM, Nurhidayati F. 2020. The mineral content and vitamin d on bone flour fish yellowfin tuna. J Phys Conf Ser 1517:012042
https://doi.org/10.1088/1742-6596/1517/1/012042 DOI: https://doi.org/10.1088/1742-6596/1517/1/012042
Taylor LN, Wood CM, McDonald G. 2003. An evaluation of sodium loss and gill metal binding properties in rainbow trout and yellow perch to explain species differences in copper tolerance. Environ Toxicol Chem. 22(9):2159-2166.
https://doi.org/10.1897/02-256 DOI: https://doi.org/10.1897/02-256
Torrado-Fonseca M, Berlanga-Silvente V. 2013. Análisis Discriminante mediante SPSS. Rev d’Innov Recer Educ. 6(2):150-166.
Tulli F, Moreno-Rojas JM, Messina CM, Trocino A, Xiccato G, Muñoz-Redondo JM, Santulli A, Tibaldi E. 2020. The use of stable isotope ratio analysis to trace European sea bass (D. labrax) originating from different farming systems. Animals. 10(11): 20-42.
https://doi.org/10.3390/ani10112042 DOI: https://doi.org/10.3390/ani10112042
[UNE] Asociación Española de Normalización (2010). UNE-EN ISO 11885: Calidad del agua. Determinación de elementos seleccionados por espectrometría de emisión óptica con plasma acoplado inductivamente (ICP-OES). Spanish written standard. 33 p.
Uotani I, Saito T, Hiranuma K, Nishikawa Y. (1990). Feeding habit of bluefin tuna Thunnus thynnus larvae in the western North Pacific Ocean. Nippon Suisan Gakkaishi. 56(5):713-717.
https://doi.org/10.2331/suisan.56.713 DOI: https://doi.org/10.2331/suisan.56.713
Vizzini S, Tramati C, Mazzola A. 2010. Comparison of stable isotope composition and inorganic and organic contaminant levels in wild and farmed bluefin tuna, Thunnus thynnus, in the Mediterranean Sea. Chemosphere. 78(10):1236-1243.
https://doi.org/10.1016/j.chemosphere.2009.12.041 DOI: https://doi.org/10.1016/j.chemosphere.2009.12.041
Walther BD, Limburg KE. 2012. The use of otolith chemistry to characterize diadromous migrations. J Fish Biol. 81(2):796-825.
https://doi.org/10.1111/j.1095-8649.2012.03371.x DOI: https://doi.org/10.1111/j.1095-8649.2012.03371.x
Warren-Myers F, Dempster T, Fjelldal PG, Hansen T, Swearer SE. 2015. An industry-scale mass marking technique for tracing farmed fish escapees. PLoS ONE. 10:e0118594
https://doi.org/10.1371/journal.pone.0118594 DOI: https://doi.org/10.1371/journal.pone.0118594
Yakubu A, Okunsebor SA. 2011. Morphometric differentiation of two Nigerian fish species (Oreochromis niloticus and Lates niloticus) using principal components and discriminant analysis. Int J Morphol. 29(4):1429-1434.
https://doi.org/10.4067/s0717-95022011000400060 DOI: https://doi.org/10.4067/S0717-95022011000400060
Zimmer AM, Brix KV, Wood CM. 2019. Mechanisms of Ca2+ uptake in freshwater and seawater-acclimated killifish, Fundulus heteroclitus, and their response to acute salinity transfer. J Comp Physiol B. 189:47-60.
https://doi.org/10.1007/s00360-018-1192-z DOI: https://doi.org/10.1007/s00360-018-1192-z