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RESEARCH ARTICLE (Open Access)

Otolith microchemistry: a useful tool for investigating stock structure of yellowfin tuna (Thunnus albacares) in the Indian Ocean

Iraide Artetxe-Arrate https://orcid.org/0000-0001-9314-6479 A E , Igaratza Fraile A , David A. Crook B , Iker Zudaire A , Haritz Arrizabalaga A , Alan Greig C and Hilario Murua A D
+ Author Affiliations
- Author Affiliations

A AZTI Tecnalia, Marine Research Division, Herrea Kaia, Portualdea s/n, E-20110 Pasaia, Gipuzkoa, Spain.

B Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia.

C School of Earth Sciences, The University of Melbourne, Vic. 3010, Australia.

D International Seafood Sustainability Foundation, 1440 G Street NW, Washington, DC 20005, USA.

E Corresponding author. Email: i.artetxe73@gmail.com

Marine and Freshwater Research 70(12) 1708-1721 https://doi.org/10.1071/MF19067
Submitted: 22 June 2018  Accepted: 7 October 2019   Published: 12 November 2019

Journal Compilation © CSIRO 2019 Open Access CC BY-NC-ND

Abstract

A better understanding of the stock structure of yellowfin tuna (Thunnus albacares) in the Indian Ocean is needed to ensure the sustainable management of the fishery. In this study, carbon and oxygen stable isotopes (δ13C and δ18O) and trace elements (138Ba, 55Mn, 25Mg and 88Sr) were measured in otoliths of young-of-the-year (YOY) and age-1 yellowfin tuna collected from the Mozambique Channel and north-west Indian Ocean regions. Elemental profiles showed variation in Ba, Mg and Mn in YOY otolith composition, but only Mn profiles differed between regions. Differences in YOY near-core chemistry were used for natal-origin investigation. Ba, Mg and Mn were sufficiently different to discriminate individuals from the two regions, in contrast with carbon and oxygen stable isotopes. A linear discriminant analysis resulted in 80% correct classification of yellowfin tuna to their natal origin. Classification success increased to 91% using a random forest algorithm. Finally, a unique larval source was detected among age-1 yellowfin tuna. The signal of these fish resembled that of YOY from a north-west Indian Ocean origin, highlighting the importance of local production. The present study supports the use of otolith chemistry as a promising approach to analyse yellowfin stock structure in the Indian Ocean.


References

Abaunza, P., Murta, A. G., Campbell, N., Cimmaruta, R., Comesaña, A. S., Dahle, G., García Santamaría, M. T., Gordo, L. S., Iversen, S. A., MacKenzie, K., Magoulas, A., Mattiucci, S., Molloy, J., Nascetti, G., Pinto, A. L., Quinta, R., Ramos, P., Sanjuan, A., Santos, A. T., Stransky, C., and Zimmermann, C. (2008). Stock identity of horse mackerel (Trachurus trachurus) in the northeast Atlantic and Mediterranean Sea: integrating the results from different stock identification approaches. Fisheries Research 89, 196–209.
Stock identity of horse mackerel (Trachurus trachurus) in the northeast Atlantic and Mediterranean Sea: integrating the results from different stock identification approaches.Crossref | GoogleScholarGoogle Scholar |

Arai, T., Kotake, A., and Kayama, S. (2005). Movements and life history patterns of the skipjack tuna Katsuwonus pelamis in the western Pacific, as revealed by otolith Sr : Ca ratios. Journal of the Marine Biological Association of the United Kingdom 85, 1211–1216.
Movements and life history patterns of the skipjack tuna Katsuwonus pelamis in the western Pacific, as revealed by otolith Sr : Ca ratios.Crossref | GoogleScholarGoogle Scholar |

Bath Martin, G., and Thorrold, S. R. (2005). Temperature and salinity effects on magnesium, manganese, and barium incorporation in otoliths of larval and early juvenile spot Leiostomus xanthurus. Marine Ecology Progress Series 293, 223–232.
Temperature and salinity effects on magnesium, manganese, and barium incorporation in otoliths of larval and early juvenile spot Leiostomus xanthurus.Crossref | GoogleScholarGoogle Scholar |

Begg, G., Friedland, K., and Pearce, J. (1999). Stock identification and its role in stock assessment and fisheries management: an overview. Fisheries Research 43, 1–8.
Stock identification and its role in stock assessment and fisheries management: an overview.Crossref | GoogleScholarGoogle Scholar |

Bouchoucha, M., Pécheyran, C., Gonzalez, J., Lenfant, P., and Darnaude, A. M. (2018). Otolith fingerprints as natural tags to identify juvenile fish life in ports. Estuarine, Coastal and Shelf Science 212, 210–218.
Otolith fingerprints as natural tags to identify juvenile fish life in ports.Crossref | GoogleScholarGoogle Scholar |

Breiman, L. (2001). Random forests. Machine Learning 45, 5–32.
Random forests.Crossref | GoogleScholarGoogle Scholar |

Campana, S., and Neilson, J. (1985). Microstructure of fish otoliths. Canadian Journal of Fisheries and Aquatic Sciences 42, 1014–1032.
Microstructure of fish otoliths.Crossref | GoogleScholarGoogle Scholar |

Campbell, J. L., Babaluk, J. A., Cooper, M., Grime, G. W., Halden, N. M., Nejedly, Z., Rajta, I., and Reist, J. D. (2002). Strontium distribution in young-of-the-year Dolly Varden otoliths: potential for stock discrimination. Nuclear Instruments & Methods in Physics Research – B. Beam Interactions with Materials and Atoms 189, 185–189.
Strontium distribution in young-of-the-year Dolly Varden otoliths: potential for stock discrimination.Crossref | GoogleScholarGoogle Scholar |

Clarke, L. M., Thorrold, S. R., and Conover, D. O. (2011). Population differences in otolith chemistry have a genetic basis in Menidia menidia. Canadian Journal of Fisheries and Aquatic Sciences 68, 105–114.
Population differences in otolith chemistry have a genetic basis in Menidia menidia.Crossref | GoogleScholarGoogle Scholar |

Craig, C. A., Jarvis, K. E., and Clarke, L. J. (2000). An assessment of calibration strategies for the quantitative and semi-quantitative analysis of calcium carbonate matrices by laser ablation–inductively coupled plasma–mass spectrometry (LA-ICP-MS). Journal of Analytical Atomic Spectrometry 15, 1001–1008.
An assessment of calibration strategies for the quantitative and semi-quantitative analysis of calcium carbonate matrices by laser ablation–inductively coupled plasma–mass spectrometry (LA-ICP-MS).Crossref | GoogleScholarGoogle Scholar |

Cutler, D. R., Edwards, T. C., Beard, K. H., Cutler, A., Hess, T. K., Gibson, J., and Lawler, J. J. (2007). Random forests for classification in ecology. Ecology 88, 2783–2792.
Random forests for classification in ecology.Crossref | GoogleScholarGoogle Scholar | 18051647PubMed |

Dammannagoda, S., Hurwood, D., and Mather, P. (2008). Evidence for fine geographical scale heterogeneity in gene frequencies in yellowfin tuna (Thunnus albacares) from the north Indian Ocean around Sri Lanka. Fisheries Research 90, 147–157.
Evidence for fine geographical scale heterogeneity in gene frequencies in yellowfin tuna (Thunnus albacares) from the north Indian Ocean around Sri Lanka.Crossref | GoogleScholarGoogle Scholar |

Daszykowski, M., Kaczmarek, K., Vander Heyden, Y., and Walczak, B. (2007). Robust statistics in data analysis – a review: basic concepts. Chemometrics and Intelligent Laboratory Systems 85, 203–219.
Robust statistics in data analysis – a review: basic concepts.Crossref | GoogleScholarGoogle Scholar |

Di Franco, A., Bulleri, F., Pennetta, A., De Benedetto, G., Clarke, K. R., and Guidetti, P. (2014). Within-otolith variability in chemical fingerprints: implications for sampling designs and possible environmental interpretation. PLoS One 9, e101701.
Within-otolith variability in chemical fingerprints: implications for sampling designs and possible environmental interpretation.Crossref | GoogleScholarGoogle Scholar | 25000202PubMed |

Elsdon, T., and Gillanders, B. (2004). Fish otolith chemistry influenced by exposure to multiple environmental variables. Journal of Experimental Marine Biology and Ecology 313, 269–284.
Fish otolith chemistry influenced by exposure to multiple environmental variables.Crossref | GoogleScholarGoogle Scholar |

Elsdon, T., and Gillanders, B. (2005). Alternative life-history patterns of estuarine fish: barium in otoliths elucidates freshwater residency. Canadian Journal of Fisheries and Aquatic Sciences 62, 1143–1152.
Alternative life-history patterns of estuarine fish: barium in otoliths elucidates freshwater residency.Crossref | GoogleScholarGoogle Scholar |

Elsdon, T. S., Wells, B. K., Campana, S. E., Gillanders, B. M., Jones, C. M., Limburg, K. E., and Walther, B. D. (2008). Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations and inferences. Oceanography and Marine Biology – an Annual Review 46, 297–330.
Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations and inferences.Crossref | GoogleScholarGoogle Scholar |

Erceg-Hurn, D., and Mirosevich, V. M. (2008). Modern robust statistical methods: an easy way to maximize the accuracy and power of your research. The American Psychologist 63, 591–601.
Modern robust statistical methods: an easy way to maximize the accuracy and power of your research.Crossref | GoogleScholarGoogle Scholar | 18855490PubMed |

Fielding, A. H., and Bell, J. F. (1997). A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation 24, 38–49.
A review of methods for the assessment of prediction errors in conservation presence/absence models.Crossref | GoogleScholarGoogle Scholar |

Fonteneau, A., and Hallier, J. P. (2015). Fifty years of dart tag recoveries for tropical tuna: a global comparison of results for the western Pacific, eastern Pacific, Atlantic, and Indian Oceans. Fisheries Research 163, 7–22.
Fifty years of dart tag recoveries for tropical tuna: a global comparison of results for the western Pacific, eastern Pacific, Atlantic, and Indian Oceans.Crossref | GoogleScholarGoogle Scholar |

Food and Agriculture Organization of the United Nations (2016). ‘The State of World Fisheries and Aquaculture 2016. Contributing to Food Security and Nutrition for All.’ (FAO: Rome, Italy.)

Fowler, A., Hamer, P., and Kemp, J. (2017). Age-related otolith chemistry profiles help resolve demographics and meta-population structure of a widely dispersed, coastal fishery species. Fisheries Research 189, 77–94.
Age-related otolith chemistry profiles help resolve demographics and meta-population structure of a widely dispersed, coastal fishery species.Crossref | GoogleScholarGoogle Scholar |

Fraile, I., Arrizabalaga, H., Santiago, J., Goñi, N., Arregi, I., Madinabeitia, S., Wells, R. J. D., and Rooker, J. R. (2016). Otolith chemistry as an indicator of movements of albacore (Thunnus alalunga) in the North Atlantic Ocean. Marine and Freshwater Research 67, 1002–1013.
Otolith chemistry as an indicator of movements of albacore (Thunnus alalunga) in the North Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |

Froese, R., and Pauly, D. (1999). Thunnus albacares (Bonnaterre, 1788): Yellowfin tuna. Available at https://www.fishbase.de/summary/Thunnus-albacares.html [Verified 22 October 2019].

Galland, G., Rogers, A., and Nickson, A. (2016). Netting billions: a global valuation of tuna. The Pew Charitable Trust, Washington, DC, USA.

Gibb, F., Régnier, T., Donald, K., and Wright, P. (2017). Connectivity in the early life history of sandeel inferred from otolith microchemistry. Journal of Sea Research 119, 8–16.
Connectivity in the early life history of sandeel inferred from otolith microchemistry.Crossref | GoogleScholarGoogle Scholar |

Hallier, J., and Fonteneau, A. (2015). Tuna aggregation and movement from tagging data: a tuna ‘hub’ in the Indian Ocean. Fisheries Research 163, 34–43.
Tuna aggregation and movement from tagging data: a tuna ‘hub’ in the Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Hallier, J., and Million, J. (2012). The Indian Ocean tuna tagging programme. In ‘Indian Ocean Tuna Tagging Symposium’, 30 October–2 November 2012, Mauritius. pp. 1–36. (Indian Ocean Tuna Commission.) Available at https://www.iotc.org/node/4332 [Verified 22 October 2019].

Hamer, P., and Jenkins, G. P. (2007). Comparison of spatial variation in otolith chemistry of two fish species and relationships with water chemistry and otolith growth. Journal of Fish Biology 71, 1035–1055.
Comparison of spatial variation in otolith chemistry of two fish species and relationships with water chemistry and otolith growth.Crossref | GoogleScholarGoogle Scholar |

Hamer, P. A., Jenkins, G. P., and Gillanders, B. M. (2005). Chemical tags in otoliths indicate the importance of local and distant settlement areas to populations of a temperate sparid, Pagrus auratus. Canadian Journal of Fisheries and Aquatic Sciences 62, 623–630.
Chemical tags in otoliths indicate the importance of local and distant settlement areas to populations of a temperate sparid, Pagrus auratus.Crossref | GoogleScholarGoogle Scholar |

Hout, M. C., Papesh, M. H., and Goldinger, S. D. (2013). Multidimensional scaling. Wiley Interdisciplinary Reviews: Cognitive Science 4, 93–103.
Multidimensional scaling.Crossref | GoogleScholarGoogle Scholar | 23359318PubMed |

Indian Ocean Tuna Commission (2017a). Status of the Indian Ocean yellowfin tuna (YFT: Thunnus albacares) resource. Available at https://www.iotc.org/sites/default/files/documents/science/species_summaries/english/Yellowfin2018.pdf [Verified 22 October 2019].

Indian Ocean Tuna Commission (2017b). Yellowfin tuna supporting information. Available at https://www.iotc.org/sites/default/files/documents/science/species_summaries/english/Yellowfin_tuna_Supporting_information.pdf [Verified 22 October 2019].

Indian Ocean Tuna Commission (2018). Nominal catch by species and gear, by vessel flag reporting country. IOTC-2018-DATASETS-NCDB. Available at http://www.iotc.org/documents/nominal-catch-species-and-gear-vessel-flag-reporting-country [Verified 1 November 2018].

International Seafood Sustainability Foundation (2017). Status of the world fisheries for tuna: November 2017. ISSF Technical Report 2017–02A, ISSF, Washington, DC, USA.

Izzo, C., Doubleday, Z., and Gillanders, B. (2016). Where do elements bind within the otoliths of fish? Marine and Freshwater Research 67, 1072–1076.
Where do elements bind within the otoliths of fish?Crossref | GoogleScholarGoogle Scholar |

Izzo, C., Reis-Santos, P., and Gillanders, B. M. (2018). Otolith chemistry does not just reflect environmental conditions: a meta-analytic evaluation. Fish and Fisheries 19, 441–454.
Otolith chemistry does not just reflect environmental conditions: a meta-analytic evaluation.Crossref | GoogleScholarGoogle Scholar |

Jones, C. M., Palmer, M., and Schaffler, J. J. (2017). Beyond Zar: the use and abuse of classification statistics for otolith chemistry. Journal of Fish Biology 90, 492–504.
Beyond Zar: the use and abuse of classification statistics for otolith chemistry.Crossref | GoogleScholarGoogle Scholar | 27325371PubMed |

Kaji, T., Tanaka, M., Oka, M., Takeuchi, H., Ohsumi, S., Teruya, K., and Hirokawa, J. (1999). Growth and morphological development of laboratory-reared yellowfin tuna Thunnus albacares larvae and early juveniles, with special emphasis on the digestive system. Fisheries Science 65, 700–707.
Growth and morphological development of laboratory-reared yellowfin tuna Thunnus albacares larvae and early juveniles, with special emphasis on the digestive system.Crossref | GoogleScholarGoogle Scholar |

Kerr, L., and Campana, S. (2014). Chemical composition of fish hard parts as a natural marker of fish stocks. In ‘Stock Identification Methods: Applications in Fishery Science’, 2nd edn. (Eds S. Cadrin, L. Kerr, and S. Mariani.) pp. 205–234. (Academic Press: Waltham, MA, USA.)

Kerr, L., Hintzen, N., and Cadrin, S. (2017). Lessons learned from practical approaches to reconcile mismatches between biological population structure and stock units of marine fish. ICES Journal of Marine Science 74, 1708–1722.
Lessons learned from practical approaches to reconcile mismatches between biological population structure and stock units of marine fish.Crossref | GoogleScholarGoogle Scholar |

Kingsford, M. J., Hughes, J. M., and Patterson, H. M. (2009). Otolith chemistry of the non-dispersing reef fish Acanthochromis polyacanthus: cross-shelf patterns from the central Great Barrier Reef. Marine Ecology Progress Series 377, 279–288.
Otolith chemistry of the non-dispersing reef fish Acanthochromis polyacanthus: cross-shelf patterns from the central Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |

Kitchens, L., Rooker, J., Reynal, L., Falterman, B., Saillant, E., and Murua, H. (2018). Discriminating among yellowfin tuna Thunnus albacares nursery areas in the Atlantic Ocean using otolith chemistry. Marine Ecology Progress Series 603, 201–213.
Discriminating among yellowfin tuna Thunnus albacares nursery areas in the Atlantic Ocean using otolith chemistry.Crossref | GoogleScholarGoogle Scholar |

Kunal, S., Kumar, G., Menezes, M., and Meena, R. (2013). Mitochondrial DNA analysis reveals three stocks of yellowfin tuna Thunnus albacares (Bonnaterre, 1788) in Indian waters. Conservation Genetics 14, 205–213.
Mitochondrial DNA analysis reveals three stocks of yellowfin tuna Thunnus albacares (Bonnaterre, 1788) in Indian waters.Crossref | GoogleScholarGoogle Scholar |

Lamont, T., Barlow, R., Morris, T., and van den Berg, M. (2014). Characterisation of mesoscale features and phytoplankton variability in the Mozambique Channel. Deep-sea Research – II. Topical Studies in Oceanography 100, 94–105.
Characterisation of mesoscale features and phytoplankton variability in the Mozambique Channel.Crossref | GoogleScholarGoogle Scholar |

LeGrande, A. N., and Schmidt, G. A. (2006). Global gridded data set of the oxygen isotopic composition in seawater. Geophysical Research Letters 33, L12604.
Global gridded data set of the oxygen isotopic composition in seawater.Crossref | GoogleScholarGoogle Scholar |

Liaw, A., and Wiener, M. (2002). Classification and regression by randomForest. R News 2, 18–22.

Limburg, K. E., and Casini, M. (2018). Effect of marine hypoxia on Baltic sea cod Gadus morhua: evidence from otolith chemical proxies. Frontiers in Marine Science 5, 482.
Effect of marine hypoxia on Baltic sea cod Gadus morhua: evidence from otolith chemical proxies.Crossref | GoogleScholarGoogle Scholar |

Limburg, K., Olson, C., Walther, Y., Dale, D., Slomp, C. P., and Høie, H. (2011). Tracking Baltic hypoxia and cod migration over millennia with natural tags. Proceedings of the National Academy of Sciences of the United States of America 108, E177–E182.
Tracking Baltic hypoxia and cod migration over millennia with natural tags.Crossref | GoogleScholarGoogle Scholar | 21518871PubMed |

Limburg, K. E., Walther, B. D., Lu, Z., Jackman, G., Mohan, J., Walther, Y., Nissling, A., Weber, P. K., and Schmitt, A. K. (2015). In search of the dead zone: use of otoliths for tracking fish exposure to hypoxia. Journal of Marine Systems 141, 167–178.
In search of the dead zone: use of otoliths for tracking fish exposure to hypoxia.Crossref | GoogleScholarGoogle Scholar |

Limburg, K. E., Wuenschel, M. J., Hüssy, K., Heimbrand, Y., and Samson, M. (2018). Making the otolith magnesium chemical calendar-clock tick: plausible mechanism and empirical evidence. Reviews in Fisheries Science & Aquaculture 26, 479–493.
Making the otolith magnesium chemical calendar-clock tick: plausible mechanism and empirical evidence.Crossref | GoogleScholarGoogle Scholar |

Loewen, T., Carriere, B., Reist, J., Halden, N., and Anderson, W. (2016). Linking physiology and biomineralization processes to ecological inferences on the life history of fishes. Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 202, 123–140.
Linking physiology and biomineralization processes to ecological inferences on the life history of fishes.Crossref | GoogleScholarGoogle Scholar |

Longhurst, A. R. (2007). The Indian Ocean. In ‘Ecological Geography of the Sea’, 2nd edn. pp. 275–320. (Academic Press: San Diego, CA, USA)

Ludsin, S., Fryer, B., and Gagnon, J. (2006). Comparison of solution-based versus laser ablation inductively coupled plasma mass spectrometry for analysis of larval fish otolith microelemental composition. Transactions of the American Fisheries Society 135, 218–231.
Comparison of solution-based versus laser ablation inductively coupled plasma mass spectrometry for analysis of larval fish otolith microelemental composition.Crossref | GoogleScholarGoogle Scholar |

Macdonald, J. I., and Crook, D. (2010). Variability in Sr : Ca and Ba : Ca ratios in water and fish otoliths across an estuarine salinity gradient. Marine Ecology Progress Series 413, 147–161.
Variability in Sr : Ca and Ba : Ca ratios in water and fish otoliths across an estuarine salinity gradient.Crossref | GoogleScholarGoogle Scholar |

Macdonald, J. I., Shelley, J. M., and Crook, D. A. (2008). A method for improving the estimation of natal chemical signatures in otoliths. Transactions of the American Fisheries Society 137, 1674–1682.
A method for improving the estimation of natal chemical signatures in otoliths.Crossref | GoogleScholarGoogle Scholar |

Macdonald, J. I., Farley, J. H., Clear, N. P., Williams, A. J., Carter, T. I., Davies, C. R., and Nicol, S. J. (2013). Insights into mixing and movement of South Pacific albacore Thunnus alalunga derived from trace elements in otoliths. Fisheries Research 148, 56–63.
Insights into mixing and movement of South Pacific albacore Thunnus alalunga derived from trace elements in otoliths.Crossref | GoogleScholarGoogle Scholar |

McCreary, J., Yu, Z., Hood, R., Vinaychandranc, P. N., Furuea, R., Ishido, A., and Richards, K. (2013). Dynamics of the Indian-Ocean oxygen minimum zones. Progress in Oceanography 112–113, 15–37.
Dynamics of the Indian-Ocean oxygen minimum zones.Crossref | GoogleScholarGoogle Scholar |

Mercier, L., Darnaude, A. M., Bruguier, O., Vasconcelos, R. P., Cabral, H. N., Costa, M. J., Lara, M., Jones, D. L., and Mouillot, D. (2011). Selecting statistical models and variable combinations for optimal classification using otolith microchemistry. Ecological Applications 21, 1352–1364.
Selecting statistical models and variable combinations for optimal classification using otolith microchemistry.Crossref | GoogleScholarGoogle Scholar | 21774435PubMed |

Olden, J. D., Joy, M. K., and Death, R. (2004). An accurate comparison of methods for quantifying variable importance in artificial neural networks using simulated data. Ecological Modelling 178, 389–397.
An accurate comparison of methods for quantifying variable importance in artificial neural networks using simulated data.Crossref | GoogleScholarGoogle Scholar |

Paton, C., Hellstrom, J., Paul, B., Woodhead, J., and Hergt, J. (2011). Iolite: freeware for the visualization and processing of mass spectrometric data. Journal of Analytical Atomic Spectrometry 26, 2508–2518.
Iolite: freeware for the visualization and processing of mass spectrometric data.Crossref | GoogleScholarGoogle Scholar |

Patterson, H., Kingsford, M., and McCulloch, M. (2004). The influence of oceanic and lagoonal plume waters on otolith chemistry. Canadian Journal of Fisheries and Aquatic Sciences 61, 898–904.
The influence of oceanic and lagoonal plume waters on otolith chemistry.Crossref | GoogleScholarGoogle Scholar |

Paul, B., Paton, C., Norris, A., Woodhead, J., Hellstrom, J., Hergt, J., and Greig, A. (2012). CellSpace: a module for creating spatially registered laser ablation images within the Iolite freeware environment. Journal of Analytical Atomic Spectrometry 27, 700–706.
CellSpace: a module for creating spatially registered laser ablation images within the Iolite freeware environment.Crossref | GoogleScholarGoogle Scholar |

Pecoraro, C., Babbucci, M., Franch, R., Rico, C., Papetti, C., Chassot, E., Bodin, N., Cariani, A., Bargelloni, L., and Tinti, F. (2018). The population genomics of yellowfin tuna (Thunnus albacares) at global geographic scale challenges current stock delineation. Scientific Reports 8, 13890.
The population genomics of yellowfin tuna (Thunnus albacares) at global geographic scale challenges current stock delineation.Crossref | GoogleScholarGoogle Scholar | 30224658PubMed |

Pita, A., Casey, J., Hawkins, S. J., Villarreal, M. R., Gutiérrez, M. J., Cabral, H., Carocci, F., Abaunza, P., Pascual, S., and Presa, P. (2016). Conceptual and practical advances in fish stock delineation. Fisheries Research 173, 185–193.
Conceptual and practical advances in fish stock delineation.Crossref | GoogleScholarGoogle Scholar |

Quartly, G., and Srokosz, M. (2004). Eddies in the southern Mozambique Channel. Deep-sea Research – II. Topical Studies in Oceanography 51, 69–83.
Eddies in the southern Mozambique Channel.Crossref | GoogleScholarGoogle Scholar |

Ranaldi, M., and Gagnon, M. (2008). Zinc incorporation in the otoliths of juvenile pink snapper (Pagrus auratus, Forster): the influence of dietary versus waterborne sources. Journal of Experimental Marine Biology and Ecology 360, 56–62.
Zinc incorporation in the otoliths of juvenile pink snapper (Pagrus auratus, Forster): the influence of dietary versus waterborne sources.Crossref | GoogleScholarGoogle Scholar |

Reglero, P., Tittensor, D., Álvarez-Berastegui, D., Aparicio-González, A., and Worm, B. (2014). Worldwide distributions of tuna larvae: revisiting hypotheses on environmental requirements for spawning habitats. Marine Ecology Progress Series 501, 207–224.
Worldwide distributions of tuna larvae: revisiting hypotheses on environmental requirements for spawning habitats.Crossref | GoogleScholarGoogle Scholar |

Régnier, T., Augley, J., Devalla, S., Robinson, C., Wrigth, P., and Neat, F. (2017). Otolith chemistry reveals seamount fidelity in a deepwater fish. Deep-sea Research – I. Oceanographic Research Papers 121, 183–189.
Otolith chemistry reveals seamount fidelity in a deepwater fish.Crossref | GoogleScholarGoogle Scholar |

Reiss, H., Hoarau, G., Dickey-Collas, M., and Wolff, W. J. (2009). Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish and Fisheries 10, 361–395.
Genetic population structure of marine fish: mismatch between biological and fisheries management units.Crossref | GoogleScholarGoogle Scholar |

Rooker, J. R., Zdanowicz, V., and Secor, D. (2001). Chemistry of tuna otoliths: assessment of base composition and postmortem handling effects. Marine Biology 139, 35–43.
Chemistry of tuna otoliths: assessment of base composition and postmortem handling effects.Crossref | GoogleScholarGoogle Scholar |

Rooker, J. R., Secor, D. H., Zdanowicz, V. S., De Metrio, G., and Relini, L. O. (2003). Identification of Atlantic bluefin tuna (Thunnus thynnus) stocks from putative nurseries using otolith chemistry. Fisheries Oceanography 12, 75–84.
Identification of Atlantic bluefin tuna (Thunnus thynnus) stocks from putative nurseries using otolith chemistry.Crossref | GoogleScholarGoogle Scholar |

Rooker, J. R., Secor, D. H., DeMetrio, G., Kaufman, A. J., Ríos, A. B., and Tičina, V. (2008a). Evidence of trans-Atlantic movement and natal homing of bluefin tuna from stable isotopes in otoliths. Marine Ecology Progress Series 368, 231–239.
Evidence of trans-Atlantic movement and natal homing of bluefin tuna from stable isotopes in otoliths.Crossref | GoogleScholarGoogle Scholar |

Rooker, J., Secor, D., DeMetrio, G., Schloesser, R., Block, B., and Neilson, J. (2008b). Natal homing and connectivity in Atlantic bluefin tuna populations. Science 322, 742–744.
Natal homing and connectivity in Atlantic bluefin tuna populations.Crossref | GoogleScholarGoogle Scholar | 18832611PubMed |

Rooker, J. R., David Wells, R. J., Itano, D. G., Thorrold, S. R., and Lee, J. M. (2016). Natal origin and population connectivity of bigeye and yellowfin tuna in the Pacific Ocean. Fisheries Oceanography 25, 277–291.
Natal origin and population connectivity of bigeye and yellowfin tuna in the Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Ruttenberg, B., Hamilton, S., and Hickford, M. (2005). Elevated levels of trace elements in cores of otoliths and their potential for use as natural tags. Marine Ecology Progress Series 297, 273–281.
Elevated levels of trace elements in cores of otoliths and their potential for use as natural tags.Crossref | GoogleScholarGoogle Scholar |

Sardenne, F., Dortel, E., Le Croizier, G., and Million, J. (2015). Determining the age of tropical tunas in the Indian Ocean from otolith microstructures. Fisheries 163, 44–57.
Determining the age of tropical tunas in the Indian Ocean from otolith microstructures.Crossref | GoogleScholarGoogle Scholar |

Schott, F., and McCreary, J. (2001). The monsoon circulation of the Indian Ocean. Progress in Oceanography 51, 1–123.
The monsoon circulation of the Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Shi, T., and Horvath, S. (2006). Unsupervised learning with random forest predictors. Journal of Computational and Graphical Statistics 15, 118–138.
Unsupervised learning with random forest predictors.Crossref | GoogleScholarGoogle Scholar |

Shiao, J., Wang, S., Yokawa, K., Ichinokawa, M., Takeuchi, Y., Chen, Y., and Shen, C. (2010). Natal origin of Pacific bluefin tuna Thunnus orientalis inferred from otolith oxygen isotope composition. Marine Ecology Progress Series 420, 207–219.
Natal origin of Pacific bluefin tuna Thunnus orientalis inferred from otolith oxygen isotope composition.Crossref | GoogleScholarGoogle Scholar |

Shuford, R. L., Dean, J. M., Stéquert, B., and LaBonne, M. (2007). Elemental fingerprints in otoliths of juvenile yellowfin tuna from spawning grounds in the Atlantic Ocean. Collective Volume of Scientific Papers ICCAT 60, 314–329.

Stepien, C. A. (1995). Population genetic divergence and geographic patterns from DNA sequences: examples from marine and freshwater fishes. American Fisheries Society Symposium 17, 263–287.

Sturrock, A. M., Hunter, E., Milton, J. A., Johnson, R. C., Waring, C. P., and Trueman, C. N. (2015). Quantifying physiological influences on otolith microchemistry. Methods in Ecology and Evolution 6, 806–816.
Quantifying physiological influences on otolith microchemistry.Crossref | GoogleScholarGoogle Scholar |

Taillebois, L., Barton, D. P., Crook, D. A., Saunders, T., Taylor, J., Hearnden, M., Saunders, R. J., Newman, S. J., Travers, M. J., Welch, D. J., Greig, A., Dudgeon, C., Maher, S., and Ovenden, J. R. (2017). Strong population structure deduced from genetics, otolith chemistry and parasite abundances explains vulnerability to localized fishery collapse in a large Sciaenid fish, Protonibea diacanthus. Evolutionary Applications 10, 978–993.
Strong population structure deduced from genetics, otolith chemistry and parasite abundances explains vulnerability to localized fishery collapse in a large Sciaenid fish, Protonibea diacanthus.Crossref | GoogleScholarGoogle Scholar | 29151854PubMed |

Tanner, S., Reis-Santos, P., and Cabral, H. (2016). Otolith chemistry in stock delineation: a brief overview, current challenges and future prospects. Fisheries Research 173, 206–213.
Otolith chemistry in stock delineation: a brief overview, current challenges and future prospects.Crossref | GoogleScholarGoogle Scholar |

Tew Kai, E., and Marsac, F. (2010). Influence of mesoscale eddies on spatial structuring of top predators’ communities in the Mozambique Channel. Progress in Oceanography 86, 214–223.
Influence of mesoscale eddies on spatial structuring of top predators’ communities in the Mozambique Channel.Crossref | GoogleScholarGoogle Scholar |

Thomas, O., Ganio, K., Roberts, B., and Swearer, S. (2017). Trace element–protein interactions in endolymph from the inner ear of fish: implications for environmental reconstructions using fish otolith chemistry. Metallomics 9, 239–249.
Trace element–protein interactions in endolymph from the inner ear of fish: implications for environmental reconstructions using fish otolith chemistry.Crossref | GoogleScholarGoogle Scholar | 28091665PubMed |

Thorrold, S. R., Jones, G. P., Planes, S., and Hare, J. A. (2006). Transgenerational marking of embryonic otoliths in marine fishes using barium stable isotopes. Canadian Journal of Fisheries and Aquatic Sciences 63, 1193–1197.
Transgenerational marking of embryonic otoliths in marine fishes using barium stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Tibshirani, R., Walther, G., and Hastie, T. (2001). Estimating the number of clusters in a data set via the gap statistic. Journal of the Royal Statistical Society – B. Statistical Methodology 63, 411–423.
Estimating the number of clusters in a data set via the gap statistic.Crossref | GoogleScholarGoogle Scholar |

Tournois, J., Darnaude, A. M., Ferraton, F., Aliaume, C., Mercier, L., and McKenzie, D. J. (2017). Lagoon nurseries make a major contribution to adult populations of a highly prized coastal fish. Limnology and Oceanography 62, 1219–1233.
Lagoon nurseries make a major contribution to adult populations of a highly prized coastal fish.Crossref | GoogleScholarGoogle Scholar |

van Hulten, M., Middag, R., Dutay, J., De Baar, H., Roy-Barman, M., Gehlen, M., Tagliabue, A., and Sterl, A. (2017). Manganese in the West Atlantic Ocean in context of the first global ocean circulation model of manganese. Biogeosiences 14, 1123–1152.
Manganese in the West Atlantic Ocean in context of the first global ocean circulation model of manganese.Crossref | GoogleScholarGoogle Scholar |

Venables, W. N., and Ripley, B. D. (2002). ‘Modern Applied Statistics with S’, 4th edn. (Springer: New York, NY, USA.)

Volk, E. C., Blakley, A., Schroder, S. L., and Kuehner, S. (2000). Otolith chemistry reflects migratory characteristics of Pacific salmonids: using otolith core chemistry to distinguish maternal associations with sea and freshwaters. Fisheries Research 46, 251–266.
Otolith chemistry reflects migratory characteristics of Pacific salmonids: using otolith core chemistry to distinguish maternal associations with sea and freshwaters.Crossref | GoogleScholarGoogle Scholar |

Walther, B. D., and Thorrold, S. (2006). Water, not food, contributes the majority of strontium and barium deposited in the otoliths of a marine fish. Marine Ecology Progress Series 311, 125–130.
Water, not food, contributes the majority of strontium and barium deposited in the otoliths of a marine fish.Crossref | GoogleScholarGoogle Scholar |

Wang, C. H., Lin, Y. T., Shiao, J. C., You, C. F., and Tzeng, W. N. (2009). Spatio-temporal variation in the elemental compositions of otoliths of southern bluefin tuna Thunnus maccoyii in the Indian Ocean and its ecological implication. Journal of Fish Biology 75, 1173–1193.
Spatio-temporal variation in the elemental compositions of otoliths of southern bluefin tuna Thunnus maccoyii in the Indian Ocean and its ecological implication.Crossref | GoogleScholarGoogle Scholar | 20738607PubMed |

Webb, S. D., Woodcock, S. H., and Gillanders, B. M. (2012). Sources of otolith barium and strontium in estuarine fish and the influence of salinity and temperature. Marine Ecology Progress Series 453, 189–199.
Sources of otolith barium and strontium in estuarine fish and the influence of salinity and temperature.Crossref | GoogleScholarGoogle Scholar |

Wells, R. D., Rooker, J. R., and Itano, D. G. (2012). Nursery origin of yellowfin tuna in the Hawaiian Islands. Marine Ecology Progress Series 461, 187–196.
Nursery origin of yellowfin tuna in the Hawaiian Islands.Crossref | GoogleScholarGoogle Scholar |

Wells, R. J. D., Kinney, M., Kohin, S., Dewar, H., Rooker, J. R., and Snodgrass, O. (2015). Natural tracers reveal population structure of albacore (Thunnus alalunga) in the eastern North Pacific. ICES Journal of Marine Science 72, 2118–2127.
Natural tracers reveal population structure of albacore (Thunnus alalunga) in the eastern North Pacific.Crossref | GoogleScholarGoogle Scholar |

Wiggert, J., Murtugudde, R., and Christian, J. (2006). Annual ecosystem variability in the tropical Indian Ocean: results of a coupled bio-physical ocean general circulation model. Deep-sea Research – II. Topical Studies in Oceanography 53, 644–676.
Annual ecosystem variability in the tropical Indian Ocean: results of a coupled bio-physical ocean general circulation model.Crossref | GoogleScholarGoogle Scholar |

Wilcox, R. (2012). ‘Introduction to Robust Estimation and Hypothesis Testing’, 3rd edn. (Academic Press: Waltham, MA, USA.)

Wolf, R., and Wilson, S. (2007). USGS reference materials program. Serving the needs of the global analytical community. USGS Fact Sheet 2007–3056, US Geological Survey, Denver, CO, USA.

Woodcock, S., Munro, A., Crook, D., and Gillanders, B. (2012). Incorporation of magnesium into fish otoliths: determining contribution from water and diet. Geochimica et Cosmochimica Acta 94, 12–21.
Incorporation of magnesium into fish otoliths: determining contribution from water and diet.Crossref | GoogleScholarGoogle Scholar |

Wright, P. J., Régnier, T., Gibb, F. M., Augley, J., and Devalla, S. (2018). Assessing the role of ontogenetic movement in maintaining population structure in fish using otolith microchemistry. Ecology and Evolution 8, 7907–7920.
Assessing the role of ontogenetic movement in maintaining population structure in fish using otolith microchemistry.Crossref | GoogleScholarGoogle Scholar | 30250672PubMed |

Zeileis, A., and Grothendieck, G. (2005). zoo: S3 infrastructure for regular and irregular time series. Journal of Statistical Software 14, 1–27.
zoo: S3 infrastructure for regular and irregular time series.Crossref | GoogleScholarGoogle Scholar |

Zhang, C., Ye, Z., Li, Z., Wan, R., Ren, Y., and Dou, S. (2016). Population structure of Japanese Spanish mackerel Scomberomorus niphonius in the Bohai Sea, the Yellow Sea and the East China Sea: evidence from random forests based on otolith features. Fisheries Science 82, 251–256.
Population structure of Japanese Spanish mackerel Scomberomorus niphonius in the Bohai Sea, the Yellow Sea and the East China Sea: evidence from random forests based on otolith features.Crossref | GoogleScholarGoogle Scholar |

Zudaire, I., Murua, H., Grande, M., and Bodin, N. (2013). Reproductive potential of yellowfin tuna (Thunnus albacares) in the western Indian Ocean. Fishery Bulletin 111, 252–264.
Reproductive potential of yellowfin tuna (Thunnus albacares) in the western Indian Ocean.Crossref | GoogleScholarGoogle Scholar |