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Otolith δ13C values as a metabolic proxy: approaches and mechanical underpinnings

Ming-Tsung Chung A D , Clive N. Trueman B , Jane Aanestad Godiksen C and Peter Grønkjær A
+ Author Affiliations
- Author Affiliations

A Department of Bioscience, Section for Aquatic Biology, Aarhus University, DK-8000 Aarhus C, Denmark.

B Ocean and Earth Science, University of Southampton Waterfront Campus, European Way, Southampton, SO14 3ZH, UK.

C Institute of Marine Research, Postbox 1870 Nordnes, NO-5817 Bergen, Norway.

D Corresponding author. Email: mingtsungchung@bios.au.dk

Marine and Freshwater Research 70(12) 1747-1756 https://doi.org/10.1071/MF18317
Submitted: 28 August 2018  Accepted: 15 January 2019   Published: 26 March 2019

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

Abstract

Knowledge of metabolic costs associated with maintenance, foraging, activity and growth under natural conditions is important for understanding fish behaviours and the bioenergetic consequences of a changing environment. Fish performance in the wild and within a complex environment can be investigated by analysing individual-level field metabolic rate and, at present, the natural stable carbon isotope tracer in otoliths offers the possibility to reconstruct field metabolic rate. The isotopic composition of carbon in fish otoliths is linked to oxygen consumption through metabolic oxidation of dietary carbon. The proportion of metabolically derived carbon can be estimated with knowledge of δ13C values of diet and dissolved inorganic carbon in the water. Over the past 10 years, new techniques to study fish ecology have been developed, and these can be used to strengthen the application of otolith δ13C values as a metabolic proxy. Here, we illustrate the great potential of the otolith δ13C metabolic proxy in combination with other valuable and well-established approaches. The novel approach of the otolith δ13C metabolic proxy allows us to track the effects of ontogenetic and environmental drivers on individual fish physiology, and removes a major obstacle to understanding and predicting the performance of free-ranging wild fish.

Additional keywords : bioenergetics, field metabolic rate, isotopic mixing models, oxygen consumption.


References

Ankjærø, T., Christensen, J. T., and Grønkjær, P. (2012). Tissue-specific turnover rates and trophic enrichment of stable N and C isotopes in juvenile Atlantic cod Gadus morhua fed three different diets. Marine Ecology Progress Series 461, 197–209.
Tissue-specific turnover rates and trophic enrichment of stable N and C isotopes in juvenile Atlantic cod Gadus morhua fed three different diets.Crossref | GoogleScholarGoogle Scholar |

Armstrong, J. D., Fallon Cousins, P. S., and Wright, P. J. (2004). The relationship between specific dynamic action and otolith growth in pike. Journal of Fish Biology 64, 739–749.
The relationship between specific dynamic action and otolith growth in pike.Crossref | GoogleScholarGoogle Scholar |

Ashford, J., and Jones, C. (2007). Oxygen and carbon stable isotopes in otoliths record spatial isolation of Patagonian toothfish (Dissostichus eleginoides). Geochimica et Cosmochimica Acta 71, 87–94.
Oxygen and carbon stable isotopes in otoliths record spatial isolation of Patagonian toothfish (Dissostichus eleginoides).Crossref | GoogleScholarGoogle Scholar |

Augley, J., Huxham, M., Fernandes, T. F., Lyndon, A. R., and Bury, S. (2007). Carbon stable isotopes in estuarine sediments and their utility as migration markers for nursery studies in the Firth of Forth and Forth Estuary, Scotland. Estuarine, Coastal and Shelf Science 72, 648–656.
Carbon stable isotopes in estuarine sediments and their utility as migration markers for nursery studies in the Firth of Forth and Forth Estuary, Scotland.Crossref | GoogleScholarGoogle Scholar |

Bade, D. L., Carpenter, S. R., Cole, J. J., Hanson, P. C., and Hesslein, R. H. (2004). Controls of δ13C‐DIC in lakes: geochemistry, lake metabolism, and morphometry. Limnology and Oceanography 49, 1160–1172.
Controls of δ13C‐DIC in lakes: geochemistry, lake metabolism, and morphometry.Crossref | GoogleScholarGoogle Scholar |

Bailey, D. M., Jamieson, A. J., Bagley, P. M., Collins, M. A., and Priede, I. G. (2002). Measurement of in situ oxygen consumption of deep-sea fish using an autonomous lander vehicle. Deep-sea Research – I. Oceanographic Research Papers 49, 1519–1529.
Measurement of in situ oxygen consumption of deep-sea fish using an autonomous lander vehicle.Crossref | GoogleScholarGoogle Scholar |

Bastow, T. P., Jackson, G., and Edmonds, J. S. (2002). Elevated salinity and isotopic composition of fish otolith carbonate: stock delineation of pink snapper, Pagrus auratus, in Shark Bay, Western Australia. Marine Biology 141, 801–806.
Elevated salinity and isotopic composition of fish otolith carbonate: stock delineation of pink snapper, Pagrus auratus, in Shark Bay, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Becker, M., Andersen, N., Erlenkeuser, H., Humphreys, M. P., Tanhua, T., and Körtzinger, A. (2016). An internally consistent dataset of δ13C-DIC in the North Atlantic Ocean – NAC13v1. Earth System Science Data 8, 559–570.
An internally consistent dataset of δ13C-DIC in the North Atlantic Ocean – NAC13v1.Crossref | GoogleScholarGoogle Scholar |

Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., and West, G. B. (2004). Toward a metabolic theory of ecology. Ecology 85, 1771–1789.
Toward a metabolic theory of ecology.Crossref | GoogleScholarGoogle Scholar |

Campana, S. E. (1990). How reliable are growth back-calculations based on otoliths? Canadian Journal of Fisheries and Aquatic Sciences 47, 2219–2227.
How reliable are growth back-calculations based on otoliths?Crossref | GoogleScholarGoogle Scholar |

Chabot, D., Steffensen, J. F., and Farrell, A. P. (2016). The determination of standard metabolic rate in fishes. Journal of Fish Biology 88, 81–121.
The determination of standard metabolic rate in fishes.Crossref | GoogleScholarGoogle Scholar | 26768973PubMed |

Chung, M.-T. (2015). Functional and life-history traits in deep-sea fishes. Ph.D. Thesis, University of Southampton, Southampton, UK.

Chung, M.-T., Trueman, C. N., Godiksen, J. A., Holmstrup, M. E., and Grønkjær, P. (2019). Field metabolic rates of teleost fishes are recorded in otolith carbonate. Communications Biology 2, 24.
Field metabolic rates of teleost fishes are recorded in otolith carbonate.Crossref | GoogleScholarGoogle Scholar | 30675522PubMed |

Clarke, A. (2006). Temperature and the metabolic theory of ecology. Functional Ecology 20, 405–412.
Temperature and the metabolic theory of ecology.Crossref | GoogleScholarGoogle Scholar |

Clarke, A., and Johnston, N. M. (1999). Scaling of metabolic rate with body mass and temperature in teleost fish. Journal of Animal Ecology 68, 893–905.
Scaling of metabolic rate with body mass and temperature in teleost fish.Crossref | GoogleScholarGoogle Scholar |

Correia, A. T., Barros, F., and Sial, A. N. (2011). Stock discrimination of European conger eel (Conger conger L.) using otolith stable isotope ratios. Fisheries Research 108, 88–94.
Stock discrimination of European conger eel (Conger conger L.) using otolith stable isotope ratios.Crossref | GoogleScholarGoogle Scholar |

Currey, L. M., Heupel, M. R., Simpfendorfer, C. A., and Williams, A. J. (2014). Inferring movement patterns of a coral reef fish using oxygen and carbon isotopes in otolith carbonate. Journal of Experimental Marine Biology and Ecology 456, 18–25.
Inferring movement patterns of a coral reef fish using oxygen and carbon isotopes in otolith carbonate.Crossref | GoogleScholarGoogle Scholar |

Deslauriers, D., Chipps, S. R., Breck, J. E., Rice, J. A., and Madenjian, C. P. (2017). Fish Bioenergetics 4.0: an R‐based modeling application. Fisheries 42, 586–596.
Fish Bioenergetics 4.0: an R‐based modeling application.Crossref | GoogleScholarGoogle Scholar |

Dufour, E., Gerdeaux, D., and Wurster, C. M. (2007). Whitefish (Coregonus lavaretus) respiration rate governs intra-otolith variation of δ13C values in Lake Annecy. Canadian Journal of Fisheries and Aquatic Sciences 64, 1736–1746.
Whitefish (Coregonus lavaretus) respiration rate governs intra-otolith variation of δ13C values in Lake Annecy.Crossref | GoogleScholarGoogle Scholar |

Elsdon, T. S., Ayvazian, S., McMahon, K. W., and Thorrold, S. R. (2010). Experimental evaluation of stable isotope fractionation in fish muscle and otoliths. Marine Ecology Progress Series 408, 195–205.
Experimental evaluation of stable isotope fractionation in fish muscle and otoliths.Crossref | GoogleScholarGoogle Scholar |

Fablet, R., Pecquerie, L., de Pontual, H., Høie, H., Millner, R., Mosegaard, H., and Kooijman, S. A. L. M. (2011). Shedding light on fish otolith biomineralization using a bioenergetic approach. PLoS One 6, e27055.
Shedding light on fish otolith biomineralization using a bioenergetic approach.Crossref | GoogleScholarGoogle Scholar | 22110601PubMed |

Farrell, A. P., Lee, C. G., Tierney, K., Hodaly, A., Clutterham, S., Healey, M., Hinch, S., and Lotto, A. (2003). Field-based measurements of oxygen uptake and swimming performance with adult Pacific salmon using a mobile respirometer swim tunnel. Journal of Fish Biology 62, 64–84.
Field-based measurements of oxygen uptake and swimming performance with adult Pacific salmon using a mobile respirometer swim tunnel.Crossref | GoogleScholarGoogle Scholar |

Filipsson, H. L., McCorkle, D. C., Mackensen, A., Bernhard, J. M., Andersson, L. S., Naustvoll, L.-J., Caballero-Alfonso, A. M., Nordberg, K., and Danielssen, D. S. (2017). Seasonal variability of stable carbon isotopes (δ13CDIC) in the Skagerrak and the Baltic Sea: distinguishing between mixing and biological productivity. Palaeogeography, Palaeoclimatology, Palaeoecology 483, 15–30.
Seasonal variability of stable carbon isotopes (δ13CDIC) in the Skagerrak and the Baltic Sea: distinguishing between mixing and biological productivity.Crossref | GoogleScholarGoogle Scholar |

Fraile, I., Arrizabalaga, H., Groeneveld, J., Kölling, M., Santos, M. N., Macías, D., Addis, P., Dettman, D. L., Karakulak, S., Deguara, S., and Rooker, J. R. (2016). The imprint of anthropogenic CO2 emissions on Atlantic bluefin tuna otoliths. Journal of Marine Systems 158, 26–33.
The imprint of anthropogenic CO2 emissions on Atlantic bluefin tuna otoliths.Crossref | GoogleScholarGoogle Scholar |

Gao, Y. W., and Beamish, R. J. (1999). Isotopic composition of otoliths as a chemical tracer in population identification of sockeye salmon (Oncorhynchus nerka). Canadian Journal of Fisheries and Aquatic Sciences 56, 2062–2068.
Isotopic composition of otoliths as a chemical tracer in population identification of sockeye salmon (Oncorhynchus nerka).Crossref | GoogleScholarGoogle Scholar |

Gao, Y. W., Joner, S. H., and Bargmann, G. G. (2001). Stable isotopic composition of otoliths in identification of spawning stocks of Pacific herring (Clupea pallasi) in Puget Sound. Canadian Journal of Fisheries and Aquatic Sciences 58, 2113–2120.
Stable isotopic composition of otoliths in identification of spawning stocks of Pacific herring (Clupea pallasi) in Puget Sound.Crossref | GoogleScholarGoogle Scholar |

Gao, Y., Dettman, D. L., Piner, K. R., and Wallace, F. R. (2010). Isotopic correlation (δ18O versus δ13C) of otoliths in identification of groundfish stocks. Transactions of the American Fisheries Society 139, 491–501.
Isotopic correlation (δ18O versus δ13C) of otoliths in identification of groundfish stocks.Crossref | GoogleScholarGoogle Scholar |

Gauldie, R. W. (1996). Biological factors controlling the carbon isotope record in fish otoliths: principles and evidence. Comparative Biochemistry and Physiology – B. Biochemistry & Molecular Biology 115, 201–208.
Biological factors controlling the carbon isotope record in fish otoliths: principles and evidence.Crossref | GoogleScholarGoogle Scholar |

Gauldie, R. W., Thacker, C. E., and Merrett, N. R. (1994). Oxygen and carbon isotope variation in the otoliths of Beryx splendens and Coryphaenoides profundicolus. Comparative Biochemistry and Physiology – A. Physiology 108, 153–159.
Oxygen and carbon isotope variation in the otoliths of Beryx splendens and Coryphaenoides profundicolus.Crossref | GoogleScholarGoogle Scholar |

Gerard, T., Malca, E., Muhling, B. A., Mateo, I., and Lamkin, J. T. (2015). Isotopic signatures in the otoliths of reef-associated fishes of southern Florida: Linkages between nursery grounds and coral reefs. Regional Studies in Marine Science 2, 95–104.
Isotopic signatures in the otoliths of reef-associated fishes of southern Florida: Linkages between nursery grounds and coral reefs.Crossref | GoogleScholarGoogle Scholar |

Gerdeaux, D., and Dufour, E. (2015). Life history traits of the fish community in Lake Annecy: evidence from the stable isotope composition of otoliths. Knowledge and Management of Aquatic Ecosystems 416, 35.
Life history traits of the fish community in Lake Annecy: evidence from the stable isotope composition of otoliths.Crossref | GoogleScholarGoogle Scholar |

Grønkjær, P. (2016). Otoliths as individual indicators: a reappraisal of the link between fish physiology and otolith characteristics. Marine and Freshwater Research 67, 881–888.
Otoliths as individual indicators: a reappraisal of the link between fish physiology and otolith characteristics.Crossref | GoogleScholarGoogle Scholar |

Grønkjær, P., Pedersen, J. B., Ankjærø, T. T., Kjeldsen, H., Heinemeier, J., Steingrund, P., Nielsen, J. M., and Christensen, J. T. (2013). Stable N and C isotopes in the organic matrix of fish otoliths: validation of a new approach for studying spatial and temporal changes in the trophic structure of aquatic ecosystems. Canadian Journal of Fisheries and Aquatic Sciences 70, 143–146.
Stable N and C isotopes in the organic matrix of fish otoliths: validation of a new approach for studying spatial and temporal changes in the trophic structure of aquatic ecosystems.Crossref | GoogleScholarGoogle Scholar |

Grossman, E. L., and Ku, T.-L. (1986). Oxygen and carbon isotope fractionation in biogenic aragonite: temperature effects. Chemical Geology. Isotope Geoscience Section 59, 59–74.
Oxygen and carbon isotope fractionation in biogenic aragonite: temperature effects.Crossref | GoogleScholarGoogle Scholar |

Guiguer, K. R. R. A., Drimmie, R., and Power, M. (2003). Validating methods for measuring δ18O and δ13C in otoliths from freshwater fish. Rapid Communications in Mass Spectrometry 17, 463–471.
Validating methods for measuring δ18O and δ13C in otoliths from freshwater fish.Crossref | GoogleScholarGoogle Scholar |

Hanson, N. N., Wurster, C. M., EIMF Todd, C. D. (2013). Reconstructing marine life-history strategies of wild Atlantic salmon from the stable isotope composition of otoliths. Marine Ecology Progress Series 475, 249–266.
Reconstructing marine life-history strategies of wild Atlantic salmon from the stable isotope composition of otoliths.Crossref | GoogleScholarGoogle Scholar |

Høie, H., Folkvord, A., and Otterlei, E. (2003). Effect of somatic and otolith growth rate on stable isotopic composition of early juvenile cod (Gadus morhua L.) otoliths. Journal of Experimental Marine Biology and Ecology 289, 41–58.
Effect of somatic and otolith growth rate on stable isotopic composition of early juvenile cod (Gadus morhua L.) otoliths.Crossref | GoogleScholarGoogle Scholar |

Høie, H., Andersson, C., Folkvord, A., and Karlsen, O. (2004a). Precision and accuracy of stable isotope signals in otoliths of pen-reared cod (Gadus morhua) when sampled with a high-resolution micromill. Marine Biology 144, 1039–1049.
Precision and accuracy of stable isotope signals in otoliths of pen-reared cod (Gadus morhua) when sampled with a high-resolution micromill.Crossref | GoogleScholarGoogle Scholar |

Høie, H., Otterlei, E., and Folkvord, A. (2004b). Temperature-dependent fractionation of stable oxygen isotopes in otoliths of juvenile cod (Gadus morhua L.). ICES Journal of Marine Science 61, 243–251.
Temperature-dependent fractionation of stable oxygen isotopes in otoliths of juvenile cod (Gadus morhua L.).Crossref | GoogleScholarGoogle Scholar |

Iacumin, P., Bianucci, G., and Longinelli, A. (1992). Oxygen and carbon isotopic composition of fish otoliths. Marine Biology 113, 537–542.
Oxygen and carbon isotopic composition of fish otoliths.Crossref | GoogleScholarGoogle Scholar |

Jamieson, R. E. (2001). Environmental history of northern cod from otolith isotopic analysis. Ph.D. Thesis, McMaster University, Hamilton, ON, Canada.

Jamieson, R. E., Schwarcz, H. P., and Brattey, J. (2004). Carbon isotopic records from the otoliths of Atlantic cod (Gadus morhua) from eastern Newfoundland, Canada. Fisheries Research 68, 83–97.
Carbon isotopic records from the otoliths of Atlantic cod (Gadus morhua) from eastern Newfoundland, Canada.Crossref | GoogleScholarGoogle Scholar |

Javor, B., and Dorval, E. (2014). Geography and ontogeny influence the stable oxygen and carbon isotopes of otoliths of Pacific sardine in the California Current. Fisheries Research 154, 1–10.
Geography and ontogeny influence the stable oxygen and carbon isotopes of otoliths of Pacific sardine in the California Current.Crossref | GoogleScholarGoogle Scholar |

Jobling, M. (1981). The influences of feeding on the metabolic rate of fishes: a short review. Journal of Fish Biology 18, 385–400.
The influences of feeding on the metabolic rate of fishes: a short review.Crossref | GoogleScholarGoogle Scholar |

Kalish, J. M. (1991a). 13C and 18O isotopic disequilibria in fish otoliths: metabolic and kinetic effects. Marine Ecology Progress Series 75, 191–203.
13C and 18O isotopic disequilibria in fish otoliths: metabolic and kinetic effects.Crossref | GoogleScholarGoogle Scholar |

Kalish, J. M. (1991b). Oxygen and carbon stable isotopes in the otoliths of wild and laboratory-reared Australian salmon (Arripis trutta). Marine Biology 110, 37–47.
Oxygen and carbon stable isotopes in the otoliths of wild and laboratory-reared Australian salmon (Arripis trutta).Crossref | GoogleScholarGoogle Scholar |

Killen, S. S., Costa, I., Brown, J. A., and Gamperl, A. K. (2007). Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope. Proceedings of the Royal Society of London – B. Biological Sciences 274, 431–438.
Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope.Crossref | GoogleScholarGoogle Scholar |

Killen, S. S., Atkinson, D., and Glazier, D. S. (2010). The intraspecific scaling of metabolic rate with body mass in fishes depends on lifestyle and temperature. Ecology Letters 13, 184–193.
The intraspecific scaling of metabolic rate with body mass in fishes depends on lifestyle and temperature.Crossref | GoogleScholarGoogle Scholar | 20059525PubMed |

Kimirei, I. A., Nagelkerken, I., Mgaya, Y. D., and Huijbers, C. M. (2013). The mangrove nursery paradigm revisited: otolith stable isotopes support nursery-to-reef movements by Indo-Pacific fishes. PLoS One 8, e66320.
The mangrove nursery paradigm revisited: otolith stable isotopes support nursery-to-reef movements by Indo-Pacific fishes.Crossref | GoogleScholarGoogle Scholar | 23776658PubMed |

Kiørboe, T., Munk, P., and Richardson, K. (1987). Respiration and growth of larval herring Clupea harengus: relation between specific dynamic action and growth efficiency. Marine Ecology Progress Series 40, 1–10.
Respiration and growth of larval herring Clupea harengus: relation between specific dynamic action and growth efficiency.Crossref | GoogleScholarGoogle Scholar |

Kroopnick, P. M. (1985). The distribution of 13C of ΣCO2 in the world oceans. Deep-Sea Research – A. Oceanographic Research Papers 32, 57–84.
The distribution of 13C of ΣCO2 in the world oceans.Crossref | GoogleScholarGoogle Scholar |

Martino, J. C., Doubleday, Z. A., and Gillanders, B. M. (2019). Metabolic effects on carbon isotope biomarkers in fish. Ecological Indicators 97, 10–16.
Metabolic effects on carbon isotope biomarkers in fish.Crossref | GoogleScholarGoogle Scholar |

McMahon, K. W., Hamady, L. L., and Thorrold, S. R. (2013). Ocean ecogeochemistry: a review. Oceanography and Marine Biology – an Annual Review 51, 321–373.

Metcalfe, N. B., Van Leeuwen, T. E., and Killen, S. S. (2016). Does individual variation in metabolic phenotype predict fish behaviour and performance? Journal of Fish Biology 88, 298–321.
Does individual variation in metabolic phenotype predict fish behaviour and performance?Crossref | GoogleScholarGoogle Scholar | 26577442PubMed |

Nelson, J., Hanson, C. W., Koenig, C., and Chanton, J. (2011). Influence of diet on stable carbon isotope composition in otoliths of juvenile red drum Sciaenops ocellatus. Aquatic Biology 13, 89–95.
Influence of diet on stable carbon isotope composition in otoliths of juvenile red drum Sciaenops ocellatus.Crossref | GoogleScholarGoogle Scholar |

Nonogaki, H., Nelson, J. A., and Patterson, W. P. (2006). Dietary histories of herbivorous loricariid catfishes: evidence from δ13C values of otoliths. Environmental Biology of Fishes 78, 13–21.
Dietary histories of herbivorous loricariid catfishes: evidence from δ13C values of otoliths.Crossref | GoogleScholarGoogle Scholar |

Pecquerie, L., Fablet, R., De Pontual, H., Bonhommeau, S., Alunno-Bruscia, M., Petitgas, P., and Kooijman, S. (2012). Reconstructing individual food and growth histories from biogenic carbonates. Marine Ecology Progress Series 447, 151–164.
Reconstructing individual food and growth histories from biogenic carbonates.Crossref | GoogleScholarGoogle Scholar |

Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.
Using stable isotopes to estimate trophic position: models, methods, and assumptions.Crossref | GoogleScholarGoogle Scholar |

Radtke, R. L. (1984). Formation and structural composition of larval striped mullet otoliths. Transactions of the American Fisheries Society 113, 186–191.
Formation and structural composition of larval striped mullet otoliths.Crossref | GoogleScholarGoogle Scholar |

Romanek, C. S., Grossman, E. L., and Morse, J. W. (1992). Carbon isotopic fractionation in synthetic aragonite and calcite: effects of temperature and precipitation rate. Geochimica et Cosmochimica Acta 56, 419–430.
Carbon isotopic fractionation in synthetic aragonite and calcite: effects of temperature and precipitation rate.Crossref | GoogleScholarGoogle Scholar |

Schloesser, R. W., Rooker, J. R., Louchuoarn, P., Neilson, J. D., and Secord, D. H. (2009). Interdecadal variation in seawater δ13C and δ18O recorded in fish otoliths. Limnology and Oceanography 54, 1665–1668.
Interdecadal variation in seawater δ13C and δ18O recorded in fish otoliths.Crossref | GoogleScholarGoogle Scholar |

Schmittner, A., Gruber, N., Mix, A. C., Key, R. M., Tagliabue, A., and Westberry, T. K. (2013). Biology and air–sea gas exchange controls on the distribution of carbon isotope ratios (δ13C) in the ocean. Biogeosciences 10, 5793–5816.
Biology and air–sea gas exchange controls on the distribution of carbon isotope ratios (δ13C) in the ocean.Crossref | GoogleScholarGoogle Scholar |

Schwarcz, H. P., Gao, Y., Campana, S., Browne, D., Knyf, M., and Brand, U. (1998). Stable carbon isotope variations in otoliths of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 55, 1798–1806.
Stable carbon isotope variations in otoliths of Atlantic cod (Gadus morhua).Crossref | GoogleScholarGoogle Scholar |

Shen, J., and Gao, Y. (2012). Stable isotope analyses in otoliths of silver carp: a pilot study in identification of natal sources and stock differences. Environmental Biology of Fishes 95, 445–453.
Stable isotope analyses in otoliths of silver carp: a pilot study in identification of natal sources and stock differences.Crossref | GoogleScholarGoogle Scholar |

Shephard, S., Trueman, C., Rickaby, R., and Rogan, E. (2007). Juvenile life history of NE Atlantic orange roughy from otolith stable isotopes. Deep-sea Research – I. Oceanographic Research Papers 54, 1221–1230.
Juvenile life history of NE Atlantic orange roughy from otolith stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Sherwood, G. D., and Rose, G. A. (2003). Influence of swimming form on otolith δ13C in marine fish. Marine Ecology Progress Series 258, 283–289.
Influence of swimming form on otolith δ13C in marine fish.Crossref | GoogleScholarGoogle Scholar |

Sherwood, G. D., and Rose, G. A. (2005). Stable isotope analysis of some representative fish and invertebrates of the Newfoundland and Labrador continental shelf food web. Estuarine, Coastal and Shelf Science 63, 537–549.
Stable isotope analysis of some representative fish and invertebrates of the Newfoundland and Labrador continental shelf food web.Crossref | GoogleScholarGoogle Scholar |

Shirai, K., Otake, T., Amano, Y., Kuroki, M., Ushikubo, T., Kita, N. T., Murayama, M., Tsukamoto, K., and Valley, J. W. (2018). Temperature and depth distribution of Japanese eel eggs estimated using otolith oxygen stable isotopes. Geochimica et Cosmochimica Acta 236, 373–383.
Temperature and depth distribution of Japanese eel eggs estimated using otolith oxygen stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Sirot, C., Grønkjær, P., Pedersen, J. B., Panfili, J., Zetina-Rejon, M., Tripp-Valdez, A., Ramos-Miranda, J., Flores-Hernandez, D., Sosa-Lopez, A., and Darnaude, A. M. (2017). Using otolith organic matter to detect diet shifts in Bardiella chrysoura, during a period of environmental changes. Marine Ecology Progress Series 575, 137–152.
Using otolith organic matter to detect diet shifts in Bardiella chrysoura, during a period of environmental changes.Crossref | GoogleScholarGoogle Scholar |

Solomon, C. T., Weber, P. K., Cech, J. J., Ingram, B. L., Conrad, M. E., Machavaram, M. V., Pogodina, A. R., and Franklin, R. L. (2006). Experimental determination of the sources of otolith carbon and associated isotopic fractionation. Canadian Journal of Fisheries and Aquatic Sciences 63, 79–89.
Experimental determination of the sources of otolith carbon and associated isotopic fractionation.Crossref | GoogleScholarGoogle Scholar |

Soofiani, N. M., and Hawkins, A. D. (1982). Energetic costs at different levels of feeding in juvenile cod, Gadus morhua L. Journal of Fish Biology 21, 577–592.
Energetic costs at different levels of feeding in juvenile cod, Gadus morhua L.Crossref | GoogleScholarGoogle Scholar |

Stock, B. C., Jackson, A. L., Ward, E. J., Parnell, A. C., Phillips, D. L., and Semmens, B. X. (2018). Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6, e5096.
Analyzing mixing systems using a new generation of Bayesian tracer mixing models.Crossref | GoogleScholarGoogle Scholar | 29942712PubMed |

Sweeting, C. J., Barry, J. T., Polunin, N. V. C., and Jennings, S. (2007). Effects of body size and environment on diet–tissue δ13C fractionation in fishes. Journal of Experimental Marine Biology and Ecology 352, 165–176.
Effects of body size and environment on diet–tissue δ13C fractionation in fishes.Crossref | GoogleScholarGoogle Scholar |

Tagliabue, A., and Bopp, L. (2008). Towards understanding global variability in ocean carbon‐13. Global Biogeochemical Cycles 22, GB1025.
Towards understanding global variability in ocean carbon‐13.Crossref | GoogleScholarGoogle Scholar |

Telmer, K., and Veizer, J. (1999). Carbon fluxes, pCO2 and substrate weathering in a large northern river basin, Canada: carbon isotope perspectives. Chemical Geology 159, 61–86.
Carbon fluxes, pCO2 and substrate weathering in a large northern river basin, Canada: carbon isotope perspectives.Crossref | GoogleScholarGoogle Scholar |

Thorrold, S. R., Campana, S. E., Jones, C. M., and Swart, P. K. (1997). Factors determining δ13C and δ18O fractionation in aragonitic otoliths of marine fish. Geochimica et Cosmochimica Acta 61, 2909–2919.
Factors determining δ13C and δ18O fractionation in aragonitic otoliths of marine fish.Crossref | GoogleScholarGoogle Scholar |

Tohse, H., and Mugiya, Y. (2008). Sources of otolith carbonate: experimental determination of carbon incorporation rates from water and metabolic CO2, and their diel variations. Aquatic Biology 1, 259–268.
Sources of otolith carbonate: experimental determination of carbon incorporation rates from water and metabolic CO2, and their diel variations.Crossref | GoogleScholarGoogle Scholar |

Treberg, J. R., Killen, S. S., MacCormack, T. J., Lamarre, S. G., and Enders, E. C. (2016). Estimates of metabolic rate and major constituents of metabolic demand in fishes under field conditions: methods, proxies, and new perspectives. Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 202, 10–22.
Estimates of metabolic rate and major constituents of metabolic demand in fishes under field conditions: methods, proxies, and new perspectives.Crossref | GoogleScholarGoogle Scholar |

Trueman, C. N., Rickaby, R., and Shephard, S. (2013). Thermal, trophic and metabolic life histories of inaccessible fishes revealed from stable-isotope analyses: a case study using orange roughy Hoplostethus atlanticus. Journal of Fish Biology 83, 1613–1636.
Thermal, trophic and metabolic life histories of inaccessible fishes revealed from stable-isotope analyses: a case study using orange roughy Hoplostethus atlanticus.Crossref | GoogleScholarGoogle Scholar | 24298954PubMed |

Trueman, C. N., Chung, M.-T., and Shores, D. (2016). Ecogeochemistry potential in deep time biodiversity illustrated using a modern deep-water case study. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 371, 20150223.
Ecogeochemistry potential in deep time biodiversity illustrated using a modern deep-water case study.Crossref | GoogleScholarGoogle Scholar | 26977063PubMed |

von Biela, V. R., Newsome, S. D., and Zimmerman, C. E. (2015). Examining the utility of bulk otolith δ13C to describe diet in wild-caught black rockfish Sebastes melanops. Aquatic Biology 23, 201–208.
Examining the utility of bulk otolith δ13C to describe diet in wild-caught black rockfish Sebastes melanops.Crossref | GoogleScholarGoogle Scholar |

Weidel, B. C., Ushikubo, T., Carpenter, S. R., Kita, N. T., Cole, J. J., Kitchell, J. F., Pace, M. L., and Valley, J. W. (2007). Diary of a bluegill (Lepomis macrochirus): daily δ13C and δ18O records in otoliths by ion microprobe. Canadian Journal of Fisheries and Aquatic Sciences 64, 1641–1645.
Diary of a bluegill (Lepomis macrochirus): daily δ13C and δ18O records in otoliths by ion microprobe.Crossref | GoogleScholarGoogle Scholar |

Weidman, C. R., and Millner, R. (2000). High-resolution stable isotope records from North Atlantic cod. Fisheries Research 46, 327–342.
High-resolution stable isotope records from North Atlantic cod.Crossref | GoogleScholarGoogle Scholar |

Wieser, W., and Medgyesy, N. (1990). Cost and efficiency of growth in the larvae of two species of fish with widely differing metabolic rates. Proceedings of the Royal Society of London – B. Biological Sciences 242, 51–56.
Cost and efficiency of growth in the larvae of two species of fish with widely differing metabolic rates.Crossref | GoogleScholarGoogle Scholar |

Wurster, C. M., and Patterson, W. P. (2003). Metabolic rate of late Holocene freshwater fish: evidence from δ13C values of otoliths. Paleobiology 29, 492–505.
Metabolic rate of late Holocene freshwater fish: evidence from δ13C values of otoliths.Crossref | GoogleScholarGoogle Scholar |

Wurster, C. M., Patterson, W. P., Stewart, D. J., Bowlby, J. N., and Stewart, T. J. (2005). Thermal histories, stress, and metabolic rates of Chinook salmon (Oncorhynchus tshawytscha) in Lake Ontario: evidence from intra-otolith stable isotope analyses. Canadian Journal of Fisheries and Aquatic Sciences 62, 700–713.
Thermal histories, stress, and metabolic rates of Chinook salmon (Oncorhynchus tshawytscha) in Lake Ontario: evidence from intra-otolith stable isotope analyses.Crossref | GoogleScholarGoogle Scholar |