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Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Effects of temperature on tissue–diet isotopic spacing of nitrogen and carbon in otolith organic matter

Jane A. Godiksen A D , Ming-Tsung Chung https://orcid.org/0000-0003-3305-3339 B , Arild Folkvord A C and Peter Grønkjær https://orcid.org/0000-0003-1337-4661 B
+ Author Affiliations
- Author Affiliations

A Institute of Marine Research, Postbox 1870 Nordnes, N-5817 Bergen, Norway.

B University of Aarhus, Department of Bioscience, Ole Worms Allé 1, DK-8000 Aarhus C, Denmark.

C University of Bergen, Department of Biological Sciences, Postbox 7803, N-5020 Bergen, Norway.

D Corresponding author. Email: jane.godiksen@hi.no

Marine and Freshwater Research 70(12) 1757-1767 https://doi.org/10.1071/MF19054
Submitted: 14 February 2018  Accepted: 1 August 2019   Published: 28 October 2019

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

Abstract

Reconstruction of the trophic position of a fish can be performed by analysing stable nitrogen and carbon isotopes in otolith protein. However, ambient temperature may affect the tissue–diet isotopic spacing of stable isotopes from diet to predator tissue and bias estimates of trophic position. To test this, otolith protein, heart and muscle tissue from a rearing experiment with juvenile cod held at different temperatures (4, 7, 10 and 14°C) were analysed. There was no significant effect of temperature on otolith δ15N, whereas muscle and heart exhibited a slight decrease in δ15N values with increasing temperature corresponding to maximum of 0.6‰ over the 10°C range. By contrast, the otolith protein δ13C values at 4 and 7°C were significantly higher than for 10 and 14°C, suggesting an approximate 1‰ increased tissue–diet enrichment at the lower temperatures. Temperature had no significant effect on muscle and heart δ13C values. Considering the annual mean variation in ocean temperatures, our results indicate that the trophic signals recorded in the otoliths will reflect changes in diet isotope values with little bias from the ambient temperature experienced by the fish.

Additional keywords: fish, food web, otolith, marine, stable isotopes.


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 |

Barnes, C., Sweeting, C. J., Jennings, S., Barry, J. T., and Polunin, N. V. C. (2007). Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Functional Ecology 21, 356–362.
Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation.Crossref | GoogleScholarGoogle Scholar |

Bates, D., Mächler, M., Bolker, B. M., and Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Bligh, E. G., and Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.
A rapid method of total lipid extraction and purification.Crossref | GoogleScholarGoogle Scholar | 13671378PubMed |

Bosley, K. L., Witting, D. A., Chambers, R. C., and Wainright, S. C. (2002). Estimating turnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes. Marine Ecology Progress Series 236, 233–240.
Estimating turnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Britton, J. R., and Busst, G. M. A. (2018). Stable isotope discrimination factors of omnivorous fishes: influence of tissue type, temperature, diet composition and formulated feeds. Hydrobiologia 808, 219–234.
Stable isotope discrimination factors of omnivorous fishes: influence of tissue type, temperature, diet composition and formulated feeds.Crossref | GoogleScholarGoogle Scholar |

Carter, C. G., Houlihan, D. F., and Owen, S. F. (1998). Protein synthesis, nitrogen excretion and long-term growth of juvenile Pleuronectes flesus. Journal of Fish Biology 53, 272–284.
Protein synthesis, nitrogen excretion and long-term growth of juvenile Pleuronectes flesus.Crossref | GoogleScholarGoogle Scholar |

Caut, S., Angulo, E., and Courchamp, F. (2009). Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443–453.
Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction.Crossref | GoogleScholarGoogle Scholar |

Cheng, L. C., Shiao, J. C., Hsiao, S. S. Y., and Wang, P. L. (2018). Fractionation of otolith nitrogen stable isotopes measured by peroxodisulfate oxidation–bacterial conversion and isotope ratio mass spectrometry. Rapid Communications in Mass Spectrometry 32, 1905–1910.
Fractionation of otolith nitrogen stable isotopes measured by peroxodisulfate oxidation–bacterial conversion and isotope ratio mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 30085368PubMed |

Colborne, S. F., Fisk, A. T., and Johnson, T. B. (2017). Tissue-specific turnover and diet–tissue discrimination factors of carbon and nitrogen isotopes of a common forage fish held at two temperatures. Rapid Communications in Mass Spectrometry 31, 1405–1414.
Tissue-specific turnover and diet–tissue discrimination factors of carbon and nitrogen isotopes of a common forage fish held at two temperatures.Crossref | GoogleScholarGoogle Scholar | 28590512PubMed |

Doi, H., Akamatsu, F., and Gonzalez, A. L. (2017). Starvation effects on nitrogen and carbon stable isotopes of animals: an insight from meta-analysis of fasting experiments. Royal Society Open Science 4, 170633.
Starvation effects on nitrogen and carbon stable isotopes of animals: an insight from meta-analysis of fasting experiments.Crossref | GoogleScholarGoogle Scholar | 29291128PubMed |

Doucett, R. R., Hooper, W., and Power, G. (1999). Identification of anadromous and nonanadromous adult brook trout and their progeny in the Tabusintac River, New Brunswick, by means of multiple-stable-isotope analysis. Transactions of the American Fisheries Society 128, 278–288.
Identification of anadromous and nonanadromous adult brook trout and their progeny in the Tabusintac River, New Brunswick, by means of multiple-stable-isotope analysis.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 |

Fischer, G., and Wiencke, C. (1992). Stable carbon isotope composition, depth distribution and fate of macroalgae from the Antarctic Peninsula region. Polar Biology 12, 341–348.
Stable carbon isotope composition, depth distribution and fate of macroalgae from the Antarctic Peninsula region.Crossref | GoogleScholarGoogle Scholar |

Focken, U. (2001). Stable isotopes in animal ecology: the effect of ration size on the trophic shift of C and N isotopes between feed and carcass. Isotopes in Environmental and Health Studies 37, 199–211.
Stable isotopes in animal ecology: the effect of ration size on the trophic shift of C and N isotopes between feed and carcass.Crossref | GoogleScholarGoogle Scholar | 11924851PubMed |

Galimov, E. M. (1985). ‘The Biological Fractionation of Isotopes.’ (Academic Press: Orlando, FL, USA.)

Grønkjær, P., Pedersen, J. B., Ankjærø, T., Kjeldsen, H., Heinemeier, J., Steingrund, P., Nilsen, 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 |

Hobson, K. A. (1999). Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120, 314–326.
Tracing origins and migration of wildlife using stable isotopes: a review.Crossref | GoogleScholarGoogle Scholar | 28308009PubMed |

Hussey, N. E., MacNeil, M. A., McMeans, B. C., Olin, J. A., Dudley, S. F. J., Cliff, G., Wintner, S. P., Fennessy, S. T., and Fisk, A. T. (2014). Rescaling the trophic structure of marine food webs. Ecology Letters 17, 239–250.
Rescaling the trophic structure of marine food webs.Crossref | GoogleScholarGoogle Scholar | 24308860PubMed |

Hüssy, K., Mosegaard, H., and Jessen, F. (2004). Effect of age and temperature on amino acid composition and the content of different protein types of juvenile Atlantic cod (Gadus morhua) otoliths. Canadian Journal of Fisheries and Aquatic Sciences 61, 1012–1020.
Effect of age and temperature on amino acid composition and the content of different protein types of juvenile Atlantic cod (Gadus morhua) otoliths.Crossref | GoogleScholarGoogle Scholar |

Kusche, H., Hillgruber, N., Rößner, Y., and Focken, U. (2018). The effect of different fish feed compositions on δ13C and δ15N signatures of sea bass and its potential value for tracking mariculture-derived nutrients. Isotopes in Environmental and Health Studies 54, 28–40.
The effect of different fish feed compositions on δ13C and δ15N signatures of sea bass and its potential value for tracking mariculture-derived nutrients.Crossref | GoogleScholarGoogle Scholar | 28819995PubMed |

Kuznetsova, A., Brockhoff, P. B., and Christensen, R. H. B. (2017). lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82, 1–26.
lmerTest package: tests in linear mixed effects models.Crossref | GoogleScholarGoogle Scholar |

Lueders-Dumont, J. A., Wang, X. T., Jensen, O. P., Sigman, D. M., and Ward, B. B. (2018). Nitrogen isotopic analysis of carbonate-bound organic matter in modern and fossil fish otoliths. Geochimica et Cosmochimica Acta 224, 200–222.
Nitrogen isotopic analysis of carbonate-bound organic matter in modern and fossil fish otoliths.Crossref | GoogleScholarGoogle Scholar |

Martínez del Rio, C., Wolf, N., Carleton, S. A., and Gannes, L. Z. (2009). Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews of the Cambridge Philosophical Society 84, 91–111.
Isotopic ecology ten years after a call for more laboratory experiments.Crossref | GoogleScholarGoogle Scholar |

McMahon, K. W., Fogel, M. L., Elsdon, T. S., and Thorrold, S. R. (2010). Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein. Journal of Animal Ecology 79, 1132–1141.
Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein.Crossref | GoogleScholarGoogle Scholar | 20629794PubMed |

McMahon, K. W., Fogel, M. L., Johnson, B. J., Houghton, L. A., and Thorrold, S. R. (2011). A new method to reconstruct fish diet and movement patterns from δ13C values in otolith amino acids. Canadian Journal of Fisheries and Aquatic Sciences 68, 1330–1340.
A new method to reconstruct fish diet and movement patterns from δ13C values in otolith amino acids.Crossref | GoogleScholarGoogle Scholar |

Moore, J. W., and Semmens, B. X. (2008). Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11, 470–480.
Incorporating uncertainty and prior information into stable isotope mixing models.Crossref | GoogleScholarGoogle Scholar | 18294213PubMed |

Morrongiello, J. R., Thresher, R. E., and Smith, D. C. (2012). Aquatic biochronologies and climate change. Nature Climate Change 2, 849–857.
Aquatic biochronologies and climate change.Crossref | GoogleScholarGoogle Scholar |

Mosegaard, H., Svedang, H., and Taberman, K. (1988). Uncoupling of somatic and otolith growth-rates in Arctic char (Salvelinus alpinus) as an effect of differences in temperature response. Canadian Journal of Fisheries and Aquatic Sciences 45, 1514–1524.
Uncoupling of somatic and otolith growth-rates in Arctic char (Salvelinus alpinus) as an effect of differences in temperature response.Crossref | GoogleScholarGoogle Scholar |

Newsome, S. D., Wolf, N., Peters, J., and Fogel, M. L. (2014). Amino acid δ13C analysis shows flexibility in the routing of dietary protein and lipids to the tissue of an omnivore. Integrative and Comparative Biology 54, 890–902.
Amino acid δ13C analysis shows flexibility in the routing of dietary protein and lipids to the tissue of an omnivore.Crossref | GoogleScholarGoogle Scholar | 25104856PubMed |

Olive, P. J. W., Pinnegar, J. K., Polunin, N. V. C., Richards, G., and Welch, R. (2003). Isotope trophic-step fractionation: a dynamic equilibrium model. Journal of Animal Ecology 72, 608–617.
Isotope trophic-step fractionation: a dynamic equilibrium model.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 |

Post, D. M., Layman, C. A., Arrington, D. A., Takimoto, G., Quattrochi, J., and Montana, C. G. (2007). Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189.
Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses.Crossref | GoogleScholarGoogle Scholar | 17225157PubMed |

Power, M., Guiguer, K. R. R. A., and Barton, D. R. (2003). Effects of temperature on isotopic enrichment in Daphnia magna: implications for aquatic food-web studies. Rapid Communications in Mass Spectrometry 17, 1619–1625.
Effects of temperature on isotopic enrichment in Daphnia magna: implications for aquatic food-web studies.Crossref | GoogleScholarGoogle Scholar | 12845588PubMed |

Righton, D. A., Andersen, K. H., Neat, F., Thorsteinsson, V., Steingrund, P., Svedang, H., Michalsen, K., Hinrichsen, H. H., Bendall, V., Neuenfeldt, S., Wright, P., Jonsson, P., Huse, G., van der Kooij, J., Mosegaard, H., Hussy, K., and Metcalfe, J. (2010). Thermal niche of Atlantic cod Gadus morhua: limits, tolerance and optima. Marine Ecology Progress Series 420, 1–13.
Thermal niche of Atlantic cod Gadus morhua: limits, tolerance and optima.Crossref | GoogleScholarGoogle Scholar |

Sacramento, P. A., Manetta, G. I., and Benedito, E. (2016). Diet-tissue discrimination factors (Δ13C and Δ15N) and turnover rate in somatic tissues of a neotropical detritivorous fish on C3 and C4 diets. Journal of Fish Biology 89, 213–219.
Diet-tissue discrimination factors (Δ13C and Δ15N) and turnover rate in somatic tissues of a neotropical detritivorous fish on C3 and C4 diets.Crossref | GoogleScholarGoogle Scholar | 26728338PubMed |

Shiao, J.-C., Shirai, K., Tanaka, K., Takahata, N., Sano, Y., Hsiao, S. S.-Y., Lee, D.-C., and Tseng, Y.-C. (2018). Assimilation of nitrogen and carbon isotopes from fish diets to otoliths as measured by nanoscale secondary ion mass spectrometry. Rapid Communications in Mass Spectrometry 32, 1250–1256.
Assimilation of nitrogen and carbon isotopes from fish diets to otoliths as measured by nanoscale secondary ion mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 29781092PubMed |

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 |

Sweeting, C. J., Barry, J., Barnes, C., Polunin, N. V. C., and Jennings, S. (2007a). Effects of body size and environment on diet–tissue δ15N fractionation in fishes. Journal of Experimental Marine Biology and Ecology 340, 1–10.
Effects of body size and environment on diet–tissue δ15N fractionation in fishes.Crossref | GoogleScholarGoogle Scholar |

Sweeting, C. J., Barry, J. T., Polunin, N. V. C., and Jennings, S. (2007b). 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 |

Trueman, C. N., McGill, R. A. R., and Guyard, P. H. (2005). The effect of growth rate on tissue–diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Communications in Mass Spectrometry 19, 3239–3247.
The effect of growth rate on tissue–diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar).Crossref | GoogleScholarGoogle Scholar | 16220502PubMed |

Vander Zanden, M. J., Cabana, G., and Rasmussen, J. B. (1997). Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Canadian Journal of Fisheries and Aquatic Sciences 54, 1142–1158.
Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data.Crossref | GoogleScholarGoogle Scholar |

Vanderklift, M., and Ponsard, S. (2003). Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136, 169–182.
Sources of variation in consumer-diet δ15N enrichment: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 12802678PubMed |

Vandermyde, J. M., and Whitledge, G. W. (2008). Otolith δ15N distinguishes fish from forested and agricultural streams in southern Illinois. Journal of Freshwater Ecology 23, 333–336.
Otolith δ15N distinguishes fish from forested and agricultural streams in southern Illinois.Crossref | GoogleScholarGoogle Scholar |

Verweij, M. C., Nagelkerken, I., Hans, I., Ruseler, S. M., and Mason, P. R. D. (2008). Seagrass nurseries contribute to coral reef fish populations. Limnology and Oceanography 53, 1540–1547.
Seagrass nurseries contribute to coral reef fish populations.Crossref | GoogleScholarGoogle Scholar |