Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Species-specific trophic enrichment factor of stable nitrogen and carbon isotopes in fish otolith organic matter

Ming-Tsung Chung A # , Yu-Yang Peng A # , Aafaq Nazir https://orcid.org/0000-0002-9236-6637 A , Yu-Chun Wang https://orcid.org/0000-0002-9105-202X B , Pei-Lin Wang A and Jen-Chieh Shiao https://orcid.org/0000-0002-3824-5738 A *
+ Author Affiliations
- Author Affiliations

A Institute of Oceanography, National Taiwan University, 1, Sec. 4, Roosevelt Road, Taipei City, 10617, Taiwan.

B Fisheries Research Institute, Council of Agriculture, 199 Hou-Ih Road, Keelung, 202008, Taiwan.

* Correspondence to: jcshiao@ntu.edu.tw
# These authors contributed equally to this paper

Handling Editor: Iwan Jones

Marine and Freshwater Research 74(11) 956-968 https://doi.org/10.1071/MF23022
Submitted: 31 January 2023  Accepted: 22 May 2023   Published: 14 June 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Although stable carbon (δ13C) and nitrogen (δ15N) isotopes are widely used to study feeding ecology, the use of these isotopes in otolith organic matter to assess the diet of fishes is rarely investigated.

Aim: This study evaluated the relationship of δ13C and δ15N values among muscle, otolith organic matter and diet. The samples were analysed using an elemental analyzer connected to isotope-ratio mass spectrometry.

Key results: The δ15N values were highest in muscle followed by otoliths, diet and plankton, although no significant difference in δ15N values was found between the otolith and diet for most of the samples. The fish collected from water reservoirs showed similar δ13C values between otolith and muscle, both of which were higher than the isotopic values of the fish diet. However, the farmed fishes showed small but significant difference in the δ13C values between muscle and otolith, which reflects diet change or commercial diet containing a mixture of different food items.

Conclusion: Otolith δ15N value can provide information about fish diet and the otolith δ13C value can act as a good proxy of muscle δ13C composition in fish species.

Implications: Otolith δ15N and δ13C values can faithfully reflect the trophic position and feeding behaviours of fish.

Keywords: calcified structure, feeding ecology, food-web structure, isotopic fractionation, otolith, stable isotopes, teleostean fish, turnover rate.


References

Ankjærø, T, Christensen, JT, 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 |

Asano, M, and Mugiya, Y (1993). Biochemical and calcium-binding properties of water-soluble proteins isolated from otoliths of the tilapia, Orecchromis niloticus. Comparative Biochemistry and Physiology – B. Comparative Biochemistry 104, 201–205.
Biochemical and calcium-binding properties of water-soluble proteins isolated from otoliths of the tilapia, Orecchromis niloticus.Crossref | GoogleScholarGoogle Scholar |

Barnes, C, Sweeting, CJ, Jennings, S, Barry, JT, and Polunin, NVC (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 |

Battonyai, I, Specziár, A, Vitál, Z, Mozsár, A, Görgényi, J, Borics, G, Tóth, LG, and Boros, G (2015). Relationship between gill raker morphology and feeding habits of hybrid bigheaded carps (Hypophthalmichthys spp.). Knowledge and Management of Aquatic Ecosystems 416, 36.
Relationship between gill raker morphology and feeding habits of hybrid bigheaded carps (Hypophthalmichthys spp.).Crossref | GoogleScholarGoogle Scholar |

Beng, KC, and Corlett, RT (2020). Applications of environmental DNA (eDNA) in ecology and conservation: opportunities, challenges and prospects. Biodiversity and Conservation 29, 2089–2121.
Applications of environmental DNA (eDNA) in ecology and conservation: opportunities, challenges and prospects.Crossref | GoogleScholarGoogle Scholar |

Borelli, G, Mayer-Gostan, N, De Pontual, H, Boeuf, G, and Payan, P (2001). Biochemical relationships between endolymph and otolith matrix in the trout (Oncorhynchus mykiss) and turbot (Psetta maxima). Calcified Tissue International 69, 356–364.
Biochemical relationships between endolymph and otolith matrix in the trout (Oncorhynchus mykiss) and turbot (Psetta maxima).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 |

Chang, N-N, Shiao, J-C, Gong, G-C, Kao, S-J, and Hsieh, C-H (2014). Stable isotope ratios reveal food source of benthic fish and crustaceans along a gradient of trophic status in the East China Sea. Continental Shelf Research 84, 23–34.
Stable isotope ratios reveal food source of benthic fish and crustaceans along a gradient of trophic status in the East China Sea.Crossref | GoogleScholarGoogle Scholar |

Chen, H-L, Chang, N-N, Hsiao, WV, Chen, W-J, Wang, C-H, and Shiao, J-C (2022). Using molecular phylogenetic and stable isotopic analysis to identify species, geographical origin and production method of mullet roes. Food Control 141, 109206.
Using molecular phylogenetic and stable isotopic analysis to identify species, geographical origin and production method of mullet roes.Crossref | GoogleScholarGoogle Scholar |

Cheng, L-C, Shiao, J-C, Hsiao, SS-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 |

Davis, AM, Blanchette, ML, Pusey, BJ, Jardine, TD, and Pearson, RG (2012). Gut content and stable isotope analyses provide complementary understanding of ontogenetic dietary shifts and trophic relationships among fishes in a tropical river. Freshwater Biology 57, 2156–2172.
Gut content and stable isotope analyses provide complementary understanding of ontogenetic dietary shifts and trophic relationships among fishes in a tropical river.Crossref | GoogleScholarGoogle Scholar |

Degens, ET, Deuser, WG, and Haedrich, RL (1969). Molecular structure and composition of fish otoliths. Marine Biology 2, 105–113.
Molecular structure and composition of fish otoliths.Crossref | GoogleScholarGoogle Scholar |

DeNiro, MJ, and Epstein, S (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.
Influence of diet on the distribution of carbon isotopes in animals.Crossref | GoogleScholarGoogle Scholar |

Descolas-Gros, C, and Fontungne, M (1990). Stable carbon isotope fractionation by marine phytoplankton during photosynthesis. Plant, Cell and Environment 13, 207–218.
Stable carbon isotope fractionation by marine phytoplankton during photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Godiksen, JA, Chung, M-T, Folkvord, A, and Grønkjær, P (2019). Effects of temperature on tissue–diet isotopic spacing of nitrogen and carbon in otolith organic matter. Marine and Freshwater Research 70, 1757–1767.
Effects of temperature on tissue–diet isotopic spacing of nitrogen and carbon in otolith organic matter.Crossref | GoogleScholarGoogle Scholar |

Graham, BS, Grubbs, D, Holland, K, and Popp, BN (2007). A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Marine Biology 150, 647–658.
A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii.Crossref | GoogleScholarGoogle Scholar |

Grønkjær, P, Pedersen, JB, Ankjærø, TT, Kjeldsen, H, Heinemeier, J, Steingrund, P, Nielsen, JM, and Christensen, JT (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 |

Gül, G, and Demirel, N (2022). Ontogenetic shift in diet and trophic role of Raja clavate inferred by stable isotopes and stomach content analysis in the Sea of Marmara. Journal of Fish Biology 101, 560–572.
Ontogenetic shift in diet and trophic role of Raja clavate inferred by stable isotopes and stomach content analysis in the Sea of Marmara.Crossref | GoogleScholarGoogle Scholar |

Heady, WN, and Moore, JW (2013). Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout. Oecologia 172, 21–34.
Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout.Crossref | GoogleScholarGoogle Scholar |

Hussey, NE, MacNeil, MA, McMeans, BC, Olin, JA, Dudley, SFJ, Cliff, G, Wintner, SP, Fennessy, ST, and Fisk, AT (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 |

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 |

Jomori, RK, Ducatti, C, Carneiro, DJ, and Portella, MC (2008). Stable carbon (δ13C) and nitrogen (δ15N) isotopes as natural indicators of live and dry food in Piaractus mesopotamicus (Holmberg, 1887) larval tissue. Aquaculture Research 39, 370–381.
Stable carbon (δ13C) and nitrogen (δ15N) isotopes as natural indicators of live and dry food in Piaractus mesopotamicus (Holmberg, 1887) larval tissue.Crossref | GoogleScholarGoogle Scholar |

Le Bourg, B, Bănaru, D, Saraux, C, Nowaczyk, A, Le Luherne, E, Jadaud, A, Bigot, JL, and Richard, P (2015). Trophic niche overlap of sprat and commercial small pelagic teleosts in the Gulf of Lions (NW Mediterranean Sea). Journal of Sea Research 103, 138–146.
Trophic niche overlap of sprat and commercial small pelagic teleosts in the Gulf of Lions (NW Mediterranean Sea).Crossref | GoogleScholarGoogle Scholar |

Lee, W-O, Zhang, M-M, Oh, C-W, Baek, J-M, and Song, K-J (2012). Age and growth of barbel steed Hemibarbus labeo in Goe-san Lake in Korea. Fisheries and Aquatic Sciences 15, 353–359.
Age and growth of barbel steed Hemibarbus labeo in Goe-san Lake in Korea.Crossref | GoogleScholarGoogle Scholar |

Lorenzoni M, Corboli M, Ghetti L, Pedicillo G, Carosi A (2007) Chapter 13: growth and reproduction of the goldfish Carassius auratus: a case study from Italy. In ‘Biological invaders in inland waters: profiles, distribution, and threats’. (Ed. F Gherardi) pp. 259–273. (Springer) https://doi.org/10.1007/978-1-4020-6029-8_13

Lueders-Dumont, JA, Wang, XT, Jensen, OP, Sigman, DM, and Ward, BB (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 |

Lueders-Dumont, JA, Sigman, DM, Johnson, BJ, Jensen, OP, Oleynik, S, and Ward, BB (2020). Comparison of the isotopic composition of fish otolith-bound organic N with host tissue. Canadian Journal of Fisheries and Aquatic Sciences 77, 264–275.
Comparison of the isotopic composition of fish otolith-bound organic N with host tissue.Crossref | GoogleScholarGoogle Scholar |

Lueders-Dumont, JA, Forden, AG, Kast, ER, Mohan, JA, Walther, BD, Sigman, DM, and Ward, BB (2022). Controls on the nitrogen isotopic composition of fish otolith organic matter: lessons from a controlled diet switch experiment. Geochimica et Cosmochimica Acta 316, 69–86.
Controls on the nitrogen isotopic composition of fish otolith organic matter: lessons from a controlled diet switch experiment.Crossref | GoogleScholarGoogle Scholar |

Madigan, DJ, Snodgrass, OE, Hyde, JR, and Dewar, H (2021). Stable isotope turnover rates and fractionation in captive California yellowtail (Seriola dorsalis): insights for application to field studies. Scientific Reports 11, 4466.
Stable isotope turnover rates and fractionation in captive California yellowtail (Seriola dorsalis): insights for application to field studies.Crossref | GoogleScholarGoogle Scholar |

McMahon, KW, Fogel, ML, Elsdon, TS, and Thorrold, SR (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 |

Myrbo, A, and Shapley, MD (2006). Seasonal water-column dynamics of dissolved inorganic carbon stable isotopic compositions (δ13CDIC) in small hardwater lakes in Minnesota and Montana. Geochimica et Cosmochimica Acta 70, 2699–2714.
Seasonal water-column dynamics of dissolved inorganic carbon stable isotopic compositions (δ13CDIC) in small hardwater lakes in Minnesota and Montana.Crossref | GoogleScholarGoogle Scholar |

Ngochera, MJ, and Bootsma, HA (2011). Temporal trends of phytoplankton and zooplankton stable isotope composition in tropical Lake Malawi. Journal of Great Lakes Research 37, 45–53.
Temporal trends of phytoplankton and zooplankton stable isotope composition in tropical Lake Malawi.Crossref | GoogleScholarGoogle Scholar |

Olive, PJW, Pinnegar, JK, Polunin, NVC, 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 |

Peiman, KS, Lin, H-Y, Power, M, Hinch, SG, Patterson, DA, and Cooke, SJ (2022). Effects of short-term decomposition on isotope values of fish tissues under natural conditions. Aquatic Ecology 56, 173–181.
Effects of short-term decomposition on isotope values of fish tissues under natural conditions.Crossref | GoogleScholarGoogle Scholar |

Peterson, BJ, and Fry, B (1987). Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.
Stable isotopes in ecosystem studies.Crossref | GoogleScholarGoogle Scholar |

Post, DM (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 |

Rolff, C (2000). Seasonal variation in δ13C and δ15N of size-fractionated plankton at a coastal station in the northern Baltic proper. Marine Ecology Progress Series 203, 47–65.
Seasonal variation in δ13C and δ15N of size-fractionated plankton at a coastal station in the northern Baltic proper.Crossref | GoogleScholarGoogle Scholar |

Rowell, K, Dettman, DL, and Dietz, R (2010). Nitrogen isotopes in otoliths reconstruct ancient trophic position. Environmental Biology of Fishes 89, 415–425.
Nitrogen isotopes in otoliths reconstruct ancient trophic position.Crossref | GoogleScholarGoogle Scholar |

Schimmelmann A (2011) Carbon, nitrogen and oxygen stable isotope ratios in chitin. In ‘Chitin: formation and diagenesis’. (Ed. NS Gupta) pp. 81–103. (Springer) https://doi.org/10.1007/978-90-481-9684-5

Shiao, J-C, Shirai, K, Tanaka, K, Takahata, N, Sano, Y, Sung-Yun Hsiao, S, 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 |

Sirot, C, Grønkjær, P, Pedersen, JB, Panfili, J, Zetina-Rejon, M, Tripp-Valdez, A, Ramos-Miranda, J, Flores-Hernandez, D, Sosa-Lopez, A, and Darnaude, A (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 |

Stephens, RB, Ouimette, AP, Hobbie, EA, and Rowe, RJ (2022). Reevaluating trophic discrimination factors (Δδ13C and Δδ15N) for diet reconstruction. Ecological Monographs 92, e1525.
Reevaluating trophic discrimination factors (Δδ13C and Δδ15N) for diet reconstruction.Crossref | GoogleScholarGoogle Scholar |

Trueman, CN, McGill, RAR, and Guyard, PH (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 |

Trzcinski, MK, Srivastava, DS, Corbara, B, Dézerald, O, Leroy, C, Carrias, J-F, Dejean, A, and Céréghino, R (2016). The effects of food web structure on ecosystem function exceeds those of precipitation. Journal of Animal Ecology 85, 1147–1160.
The effects of food web structure on ecosystem function exceeds those of precipitation.Crossref | GoogleScholarGoogle Scholar |

Vandermyde, JM, and Whitledge, GW (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 |

Vane, K, Wallsgrove, NJ, Ekau, W, and Popp, BN (2018). Reconstructing lifetime nitrogen baselines and trophic position of Cynoscion acoupa from δ15N values of amino acids in otoliths. Marine Ecology Progress Series 597, 1–11.
Reconstructing lifetime nitrogen baselines and trophic position of Cynoscion acoupa from δ15N values of amino acids in otoliths.Crossref | GoogleScholarGoogle Scholar |

Xinping Z (2022) Cultured aquatic species innformation programme: Cirrhinus molitorella (Valenciennes 1844). (Food and Agriculture Organization of the United Nations, Fisheries and Aquaculture Division: Rome, Italy) Available at https://www.fao.org/fishery/en/culturedspecies/cirrhinus_molitorella/en

Zanden, MJV, and Rasmussen, JB (2001). Variation in δ13C and δ15N trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46, 2061–2066.
Variation in δ13C and δ15N trophic fractionation: implications for aquatic food web studies.Crossref | GoogleScholarGoogle Scholar |