Skip to main content
SpringerLink
Log in

Matching and mismatching stable isotope (δ13C and δ15N) ratios in fin and muscle tissue among fish species: a critical review

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Using non-lethal tissue sampling for stable isotope analysis has become standard in many fields, but not for fishes, despite being desirable when species are rare or protected, when repeated sampling of individuals is required or where removal may bias other analyses. Here, we examine the utility of fish dorsal fin membrane as an alternative to muscle for analyzing δ13C and δ15N ratios in two reef fish species (blue cod Parapercis colias and spotty Notolabrus celidotus) that have differing feeding modes. Both species exhibited evidence of size-based feeding from fin δ15N values, but not from muscle. Blue cod fin δ15N increased steadily throughout the sampled size range (213–412 mm fork length), whereas spotty exhibited a distinct ontogenetic diet shift at approximately 120–140 mm fork length after which size-based feeding did not occur. Fin membrane was higher than muscle in δ13C in both species and in δ15N for blue cod, but fin δ15N was lower than muscle in spotty. The δ13C and δ15N fin–muscle offsets were constant in spotty regardless of size, while in blue cod, δ13C was constant with fish size, but δ15N offsets increased with increasing fish size. Non-lethal sampling utilizing fin tissue can be employed to estimate stable isotope values of muscle in fishes, but it is necessary to assess relationships among tissues and the effects of fish size on isotope values a priori for each species studied. Our data indicated that fin membrane may be a more sensitive tissue than muscle for detecting size-based feeding in some fish species using stable isotopes. A critical literature review revealed inconsistencies in tissue types tested, little understanding of tissue-specific trophic shift or turnover rates, and pseudo-replicated analyses leading to erroneous postulating of 1:1 relationships between tissues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andvik RT, VanDeHey JA, Fincel MJ, French WE, Bertrand KN, Chipps SR, Klumb RA, Graeb BDS (2010) Application of non-lethal stable isotope analysis to assess feeding patterns of juvenile pallid sturgeon Scaphirhynchus albus: a comparison of tissue types and sample preservation methods. J Appl Ichthyol 26:831–835. doi:10.1111/j.1439-0426.2010.01527.x

    Article  CAS  Google Scholar 

  • Bearhop S, Furness RW, Hilton GM, Votier SC, Waldron S (2003) A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Funct Ecol 17:270–275. doi:10.1046/j.1365-2435.2003.00725.x

    Article  Google Scholar 

  • Blanco A, Deudero S, Box A (2009) Muscle and scale isotopic offset of three fish species in the Mediterranean Sea: Dentex dentex, Argyrosomus regius and Xyrichtys novacula. Rapid Commun Mass Spectrom 23:2321–2328. doi:10.1002/rcm.4154

    Article  CAS  Google Scholar 

  • Bodin N, Budzinski H, Le Menach K, Tapie N (2009) ASE extraction method for simultaneous carbon and nitrogen stable isotope analysis in soft tissues of aquatic organisms. Anal Chim Acta 643:54–60. doi:10.1016/j.aca.2009.03.048

    Article  CAS  Google Scholar 

  • Champagne CE, Austin JD, Jelks HL, Jordan F (2008) Effects of fin clipping on survival and position-holding behavior of brown darters, Etheostoma edwini. Copeia 2008:916–919. doi:10.1643/ci-07-153

    Article  Google Scholar 

  • Cherel Y, Hobson KA, Hassani S (2005) Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115. doi:10.1086/425202

    Article  Google Scholar 

  • Church MR, Ebersole JL, Rensmeyer KM, Couture RB, Barrows FT, Noakes DLG (2009) Mucus: a new tissue fraction for rapid determination of fish diet switching using stable isotope analysis. Can J Fish Aquat Sci 66:1–5

    Article  CAS  Google Scholar 

  • Dempson JB, Power M (2004) Use of stable isotopes to distinguish farmed from wild Atlantic salmon, Salmo salar. Ecol Freshwat Fish 13:176–184. doi:10.1111/j.1600-0633.2004.00057

  • Finlay JC, Khandwala S, Power ME (2002) Spatial scales of carbon flow in a river food web. Ecology 83:1845–1859. doi:10.1890/0012-9658(2002)083[1845:ssocfi]2.0.co;2

    Google Scholar 

  • Francis M (2001) Coastal fishes of New Zealand—an identification guide. Reed Books, Auckland

    Google Scholar 

  • Gálvan DE, Sweeting CJ, Reid WDK (2010) Power of stable isotope techniques to detect size-based feeding in marine fishes. Mar Ecol Prog Ser 407:271–278. doi:10.3354/meps08528

    Article  Google Scholar 

  • German DP, Miles RD (2010) Stable carbon and nitrogen incorporation in blood and fin tissue of the catfish Pterygoplichthys disjunctivus (Siluriformes, Loricariidae). Environ Biol Fishes 89:117–133. doi:10.1007/s10641-010-9703-0

    Article  Google Scholar 

  • Greenwood NDW, Sweeting CJ, Polunin NVC (2010) Elucidating the trophodynamics of four coral reef fishes of the Solomon Islands using δ15N and δ13C. Coral Reefs 29:785–792. doi:10.1007/s00338-010-0626-1

    Article  Google Scholar 

  • Hamilton SL, Caselle JE, Lantz CA, Egloff TL, Kondo E, Newsome SD, Loke-Smith K, Pondella DJ II, Young KA, Lowe CG (2011) Extensive geographic and ontogenetic variation characterizes the trophic ecology of a temperate reef fish on southern California (USA) rocky reefs. Mar Ecol Prog Ser 429:227–244. doi:10.3354/meps09086

    Article  Google Scholar 

  • Hanisch JR, Tonn WM, Paszkowski CA, Scrimgeour GJ (2010) δ13C and δ15N signatures in muscle and fin tissues: nonlethal sampling methods for stable isotope analysis of salmonids. N Am J Fish Manag 30:1–11. doi:10.1577/m09-048.1

    Article  Google Scholar 

  • Hesslein RH, Hallard KA, Ramlal P (1993) Replacement of sulphur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Can J Fish Aquat Sci 50:2071–2076

    Article  CAS  Google Scholar 

  • Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Can J Fish Aquat Sci 53:528–533. doi:10.1139/cjfas-53-3-528

    Article  Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211. doi:10.2307/1942661

  • Jardine TD, Gray MA, McWilliam SM, Cunjak RA (2005) Stable isotope variability in tissues of temperate stream fishes. Trans Am Fish Soc 134:1103–1110. doi:10.1577/t04-124.1

    Article  CAS  Google Scholar 

  • Jardine TD, Hunt RJ, Pusey BJ, Bunn SE (2011) A non-lethal sampling method for stable carbon and nitrogen isotope studies of tropical fishes. Mar Freshw Res 62:83–90. doi:10.1071/mf10211

    Article  CAS  Google Scholar 

  • Jennings S, Reñones O, Morales-Nin B, Polunin NVC, Moranta J, Coll J (1997) Spatial variation in the 15N and 13C stable isotope composition of plants, invertebrates and fishes on Mediterranean reefs: implications for the study of trophic pathways. Mar Ecol Prog Ser 146:109–116

    Article  Google Scholar 

  • Jiang WM, Carbines G (2002) Diet of blue cod, Parapercis colias, living on undisturbed biogenic reefs and on seabed modified by oyster dredging in Foveaux Strait, New Zealand. Aquat Conserv: Mar Freshw Ecosyst 12:257–272. doi:10.1002/aqc.495

    Article  Google Scholar 

  • Jones GP (1984) The influence of habitat and behavioural interactions on the local distribution of the wrasse, Pseudolabrus celidotus. Environ Biol Fishes 10:43–58

    Article  Google Scholar 

  • Kelly MH, Hagar WG, Jardine TD, Cunjak RA (2006) Nonlethal sampling of sunfish and slimy sculpin for stable isotope analysis: how scale and fin tissue compare with muscle tissue. N Am J Fish Manag 26:921–925. doi:10.1577/m05-084.1

    Article  Google Scholar 

  • Matich P, Heithaus MR, Layman CA (2010) Size-based variation in intertissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinus leucas) and tiger sharks (Galeocerdo cuvier). Can J Fish Aquat Sci 67:877–885. doi:10.1139/f10-037

    Article  CAS  Google Scholar 

  • McCarthy ID, Waldron S (2000) Identifying migratory Salmo trutta using carbon and nitrogen stable isotope ratios. Rapid Commun Mass Spectrom 14:1325–1331. doi:10.1002/1097-0231(20000815)14:15<1325:aid-rcm980>3.0.co;2-a

    Article  CAS  Google Scholar 

  • McIntyre PB, Flecker AS (2006) Rapid turnover of tissue nitrogen of primary consumers in tropical freshwaters. Oecologia 148:12–21. doi:10.1007/s00442-005-0354-3

    Google Scholar 

  • Nelson J, Chanton J, Coleman F, Koenig C (2011) Patterns of stable carbon isotope turnover in gag, Mycteroperca microlepis, an economically important marine piscivore determined with a non-lethal surgical biopsy procedure. Environ Biol Fishes 90:243–252. doi:10.1007/s10641-010-9736-4

    Article  Google Scholar 

  • Newcombe EM, Taylor RB (2010) Trophic cascade in a seaweed-epifauna-fish food chain. Mar Ecol Prog Ser 408:161–167. doi:10.3354/meps08589

    Article  Google Scholar 

  • Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231

    Article  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718. doi:10.2307/3071875

    Article  Google Scholar 

  • Pratt TC, Fox MG (2002) Effect of fin clipping on overwinter growth and survival of age-0 walleyes. N Am J Fish Manage 22:1290–1294. doi:10.1577/1548-8675(2002)022<1290:eofcoo>2.0.co;2

    Article  Google Scholar 

  • Rasmussen JB, Trudeau V (2010) How well are velocity effects on partial derivative 13C signatures transmitted up the food web from algae to fish? Freshwat Biol 55:1303–1314. doi:10.1111/j.1365-2427.2009.02354.x

    Google Scholar 

  • Rodgers KL, Wing SR (2008) Spatial structure and movement of blue cod Parapercis colias in Doubtful Sound, New Zealand, inferred from δ13C and δ15N. Mar Ecol Prog Ser 359:239–248. doi:10.3354/meps07349

    Article  Google Scholar 

  • Rolfhus KR, Sandheinrich MB, Wiener JG, Bailey SW, Thoreson KA, Hammerschmidt CR (2008) Analysis of fin clips as a nonlethal method for monitoring mercury in fish. Environ Sci Technol 42:871–877. doi:10.1021/es071427+

    Article  CAS  Google Scholar 

  • Rounick JS, Hicks BJ (1985) The stable carbon isotope ratios of fish and their invertebrate prey in four New Zealand rivers. Freshwat Biol 15:207–214. doi:10.1111/j.1365-2427.1985.tb00193.x

  • Sanderson BL, Tran CD, Coe HJ, Pelekis V, Steel EA, Reichert WL (2009) Nonlethal sampling of fish caudal fins yields valuable stable isotope data for threatened and endangered fishes. Trans Am Fish Soc 138:1166–1177. doi:10.1577/t08-086.1

    Article  Google Scholar 

  • Scharf FS, Juanes F, Rountree RA (2000) Predator size—prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208:229–248. doi:10.3354/meps208229

    Article  Google Scholar 

  • Schroeder GL (1983) Stable isotope ratios as naturally occurring tracers in the aquaculture food web. Aquaculture 30:203–210. doi:10.1016/0044-8486(83)90162-x

    Google Scholar 

  • Schwarcz HP (1991) Some theoretical aspects of isotope paleodiet studies. J Archaeol Sci 18:261–275

    Article  Google Scholar 

  • Sinnatamby RN, Dempson JB, Power M (2008) A comparison of muscle- and scale-derived δ13C and δ15N across three life-history stages of Atlantic salmon, Salmo salar. Rapid Commun Mass Spectrom 22:2773–2778. doi:10.1002/rcm.3674

    Article  CAS  Google Scholar 

  • Suring E, Wing SR (2009) Isotopic turnover rate and fractionation in multiple tissues of red rock lobster (Jasus edwardsii) and blue cod (Parapercis colias): consequences for ecological studies. J Exp Mar Biol Ecol 370:56–63. doi:10.1016/j.jembe.2008.11.014

    Article  CAS  Google Scholar 

  • Suzuki KW, Kasai A, Nakayama K, Tanaka M (2005) Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration. Can J Fish Aquat Sci 62:671–678. doi:10.1139/f04-231

    Article  Google Scholar 

  • Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20:595–601. doi:10.1002/rcm.2347

    Article  CAS  Google Scholar 

  • Sweeting CJ, Barry J, Barnes C, Polunin NVC, Jennings S (2007a) Effects of body size and environment on diet-tissue δ15N fractionation in fishes. J Exp Mar Biol Ecol 340:1–10. doi:10.1016/j.jembe.2006.07.023

    Article  CAS  Google Scholar 

  • Sweeting CJ, Barry JT, Polunin NVC, Jennings S (2007b) Effects of body size and environment on diet-tissue δ13C fractionation in fishes. J Exp Mar Biol Ecol 352:165–176. doi:10.1016/j.jembe.2007.07.007

    Article  Google Scholar 

  • Syväranta J, Cucherousset J, Kopp D, Crivelli A, Céréghino R, Santoul F (2010) Dietary breadth and trophic position of introduced European catfish Silurus glanis in the River Tarn (Garonne River basin), southwest France. Aquat Biol 8:137–144. doi:10.3354/ab00220

    Google Scholar 

  • Tarroux A, Ehrich D, Lecomte N, Jardine TD, Bety J, Berteaux D (2010) Sensitivity of stable isotope mixing models to variation in isotopic ratios: evaluating consequences of lipid extraction. Method Ecol Evol 1:231–241. doi:10.1111/j.2041-210X.2010.00033.x

    Google Scholar 

  • Tronquart NH, Mazeas L, Reuilly-Manenti L, Zahm A, Belliard J (2012) Fish fins as non-lethal surrogates for muscle tissues in freshwater food web studies using stable isotopes. Rapid Commun Mass Spectrom 26:1603–1608. doi:10.1002/rcm.6265

    Article  CAS  Google Scholar 

  • Valadares S, Planas M (2012) Non-lethal dorsal fin sampling for stable isotope analysis in seahorses. Aquat Ecol 46:363–370

    Article  Google Scholar 

  • Vinson MR, Budy P (2011) Sources of variability and comparability between salmonid stomach contents and isotopic analyses: study design lessons and recommendations. Can J Fish Aquat Sci 68:137–151. doi:10.1139/f10-117

    Article  Google Scholar 

  • Vizzini S, Mazzola A (2009) Stable isotopes and trophic positions of littoral fishes from a Mediterranean marine protected area. Environ Biol Fishes 84:13–25. doi:10.1007/s10641-008-9381-3

    Article  Google Scholar 

  • Wagner CP, Einfalt LM, Scimone AB, Wahl DH (2009) Effects of fin-clipping on the foraging behavior and growth of age-0 muskellunge. N Am J Fish Manag 29:1644–1652. doi:10.1577/m08-214.1

    Article  Google Scholar 

  • Watanabe Y, Seikai T, Tominaga O (2005) Estimation of growth and food consumption in juvenile Japanese flounder Paralichthys olivaceus using carbon stable isotope ratio δ13C under laboratory conditions. J Exp Mar Biol Ecol 326:187–198. doi:10.1016/j.jembe.2005.05.020

    Article  Google Scholar 

  • Witting DA, Chambers RC, Bosley KL, Wainright SC (2004) Experimental evaluation of ontogenetic diet transitions in summer flounder (Paralichthys dentatus), using stable isotopes as diet tracers. Can J Fish Aquat Sci 61:2069–2084. doi:10.1139/f04-156

    Google Scholar 

  • Wolf N, Carleton SA, del Rio CM (2009) Ten years of experimental animal isotopic ecology. Funct Ecol 23:17–26. doi:10.1111/j.1365-2435.2009.01529.x

    Article  Google Scholar 

Download references

Acknowledgments

We thank Darren Stevens and Kimberley Maxwell for their assistance with muscle and fin membrane sampling and Andrew Marriner for help with the preparation and weighing of standards and samples for CF-IRMS analysis. We are grateful to Andrew Baxter (Department of Conservation, Nelson) for his assistance in securing permission to sample within the Horoirangi Marine Reserve and to Beth Sanderson (NOAA-NMFS) for helpful suggestions and providing data for Table 2. This work was funded by the New Zealand Department of Conservation (DOC investigation number 4181) and the NIWA Capability Fund (Project CF104300).

Author information

Authors and Affiliations

  1. National Institute of Water and Atmospheric Research Ltd., P.O. Box 893, Nelson, 7040, New Zealand

    Trevor J. Willis, Sean J. Handley, Dan G. Cairney & Michael J. Page

  2. School of Marine Science and Technology, Newcastle University, Newcastle Upon Tyne, NE1 7RU, UK

    Christopher J. Sweeting

  3. National Institute of Water and Atmospheric Research Ltd., Private Bag 14-901, Hataitai, Wellington, New Zealand

    Sarah J. Bury & Julie C. S. Brown

  4. Department of Conservation, P.O. Box 10420, The Terrace, Wellington, 6143, New Zealand

    Debbie J. Freeman

  5. Institute of Marine Sciences, School of Biological Sciences, University of Portsmouth, Ferry Road, Eastney, Portsmouth, PO4 9LY, UK

    Trevor J. Willis

Authors
  1. Trevor J. Willis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christopher J. Sweeting
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sarah J. Bury
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sean J. Handley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Julie C. S. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Debbie J. Freeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dan G. Cairney
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michael J. Page
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Trevor J. Willis.

Additional information

Communicated by C. Harrod.

Trevor J. Willis and Christopher J. Sweeting: Equal authorship.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Willis, T.J., Sweeting, C.J., Bury, S.J. et al. Matching and mismatching stable isotope (δ13C and δ15N) ratios in fin and muscle tissue among fish species: a critical review. Mar Biol 160, 1633–1644 (2013). https://doi.org/10.1007/s00227-013-2216-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2216-6

Keywords

Search

Navigation