[en] Rationale: Intrinsic biogeochemical markers, such as stable isotope ratios of carbon, nitrogen and sulphur are increasingly used to trace the trophic ecology of marine top predators. However, insufficient knowledge of fractionation processes in tissues continues to hamper the use of these markers.Methods: We performed a controlled feeding experiment with eight juvenile hooded seals (Cystophora cristata) that were held on a herring-based diet (Clupea harengus) for two years. Stable isotope ratios were measured via isotope ratio mass spectrometry in three of their tissues and related to values of these markers in their diet. Results: Diet-tissue isotope enrichment (trophic enrichment factor, TEF) values between dietary herring and seal tissues for carbon (Δ13C) were + 0.7 ‰ for red blood cells, + 1.9 ‰ for hair and + 1.1 ‰ for muscle. The TEFs for nitrogen trophic (Δ15N) were + 3.3 ‰ for red blood cells, + 3.6 ‰ for hair and + 4.3 ‰ for muscle. For sulphur, the Δ34S values were +1.1 ‰ for red blood cells, + 1.0 ‰ for hair and + 0.9 ‰ for muscle.Conclusions: These enrichment values were greater than those previously measured in adult seals. This increase may be related to the higher rate of protein synthesis and catabolism in growing animals. This study is the first report on sulphur isotope enrichment values for a marine mammal species.
Research Center/Unit :
MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
Disciplines :
Environmental sciences & ecology
Author, co-author :
Pinzone, Marianna ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Acquarone, Mario
Huyghebaert, Loreen ; Centre Hospitalier Universitaire de Liège - CHU > Service de chimie clinique
Sturaro, Nicolas ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Michel, Loïc ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Siebert, Ursula; Institute of Aquatic and Terrestrial Wildlife ITAW
Das, Krishna ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Language :
English
Title :
Carbon, Nitrogen and Sulphur isotopic fractionation in captive juvenile hooded seal (Cystophora cristata): application for diet analysis
Atwell L, Hobson KA, Welch HE. Biomagnification and bioaccumulation of mercury in an arctic food web: insights from stable nitrogen isotopes analysis. Can J Fish Aquat Sci. 1998;55:1114.
Layman CA, Arrington DA, Montaña CG, Post DM. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology. 2007;88:42.
Ramos R, Gonzalez-Solis J. Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front Ecol Environ. 2012;10:258.
Boecklen WJ, Yarnes CT, Cook BA, James AC. On the use of stable isotopes in trophic ecology. Annu Rev Ecol Evol Syst. 2011;42:411.
Newsome SD, Clementz MT, Koch PL, et al. Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mamm Sci. 2010;26:509.
Connolly RM, Schlacher TA. Sample acidification significantly alters stable isotope ratios of sulfur in aquatic plants and animals. Mar Ecol Prog Ser. 2013;493:1.
Caut S, Angulo E, Courchamp F. Variation in discrimination factors (Δ15N and Δ13C): The effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol. 2009;46:443.
Roth JD, Hobson KA. Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive seals: implications for dietary reconstruction. Can J Zool. 1996;78:848.
Hobson KA, Schell DM, Renouf D, Noseworthy E. 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. 1996;53:528.
Wolf N, Carleton SA, Martínez del Rio C. Ten years of experimental animal isotopes ecology. Funct Ecol. 2009;23:17.
Fossi MC, Marsili L. The use of non-destructive biomarkers in the study of marine mammals. Biomarkers. 1997;2:205.
Jaspers VLB, Voorspoels S, Covaci A, Lepoint G, Eens M. Evaluation of the usefulness of bird feathers as a non-destructive biomonitoring tool for organic pollutants: A comparative and meta-analytical approach. Environ Int. 2007;33:328.
Weijs L, Covaci A, Yang RSH, Das K, Blust R. A non-invasive approach to study lifetime exposure and bioaccumulation of PCBs in protected marine mammals: PBPK modeling in harbor porpoises. Toxicol Appl Pharmacol. 2011;256:136.
Lesage V, Hammill MO, Kovacs KM. Diet-tissue fractionation of stable carbon and nitrogen isotopes in phocid seals. Mar Mamm Sci. 2002;18:182.
Bond AL, Diamond AW. Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl. 2011;21:1017.
Phillips DL, Inger R, Bearhop S, et al. Best practices for use of stable isotope mixing models in food web studies. Can J Fish Aquat Sci. 2014;835:823.
Kovacs KM. Cystophora cristata, hooded seal. IUCN Red List Threat Species. 2016;17:
Bellido JJ, Castillo JJ, Farfán MA, Martín JJ, Mons JL, Real R. First records of hooded seals (Cystophora cristata) in the Mediterranean Sea. Mar Biodivers Rec. 2008. https://doi.org/10.1017/S1755267207007804
Laidre KL, Stirling I, Lowry LF, Wiig, Heide-Jørgensen MP, Ferguson SH. Quantifying the sensitivity of arctic marine mammals to climate-induced habitat change. Ecol Appl. 2008;18:97.
Friedlaender AS, Johnston DW, Fink SL, Lavigne DM. Variation in ice cover on the east coast of Canada, Implications for harp and hooded seals. Environment. 2006;29:1.
Øigård TA, Haug T, Nilssen KT. Current status of hooded seals in the Greenland Sea. Victims of climate change and predation? Biol Conserv. 2014;172:29.
Healy K, Kelly SBA, Guillerme T, Inger R, Bearhop S, Jackson AL. Predicting trophic discrimination factor using Bayesian inference and phylogenetic, ecological and physiological data. DEsIR:Discrimination estimation in R. PeerJPreprints. 2016. https://doi.org/10.7287/peerj.preprints.1950v3
Gentry RL, Holt JR. Equipment and techniques for handling northern fur seals. NOAA Technical Report NMFS SSRF-758. 1982;15.
Wiig Ø. Morphometric variation in the hooded seal (Cystophora cristata). J Zool London. 1985;206:497.
Coplen TB. Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom. 2011;25:2538.
McConnaughey T, McRoy CP. Foodweb structure and the fractionation of carbon isotopes in the Bering Sea. Mar Biol. 1979;53:257.
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG. Getting to the fat of the matter: Models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia. 2007;152:179.
Lazic SE. Package "desiR 1.2". 2016;12.
Bearhop S, Waldron S, Votier SC, Furness RW. Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool. 2002;75:451.
Hobson KA, Clark RG. Assessing avian diets using stable isotopes II: Factors influencing diet-tissue fractionation. Condor. 1992;94:189.
Germain LR, Koch PL, Harvey J, McCarthy MD. Nitrogen isotope fractionation in amino acids from harbor seals: Implications for compound-specific trophic position calculations. Mar Ecol Prog Ser. 2013;482:265.
Germain LR, Mccarthy MD, Koch PL, Harvey JT. Stable carbon and nitrogen isotopes in multiple tissues of wild and captive harbor seals (Phoca vitulina) off the California coast. Mar Mamm Sci. 2012;28:542.
Roth JD, Hobson KA. Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction. Can J Zool. 2000;78:848.
Beltran RS, Peterson SH, McHuron EA, Reichmuth C, Hückstädt LA, Costa DP. Seals and sea lions are what they eat, plus what? Determination of trophic discrimination factors for seven pinniped species. Rapid Commun Mass Spectrom. 2016;30:1115.
Kurle CM. Stable-isotope ratios of blood components from captive northern fur seals (Callorhinus ursinus) and their diet: applications for studying the foraging ecology of wild otariids. Can J Zool. 2002;80:902.
McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos. 2003;102:378.
Kelly JF. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool. 2000;78:1.
Hesslein RH, Hallard KA, Ramlal P. Replacement of sulfur, 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. 1993;50:2071.
Vander Zanden MJ, Rasmussen JB. Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnol Oceanogr. 2001;46:2061.
Vanderklift MA, Ponsard S. Sources of variation in consumer-diet δ15N enrichment: A meta-analysis. Oecologia. 2003;136:169.
Ambrose SH, Norr L. Carbon isotopic evidence for routing of dietary protein to bone collagen, and whole diet to bone apatite carbonate: purified diet growth experiments. In: Lambert J, Grupe G, eds. Prehistoric Human Bone: Archaeology at the Molecular Level. Berlin: Springer-Verlag; 1993:1-37.
Kelly LJ, Martinez C, Rio D. The fate of carbon in growing fish: An experimental study of isotopic routing. Phy.ihhgiciil und Biochem Zool. 2010;83:473.
Trueman CN, McGill RAR, Guyard PH. The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Commun Mass Spectrom. 2005;19:3239.
Kovacs KM, Lavigne DM. Maternal investment and neonatal growth in phocid seals. J Anim Ecol. 1986;55:1035.
Arnould JPY, Luque SP, Guinet C, Costa DP, Kingston J, Shaffer SA. The comparative energetics and growth strategies of sympatric Antarctic and subantarctic fur seal pups at Iles Crozet. J Exp Biol. 2003;206:4497.
Martínez del Rio C, Carleton SA. How fast and how faithful: the dynamics of isotopic incorporation into animal tissues. J Mammal. 2012;93:353.
Alonso JC, Huecas V, Alonso JA, Abelenda M, Muñoz-Pulido R, Puerta ML. Hematology and blood chemistry of adulto white storks (Ciconia ciconia). Comp Biochem Physiol. 1991;98:395.
Reitsema LJ. Beyond diet reconstruction: Stable isotope applications to human physiology, health, and nutrition. Am J Hum Biol. 2013;25:445.
Petzke KJ, Feist T, Fleig WE, Metges CC. Nitrogen isotopic composition in hair protein is different in liver cirrhotic patients. Rapid Commun Mass Spectrom. 2006;20:2973.
Hobson K, Clark R. Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor. 1992;94:181.
Pearson SF, Levey DJ, Greenberg CH, Martínez Del Rio C. Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia. 2003;135:516.
Robbins CT, Felicetti LA, Sponheimer M. The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia. 2005;144:534.
Adams TS, Sterner RW. The effect of dietary nitrogen content on trophic level 15N enrichment. Limnol Oceanogr. 2000;45:601.
Cherel Y, Hobson KA, Bailleul F, Groscolas R. Nutrition, physiology, and stable isotopes: New information from fasting and molting penguins. Ecology. 2005;86:2881.
Hayes JM. Fractionation of the isotopes of carbon and hydrogen in biosynthetic processes. Rev Mineral Geochem. 2001;43:225.
Howland MR, Corr LT, Young SMM, et al. Expression of the dietary isotope signal in the compound-specific δ13C values of pig bone lipids and amino acids. Int J Osteoarchaeol. 2003;13:54.
Hare PE, Fogel ML, Stafford TWJ, Mitchelf AD, Hoeringa TC. The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. J Archaeol Sci. 1991;18:277.
Atherton PJ, Smith K. Muscle protein synthesis in response to nutrition and exercise. J Physiol. 2012;590:1049.
Brosnan J, Brosnan M. The sulfur-containing amino acids: An overview. J Nutr. 2006;136:16365.
Parcell S, Cand ND. Sulfur in human nutrition applications in medicine. Altern Med Rev. 2002;7:22.
Bragulla HH, Homberger DG. Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. J Anat. 2009;214:516.
Kanatous SB, Hawke TJ, Trumble SJ, et al. The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals. J Exp Biol. 2008;211:2559.
Vázquez-Medina JP, Zenteno-Savín T, Elsner R. Glutathione protection against dive-associated ischemia/reperfusion in ringed seal tissues. J Exp Mar Biol Ecol. 2007;345:110.
