Naturally-occurring stable isotopes as direct measures of larval feeding efficiency, nutrient incorporation and turnover

Aquaculture

Volumn 315, Issue 1-2, 2011, Pages 95-103

  Le Vay, Lewis ^a   Gamboa Delgado, Julián ^b  

^a BANGOR UNIVERSITY   (United Kingdom)

^b UNIVERSIDAD AUTÓNOMA DE NUEVO LEÓN   (Mexico)

Author keywords

Assimilation; Larval nutrition; Metabolic turnover; Stable isotopes

Indexed keywords

AQUATIC ECOSYSTEM; ARTIFICIAL DIET; ASSIMILATION EFFICIENCY; BIOACCUMULATION; ENERGY FLOW; EXPERIMENTAL CULTURE; FOOD CHAIN; GROWTH RATE; HATCHERY; INVERTEBRATE; ISOTOPIC ANALYSIS; ISOTOPIC COMPOSITION; LARVICULTURE; MESOCOSM; PLANKTON; STABLE ISOTOPE; TURNOVER;

ARTEMIA; ROTIFERA;

EID: 84879223991     PISSN: 00448486     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquaculture.2010.03.033     Document Type: Article

References (109)

1. Al-Maslamani, I.A., 2006. Feeding and nutrition in the marine shrimp Penaeus semisulcatus. PhD Thesis. University of Wales, UK. 179pp.
2. Al-Maslamani I., Le Vay L., Kennedy H. Feeding on intertidal microbial mats by postlarval tiger shrimp, Penaeus semisulcatus De Haan. Mar. Biol. 2009, 156:2001-2009.
3. Bell M.V., Dick J.R., Anderson T.R., Pond D.W. Application of liposome and stable isotope tracer techniques to study polyunsaturated fatty acid biosynthesis in marine zooplankton. J. Plankton Res. 2007, 29:417-422.
4. Beltran M., Fernandez-Borras J., Medale F., Perez-Sanchez J., Kaushik S., Blasco J. Natural abundance of 15N and 13C in fish tissues and the use of stable isotopes as dietary protein tracers in rainbow trout and gilthead sea bream. Aquacult. Nutr. 2008, 15:9-18.
5. Ben-David M., Hanley T.A., Klein D.R., Schell D.M. Seasonal changes in diets of coastal and riverine mink: the role of spawning Pacific salmon. Can. J. Zool. 1997, 75:803-811.
6. Berthold H.K., Hachey D.L., Reeds P.J., Thomes O.P., Klein P.D. Uniformly 13C-labeled algal protein used to determine amino acid essentiality in vivo. PNAS 1991, 88:8091-8095.
7. Bombeo-Tuburan I., Guanzon N.G., Schroeder G.L. Production of Penaeus monodon (Fabricius) using four natural food types in an extensive system. Aquaculture 1993, 112:57-65.
8. Bosley K.L., Witting D.A., Chambers R.C., Wainright S.C. Estimating urnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes. Mar. Ecol. Prog. Ser. 2002, 236:233-240.
9. Burford M.A., Preston N.P., Glibert P.M., Dennison W.C. Tracing the fate of 15N-enriched feed in an intensive shrimp system. Aquaculture 2002, 206:199-216.
10. Burford M.A., Preston N.P., Minh T.H., Hoa T.T.T., Bunn S.E., Fry V.M. Dominant sources of dietary carbon and nitrogen for shrimp reared in extensive rice-shrimp ponds. Aquac. Res. 2004, 35:194-203.
11. Burford M.A., Sellars M.J., Arnold S.J., Keys S.J., Crocos P.J., Preston N.P. Contribution of the natural biota associated with substrates to the nutritional requirements of post-larval shrimp (Penaeus esculentus) in high-density rearing systems. Aquac. Res. 2004, 35:508-515.
12. Cabana G., Rasmussen J.B. Comparison of aquatic food chains using nitrogen isotopes. Proc. Natl Acad. Sci. U. S. A. 1996, 93:10844-10847.
13. Carter C.G., Owen S.F., He Z.Y., Watt P.W., Scrimgeour C., Houlihan D.F., Rennie M.J. Determination of protein synthesis in rainbow trout, Onchorhynchus mykiss, using a stable isotope. J. Exp. Biol. 1994, 189:279-284.
14. Carter C.G., Houlihan D.F., Owen S.F. Protein synthesis, nitrogen excretion and long-term growth of Pleuronectes flesus. J. Fish Biol. 1998, 53:272-284.
15. 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, 46:443-453.
16. Chikaraishi Y., Kashiyama Y., Ogawa N.O., Kitazato H., Ohkouchi N. Metabolic control of nitrogen isotope composition of amino acids in macroalgae and gastropods: implications for aquatic food web studies. Mar. Ecol. Prog. Ser. 2007, 342:85-90.
17. Comtet T., Riera P. δ13C and δ15N changes after dietary shift in veliger larvae of the slipper limpet Crepidula fornicata: an experimental evidence. Helgol. Mar. Res. 2006, 60:281-288.
18. Conceição L.E.C., Skjermo J., Skjåk-Bræk G., Verreth J.A.J. Effect of an immunostimulating alginate on protein turnover of turbot (Scophthalmus maximus L) larvae. Fish Physiol. Biochem. 2001, 24:207-212.
19. Conceição L.E.C., Morais S., Rønnestad I. Tracers in fish larvae nutrition: a review of methods and applications. Aquaculture 2007, 267:62-75.
20. Crawley K.R., Hyndes G.A., Vanderklift M.A. Variation among diets in discrimination of δ13C and δ15N in the amphipod Allorchestes compressa. J. Exp. Mar. Biol. Ecol. 2007, 349:370-377.
21. DeNiro M.J., Epstein S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Ac. 1978, 42:495-506.
22. DeNiro M.J., Epstein S. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Ac. 1981, 45:341-351.
23. Dittel A.I., Epifanio C.E., Cifuentes L.A., Kirchman D.L. Carbon and nitrogen sources for shrimp postlarvae fed natural diets from a tropical mangrove system. Estuar. Coas. Shelf S. 1997, 45:629-637.
24. Epp M.A., Ziemann D.A., Schell D.M. Carbon and nitrogen dynamics in zero-water exchange shrimp culture as indicated by stable isotope tracers. Aquac. Res. 2002, 33:839-846.
25. Fantle M.S., Dittel A.I., Schwalm S., Epifanio C.E., Fogel M.L. A foodweb analysis of the juvenile crab Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 1999, 120:416-426.
26. Fraser K.P.P., Rogers A.D. Protein metabolism in marine animals: the underlying mechanism of growth. Adv. Mar. Biol. 2007, 52:267-362.
27. Fraser K.P.P., Lyndon A.R., Houlihan D.F. Protein synthesis and growth in juvenile Atlantic halibut, Hippoglossus hippoglossus (L.): application of 15N stable isotope tracer. Aquac. Res. 1998, 29:289-298.
28. Fry B. Stable isotope diagrams of freshwater food webs. Ecology 1991, 72:2293-2297.
29. Fry B. Stable Isotope Ecology 2006, Springer Science, NY, USA, 390pp.
30. Fry B., Arnold C. Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 1982, 54:200-204.
31. Fry B., Sherr E.B. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib. Mar. Sci. 1984, 27:13-47.
32. Gamboa-Delgado J., Le Vay L. Nitrogen stable isotopes as indicators of the relative contribution of soy protein and fish meal to tissue growth in Pacific white shrimp (Litopenaeus vannamei) fed compound diets. Aquaculture 2009, 291:115-123.
33. Gamboa-Delgado J., Le Vay L. Artemia replacement in co-feeding regimes for mysis and postlarval stages of Litopenaeus vannamei: nutritional contribution of inert diets to tissue growth as indicated by natural carbon stable isotopes. Aquaculture 2009, 297:128-135.
34. Gamboa-Delgado J., Cañavate J.P., Zerolo R., Le Vay L. Natural carbon stable isotope ratios as indicators of the relative contribution of live and inert diets to growth in larval Senegalese sole (Solea senegalensis). Aquaculture 2008, 280:190-197.
35. Garlick P.J., McNurlan M.A., Preedy V.R. A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of phenylalanine-H-3. Biochem. J. 1980, 192:719-723.
36. Gentsch E., Kreibich T., Hagen W., Niehoff B. Dietary shifts in the copepod Temora longicornis during spring: evidence from stable isotope signatures, fatty acid biomarkers and feeding experiments. J. Plankton Res. 2009, 31:45-60.
37. Hentschel B.T. Intraspecific variations in δ13C indicate ontogenetic diet changes in deposit-feeding polychaetes. Ecology 1998, 79:1357-1370.
38. Herzka S.Z., Holt G.J. Changes in isotopic composition of red drum (Sciaenops ocellatus) larvae in response to dietary shifts: potential applications to settlement studies. Can. J. Fish. Aquat. Sci. 2000, 57:137-147.
39. Herzka S.Z., Holt S.A., Holt J.G. Documenting the settlement history of individual fish larvae using stable isotope ratios: model development and validation. J. Exp. Mar. Biol. Ecol. 2001, 265:49-74.
40. Hesslein R.H., Hallard K.A., 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 34S, 13C, and 15N. Can. J. Fish. Aquat. Sci. 1993, 50:2071-2076.
41. Hinga K.R., Arthur M.A., Pilson M.E.Q., Whitaker D. Carbon isotope fractionation by marine phytoplankton in culture: the effects of CO2 concentration, pH, temperature, and species. Global Biogeochem. Cycles 1994, 8:91-102.
42. Hino A., Aoki S., Ushiro M. Nitrogen flow in the rotifer Brachionus rotundiformis and its significance in mass cultures. Hydrobiologia 2004, 358:77-82.
43. Hobson K.A., Smith R.J.F., Sorensen P.W. Applications of stable isotope analysis to tracing nutrient sources of Hawaiian gobioid fishes and other stream organisms. Biology of Hawaiian Streams and Estuaries 2006, Hawai'i, Bishop Museum Bulletin in Cultural and Environmental Studies, Honolulu. N.L. Evenhuis, J.M. Fitzsimons (Eds.).
44. Houlihan D.F., Hall S.J., Gray C., Noble B.S. Growth rates and protein turnover in Atlantic cod, Gadus morhua. Can. J. Fish. Aquat. Sci. 1988, 45:951-964.
45. Houlihan D.F., McCarthy I.D., Carter C.G., Marttin F. Protein turnover and amino acid flux in fish larvae. ICES Mar. Sci. Symp. 1995, 201:87-99.
46. Houlihan D.F., Carter C.G., McCarthy I.D. Protein turnover in animals. Chapter 1. Nitrogen Metabolism and Excretion 1995, 1-31. CRC Press, Boca Raton, FL, USA. P.J. Walsh, P. Wright (Eds.).
47. Johnston A.M., Raven J.A. Effect of aeration rates on growth rates and natural abundance of 13C/l2C ratio of Phaeodactylum tricornuttlrn. Mar. Ecol. Prog. Ser. 1992, 87:295-300.
48. Jomori R.K., Ducatti C., Carneiro D.J., Portella M.C. Stable carbon (δ13C) and nitrogen (δ15N) isotopes as natural indicators of live and dry food in Piaractus mesopotamicus (Holmberg, 1887) larval tissue. Aquac. Res. 2008, 39:370-381.
49. Kelly J.F. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can. J. Zool. 2000, 78:1-27.
50. Koven W.M., Parra G., Kolkovski S., Tandler A. The effect of dietary phosphatidylcholine and its constituent fatty acids on microdiet ingestion and fatty acid absorption rate in gilthead seabream, Sparus auratus, larvae. Aquac. Nutr. 1998, 4:39-45.
51. Krummen M., Hilkert A.W., Juchelka D., Duhr A., Schluter H.-J., Pesch R. A new concept for isotope ratio monitoring liquid chromatography/mass spectrometry. Rap. Comm. Mass Spectrom. 2004, 18:2260-2266.
52. Leboulanger C., Descolas-Gros C., Fontugne M.R., Benteleb I., Jupin H. Interspecific variability and environmental influence on particulate organic carbon δ13C in cultured marine phytoplankton. J. Plankton Res. 1995, 17:2079-2091.
53. Lindholm M., Hessen D.O. Zooplankton succession on seasonal floodplains: surfing on a wave of food. Hydrobiology 2007, 592:95-104.
54. MacAvoy S.E., Macko S.A., Arneson L.S. Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Can. J. Zool. 2005, 83:631-641.
55. Martínez del Rio C., Wolf B.O. Mass-balance models for animal isotopic ecology. Physiological and Ecological Adaptations to Feeding in Vertebrates 2005, 141-174. Science Publishers, Enfield, NH. J.M. Starck, T. Wang (Eds.).
56. Zuanon J.A.S., Pezzato A.C., Ducatti C., Barros M.M., Pezzato L.E., Passos J.R.S. Muscle δ13C change in Nile tilapia (Oreochromis niloticus) fingerlings fed on C3- or C4-cycle plants grain-based diets. Comp. Biochem. Physiol. 2007, 147:761-765.
57. Martínez del Rio C., Wolf N., Carleton S.A., Gannes L.Z. Isotopic ecology ten years after a call for more laboratory experiments. Biol. Rev. 2009, 84:91-111.
58. Matsuda H., Takenouchi T., Tanaka S., Watanabe S. Relative contribution of Artemia and mussel as food for cultured middle-stage Panulirus japonicus phyllosomata as determined by stable nitrogen isotope analysis. N.Z. J. Mar. Freshwat. Res. 2009, 43:217-224.
59. McClelland J.W., Montoya J.P. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 2002, 83:2173-2180.
60. McCullagh J., Gaye-Siessegger J., Focken U. Determination of underivatized amino acid δ13C by liquid chromatography/isotope ratio mass spectrometry for nutritional studies: the effect of dietary non-essential amino acid profile on the isotopic signature of individual amino acids in fish. Rap. Commun. Mass Spect. 2008, 22:1817-1822.
61. McCutchan J.H., Lewis W.M., Kendall C., McGrath C.C. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 2003, 102:378-390.
62. McIntyre P.B., Flecker A.S. Rapid turnover of tissue nitrogen of primary consumers in tropical freshwaters. Oecologia 2006, 148:12-21.
63. Michener R.H., Schell D.M. Stable isotope ratios as tracers in marine aquatic food webs. Stable Isotopes in Ecology and Environmental Science. Chapter 7 1994, Vol 1. Blackwell scientific publications, Oxford, UK, 138-157pp. K. Lajtha, R.H. Michener (Eds.).
64. Minagawa M., Wada E. Stepwise enrichment of δ15N along food chains: further evidence and the relation between δ15N and animal age. Geochim. Cosmochom. Acta 1984, 48:1135-1140.
65. Moens T., Bouillon S., Gallucci F. Dual stable isotope abundances unravel trophic position of estuarine nematodes. J. Mar. Biol. Ass. UK 2005, 85:1401-1407.
66. Morais S., Koven W., Rønnestad I., Dinis M.T., Conceição L.E.C. Dietary protein/lipid ratio affects growth and amino acid and fatty acid absorption and metabolism in Senegalese sole (Solea senegalensis Kaup 1858) larvae. Aquaculture 2005, 246:347-357.
67. Nunes A.J.P., Gesteira T.C.V., Goddard S. Food ingestion and assimilation by the Southern brown shrimp Penaeus subtilis under semi-intensive culture in NE Brazil. Aquaculture 1997, 149:121-136.
68. O'Brien D.M., Boggs C.L., Fogel M.L. Pollen feeding in the butterfly Heliconius charitonia isotopic evidence for essential amino acid transfer from pollen to eggs. P. R. Soc. Lond. B Biol. 2003, 270:2631-2636.
69. O'Brien D.M., Boggs C.L., Fogel M.L. The amino acids used in reproduction by butterflies: a comparative study of dietary sources using compound-specific stable isotope analysis. Physiol. Biochem. Zool. 2005, 78:819-827.
70. Parker P.L., Anderson R.K., Lawrence A. A δ13C and δ15N tracer study of nutrition in aquaculture: Pennaeus vannamei in a pond growth system. Stable Isotopes in Ecological Research 1989, 288-307. Springer-Verlag, New York. P.W. Rundel, J.R. Ehleringr, K.A. Nagy (Eds.).
71. Parrish C.C., Whiticar M., Puvanendran V. Is ω6 docosapentaenoic acid an essential fatty acid during early ontogeny in marine fauna?. Limnol. Oceanogr. 2007, 52:476-479.
72. Pearson D.F., Levey D.J., Greenberg C.H., Martinez del Rio C. Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 2003, 135:516-523.
73. Peterson B.J., Fry B. Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Syst. 1987, 18:293-320.
74. Phillips D.L., Gregg J.W. Uncertainty in source partitioning using stable isotopes. Oecologia 2001, 127:171-179. see also erratum, Oecologia 128, 204.
75. Yokoyama H., Tamaki A., Harada K., Shimoda K., Koyama K., Ishihi Y. Variability of diet tissue isotopic fractionation in estuarine macrobenthos. Mar. Ecol. Prog. Ser. 2005, 296:115-128.
76. Phillips D.L., Gregg J.W. Source partitioning using stable isotopes: coping with too many sources. Oecologia 2003, 136:261-269.
77. Post D.M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002, 83:703-718.
78. Power M., Guiguer K.R.R.A., Barton D.R. Effects of temperature on isotopic enrichment in Daphnia magna: implications for aquatic food-web studies. Rapid Comm. Mass Spectrom. 2003, 17:1619-1625.
79. Preston T. The measurement of stable isotope natural abundance variations. Plant Cell Environ. 1992, 15:1091-1097.
80. Preston T., Slater C. Mass spectrometric analysis of stable isotope labelled amino acid tracers. P. Nutr. Soc. 1994, 53:363-372.
81. Robbins C.T., Felicetti L.A., Sponheimer M. The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 2005, 144:534-540.
82. Rønnestad I., Rojas-García C.R., Tonheim S.K., Conceição L.E.C. In vivo studies of digestion and nutrient assimilation in marine fish larvae. Aquaculture 2001, 201:161-175.
83. Rossi F., Herman P.M.J., Middelburg J.J. Interspecific and intraspecific variation of ω13C and ω15N in deposit- and suspension-feeding bivalves (Macoma balthica and Cerastoderma edule): evidence of ontogenetic changes in feeding mode of Macoma balthica. Limnol. Oceanogr. 2004, 49:408-414.
84. Saavedra M., Beltran M., Pousão-Ferreira P., Dinis M.T., Blasco J., Conceição L.E.C. Evaluation of bioavailability of individual amino acids in Diplodus puntazzo larvae: towards the ideal dietary amino acid profile. Aquaculture 2007, 263:192-198.
85. Sato M., Sasaki H., Fukuchi M. Stable isotopic compositions of over-wintering copepods in the arctic and subarctic waters and implications for the feeding history. J. Mar. Syst. 2002, 38:165-174.
86. Schlechtriem C., Focken U., Becker K. Stable isotopes as a tool for nutrient assimilation studies in larval fish feeding on live food. Aquat. Ecol. 2004, 38:93-100.
87. Schlechtriem C., Focken U., Becker K. Digestion and assimilation of the free-living nematode Panagrellus redivivus fed to first feeding coregonid larvae: evidence from histological and isotopic studies. J. World Aquac. Soc. 2005, 36:24-31.
88. Schmidt K., McClelland J.W., Mente E., Montoya J.P., Atkinson A., Voss M. Trophic-level interpretation based on delta N-15 values: implications of tissue-specific fractionation and amino acid composition. Mar. Ecol. Progr. Ser. 2004, 266:43-58.
89. Schroeder G.L. Sources of fish and prawn growth in polyculture ponds as indicated by ω13C analysis. Aquaculture 1983, 35:29-42.
90. Schwamborn R., Ekau W., Voss M., Saint-Paul U. How important are mangroves as a carbon source for decapod crustacean larvae in a tropical estuary?. Mar. Ecol. Prog. Ser. 2002, 229:195-205.
91. Spero H.J., Andreasen D.J., Sorgeloos E. Carbon and nitrogen isotopic composition of different strains of Artemia sp. Int. J. Salt Lake Res. 1993, 2:133-139.
92. Stenroth P., Holmqvist N., Nyström P., Berglund O., Larsson P., Granéli W. Stable isotopes as an indicator of diet in omnivorous crayfish (Pacifastacus leniusculus): the influence of tissue, sample treatment and season. Can. J. Fish. Aquat. Sci. 2006, 63:821-831.
93. Teshima S., Kanasawa A. Biosynthesis of sterols in the lobster, Panulirus japonica, the prawn, Penaeus japonicus, and the crab, Ponunus trituberculatus. Comp. Biochem. Physiol. 1971, 38B:597-602.
94. Teshima S., Kanasawa A., Okamoto H. Sterol biosynthesis from acetate and the fate of dietary cholesterol and desmosterol in crabs. Bull. Jpn. Soc. Sci. Fish. 1976, 42:1273-1280.
95. Teshima S., Kanazawa A., Kakuta Y. Role of dietary phospholipids in the transport of [14C] cholesterol in the prawn. Bull. Jpn. Soc. Sci. Fish. 1986, 52:719-723.
96. Teshima S., Kanazawa A., Kakuta Y. Role of dietary phospholipids in the transport of [14C] tripalmitin in the prawn. Bull. Jpn. Soc. Sci. Fish. 1986, 52:519-524.
97. Tibbets T., Wheeless L., Martínez del Rio C.M. Isotopic enrichment without change in diet: an ontogenetic shift in δ15N during insect metamorphosis. Funct. Ecol. 2008, 22:109-113.
98. Tieszen L.L., Boutton T.W., Tesdahl K.G., Slade N.A. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 1983, 57:32-37.
99. Trimborn, S., 2008. Inorganic carbon acquisition of marine phytoplankton with emphasis on selected diatom species, Bremen, Univ., Diss., 155pp., Bremen, Univ., Dissertation. http://nbn-resolving.de/urn:nbn:de:gbv:46-diss000109393.
100. Van der Zanden M.J., Rasmussen J.B. Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol. Oceanogr. 2001, 46:2061-2066.
101. Van der Zanden M.J., Hulshof M., Ridgway M.S., Rasmussen J.B. Application of stable isotope techniques to trophic studies of age-0 smallmouth bass. Trans. Am. Fish. Soc. 1998, 127:729-739.
102. Yoshioka T., Wada E., Hayashi H. A stable isotope study on seasonal food web dynamics in a eutrophic lake. Ecology 1994, 75:835-846.
103. Van der Zanden M.J., Shuter B.J., Lester N., Rasmussen J.B. Patterns of food chain lengths in lakes: a stable isotope study. Am. Nat. 1999, 154:406-416.
104. Vanderklift M.A., Ponsard S. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 2003, 136:169-182.
105. Verschoor A.M., Boonstra H., Meijer T. Application of stable isotope tracers to studies of zooplankton feeding, using the rotifer Brachionus calyciflorus as an example. Hydrobiologia 2005, 546:535-549.
106. Waddington K., MacArthur L. Diet quality and muscle tissue location influence consumer-diet discrimination in captive-reared rock lobsters (Panulirus cygnus). Mar. Biol. 2008, 154:569-576.
107. Waterlow J.C. Protein turnover 2006, CABI International, Oxfordshire, UK, 320pp.
108. Yokoyama H., Abo K., Ishihi Y. Quantifying aquaculture-derived organic matter in the sediment in and around a coastal fish farm using stable carbon and nitrogen isotope ratios. Aquaculture 2006, 254:411-425.
109. Yokoyama H., Ishihi Y., Yamamoto S. Diet-tissue isotopic fractionation of the Pacific oyster Crassostrea gigas. Mar. Ecol. Prog. Ser. 2008, 358:173-179.