Trophic-level interpretation based on δ15N values: Implications of tissue-specific fractionation and amino acid composition

Marine Ecology Progress Series

Volumn 266, Issue , 2004, Pages 43-58

  Schmidt, Katrin ^a,d   McClelland, James W ^b,e   Mente, Eleni ^c   Montoya, Joseph P ^b   Atkinson, Angus ^d   Voss, Maren ^a  

^a LEIBNIZ INSTITUTE FOR BALTIC SEA RESEARCH   (Germany)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d BRITISH ANTARCTIC SURVEY   (United Kingdom)

^e ECOSYSTEMS CENTER   (United States)

Author keywords

Amino acids; Euphausia superba; Female; Male; Stable isotopes; Tissue; 15N

Indexed keywords

AMINO ACID; BIOCHEMICAL COMPOSITION; DIET; METABOLISM; METHODOLOGY; PHYSIOLOGY; STABLE ISOTOPE; TROPHIC INTERACTION; ZOOPLANKTON;

SOUTHERN OCEAN;

EUPHAUSIA; EUPHAUSIA SUPERBA; EUPHAUSIACEA; INVERTEBRATA;

EID: 1342268746     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps266043     Document Type: Article

References (73)

1. Adams E, Frank L (1980) Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 49:1005-1061
2. 15N enrichment. Limnol Oceanogr 45:601-607
3. Ballantyne JS (2001) Amino acid metabolism. In: Wright PA, Anderson PM (eds) Nitrogen excretion. Academic Press, London, p 77-107
4. Carter CG, Houlihan DF (2001) Protein synthesis. In: Wright PA, Anderson PM (eds) Nitrogen excretion. Academic Press, London, p 31-75
5. Chang CF, Lee FY, Huang YS (1993) Purification and characterization of vitellin from the mature ovaries of prawn, Penaeus monodon. Comp Biochem Physiol 1056:409-414
6. Claybrook DL (1983) Nitrogen metabolism. In: Mantel LH (ed) The biology of Crustacea, Vol. 5. Internal anatomy and physiological regulation. Academic Press, New York, p 163-213
7. Conceição LEC, d Meeren T, Verreth JAJ, Evjen MS, Houlihan DF, Fyhn HJ (1997) Amino acid metabolism and protein turnover in larval turbot (Scophthalmus maximus) fed natural zooplankton or Artemia. Mar Biol 129:255-265
8. Cripps GC, Watkins JL, Hill HJ, Atkinson A (1999) Fatty acid content of Antarctic krill Euphausia superba at South Georgia related to regional populations and variations in diet. Mar Ecol Prog Ser 181:177-188
9. Cuzin-Roudy J (2000) Seasonal reproduction, multiple spawning, fecundity in the northern krill, Meganyctiphanes norvegica, Antarctic krill, Euphausia superba. In: Proc 2nd Int Krill Symp, Santa Cruz, California, August 1999. Can J Fish Aquat Sci 57:6-15
10. Dali W, Smith DM (1987) Changes in protein-bound and free amino acids in the muscle of the tiger prawn Penaeus esculentus during starvation. Mar Biol 95:509-520
11. DeNiro M J, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341-351
12. Dy-Penaflorida V, Millamena OM (1990) Variation in the biochemical composition of Penaeus monodon tissues during the reproductive cycle. Isr J Aquac Bamidgeh 42:84-90
13. Fantle MS, Dittel AI, Schwalm SM, Epifanio CE, Fogel ML (1999) A food web analysis of the juvenile blue crab, Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120:416-426
14. Ferguson CF, Raymont JKB (1974) Biochemical studies on marine zooplankton. XII Further investigations on Euphausia superba Dana. J Mar Biol Assoc UK 54:719-725
15. Gannes LZ, O'Brien DM, d Rio CM (1997) Stable isotopes in animal ecology: assumptions, caveats, a call for more laboratory experiments. Ecology 78:1271-1276
16. Gunasekera RM, Shim KF, Lam TJ (1997) Influence of dietary protein content on the distribution of amino acids in oocytes, serum and muscle of Nile tilapia, Oreochromis niloticus (L). Aquaculture 152:205-221
17. Hare PE, Fogel ML, Stafford TW, Mitchell Jr AD, Hoering TC (1991) The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. J Archaeolog Sci 18:77-292
18. Hawkins AJS (1985) Relationships between the synthesis and breakdown of protein, dietary absorption and turnovers of nitrogen and carbon in the blue mussel, Mytilus edulis L. Oecologia 66:29-42
19. Hewitt DR (1992) Response of protein turnover in the brown tiger prawn Penaeus esculentus to variation in dietary protein content. Comp Biochem Physiol 103A:183-187
20. Hird FJR, Cianciosi SC, McLean RM (1986) Investigations of the origin and metabolism of the carbon skeleton of ornithine, arginine and proline in selected animals. Comp Biochem Physiol 836:179-184
21. 13C in tissues. Condor 94:181-188
22. Hobson KA, Clark RG (1992b) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189-197
23. 15N analysis. Mar Ecol Prog Ser 84:9-18
24. Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissue due to fasting and nutritional stress: implications for isotopic analysis of diet. Condor 95:388-394
25. 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
26. Hochachka PW, Mommsen TP, Storey J, Storey KB, Johansen K, French CJ (1983) The relationship between arginine and proline metabolism in cephalopods. Mar Biol Lett 4:1-21
27. 13C) analyses. Mar Ecol Prog Ser 198:273-281
28. Hopkins TL, Lancraft TM, Torres JJ, Donelley J (1993) Community structure and trophic ecology of zooplankton in the Scotia Sea marginal ice zone in winter (1988). Deep-Sea Res 40:81-105
29. Houlihan DF, Waring CP, Mathers E, Gray C (1990) Protein synthesis and oxygen consumtion of the shore crab Carcinus maenas after a meal. Physiol Zool 63:735-756
30. Houlihan DF, Carter CG, McCarthy ID (1995) Protein synthesis in fish. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fish. Elsevier Science BV, Amsterdam, p 191-220
31. Ikeda T, Dixon P (1982) Body shrinkage as a possible overwintering mechanism of the Antarctic krill, Euphausia superba Dana. J Exp Mar Biol Ecol 62:143-151
32. Kiørboe T, Munk P, Richardson K (1987) Respiration and growth of larval herring Clupea harengus: relation between specific dynamic action and growth efficiency. Mar Ecol Prog Ser 40:1-10
33. Kiyashko SI, Narita T, Wada E (2001) Contribution of methanotrophs to freshwater macroinvertebrates: evidence from stable isotope ratios. Aquat Microb Ecol 24:203-207
34. Kurie CM (2002) 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 80:902-909
35. Lee EH, Kim SK, Cho DJ, Han BH (1979) Processing of krill soluble and its amino acid composition. Bull Korean Fish Soc 12:235-240
36. Lesage V, Hammill MO, Kovacs KM (2001) Marine mammals and the community structure of the Estuary and Gulf of St Lawrence, Canada: evidence from stable isotope analysis. Mar Ecol Prog Ser 210:203-221
37. Macko SA, Lee WY, Parker PL (1982) Nitrogen and carbon isotope fractionation by two species of marine amphipods: laboratory and field studies. J Exp Mar Biol Ecol 63:145-150
38. Macko SA, Fogel-Estep ML, Engel MH, Hare PE (1986) Kinetic fractionation of nitrogen isotopes during amino acid transamination. Geochem Cosmochim Acta 50:2143-2146
39. Macko SA, Fogel-Estep ML, Engel MH, Hare PE (1987) Isotopic fractionation of nitrogen and carbon in the synthesis of amino acids by microorganisms. Chemical Geol 65:79-92
40. Makarov RR, Denys CJ (1981) Stages of sexual maturity of Euphausia superba. Biomass handbook no. 11. SCAR, Cambridge, p 1-13
41. Mayzaud P, Albessard E, Cuzin-Roudy J (1998) Changes in lipid composition of the Antarctic krill Euphausia superba in the Indian sector of the Antarctic Ocean: influence of geographical location, sexual maturity stage and distribution among organs. Mar Ecol Prog Ser 173:149-162
42. McClelland JW, Montoya JP (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83:2173-2180
43. McCoid V, Miget R, Finne G (1984) Effect of environmental salinity on the free amino acid composition and concentration in penaeid shrimp. J Food Sci 49:327-330
44. 15N isotopic abundances in physiological samples: a pilot study on amino acid synthesis in the upper gastrointestinal tract of minipigs. J Mass Spectrometry 31:367-376
45. Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine aquatic food webs. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and enviromental science. Blackwell Scientific Publications, Oxford, p 138-158
46. Nelson DL, Cox MM (2001) Lehninger Biochemie, 3rd edn. Springer-Verlag, Berlin
47. Ng WK, Hung SSO (1994) Amino acid composition of whole body, egg and selected tissues of white sturgeon (Acipenser transmontanus). Aquaculture 126:329-39
48. Nicol S (2000) Understanding krill growth and aging: the contribution of experimental studies. Can J Fish Aquat Sci 57:168-177
49. Nicol S, Stolp M, Cochran T, Geijsel P, Marshall J (1992) Summer growth and shrinkage of Antarctic krill Euphausia superba from the Indian Ocean sector of the Southern Ocean during summer. Mar Ecol Prog Ser 89:175-181
50. O'Reilly CM, Hecky RE, Cohen AS, Plisnier PD (2002) Interpreting stable isotopes in food webs: recognizing the role of time averaging at different trophic levels. Limnol Oceanogr 47:306-309
51. Partmann W (1981) Freie und gesamte Aminosäuren im Muskelfleisch vom Weissblutfisch (Champsocephalus gunnari Lönnberg) und vom Krill (Euphausia superba Dana). Z Ernährwiss 20:163-171
52. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293-320
53. 15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225-231
54. Pond D, Watkins J, Priddle J, Sargent J (1995) Variation in the lipid content and composition of Antarctic krill Euphausia superba at South Georgia. Mar Ecol Prog Ser 117:49-57
55. Priddle J, Watkins J, Morris D, Ricketts C, Buchholz F (1990) Variation of feeding by krill in swarms. J Plankton Res 12:1189-1205
56. Quetin LB, Ross RM (1991) Behavioral and physiological characteristics of the Antarctic krill, Euphausia superba. Am Zool 31:49-63
57. Qui YW, Ng TB, Chu KH (1997) Purification and characterization of vitellin from the ovaries of the shrimp Metapenaeus ensis (Crustacea: Decapoda: Penaeidae). Invertebr Reprod Dev 31:217-223
58. 12C in Weddell Sea invertebrates: implications for feeding diversity. Mar Ecol Prog Ser 77:1-6
59. Ross RM, Quetin LB (2000) Reproduction in Euphausiacea. In: Everson I (ed) Krill: biology, ecology and fisheries. Blackwells, New York, p 150-181
60. Schmidt K, Atkinson A, Stübing D, McClelland JW, Montoya JP, Voss M (2003) trophic relationships among Southern Ocean copepods and krill: some uses and limitations of a stable isotope approach. Limnol Oceanogr 48:277-289
61. 13C techniques. Mar Biol 103:433-443
62. Schwamborn R, Ekau W, Voss M, Saint-Paul U (2002) How important are mangroves as a carbon source for decapod crustacean larvae in a tropical estuary? Mar Ecol Prog Ser 229:195-205
63. Srinivasagam RT, Raymont JE, Moodie CF, Raymont JKB (1971) Biochemical studies on marine zooplankton. X. The amino acid composition of Euphausia superba, Meganyctiphanes norvegica and Neomysis integer. J Mar Biol Assoc UK 51:917-925
64. 15N for tracer studies. J Agric Sci 90:7-9
65. 13C analysis of diet. Oecologia 57:32-37
66. Tom M, Fingermann M, Hayes TK, Johnson V, Kerner B, Lubzens E (1992) A comparative study of the ovarian proteins from two penaid shrimps, Penaeus semisulcatus de Haan and Penaeus vannamei (Boone). Comp Biochem Physiol 1026:483-490
67. Torres C (1973) Variations du pool des acides aminés libres du musclé abdominal de Penaeus kerathurus au cours du cycle d'intermue, et au cours du jeûne. Comp Biochem Physiol 45B:1-12
68. Virtue P, Nicol S, Nichols PD (1993) Changes in the digestive gland of Euphausia superba during short-term starvation: lipid class, fatty acid and sterol content and composition. Mar Biol 117:441-448
69. Virtue P, Nichols PD, Nicol S, Hosie G (1996) Reproductive trade off in male Antarctic krill. Mar Biol 126:521-527
70. Volz DC, Kawaguchi T, Chandler GT (2002) Purification and characterization of the common yolk protein, vitellin, from the estuarine amphipod Leptocheirus plumulosus. Prep Biochem Biotechnol 32:103-116
71. 13C abundances in the Antarctic Ocean with emphasis on the biogeochemical structure of the food web. Deep-Sea Res 34:829-841
72. Wilson RP, Poe WE (1985) Relationship of whole body and egg essential amino acid patterns to amino acid requirement patterns in channel catfish, Ictalurus punctatus. Comp Biochem Physiol 806:385-388
73. Zhang N, Yamashita Y, Nozaki Y (2002) Effect of protein hydrolysate from Antarctic krill meat on the state of water and denaturation by dehydration of lizard fish myofibrils. Fish Sci 68:672-679