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Marine Biology

, Volume 158, Issue 12, pp 2847–2862 | Cite as

Carbon, nitrogen and phosphorus elemental stoichiometry in aquacultured and wild-caught fish and consequences for pelagic nutrient dynamics

  • Marie CzamanskiEmail author
  • Adi Nugraha
  • Philippe Pondaven
  • Marine Lasbleiz
  • Annick Masson
  • Nicolas Caroff
  • Robert Bellail
  • Paul Tréguer
Original Paper

Abstract

The elemental carbon (C), nitrogen (N) and phosphorus (P) compositions of the whole-body and gut content of wild marine fish inhabiting the Bay of Biscay (Northeast Atlantic) were studied. Furthermore, the literature was examined for studies of aquacultured fish, reporting the elemental composition of the whole-body fish, that of their food, and nutrient assimilation and gross growth efficiencies (GGE). In both wild-caught and aquacultured fish, significant differences in C, N and P elemental composition were found between species, with P being the most variable component. Differences among species in terms of C, N and P content could be explained by varying proportions of storage compounds in whole-body fish, and varying degrees of ossification. Aquacultured fish feces were found to be P-rich, because of a lower P assimilation efficiency, compared to C or N assimilation efficiencies. Examination of aquacultured fish literature also revealed that C, N and P GGE and nutrient resupply ratios agreed with basic principles of homeostatic regulation of whole-body fish elemental composition. Extrapolation of the results to broader marine systems indicated that fish may be important for conveying nutrients toward the ocean interior.

Keywords

Fecal Pellet Wild Fish Assimilation Efficiency Homeostatic Regulation Accumulation Efficiency 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This research was funded by the EU Marie Curie EST project METAOCEANS (MEST-CT-2005-019678) and supported by INSU/CNRS. The writers would like to thank Herwig Stibor and three anonymous reviewers for constructive comments on the manuscript.

Supplementary material

227_2011_1783_MOESM1_ESM.pdf (339 kb)
Supplementary material 1 (PDF 339 kb)
227_2011_1783_MOESM2_ESM.pdf (150 kb)
Supplementary material 2 (PDF 149 kb)
227_2011_1783_MOESM3_ESM.pdf (9 kb)
Supplementary material 3 (PDF 9 kb)

References

  1. Aguado F, Martinez FJ, Garcia-Garcia B (2004) In vivo total nitrogen and total phosphorous digestibility in Atlantic bluefin tuna (Thunnus thynnus thynnus Linnaeus, 1758) under industrially intensive fattening conditions in Southeast Spain Mediterranean coastal waters. Aquac Nutr 10:413–419CrossRefGoogle Scholar
  2. Andersen T (1997) Pelagic nutrient cycles: herbivores as sources and sinks for nutrients. Springer, BerlinGoogle Scholar
  3. Anderson TR, Hessen DO (2005) Threshold elemental ratios for carbon versus phosphorus limitation in Daphnia. Freshw Biol 50:2063–2075CrossRefGoogle Scholar
  4. Anderson TR, Hessen DO, Elser JJ, Urabe J (2005) Metabolic stoichiometry and the fate of excess carbon and nutrients in consumers. Am Nat 165:1–15CrossRefGoogle Scholar
  5. Bartell SM, Kitchell JF (1978) Seasonal impact of planktivory on phosphorus release by Lake Wingra zooplankton. Verh Int Ver Limnol 20:466–474Google Scholar
  6. Beers JR (1966) Studies on the chemical composition of the major zooplankton groups in the Sargasso Sea off Bermuda. Limnol Oceanogr 11:520–528CrossRefGoogle Scholar
  7. Boersma MN, Aberle F, Hantzsche M, Schoo KL, Wiltshire KH, Malzahn AM (2008) Nutritional limitation travels up the food chain. Int Rev Hydrobiol 93:479–488CrossRefGoogle Scholar
  8. Childress JJ, Nygaard MH (1973) The chemical composition of midwater fishes as a function of depth of occurrence off southern California. Deep Sea Res I 20:1093–1109Google Scholar
  9. Childress JJ, Price MH, Favuzzi J, Cowles D (1990) Chemical composition of midwater fishes as a function of depth of occurrence off the Hawaiian Islands: food availability as a selective factor? Mar Biol 105:235–246CrossRefGoogle Scholar
  10. Clarke A (2008) Ecological stoichiometry in six species of Antarctic marine benthos. Mar Ecol Prog Ser 369:25–37Google Scholar
  11. Dantas MC, Attayde JL (2007) Nitrogen and phosphorus content of some temperate and tropical freshwater fishes. J Fish Biol 70:100–108CrossRefGoogle Scholar
  12. Deegan LA (1986) Changes in body composition and morphology of young-of-the-year gulf menhaden, Brevoortia patronus Goode, in Fourleague Bay, Louisiana. J Fish Biol 29:403–415CrossRefGoogle Scholar
  13. Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–751CrossRefGoogle Scholar
  14. Fernández F, Miquel AG, Guinea J, Martinez R (1998) Digestion and digestibility in gilthead sea bream (Sparus aurata): the effect of diet composition and ration size. Aquaculture 166:67–84CrossRefGoogle Scholar
  15. Finkel ZV, Quigg A, Raven JA, Reinfelder JR, Schofield OE, Falkowski PG (2006) Irradiance and the elemental stoichiometry of marine phytoplankton. Limnol Oceanogr 51:2690–2701CrossRefGoogle Scholar
  16. Gasol JM, del Giorgio PA, Duarte CM (1997) Biomass distribution in marine planktonic communities. Limnol Oceanogr 42:1353–1363CrossRefGoogle Scholar
  17. Geesey GG, Alexander GV, Bray RN, Miller AC (1984) Fish fecal pellets are a source of minerals for inshore reef communities. Mar Ecol Prog Ser 15:19–25CrossRefGoogle Scholar
  18. Geider RJ, La Roche J (2002) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol 37:1–17CrossRefGoogle Scholar
  19. Gillooly JF, Allen AP, Brown H, Elser JJ, Martinez del Rio C, Savage VM, West GB, Woodruff WH, Woods HA (2005) The metabolic basis of whole-organism RNA and phosphorus content. Proc Nat Acad Sci 102:11923–11927CrossRefGoogle Scholar
  20. Gismervik I (1997) Stoichiometry of some marine planktonic crustaceans. J Plankton Res 19:279–285CrossRefGoogle Scholar
  21. Hassett RP, Cardinale B, Stabler LB, Elser JJ (1997) Ecological stoichiometry of N and P in pelagic ecosystems: comparison of lakes and oceans with emphasis on the zooplankton-phytoplankton interaction. Limnol Oceanogr 42:648–662CrossRefGoogle Scholar
  22. Hendrixson HA, Sterner RW, Kay AD (2007) Elemental composition of fresh water fishes in relation to phylogeny, allometry and ecology. J Fish Biol 70:121–140CrossRefGoogle Scholar
  23. Hirst AG, Kiørboe T (2002) Mortality of marine planktonic copepods: Global rates and patterns. Mar Ecol Prog Ser 230:195–209CrossRefGoogle Scholar
  24. Hjerne O, Hansson S (2002) The role of fish and fisheries in Baltic Sea nutrient dynamics. Limnol Oceanogr 47:1023–1032CrossRefGoogle Scholar
  25. Hua K, Bureau DP (2006) Modelling digestible phosphorus content of salmonid fish feeds. Aquaculture 254:455–465CrossRefGoogle Scholar
  26. Igushi N, Ikeda T (2004) Metabolism and elemental composition of aggregate and solitary forms of Salpa thompsoni (Tunicata: Thaliacea) in waters off the Antartic Peninsula during austral summer 1999. J Plankton Res 26:1025–1037Google Scholar
  27. Ikeda T, Mitchell AW (1982) Oxygen uptake, ammonia excretion and phosphate excretion by krill and other antarctic zooplankton in relation to their body size and chemical composition. Mar Biol 71:283–298CrossRefGoogle Scholar
  28. Karl DM, Björkman KM, Dore JE, Fujieki L, Hebel DV, Houlihan T, Letelier RM, Tupas LM (2001) Ecological nitrogen-to-phosphorus stoichiometry at station ALOHA. Deep Sea Res II 48:1529–1566CrossRefGoogle Scholar
  29. Klausmeier CA, Litchman E, Levin SA (2004) Phytoplankton growth and stoichiometry under multiple nutrient limitation. Limnol Oceanogr 49:1463–1470CrossRefGoogle Scholar
  30. Kraft CE (1992) Estimates of phosphorus and nitrogen cycling by fish using a bioenergetics approach. Can J Fish Aquat Sci 49:2596–2604CrossRefGoogle Scholar
  31. Lam V, Pauly D (2005) Mapping the global biomass of mesopelagic fishes. Sea Around US Project Newsletter, July/August, 30:4Google Scholar
  32. Landry MR, Calbet A (2004) Microzooplankton production in the oceans. ICES J Mar Sci 61:501–507CrossRefGoogle Scholar
  33. Larsson U, Hajdu S, Walve J, Elmgren R (2001) Baltic Sea nitrogen fixation estimated from the summer increase in upper mixed layer total nitrogen. Limnol Oceanogr 46:811–820CrossRefGoogle Scholar
  34. Le Borgne R (1982) Zooplankton production in the eastern tropical Atlantic Ocean: net growth efficiency and P:B in terms of carbon, nitrogen and phosphorus. Limnol Oceanogr 27:681–698CrossRefGoogle Scholar
  35. Mahe K, Amara R, Bryckaert T, Kacher M, Brylinski JM (2007) Ontogenetic and spatial variation in the diet of hake (Merluccius merluccius) in the Bay of Biscay and the Celtic Sea. ICES J Mar Sci 64:1210–1219Google Scholar
  36. Mayor DJ, Anderson TR, Pond DW, Irigoien X (2009) Egg production and associated losses of carbon, nitrogen and fatty acids from maternal biomass in Calnus finmarchicus before the spring bloom. J Mar Syst 78:505–510CrossRefGoogle Scholar
  37. Moutin T, Van Den Broeck N, Beker B, Dupouy C, Rimmelin P, Le Bouteiller A (2005) Phosphate availability controls Trichodesmium spp. biomass in the SW Pacific Ocean. Mar Ecol Prog Ser 297:15–21CrossRefGoogle Scholar
  38. Nugraha A, Pondaven P, Tréguer P (2010) Influence of consumer-driven nutrient recycling on primary production and the distribution of N and P in the ocean. Biogeosciences 7(4):1285–1305CrossRefGoogle Scholar
  39. Pertola S, Koski M, Viitasalo M (2001) Stoichiometry of mesozooplankton in N- and P-limited areas of the Baltic Sea. Mar Biol 140:425–434Google Scholar
  40. Pilati A, Vanni MJ (2007) Ontogeny, diet shifts, and nutrient stoichiometry in fish. Oikos 116:1663–1674CrossRefGoogle Scholar
  41. Pinnegar JK, Polunin NVC (2006) Planktivorous damselfish support significant nitrogen and phosphorus fluxes to Mediterranean reefs. Mar Biol 148:1089–1099CrossRefGoogle Scholar
  42. Pinnegar JK, Polunin NVC, Videler JJ, de Wiljes JJ (2007) Daily carbon, nitrogen and phosphorus budgets for the Mediterranean planktivorous damselfish Chromis chromis. J Exp Mar Biol Ecol 352:378–391CrossRefGoogle Scholar
  43. Platt T, Irwin B (1973) Caloric content of phytoplankton. Limnol Oceanogr 18:306–310CrossRefGoogle Scholar
  44. Quigg A, Finkel ZV, Irwin AJ, Rosenthal Y, Ho TY, Reinfelder JR, Schofield O, Morel FMM, Falkowski PG (2003) The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425:291–294CrossRefGoogle Scholar
  45. Radchenko VI (2007) Mesopelagic fish community supplies “biological pump”. Raffles Bull Zool 14:265–271Google Scholar
  46. Robinson BH, Bailey TG (1981) Sinking rates and dissolution of midwater fish fecal matter. Mar Biol 65:135–142CrossRefGoogle Scholar
  47. Roger C (1978) Azote et phosphore chez un crustacé macroplanctonique, Meganyctiphanes norvegica (M. Sars) (Euphausiacea): excrtion minrale et constitution. J Exp Mar Biol Ecol 33:57–83CrossRefGoogle Scholar
  48. Spitz J, Mourocq E, Schoen V, Ridoux V (2010) Proximate composition and energy content of forage species from the Bay of Biscay: high- or low-quality food? ICES J Mar Sci 67:909–915CrossRefGoogle Scholar
  49. Sterner RW (1990) The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the algal competitive arena. Am Nat 136:209–229CrossRefGoogle Scholar
  50. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  51. Sterner RW, George NB (2000) Carbon, nitrogen, and phosphorus stoichiometry of cyprinid fishes. Ecology 81:127–140CrossRefGoogle Scholar
  52. Strickland JDH, Parsons TR (1972) A practical handbook of sea-water analysis, 2nd edn. J Fish Res Bd Canada, vol 167, p 311Google Scholar
  53. Threlkeld ST (1988) Planktivory and planktivore biomass effects on zooplankton, phytoplankton, and the trophic cascade. Limnol Oceanogr 33:1362–1375CrossRefGoogle Scholar
  54. Touratier F, Field JG, Moloney CL (2001) A stoichiometric model relating growth substrate quality (C:N:P ratios) to N:P ratios in the products of heterotrophic release and excretion. Ecol Model 139:265–291CrossRefGoogle Scholar
  55. Tyrrell T (1999) The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400:525–531CrossRefGoogle Scholar
  56. Uye S, Matsuda O (1988) Phosphorus content of zooplancton from the Inland Sea of Japan. J Oceanogr 44:280–286Google Scholar
  57. Van de Waal DB, Verschoor AM, Verspagen JMH, van Donk E, Huisman J (2010) Climate-driven changes in the ecological stoichiometry of aquatic ecosystems. Front Ecol 8:145–152CrossRefGoogle Scholar
  58. Vanni MJ, Layne CD, Arnott SE (1997) “Top-down” trophic interactions in lakes: effects of fish on nutrient dynamics. Ecology 78:1–20Google Scholar
  59. Vanni MJ, Flecker AS, Hood JM, Headworth JL (2002) Stoichiometry of nutrient cycling by vertebrates in a tropical stream: linking species identity and ecosystem processes. Ecol Lett 5:285–293CrossRefGoogle Scholar
  60. Vanni MJ, Bowling AM, Dickman EM, Hale RS, Higgins KA, Horgan MJ, Knoll LB, Renwick WH, Stein RA (2006) Nutrient cycling by fish supports relatively more primary production as lake productivity increases. Ecology 87:1696–1709CrossRefGoogle Scholar
  61. Walve J, Larsson U (1999) Carbon, nitrogen and phosphorus stoichiometry of crustacean zooplankton in the Baltic Sea: implications for nutrient recycling. J Plankt Res 21:2309–2321CrossRefGoogle Scholar
  62. Wu J, Sunda W, Boyle EA, Karl DM (2000) Phosphate depletion in the western North Atlantic Ocean. Science 289:759–762CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Marie Czamanski
    • 1
    Email author
  • Adi Nugraha
    • 1
  • Philippe Pondaven
    • 1
  • Marine Lasbleiz
    • 1
  • Annick Masson
    • 1
  • Nicolas Caroff
    • 2
  • Robert Bellail
    • 3
  • Paul Tréguer
    • 1
  1. 1.Laboratoire des Sciences de l’Environnement Marin, Institut Universitaire Européen de la Mer, IUEMUniversité Européenne de Bretagne, Université de Brest, LEMAR, UMR 6539, CNRS, IRDPlouzanéFrance
  2. 2.STH/Laboratoire de Biologie HalieutiqueIFREMERPlouzanéFrance
  3. 3.STH/Laboratoire de Biologie HalieutiqueIFREMERLorientFrance

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