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

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.

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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 10:413–419

    Article  Google Scholar 

  2. Andersen T (1997) Pelagic nutrient cycles: herbivores as sources and sinks for nutrients. Springer, Berlin

    Google Scholar 

  3. Anderson TR, Hessen DO (2005) Threshold elemental ratios for carbon versus phosphorus limitation in Daphnia. Freshw Biol 50:2063–2075

    Article  Google 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 165:1–15

    Article  Google Scholar 

  5. Bartell SM, Kitchell JF (1978) Seasonal impact of planktivory on phosphorus release by Lake Wingra zooplankton. Verh Int Ver Limnol 20:466–474

    Google Scholar 

  6. Beers JR (1966) Studies on the chemical composition of the major zooplankton groups in the Sargasso Sea off Bermuda. Limnol Oceanogr 11:520–528

    Article  CAS  Google 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 93:479–488

    Article  Google 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 20:1093–1109

    CAS  Google 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 105:235–246

    Article  Google Scholar 

  10. Clarke A (2008) Ecological stoichiometry in six species of Antarctic marine benthos. Mar Ecol Prog Ser 369:25–37

    Google Scholar 

  11. Dantas MC, Attayde JL (2007) Nitrogen and phosphorus content of some temperate and tropical freshwater fishes. J Fish Biol 70:100–108

    Article  CAS  Google 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 29:403–415

    Article  Google Scholar 

  13. Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–751

    Article  Google 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 166:67–84

    Article  Google 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 51:2690–2701

    Article  CAS  Google Scholar 

  16. Gasol JM, del Giorgio PA, Duarte CM (1997) Biomass distribution in marine planktonic communities. Limnol Oceanogr 42:1353–1363

    Article  CAS  Google 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 15:19–25

    Article  Google 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 37:1–17

    Article  Google 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 102:11923–11927

    Article  CAS  Google Scholar 

  20. Gismervik I (1997) Stoichiometry of some marine planktonic crustaceans. J Plankton Res 19:279–285

    Article  Google 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 42:648–662

    Article  CAS  Google 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 70:121–140

    Article  Google Scholar 

  23. Hirst AG, Kiørboe T (2002) Mortality of marine planktonic copepods: Global rates and patterns. Mar Ecol Prog Ser 230:195–209

    Article  Google Scholar 

  24. Hjerne O, Hansson S (2002) The role of fish and fisheries in Baltic Sea nutrient dynamics. Limnol Oceanogr 47:1023–1032

    Article  Google Scholar 

  25. Hua K, Bureau DP (2006) Modelling digestible phosphorus content of salmonid fish feeds. Aquaculture 254:455–465

    Article  CAS  Google 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 26:1025–1037

    Google 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 71:283–298

    Article  Google 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 48:1529–1566

    Article  CAS  Google Scholar 

  29. Klausmeier CA, Litchman E, Levin SA (2004) Phytoplankton growth and stoichiometry under multiple nutrient limitation. Limnol Oceanogr 49:1463–1470

    Article  Google Scholar 

  30. Kraft CE (1992) Estimates of phosphorus and nitrogen cycling by fish using a bioenergetics approach. Can J Fish Aquat Sci 49:2596–2604

    Article  CAS  Google Scholar 

  31. Lam V, Pauly D (2005) Mapping the global biomass of mesopelagic fishes. Sea Around US Project Newsletter, July/August, 30:4

  32. Landry MR, Calbet A (2004) Microzooplankton production in the oceans. ICES J Mar Sci 61:501–507

    Article  Google 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 46:811–820

    Article  CAS  Google 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 27:681–698

    Article  Google 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 64:1210–1219

    Google 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 78:505–510

    Article  Google 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 297:15–21

    Article  CAS  Google 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):1285–1305

    Article  CAS  Google Scholar 

  39. Pertola S, Koski M, Viitasalo M (2001) Stoichiometry of mesozooplankton in N- and P-limited areas of the Baltic Sea. Mar Biol 140:425–434

    Google Scholar 

  40. Pilati A, Vanni MJ (2007) Ontogeny, diet shifts, and nutrient stoichiometry in fish. Oikos 116:1663–1674

    Article  Google Scholar 

  41. Pinnegar JK, Polunin NVC (2006) Planktivorous damselfish support significant nitrogen and phosphorus fluxes to Mediterranean reefs. Mar Biol 148:1089–1099

    Article  Google 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 352:378–391

    Article  CAS  Google Scholar 

  43. Platt T, Irwin B (1973) Caloric content of phytoplankton. Limnol Oceanogr 18:306–310

    Article  Google 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 425:291–294

    Article  CAS  Google Scholar 

  45. Radchenko VI (2007) Mesopelagic fish community supplies “biological pump”. Raffles Bull Zool 14:265–271

    Google Scholar 

  46. Robinson BH, Bailey TG (1981) Sinking rates and dissolution of midwater fish fecal matter. Mar Biol 65:135–142

    Article  Google 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 33:57–83

    Article  CAS  Google 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 67:909–915

    Article  Google Scholar 

  49. Sterner RW (1990) The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the algal competitive arena. Am Nat 136:209–229

    Article  Google Scholar 

  50. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  51. Sterner RW, George NB (2000) Carbon, nitrogen, and phosphorus stoichiometry of cyprinid fishes. Ecology 81:127–140

    Article  Google Scholar 

  52. Strickland JDH, Parsons TR (1972) A practical handbook of sea-water analysis, 2nd edn. J Fish Res Bd Canada, vol 167, p 311

  53. Threlkeld ST (1988) Planktivory and planktivore biomass effects on zooplankton, phytoplankton, and the trophic cascade. Limnol Oceanogr 33:1362–1375

    Article  Google 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 139:265–291

    Article  CAS  Google Scholar 

  55. Tyrrell T (1999) The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400:525–531

    Article  CAS  Google Scholar 

  56. Uye S, Matsuda O (1988) Phosphorus content of zooplancton from the Inland Sea of Japan. J Oceanogr 44:280–286

    Google 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 8:145–152

    Article  Google Scholar 

  58. Vanni MJ, Layne CD, Arnott SE (1997) “Top-down” trophic interactions in lakes: effects of fish on nutrient dynamics. Ecology 78:1–20

    Google 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 5:285–293

    Article  Google 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 87:1696–1709

    Article  Google 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 21:2309–2321

    Article  Google Scholar 

  62. Wu J, Sunda W, Boyle EA, Karl DM (2000) Phosphate depletion in the western North Atlantic Ocean. Science 289:759–762

    Article  CAS  Google Scholar 

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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.

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Correspondence to Marie Czamanski.

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Communicated by X. Irigoien.

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Czamanski, M., Nugraha, A., Pondaven, P. et al. Carbon, nitrogen and phosphorus elemental stoichiometry in aquacultured and wild-caught fish and consequences for pelagic nutrient dynamics. Mar Biol 158, 2847–2862 (2011). https://doi.org/10.1007/s00227-011-1783-7

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Keywords

  • Fecal Pellet
  • Wild Fish
  • Assimilation Efficiency
  • Homeostatic Regulation
  • Accumulation Efficiency