Isótopos estables como trazadores nutricionales naturales en larvas y juveniles de Litopenaeus vannamei y Solea senegalensis


  • Julián Gamboa-Delgado Bangor University

Palabras clave:

Trazadores nutricionales, isótopos estables, carbono, nitrógeno dietario, Litopenaeus vannamei, Solea senegalensis


Los isótopos estables han sido ampliamente utilizados como marcadores nutricionales no-peligrosos para
estimar flujos de nutrientes y energía en ecosistemas acuáticos. Los sistemas acuícolas son altamente
viables para realizar evaluaciones isotópicas debido a que en su mayoría representan cadenas alimenticias
cortas y controladas. El presente trabajo muestra una breve revisión de estudios que se han enfocado en
utilizar las diferencias naturales en la composición isotópica de diversos ingredientes, dietas y organismos
consumidores para determinar contribuciones nutricionales al crecimiento. Adicionalmente se presenta
una serie de aplicaciones actuales en las cuales camarón blanco del Pacifico (L. vannamei) y lenguado de
Senegal (S. senegalensis) fueron utilizados como organismos modelo. La contribución nutricional de
harina de pescado y proteína de soya al crecimiento del camarón blanco fue evaluada al formular dietas
con proporciones variables de nitrógeno suministrado por ambos ingredientes. Las contribuciones de
nitrógeno al crecimiento fueron mayores a partir de la harina de pescado. En dos experimentos
adicionales, se cuantificó la incorporación de carbono dietario proveniente de alimento vivo (Artemia) e
inerte consumido por larvas y postlarvas de camarón y lenguado cultivados bajo diferentes regímenes de
co-alimentación. Los aportes nutricionales provenientes del alimento vivo fueron mayores que los
suministrados por el alimento inerte. La estimación de cambios isotópicos en tejido a diferentes tiempos
permitió distinguir la dilución isotópica debida solo a crecimiento y la causada por las tasas metabólicas
de recambio de nutrientes en tejido.


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Akiyama D.M. (1989) Soybean meal utilization by marine shrimp. In: Proceedings of the world congress on vegetable protein utilization in human food and animal feedstuffs (ed. by T.H. Applewhite). Singapore, Oct. 1988 pp. 252–265. American Oil Chemists Society, Champaign, IL.

Alam M.S., Teshima S., Koshio S., Ishikawa M., Hernandez L.H.H., Uyan O. Michael, F.R. (2005) Supplemental effects of coated methionine and/or lysine to soy protein diet for juvenile kuruma shrimp, Marsupenaeus japonicus. Aquaculture 248, 13–19.

Al-Maslamani I.A.M.J. (2006) Feeding and nutrition in the marine shrimp Penaeus semisulcatus. PhD Thesis. 179 pp.University of Wales, UK.

Barclay W., Zeller S. (1996) Nutritional enhancement of n−3 and n−6 fatty acids in rotifers and Artemia nauplii by feeding spray-dried Schizochytrium sp. Journal of the World Aquaculture Society 27, 314–322.

Barnabe G., Guissi A. (1994) Adaptations of the feeding behaviour of larvae of the sea bass (Dicentrarchus labrax L.), to an alternating live-food/compound-food feeding regime. Aquaculture and Fisheries Management 25, 537–546.

Bell M.V., Dick J.R., Anderson T.R., Pond D.W. (2007) Application of liposome and stable isotope tracer techniques to study polyunsaturated fatty acid biosynthesis in marine zooplankton. Journal of Plankton Research 29, 417-422.

Bombeo-Tuburan I., Guanzon N.G., Schroeder, G.L. (1993) Production of Penaeus monodon (Fabricius) using four natural food types in an extensive system. Aquaculture 112, 57–65.

Bosley K.L., Witting D.A. Chambers R.C., Wainright S.C. (2002) Estimating turnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes. Marine Ecology Progress Series 236, 233–240.

Burford M.A., Sellars M.J., Arnold S.J. Keys S.J, Crocos P.J., Preston N.P. (2004) Contribution of the natural biota associated with substrates to the nutritional requirements of post-larval shrimp (Penaeus esculentus) in high-density rearing systems. Aquaculture Research 35, 508-515.

Burford M.A., Preston N.P., Glibert P.M., Dennison W.C. (2002) Tracing the fate of 15N-enriched feed in an intensive shrimp system. Aquaculture 206, 199–216.

Cabana G., Rasmussen, J.B. (1996) Comparison of aquatic food chains using nitrogen isotopes. Proceeding of the National Academy of Sciences 93, 10844 –10847.

Calderon F.R.O., Imai D.M., Arce S.M., Argue B.J., Moss, S.M. (2004) Performance of larval and postlarval Pacific white shrimp, Litopenaeus vannamei (Boone) fed two commercial liquid diet supplements. Journal of Applied Aquaculture 15, 21–36.

Carter C.G., Owen S.F., He Z.Y., Watt P.W., Scrimgeour C., Houlihan D.F., Rennie M.J. (1994) Determination of protein synthesis in rainbow trout, Onchorhynchus mykiss, using a stable isotope. Journal of Experimental Biology 189, 279–28

Cherel Y., Hobson K.A., Hassani S. (2005) Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiological and Biochemical Zoology 78, 106–115.

Cañavate J.P., Fernández-Díaz C. (1999) Influence of co-feeding larvae with live and inert diets on weaning the sole Solea senegalensis onto commercial dry feeds. Aquaculture 174, 255–263.

Chikaraishi Y., Kashiyama Y., Ogawa N.O., Kitazato H., Ohkouchi N. (2007) Metabolic control of nitrogen isotope composition of amino acids in macroalgae and gastropods: implications for aquatic food web studies. Marine Ecology Progress Series 342, 85-90.

Conceição L.E.C., Skjermo J., Skjåk-Bræk G., Verreth J.A.J. (2001) Effect of an immunostimulating alginate on protein turnover of turbot (Scophthalmus maximus L.) larvae. Fish Physiology and Biochemistry 24, 207-212.

Coutteau P., Geurden I., Camara M.R., Bergot P., Sorgeloos P. (1997) Review on the dietary effects of phospholipids in fish and crustacean larviculture. Aquaculture 155, 149–164.

Crawley K.R., Hyndes G.A., Vanderklift M.A. (2007) Variation among diets in discrimination of δ13C and δ15N in the amphipod Allorchestes compressa. Journal of Experimental Marine Biology and Ecology 349, 370-377.

D'Avanzo C., Alber M., Valiela I. (1991) Nitrogen assimilation from amorphous detritus by two coastal consumers. Estuarine Coastal and Shelf Science 33, 203–209.

DeNiro M.J., Epstein S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.

DeNiro M.J., Epstein S. (1978) Influence of diet on the distribution of carbon isotope ratios in animals. Geochimica et Cosmochimica Acta 42, 495–506.

Epp M.A, Ziemann D.A., Schell D.M. (2002) Carbon and nitrogen dynamics in zero-water exchange shrimp culture as indicated by stable isotope tracers. Aquaculture Research 33, 839-846.

Evans C.J., Evershed R.P., Black H.I.J, Ineson P. (2003) Compound-specific stable isotope analysis of soil mesofauna using thermally assisted hydrolysis and methylation for ecological investigations. Analytical Chemistry 75, 6056–6062.

Fantle M.S., Dittel A.I., Schwalm S., Epifanio C.E., Fogel M.L. (1999) A foodweb analysis of the juvenile crab Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120, 416-426

Forster I.P., Dominy W., Tacon A.G.J. (2002) Use of soy protein concentrates in shrimp feeds. International Aqua Feed 5, 17–19.

Fraser K.P.P., Rogers A.D. (2007) Protein metabolism in marine animals: the underlying mechanism of growth. Advances in Marine Biology 52, 267–362.

Fry, B. (2006) Stable Isotope Ecology. Springer Science. NY, USA. 390 pp.

Fry B., Arnold C. (1982) Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54, 200–204.

Gamboa-Delgado J. (2009) Application of natural stable isotopes in aquaculture nutrition. PhD Thesis. University of Wales-Bangor, UK. 180 pp.

Gamboa-Delgado J., Le Vay L. (2009a) 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 291, 115-123.

Gamboa-Delgado J., Le Vay L. (2009b) 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 297, 128-135.

Gamboa-Delgado J., Cañavate J.P., Zerolo R., Le Vay L. (2008) 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 280, 190-197.

Gannes L.Z., O’Brien D.M., Martinez del Rio C. (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78, 1271–1276.

Garlick P.J., McNurlan M.A., Preedy V.R. (1980) A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of 3H-phenylalanine. Biochemical Journal 192, 719–723.

Gentsch E., Kreibich T., Hagen W., Niehoff B. (2009) Dietary shifts in the copepod Temora longicornis during spring: evidence from stable isotope signatures, fatty acid biomarkers and feeding experiments. Journal of Plankton Research 31, 45-60.

Gouveia A., Davies S.J. (2000) Inclusion of an extruded dehulled pea seed meal in diets for juvenile European sea bass (Dicentrarchus labrax). Aquaculture 182, 183–193.

Guillaume J., Kaushik S., Bergot P., Metailler R. (Eds) (2001) Nutrition and Feeding of Fish and Crustaceans. Springer Verlag, Heidelberg, Germany. 408 pp.

Han K., Geurden I., Sorgeloos P. (2001) Fatty acid changes in enriched and subsequently starved Artemia franciscana nauplii enriched with different essential fatty acids. Aquaculture 199, 93–105.

Hentschel B.T. (1998) Intraspecific variations in δ13C indicate ontogenetic diet changes in deposit-feeding polychaetes. Ecology 79, 1357–1370.

Hesslein R.H., Hallard K.A., Ramlal P. (1993) 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. Canadian Journal of Fisheries and Aquatic Sciences 50, 2071–2076

Herzka S.Z., Holt G.J. (2000) Changes in isotopic composition of red drum (Sciaenops ocellatus) larvae in response to dietary shifts: potential applications to settlement studies. Canadian Journal of Fisheries and Aquatic Sciences 57, 137-147.

Hinga K.R., Arthur M.A., Pilson M.E.Q. Whitaker D. (1994) Carbon isotope fractionation by marine phytoplankton in culture: The effects of CO2 concentration, pH, temperature, and species. Global Biogeochemical Cycles, 8, 91-102.

Hobson K.A., Smith R.J.F, Sorensen P.W. (2006) Applications of stable isotope analysis to tracing nutrient sources of Hawaiian gobioid fishes and other stream organisms. In: Evenhuis, N.L. &

Fitzsimons, J.M. (eds.), Biology of Hawaiian Streams and Estuaries. Bishop Museum Bulletin in Cultural and Environmental Studies, Honolulu, Hawaii.

Hobson K.A., Clark R.G. (1992) Assessing avian diets using stable isotopes 1: turnover of 13C in tissues. Condor 94, 181–188.

Houlihan D.F., Carter C.G., McCarthy I.D. (1995) Protein turnover in animals. Chapter 1. In: Nitrogen metabolism and excretion. (ed. by Walsh, P.J. and Wright, P.). CRC Press. Boca Raton, FL, USA. pp. 1-31.

Houlihan D.F., Hall S.J., Gray C., Noble B.S. (1988) Growth rates and protein turnover in Atlantic cod, Gadus morhua. Canadian Journal of Fisheries and Aquatic Sciences 45, 951-964.

Jardine T.D. MacLatchy D.L., Fairchild W.L., Cunjak, R.A., Brown, S.B. (2004) Rapid carbon turnover during growth of Atlantic salmon (Salmo salar) smolts in seawater, and evidence of food consumption by growth-stunts. Hydrobiologia 527, 63–75.

Jomori R.K., Ducatti C., Carneiro D.J., Portella M.C. (2008) Stable carbon (δ13C) and nitrogen (δ15N) isotopes as natural indicators of live and dry food in Piaractus mesopotamicus (Holmberg, 1887) larval tissue. Aquaculture Research 39, 370–381.

Le Vay L., Gamboa-Delgado J. (2010) Naturally-occurring stable isotopes as direct measures of larval feeding efficiency, nutrient incorporation and turnover. Aquaculture. In press. doi:10.1016/j.aquaculture.2010.03.033

Lindholm M., Hessen D.O. (2007) Zooplankton succession on seasonal floodplains: surfing on a wave of food. Hydrobiologia 592, 95-104.

Liu H., Kelly M.S., Cook E.J., Black K.D., Orr H., Zhu J.X., Dong S.L. (2007) The effect of diet type on growth and fatty acid composition of sea urchin larvae, I. Paracentrotus lividus (Lamarck, 1816) (Echinodermata). Aquaculture 265, 247–262.

MacAvoy S.E., Arneson L.S., Bassett E. (2006) Correlation of metabolism with tissue carbon and nitrogen turnover rate in small mammals. Oecologia 150, 190 – 201.

MacAvoy S.E., Macko S.A., Arneson L.S. (2005) Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Canadian Journal of Zoology 83, 631–641.

McClelland J.W., Montoya J.P. (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83, 2173-2180.

McCullagh J., Gaye-Siessegger J., Focken U. (2008) 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. Rapid Communications in Mass Spectrometry 22, 1817-1822.

Martínez del Rio C., Wolf N., Carleton S.A., Gannes, L.Z. (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biology Reviews 84, 91-111.

Martínez del Rio C., Wolf B.O. (2005) Mass-balance models for animal isotopic ecology. In: Physiological and ecological adaptations to feeding in vertebrates. (ed. by Starck, J.M., Wang. T.). Science Publishers, Enfield, NH, pp. 141-174.

Matsuda H., Takenouchi T., Tanaka S., Watanabe S. (2009) Relative contribution of Artemia and mussel as food for cultured middle-stage Panulirus japonicus phyllosomata as determined by stable nitrogen isotope analysis. New Zealand Journal of Marine and Freshwater Research 43, 217–224.

Michener R.H., Schell D.M. (1994) Stable isotope ratios as tracers in marine aquatic food webs In: Stable isotopes in ecology and environmental science. Chapter 7. Vol 1 (ed. by Lajtha, K. and Michener, R.H.) Blackwell scientific publications. Oxford, UK. 138-157 pp.

Minagawa M., Wada E. (1984) Stepwise enrichment of δ15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.

Moens T., Bouillon S., Gallucci F. (2005) Dual stable isotope abundances unravel trophic position of estuarine nematodes. Journal of the Marine Biological Association of the United Kingdom 85, 1401–1407.

Nghia T.T., Wille M., Vandendriessche S., Vinh Q.T., Sorgeloos P. (2007) Influence of highly unsaturated fatty acids in the live food on larviculture of mud crab Scylla paramamosain. Aquaculture Research 38, 1512–1528.

O'Brien D.M., Boggs C.L., Fogel M.L. (2005) The amino acids used in reproduction by butterflies: A comparative study of dietary sources using compound-specific stable isotope analysis. Physiological and Biochemical Zoology 78, 819-827.

O’Brien D.M., Boggs C.L., Fogel M.L. (2003) Pollen feeding in the butterfly Heliconius charitonia isotopic evidence for essential amino acid transfer from pollen to eggs. Proceedings of the Royal Society of London Series B - Biological Sciences 270, 2631–2636.

Pearson D.F., Levey D.J., Greenberg C.H., Martinez del Rio C. (2003) Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135, 516–523.

Peterson B.J., Fry B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293-320.

Phillips D.L., Gregg J.W. (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261-269

Phillips D.L., Gregg J.W. (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127, 171–179. (see also erratum, Oecologia 128, 204).

Power M., Guiguer K.R.R.A., Barton D.R. (2003) Effects of temperature on isotopic enrichment in Daphnia magna: implications for aquatic food-web studies. Rapid Communications in Mass Spectrometry 17, 1619-1625.

Preston N.P., Smith D.M., Kellaway D.M., Bunn S.E. (1996) The use of enriched 15N as an indicator of the assimilation of individual protein sources from compound diets for juvenile Penaeus monodon. Aquaculture 147, 249–259.

Robbins C.T., Felicetti L.A., Sponheimer M. (2005) The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144, 534–540.

Rossi F., Herman P.M.J., Middelburg J.J. (2004) Interspecific and intraspecific variation of δ13C and δ15N in deposit- and suspension-feeding bivalves (Macoma balthica and Cerastoderma edule): evidence of ontogenetic changes in feeding mode of Macoma balthica. Limnology and Oceanography 49, 408–414.

Roth J.D., Hobson K.A. (2000) Stable carbon and nitrogen isotopic fractionation between diet and tissue ofcaptive red fox: implications for dietary reconstruction. Canadian Journal of Zoology 78, 848-852.

Sato M., Sasaki H., Fukuchi M. (2002) Stable isotopic compositions of over-wintering copepods in the arctic and subarctic waters and implications for the feeding history. Journal of Marine Systems 38, 165–174.

Schlechtriem C., Focken U., Becker K. (2004) Stable isotopes as a tool for nutrient assimilation studies in larval fish feeding on live food. Aquatic Ecology 38, 93-100.

Schroeder G.L. (1983) Sources of fish and prawn growth in polyculture ponds as indicated by δ13C analysis. Aquaculture 35, 29–42.

Shewbart K.L., Meis W.L., Ludwig P.D. (1972) Identification and quantitative analysis of the amino acids present in protein of the brown shrimp, Penaeus aztecus. Marine Biology 16, 64–67.

Southgate P.C., Partridge G.J. (1998) Development of artificial diets for marine finfish larvae: problems and prospects. In: De Silva, S.S. (Ed), Tropical Mariculture. Academic Press, London, U.K., pp. 151–170.

Spero H.J., Andreasen D.J., Sorgeloos E. (1993) Carbon and nitrogen isotopic composition of different strains of Artemia sp. International Journal of Salt Lake Research 2, 133-139.

Stenroth P., Holmqvist N., Nyström P., Berglund O., Larsson P., Granéli W. (2006) Stable isotopes as an indicator of diet in omnivorous crayfish (Pacifastacus leniusculus): the influence of tissue, sample treatment and season. Canadian Journal of Fisheries and Aquatic Sciences 63, 821-831.

Tieszen L.L., Boutton T.W., Tesdahl K.G., Slade N.A. (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57, 32-37.

Van der Zanden M.J., Hulshof M., Ridgway M.S., Rasmussen J.B. (1998) Application of stable isotope techniques to trophic studies of age-0 smallmouth bass. Transactions of the American Fisheries Society 127, 729-739

Verschoor A.M., Boonstra H., Meijer T. (2005) Application of stable isotope tracers to studies of zooplankton feeding, using the rotifer Brachionus calyciflorus as an example. Hydrobiologia, 546, 535–549.

Villamar D.E., Langdon C.J. (1993) Delivery of dietary components to larval shrimp (Penaeus vannamei) by means of complex microcapsules. Marine Biology 115, 635–642.

Yokoyama H., Abo K., Ishihi Y. (2006) Quantifying aquaculture-derived organic matter in the sediment in and around a coastal fish farm using stable carbon and nitrogen isotope ratios. Aquaculture 254, 411-425.

Yokoyama H., Tamaki A., Harada K., Shimoda K., Koyama K., Ishihi Y. (2005) Variability of diet tissue isotopic fractionation in estuarine macrobenthos. Marine Ecology Progress Series 296, 115–128.

Yoshioka T. Wada E., Hayashi H. (1994) A stable isotope study on seasonal food web dynamics in a eutrophic lake. Ecology 75, 835-846.


Cómo citar

Gamboa-Delgado, J. (2010). Isótopos estables como trazadores nutricionales naturales en larvas y juveniles de Litopenaeus vannamei y Solea senegalensis. Avances En Nutrición Acuicola. Recuperado a partir de

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