Isotopic turnover rate and trophic fractionation of nitrogen in shrimp Litopenaeus vannamei (Boone) by experimental mesocosms: implications for the estimation of the relative contribution of diets
2015; Wiley; Volume: 47; Issue: 10 Linguagem: Inglês
10.1111/are.12757
ISSN1365-2109
AutoresElsa I. Bojorquez-Mascareño, Martín Federico Soto-Jiménez,
Tópico(s)Marine Bivalve and Aquaculture Studies
ResumoAquaculture ResearchVolume 47, Issue 10 p. 3070-3087 Original Article Isotopic turnover rate and trophic fractionation of nitrogen in shrimp Litopenaeus vannamei (Boone) by experimental mesocosms: implications for the estimation of the relative contribution of diets Elsa I Bójorquez-Mascareño, Elsa I Bójorquez-Mascareño Posgrado en Ciencias del Mar y Limnología, Universidad NacionalAutónoma de México, Mazatlán, MéxicoSearch for more papers by this authorMartín F Soto-Jiménez, Corresponding Author Martín F Soto-Jiménez [email protected] Instituto de Ciencias del Mar y Limnología, Universidad NacionalAutónoma de México, Mazatlán, MéxicoCorrespondence: M F Soto-Jiménez, Unidad Académica Mazatlán, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mazatlan, Sinaloa, México. E-mail: [email protected]Search for more papers by this author Elsa I Bójorquez-Mascareño, Elsa I Bójorquez-Mascareño Posgrado en Ciencias del Mar y Limnología, Universidad NacionalAutónoma de México, Mazatlán, MéxicoSearch for more papers by this authorMartín F Soto-Jiménez, Corresponding Author Martín F Soto-Jiménez [email protected] Instituto de Ciencias del Mar y Limnología, Universidad NacionalAutónoma de México, Mazatlán, MéxicoCorrespondence: M F Soto-Jiménez, Unidad Académica Mazatlán, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mazatlan, Sinaloa, México. E-mail: [email protected]Search for more papers by this author First published: 09 April 2015 https://doi.org/10.1111/are.12757Citations: 3Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract The effect of size and diet on the relative contribution of growth and metabolic turnover to changes in isotopic composition of whiteleg shrimp Litopenaeus vannamei was examined by mesocosm experiments. Trough testing different diet types (natural and commercial formulated foods and combinations) and feeding scenarios (satiation, limited-fed and starvation), we determined the growth (k) and metabolic (m) turnover, rate of isotopic turnover (t50) and isotopic fractionation of N (Δ15N) during different growth stages [from postlarvae (PL20's) to large juveniles], under controlled conditions. Results revealed that L. vannamei is a diet sensitive species with growth and metabolic processes controlled by the quantity (feeding rate) and quality (in terms of C:N) of food. Relative to the total isotopic change (k + m), the contribution of growth decreased with size shrimp from PL20's to largest juveniles. Metabolic turnover also decreased, but showed an elevated variability. Coefficient k in limited-fed and starved specimens was lower than those on satiation; m showed the opposite trend. Δ15N values averaged from 0.30‰ to 3.5‰ (1.87 ± 0.87‰) in satiated L. vannamei, but increased to 2.59–3.09 and 3.28–4.81‰ in limited-fed and starved specimens. Δ15N increased with a diet's C:N, indicating an effect of diet quality on isotopic discrimination and also increased with shrimp size, indicating the influence of the metabolic changes. Variations in Δ15N need to be considered in nutrition studies to estimate correctly the temporal relationship between an organism's isotope ratio and its diet and to analyse the variations of food availability or preferences along a culture cycle. References Adams S.A. & Sterner R.W. (2000) The effect of dietary nitrogen content on trophic level 15N enrichment. Limnology and Oceanography 45, 601–607. Al-Maslamani I., Le Vay L. & Kennedy H. (2009) Feeding on intertidal microbial mats by postlarval tiger shrimp, Penaeus semisulcatus De Haan. Marine Biology 156, 2001–2009. Amezcua F. & Soto-Jiménez M.F. (2014) Current state of aquaculture in México. Fisheries, 39, 455–555. Bojórquez-Mascareño E.I. & Soto-Jiménez M.F. (2013) Effects of natural diet on growth on white-leg shrimp Litopenaeus vannamei under experimental mesocosms emulating an intensive culture system. Journal of Aquaculture Research Development 4, 163. Burnham K.P. & Anderson D.R. (2002) Model Selection and Inference: A Practical Information-Theoretic Approach ( 2nd edn). Springer-Verlag, New York, NY, USA. Cabana G. & Rasmussen J.B. (1996) Comparison of aquatic food chains using nitrogen isotopes. Proceeding National Academy Science 93, 10844–10847. Caut S., Angulo E. & Courchamp F. (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443–453. 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 Experimental Marine Biology and Ecology 349, 370–377. De Niro M.J. & Epstein S. (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506. DeNiro M.J. & Epstein S. (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351. Fantle M.S., Dittel A.I., Schwalm S.M., Epifanio C.E. & Fogel M.L. (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. Food and Agriculture Organization of the United Nations (FAO). (2012) The State of World Fisheries and Aquaculture. Fisheries and Aquaculture Department, FAO, Rome. Fry B. & Arnold C. (1982) Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54, 200–204. Gamboa-Delgado J. & Le Vay L. (2009a) Artemia replacement in cofeeding 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. & Le Vay L. (2009b) Natural stable isotopes as indicators of the relative contribution of soy protein and fishmeal to tissue growth in Pacific white shrimp (Litopenaeus vannamei) fed compound diets. Aquaculture 291, 115–123. 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. Gamboa-Delgado J., Peña-Rodríguez A., Ricque-Marie D. & Cruz-Suárez L.E. (2011) Assessment of nutrient allocation and metabolic turnover rate in Pacific white shrimp Litopenaeus vannamei co-fed live macroalgae Ulva clathrata and inert feed: dual stable isotope analysis. Journal of Shellfish Research 30, 969–978. Gamboa-Delgado J., Rojas-Casas M.G., Nieto-López M.G. & Cruz-Suárez L.E. (2012) Simultaneous estimation of the nutrition contribution of fish meal, soy protein isolate and corn gluten to the growth of Pacific white shrimp (Litopenaeus vannamei) using dual stable isotope analysis. Aquaculture 380–383, 33–40. Gannes L.Z., O'Brien D.M. & Martínez del Rio C. (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78, 1271–1276. Gaye-Siessegger J., Focken U., Muetzel S., Abel H. & Becker K. (2004) Feeding level and individual metabolic rate affect δ13C and δ15N values in carp: implications for food web studies. Oecologia 138, 175–183. Hays G.C., Adams C.R., Broderick A.C., Godley B.J., Lucas D.J., Metcalfe J.D. & Prior A.A. (2000) The diving behavior of green turtles at Ascension Island. Animal Behaviors 59, 577–586. Herzka S.Z. (2005) Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuarine, Coastal and Shelf Science 64, 58–69. 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. Hesslein R.H., Hallard K.A. & Ramlal P. (1993) Replacement of sulfur, carbon, and nitrogen in tissue of growing broad white fish (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. Hobson K.A. & Clark R.G. (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94, 181–188. Hobson K.A., Alisauskas R.T. & Clark R.G. (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analysis of diet. Condor 95, 388–394. Houlihan D.F. (1991) Protein turnover in ectotherms and its relationship to energetics. In: Advances in Comparative and Environmental Physiology, Vol. 7 (ed. by R. Gilles), pp. 1–43. Springer-Verlag, Berlin. 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. Kelly J.F. (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78, 1–27. Kusher D.I., Smith S.E. & Cailliet G.M. (1992) Validated age and growth of the leopard shark, Triakis semifasciata, with comments on reproduction. Environmental Biology Fishes 35, 187–203. Le Vay L. & Gamboa-Delgado J. (2011) Naturally-occurring stable isotopes as direct measures of larval feeding efficiency, nutrient incorporation and turnover. Aquaculture 315, 95–103. Lyndon A.R., Houlihan D.F. & Hall S.J. (1992) The effect of short term fasting and a single meal on protein synthesis and oxygen consumption in cod, Gadus morhua. Journal Comparative Physiology B 162, 209–215. Macko S.A., Fogel E.M.L., Engel M.H. & Hare P.E. (1986) Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochimica et Cosmochimica Acta 50, 2143–2146. Madigan D.J., Litvin S.Y., Popp B.N., Carlisle A.B., Farwell C.J. & Block B.A. (2012) Tissue turnover rates and isotopic trophic discrimination factors in the endothermic teleost, Pacific bluefin tuna (Thunnus orientalis). PLoS ONE 7, e49220. Malpica-Cruz L., Herzka S.Z., Sosa-Nishizaki O. & Lazo J.P. (2012) Tissue-specific isotope trophic discrimination factors and turnover rates in a marine elasmobranch: empirical and modeling results. Canadian Journal of Fisheries and Aquatic Sciences 69, 551–564. 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 J.M. Starck & T. Wang), pp. 141–174. Science Publishers, Enfield, NH, USA. Martínez del Rio C., Wolf N., Carleton S.A. & Gannes L.Z. (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84, 91–111. Martínez-Rocha L., Gamboa-Delgado J., Nieto-López M., Ricque-Marie D. & Cruz-Suárez L.E. (2013) Incorporation of dietary nitrogen from fish meal and pea meal (Pisum sativum) in muscle tissue of Pacific white shrimp (Litopenaeus vannamei) fed low protein compound diets. Aquaculture Research 44, 847–859. McCutchan J.H., Lewis W.M., Kendall C. & McGrath C.C. (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102, 378–390. Mente E., Coutteau P., Houlihan D.F., Davidson I. & Sorgeloos P. (2002) Protein turnover, amino acid profile and amino acid flux in juvenile shrimp Litopenaeus vannamei Boone: effects of dietary protein source. Journal of Experimental Biology 205, 3107–3122. Minagawa M. & Wada E. (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140. Olive P.J.W., Pinnegar J.K., Polulin N.V.C., Richards G. & Welch R. (2003) Isotope trophic-step fractionation: a dynamic equilibrium model. Journal of Animal Ecology 72, 608–617. Overman N.C. & Parrish D.L. (2001) Stable isotope composition of walleye: δ15N accumulation with age and area-specific differences in δ13C. Canadian Journal of Fisheries and Aquatic Sciences 58, 1253–1260. Owen S.F., McCarthy I.D., Watt P.W., Ladero V., Sanchez J.A., Houlihan D.F. & Rennie M.J. (1999) In vivo rates of protein synthesis in Atlantic salmon (Salmo salar L.) smolts measured using a single flooding dose injection of 15N-phe. Fish Physiology and Biochemistry 20, 87–94. Páez-Osuna F., Gracia A., Flores-Verdugo F., Lyle-Fritch L.P., Alonso-Rodríguez R., Roque A. & Ruiz-Fernández A.C. (2003) Shrimp aquaculture development and the environment in the Gulf of California ecoregion. Marine Pollution Bulletin 46, 806–815. Pearson S.F., Levey D.J., Greenberg C.H. & Martínez 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. Perga M. & Grey J. (2010) Laboratory measures of isotopic discrimination factors: comments on Caut, Angulo & Couchamp (2008, 2009). Journal of Applied Ecology 47, 942–947. Peterson B.J. & Fry B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecological Systems 18, 293–320. Ponsard S. & Arditi R. (2000) What can stable isotopes (δ15N and δ13C) tell about the food web of soil macro-invertebrates? Ecology 81, 852–864. Post D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718. Post D.M., Pace M.L. & Hairston N.G. (2000) Ecosystem size determines food-chain length in lakes. Nature 405, 1047–1049. Robbins C., Felicetti L. & Sponheimer M. (2005) The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144, 534–540. Rosas C., Cuzon G., Gaxiola G., LePriol Y., Pascual C., Rossignyol J., Contreras F., Sánchez A. & van Wormhoudt A. (2001) Metabolism and growth of juveniles of Litopenaeus vannamei: effect of salinity and dietary carbohydrate levels. Journal of Experimental Marine Biology and Ecology 259, 1–22. Rosas C., Cuzon G., Taboada G., Pascual C., Gaxiola G. & van Wormhoudt A. (2001) Effect of dietary protein and energy levels (P/E) on growth, oxygen consumption, hemolymph and digestive gland carbohydrates, nitrogen excretion and osmotic pressure of Litopenaeus vannamei and L. setiferus juveniles (Crustacea; Decapoda; Penaeidae). Aquaculture Research 32, 1–20. Roth J.D. & Hobson K.A. (2000) Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction. Canadian Journal of Zoology 78, 848–852. 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? Marine Ecology Progress Series 229, 195–205. 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. Vander Zanden M.J. & Rasmussen J.B. (2001) Variation in d 15N and d13C trophic fractionation: implications for aquatic food web studies. Limnology & Oceanography 46, 2061–2066. Vanderklift M.A. & Ponsard S. (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136, 169–182. Waddington K. & MacArthur L. (2008) Diet quality and muscle tissue location influence consumer–diet discrimination in captive-reared rock lobsters (Panulirus cygnus). Marine Biology 154, 569–576. Wolfe R.R. & Chinkes D.L. (2005) Isotope Tracers Metabolic Research: Principles and Practice of Kinetic Analysis ( 2nd edn). Wiley-Liss, Hoboken, NJ, USA. 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. Zar J.H. (2010) Biostatistical Analysis ( 5th edn). Pearson Education, Upper Saddle River, NJ, USA. ISBN 978-0131008465. Citing Literature Volume47, Issue10October 2016Pages 3070-3087 ReferencesRelatedInformation
Referência(s)