Diet-tissue discrimination factors of three neotropical freshwater fishes and a comparison of the trophic position

Submitted: 3 October 2023
Accepted: 1 December 2023
Published: 21 December 2023
Abstract Views: 1130
PDF: 133
Supplementary: 28
HTML: 3
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

The trophic discrimination factor (TDF) is a key parameter for stable isotope analysis and due to a lack of species-specific TDFs, mean universal values have been used, resulting in uncertainties about the trophic position of species and a call for more experiments. In this study, we have addressed the lack of experimental species-specific TDFs conducting three experiments of 128 days each to determine the TDF (muscle and liver) of three species, the piscivore Pseudoplatystoma corruscans (Spix & Agassiz, 1829), and the omnivores Piaractus mesopotamicus (Holmberg, 1887) and Astyanax lacustris (Lütken, 1875), tropical fishes native to the La Plata River basin. Then, we calculated the trophic position (TP) using the mean universal TDF from literature and the species-specific TDF produced in this study for Pseudoplatystoma corruscans. We estimated the TDFs for the three species through experiment and the values found differed from the mean universal TDF in the literature. Moreover, the TP was lower when using the species-specific TDFs. The TP is important for several analyses, including its use in functional diversity. Therefore, we recommend using species-specific TDF values for calculating TP once it differs from the results calculated with mean universal TDF.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Abimorad EG, Carneiro DJ, 2007. Digestibility and performance of pacu (Piaractus mesopotamicus) juveniles - fed diets containing different protein, lipid and carbohydrate levels. Aquacult. Nutr. 13:1-9. DOI: https://doi.org/10.1111/j.1365-2095.2007.00438.x
Auer SK, Dick CA, Metcalfe NB, Reznick DN, 2018. Metabolic rate evolves rapidly and in parallel with the pace of life history. Nat. Commun. 9:1-6. DOI: https://doi.org/10.1038/s41467-017-02514-z
Barnes C, Sweeting CJ, Jennings S, Barry JT, Polunin NVC, 2007. Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Funct. Ecol. 21:356-362. DOI: https://doi.org/10.1111/j.1365-2435.2006.01224.x
Bennett E, Basurto X, Virdin J, Lin X, Betances SJ, Smith MD, et al., 2021. Recognize fish as food in policy discourse and development funding. Ambio 50:981-989. DOI: https://doi.org/10.1007/s13280-020-01451-4
Britton JR, Busst GMA, 2017. Stable isotope discrimination factors of omnivorous fishes: influence of tissue type, temperature, diet composition and formulated feeds. Hydrobiologia 808:219-234. DOI: https://doi.org/10.1007/s10750-017-3423-9
Busst GMA, Britton JR, 2016. High variability in stable isotope diet-tissue discrimination factors of two omnivorous freshwater fishes in controlled ex situ conditions. J. Exp. Biol. 219:1060-1068. DOI: https://doi.org/10.1242/jeb.137380
Canseco JA, Niklitschek EJ, Harrod C, 2022. Variability in δ13C and δ15N trophic discrimination factors for teleost fishes: a meta-analysis of temperature and dietary effects. Rev. Fish Biol. Fish. 32:313-329. DOI: https://doi.org/10.1007/s11160-021-09689-1
Caut S, Jowers MJ, Michel L, Lepoint G, Fisk A, 2013. Diet- and tissue-specific incorporation of isotopes in the shark Scyliorhinus stellaris, a North Sea mesopredator. Mar. Ecol. Prog. 492:185-198. DOI: https://doi.org/10.3354/meps10478
Colborne SF, Fisk AT, Johnson TB, 2017. Tissue-specific turnover and diet-tissue discrimination factors of carbon and nitrogen isotopes of a common forage fish held at two temperatures. Rapid Commun. Mass Spectrom. 31:1405-1414. DOI: https://doi.org/10.1002/rcm.7922
Deleens E, Lerman JC, Nato A, Moyse A, 1974. Carbon isotope discrimination by the carboxylating reactions in C3, C4 and CAM Plants. Proceedings of the Third International Congress on Photosynthesis Rehovot, Israel, p. 1267-1276. Amsterdam, Elsevier.
Deniro MJ, Epstein S, 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45:341-351. DOI: https://doi.org/10.1016/0016-7037(81)90244-1
Faria ACEA, Benedito E, 2011. Quality and digestibility of food ingested by various trophic fish groups in the Upper Paraná River floodplain. Rev. Biol. Trop. 59:85-101.
Gannes LZ, O’Brien DM, Martínez del Rio C, 1997. Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271-1276. DOI: https://doi.org/10.1890/0012-9658(1997)078[1271:SIIAEA]2.0.CO;2
García-Pérez OD, Cruz-Valdez JC, Ramírez-Martínez C, Villarreal-Cavazos D, Gamboa-Delgado J, 2018. Exploring the contribution of dietary protein from poultry by-product meal and fish meal to the growth of catfish Ictalurus punctatus by means of nitrogen stable isotopes. Lat. Am. J. Aquat. Res. 46:37-44. DOI: https://doi.org/10.3856/vol46-issue1-fulltext-5
Graça WJ, Pavanelli CS, 2007. [Peixes da planície de inundação do alto rio Paraná e áreas adjacentes].[Book in Portuguese]. Maringá: Editora da Universidade Estadual de Maringá.
Hahn NS, Fugi R, Peretti D, Russo MR, Loureiro-Crippa VE, 2002. [Estrutura trófica da ictiofauna da planície de inundação do alto rio Paraná], p. 123-126. In: A. E. A. M. Vazzoler, A. A. Agostinho, N. S. Hahn (eds.), [A Planície de Inundação do Alto rio Paraná].[Book in Portuguese]. Maringá: Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura.
Heady WN, Moore JW, 2013. Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout. DOI: https://doi.org/10.1007/s00442-012-2483-9
Oecologia 172:21-34.
Hobson KA, Clark RG, 1992. Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181-188. DOI: https://doi.org/10.2307/1368807
Hoeinghaus DJ, Agostinho AA, Gomes LC, Pelicice FM, Okada EK, Latini JD, et al., 2009. Effects of river impoundment on ecosystem services of large tropical rivers: embodied energy and market value of artisanal fisheries. Conserv. Biol. 23:1222-1231. DOI: https://doi.org/10.1111/j.1523-1739.2009.01248.x
Jepsen DB, Winemiller KO, 2002. Structure of tropical river food webs revealed by stable isotope ratios. Oikos 96:46-55. DOI: https://doi.org/10.1034/j.1600-0706.2002.960105.x
Kadye WT, Redelinghuys S, Parnel AC, Booth A, 2020. Exploring source differences on diet‑tissue discrimination factors in the analysis of stable isotope mixing models. Sci. Rep. 10:15816. DOI: https://doi.org/10.1038/s41598-020-73019-x
Layman CG, Arrington DA, Montaña CG, Post DM, 2007. Can stable isotopes ratios provide for community-wide measures of trophic structure? Ecology 88:42-48. DOI: https://doi.org/10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2
Madigan DJ, Snodgrass OE, Hyde JR, Dewar H, 2021. Stable isotope turnover rates and fractionation in captive California yellowtail (Seriola dorsalis): insights for application to field studies. Sci. Rep. 11:4466. DOI: https://doi.org/10.1038/s41598-021-83880-z
Maitland BM, Martínez del Rio C, Rahel FJ, 2021. Effect of temperature on 13C and 15N incorporation rates and discrimination factors in two North American fishes. Can. J. Fish. Aquat. Sci. 78:1833-1840. DOI: https://doi.org/10.1139/cjfas-2021-0057
Martínez del Rio C, Wolf N, Carleton SA, Gannes LZ, 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biol. Rev. Camb. Philos. Soc. 84: 91-111. DOI: https://doi.org/10.1111/j.1469-185X.2008.00064.x
Maruyama A, Tanahashi E, Hirayama T, Yonekura R, 2016. A comparison of changes in stable isotope ratios in the epidermal mucus and muscle tissue of slow-growing adult catfish. Ecol. Freshw. Fish. 26:636-642. DOI: https://doi.org/10.1111/eff.12307
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J, 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858. DOI: https://doi.org/10.1038/35002501
McConnaughey T, Macroy CP, 1979. Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Mar. Biol. 53:57-262. DOI: https://doi.org/10.1007/BF00952434
McCutchan Jr JH, Lewis Jr WM, Kendall C, McGrath CC, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102:378-390. DOI: https://doi.org/10.1034/j.1600-0706.2003.12098.x
Minagawa M, Wada E, 1984. Stepwise enrichment of 15N along food-chains-further evidence and the relation between δ15N and animal age. Geochim. Cosmochim. Acta 48:1135-1149. DOI: https://doi.org/10.1016/0016-7037(84)90204-7
Nahon S, Séité S, Lefebvre S, Kolasinski J, Aguirre P, Geurden I, 2020. How protein quality drives incorporation rates and trophic discrimination of carbon and nitrogen stable isotope ratios in a freshwater first-feeding fish. Freshwater Biol. 65:1870-1882. DOI: https://doi.org/10.1111/fwb.13578
Nawrocki B, McLeod AM, Hussey NE, Colborne SF, Papa JD, Fisk AT, 2020. Assessing trophic position quantification methods for three piscivorous freshwater fish using stable isotopes and stomach contents. J. Great Lakes Res. 46:578-588. DOI: https://doi.org/10.1016/j.jglr.2020.03.017
Ota RR, Deprá GC, Graça WJ, Pavanelli CS, 2018.[ Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated].[Article in Portuguese with English abstract]. Neotrop. Ichthyol. 16:e170094. DOI: https://doi.org/10.1590/1982-0224-20170094
Pereira LP, Benedito E, 2007. [Isótopos estáveis em estudos ecológicos: métodos, aplicações e perspectivas].[Article in Portuguese]. Rev. Biocie. 13:16-27.
Peterson BJ, Fry B, 1987. Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Evol. 18:293-320. DOI: https://doi.org/10.1146/annurev.es.18.110187.001453
Philippsen JS, Benedito E, 2013. [Fator de discriminação na ecologia trófica de peixes: uma revisão sobre as fontes de variação e os métodos de obtenção].[Article in Portuguese with English abstract]. Oecol. Aust. 17:205-216. DOI: https://doi.org/10.4257/oeco.2013.1702.03
Post DM, 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703-718. DOI: https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
Quezada-Romegialli C, Jackson AL, Hayden B, Kahilainen KK, Lopes C, Harrod C, 2018. tRophicPosition, an R package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol. Evol. 9:1592-1599. DOI: https://doi.org/10.1111/2041-210X.13009
R Core Team. R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing: 2022.
Reis AS, Albrecht MP, Bunn S, 2020. Food web pathways for fish communities in small tropical streams. Freshwater Biol. 65:893-907. DOI: https://doi.org/10.1111/fwb.13471
Roth JD, Hobson KA, 2000. Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction. Can. J. Zool. 78:848-852. DOI: https://doi.org/10.1139/z00-008
Sacramento PA, Manetta GI, BeneditoE, 2016. Diet-tissue discrimination factors (Δ13C and Δ15N) and turnover rate in somatic tissues of a Neotropical detritivorous fish on C3 and C4 diets. J. Fish Biol. 89:213-219. DOI: https://doi.org/10.1111/jfb.12859
Sawada H, Fujiwara S, Tanaka R, Yonekura R, Maruyama A, 2021. Turnover rates for muscle, mucus and ovary tissues of ayu fish (Plecoglossus altivelis altivelis) in multiple stages determined through carbon and nitrogen stable isotope analyses. Ecol. Freshw. Fish 30:466-477. DOI: https://doi.org/10.1111/eff.12597
Scharnweber K, Andersson ML, Chaguaceda F, EklövP, 2021. Intraspecific differences in metabolic rates shape carbon stable isotope trophic discrimination factors of muscle tissue in the common teleost Eurasian perch (Perca fluviatilis). Ecol. Evol. 11:9804-9814. DOI: https://doi.org/10.1002/ece3.7809
Smith BN, Epstein S, 1971. Two categories of 13C/12C ratios for higher plants. Plant Physiol. 47:380-384. DOI: https://doi.org/10.1104/pp.47.3.380
Takahashi LS, Ha N, Pereira MM, Biller-Takahashi JD, Urbinati EC, 2018. Carbohydrate tolerance in the fruit-eating fish Piaractus mesopotamicus (Holmberg, 1887). Aquat. Res. 49:1182-1188. DOI: https://doi.org/10.1111/are.13571
Tieszen LL, Boutton TW, Tesdahl KG, Slade NA, 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32-37. DOI: https://doi.org/10.1007/BF00379558
Underwood W, Anthony R, Gwaltney-Brant S, Poison ASPCA, Meyer R, 2013. AVMA guidelines for the euthanasia of animals: 2013 edition. Schaumburg: American Veterinary Medical Association.
Urabe J, 1995. Direct and indirect effects of zooplankton on seston stoichiometry. Ecoscience 2:286-296. DOI: https://doi.org/10.1080/11956860.1995.11682296
Vander Zanden MJ, Rasmussen JB, 2001. Variation in δ15N and δ13C trophic fractionation: implications for aquatic food webs studies. Limnol. Oceanogr. 46:2061-2066. DOI: https://doi.org/10.4319/lo.2001.46.8.2061
Vidotto-Magnoni AP, Kurchevski G, Lima FP, Nobile AB, Garcia DA, Casimiro AC, et al., 2021. Population biology of Astyanax lacustris (Pisces, Characiformes) in a Neotropical reservoir and its tributaries. An. Acad. Bras. Cienc. 93:e20190565. DOI: https://doi.org/10.1590/0001-3765202120190565
Villar PC, Ribeiro WC, Sant’anna FM, 2018. Transboundary governance in the La Plata River basin: status and prospects. Water Int. 43:978-995. DOI: https://doi.org/10.1080/02508060.2018.1490879
Winter ER, Nolan ET, Busst GMA, Britton JR, 2019. Estimating stable isotope turnover rates of epidermal mucus and dorsal muscle for an omnivorous fish using a diet-switch experiment. Hydrobiologia 828:245-258. DOI: https://doi.org/10.1007/s10750-018-3816-4
Zhou H, Gu B, 2020. Using stable isotope analysis to assess the relationship among dietary protein sources, growth, nutrient turnover and incorporation in Nile tilapia (Oreochromis niloticus). Aquacult. Nutr. 26:1443-1452. DOI: https://doi.org/10.1111/anu.13091

Edited by

Diego Fontaneto, National Research Council, Water Research Institute (CNR-IRSA), Verbania Pallanza, Italy
Matheus Maximilian Ratz Scoarize, Graduate Program in Ecology of Inland Water Ecosystems (PEA), Research Nucleus in Limnology, Ichthyology and Aquaculture (NUPELIA) - State University of Maringá

 Australian Rivers Institute (ARI), Griffith University, Brisbane, Australia

How to Cite

Manetta, Gislaine Iachstel, Matheus Maximilian Ratz Scoarize, Driele Delanira-Santos, Patrícia Almeida Sacramento, Vinícius de Andrade Urbano, and Evanilde Benedito. 2023. “Diet-Tissue Discrimination Factors of Three Neotropical Freshwater Fishes and a Comparison of the Trophic Position”. Journal of Limnology 82 (1). https://doi.org/10.4081/jlimnol.2023.2159.