Skip to main content

Advertisement

SpringerLink
Log in

Stomach contents and stable isotope analysis reveal ontogenetic shifts and spatial variability in Brama australis diet

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

Many marine fisheries rely on production and energy flow in the pelagic zone; thus, sustainable management of exploited pelagic fishes benefits from insight into temporal, spatial, and ontogenetic variability in the trophic ecology of these species. Here, we analyze stomach contents and stable isotopes to reveal spatial variability (focusing on two fishing grounds, north and south of an oceanographic barrier in the Pacific Ocean) and ontogenetic changes (contrasting immature and mature) in Southern Ray’s Bream (Brama australis) diet composition in Chilean waters. Stomach contents analysis indicated that euphausiids were predominant components of the diet in both fishing grounds and ontogenetic stages. Patterns of prey long-term assimilation, revealed in Bayesian mixing models of predator and prey isotopic values of δ15N and δ13C, differed from diet as indicated in stomach contents. Shrimps and crustacean larvae were more important than euphausiids in the northern and southern fishing ground, respectively. In both fishing grounds, diet shifted after maturity towards increased use of shrimps. Combining methods of stomach contents analysis and stable isotopes analysis is a powerful approach to determining predator–prey relationships and energy flow in pelagic fishes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

This project had all the fishing certificates to capture and operate in the waters of the Chilean territory.

References

  • Arancibia H, Alarcón R, Barros M et al (2017) Actualización de parámetros de historia de vida de reineta (Brama australis) en aguas nacionales Technical Report. Chil Fish Res Fund FIPA. 20:309

    Google Scholar 

  • Brown SC, Bizzarro JJ, Cailliet GM, Ebert DA (2012) Breaking with tradition: redefining measures for diet description with a case study of the Aleutian skate Bathyraja aleutica (Gilbert 1896). Environ Biol Fishes 95(1):3–20. https://doi.org/10.1007/s10641-011-9959-z

    Article  Google Scholar 

  • Camus PA (2001) Biogeografía marina de Chile continental. Rev Chil Hist Nat 74:587–617

    Article  Google Scholar 

  • Canales-Aguirre C, Herrera-Yanez V, Ferrada-Fuentes S, Galleguillos R (2018) Stowaways in the catch: identification of Xenobrama microlepis in the haul fishery for Brama australis. Rev Biol Mar Oceanogr 53:7–13

    Article  Google Scholar 

  • Castillo-Jordán C, Wayte SE, Tuck GN et al (2019) Implications of a climate-induced recruitment shift in the stock assessment of Patagonian grenadier (Macruronus magellanicus) in Chile. Fish Res 212:114–122

    Article  Google Scholar 

  • 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. J Appl Ecol 46:443–453

    Article  CAS  Google Scholar 

  • Edwards MS, Konar B (2020) Trophic downgrading reduces spatial variability on rocky reefs. Sci Rep 10:18079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flotemersch JE, Shattuck SM, Aho KB et al (2019) Factors influencing social demands of aquatic ecosystems. Ecol Soc 24:1–9

    Article  PubMed  PubMed Central  Google Scholar 

  • Fry B (2013) Alternative approaches for solving underdetermined isotope mixing problems. Mar Ecol Prog Ser 472:1–13

    Article  CAS  Google Scholar 

  • Garcia C, Chong J (2002) Composicion de la dieta de Brama australis Valenciennes 1837 en la zona centro-sur de Chile (VIII Region) en otono 2000 y verano 2001. Gayana 66:225–230

    Google Scholar 

  • Gelman A, Carlin JB, Stern HS, Dunson DB, Vehtari A, Rubin DB (2015) Bayesian data analysis. Chapman and Hall/CRC, Boca Raton FL

    Google Scholar 

  • Gerking SD (1994) Feeding ecology of fish. Elsevier, Arizona AZ

    Google Scholar 

  • Grey J, Thackeray SJ, Jones RI, Shine A (2002) Ferox Trout (Salmo trutta) as `Russian dolls’: complementary gut content and stable isotope analyses of the Loch Ness foodweb. Freshw Biol 47:1235–1243

    Article  Google Scholar 

  • Griffiths HJ, Waller CL (2016) The first comprehensive description of the biodiversity and biogeography of Antarctic and Sub-Antarctic intertidal communities. J Biogeogr 43:1143–1155

    Article  Google Scholar 

  • Horn PL, Forman JS, Dunn MR (2013) Moon phase influences the diet of southern Ray’s bream Brama australis. J Fish Biol 82:1376–1389

    Article  CAS  PubMed  Google Scholar 

  • Klarian SA, Canales-Cerro C, Barría P et al (2018a) New insights on the trophic ecology of blue (Prionace glauca) and shortfin mako sharks (Isurus oxyrinchus) from the oceanic eastern South Pacific. Mar Biol Res 14:173–182

    Article  Google Scholar 

  • Klarian SA, Molina-Burgos BE, Saavedra A et al (2018b) New insights on feeding habits of the southern blue whiting Micromesistius australis Norman, 1937 in eastern South Pacific waters. J Appl Ichthyol 34:694–697

    Article  Google Scholar 

  • Litz MNC, Miller JA, Copeman LA et al (2017) Ontogenetic shifts in the diets of juvenile Chinook Salmon: new insight from stable isotopes and fatty acids. Environ Biol Fishes 100:337–360

    Article  Google Scholar 

  • Logan JM, Jardine TD, Miller TJ et al (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J Anim Ecol 77:838–846

    Article  PubMed  Google Scholar 

  • Michener R, Kaufman L (2007) Stable isotope ratios as tracers in marine food webs: an update. In: Michener R, Lajtha K (eds) Stable Isotopes in Ecology and Environmental Science, 2nd edn. Blackwell Publishing, Malden MA, pp 238–282

    Chapter  Google Scholar 

  • Nielsen JM, Clare EL, Hayden B et al (2018) Diet tracing in ecology: method comparison and selection. Methods Ecol Evol 9:278–291

    Article  Google Scholar 

  • Parnell AC, Phillips DL, Bearhop S et al (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399

    Google Scholar 

  • Pavlov YP (1994) Data on the ecology and population of the southern pomfret Brama australis in the southeastern Pacific. Vopr Ikhtiol 34:124–126

    Google Scholar 

  • Pease AA, Soria-Barreto M, González-Díaz AA, Rodiles-Hernández R (2020) Seasonal variation in trophic diversity and relative importance of basal resources supporting tropical river fish assemblages in Chiapas, Mexico. Trans Am Fish Soc 149:753–769

    Article  Google Scholar 

  • Pethybridge HR, Choy CA, Polovina JJ, Fulton EA (2018) Improving marine ecosystem models with biochemical tracers. Ann Rev Mar Sci 10:199–228

    Article  PubMed  Google Scholar 

  • Phillips DL, Inger R, Bearhop S et al (2014) Best practices for use of stable isotope mixing models in food-web studies. Can J Zool 92:823–835

    Article  Google Scholar 

  • Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125

    Article  PubMed  Google Scholar 

  • Pizarro J, Docmac F, Harrod C (2019) Clarifying a trophic black box: stable isotope analysis reveals unexpected dietary variation in the Peruvian anchovy Engraulis ringens. PeerJ 7:e6968

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013. Version 3.5.1URL https://www.R-project.org/

  • Rogers AD (2007) Evolution and biodiversity of Antarctic organisms: a molecular perspective. Philos Trans R Soc Lond B Biol Sci 362:2191–2214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • San Martín MA, Leal E, Canales TM (2017) Spatial and bathymetric occurrence of Brama australis off the Chilean Coast and in the South Pacific Ocean. Rev Biol Mar Oceanogr 52:405–409

    Article  Google Scholar 

  • Santa Cruz F, Oyarzun C, Aedo G, Galvez P (2014) Southern Ray’s Bream (Brama australis) summer feeding habits off central Chile. Lat Am J Aquat Res 42:1200–1204

    Article  Google Scholar 

  • Shannon LJ, Ortega-Cisneros K, Lamont T et al (2020) Exploring temporal variability in the southern Benguela ecosystem over the past four decades using a time-dynamic ecosystem model. Front Mar Sci 7:540. https://doi.org/10.3389/fmars.2020.00540

    Article  Google Scholar 

  • Stock BC, Semmens BX (2018) MixSIAR. Version version 1.0. 2013URL https://cran.r-project.org/web/packages/MixSIAR/index.html

  • Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet d15N enrichment: a meta-analysis. Oecologia 136:169–182

    Article  PubMed  Google Scholar 

  • Waters JM (2008) Driven by the west wind drift? A synthesis of southern temperate marine biogeography, with new directions for dispersalism. J Biogeogr 35:417–427

    Article  Google Scholar 

  • Worm B, Hilborn R, Baum JK et al (2009) Rebuilding global fisheries. Sci 325:578–585

    Article  CAS  Google Scholar 

  • Wuenschel MJ, Jugovich AR, Hare JA (2006) Estimating the energy density of fish: the importance of ontogeny. Trans Am Fish Soc 135:379–385

    Article  Google Scholar 

Download references

Acknowledgements

Our special gratitude goes to the fishermen who provided the samples and the colleagues who helped opening stomachs: Consuelo Salas and Diego Riquelme.

Funding

The Fisheries Research Fund FIPA funded this work with the Project FIPA 2015–20 Update of the life history parameters of the “bream” (Brama australis) in Chilean waters (link: http://www.subpesca.cl/fipa/613/w3-propertyname-681.html).

Author information

Authors and Affiliations

  1. Centro de Investigación Marina Quintay CIMARQ, Universidad Andres Bello, Facultad de Ciencias de La Vida, Viña del Mar, Chile

    Sebastian A. Klarian, María Francisca Hernández, Juan Antonio Valdes & Francisco Fernandoy

  2. Department of Ecology and Evolutionary Biology, University of Connecticut, U-3043 Storrs, Storrs, CT, 06269-3043, USA

    Sebastian A. Klarian & Eric T. Schultz

  3. Interdisciplinary Center for Aquaculture Research (INCAR), Concepción, Chile

    Juan Antonio Valdes

  4. Departamento Ciencias Biológicas, Universidad Andres Bello, Facultad de Ciencias de La Vida, Santiago, Chile

    Juan Antonio Valdes

  5. Departamento Oceanografía, Facultad de Ciencias Naturales Y Oceanográficas, Universidad de Concepción, P.O. Box 160-C, Concepción, Chile

    Mónica E. Barros, Sergio Neira & Hugo Arancibia

  6. Programa de Doctorado en Ciencias Con Mención en Manejo de Recursos Acuáticos Renovables (MaReA), Departamento de Oceanografía, Facultad de Ciencias Naturales Y Oceanográficas, Universidad de Concepción, P.O. Box 160-C, Concepción, Chile

    Mónica E. Barros, Sergio Neira & Hugo Arancibia

Authors
  1. Sebastian A. Klarian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric T. Schultz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. María Francisca Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan Antonio Valdes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francisco Fernandoy
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mónica E. Barros
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sergio Neira
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hugo Arancibia
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Sebastian A Klarian, Maria Francisca Hernandez, Monica Barros, and Juan Antonio Valdes. The first draft of the manuscript was written by Sebastian A. Klarian, Eric T. Schultz, and Hugo Arancibia, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sebastian A. Klarian.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 13 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Klarian, S.A., Schultz, E.T., Hernández, M.F. et al. Stomach contents and stable isotope analysis reveal ontogenetic shifts and spatial variability in Brama australis diet. Environ Biol Fish 105, 1673–1682 (2022). https://doi.org/10.1007/s10641-022-01365-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-022-01365-y

Keywords

Search

Navigation