Is there an indication of the origin of nutrient supply in different morphological structures of macrofauna at two different Brazilian southeastern sandy beaches? Comparison by C and N stable isotopes

  • Tito C. M. AlmeidaEmail author
  • Pedro F. P. Rocha
  • Ilana R. Zalmon
  • Marcelo G. Almeida
  • Carlos E. Rezende
  • Claudemir M. RadetskiEmail author
Research Article


The goals of this study were to analyze if there is a difference in the stable isotopic ratio (δ13C and δ15N) of macrobenthic species sampled at two sandy beaches (one close to a river mouth and the other far from any freshwater input) and to identify differences in the stable isotopic ratio (δ13C and δ15N) in different body parts of three representative species of two Brazilian sandy beach macrofaunas: the polychaete Hemipodia californiensis, the mollusk bivalve Donax hanleyanus, and the crustacean decapod Emerita brasiliensis. No significant differences were detected in the δ13C stable isotopic ratio between the two sites analyzed; however, in the δ15N stable isotopic ratio, a significant difference was observed. Regarding the intraspecific response of stable isotopic ratio, D. hanleyanus showed a significant difference in carbon among different body part structures, while a trend for significance was observed for nitrogen isotopes. The differences were significant for both isotopes in E. brasiliensis, and no differences were observed among the body part structures in H. californiensis. There were significant differences in E. brasiliensis carapaces with regard to the δ15N stable isotopic ratio between the muscle and the whole body. Although the δ13C and δ15N stable isotopic ratio differs significantly in the digestive tract, muscles, and whole body of D. hanleyanus, such differences were not enough to determine changes in their trophic levels and food sources. Similar stable isotopic ratios were observed in the whole body, proboscis, and teeth of H. californiensis, highlighting this species as the top predator. In conclusion, stable isotopic analysis of benthic trophic structure can be employed as a tool in coastal management plans or environmental impact studies.


Stable isotopes δ13C and δ15Macrofauna morphological structure Sandy beach Beach ecology Trophic network 


Funding information

This study received financial support from the Universidade Estadual do Norte Fluminense (Brazil). T.C.M. Almeida received grants from Brazilian agencies FAPERJ (no. 102.004/2013) and CNPq (no. 158504/2014-3).


  1. Antonio ES, Kasai A, Ueno M, Kurikawa Y, Tsuchiya K, Toyohara H, Ishihi Y, Yokoyama H, Yamashita Y (2010) Consumption of terrestrial organic matter by estuarine molluscs determined by analyses of their stable isotopes and cellulase activity. Estuar Coast Shelf Sci 86:401–407CrossRefGoogle Scholar
  2. Bergamino L, Lercari D, Defeo O (2011) Food web structure of sandy beaches: temporal and spatial variation using stable isotope analyses. Estuar Coast Shelf Sci 91:536–543CrossRefGoogle Scholar
  3. Bongiorni L, Fiorentino F, Auriemma R, Aubry FB, Camatti E, Camin F, Nasi F, Pansera M, Ziller L, Grall J (2016) Food web of a confined and anthropogenically affected coastal basin (the Mar Piccolo of Taranto) revealed by carbon and nitrogen stable isotopes analyses. Environ Sci Pollut Res 23:2725–12738CrossRefGoogle Scholar
  4. Carreira RS, Cordeiro LGMS, Oliveira DRP, Baêta A, Wagener ALR (2015) Source and distribution of organic matter in sediments in the SE Brazilian continental shelf influenced by river discharges: an approach using stable isotopes and molecular markers. J Mar Syst 141:80–89CrossRefGoogle Scholar
  5. Corbisier TN, Soares LSH, Petti MAV, Muto EY, Silva MHC, McClelland J, Valiela I (2006) Use of isotopic signatures to assess the food web in a tropical shallow marine ecosystem of Southeastern Brazil. Aquat Ecol 40:381–390CrossRefGoogle Scholar
  6. Corbisier TN, Petti MAV, Soares LS, Muto EY, Bromberg S, Valiela I (2014) Trophic structure of benthic communities in the Cabo Frio upwelling system (southeastern Brazilian shelf): a temporal study using stable isotope analyses. Mar Ecol Prog Ser 512:23–38CrossRefGoogle Scholar
  7. Cordeiro LGMS, Wagener ALR, Carreira RS (2018) Organic matter in sediments of a tropical and upwelling influenced region of the Brazilian continental margin (Campos Basin, Rio de Janeiro). Org Geochem 120:86–98CrossRefGoogle Scholar
  8. Di Beneditto APM, Rezende CE, Camargo PB, Kehrig HA (2013) Trophic niche comparison between two predators in northern Rio de Janeiro State, Brazil: a stable isotopes approach. Biota Neotrop 13:29–33CrossRefGoogle Scholar
  9. Estes L, Elsen PR, Treuer T, Ahmed L, Caylor K, Chang J, Choi JJ, Ellis E (2018) The spatial and temporal domains of modern ecology. Nat Ecol Evol 2:819–826. CrossRefGoogle Scholar
  10. Fauchald K, Jumars PA (1979) The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol 17:193–284Google Scholar
  11. France RL (1994) Nitrogen isotopic composition of marine and freshwater invertebrates. Mar Ecol Prog Ser 115:205–207CrossRefGoogle Scholar
  12. Franco MAL (2013) Uso de ferramentas múltiplas na investigação do impacto de um recife artificial sobre uma assembleia de peixes transientes no norte do estado do Rio de Janeiro. Doctoral dissertation Thesis, North Rio de Janeiro University, RJ, BrazilGoogle Scholar
  13. Fry B (2006) Stable isotope ecology. Springer, New YorkCrossRefGoogle Scholar
  14. Fry B, Mumford PL, Tam F, Fox DD, Warren GL, Havens KE, Steinman AD (1999) Trophic position and individual feeding histories of fish from Lake Okeechobee, Florida. Can J Fish Aquat Sci 56:590–600CrossRefGoogle Scholar
  15. Gustafson L, Showers W, Kwak T, Levine J, Stoskopf M (2007) Temporal and spatial variability in stable isotope compositions of a freshwater mussel: implications for biomonitoring and ecological studies. Oecologia 152:140–150CrossRefGoogle Scholar
  16. Han E, Park HJ, Bergamino L, Choi KS, Choy EJ, Yu OH, Kang CK (2015) Stable isotope analyses of a newly established macrofaunal food web 1.5 years after the Hebei Spirit oil spill. Mar Pollut Bull 90:167–180CrossRefGoogle Scholar
  17. Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI (2006) A revised model for lipid-normalizing δ13C values from aquatic organisms, with implications for isotope mixing models. J Appl Ecol 43:1213–1222CrossRefGoogle Scholar
  18. Kogure Y (2004) Stable carbon and nitrogen isotope analyses of the sublittoral benthic food web structure of an exposed sandy beach. Bul Biogeog Soc Jpn 59:15–25Google Scholar
  19. Krüger GCT, de Carvalho CEV, Suzuki MS (2006) Dissolved nutrient, chlorophyll-a and DOC dynamic under distinct riverine discharges and tidal cycles regimes at the Paraiba do Sul River estuary, RJ, Brazil. J Coast Res 39:724–730Google Scholar
  20. Levin AS (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967CrossRefGoogle Scholar
  21. Liao E, Lu W, Yan X-H, Jiang Y, Kidwell A (2015) The coastal ocean response to the global warming acceleration and hiatus. Sci Rep 5:16630. CrossRefGoogle Scholar
  22. Manetta G, Benedito-Cecilio E (2003) Aplicação da técnica de isótopos estáveis na estimativa da taxa de turnover em estudos ecológicos: uma síntese. Acta Sci Biol Sci 25:121–129CrossRefGoogle Scholar
  23. Mateo MA, Serrano O, Serrano L, Michener RH (2008) Effects of sample preparation on stable isotope ratio of carbon and nitrogen in marine invertebrates: implications for food web studies using stable isotopes. Oecologia 157:105–115CrossRefGoogle Scholar
  24. McLachlan A, Brown AC (2006) Ecology of sandy shores. Academic, New YorkGoogle Scholar
  25. Michener R, Lajtha K (2008) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell Publishing Ltd, OxfordGoogle Scholar
  26. Olsen YS, Fox SE, Hofmann L, Valiela I (2013) Benthic community composition and faunal stable isotopic signatures differ across small spatial scales in a temperate estuary. Mar Environ Res 86:12–20CrossRefGoogle Scholar
  27. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Ver Ecol Syst 18:293–320CrossRefGoogle Scholar
  28. Petracco M (2008) Produção secundária da macrofauna bentônica da zona entremarés no segmento norte da praia do Una, litoral sul do Estado de São Paulo. Tese de Doutorado, Instituto Oceanográfico, Universidade de São Paulo, 236pGoogle Scholar
  29. Pinotti RM, Minasi DM, Colling LA, Bemvenuti CE (2014) A review on macrobenthic trophic relationships along subtropical sandy shores in southernmost Brazil. Biota Neotrop 14(3):e20140069CrossRefGoogle Scholar
  30. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  31. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189CrossRefGoogle Scholar
  32. Thrush SF, Hewitt JE, Gibbs M, Lundquist C, Norkko A (2006) Functional role of large organisms in intertidal communities: community effects and ecosystem function. Ecosystems 9:1029–1040CrossRefGoogle Scholar
  33. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analyses of variance. Cambridge University Press, CambridgeGoogle Scholar
  34. UNEP (2002) Oceans and coastal areas. Coastal threats [online] Cited November 2004. Available at
  35. van der Linden PRA (2017) A trait-based approach to investigate macrobenthic community functioning in estuarine and coastal ecosystems. Universidade de Coimbra. Tese de doutoramento. Available at 18 Oct 2018
  36. Yokoyama H, Tamaki A, Harada K, Shimoda K, Koyama K, Ishihi Y (2005) Variability of diet-tissue isotopic fractionation in estuarine macrobenthos. Mar Ecol Prog Ser 296:115–128CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratório de Ecologia de ComunidadesUniversidade do Vale do Itajaí (UNIVALI)ItajaíBrazil
  2. 2.Centro de Biociências e Biotecnologia, Laboratório de Ciências AmbientaisUniversidade Estadual do Norte FluminenseRio de JaneiroBrazil

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