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Elemental Concentrations in the Shells of the Mussel Perna perna: Discrimination of Origin

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Abstract

The potential use of elemental concentrations and element:calcium (Ca) ratios as indicators of provenance for bivalve mollusks on the Brazilian coast is evaluated herein for the first time. The approach was applied to shells of the mussel Perna perna (target of extractive fisheries) from geographically close areas but under distinct environmental and anthropogenic influences. Both concentrations of the elements normalized by Ca and the total concentrations can be applied to discriminate the mussels’ origin. However, the canonical approach using the total concentrations indicated variations regarding the discriminatory power, and the concentrations of the elements normalized by Ca were more robust in differentiating the provenance of the shells. The origin of mussels was better discriminated by six elementary ratios: Al:Ca, Fe:Ca, K:Ca, Mg:Ca, Mn:Ca and Na:Ca. Thus, monitoring studies aiming to discriminate the origin of P. perna individuals along their distribution based on these elementary ratios of the shell are recommended.

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Data Availability

The data that support this study are available from the corresponding author upon reasonable request.

References

  1. Gosling E (2015) Marine Bivalve Molluscs. Wiley-Blackwell, Hoboken

    Book  Google Scholar 

  2. Gonçalves TS, Lima DF, Di Beneditto APM, Franco RWA (2021) Free radicals in the Perna perna mussel shell. Radiat Phys Chem 188:109674. https://doi.org/10.1016/j.radphyschem.2021.109674

  3. Vaughn CC, Hoellein TJ (2018) Bivalve Impacts in Freshwater and Marine Ecosystems. Annu Rev Ecol Evol Syst 49:183–208. https://doi.org/10.1146/annurev-ecolsys-110617-062703

    Article  Google Scholar 

  4. Bertine KK, Goldberg ED (1972) Trace elements in clams, mussels, and shrimp. Limnol Oceanogr 17:877–884. https://doi.org/10.4319/lo.1972.17.6.0877

    Article  CAS  Google Scholar 

  5. Lindh U, Mutvei H, Sunde T, Westermark T (1988) Environmental history told by mussel shells. Nucl Instruments Methods Phys Res Sect B Beam Interact Mater Atoms 30:388–392. https://doi.org/10.1016/0168-583X(88)90030-4

    Article  Google Scholar 

  6. Bellotto VR, Miekeley N (2007) Trace metals in mussel shells and corresponding soft tissue samples: a validation experiment for the use of Perna perna shells in pollution monitoring. Anal Bioanal Chem 389:769–776. https://doi.org/10.1007/s00216-007-1420-y

    Article  CAS  PubMed  Google Scholar 

  7. Merschel G, Bau M (2015) Rare earth elements in the aragonitic shell of freshwater mussel Corbicula fluminea and the bioavailability of anthropogenic lanthanum, samarium and gadolinium in river water. Sci Total Environ 533:91–101. https://doi.org/10.1016/j.scitotenv.2015.06.042

    Article  CAS  PubMed  Google Scholar 

  8. Silva EP, Souza RCCL, Lima TA et al (2018) Zooarchaeological evidence that the brown mussel (Perna perna) is a bioinvader of coastal Brazil. Holocene 28:1771–1780. https://doi.org/10.1177/0959683618788670

    Article  Google Scholar 

  9. Henriques MB, Marques HL de A, Barrella W, Pereira OM (2001) Estimativa do tempo de recuperação de um banco natural do mexilhão Perna perna (Linnaeus, 1758) na Baía de Santos, estado de São Paulo. Holos Environ 1:85–100. https://doi.org/10.14295/holos.v1i2.1619

  10. Resgalla Jr C, Weber LI, Conceição MB da (2008) O mexilhão Perna perna (L.): Biologia, ecologia e aplicações, 1st edn. Interciência, Rio de Janeiro

  11. Pierri BS, Fossari TD, Magalhães ARM (2016) O mexilhão Perna perna no Brasil: nativo ou exótico? Arq Bras Med Veterinária e Zootec 68:404–414. https://doi.org/10.1590/1678-4162-8534

    Article  Google Scholar 

  12. Antunes RM, Mesquita E de FM de (2018) Exploração extrativa do mexilhão Perna perna (Mollusca: Bivalvia) no estado do Rio de Janeiro e suas questões socioculturais, educacionais, governamentais, ambientais e de saúde coletiva: uma revisão de literatura. Rev Vértices 20:304–316. https://doi.org/10.19180/1809-2667.v20n32018p304-316

  13. Avelar WEP, Mantelatto FLM, Tomazelli AC et al (2000) (2000) The marine mussel Perna perna (Mollusca, Bivalvia, Mytilidae) as an Indicator of contamination by Heavy Metals in the Ubatuba Bay, SÃo Paulo, Brazil. Water Air Soil Pollut 1181(118):65–72. https://doi.org/10.1023/A:1005109801683

    Article  Google Scholar 

  14. Catharino MGM, Vasconcellos MBA, de Sousa ECPM et al (2008) Biomonitoring of Hg, Cd, Pb and other elements in coastal regions of São Paulo State, Brazil, using the transplanted mussel Perna perna (Linnaeus, 1758). J Radioanal Nucl Chem 278:547–551. https://doi.org/10.1007/s10967-008-1003-1

    Article  CAS  Google Scholar 

  15. Seo D, Vasconcellos MBA, Saiki M et al (2012) Vanadium biomonitoring by using Perna perna (Linnaeus, 1758) mussels transplanted in the coast of the State of São Paulo, Brazil. J Radioanal Nucl Chem 291:101–105. https://doi.org/10.1007/s10967-011-1238-0

    Article  CAS  Google Scholar 

  16. Sorte CJB, Etter RJ, Spackman R, et al (2013) Elemental fingerprinting of mussel shells to predict population sources and redistribution potential in the Gulf of Maine. PLoS One 8:e80868. https://doi.org/10.1371/journal.pone.0080868

  17. Cathey AM, Miller NR, Kimmel DG (2014) Spatiotemporal stability of trace and minor elemental signatures in early larval shell of the Northern Quahog (Hard Clam) Mercenaria mercenaria. J Shellfish Res 33:247–255. https://doi.org/10.2983/035.033.0124

    Article  Google Scholar 

  18. Becker BJ, Levin LA, Fodrie FJ, McMillan PA (2007) Complex larval connectivity patterns among marine invertebrate populations. Proc Natl Acad Sci 104:3267–3272. https://doi.org/10.1073/pnas.0611651104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Norrie C, Dunphy B, Baker J, Lundquist C (2016) Local-scale variation in trace elemental fingerprints of the estuarine bivalve Austrovenus stutchburyi within and between estuaries. Mar Ecol Prog Ser 559:89–102. https://doi.org/10.3354/meps11890

    Article  CAS  Google Scholar 

  20. Norrie CR, Dunphy BJ, Ragg NLC, Lundquist CJ (2019) Comparative influence of genetics, ontogeny and the environment on elemental fingerprints in the shell of Perna canaliculus. Sci Rep 9:1–11. https://doi.org/10.1038/s41598-019-44947-0

    Article  CAS  Google Scholar 

  21. Brasil (2006) Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA). Instrução normativa n 105, de 20 de julho de 2006. Diário Of da União

  22. Thomsen V, Schatzlein D, Mercuro D (2003) Limits of Detection in Spectroscopy. Spectroscopy 18:112–114

    CAS  Google Scholar 

  23. Skoog DA, Leary JJ (1992) Principles of instrumental analysis, 4th edn. Saunders College Publishing, Forth Worth

    Google Scholar 

  24. Chand V, Prasad S (2013) ICP-OES assessment of heavy metal contamination in tropical marine sediments: a comparative study of two digestion techniques. Microchem J 111:53–61. https://doi.org/10.1016/J.MICROC.2012.11.007

    Article  CAS  Google Scholar 

  25. R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  26. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Book  Google Scholar 

  27. Altman N, Krzywinski M (2016) Regression diagnostics. Nat Methods 13:385–386. https://doi.org/10.1038/nmeth.3854

    Article  CAS  Google Scholar 

  28. O’Connor BP (2022) DFA.CANCOR: linear discriminant function and canonical correlation analysis. https://rdrr.io/cran/DFA.CANCOR/

  29. Nędzarek A, Czerniejewski P, Tórz A (2021) A comparison of the concentrations of heavy metals in modern and medieval shells of swollen river mussels (Unio tumidus) from the Szczecin Lagoon, SW Baltic basin. Mar Pollut Bull 163. https://doi.org/10.1016/j.marpolbul.2020.111959

  30. Giarratano E, Duarte CA, Amin OA (2010) Biomarkers and heavy metal bioaccumulation in mussels transplanted to coastal waters of the Beagle Channel. Ecotoxicol Environ Saf 73:270–279. https://doi.org/10.1016/J.ECOENV.2009.10.009

    Article  CAS  PubMed  Google Scholar 

  31. Chandurvelan R, Marsden ID, Glover CN, Gaw S (2016) Biomarker responses of mussels exposed to earthquake disturbances. Estuar Coast Shelf Sci 182:98–111. https://doi.org/10.1016/j.ecss.2016.09.008

    Article  CAS  Google Scholar 

  32. Hariharan G, Purvaja R, Robin RS, Ramesh R (2016) Evaluation of the multiple biomarkers on identification of the vulnerable coastal pollution hotspots. Environ Sci Pollut Res 23:23281–23290. https://doi.org/10.1007/s11356-016-7548-6

    Article  CAS  Google Scholar 

  33. Klecka W (1980) Discriminant analysis. SAGE Publications, Thousand Oaks

    Book  Google Scholar 

  34. Freitas PS, Clarke LJ, Kennedy H et al (2006) Environmental and biological controls on elemental (Mg/Ca, Sr/Ca and Mn/Ca) ratios in shells of the king scallop Pecten maximus. Geochim Cosmochim Acta 70:5119–5133. https://doi.org/10.1016/J.GCA.2006.07.029

    Article  CAS  Google Scholar 

  35. Barats A, Amouroux D, Pécheyran C et al (2008) High-frequency archives of manganese inputs to coastal waters (Bay of Seine, France) resolved by the LA-ICP-MS analysis of calcific growth layers along scallop shells (Pecten maximus). Environ Sci Technol 42:86–92. https://doi.org/10.1021/es0701210

    Article  CAS  PubMed  Google Scholar 

  36. Steinhardt J, Butler PG, Carroll ML, Hartley J (2016) The application of long-lived bivalve sclerochronology in environmental baseline monitoring. Front Mar Sci 0:176. https://doi.org/10.3389/FMARS.2016.00176

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Acknowledgements

We are indebted to B.C.V. Oliveira for chemical elements analysis. This research was funding by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (grant no. 302.598/2021-9), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (grants no. E-26/210.498/2019, E-26/200.797/2021 and E-26/200.586/2022), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Financial Code 001.

Funding

DFL and TSG: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES), Financial Code 001.

IAP: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), E-26/200.586/2022.

APMDB: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), 302.598/2021–9 and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), E-26/200.797/2021.

RWAF: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), E-26/210.498/2019.

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Authors and Affiliations

  1. Laboratório de Ciências Físicas, Universidade Estadual Do Norte Fluminense Darcy Ribeiro, Av. Alberto Lamego, 2000, Campos Dos Goytacazes, RJ, 28013-602, Brazil

    Dayvison Felismindo Lima, Thaluana Silva Gonçalves & Roberto Weider de Assis Franco

  2. Laboratório de Ciências Ambientais, Universidade Estadual Do Norte Fluminense Darcy Ribeiro, Av. Alberto Lamego, 2000, Campos Dos Goytacazes, RJ, 28013-602, Brazil

    Inácio Abreu Pestana & Ana Paula Madeira Di Beneditto

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  1. Dayvison Felismindo Lima
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  2. Thaluana Silva Gonçalves
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  3. Inácio Abreu Pestana
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  4. Ana Paula Madeira Di Beneditto
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  5. Roberto Weider de Assis Franco
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APMDB and RWAF designed the study, interpreted the results and edited the manuscript. DFL, TSG and IAP performed de statistics study, interpreted the results and edited the manuscript. All authors read and approved the final manuscript.

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Correspondence to Roberto Weider de Assis Franco.

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Lima, D.F., Gonçalves, T.S., Pestana, I.A. et al. Elemental Concentrations in the Shells of the Mussel Perna perna: Discrimination of Origin. Biol Trace Elem Res 202, 1279–1287 (2024). https://doi.org/10.1007/s12011-023-03734-9

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