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Isotopic ratios of Perna perna mussel in southeast Brazil using the COVID-19 pandemic as temporal reference

Published online by Cambridge University Press:  24 September 2025

Ana Paula Madeira Di Beneditto*
Affiliation:
Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil
Dayvison Felismindo Lima
Affiliation:
Laboratório de Ciências Físicas, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil
Keltony de Aquino Ferreira
Affiliation:
Laboratório de Ecologia de Sedimentos, Departamento de Biologia Marinha, Universidade Federal Fluminense, Niterói, RJ, Brazil Instituto Serrapilheira, Rio de Janeiro, RJ, Brazil
Inácio Abreu Pestana
Affiliation:
Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil Departamento de Geoquímica, Campus do Valonguinho, Universidade Federal Fluminense, Instituto de Química, Niterói, RJ, Brazil
Roberto Weider de Assis Franco
Affiliation:
Laboratório de Ciências Físicas, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil
*
Corresponding author: Ana Paula Madeira Di Beneditto; Email: anadibeneditto@gmail.com

Abstract

Perna perna mussel is a coastal benthic filter-feeder widely cultivated in mytiliculture farms and serves as a resource for local communities engaged in its harvest along the Brazilian coast. This study presents the isotopic ratios (δ13C and δ15N) in the soft tissues of adult mussels from six natural populations in Rio de Janeiro State, southeast Brazil, to evaluate whether they are sensitive enough to distinguish the origin of specimens. The COVID-19 pandemic served as temporal reference, as the quality of coastal waters was influenced by the restrictions imposed during the pandemic. The mean values of δ13C and δ15N ranged from −19.5‰ to −17.3‰, and 6.2‰ to 10.5‰, respectively. The spatial variation of δ13C-δ15N data in the analysed mussels was greater than the temporal variation. The k-means clustering method correctly identified 80% of populations during the pre-pandemic period, 67% in the pandemic, and 50% in the post-pandemic. In most samples, the spatial variation of δ15N (tracer of food source variability) was the primary variable distinguishing the groups of mussels. The isotopic ratios did not reveal a clear trend when using the COVID-19 pandemic as temporal reference. Consequently, the positive environmental changes brought about by the suspension or reduction of anthropogenic activities in coastal waters during the pandemic had minimal impact on the isotopic ratios of mussels at most sampling sites. The utilisation of δ13C-δ15N data to trace the origin of P. perna mussel from natural banks was only partially effective in distinguishing the origin of natural populations across the studied area.

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Research Article
Copyright
© The Author(s), 2025. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom.

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References

Allan, EL, Ambrose, ST, Richoux, NB and Froneman, PW (2010) Determining spatial changes in the diet of nearshore suspension-feeders along the South African coastline: Stable isotope and fatty acid signatures. Estuarine, Coastal and Shelf Science 87, 463471.CrossRefGoogle Scholar
Anderson, MJ (2001) A new method for non‐parametric multivariate analysis of variance. Austral Ecology 26, 3246.Google Scholar
Anderson, MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). In Balakrisnan, N, Colton, T, Everitt, B, Piegorsch, W, Ruggeri, F and Teugels, J ((eds)), Wiley Statsref: statistics Reference Online. New Jersey, EUA: John Wiley and Sons, 115.Google Scholar
Antunes, RM and Mesquita, EFM (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. Revista Vértices 20, 304316.10.19180/1809-2667.v20n32018p304-316CrossRefGoogle Scholar
Barnes, C, Jennings, S and Barry, JT (2009) Environmental correlates of large-scale spatial variation in the δ13C of marine animals. Estuarine, Coastal and Shelf Science 81, 368374.10.1016/j.ecss.2008.11.011CrossRefGoogle Scholar
Berry, PF and Schleyer, MH (1983) The brown mussel Perna perna on the Natal coast, South Africa: Utilization of available food and energy budget. Marine Ecology Progress Series 13, 201210.CrossRefGoogle Scholar
Buzzi, NS, Menéndez, MC, Truchet, DM, Delgado, AL and Fernández, MDS (2022) An overview on metal pollution on touristic sandy beaches: Is the COVID-19 pandemic an opportunity to improve coastal management? Marine Pollution Bulletin 174, 113275.10.1016/j.marpolbul.2021.113275CrossRefGoogle Scholar
Coelho-Souza, SA, López, MS, Guimarães, JRD, Coutinho, R and Candella, RN (2012) Biophysical interactions in the Cabo Frio upwelling system, southeastern Brazil. Brazilian Journal of Oceanography 60, 353365.10.1590/S1679-87592012000300008CrossRefGoogle Scholar
Cui, L, Jiang, Z, Huang, X, Liu, S and Wu, Y (2023) Identification of food sources in tropical seagrass bed food web using triple stable isotopes and fatty acid signatures. Frontiers in Marine Science 10, 1093181.10.3389/fmars.2023.1093181CrossRefGoogle Scholar
de A Ferreira, K, Braga, AA and Di Beneditto, APM (2021) Can stable isotopes be applied to determine shrimp stocks origin in SE Brazil? An approach for utilization in fishery management. Ocean and Coastal Management 205, 105500.10.1016/j.ocecoaman.2020.105500CrossRefGoogle Scholar
de A Ferreira, K, Braga, AA and Di Beneditto, APM (2022) Interspecific and intraspecific comparison of the isotopic niche of shrimps targets of fishing in south-eastern Brazil. Journal of the Marine Biological Association of the United Kingdom 102, 338344.CrossRefGoogle Scholar
Del Rio-lavín, A, Weber, J, Molkentin, J, Jiménez, E, Artetxe-Arrate, I and Pardo, MA (2022) Stable isotope and trace element analysis for tracing the geographical origin of the Mediterranean mussel (Mytilus galloprovincialis) in food authentication. Food Control 139, 109069.CrossRefGoogle Scholar
Di Beneditto, APM, Pestana, IA, Lima, DF and Franco, RWA (2024) Chemical elements in mussels: Insights into changes in coastal environments due to the COVID-19 pandemic. Marine Pollution Bulletin 206, 116815.10.1016/j.marpolbul.2024.116815CrossRefGoogle ScholarPubMed
Edward, JKP, Jayanthi, M, Malleshappa, H, Jeyasanta, KI, Laju, RL, Patterson, J, Raj, KD, Mathews, G, Marimuthu, AS and Grimsditch, G (2021) COVID-19 lockdown improved the health of coastal environment and enhanced the population of reef-fish. Marine Pollution Bulletin 165, 12124.Google Scholar
Fry, B (2008) Stable Isotope Ecology, 1st edn. New York: Springer-Verlag.Google Scholar
Hill, JM, McQuaid, CD and Kaehler, S (2006) Biogeographic and nearshore-offshore trends in isotope ratios of intertidal mussels and their food sources around the coast of Southern Africa. Marine Ecology Progress Series 318, 6373.10.3354/meps318063CrossRefGoogle Scholar
Jablonski, S, Azevedo, ADF and Moreira, LHA (2006) Fisheries and conflicts in Guanabara Bay, Rio de Janeiro, Brazil. Brazilian Archives of Biology and Technology 49, 7991.10.1590/S1516-89132006000100010CrossRefGoogle Scholar
Kang, X, Zhao, Y, Tan, Z, Ning, J, Zhai, Y and Zheng, G (2022) Evaluation of multivariate data analysis for marine mussels Mytilus edulis authentication in China: Based on stable isotope ratio and compositions of C, N, O and H. Journal of Food Composition and Analysis 111, 104627.10.1016/j.jfca.2022.104627CrossRefGoogle Scholar
Kassambara, A and Mundt, F (2020) Factoextra: Extract and visualize the results of multivariate data analyses. R package version 1.0.7.Google Scholar
Li, L, Ren, W, Dong, S and Feng, J (2018) Investigation of geographic origin, salinity and feed on stable isotope profile of Pacific white shrimp (Litopenaeus vannamei). Aquaculture Research 49, 10291036.CrossRefGoogle Scholar
Lima, DF, Di Beneditto, APM, Pestana, IA and Franco, RWA (2024a) Hazardous elements in the edible portion of Perna perna mussels: Relation with the COVID-19 pandemic period and assessment of the risk to human health. Archives of Environmental Contamination and Toxicology 87, 175186.CrossRefGoogle Scholar
Lima, DF, Gonçalves, TS, Pestana, IA, Di Beneditto, APM and Franco, RWA (2024b) Elemental concentrations in the shells of the mussel Perna perna: Discrimination of origin. Biological Trace Elements Research 202, 12791287.10.1007/s12011-023-03734-9CrossRefGoogle Scholar
Maechler, M, Rousseeuw, P, Struyf, A, Hubert, M and Hornik, K (2019) Cluster: Cluster analysis basics and extensions. R package version 2.1.0.Google Scholar
Marenzi, AWC and Branco, JO (2005) O mexilhão Perna perna (Linnaeus) (Bivalvia, Mytilidae) em cultivo na Armação do Itapocoroy, Santa Catarina, Brasil. Revista Brasileira de Zoologia 22, 394399.10.1590/S0101-81752005000200013CrossRefGoogle Scholar
McClelland, JW, Holl, CM and Montoya, JP (2003) Relating low δ15N values of zooplankton to N2-fixation in the tropical North Atlantic: Insights provided by stable isotope ratios of amino acids. Deep-Sea Research Part A: Oceanographic Research Papers 50, 849861.10.1016/S0967-0637(03)00073-6CrossRefGoogle Scholar
Ortea, I and Gallardo, JM (2015) Investigation of production method, geographical origin and species authentication in commercially relevant shrimps using stable isotope ratio and/or multi-element analyses combined with chemometrics: An exploratory analysis. Food Chemistry 170, 145153.10.1016/j.foodchem.2014.08.049CrossRefGoogle ScholarPubMed
Pierri, BS, Fossari, TD and Magalhães, ARM (2016) O mexilhão Perna perna no Brasil: Nativo ou exótico? Arquivo Brasileiro de Medicina Veterinária E Zootecnia 68, 404414.CrossRefGoogle Scholar
Post, DM, Layman, CA, Arrington, DA, Takimoto, G, Quattrochi, J and Montaña, CG (2007) Getting to the fat of the matter: Models, methods, and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179189.CrossRefGoogle Scholar
Puccinelli, E, McQuaid, CD, Dobretsov, S and Christofoletti, RA (2019) Coastal upwelling affects filter-feeder stable isotope composition across three continents. Marine Environmental Research 147, 1323.10.1016/j.marenvres.2019.03.015CrossRefGoogle ScholarPubMed
Resgalla, JC, Weber, LI and Conceição da, MD (2008) O Mexilhão Perna perna (L.): Biologia, Ecologia E Aplicações, 1st edn. Rio de Janeiro: Interciência.Google Scholar
Rodrigues, SV, Marinho, MM, Jonck, CCC, Gonçalves, ES, Brant, VF, Paranhos, P, Curbelo, MP and Falcão, AP (2014) Phytoplankton community structures in shelf and oceanic waters off southeast Brazil (20°–25°S), as determined by pigment signatures. Deep Sea Research Part I: Oceanographic Research Papers 88, 4762.10.1016/j.dsr.2014.03.006CrossRefGoogle Scholar
Silva, EP, Souza, RC, Lima, TA, Fernandes, FC, Macario, KD, Netto, BM, Alves, EQ, Carvalho, C, Aguilera, O and Duarte, MR (2018) Zooarchaeological evidence that the brown mussel (Perna perna) is a bioinvader of coastal Brazil. The Holocene 28, 17711780.10.1177/0959683618788670CrossRefGoogle Scholar
Veselý, L, Ercoli, F, Ruokonen, TJ, Bláha, M, Duras, J, Haubrock, PJ, Kainz, M, Hämäläinen, H, Buřič, M and Kouba, A (2023) Strong temporal variation of consumer δ13C value in an oligotrophic reservoir is related to water level fluctuation. Scientific Reports 13, 3642.CrossRefGoogle Scholar
Wickham, H, Averick, M, Bryan, J, Chang, W, McGowan, LD, François, R, Grolrmund, G, Hayes, A, Henry, L, Hester, J, Kuhn, M, Pedersen, TL, Miller, E, Bache, SM, Müller, K, Ooms, J, Robinsos, D, Seidel, DP, Spinu, V, Takahashi, K, Vaughan, D, Wilke, C, Woo, K and Yutani, H (2019) Welcome to the Tidyverse. Journal of Open-Source Software 4, 1686.10.21105/joss.01686CrossRefGoogle Scholar
Wilson, JSE, McGill, RAR, Steingrund, P and Trueman, CN (2025) Tracing the geographic origin of Atlantic cod products using stable isotope analysis. Rapid Communications in Mass Spectrometry 39(S1), e9861.10.1002/rcm.9861CrossRefGoogle ScholarPubMed
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