Articles | Volume 44, issue 2
https://doi.org/10.5194/jm-44-237-2025
© Author(s) 2025. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/jm-44-237-2025
© Author(s) 2025. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
29 Aug 2025
Research article |
| 29 Aug 2025
| 29 Aug 2025
Towards a more integrative approach for environmental decision-making in Brazilian transitional waters: improving biomonitoring surveys with a benthic foraminiferal biotic index
Vincent M. P. Bouchet
CORRESPONDING AUTHOR
Univ. Lille, CNRS, IRD, Univ. Littoral Côte d'Opale, UMR 8187, LOG, Laboratoire d'Océanologie et de Géosciences, Station Marine de Wimereux, 59000 Lille, France
Silvia Helena de Mello e Sousa
Instituto Oceanográfico, Universidade de São Paulo (IOUSP), Pça. do Oceanográfico, 191, Butantã, São Paulo, 05508 120, Brazil
Carla Bonetti
Coordenadoria de Oceanografia, Universidade Federal de Santa Catarina (UFSC), Florianópolis, Santa Catarina, Brazil
Leticia Burone
Cincytema, Sección Oceanología, Instituto de Ecología y Ciencias Ambientales, Facultad de Ciencias, Universidad de la República, Iguá 4225, Montevideo 11400, Uruguay
Pierre Belart
Departamento de Ciências Naturais, Universidade Federal do Estado do Rio de Janeiro – UNIRIO, Rio de Janeiro, Rio de Janeiro, Brazil
Wania Duleba
Universidade de São Paulo (USP), Escola de Artes, Ciências e Humanidades (EACH), Rua Arlindo Béttio, 1000 – Ermelino Matarazzo, São Paulo – SP, 03828-000, Brazil
Fabio Francescangeli
Department of Geosciences, University of Fribourg, Chemin Du Musée 6, 1700 Fribourg/Freiburg, Switzerland
Fabrizio Frontalini
Department of Pure and Applied Sciences (DiSPeA), University of Urbino “Carlo Bo”, Campus Scientifico Enrico Mattei, Località Crocicchia, 61029 Urbino, Italy
Lazaro Laut
Departamento de Ciências Naturais, Universidade Federal do Estado do Rio de Janeiro – UNIRIO, Rio de Janeiro, Rio de Janeiro, Brazil
Débora S. Raposo
German Federation for Biological Data – GFBio e.V., Mary-Somerville-Strasse 2–4, 28359 Bremen, Germany
André R. Rodrigues
Universidade Federal do Espírito Santo, UFES, Vitória, ES, Brazil
Sibelle Trevisan Disaró
Universidade Federal do Paraná, Museu de Ciências Naturais, Laboratório de Foraminíferos e Micropaleontologia Ambiental, Av. Cel. Francisco H. Dos Santos, 100 – Jardim Américas, CEP 81530-000, Curitiba, PR, Brazil
Daniel Vicente Pupo
Universidade Federal do Paraná, Museu de Ciências Naturais, Laboratório de Foraminíferos e Micropaleontologia Ambiental, Av. Cel. Francisco H. Dos Santos, 100 – Jardim Américas, CEP 81530-000, Curitiba, PR, Brazil
Fabrício Leandro Damasceno
Faculdade de Geologia, Departamento de Paleontologia e Estratigrafia, Universidade do Estado do Rio de Janeiro (UERJ), R. São Francisco Xavier,524 – Lab 4037F – Maracanã, Rio de Janeiro 20550-900, Brazil
Jean-Charles Pavard
CORRESPONDING AUTHOR
Univ. Lille, CNRS, IRD, Univ. Littoral Côte d'Opale, UMR 8187, LOG, Laboratoire d'Océanologie et de Géosciences, Station Marine de Wimereux, 59000 Lille, France
Department of Marine Science, University of Gothenburg, Gothenburg, Sweden
Maria Virgínia Alves Martins
Faculdade de Geologia, Departamento de Paleontologia e Estratigrafia, Universidade do Estado do Rio de Janeiro (UERJ), R. São Francisco Xavier,524 – Lab 4037F – Maracanã, Rio de Janeiro 20550-900, Brazil
Department of Geosciences, Aveiro University, GeoBioTec, Campus de Santiago, 3810-197 Aveiro, Portugal
Related authors
Dewi Langlet, Florian Mermillod-Blondin, Noémie Deldicq, Arthur Bauville, Gwendoline Duong, Lara Konecny, Mylène Hugoni, Lionel Denis, and Vincent M. P. Bouchet
Biogeosciences, 20, 4875–4891, https://doi.org/10.5194/bg-20-4875-2023, https://doi.org/10.5194/bg-20-4875-2023, 2023
Short summary
Short summary
Benthic foraminifera are single-cell marine organisms which can move in the sediment column. They were previously reported to horizontally and vertically transport sediment particles, yet the impact of their motion on the dissolved fluxes remains unknown. Using microprofiling, we show here that foraminiferal burrow formation increases the oxygen penetration depth in the sediment, leading to a change in the structure of the prokaryotic community.
Julien Richirt, Magali Schweizer, Aurélia Mouret, Sophie Quinchard, Salha A. Saad, Vincent M. P. Bouchet, Christopher M. Wade, and Frans J. Jorissen
J. Micropalaeontol., 40, 61–74, https://doi.org/10.5194/jm-40-61-2021, https://doi.org/10.5194/jm-40-61-2021, 2021
Short summary
Short summary
The study presents (1) a validation of a method which was previously published allowing us to recognize different Ammonia phylotypes (T1, T2 and T6) based only on their morphology and (2) a refined biogeographical distribution presented here supporting the putatively invasive character of phylotype T6. Results suggest that phylotype T6 is currently spreading out and supplanting autochthonous phylotypes T1 and T2 along the coastlines of the British Isles and northern France.
João M. F. Ramos, Jairo F. Savian, Daniel R. Franco, Milene F. Figueiredo, Rodolfo Coccioni, and Fabrizio Frontalini
EGUsphere, https://doi.org/10.5194/egusphere-2025-3832, https://doi.org/10.5194/egusphere-2025-3832, 2025
This preprint is open for discussion and under review for Climate of the Past (CP).
Short summary
Short summary
During the Aptian–Albian interval of the Cretaceous, Earth's climate changed significantly due to volcanism, atmospheric shifts, and reorganised ocean circulation. These changes influenced marine sediments, especially reddish Cretaceous oceanic red beds (CORBs), which reflect intervals of deep-ocean oxygenation. This study analysed sediment cores from ODP Site 1049 (North Atlantic) to determine when CORBs formed and whether similar patterns occurred in other basins, such as the Tethys.
Irina Polovodova Asteman, Emilie Jaffré, Agata Olejnik, Maria Holzmann, Mary McGann, Kjell Nordberg, Jean-Charles Pavard, Delia Rösel, and Magali Schweizer
J. Micropalaeontol., 44, 119–143, https://doi.org/10.5194/jm-44-119-2025, https://doi.org/10.5194/jm-44-119-2025, 2025
Short summary
Short summary
Small boat harbours are suggested to cause pollution and alien species introductions. Here we analysed surface sediments in Hinsholmskilen harbour (Sweden) for benthic foraminifera and potentially toxic elements. Molecular and morphological analyses of foraminifera show the presence of two alien species, Trochammina hadai and Ammonia confertitesta, whilst pollution is mostly low for Cd, Co, Ni, and Pb. In contrast, As, Zn, Cu, Hg, and Cr have high levels due to the use of these elements in boat paints.
Dewi Langlet, Florian Mermillod-Blondin, Noémie Deldicq, Arthur Bauville, Gwendoline Duong, Lara Konecny, Mylène Hugoni, Lionel Denis, and Vincent M. P. Bouchet
Biogeosciences, 20, 4875–4891, https://doi.org/10.5194/bg-20-4875-2023, https://doi.org/10.5194/bg-20-4875-2023, 2023
Short summary
Short summary
Benthic foraminifera are single-cell marine organisms which can move in the sediment column. They were previously reported to horizontally and vertically transport sediment particles, yet the impact of their motion on the dissolved fluxes remains unknown. Using microprofiling, we show here that foraminiferal burrow formation increases the oxygen penetration depth in the sediment, leading to a change in the structure of the prokaryotic community.
Michel Michaelovitch de Mahiques, Roberto Violante, Paula Franco-Fraguas, Leticia Burone, Cesar Barbedo Rocha, Leonardo Ortega, Rosangela Felicio dos Santos, Bianca Sung Mi Kim, Rubens Cesar Lopes Figueira, and Marcia Caruso Bícego
Ocean Sci., 17, 1213–1229, https://doi.org/10.5194/os-17-1213-2021, https://doi.org/10.5194/os-17-1213-2021, 2021
Short summary
Short summary
In this work we used a concept called geochemical fingerprinting, with isotopes of neodymium and lead as tools to recognize the main sources and the physical processes responsible for the transport and deposition of sediments on a large area of the South Atlantic margin. Distinct sources, such as Antarctica, the Andean Cordillera, the Río de la Plata basin, and old rocks from the Brazilian shield, are identified.
Julien Richirt, Magali Schweizer, Aurélia Mouret, Sophie Quinchard, Salha A. Saad, Vincent M. P. Bouchet, Christopher M. Wade, and Frans J. Jorissen
J. Micropalaeontol., 40, 61–74, https://doi.org/10.5194/jm-40-61-2021, https://doi.org/10.5194/jm-40-61-2021, 2021
Short summary
Short summary
The study presents (1) a validation of a method which was previously published allowing us to recognize different Ammonia phylotypes (T1, T2 and T6) based only on their morphology and (2) a refined biogeographical distribution presented here supporting the putatively invasive character of phylotype T6. Results suggest that phylotype T6 is currently spreading out and supplanting autochthonous phylotypes T1 and T2 along the coastlines of the British Isles and northern France.
Cited articles
Aguado-Giménez, F., Marin, A., Montoya, S., Marin-Guirao, L., Piedecausa, A., and Garcia-Garcia, B.: Comparison between some procedures for monitoring offshore cage cultures in western Mediterranean Sea: sampling methods and impact indicators in soft substrata, Aquaculture, 271, 357–370, 2007.
Alve, E.: Benthic foraminiferal responses to estuarine pollution: a review, J. Foramin. Res., 25, 190–203, 1995.
Alve, E. and Murray, J. W.: Marginal marine environments of the Skagerrak and Kattegat: a baseline study of living (stained) benthic foraminiferal ecology, Palaeogeogr. Palaeocl., 146, 171–193, 1999.
Alve, E., Lepland, A., Magnusson, J., and Backer-Owe, K.: Monitoring strategies for re-establishment of ecological reference conditions: Possibilities and limitations, Mar. Pollut. Bull., 59, 297–310, https://doi.org/10.1016/j.marpolbul.2009.08.011, 2009.
Alve, E., Korsun, S., Schönfeld, J., Dijkstra, N., Golikova, E., Hess, C., Husum, K., and Panieri, G.: Foram-AMBI: A sensitivity index based on benthic foraminiferal faunas from North-East Atlantic and Arctic fjords, continental shelves and slopes, Mar. Micropaleontol., 122, 1–12, https://doi.org/10.1016/j.marmicro.2015.11.001, 2016.
Alve, E., Hess, S., Bouchet, V. M. P., Dolven, J. K., and Rygg, B.: Intercalibration of benthic foraminiferal and macrofaunal biotic indices: an example from the Norwegian Skagerrak coast (NE North Sea), Ecol. Indic., 96, 107–115, 2019.
Angel, D. L., Verghese, S., Lee, J. J., Saleh, A. M., Zuber, D., Lindell, D., and Symons, A.: Impact of a net cage fish farm on the distribution of benthic foraminifera in the northern Gulf of Eilat (Aqaba, Red Sea), J. Foramin. Res., 30, 54–65, 2000.
Armynot du Châtelet, E., Debenay, J.-P., and Soulard, R.: Foraminiferal proxies for pollution monitoring in moderately polluted harbors, Environ. Pollut., 127, 27–40, https://doi.org/10.1016/s0269-7491(03)00256-2, 2004.
Bakke, T., Kalqvist, T., Ruus, A., Breedveld, G. D., and Hylland, K.: Development of sediment quality criteria in Norway, J. Soil. Sediment., 10, 172–178, 2010.
Baptista Neto, J. A., Smith, B. J., and McAlister, J. J.: Heavy metal concentration in surface sediments in a nearshore environment, Jurujuba Sound, Southeast Brazil, Environ. Pollut., 109, 1–9, 2000.
Baptista Neto, J. A., Gingele, F. X., Leipe, T., and Brehme, I.: Spatial distribution of heavy metals in surficial sediments from Guanabara Bay: Rio de Janeiro, Brazil, Environ. Geol., 49, 1051–1063, https://doi.org/10.1007/s00254-005-0149-1, 2006.
Baptista Neto, J. A., Barreto, C. F., Silva, M. A. M., Smith, B. J., Mcallister, J. J., and Vilela, C. G.: Nearshore sedimentation as a record of land use change and erosion: Jurujuba Sound, Niterói, SE Brazil, Ocean Coast Manage., 77, 31–39, https://doi.org/10.1016/j.ocecoaman.2012.04.022, 2013.
Barillé-Boyer, A.-L., Barillé, L., Masse, H., Razet, D., and Heral, M.: Correction for particulate organic matter as estimated by loss on ignition in estuarine ecosystems, Estuar. Coast. Shelf S., 58, 147–153, 2003.
Barras, C., Jorissen, F. J., Labrune, C., Andral, B., and Boissery, P.: Live benthic foraminiferal faunas from the French mediterranean coast: towards a new biotic index of environmental quality, Ecol. Indic., 36, 719–743, 2014.
Belart, P., Clemente, I., Raposo, D., Habib, R., Volino, E., Villar, A., Alves Martins, M., Fontana, L., Lorini, M., Panigai, G., Frontalini, F., Figueiredo, M., Vasconcelos, S., and Laut, L.: Living and dead Foraminifera as bioindicators in Saquarema Lagoon System, Brazil, Lat. Am. J. Aquat. Res., 46, 1055–1072, https://doi.org/10.3856/vol46-issue5-fulltext-18, 2018.
Bigot, L., Grémare, A., Amouroux, J. M., Frouin, P., Maire, O., and Gaertner, J. C.: Assessment of the ecological quality status of soft-bottoms in Reunion Island (tropical Southwest Indian Ocean) using AZTI marine biotic indices, Mar. Pollut. Bull., 56, 704–722, 2008.
Birks, H. J. B., Line, J. M., Juggins, S., Stevenson, A. C., and Ter Braak, C. J. F.: Diatoms and pH reconstruction, Phil. T. R. Soc. Lon. B, 327, 263–278, 1990.
Blanchet, H., Lavesque, N., Ruellet, T., Dauvin, J.-C., Sauriau, P. G., Desroy, N., Desclaux, C., Leconte, M., Bachelet, G., Janson, A.-L., Bessineton, C., Duhamel, S., Jourde, J., Mayot, S., Simon, S., and de Montaudouin, X.: Use of biotic indices in semi-enclosed coastal ecosystems and transitional waters habitats – implications for the implementation of the European water framework directive, Ecol. Indic., 8, 360–372, 2008.
Borja, A. and Muxika, I.: Guidelines for the use of AMBI (AZTI's Marine Biotic Index) in the assessment of the benthic ecological quality, Mar. Pollut. Bull., 50, 787–789, 2005.
Borja, A., Franco, J., and Perez, V.: A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments, Mar. Pollut. Bull., 40, 1100–1114, 2000.
Bouchet, V. M. P.: Dynamique et réponse fonctionnelle des foraminifères et de la macrofaune benthiques en zone ostréicole dans les pertuis charentais, Thèse de doctorat, University of Angers, 404 pp., http://www.theses.fr/2007ANGE0045 (last access: 14 August 2025), 2007.
Bouchet, V. M. P. and Sauriau, P.-G.: Influence of oyster culture practices and environmental conditions on the ecological quality of intertidal mudflats in the Pertuis Charentais (SW France): a multi-index approach, Mar. Pollut. Bull., 56, 1898–1912, 2008.
Bouchet, V. M. P., Goberville, E., and Frontalini, F.: Benthic foraminifera to assess the Ecological Quality Status of Italian transitional waters, Ecol. Indic., 84, 130–139, 2018a.
Bouchet, V. M. P., Telford, R. J., Rygg, B., Oug, E., and Alve, E.: Can benthic foraminifera serve as proxies for changes in benthic macrofaunal community structure? Implications for the definition of reference conditions, Mar. Environ. Res., 137, 24–36, 2018b.
Bouchet, V. M. P., Alve, E., Rygg, B., and Telford, R. J.: Benthic foraminifera provide a promising tool for ecological quality assessment of marine waters, Ecol. Indic., 23, 66–75, 2012.
Bouchet, V. M. P., Deldicq, N., Baux, N., Dauvin, J.-C., Pezy, J.-P., Seuront, L., and Méar, Y.: Benthic foraminifera to assess ecological quality statuses: the case of salmon fish farming, Ecol. Indic., 117, 106607, https://doi.org/10.1016/j.ecolind.2020.106607, 2020.
Bouchet, V. M. P., Frontalini, F., Francescangeli, F., Sauriau, P.-G., Geslin, E., Martins, M. V. A., Almogi-Labin, A., Avnaim-Katav, S., Di Bella, L., Cearreta, A., Coccioni, R., Costelloe, A., Dimiza, M. D., Ferraro, L., Haynert, K., Martinez-Colon, M., Melis, R., Schweizer, M., Triantaphyllou, M., Tsujimoto, A., Wilson, B., and Armynot du Châtelet, E.: Indicative value of benthic foraminifera for biomonitoring: assignment to ecological groups of sensibility to total organic carbon of species from European intertidal areas and transitional waters, Mar. Pollut. Bull., 164, 112071, https://doi.org/10.1016/j.marpolbul.2021.112071, 2021.
Bouchet, V. M. P., Sousa, S. H. M., Bonetti, C., Burone, L., Belart, P., Duleba, W., Francescangeli, F., Frontalini, F., Laut, L., Raposo, D., Rodrigues, A., Disaró, S. T., Pupo, D., Damasceno, F., Pavard, J.-C., Martins, M. V. A.: Living foraminifera relative abundances and total organic carbon in Brazilian transitional waters, Mendeley Data [data set], https://doi.org/10.17632/nw4xd5ymgd.1, 2025.
Brauko, K. M., Muniz, P., de Castro Martins, C., and da Cunha Lana, P.: Assessing the suitability of five benthic indices for environmental health assessment in a large subtropical South American estuary, Ecol. Indic., 64, 258–265, 2016.
Brazil: Lei no 6.938, de 31 de agosto de 1981. Dispõe sobre a Política Nacional do Meio Ambiente, seus fins e mecanismos de formulação e aplicação, e dá outras providências. Diário Oficial da União, Brasília, DF: Imprensa Oficial, http://www.planalto.gov.br/ccivil_03/leis/l6938.htm (last access: 14 August 2025), 1981.
Brazil: Conselho Nacional de Meio Ambiente. Resolução CON- AMA no 357, de 17 de março de 2005. Dispõe sobre a classificação dos corpos de água e diretrizes ambientais para o seu enquadramento, bem como estabelece as condições e padrões de lançamento de efluentes, e dá outras providências. Diário Oficial da União, Brasília, DF: Imprensa Oficial, https://conama.mma.gov.br/index.php?id=15876 (last access: 14 August 2025), 2005.
Burone, L. and Pires-Vanin, A. M. S.: Foraminiferal assemblages in Ubatuba Bay, south-eastern Brazilian coast, Sci. Mar., 70, 203–217, 2006.
Burone, L., Venturini, N., Sprechmann, P., Valente, P., and Muniz, P.: Foraminiferal responses to polluted sediments in the Montevideo coastal zone, Uruguay, Mar. Pollut. Bull., 52, 61–73, https://doi.org/10.1016/j.marpolbul.2005.08.007, 2006.
Calvo-Marcilese, L. and Langer, M. R.: Breaching biogeographic barriers: the invasion of Haynesina germanica (Foraminifera, Protista) in the Bahía Blanca estuary, Argentina, Biol. Invasions, 12, 3299–3306, 2010.
Checon, H. H., Corte, G. N., Muniz, P., Brauko, K. M., Di Domenico, M., Bícego, M. C., Siegle, E., Figueira, R. C. L., and Amaral, A. C. Z.: Unraveling the performance of the benthic index AMBI in a subtropical bay: The effects of data transformations and exclusion of low-reliability sites, Mar. Pollut. Bull., 126, 438–448, 2018.
Cotovicz Jr., L. C., Knoppers, B. A., Brandini, N., Costa Santos, S. J., and Abril, G.: A strong CO2 sink enhanced by eutrophication in a tropical coastal embayment (Guanabara Bay, Rio de Janeiro, Brazil), Biogeosciences, 12, 6125–6146, https://doi.org/10.5194/bg-12-6125-2015, 2015.
Damasceno, F. L., Martins, M. V. A., Frontalini, F., Pawlowski, J., Cermakova, K., Angeles, I. B., Costa Santos, L. G., Filho, J. G. M., Francescangeli, F., Senez-Mello, T. M., Castelo, W. F. L., Rebouças, R. C., Duleba, W., Sousa, S. H. M., Laut, L., and Antonioli, L.: Assessment of the ecological quality status of the Sepetiba Bay (SE Brazil): When metabarcoding meets morphology on foraminifera, Mar. Environ. Res., 195, 106340, https://doi.org/10.1016/j.marenvres.2024.106340, 2024.
Darling, K. F. and Wade, C. M.: The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes, Mar. Micropaleontol., 67, 216–238, 2008.
Dauvin, J.-C. and Ruellet, T.: Polychaete/amphipod ratio revisited, Mar. Pollut. Bull., 55, 215–224, 2007.
Dauvin, J.-C., Bellan, G., and Bellan-Santini, D.: Benthic indicators: From subjectivity to objectivity – Where is the line?, Mar. Pollut. Bull., 60, 947–953, 2010.
Dauvin, J. C., Alizier, S., Rolet, C., Bakalem, A., Bellan, G., Gesteira, J. G., Grimes, S., De-La-Ossa-Carretero, J., and Del-Pilar-Ruso, Y.: Response of different benthic indices to diverse human pressures, Ecol. Indic., 12, 143–153, 2012.
Debenay, J.-P., Eichler, B. B., Duleba, W., Bonetti, C., and Eichler-Coelho, P.: Water stratification in coastal lagoons: its influence on foraminiferal assemblages in two Brazilian lagoons., Mar. Micropaleontol., 35, 65–89, 1998.
Diaz, R. and Rosenberg, R.: Spreading dead zones and consequences for marine ecosystems, Science, 321, 926–929, 2008.
Dimiza, M. D., Triantaphyllou, M. V., Koukousioura, O., Hallock, P., Simboura, N., Karageorgis, A. P., and Papathanassiou, E.: The Foram Stress Index: A new tool for environmental assessment of soft-bottom environments using benthic foraminifera. A case study from the Saronikos Gulf, Greece, Eastern Mediterranean, Ecol. Indic., 60, 611–621, 2016.
Dubois, A., Barras, C., Pavard, J.-C., Donnay, A., Beatrix, M., and Bouchet, V. M. P.: Distribution patterns of benthic foraminifera in fish farming areas (Corsica, France): implications for the implementation of biotic indices in biomonitoring studies, Water, 13, 2821, https://doi.org/10.3390/w13202821, 2021.
Duleba, W., Teodoro, A. C., Debenay, J.-P., Alves Martins, M. V., Gubitoso, S., Pregnolato, L. A., Lerena, L. M., Prada, S. M., and Bevilacqua, J. E.: Environmental impact of the largest petroleum terminal in SE Brazil: a multiproxy analysis based on sediment geochemistry and living benthic foraminifera, PLoS One, 13, e0191446, https://doi.org/10.1371/journal.pone.0191446, 2018.
Eichler, P., McGann, M., Rodrigues, A. R., Mendonça, A., Amorim, A., Bonetti, C., Cordeiro de Farias, C., Mello e Sousa, S. H., Vital, H., and Praxedes Gome, M.: The occurrence of the invasive foraminifera Trochammina hadai Uchio in Flamengo Inlet, Ubatuba, São Paulo State, Brazil, Micropalaeontology, 64, 391–402, 2018.
Eichler, P. P. B., Eichler, B. B., de Miranda, L. B., Pereira, E. R. M., Kfouri, P. B. P., Pimenta, F. M., Bérgamo, A. L., and Vilela, C. G.: Benthic foraminiferal response to variations in temperature, salinity, dissolved oxygen and organic carbon. the Guanabara Bay, Rio de Janeiro, Brazil, Anuario do Instituto de Geociencias, 26, 36–51, 2003.
European Communities: Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy, Off. J. Eur. Communities, 43, 75, https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:02000L0060-20140101 (last access: 14 August 2025), 2000.
Filippos, L. S., Duleba, W., Hohenegger, J., Pregnolato, L. A., Bouchet, V. M. P., and Martins, M. V. A.: Domestic Sewage Outfall Severely Altered Environmental Conditions, Foraminiferal Communities, and Ecological Quality Statuses in Front of the Nearshore Beach of Cigarras (SE Brazil), Water, 15, 405, https://doi.org/10.3390/w15030405, 2023.
Fouet, M. P. A., Singer, D., Coynel, A., Héliot, S., Howa, H., Lalande, J., Mouret, A., Schweizer, M., Tcherkez, G., and Jorissen, F. J.: Foraminiferal Distribution in Two Estuarine Intertidal Mudflats of the French Atlantic Coast: Testing the Marine Influence Index, Water, 14, 645, https://doi.org/10.3390/w14040645, 2022.
Francescangeli, F., Quijada, M., Armynot du Châtelet, E., Frontalini, F., Trentesaux, A., Billon, G., and Bouchet, V. M. P.: Multidisciplinary study to monitor consequences of pollution on intertidal benthic ecosystems (Hauts de France, English Channel, France): comparison with natural areas, Mar. Environ. Res., 160, 105034, https://doi.org/10.1016/j.marenvres.2020.105034, 2020.
Grémare, A., Labrune, C., Vanden Berghe, E., Amouroux, J. M., Bachelet, G., Zettler, M. L., Vanaverbeke, J., Fleischer, D., Bigot, L., Maire, O., Deflandre, B., Craeymeersch, J., Degraer, S., Dounas, C., Duineveld, G., Heip, C., Herrmann, M., Hummel, H., Karakassis, I., Kedra, M., Kendall, M., Kingston, P., Laudien, J., Occhipinti-Ambrogi, A., Rachor, E., Sardá, R., Speybroeck, J., Van Hoey, G., Vincx, M., Whomersley, P., Willems, W., Wlodarska-Kowalczuk, M., and Zenetos, A.: Comparison of the performances of two biotic indices based on the MacroBen database, Mar. Ecol. Prog. Ser., 382, 297–311, 2009.
Hayward, B. W., Le Coze, F., Vachard, D., and Gross, O.: World Foraminifera Database, WORMS [data set], https://doi.org/10.14284/305, 2020b.
Hayward, B. W., Le Coze, F., Vandepitte, L., and Vanhoorne, B.: Foraminifera in the World Register of Marine Species (WoRMS) taxonomic database, J. Foramin. Res., 50, 291–300, https://doi.org/10.2113/gsjfr.50.3.291, 2020a.
Heinzl, H. and Leisch, F.: irr: Various Coefficients of Interrater Reliability and Agreement, R package version 0.84.1 [code], https://CRAN.R-project.org/package=irr (last access: 14 August 2025), 2022.
Hyams-Kazphan, O., Almogi-Labin, A., Benjamini, C., and Herut, B.: Natural oligotrophy vs. pollution-induced eutrophy on the SE Mediterranean shallow shelf (Israel): environmental parameters and benthic foraminifera, Mar. Pollut. Bull., 58, 1888–1902, 2009.
IBGE: Rio de Janeiro, in: Anuario Estatístico Do Brasil, vol. 74, https://biblioteca.ibge.gov.br/visualizacao/periodicos/20/aeb_2014.pdf (last access: 13 February 2022), 2014.
Jesus, S. d. S. M., Frontalini, F., Bouchet, V. M. P., Yamashita, C., Sartoretto, J. R., Figueira, R. C. L., and Sousa, S. H. M.: Reconstruction of paleo-ecological quality statuses in an anthropogenised estuary using benthic foraminifera: the Santos estuary (São Paulo State, SE Brazil), Mar. Environ. Res., 162, 105121, https://doi.org/10.1016/j.marenvres.2020.105121, 2020.
Jorissen, F. J., Nardelli, M. P., Almogi-Labin, A., Barras, C., Bergamin, L., Bicchi, E., El Kateb, A., Ferraro, L., McGann, M., Morigi, C., Romano, E., Sabbatini, A., Schweizer, M., and Spezzaferri, S.: Developing Foram-AMBI for biomonitoring in the Mediterranean: Species assignments to ecological categories, Mar. Micropaleontol., 140, 33–45, 2018.
Jorissen, F., Fouet, M., Armynot du Châtelet, É., Barras, C., Bouchet, V., Daviray, M., Francescangeli, F., Geslin, E., Le Moigne, D., Licari, L., Mojtahid, M., Nardelli, M.-P., Pavard, J.-C., Rolland, A., Schweizer, M., and Singer, D.: Foraminifères estuariens de la façade atlantique française : Guide de détermination, Zenodo, https://doi.org/10.5281/zenodo.14197875, 2023.
Keeley, N. B., Macleod, C. K., and Forrest, B. M.: Combining best professional judgement and quantile regression splines to improve characterisation of macrofaunal responses to enrichment, Ecol. Indic., 12, 154–166, https://doi.org/10.1016/j.ecolind.2011.03.022, 2012.
Klootwijk, A. T. and Alve, E.: Does the analysed size fraction of benthic foraminifera influence the ecological quality status and the interpretation of environmental conditions? Indications from two northern Norwegian fjords, Ecol. Indic., 135, 108423, https://doi.org//10.1016/j.ecolind.2021.108423, 2022.
Kütter, V. T., Almeida Moreira, V., Tavares Kütter, M., Vieira Silva-Filho, E., Duarte Marques, E., Garnier, J., and Dausacker Bidone, E.: Metal bioavailability and distribution in the fish community in a tropical estuary, Sepetiba Bay, Rio De Janeiro, Brazil, Geochimica Brasiliensis, 351, 17–38, https://doi.org/10.21715/GB2358-2812.2021351017, 2021.
Labrune, C., Amouroux, J.-M., Sarda, R., Dutrieux, E., Thorin, S., Rosenberg, R., and Grémare, A.: Characterization of the ecological quality of the coastal Gulf of Lions (NW Mediterrenean). A comparative approach based on three biotic indices, Mar. Pollut. Bull., 52, 34–47, 2006.
Landis, J. R. and Koch, G. G.: The measurement of observer agreement for categorical data, Biometrics, 33, 159–174, 1977.
Laut, L., Martins, M. V. A., Frontalini, F., Ballalai, J. M., Belart, P., Habib, R., Fontana, L. F., Clemente, I. M. M. M., Lorini, M. L., Filho, J. G. M., Laut, V. M., and Figueiredo, M. S. L.: Assessment of the trophic state of a hypersaline-carbonatic environment: Vermelha Lagoon (Brazil), PLoS ONE, 12, e0184819, https://doi.org/10.1371/journal.pone.0184819, 2017.
Laut, L., Matta, G., Camara, G., Belart, P., Clemente, I., Ballalai, J., Volino, E., and Couto, E. C. G.: Living and dead foraminifera assemblages as environmental indicators in the Almada River Estuary, Ilhéus, northeastern Brazil, J. S. Am. Earth Sci., 105, 102883, https://doi.org/10.1016/j.jsames.2020.102883, 2021.
Laut, L., Belart, P., Carelli, T., Martins, M. V. A., and Laut, V.: Insights into the Ecology of Foraminifera from the Most Hypersaline Lagoon in Brazil: Vermelha Lagoon, Estuar. Coast., 45, 2632–2649, https://doi.org/10.1007/s12237-022-01073-x, 2022.
Laut, L. L. M., Martins, V., da Silva, F. S., Crapez, M. A. C., Fontana, L. F., Carvalhal-Gomes, S. B. V., and Souza, R. C. C. L.: Foraminifera, thecamoebians, and bacterial activity in polluted intertropical and subtropical Brazilian estuarine systems, J. Coastal Res., 32, 56–69, 2016.
Lavesque, N., Blanchet, H., and de Montaudouin, X.: Development of a multimetric approach to assess perturbation of benthic macrofauna in Zostera noltii beds, J. Exp. Mar. Biol. Ecol., 368, 101–112, 2009.
Leong, L. S. and Tanner, P. A.: Comparison of methods for determination of organic carbon in marine sediment, Mar. Pollut. Bull., 38, 875–879, 1999.
Luczak, C., Janquin, M.-A., and Kupka, A.: Simple standard procedure for the routine determination of organic matter in marine sediment, Hydrobiologia, 345, 87–94, 1997.
Martins, M. V. A., Zaaboub, N., Aleya, L., Frontalini, F., Pereira, E., Miranda, P., Mane, M., Rocha, F., Laut, L., and El Bour, M.: Environmental Quality Assessment of Bizerte Lagoon (Tunisia) Using Living Foraminifera Assemblages and a Multiproxy Approach, Plos One, 10, e0137250, https://doi.org/10.1371/journal.pone.0137250, 2015.
Martins, M. V. A., Hohenegger, J., Martiìnez-Coloìn, M., Frontalini, F., Bergamaschi, S., Laut, L., Belart, P., Mahiques, M., Pereira, E., Rodrigues, R., Terroso, D., Miranda, P., Geraldes, M. C., Villena, H. H., Reisi, T., Socorro, O. A. A., Sousa, S. H. M., Yamashita, C., and Rocha, F.: Ecological quality status of the NE sector of the Guanabara Bay (Brazil): A case of living benthic foraminiferal resilience, Mar. Pollut. Bull., 158, 111449, https://doi.org/10.1016/j.marpolbul.2020.111449, 2020.
McLusky, D. S. and Elliott, M.: Transitional waters: a new approach, semantics or just muddying the waters?, Estuar. Coast. Shelf S., 71, 359–363, 2007.
Melis, R., Celio, M., Bouchet, V. M. P., Varagona, G., Bazzaro, M., Crosera, M., and Pugliese, N.: Seasonal Response of benthic foraminifera to anthropogenic pressure in two stations of the Gulf of Trieste (northern Adriatic Sea): the marine protected area of Miramare versus the Servola water sewage outfall, Mediterr. Mar. Sci., 20, 120–141, 2019.
Muniz, P., Venturini, N., Pires-Vanin, A. M. S., Tommasi, L. R., and Borja, A.: Testing the applicability of a Marine Biotic Index (AMBI) to assessing the ecological quality of soft-bottom benthic communities, in the South America Atlantic region, Mar. Pollut. Bull., 50, 624–637, 2005.
Muniz, P., Venturini, N., Hutton, M., Kandratavicius, N., Pita, A., Brugnoli, E., Burone, L., and García-Rodríguez, F.: Ecosystem health of Montevideo coastal zone: A multi approach using some different benthic indicators to improve a ten-year-ago assessment, J. Sea Res., 65, 38–50, 2011.
Nunes, M., Martins, M. V. A., Frontalini, F., Bouchet, V. M. P., Francescangeli, F., Hohenegger, J., Figueira, R., Senez-Mello, T. M., Castelo, W. F. L., Damasceno, F. L., Laut, L., Duleba, W., Sousa, S. H. M., Antonioli, L., and Geraldes, M. C.: Inferring the ecological quality status based on living benthic foraminiferal indices in transitional areas of the Guanabara bay (SE Brazil), Environ. Pollut., 320, 121003, https://doi.org/10.1016/j.envpol.2023.121003, 2023.
O'Brien, P., Polovodova Asteman, I., and Bouchet, V. M. P.: Benthic foraminiferal indices and environmental quality assessment of transitional waters: a review of current challenges and future research perspectives, Water, 13, 1898, https://doi.org/10.3390/w13141898, 2021.
O'Malley, B. J., Schwing, P. T., Martínez-Colón, M., Spezzaferri, S., Machain-Castillo, M. L., Larson, R. A., Brooks, G. R., Ruiz-Fernandez, A. C., and Hollander, D. J.: Development of a benthic foraminifera based marine biotic index (Foram-AMBI) for the Gulf of Mexico: A decision support tool, Ecol. Indic., 120, 106916, https://doi.org/10.1016/j.ecolind.2020.106916, 2021.
Parent, B., Barras, C., Bicchi, E., Charrieau, L. M., Choquel, C., Bénéteau, É., Maillet, G. M., and Jorissen, F. J.: Comparison of Four Foraminiferal Biotic Indices Assessing the Environmental Quality of Coastal Mediterranean Soft Bottoms, Water, 13, 3193, https://doi.org/10.3390/w13223193, 2021.
Pavard, J.-C., Richirt, J., Seuront, L., Blanchet, H., Fouet, M. P. A., Humbert, S., Gouillieux, B., Duong, G., and Bouchet, V. M. P.: The great shift: the non-indigenous species Ammonia confertitesta (Foraminifera, Rhizaria) outcompete indigenous Ammonia species in the Gironde estuary (France), Estuar. Coast. Shelf S., 289, 108378, https://doi.org/10.1016/j.ecss.2023.108378, 2023.
Pusceddu, A., Dell'Anno, A., Danovaro, R., Manini, E., Sara, G., and Fabiano, M.: Enzymatically hydrolyzable protein and carbohydrate sedimentary pools as indicators of the trophic state of detritus sink systems: a case study in a Mediterranean coastal lagoon, Estuaries, 26, 641–650, 2003.
Raposo, D., Clemente, I., Figueiredo, M., Vilar, A., Lorini, M. L., Frontalini, F., Martins, M. V. A., Belart, P., Fontana, L., Habib, R., and Laut, L.: Benthic foraminiferal and organic matter compounds as proxies of environmental quality in a tropical coastal lagoon: The Itaipu lagoon (Brazil), Mar. Pollut. Bull., 129, 114–125, https://doi.org/10.1016/j.marpolbul.2018.02.018, 2018.
Raposo, D., Frontalini, F., Clemente, I., Couto, E. d. C. G., Veriìssimo, F., and Laut, L.: Benthic Foraminiferal Response to Trace Elements in a Tropical Mesotidal Brazilian Estuary, Estuar. Coast., 45, 2610–2631, 2022.
Ribeiro, A. P., Figueiredo, A. M. G., Santos, J. O. d., Ferreira, P. A. d. L., Graudenz, G. S., Ruiz, M. S., Mahiques, M. M. d., Figueira, R. C. L., and Wasserman, J. C. F. A.: Effects of contamination with toxic metals on the environmental quality of Sepetiba Bay SE Brazil: The case of Ingá Company, Management of Environmental Quality, 26, 538–551, https://doi.org/10.1108/MEQ-06-2013-0074, 2015.
Rodrigues, A. R., Díaz, T. L., and Pellizari, V. H.: Living Foraminifera in a Brazilian Subtropical Coastal Environment (Flamengo Inlet, Ubatuba, São Paulo State–Brazil), in: Approaches to Study Living Foraminifera, edited by: Kitazato, H. and Bernhard, J. M., Environmental Science and Engineering, Springer, Tokyo, 195–227, https://doi.org/10.1007/978-4-431-54388-6_11, 2014.
Rovai, A. S., Twilley, R. R., Worthington, T. A., and Riul, P.: Brazilian mangroves: blue carbon hotspots of national and global relevance to natural climate solutions, Frontiers in Forests and Global Change, 4, 787533, https://doi.org/10.3389/ffgc.2021.787533, 2022.
Rudorff, N. M., Bonetti, C., and Bonetti Filho, J.: Suspended shellfish culture impacts on the benthic layer: a case study in Brazilian subtropical waters, Braz. J. Oceanogr., 60, 221–234, 2012.
Schintu, M., Marrucci, A., Marras, B., Galgani, F., Buosi, C., Ibba, A., and Cherchi, A.: Heavy metal accumulation in surface sediments at the port of Cagliari (Sardinia, western Mediterranean): environmental assessment using sequential extractions and benthic foraminifera, Mar. Pollut. Bull., 11, 45–56, 2016.
Schönfeld, J., Alve, E., Geslin, E., Jorissen, F., Korsun, S., Spezzaferri, S., Abramovich, S., Almogi-Labin, A., Armynot du Chatelet, E., Barras, C., Bergamin, L., Bicchi, E., Bouchet, V. M. P., Cearreta, A., Di Bella, L., Dijkstra, N., Disaró, S. T., Ferraro, L., Frontalini, F., Gennari, G., Golikova, E., Haynert, K., Hess, S., Husum, K., Martins, V., McGann, M., Oron, S., Romano, E., Mello Sousa, S., and Tsujimoto, A.: The FOBIMO (FOraminiferal BIo-MOnitoring) initiative – Towards a standardised protocol for soft-bottom benthic foraminiferal monitoring studies, Mar. Micropaleontol., 94–95, 1–13, 2012.
Simboura, N. and Zenetos, A.: Benthic indicators to use in ecological quality classification of Mediterranean soft bottom marine ecosystems, including a new biotic index, Mediterr. Mar. Sci., 3, 77–111, 2002.
Simpson, G. L. and Oksanen, J.: analogue: Analogue and weighted averaging methods for palaeoecology, R-Project.org [code], https://doi.org/10.32614/CRAN.package.analogue, 2021.
Sokal, R. R. and Rohlf, F. J.: Biometry, W. H. Freeman, ISBN-13 978-0-7167-2411-7, 1995.
Sousa, S., Yamashita, C., Semensatto, D. J., Santarosa, A., Iwai, I., Omachi, C., Disaró, S. T., Martins, M. V., Barbosa, C., Bonetti, C., Vilela, C., Laut, L., Turra, T., Alve, E., Armynot du Châtelet, E., V.M.P., B., Burone, L., Carmo, A., Figueira, R., Figueiredo, M., Frontalini, F., Geslin, E., Lamparelli, C., Licari, L., Lorini, M., Lourenço, R., Mahiques, M., Martin, T., Mello, R., Millo, C., Moreira, D., Pawlowski, J., Rodrigues, A., and Siegle, E.: Opportunities and challenges in incorporating benthic foraminifera in marine and coastal environmental biomonitoring of soft sediments: from science to regulation and practice, Journal of Sedimentary Environments, 5, 257–265, 2020.
Souza, A. M., Rocha, D. S., Guerra, J. V., Cunha, B. A., Martins, M. V. A., and Geraldes, M. C.: Metal concentrations in marine sediments of the Rio de Janeiro Coast Brazil: A proposal to establish new acceptable levels of contamination, Mar. Pollut. Bull., 165, 112113, doi.org/10.1016/j.marpolbul.2021.112113, 2021a.
Souza, F. M., Gilbert, E. R., Brauko, K. M., Lorenzi, L., Machado, E., and Camargo, M. G.: Macrobenthic community responses to multiple environmental stressors in a subtropical estuary, PeerJ, 9, e12427, https://doi.org/10.7717/peerj.12427, 2021b.
Stal, L. J.: Cyanobacterial mats and stromatolites, in: Ecology of Cyanobacteria II: Their Diversity in Space and Time, edited by: Whitton, A. B., Springer, Dordrecht, 65–125, https://doi.org/10.1007/978-94-007-3855-3_4, 2012.
Ter Braak, C. J. F.: Unimodal Models to Relate Species to Environment, University of Wageningen, https://edepot.wur.nl/201452 (last access: 14 August 2025), 1987.
Valença, A. P. and Santos, P. J.: Macrobenthic community for assessment of estuarine health in tropical areas (Northeast, Brazil): review of macrofauna classification in ecological groups and application of AZTI Marine Biotic Index, Mar. Pollut. Bull., 64, 1809–1820, 2012.
Veileder: Klassifisering av miljøtilstand i vann, https://www.vannportalen.no/veiledere/klassifiseringsveileder/ (last access: 14 August 2025), 2018.
Viaroli, P., Bartoli, M., Giordani, G., Magni, P., and Welsh, D. T.: Biogeochemical indicators as tools for assessing sediment quality/vulnerability in transitional aquatic ecosystems, Aquat. Conserv., 14, 19–29, https://doi.org/10.1002/aqc.647, 2004.
Vilela, C. G., Batista, D. S., Baptista-Neto, J. A., Crapez, M., and McAllister, J. J.: Benthic foraminifera distribution in high polluted sediments from Niterói Harbor (Guanabara Bay), Rio de Janeiro, Brazil, An. Acad. Bras. Cienc., 76, 161–171, 2004.
Zettler, M. L., Proffitt, C. E., Darr, A., Degraer, S., Devriese, L., Greathead, C., Kotta, J., Magni, P., Martin, G., Reiss, H., Speybroeck, J., Tagliapietra, D., Van Hoey, G., and Ysebaert, T.: On the myths of indicator species: issues and further consideration in the use of static concepts for ecological applications, Plos One, 8, e78219, https://doi.org/10.1371/journal.pone.0078219, 2013.
Short summary
This study evaluates benthic foraminifera as indicators of environmental health in Brazil’s coastal waters and tests Foram-AMBI using a regional species list and criteria for ecological quality status (EcoQS). A total of 95 species were classified into five groups based on their response to total organic carbon. Data from Sepetiba Bay and Guanabara Bay validated these groups, showing that Foram-AMBI accurately reflects ecological conditions. The study highlights the importance of regional species lists for biomonitoring.
This study evaluates benthic foraminifera as indicators of environmental health in Brazil’s...
