[en] Living benthic foraminifera, known as environmental bio-indicators of both natural and anthropogenic conditions in marine environments, were investigated in the coastal environment of Roscoff Aber Bay (Brittany, France). Eight sampling sites subject to natural variations (freshwater inputs, tides) and/or anthropogenic impacts (pollution, eutrophication) were studied over four seasons in 2021-2022 (November, February, May, August). We sought to understand the spatial distribution of foraminiferal populations within and between sampling sites over the different seasons and to identify sensitive species and those tolerant to anthropogenic impacts. To this end, sedimentary and biogeochemical characteristics of the sediments were examined by measuring grain size, temperature, oxygen, salinity, pH, environmental pigment concentration (chl a and phaeopigments), total organic carbon (TOC), isotopic ratios of carbon (δ13C), nitrogen (δ15N) and sulfide (δ34S), and chl a fluorescence. Considering these parameters as potential driving factors, four environments were distinguished among the sampling sites: open water, terrestrial, oligotrophic and eutrophic. These showed an increasing gradient of organic supply as well as very different microbial activities, highlighted by carbon and sulfide isotopic ratios. Foraminiferal population study revealed the dominant species characterising these main environments. The lowest abundance but highest diversity of foraminifera was found in the harbour site, associated with the dominance of Haynesina germanica, suggesting this species is tolerant to eutrophic environments and anthropogenic impacts. Open water was dominated by Ammonia beccarii and Elphidium crispum, while Quinqueloculina seminula was the most abundant species in the site with the greatest terrestrial influence. Interestingly, the observed organic enrichment of the harbour due to anthropogenic activities (fisheries, waste deposits, etc.) does not seem to significantly affect foraminiferal diversity. Overall, the benthic foraminiferal species in Roscoff Aber Bay appear to be an excellent proxy for marine environmental conditions under various natural and anthropogenic influences.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
This work was supported by the BLUE REVOLUTION project (Biodiversity underestimation in our bLUe planEt: artificial intelligence REVOLUTION in benthic taxonomy) funded by the Interdisciplinary Graduate School for the Blue Planet (ISBlue; ANR-17-EURE-0015) and Ifremer (Institut fran\u00E7ais de recherche pour l\u2019exploitation de la mer). DZ was supported by the project \u201CMassive mEIOfauna DiscoverY of new Species of our oceans and SEAs (MEIODYSSEA) funded by the Sasakawa Peace Foundation. RR was supported by the ISA-IFREMER Collaboration in support of the capacity development of national from developing States, by the Ifremer Marine Mineral Resources project (REMIMA project) and by the French National Research Agency under France 2030 (reference ANR-22-MAFM-0001). This work was supported by the BLUE REVOLUTION project (Biodiversity underestimation in our bLUe planEt: artificial intelligence REVOLUTION in benthic taxonomy) funded by the Interdisciplinary Graduate School for the Blue Planet (ISBlue; ANR-17-EURE-0015) and Ifremer (Institut fran\u00E7ais de recherche pour l\u2019exploitation de la mer). DZ was supported by the project \u201CMassive mEIOfauna DiscoverY of new Species of our oceans and SEAs (MEIODYSSEA) funded by the Sasakawa Peace Foundation. RR was supported by the ISA-IFREMER Collaboration in support of the capacity development of national from developing States, by the Ifremer Marine Mineral Resources project (REMIMA project) and by the French National Research Agency under France 2030 (reference ANR-22-MAFM-0001). The authors thank Sarah Garric and Christophe Six for their help and support with the HPLC analysis of the sediment pigments and the interpretation of the various dendrograms. The authors would also like to thank Valentine Foulquier for her help with the field collection, extraction and technical analysis of the samples. The authors are grateful to the SOMLIT platform for providing temporal data from November 2021 to August 2022 for the ESTACADE point. The authors thank Nicolas Gayet for his help in acquiring SEM images of the foraminifera. The authors would also like to thank Victor Simon for the loan of temperature, pH and salinity probes and Christelle Simon Colin for the loan of the freeze-drying machine. Finally, the authors would like to thank the scientific managers of the ESTACADE stations and the SOMLIT coordinator.
Balsamo M, Semprucci F, Frontalini F, Coccioni R. Meiofauna as a Tool for Marine Ecosystem Biomonitoring. In: Cruzado A, editor. Marine Ecosystems. InTech; 2012. https://doi.org/10.5772/34423
Alve E. Benthic foraminiferal responses to estuarine pollution; a review. The Journal of Foraminiferal Research. 1995; 25: 190–203. https://doi.org/10.2113/gsjfr.25.3.190
Vassallo P, Fabiano M, Vezzulli L, Sandulli R, Marques J, Jorgensen S. Assessing the health of coastal marine ecosystems: A holistic approach based on sediment micro and meio-benthic measures. Ecological Indicators. 2006; 6: 525–542. https://doi.org/10.1016/j.ecolind.2005.07.003
Altenbach A, Sarnthein M. Productivity Record in Benthic. 1989.
Gooday AJ, Levin LA, Linke P, Heeger T. The role of benthic foraminifera in deep-sea food webs and carbon cycling. Deep-sea food chains and the global carbon cycle. 1992; 63–91.
Du Châtelet EA, Gebhardt K, Langer MR. Coastal pollution monitoring: Foraminifera as tracers of environmental perturbation in the port of Boulogne-sur-Mer (Northern France). njgpa. 2011; 262: 91–116. https://doi.org/10.1127/0077-7749/2011/0187
Mojtahid M, Jorissen F, Pearson TH. Comparison of benthic foraminiferal and macrofaunal responses to organic pollution in the Firth of Clyde (Scotland). Marine Pollution Bulletin. 2008; 56: 42–76. https://doi.org/10.1016/j.marpolbul.2007.08.018 PMID: 18054967
Arieli RN, Almogi-Labin A, Abramovich S, Herut B. The effect of thermal pollution on benthic foraminiferal assemblages in the Mediterranean shoreface adjacent to Hadera power plant (Israel). Marine Pollution Bulletin. 2011; 62: 1002–1012. https://doi.org/10.1016/j.marpolbul.2011.02.036 PMID: 21420692
Ernst SR, Morvan J, Geslin E, Le Bihan A, Jorissen FJ. Benthic foraminiferal response to experimentally induced Erika oil pollution. Marine Micropaleontology. 2006; 61: 76–93. https://doi.org/10.1016/j.marmicro.2006.05.005
Alve E, Korsun S, Schönfeld J, Dijkstra N, Golikova E, Hess S, et al. Foram-AMBI: A sensitivity index based on benthic foraminiferal faunas from North-East Atlantic and Arctic fjords, continental shelves and slopes. Marine Micropaleontology. 2016; 122: 1–12.
Schönfeld J, Alve E, Geslin E, Jorissen F, Korsun S, Spezzaferri S. The FOBIMO (FOraminiferal BIo-MOnitoring) initiative—Towards a standardised protocol for soft-bottom benthic foraminiferal monitoring studies. Marine Micropaleontology. 2012; 94–95: 1–13. https://doi.org/10.1016/j.marmicro.2012.06.001
Jorissen F, Nardelli MP, Almogi-Labin A, Barras C, Bergamin L, Bicchi E, et al. Developing Foram-AMBI for biomonitoring in the Mediterranean: Species assignments to ecological categories. Marine Micropaleontology. 2018; 140: 33–45.
Bouchet VM, Frontalini F, Francescangeli F, Sauriau P-G, Geslin E, Martins MVA, et al. Indicative value of benthic foraminifera for biomonitoring: Assignment to ecological groups of sensitivity to total organic carbon of species from European intertidal areas and transitional waters. Marine Pollution Bulletin. 2021; 164: 112071. https://doi.org/10.1016/j.marpolbul.2021.112071 PMID: 33549924
Jorissen FJ, Fouet MPA, Singer D, Howa H. The Marine Influence Index (MII): A Tool to Assess Estuarine Intertidal Mudflat Environments for the Purpose of Foraminiferal Biomonitoring. Water. 2022; 14: 676. https://doi.org/10.3390/w14040676
O’Brien PA, Polovodova Asteman I, Bouchet VM. Benthic foraminiferal indices and environmental quality assessment of transitional waters: a review of current challenges and future research perspectives. Water. 2021; 13: 1898.
Elliott M, Quintino V. The Estuarine Quality Paradox, Environmental Homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Marine Pollution Bulletin. 2007; 54: 640–645. https://doi.org/10.1016/j.marpolbul.2007.02.003 PMID: 17418874
Dauvin J-C, Vallet C, Mouny P, Zouhiri S. Main characteristics of the boundary layer macrofauna in the English Channel. In: Liebezeit G, Dittmann S, Kröncke I, editors. Life at Interfaces and Under Extreme Conditions. Dordrecht: Springer Netherlands; 2000. pp. 139–156. https://doi.org/10.1007/978-94-011-4148-2_13
Hubas C, Davoult D, Cariou T, Artigas L. Factors controlling benthic metabolism during low tide along a granulometric gradient in an intertidal bay (Roscoff Aber Bay, France). Mar Ecol Prog Ser. 2006; 316: 53–68. https://doi.org/10.3354/meps316053
De Bettignies F, Dauby P, Lepoint G, Riera P, Bocher E, Bohner O, et al. Temporal succession of a macrofaunal community associated with kelp fragment accumulations in an in situ experiment. Mar Ecol Prog Ser. 2020; 656: 109–121. https://doi.org/10.3354/meps13391
Chauris L. L’anse de l’Aber en Roscoff. Un ancien marais littoral envahi par la mer. Penn ar Bed (Brest). 1988; 18: 1–11.
Hourdez S, Boidin-Wichlacz C, Jollivet D, Massol F, Rayol MC, Bruno R, et al. Investigation of Capitella spp. symbionts in the context of varying anthropic pressures: First occurrence of a transient advantageous epibiosis with the giant bacteria Thiomargarita sp. to survive seasonal increases of sulfides in sediments. Science of the Total Environment. 2021; 798: 149149. https://doi.org/10.1016/j.scitotenv.2021.149149 PMID: 34375231
Guilloux L, Rigaut-Jalabert F, Jouenne F, Ristori S, Viprey M, Not F, et al. An annotated checklist of Marine Phytoplankton taxa at the SOMLIT-Astan time series off Roscoff (Western English Channel, France): data collected from 2000 to 2010. Cah Biol Mar. 2013; 54: 247–256.
Caracciolo M, Rigaut-Jalabert F, Romac S, Mahé F, Forsans S, Gac J, et al. Seasonal dynamics of marine protist communities in tidally mixed coastal waters. Molecular Ecology. 2022; 31: 3761–3783. https://doi.org/10.1111/mec.16539 PMID: 35593305
Rombouts I, Simon N, Aubert A, Cariou T, Feunteun E, Guérin L, et al. Changes in marine phytoplankton diversity: Assessment under the Marine Strategy Framework Directive. Ecological Indicators. 2019; 102: 265–277.
Stagnol D, Renaud M, Davoult D. Effects of commercial harvesting of intertidal macroalgae on ecosystem biodiversity and functioning. Estuarine, Coastal and Shelf Science. 2013; 130: 99–110.
Migné A, Bordeyne F, Davoult D. Long-term survey of intertidal rocky shore macrobenthic community metabolism and structure after primary succession. 2023.
Riera P, Escaravage C, Leroux C. Trophic ecology of the rocky shore community associated with the Ascophyllum nodosum zone (Roscoff, France): a δ13C vs δ15N investigation. Estuarine, Coastal and Shelf Science. 2009; 81: 143–148.
Boidin-Wichlacz C, Andersen AC, Jouy N, Hourdez S, Tasiemski A. A single coelomic cell type is involved in both immune and respiratory functions of the coastal bioindicator annelid: Capitella C-Channel1 from the English Channel. Developmental & Comparative Immunology. 2024; 153: 105132. https://doi.org/10.1016/j.dci.2024.105132 PMID: 38181832
Leclerc J, Riera P, Noël LM, Leroux C, Andersen AC. Trophic ecology of P omatoschistus microps within an intertidal bay (R oscoff, F rance), investigated through gut content and stable isotope analyses. Marine Ecology. 2014; 35: 261–270.
Riera P. Trophic plasticity of the gastropod Hydrobia ulvae within an intertidal bay (Roscoff, France): A stable isotope evidence. Journal of Sea Research. 2010; 63: 78–83.
Rullier F. Etude bionomique de l’Aber de Roscoff. Université de Paris, Station biologique de Roscoff; 1959.
Heip C, Magda V, Guido V. The ecology of marine nematodes. Oceanography and Marine Biology: an annual review. 1985; 23: 399–489.
Mason WT, Yevich PP. The Use of Phloxine B and Rose Bengal Stains to Facilitate Sorting Benthic Samples. Transactions of the American Microscopical Society. 1967; 86: 221–223. https://doi.org/10.2307/3224697
Liénart C, Savoye N, David V, Ramond P, Rodriguez Tress P, Hanquiez V, et al. Dynamics of particulate organic matter composition in coastal systems: Forcing of spatio-temporal variability at multi-systems scale. Progress in Oceanography. 2018; 162: 271–289. https://doi.org/10.1016/j.pocean.2018.02. 026
Dessandier P-A, Bonnin J, Kim J-H, Bichon S, Grémare A, Deflandre B, et al. Lateral and vertical distributions of living benthic foraminifera off the Douro River (western Iberian margin): Impact of the organic matter quality. Marine Micropaleontology. 2015; 120: 31–45. https://doi.org/10.1016/j.marmicro.2015.09.002
Zapata M, Rodríguez F, Garrido J. Separation of chlorophylls and carotenoids from marine phytoplankton:a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar Ecol Prog Ser. 2000; 195: 29–45. https://doi.org/10.3354/meps195029
Coplen TB. Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Communications in Mass Spectrometry. 2011; 25: 2538–2560. https://doi.org/10.1002/rcm.5129 PMID: 21910288
Shannon C, Weaver W. The Mathematical Theory of Communication. Urbana: Illinois Press. 1964.
Buzas MA, Gibson TG. Species diversity: benthonic foraminifera in western North Atlantic. Science. 1969; 163: 72–75. https://doi.org/10.1126/science.163.3862.72 PMID: 17780177
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nature methods. 2012; 9: 676–682. https://doi.org/10.1038/nmeth.2019 PMID: 22743772
Ostu N. A threshold selection method from gray-level histograms. IEEE Trans SMC. 1979; 9: 62.
Legendre P, Legendre L. Numerical ecology. Elsevier; 2012.
Goldstein ST, Richardson EA. Fine structure of the foraminifer Haynesina germanica (Ehrenberg) and its sequestered chloroplasts. Marine Micropaleontology. 2018; 138: 63–71. https://doi.org/10.1016/j.marmicro.2017.10.010
Christa G. Kleptoplasty. Current Biology. 2023; 33: R465–R467. https://doi.org/10.1016/j.cub.2023.03. 036 PMID: 37279674
Langezaal A, Van Bergen P, Van der Zwaan G. The recovery of benthic foraminifera and bacteria after disturbance: experimental evidence. Journal of Experimental Marine Biology and Ecology. 2004; 312: 137–170.
Ohga T, Kitazato H. Seasonal changes in bathyal foraminiferal populations in response to the flux of organic matter (Sagami Bay, Japan). Terra Nova. 1997; 9: 33–37.
Murray JW, Alve E. Major aspects of foraminiferal variability (standing crop and biomass) on a monthly scale in an intertidal zone. The Journal of Foraminiferal Research. 2000; 30: 177–191.
Debenay J-P, Geslin E, Eichler BB, Duleba W, Sylvestre F, Eichler P. Foraminiferal assemblages in a hypersaline lagoon, Araruama (RJ) Brazil. The Journal of Foraminiferal Research. 2001; 31: 133–151.
Phipps M, Jorissen F, Pusceddu A, Bianchelli S, De Stigter H. Live benthic foraminiferal faunas along a bathymetrical transect (282–4987 m) on the Portuguese margin (NE Atlantic). Journal of Foraminiferal Research. 2012; 42: 66–81. https://doi.org/10.2113/gsjfr.42.1.66
Dessandier P, Bonnin J, Kim J, Bichon S, Deflandre B, Grémare A, et al. Impact of organic matter source and quality on living benthic foraminiferal distribution on a river-dominated continental margin: A study of the Portuguese margin. JGR Biogeosciences. 2016; 121: 1689–1714. https://doi.org/10.1002/ 2015JG003231
Mendes I, Rosa F, Dias J, Schönfeld J, Ferreira Ó, Pinheiro J. Inner shelf paleoenvironmental evolution as a function of land–ocean interactions in the vicinity of the Guadiana River, SW Iberia. Quaternary International. 2010; 221: 58–67.
Armynot du Châtelet E, Debenay J-P, Soulard R. Foraminiferal proxies for pollution monitoring in moderately polluted harbors. Environmental Pollution. 2004; 127: 27–40. https://doi.org/10.1016/s0269-7491(03)00256-2 PMID: 14553992
Martins VA, Frontalini F, Tramonte KM, Figueira RCL, Miranda P, Sequeira C, et al. Assessment of the health quality of Ria de Aveiro (Portugal): Heavy metals and benthic foraminifera. Marine Pollution Bulletin. 2013; 70: 18–33. https://doi.org/10.1016/j.marpolbul.2013.02.003 PMID: 23582314
Fouet MPA, Singer D, Coynel A, Héliot S, Howa H, Lalande J, et al. Foraminiferal Distribution in Two Estuarine Intertidal Mudflats of the French Atlantic Coast: Testing the Marine Influence Index. Water. 2022; 14: 645. https://doi.org/10.3390/w14040645
Alve E, Murray JW. Marginal marine environments of the Skagerrak and Kattegat: a baseline study of living (stained) benthic foraminiferal ecology. Palaeogeography, Palaeoclimatology, Palaeoecology. 1999; 146: 171–193. https://doi.org/10.1016/S0031-0182(98)00131-X
Ouisse V, Riera P, Migné A, Leroux C, Davoult D. Freshwater seepages and ephemeral macroalgae proliferation in an intertidal bay: I Effect on benthic community structure and food web. Estuarine, Coastal and Shelf Science. 2011; 91: 272–281. https://doi.org/10.1016/j.ecss.2010.10.034
Migné A, Ouisse V, Hubas C, Davoult D. Freshwater seepages and ephemeral macroalgae proliferation in an intertidal bay: II. Effect on benthic biomass and metabolism. Estuarine, Coastal and Shelf Science. 2011; 92: 161–168. https://doi.org/10.1016/j.ecss.2010.12.023
Wilkinson M, Telfer T, Grundy S. Geographical variation in the distributions of macroalgae in estuaries. Netherlands Journal of Aquatic Ecology. 1995; 29: 359–368. https://doi.org/10.1007/BF02084235
Murray JW. Ecology and applications of benthic foraminifera. Cambridge university press; 2006.
Sadanandan H, Dharmalingam SN, Mouttoucomarassamy S. Benthic foraminifera as bio-indicator of marine pollution in the southwestern Bay of Bengal, India. Environ Sci Pollut Res. 2023 [cited 27 Jun 2024]. https://doi.org/10.1007/s11356-023-29367-y PMID: 37642911
Fontanier C, Mamo B, Dubosq N, Lamarque B, Rigaud S, Schmidt S, et al. Seasonal variability of living benthic foraminifera from the West-Gironde mud patch (Bay of Biscay, NE Atlantic): Three contrasted periods under the stereomicroscope. Continental Shelf Research. 2023; 268: 105117. https://doi.org/10.1016/j.csr.2023.105117
Kitazato H, Nakatsuka T, Shimanaga M, Kanda J, Soh W, Kato Y, et al. Long-term monitoring of the sedimentary processes in the central part of Sagami Bay, Japan: rationale, logistics and overview of results. Progress in Oceanography. 2003; 57: 3–16. https://doi.org/10.1016/S0079-6611(03)00047-8
Nomaki H. Behavior and response of deep-sea benthic foraminifera to freshly supplied organic matter: a laboratory feeding experiment in microcosm environments. The Journal of Foraminiferal Research. 2005; 35: 103–113. https://doi.org/10.2113/35.2.103
Vidović J, Dolenec M, Dolenec T, Karamarko V, Žvab Rožič P. Benthic foraminifera assemblages as elemental pollution bioindicator in marine sediments around fish farm (Vrgada Island, Central Adriatic, Croatia). Marine Pollution Bulletin. 2014; 83: 198–213. https://doi.org/10.1016/j.marpolbul.2014.03.051 PMID: 24768261
Alve E. Benthic foraminifera in sediment cores reflecting heavy metal pollution in Sorfjord, western Norway. The Journal of Foraminiferal Research. 1991; 21: 1–19. https://doi.org/10.2113/gsjfr.21.1.1
Frontalini F, Buosi C, Da Pelo S, Coccioni R, Cherchi A, Bucci C. Benthic foraminifera as bio-indicators of trace element pollution in the heavily contaminated Santa Gilla lagoon (Cagliari, Italy). Marine Pollution Bulletin. 2009; 58: 858–877. https://doi.org/10.1016/j.marpolbul.2009.01.015 PMID: 19268977
Dauvin J-C. Paradox of estuarine quality: Benthic indicators and indices, consensus or debate for the future. Marine Pollution Bulletin. 2007; 55: 271–281. https://doi.org/10.1016/j.marpolbul.2006.08.017 PMID: 17007892
