Foraminiferal community response to seasonal anoxia in Lake Grevelingen (the Netherlands) Julien Richirt, Bettina Riedel, Aurélia Mouret, Magali Schweizer, Dewi Langlet, Dorina Seitaj, Filip Meysman, Caroline Slomp, Frans Jorissen To cite this version: Julien Richirt, Bettina Riedel, Aurélia Mouret, Magali Schweizer, Dewi Langlet, et al.. Foraminiferal community response to seasonal anoxia in Lake Grevelingen (the Netherlands). Biogeosciences, Eu- ropean Geosciences Union, 2020, 17 (6), pp.1415-1435. 10.5194/bg-17-1415-2020. hal-02514878 HAL Id: hal-02514878 https://hal.archives-ouvertes.fr/hal-02514878 Submitted on 9 Oct 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution - NoDerivatives| 4.0 International License Biogeosciences, 17, 1415–1435, 2020 https://doi.org/10.5194/bg-17-1415-2020 © Author(s) 2020. This work is distributed under the Creative Commons Attribution 4.0 License. Foraminiferal community response to seasonal anoxia in Lake Grevelingen (the Netherlands) Julien Richirt1, Bettina Riedel1,2, Aurélia Mouret1, Magali Schweizer1, Dewi Langlet1,3, Dorina Seitaj4, Filip J. R. Meysman5,6, Caroline P. Slomp7, and Frans J. Jorissen1 1UMR 6112 LPG-BIAF Recent and Fossil Bio-Indicators, University of Angers, 2 Boulevard Lavoisier, 49045 Angers, France 2First Zoological Department, Vienna Museum of Natural History, Burgring 7, 1010 Vienna, Austria 3Univ. Lille, CNRS, Univ. Littoral Côte d’Opale, UMR8187, LOG, Laboratoire d’Océanologie et de Géosciences, 62930 Wimereux, France 4Department of Ecosystem Studies, Royal Netherlands Institute for Sea Research (NIOZ), Yerseke, the Netherlands 5Department of Biology, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium 6Department of Biotechnology, Delft University of Technology, 2629 HZ Delft, the Netherlands 7Department of Earth Sciences (Geochemistry), Faculty of Geosciences, Utrecht University, Princetonlaan 8a, 3584 CB Utrecht, the Netherlands Correspondence: Julien Richirt ([email protected]) Received: 23 September 2019 – Discussion started: 1 October 2019 Revised: 6 February 2020 – Accepted: 10 February 2020 – Published: 20 March 2020 Abstract. Over the last decades, hypoxia in marine coastal surface sediment resulted in an almost complete disappear- environments has become more and more widespread, pro- ance of the foraminiferal community. Conversely, at the shal- longed and intense. Hypoxic events have large consequences lower site (23 m), where the duration of anoxia and free H2S for the functioning of benthic ecosystems. In severe cases, was shorter (1 month or less), a dense foraminiferal com- they may lead to complete anoxia and the presence of toxic munity was found throughout the year except for a short pe- sulfides in the sediment and bottom-water, thereby strongly riod after the stressful event. Interestingly, at both sites, the affecting biological compartments of benthic marine ecosys- foraminiferal community showed a delayed response to the tems. Within these ecosystems, benthic foraminifera show a onset of anoxia and free H2S, suggesting that the combina- high diversity of ecological responses, with a wide range of tion of anoxia and free H2S does not lead to increased mortal- adaptive life strategies. Some species are particularly resis- ity, but rather to strongly decreased reproduction rates. At the tant to hypoxia–anoxia, and consequently it is interesting to deepest site, where highly stressful conditions prevailed for 1 study the whole foraminiferal community as well as species- to 2 months, the recovery time of the community takes about specific responses to such events. Here we investigated the half a year. In Lake Grevelingen, Elphidium selseyense and temporal dynamics of living benthic foraminiferal commu- Elphidium magellanicum are much less affected by anoxia nities (recognised by CellTracker™ Green) at two sites in and free H2S than Ammonia sp. T6. We hypothesise that this the saltwater Lake Grevelingen in the Netherlands. These is not due to a higher tolerance for H2S, but rather related to sites are subject to seasonal anoxia with different durations the seasonal availability of food sources, which could have and are characterised by the presence of free sulfide (H2S) been less suitable for Ammonia sp. T6 than for the elphidi- in the uppermost part of the sediment. Our results indicate ids. that foraminiferal communities are impacted by the pres- ence of H2S in their habitat, with a stronger response in the case of longer exposure times. At the deepest site (34 m), in summer 2012, 1 to 2 months of anoxia and free H2S in the Published by Copernicus Publications on behalf of the European Geosciences Union. 1416 J. Richirt et al.: Foraminiferal community response to seasonal anoxia 1 Introduction last decades, so that a large amount of environmental data are available (e.g. Wetsteijn, 2011; Donders et al., 2012). Hypoxia affects numerous marine environments, from the The annual net primary production in the Den Osse Basin open ocean to coastal areas. Over the last decades, a general (i.e. 225 g C m−2 yr−1; Hagens et al., 2015) is comparable to decline in oxygen concentration was observed in marine wa- other estuarine systems in Europe (Cloern et al., 2014). How- ters (Stramma et al., 2012), with an extent varying between ever, there is almost no nutrient input from external sources; the concerned regions. In coastal areas, oxygen concentra- thus primary production is largely based on autochthonous tions have been estimated to decrease 10 times faster than recycling (> 90 %; Hagens et al., 2015), both in the water col- in the open ocean, with indications of a recent acceleration, umn and in the sediment, with a very strong pelagic–benthic expressed by increasing frequency, intensity, extent and du- coupling (de Vries and Hopstaken, 1984). The benthic envi- ration of hypoxic events (Diaz and Rosenberg, 2008; Gilbert ronment is characterised by the presence of two antagonis- et al., 2010). This is due to the combination of (1) global tic groups of bacteria, with contrasting seasonal population warming, which is strengthening seasonal stratification of the dynamics (i.e. cable bacteria in winter–spring and Beggia- water column and decreasing oxygen solubility, and (2) eu- toaceae in autumn–winter), which have a profound impact trophication resulting from increased anthropogenic nutri- on all biogeochemical cycles in the sediment column (Seitaj ent and/or organic matter input, which is enhancing benthic et al., 2015; Sulu-Gambari et al., 2016a, b). The combination oxygen consumption in response to increased primary pro- of hypoxia–anoxia with sulfidic conditions, which is rather duction (Diaz and Rosenberg, 2008). Bottom-water hypoxia unusual in coastal systems without external nutrient input, has serious consequences for the functioning of all benthic and the activity of antagonistic bacterial communities makes ecosystem compartments (see Riedel et al., 2016, for a re- Lake Grevelingen a very peculiar environment. In the Den view). Benthic faunas are strongly impacted by these events Osse Basin, seasonal anoxia coupled with the presence of (Diaz and Rosenberg, 1995), even though the meiofauna, H2S at or very close to the sediment–water interface occurs especially foraminifera, appears to be less sensitive to low in summer (i.e. between July–September). However, euxinia dissolved oxygen (DO) concentrations than the macrofauna (i.e. diffusion of free H2S in the water column) does not oc- (e.g. Josefson and Widbom, 1988). Many foraminiferal taxa cur, because of cable bacterial activity (Seitaj et al., 2015). are able to withstand seasonal hypoxia–anoxia (see Koho et Although the tolerance of foraminifera towards low DO al., 2012, for a review), and consequently they can play a ma- contents and long-term anoxia (from weeks to 10 months) jor role in carbon cycling in ecosystems affected by seasonal has been well documented for many species from different low-oxygen concentrations (Woulds et al., 2007). Anoxia types of environments in laboratory culture (e.g. Moodley is often accompanied by free sulfide (H2S) in pore and/or and Hess, 1992; Alve and Bernhard, 1995; Bernhard and bottom waters (e.g. Jørgensen, 1982; Seitaj et al., 2015), Alve, 1996; Moodley et al., 1997; Duijnstee et al., 2003, which is considered very harmful for the benthic macrofauna 2005; Geslin et al., 2004, 2014; Ernst et al., 2005; Pucci et (Wang and Chapman, 1999). Neutral molecular H2S can dif- al., 2009; Koho et al., 2011) as well as in field studies (e.g. fuse through cellular membranes and inhibits the function- Piña-Ochoa et al., 2010b; Langlet et al., 2013, 2014), their ing of cytochrome c oxidase (a mitochondrial enzyme in- tolerance of free H2S is still debated. In the vast majority of volved in ATP production), finally inhibiting aerobic respi- previous studies, no decrease in the total abundances of living ration (Nicholls and Kim, 1982; Khan et al., 1990; Dorman foraminifera (i.e. strongly increased mortality) was observed