BG Biogeosciences BG Biogeosciences 1726-4189 Copernicus Publications Göttingen, Germany 10.5194/bg-11-1775-2014 Foraminiferal species responses to in situ, experimentally induced anoxia in the Adriatic Sea Langlet D. https://orcid.org/0000-0002-2201-0897 1 Baal C. 2 Geslin E. 1 Metzger E. 1 Zuschin M. 2 Riedel B. 3 Risgaard-Petersen N. 4 Stachowitsch M. 3 Jorissen F. J. 1 Université d'Angers, UMR6112 CNRS LPG-BIAF – Bio-Indicateurs Actuels et Fossiles, 2 Boulevard Lavoisier, 49045 Angers Cedex, France University of Vienna, Department of Palaeontology, Althanstrasse 14, 1090 Vienna, Austria University of Vienna, Department of Limnology and Oceanography, Althanstrasse 14, 1090 Vienna, Austria Aarhus University, Center for Geomicrobiology, Department of Bioscience, 8000 Aarhus C, Denmark 04 04 2014 11 7 1775 1797 Copyright: © 2014 D. Langlet et al. 2014 This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/ This article is available from https://bg.copernicus.org/articles/11/1775/2014/bg-11-1775-2014.html The full text article is available as a PDF file from https://bg.copernicus.org/articles/11/1775/2014/bg-11-1775-2014.pdf

Anoxia was successfully induced in four benthic chambers installed at 24 m depth in the northern Adriatic Sea for periods varying from 9 days to 10 months. During the 10-month period, species richness significantly decreased. Although no significant change in Shannon diversity and evenness was observed, the composition of the foraminiferal assemblages changed with time. This change is due to interspecific differences in tolerance to anoxia. <i>Reophax nanus</i>, <i>Textularia agglutinans</i> and <i>Quinqueloculina stelligera</i> all showed a significant decrease with time, strongly suggesting they are sensitive to anoxia. Conversely, <i>Eggerella scabra</i>, <i>Bulimina marginata</i>, <i>Lagenammina atlantica</i>, <i>Hopkinsina pacifica</i> and <i>Bolivina pseudoplicata</i> appeared to be resistant to the experimental conditions. <i>Quinqueloculina seminula</i> was apparently sensitive to anoxia but showed a clear standing stock increase during the first month of the experiment, which we interpret as an opportunistic response to increasing organic matter availability due to the degradation of the dead macrofaunal organisms. None of the anoxia-sensitive species is able to accumulate intracellular nitrates. Nitrate accumulation could be shown for some tested specimens of the dominant anoxia-tolerant species <i>E. scabra</i> and <i>B. marginata</i>. However, tests on the denitrification capacity of these taxa yielded negative results, suggesting that their resistance to long-term anoxia is not due to their ability to denitrify.

 References Alve, E. and Bernhard, J.: Vertical migratory response of benthic foraminifera to controlled oxygen concentrations in an experimental mesocosm, Mar. Ecol.-Prog. Ser., 116, 137–151, <a href="http://dx.doi.org/10.3354/meps116137">https://doi.org/10.3354/meps116137</a>, 1995. Alve, E. and Goldstein, S. T.: Dispersal, survival and delayed growth of benthic foraminiferal propagules, J. Sea Res., 63, 36–51, 2010. Andersen, K., Kjær, T., and Revsbech, N. P.: An oxygen insensitive microsensor for nitrous oxide, Sens. Actuators B Chem., 81, 42–48, <a href="http://dx.doi.org/10.1016/S0925-4005(01)00924-8">https://doi.org/10.1016/S0925-4005(01)00924-8</a>, 2001. Armynot du Châtelet, E., Bout-Roumazeilles, V., Coccioni, R., Frontalini, F., Guillot, F., Kaminski, M. A., Recourt, P., Riboulleau, A., Trentesaux, A., Tribovillard, N., and Ventalon, S.: Environmental control on shell structure and composition of agglutinated foraminifera along a proximal–distal transect in the Marmara Sea, Mar. Geol., 335, 114–128, <a href="http://dx.doi.org/10.1016/j.margeo.2012.10.013">https://doi.org/10.1016/j.margeo.2012.10.013</a>, 2013. Barmawidjaja, D. M., Jorissen, F. J., Puskaric, S., and van der Zwaan, G. J.: Microhabitat selection by benthic Foraminifera in the northern Adriatic Sea, J. Foraminifer. Res., 22, 297–317, <a href="http://dx.doi.org/10.2113/gsjfr.22.4.297">https://doi.org/10.2113/gsjfr.22.4.297</a>, 1992. Barmawidjaja, D., Van der Zwaan, G., Jorissen, F., and Puskaric, S.: 150 years of eutrophication in the northern Adriatic Sea: evidence from a benthic foraminiferal record, Mar. Geol., 122, 367–384, 1995. 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, <a href="http://dx.doi.org/10.1016/j.ecolind.2013.09.028">https://doi.org/10.1016/j.ecolind.2013.09.028</a>, 2014. Bernhard, J. M.: Postmortem Vital Staining in Benthic Foraminifera; Duration and Importance in Population and Distributional Studies, J. Foraminifer. Res., 18, 143–146, <a href="http://dx.doi.org/10.2113/gsjfr.18.2.143">https://doi.org/10.2113/gsjfr.18.2.143</a>, 1988. Bernhard, J. M.: Distinguishing Live from Dead Foraminifera: Methods Review and Proper Applications, Micropaleontology, 46, 38–46, 2000. Bernhard, J. M. and Reimers, C. E.: Benthic foraminiferal population fluctuations related to anoxia: Santa Barbara Basin, Biogeochemistry, 15, 127–149, <a href="http://dx.doi.org/10.1007/BF00003221">https://doi.org/10.1007/BF00003221</a>, 1991. Bernhard, J. M. and Sen Gupta, B. K.: Foraminifera of oxygen-depleted environments, in Modern Foraminifera, 201–216, Springer Netherlands, available at: <a href="http://link.springer.com/chapter/10.1007/0-306-48104-9_12">http://link.springer.com/chapter/10.1007/0-306-48104-9_12</a> (last access: 12 March 2013), 1999. Bernhard, J. M., Ostermann, D. R., Williams, D. S., and Blanks, J. K.: Comparison of two methods to identify live benthic foraminifera: A test between Rose Bengal and CellTracker Green with implications for stable isotope paleoreconstructions, Paleoceanography, 21, PA4210, <a href="http://dx.doi.org/10.1029/2006PA001290">https://doi.org/10.1029/2006PA001290</a>, 2006. Bernhard, J. M., Casciotti, K. L., McIlvin, M. R., Beaudoin, D. J., Visscher, P. T., and Edgcomb, V. P.: Potential importance of physiologically diverse benthic foraminifera in sedimentary nitrate storage and respiration, J. Geophys. Res., 117, G03002, <a href="http://dx.doi.org/10.1029/2012JG001949">https://doi.org/10.1029/2012JG001949</a>, 2012. Blackwelder, P., Hood, T., Alvarez-Zarikian, C., Nelsen, T. A., and McKee, B.: Benthic foraminifera from the NECOP study area impacted by the Mississippi River plume and seasonal hypoxia, Quat. Int., 31, 19–36, <a href="http://dx.doi.org/10.1016/1040-6182(95)00018-E">https://doi.org/10.1016/1040-6182(95)00018-E</a>, 1996. Blasnig, M., Riedel, B., Zuschin, M., Schiemer, L., and Stachowitsch, M.: Short-term post-mortality predation and scavenging and longer-term recovery after anoxia in the northern Adriatic Sea, Biogeosciences Discuss., 10, 4367–4401, <a href="http://dx.doi.org/10.5194/bgd-10-4367-2013">https://doi.org/10.5194/bgd-10-4367-2013</a>, 2013. Boltovskoy, E. and Lena, H.: On the Decomposition of the Protoplasm and the Sinking Velocity of the Planktonic Foraminifers, Int. Rev. Gesamten Hydrobiol. Hydrogr., 55, 797–804, <a href="http://dx.doi.org/10.1002/iroh.19700550507">https://doi.org/10.1002/iroh.19700550507</a>, 1970. 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, <a href="http://dx.doi.org/10.1016/j.ecolind.2012.03.011">https://doi.org/10.1016/j.ecolind.2012.03.011</a>, 2012. Burdige, D. J.: Geochemistry of marine sediments, Princeton University Press., 2006. Burgess, R.: An improved protocol for separating meiofauna from sediments using colloidal silica sols, Mar. Ecol.-Prog. Ser., 214, 161–165, 2001. Cearreta, A., Irabien, M. J., Leorri, E., Yusta, I., Croudace, I. W., and Cundy, A. B.: Recent Anthropogenic Impacts on the Bilbao Estuary, Northern Spain: Geochemical and Microfaunal Evidence, Estuar. Coast. Shelf S., 50, 571–592, <a href="http://dx.doi.org/10.1006/ecss.1999.0582">https://doi.org/10.1006/ecss.1999.0582</a>, 2000. Celia Magno, M., Bergamin, L., Finoia, M. G., Pierfranceschi, G., Venti, F., and Romano, E.: Correlation between textural characteristics of marine sediments and benthic foraminifera in highly anthropogenically-altered coastal areas, Mar. Geol., 315–318, 143–161, <a href="http://dx.doi.org/10.1016/j.margeo.2012.04.002">https://doi.org/10.1016/j.margeo.2012.04.002</a>, 2012. Chambers, J. M. and Hastie, T.: Statistical models in S, Chapman & Hall London, available at: <a href="http://www.lavoisier.fr/livre/notice.asp?id=OKRW3SA2OKOOWW">http://www.lavoisier.fr/livre/notice.asp?id=OKRW3SA2OKOOWW</a> (last access: 12 March 2013), 1992. Debenay, J.-P., Bicchi, E., Goubert, E., and Armynot du Châtelet, E.: Spatio-temporal distribution of benthic foraminifera in relation to estuarine dynamics (Vie estuary, Vendée, W France), Estuar. Coast. Shelf S., 67, 181–197, <a href="http://dx.doi.org/10.1016/j.ecss.2005.11.014">https://doi.org/10.1016/j.ecss.2005.11.014</a>, 2006. De Rijk, S., Jorissen, F. J., Rohling, E. J., and Troelstra, S. R.: Organic flux control on bathymetric zonation of Mediterranean benthic foraminifera, Mar. Micropaleontol., 40, 151–166, <a href="http://dx.doi.org/10.1016/S0377-8398(00)00037-2">https://doi.org/10.1016/S0377-8398(00)00037-2</a>, 2000. de Stigter, H. C., Jorissen, F. J., van der and Zwaan, G. J.: Bathymetric distribution and microhabitat partitioning of live (Rose Bengal stained) benthic Foraminifera along a shelf to bathyal transect in the southern Adriatic Sea, J. Foraminifer. Res., 28, 40–65, 1998. De Troch, M., Roelofs, M., Riedel, B., and Grego, M.: Structural and functional responses of harpacticoid copepods to anoxia in the Northern Adriatic: an experimental approach, Biogeosciences, 10, 4259–4272, <a href="http://dx.doi.org/10.5194/bg-10-4259-2013">https://doi.org/10.5194/bg-10-4259-2013</a>, 2013. Diaz, R. J. and Rosenberg, R.: Spreading dead zones and consequences for marine ecosystems, Science, 321, 926–929, 2008. Di Bella, L., Bellotti, P., Frezza, V., Bergamin, L., and Carboni, M. G.: Benthic foraminiferal assemblages of the imperial harbor of Claudius (Rome): Further paleoenvironmental and geoarcheological evidences, The Holocene, 21, 1245–1259, <a href="http://dx.doi.org/10.1177/0959683611405239">https://doi.org/10.1177/0959683611405239</a>, 2011. Di Leonardo, R., Bellanca, A., Capotondi, L., Cundy, A., and Neri, R.: Possible impacts of Hg and PAH contamination on benthic foraminiferal assemblages: An example from the Sicilian coast, central Mediterranean, Sci. Total Environ., 388, 168–183, <a href="http://dx.doi.org/10.1016/j.scitotenv.2007.08.009">https://doi.org/10.1016/j.scitotenv.2007.08.009</a>, 2007. Diz, P. and Francés, G.: Distribution of live benthic foraminifera in the Ría de Vigo (NW Spain), Mar. Micropaleontol., 66, 165–191, <a href="http://dx.doi.org/10.1016/j.marmicro.2007.09.001">https://doi.org/10.1016/j.marmicro.2007.09.001</a>, 2008. Donnici, S. and Serandrei Barbero, R.: The benthic foraminiferal communities of the northern Adriatic continental shelf, Mar. Micropaleontol., 44, 93–123, <a href="http://dx.doi.org/10.1016/S0377-8398(01)00043-3">https://doi.org/10.1016/S0377-8398(01)00043-3</a>, 2002. Duchemin, G., Jorissen, F. J., Le Loc'h, F., Andrieux-Loyer, F., Hily, C., and Thouzeau, G.: Seasonal variability of living benthic foraminifera from the outer continental shelf of the Bay of Biscay, J. Sea Res., 59, 297–319, <a href="http://dx.doi.org/10.1016/j.seares.2008.03.006">https://doi.org/10.1016/j.seares.2008.03.006</a>, 2008. Duijnstee, I. A. P., de Nooijer, L. J., Ernst, S. R., and van der Zwaan, G. J.: Population dynamics of benthic shallow-water foraminifera: effects of a simulated marine snow event, Mar. Ecol.-Prog. Ser., 285, 29–42, 2005. Duijnstee, I., Ernst, S., and Van der Zwaan, G.: Effect of anoxia on the vertical migration of benthic foraminifera, Mar. Ecol.-Prog. Ser., 246, 85–94, 2003. Duijnstee, I., de Lugt, I., Vonk Noordegraaf, H., and van der Zwaan, B.: Temporal variability of foraminiferal densities in the northern Adriatic Sea, Mar. Micropaleontol., 50, 125–148, <a href="http://dx.doi.org/10.1016/S0377-8398(03)00069-0">https://doi.org/10.1016/S0377-8398(03)00069-0</a>, 2004. Duros, P., Fontanier, C., Metzger, E., Pusceddu, A., Cesbron, F., de Stigter, H. C., Bianchelli, S., Danovaro, R., and Jorissen, F. J.: Live (stained) benthic foraminifera in the Whittard Canyon, Celtic margin (NE Atlantic), Deep-Sea Res. Pt. I, 58, 128–146, <a href="http://dx.doi.org/10.1016/j.dsr.2010.11.008">https://doi.org/10.1016/j.dsr.2010.11.008</a>, 2011. Ernst, S. and van der Zwaan, B.: Effects of experimentally induced raised levels of organic flux and oxygen depletion on a continental slope benthic foraminiferal community, Deep Sea Res. Part Oceanogr. Res. Pap., 51, 1709–1739, <a href="http://dx.doi.org/10.1016/j.dsr.2004.06.003">https://doi.org/10.1016/j.dsr.2004.06.003</a>, 2004. Ernst, S., Duijnstee, I., and van der Zwaan, B.: The dynamics of the benthic foraminiferal microhabitat: recovery after experimental disturbance, Mar. Micropaleontol., 46, 343–361, <a href="http://dx.doi.org/10.1016/S0377-8398(02)00080-4">https://doi.org/10.1016/S0377-8398(02)00080-4</a>, 2002. Ernst, S., Bours, R., Duijnstee, I., and van der Zwaan, B.: Experimental effects of an organic matter pulse and oxygen depletion on a benthic foraminiferal shelf community, J. Foraminifer. Res., 35, 177–197, <a href="http://dx.doi.org/10.2113/35.3.177">https://doi.org/10.2113/35.3.177</a>, 2005. Ernst, S. R., Morvan, J., Geslin, E., Le Bihan, A., and Jorissen, F. J.: Benthic foraminiferal response to experimentally induced Erika oil pollution, Mar. Micropaleontol., 61, 76–93, <a href="http://dx.doi.org/10.1016/j.marmicro.2006.05.005">https://doi.org/10.1016/j.marmicro.2006.05.005</a>, 2006. Faganeli, J., Avčin, A., Fanuko, N., Malej, A., Turk, V., Tušnik, P., Vrišer, B., and Vukovič, A.: Bottom layer anoxia in the central part of the Gulf of Trieste in the late summer of 1983, Mar. Pollut. Bull., 16, 75–78, <a href="http://dx.doi.org/10.1016/0025-326X(85)90127-4">https://doi.org/10.1016/0025-326X(85)90127-4</a>, 1985. Filipsson, H. L. and Nordberg, K.: Climate variations, an overlooked factor influencing the recent marine environment. An example from Gullmar Fjord, Sweden, illustrated by benthic foraminifera and hydrographic data, Estuar. Coasts, 27, 867–881, 2004. Frontalini, F. and Coccioni, R.: Benthic foraminifera as bioindicators of pollution: A review of Italian research over the last three decades, Rev. Micropaléontol., 54, 115–127, <a href="http://dx.doi.org/10.1016/j.revmic.2011.03.001">https://doi.org/10.1016/j.revmic.2011.03.001</a>, 2011. Geslin, E., Barras, C., Langlet, D., Kim, J.-H., Bonnin, J., Metzger, E., and Jorissen, F. J.: Survival, Reproduction and Calcification of Three Benthic Foraminiferal Species in Response to Experimentally Induced Hypoxia, in: Experimental Approaches in Foraminifera: Collection, Maintenance and Experiments, edited by: Bernhard, J. and Kitazato, H., Berlin, 2014. Giani, M., Djakovac, T., Degobbis, D., Cozzi, S., Solidoro, C., and Umani, S. F.: Recent changes in the marine ecosystems of the northern Adriatic Sea, Estuar. Coast. Shelf S., 115, 1–13, <a href="http://dx.doi.org/10.1016/j.ecss.2012.08.023">https://doi.org/10.1016/j.ecss.2012.08.023</a>, 2012. Glud, R. N.: Oxygen dynamics of marine sediments, Mar. Biol. Res., 4, 243–289, <a href="http://dx.doi.org/10.1080/17451000801888726">https://doi.org/10.1080/17451000801888726</a>, 2008. Goineau, A., Fontanier, C., Jorissen, F. J., Lansard, B., Buscail, R., Mouret, A., Kerhervé, P., Zaragosi, S., Ernoult, E., Artéro, C., Anschutz, P., Metzger, E., and Rabouille, C.: Live (stained) benthic foraminifera from the Rhône prodelta (Gulf of Lion, NW Mediterranean): Environmental controls on a river-dominated shelf, J. Sea Res., 65, 58–75, <a href="http://dx.doi.org/10.1016/j.seares.2010.07.007">https://doi.org/10.1016/j.seares.2010.07.007</a>, 2011. Goineau, A., Fontanier, C., Jorissen, F., Buscail, R., Kerhervé, P., Cathalot, C., Pruski, A. M., Lantoine, F., Bourgeois, S., Metzger, E., Legrand, E., and Rabouille, C.: Temporal variability of live (stained) benthic foraminiferal faunas in a river-dominated shelf – Faunal response to rapid changes of the river influence (Rhône prodelta, NW Mediterranean), Biogeosciences, 9, 1367–1388, <a href="http://dx.doi.org/10.5194/bg-9-1367-2012">https://doi.org/10.5194/bg-9-1367-2012</a>, 2012. Grego, M., Riedel, B., Stachowitsch, M., and De Troch, M.: Meiofauna winners and losers of coastal hypoxia: case study harpacticoid copepods, Biogeosciences, 11, 281–292, <a href="http://dx.doi.org/10.5194/bg-11-281-2014">https://doi.org/10.5194/bg-11-281-2014</a>, 2014. Haig, D. W.: Buliminid foraminifera from inner neritic sand and mud facies of the Papuan Lagoon, New Guinea, J. Foraminifer. Res., 23, 162–179, <a href="http://dx.doi.org/10.2113/gsjfr.23.3.162">https://doi.org/10.2113/gsjfr.23.3.162</a>, 1993. Hannah, F. and Rogerson, A.: The Temporal and Spatial Distribution of Foraminiferans in Marine Benthic Sediments of the Clyde Sea Area, Scotland, Estuar. Coast. Shelf S., 44, 377–383, 1997. Hayek, L.-A. C. and Buzas, M. A.: Surveying Natural Populations, Columbia University Press, 1997. Heinz, P., Kitazato, H., Schmiedl, G., and Hemleben, C.: Response of Deep-Sea Benthic Foraminifera from the Mediterranean Sea to Simulated Phytoplankton Pulses Under Laboratory Conditions, J. Foraminifer. Res., 31, 210–227, <a href="http://dx.doi.org/10.2113/31.3.210">https://doi.org/10.2113/31.3.210</a>, 2001. Helly, J. J. and Levin, L. A.: Global distribution of naturally occurring marine hypoxia on continental margins, Deep-Sea Res. Pt. I, 51, 1159–1168, <a href="http://dx.doi.org/10.1016/j.dsr.2004.03.009">https://doi.org/10.1016/j.dsr.2004.03.009</a>, 2004. Hess, S. and Kuhnt, W.: Deep-sea benthic foraminiferal recolonization of the 1991 Mt. Pinatubo ash layer in the South China Sea, Mar. Micropaleontol., 28, 171–197, <a href="http://dx.doi.org/10.1016/0377-8398(95)00080-1">https://doi.org/10.1016/0377-8398(95)00080-1</a>, 1996. Høgslund, S., Revsbech, N. P., Cedhagen, T., Nielsen, L. P., and Gallardo, V. A.: Denitrification, nitrate turnover, and aerobic respiration by benthic foraminiferans in the oxygen minimum zone off Chile, J. Exp. Mar. Biol. Ecol., 359, 85–91, 2008. Hohenegger, J., Piller, W., and Baal, C.: Reasons for Spatial Microdistributions of Foraminifers in an Intertidal Pool (Northern Adriatic Sea), Mar. Ecol., 10, 43–78, <a href="http://dx.doi.org/10.1111/j.1439-0485.1989.tb00065.x">https://doi.org/10.1111/j.1439-0485.1989.tb00065.x</a>, 1989. Hohenegger, J., Piller, W. E., and Baal, C.: Horizontal and vertical spatial microdistribution of foraminifers in the shallow subtidal Gulf of Trieste, northern Adriatic Sea, J. Foraminifer. Res., 23, 79–101, <a href="http://dx.doi.org/10.2113/gsjfr.23.2.79">https://doi.org/10.2113/gsjfr.23.2.79</a>, 1993. Hyams-Kaphzan, 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, <a href="http://dx.doi.org/10.1016/j.marpolbul.2009.07.010">https://doi.org/10.1016/j.marpolbul.2009.07.010</a>, 2009. Jorissen, F. J.: The distribution of benthic foraminifera in the Adriatic Sea, Mar. Micropaleontol., 12, 21–48, <a href="http://dx.doi.org/10.1016/0377-8398(87)90012-0">https://doi.org/10.1016/0377-8398(87)90012-0</a>, 1987. Jorissen, F. J.: Benthic foraminifera from the Adriatic Sea?: principles of phenotypic variation, Utrecht Micropaleontol. Bull., 37, 176 pp., 1988. Jorissen, F. J.: Benthic foraminiferal microhabitats below the sediment-water interface, in Modern Foraminifera, 161–179, Springer Netherlands, available at: <a href="http://link.springer.com/chapter/10.1007/0-306-48104-9_10">http://link.springer.com/chapter/10.1007/0-306-48104-9_10</a> (last access: 12 March 2013), 1999. Jorissen, F. J., Barmawidjaja, D. M., Puskaric, S., and van der Zwaan, G. J.: Vertical distribution of benthic foraminifera in the northern Adriatic Sea: The relation with the organic flux, Mar. Micropaleontol., 19, 131–146, <a href="http://dx.doi.org/10.1016/0377-8398(92)90025-F">https://doi.org/10.1016/0377-8398(92)90025-F</a>, 1992. Jorissen, F. J., Wittling, I., Peypouquet, J. P., Rabouille, C., and Relexans, J. C.: Live benthic foraminiferal faunas off Cape Blanc, NW-Africa: Community structure and microhabitats, Deep Sea Res. Pt. I, 45, 2157–2188, <a href="http://dx.doi.org/10.1016/S0967-0637(98)00056-9">https://doi.org/10.1016/S0967-0637(98)00056-9</a>, 1998. Koho, K. A. and Piña-Ochoa, E.: Benthic Foraminifera: Inhabitants of Low-Oxygen Environments, in Anoxia, edited by: Altenbach, A. V., Bernhard, J. M., and Seckbach, J., 249–285, Springer Netherlands, available at: <a href="http://link.springer.com/chapter/10.1007/978-94-007-1896-8_14">http://link.springer.com/chapter/10.1007/978-94-007-1896-8_14</a> (last access: 20 February 2013), 2012. Koron, N., Ogrinc, N., Metzger, E., Riedel, B., and Faganeli, J.: Diagenesis and benthic fluxes of nutrients and metals during experimentally induced anoxia in the Gulf of Trieste (northern Adriatic Sea), Biogeosciences Discuss., 10, 11729–11755, <a href="http://dx.doi.org/10.5194/bgd-10-11729-2013">https://doi.org/10.5194/bgd-10-11729-2013</a>, 2013. Langezaal, A. M., Jorissen, F. J., Braun, B., Chaillou, G., Fontanier, C., Anschutz, P., and van der Zwaan, G. J.: The influence of seasonal processes on geochemical profiles and foraminiferal assemblages on the outer shelf of the Bay of Biscay, Cont. Shelf Res., 26, 1730–1755, <a href="http://dx.doi.org/10.1016/j.csr.2006.05.005">https://doi.org/10.1016/j.csr.2006.05.005</a>, 2006. Langlet, D., Geslin, E., Baal, C., Metzger, E., Lejzerowicz, F., Riedel, B., Zuschin, M., Pawlowski, J., Stachowitsch, M., and Jorissen, F. J.: Foraminiferal survival after long-term in situ experimentally induced anoxia, Biogeosciences, 10, 7463–7480, <a href="http://dx.doi.org/10.5194/bg-10-7463-2013">https://doi.org/10.5194/bg-10-7463-2013</a>, 2013. Mackensen, A., Schumacher, S., Radke, J., and Schmidt, D. N.: Microhabitat preferences and stable carbon isotopes of endobenthic foraminifera: clue to quantitative reconstruction of oceanic new production?, Mar. Micropaleontol., 40, 233–258, <a href="http://dx.doi.org/10.1016/S0377-8398(00)00040-2">https://doi.org/10.1016/S0377-8398(00)00040-2</a>, 2000. Malej, A. and Malacic, V.: Factors affecting bottom layer oxygen depletion in the Gulf of Trieste (Adriatic Sea), Ann. Istrske Mediter. Stud. Hist. Nat., 6, 33–42, 1995. Mateu-Vicens, G., Box, A., Deudero, S., and Rodríguez, B.: Comparative Analysis of Epiphytic Foraminifera in Sediments Colonized by Seagrass <i>Posidonia oceanica</i> and Invasive Macroalgae <i>Caulerpa</i> spp., J. Foraminifer. Res., 40, 134–147, <a href="http://dx.doi.org/10.2113/gsjfr.40.2.134">https://doi.org/10.2113/gsjfr.40.2.134</a>, 2010. McIntyre, A. D. and Warwick, R. M.: Meiofauna techniques, in: Methods for the Study of Marine Benthos, edited by: Holme, N. A. and McIntyre, A. D., Oxford, 217–244, 1984. Mendes, I., Dias, J. A., Schönfeld, J., and Ferreira, Ó.: Distribution of living benthic foraminifera on the northern gulf of Cadiz continental shelf, J. Foraminifer. Res., 42, 18–38, <a href="http://dx.doi.org/10.2113/gsjfr.42.1.18">https://doi.org/10.2113/gsjfr.42.1.18</a>, 2012. Metzger, E., Langlet, D., Viollier, E., Koron, N., Riedel, B., Stachowitsch, M., Faganeli, J., Tharaud, M., Geslin, E., and Jorissen, F.: Artificially induced migration of redox layers in a coastal sediment from the Northern Adriatic, Biogeosciences Discuss., 10, 12029–12063, <a href="http://dx.doi.org/10.5194/bgd-10-12029-2013">https://doi.org/10.5194/bgd-10-12029-2013</a>, 2013. Middelburg, J. J. and Levin, L. A.: Coastal hypoxia and sediment biogeochemistry, Biogeosciences, 6, 1273–1293, <a href="http://dx.doi.org/10.5194/bg-6-1273-2009">https://doi.org/10.5194/bg-6-1273-2009</a>, 2009. Mojtahid, M., Jorissen, F., Durrieu, J., Galgani, F., Howa, H., Redois, F., and Camps, R.: Benthic foraminifera as bio-indicators of drill cutting disposal in tropical east Atlantic outer shelf environments, Mar. Micropaleontol., 61, 58–75, <a href="http://dx.doi.org/10.1016/j.marmicro.2006.05.004">https://doi.org/10.1016/j.marmicro.2006.05.004</a>, 2006. Mojtahid, M., Jorissen, F., and Pearson, T. H.: Comparison of benthic foraminiferal and macrofaunal responses to organic pollution in the Firth of Clyde (Scotland), Mar. Pollut. Bull., 56, 42–76, <a href="http://dx.doi.org/10.1016/j.marpolbul.2007.08.018">https://doi.org/10.1016/j.marpolbul.2007.08.018</a>, 2008. Mojtahid, M., Jorissen, F., Lansard, B., Fontanier, C., Bombled, B., and Rabouille, C.: Spatial distribution of live benthic foraminifera in the Rhône prodelta: Faunal response to a continental–marine organic matter gradient, Mar. Micropaleontol., 70, 177–200, <a href="http://dx.doi.org/10.1016/j.marmicro.2008.12.006">https://doi.org/10.1016/j.marmicro.2008.12.006</a>, 2009. Moodley, L. and Hess, C.: Tolerance of infaunal benthic foraminifera for low and high oxygen concentrations, Biol. Bull., 183, 94–98, 1992. Moodley, L., van der Zwaan, G. J., Herman, P. M. J., Kempers, L., and van Breugel, P.: Differential response of benthic meiofauna to anoxia with special reference to Foraminifera (Protista: Sarcodina), Mar. Ecol.-Prog. Ser., 158, 151–163, <a href="http://dx.doi.org/10.3354/meps158151">https://doi.org/10.3354/meps158151</a>, 1997. Moodley, L., Schaub, B. E. M., van der Zwaan, G. J., and Herman, P. M. J.: Tolerance of benthic foraminifera (Protista: Sarcodina) to hydrogen sulphide, Mar. Ecol.-Prog. Ser., 169, 77–86, <a href="http://dx.doi.org/10.3354/meps169077">https://doi.org/10.3354/meps169077</a>, 1998. Murray, J. W.: Ecology And Applications of Benthic Foraminifera, Cambridge University Press, 2006. Murray, J. W. and Bowser, S. S.: Mortality, Protoplasm Decay Rate, and Reliability of Staining Techniques to Recognize "living" Foraminifera: A Review, J. Foraminifer. Res., 30, 66–70, <a href="http://dx.doi.org/10.2113/0300066">https://doi.org/10.2113/0300066</a>, 2000. Nomaki, H., Heinz, P., Hemleben, C., and Kitazato, H.: Behavior and Response of Deep-Sea Benthic Foraminifera to Freshly Supplied Organic Matter: A Laboratory Feeding Experiment in Microcosm Environments, J. Foraminifer. Res., 35, 103–113, <a href="http://dx.doi.org/10.2113/35.2.103">https://doi.org/10.2113/35.2.103</a>, 2005. Nordberg, K., Gustafsson, M., and Krantz, A. L.: Decreasing oxygen concentrations in the Gullmar Fjord, Sweden, as confirmed by benthic foraminifera, and the possible association with NAO, J. Mar. Syst., 23, 303–316, 2000. Pearson, T. H. and Rosenberg, R.: A comparative study of the effects on the marine environment of wastes from cellulose industries in Scotland and Sweden, Amibo, 5, 77–79, 1976. Piña-Ochoa, E., Høgslund, S., Geslin, E., Cedhagen, T., Revsbech, N. P., Nielsen, L. P., Schweizer, M., Jorissen, F., Rysgaard, S., and Risgaard-Petersen, N.: Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida, P. Natl. Acad. Sci. USA, 107, 1148–1153, 2010. Pucci, F., Geslin, E., Barras, C., Morigi, C., Sabbatini, A., Negri, A., and Jorissen, F.: Survival of benthic foraminifera under hypoxic conditions: Results of an experimental study using the CellTracker Green method, Mar. Pollut. Bull., 59, 336–351, 2009. R Development Core Team: R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, available at: <a href="http://www.R-project.org/">http://www.R-project.org/</a>, 2011. Riedel, B., Zuschin, M., Haselmair, A., and Stachowitsch, M.: Oxygen depletion under glass: Behavioural responses of benthic macrofauna to induced anoxia in the Northern Adriatic, J. Exp. Mar. Biol. Ecol., 367, 17–27, <a href="http://dx.doi.org/10.1016/j.jembe.2008.08.007">https://doi.org/10.1016/j.jembe.2008.08.007</a>, 2008. Riedel, B., Zuschin, M., and Stachowitsch, M.: Tolerance of benthic macrofauna to hypoxia and anoxia in shallow coastal seas: a realistic scenario, Mar. Ecol.-Prog. Ser., 458, 39–52, <a href="http://dx.doi.org/10.3354/meps09724">https://doi.org/10.3354/meps09724</a>, 2012. Riedel, B., Pados, T., Pretterebner, K., Schiemer, L., Steckbauer, A., Haselmair, A., Zuschin, M., and Stachowitsch, M.: Effect of hypoxia and anoxia on invertebrate behaviour: ecological perspectives from species to community level, Biogeosciences Discuss., 10, 14333–14438, <a href="http://dx.doi.org/10.5194/bgd-10-14333-2013">https://doi.org/10.5194/bgd-10-14333-2013</a>, 2013. Risgaard-Petersen, N., Langezaal, A. M., Ingvardsen, S., Schmid, M. C., Jetten, M. S. M., Op Den Camp, H. J. M., Derksen, J. W. M., Piña-Ochoa, E., Eriksson, S. P., Nielsen, L. P., Revsbech, N. P., Cedhagen, T., and Van Der Zwaan, G. J.: Evidence for complete denitrification in a benthic foraminifer, Nature, 443, 93–96, 2006. Romano, E., Bergamin, L., Ausili, A., Pierfranceschi, G., Maggi, C., Sesta, G., and Gabellini, M.: The impact of the Bagnoli industrial site (Naples, Italy) on sea-bottom environment. Chemical and textural features of sediments and the related response of benthic foraminifera, Mar. Pollut. Bull., 59, 245–256, <a href="http://dx.doi.org/10.1016/j.marpolbul.2009.09.017">https://doi.org/10.1016/j.marpolbul.2009.09.017</a>, 2009. Sabbatini, A., Bonatto, S., Gooday, A. J., Morigi, C., Pancotti, I., Pucci, F., and Negri, A.: Modern benthic foraminifers at Northern shallow sites of Adriatic Sea and soft-walled, monothalamous taxa: a brief overview, Micropaleontology, 56, 359–376, 2010. Sabbatini, A., Bonatto, S., Bianchelli, S., Pusceddu, A., Danovaro, R., and Negri, A.: Foraminiferal assemblages and trophic state in coastal sediments of the Adriatic Sea, J. Mar. Syst., 105–108, 163–174, <a href="http://dx.doi.org/10.1016/j.jmarsys.2012.07.009">https://doi.org/10.1016/j.jmarsys.2012.07.009</a>, 2012. Schmiedl, G., de Bovée, F., Buscail, R., Charrière, B., Hemleben, C., Medernach, L., and Picon, P.: Trophic control of benthic foraminiferal abundance and microhabitat in the bathyal Gulf of Lions, western Mediterranean Sea, Mar. Micropaleontol., 40, 167–188, <a href="http://dx.doi.org/10.1016/S0377-8398(00)00038-4">https://doi.org/10.1016/S0377-8398(00)00038-4</a>, 2000. Schumacher, S., Jorissen, F. J., Dissard, D., Larkin, K. E., and Gooday, A. J.: Live (Rose Bengal stained) and dead benthic foraminifera from the oxygen minimum zone of the Pakistan continental margin (Arabian Sea), Mar. Micropaleontol., 62, 45–73, <a href="http://dx.doi.org/10.1016/j.marmicro.2006.07.004">https://doi.org/10.1016/j.marmicro.2006.07.004</a>, 2007. Scott, D. B., Medioli, F. S., and Schafer, C. T.: Monitoring in coastal environments using foraminifera and thecamoebian indicators, Cambridge University Press, available at: <a href="www.cambridge.org/0521561736">www.cambridge.org/0521561736</a> (last access: 27 September 2012), 2001. Semensatto Jr., D. L., Funo, R. H. F., Dias-Brito, D., and Coelho Jr., C.: Foraminiferal ecological zonation along a Brazilian mangrove transect: Diversity, morphotypes and the influence of subaerial exposure time, Rev. Micropaléontol., 52, 67–74, <a href="http://dx.doi.org/10.1016/j.revmic.2008.06.004">https://doi.org/10.1016/j.revmic.2008.06.004</a>, 2009. Smith, M. S., Firestone, M. K., and Tiedje, J. M.: The Acetylene Inhibition Method for Short-term Measurement of Soil Denitrification and its Evaluation Using Nitrogen-131, Soil Sci. Soc. Am. J., 42, 611, <a href="http://dx.doi.org/10.2136/sssaj1978.03615995004200040015x">https://doi.org/10.2136/sssaj1978.03615995004200040015x</a>, 1978. Stachowitsch, M.: Mass Mortality in the Gulf of Trieste: The Course of Community Destruction, Mar. Ecol., 5, 243–264, <a href="http://dx.doi.org/10.1111/j.1439-0485.1984.tb00124.x">https://doi.org/10.1111/j.1439-0485.1984.tb00124.x</a>, 1984. Stachowitsch, M., Riedel, B., Zuschin, M., and Machan, R.: Oxygen depletion and benthic mortalities: The first in situ experimental approach to documenting an elusive phenomenon, Limnol. Oceanogr.-Methods, 5, 344–352, 2007. Tsuchiya, M., Tazume, M., and Kitazato, H.: Molecular characterization of the non-costate morphotypes of buliminid foraminifers based on internal transcribed region of ribosomal DNA (ITS rDNA) sequence data, Mar. Micropaleontol., 69, 212–224, <a href="http://dx.doi.org/10.1016/j.marmicro.2008.07.008">https://doi.org/10.1016/j.marmicro.2008.07.008</a>, 2008. Walton, W. R.: Techniques for recognition of living foraminifera, in: Contributions from the Cushman Foundation for Foraminiferal Research, Scripps Institution of Oceanography, 3, 56–60, 1952. Wieser, W. and Kanwisher, J.: Ecological and physiological studies on marine nematodes from a small salt marsh near Woods Hole, Massachusetts, Limnol. Oceanogr., 6, 262–270, 1961. Zwaan, G. J. V. D. and Jorissen, F. J.: Biofacial patterns in river-induced shelf anoxia, Geol. Soc. Lond. Spec. Publ., 58, 65–82, <a href="http://dx.doi.org/10.1144/GSL.SP.1991.058.01.05">https://doi.org/10.1144/GSL.SP.1991.058.01.05</a>, 1991.