The contribution of benthic foraminifera to sediment bioturbation has widely been overlooked despite their huge abundance in intertidal soft sediments. In this preliminary study, we specifically chose to focus on two key species of benthic foraminifera in temperate intertidal mudflats, Quinqueloculina seminula and Ammonia tepida , and first experimentally investigated their individual movements at the sediment surface. We subsequently derived from these observations the individual-level surface sediment reworking rates, and used the actual abundance of these species to extrapolate these rates at the population level. Individual surface sediment reworking rates SSRR i ranged between 0.13 and 0.32 cm 2 · ind -1 · day -1 for Q. seminula , and between 0.12 and 0.28 cm 2 · ind -1 · day -1 for A. tepida . Population-level surface sediment reworking rates were subsequently estimated as ranging between 11,484 and 28,710 cm 2 · m -2 · day -1 for Q. seminula and 27,876 and 65,044 cm 2 · m -2 · day -1 for A. tepida . Noticeably, these reworking rates are comparable to, and eventually even higher than, the rates reported in the literature for populations of intertidal macro-invertebrates, such as the annelid polychaete Melinna palmata and the bivalve Abra ovata . Taken together these results suggest that despite their minute size intertidal benthic foraminifera are, thanks to their abundance, non-negligible contributors to the reworking of surface sediment, and may then play an unanticipated role in the benthic ecosystem functioning, through e.g. the enhancement of fluxes at the sediment-water interface.
Kristensen, E., Penha-Lopes, G., Delefosse, M., Valdemarsen, T., Quintana, C.O. and Banta, G.T. (2012) What Is Bioturbation? The Need for a Precise Definition for Fauna in Aquatic Sciences. Marine Ecology Progress Series, 446, 285-302. https://doi.org/10.3354/meps09506
Mermillod-Blondin, F. and Rosenberg, R. (2006) Ecosystem Engineering: The Impact of Bioturbation on Biogeochemical Processes in Marine and Freshwater Benthic Habitats. Aquatic Science, 68, 434-442. https://doi.org/10.1007/s00027-006-0858-x
Giere, O. (2009) Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediments. 2nd Edition, Springer Press, Berlin.
Aller, R.C. and Aller, J.Y. (1992) Meiofauna and Solute Transport in Marine Muds. Limnology & Oceanography, 37, 1018-1033. https://doi.org/10.4319/lo.1992.37.5.1018
Pike, J., Bernhard, J.M., Moreton, S.G. and Butler, I.B. (2010) Microbioirrigation of Marine Sediments in Dysoxic Environments: Implications for Early Sediment Fabric Formation and Diagenetic Processes. Geology, 29, 923-926. https://doi.org/10.1130/0091-7613(2001)029 2.0.CO;2
Nascimento, F.J.A., Naslund, J. and Elmgren, R. (2012) Meiofauna Enhances Organic Matter Mineralization in Soft Sediment Ecosystems. Limnology & Oceanography, 57, 338-346. https://doi.org/10.4319/lo.2012.57.1.0338
Bonaglia, S., Nascimento, F.J.A., Bartoli, M., Klawonn, I. and Brüchert, V. (2014) Meiofauna Increases Bacterial Denitrification in Marine Sediments. Nature Communications, 5, 1-9. https://doi.org/10.1038/ncomms6133
Queirós, A.M., Birchenough, S.N., Bremner, J., Godbold, J.A., Parker, R.E., Romero-Ramirez, A., Reiss, H., Solan, M., Somerfield, P.J., Van Colen, C., Van Hoey, G. and Widdicombe, S. (2013) A Bioturbation Classification of European Marine Infaunal Invertebrates. Ecology & Evolution, 3, 3958-3985. https://doi.org/10.1002/ece3.769
Schratzberger, M. and Ingels, J. (2018) Meiofauna Matters: The Roles of Meiofauna in Benthic Ecosystems. Journal of Experimental Marine Biology and Ecology, 502, 12-25. https://doi.org/10.1016/j.jembe.2017.01.007
Murray, J. (2006) Ecology and Applications of Benthic Foraminifera. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511535529
Langer, M.R. (2008) Assessing the Contribution of Foraminiferan Protists to Global Ocean Carbonate Production. Journal of Eukaryotic Microbiology, 55, 163-169. https://doi.org/10.1111/j.1550-7408.2008.00321.x
Moodley, L., Boschker, H.T.S., Middelburg, J.J., Pel, R., Herman, P.M.J., de Deckere, E. and Heip, C.H.R. (2000) Ecological Significance of Benthic Foraminifera: 13C Labelling Experiments. Marine Ecology Progress Series, 202, 289-295. https://doi.org/10.3354/meps202289
Risgaard-Petersen, N., Langezaal, A.M., Ingvardsen, S., Schmid, M.C., Jetten, M.S.M., Opden Camp, H.J.M., Derksen, J.W.M., Pina-Ochoa, E., Eriksson, S.P., Nielsen, L.P., Revsbech, N.P., Cedhagen, T. and van der Zwaan, G.J. (2006) Evidence for Complete Denitrification in a Benthic Foraminifer. Nature, 443, 93-96. https://doi.org/10.1038/nature05070
Heinz, P., Geslin, E. and Hemleben, C. (2005) Laboratory Observations of Benthic Foraminiferal Cysts. Marine Biology Research, 2, 149-159. https://doi.org/10.1080/17451000510019114
Seuront, L. and Bouchet, V.M.P. (2015) The Devil Lies in Details: New Insights into the Behavioural Ecology of Benthic Foraminifera. Journal of Foraminiferal Research, 45, 390-401. https://doi.org/10.2113/gsjfr.45.4.390
Jauffrais, T., Jesus, B., Geslin, E., Briand, F. and Martin Jézéquel, V. (2016) Locomotion Speed of the Benthic Foraminifer Ammonia tepida Exposed to Different Nitrogen and Carbon Sources. Journal of Sea Research, 118, 52-58. https://doi.org/10.1016/j.seares.2016.07.001
Severin, K.P., Culver, S.J. and Blanpied, C. (1982) Burrows and Trails Produced by Quinqueloculina impressa Reuss, a Benthic Foraminifer, in Fine-Grained Sediment. Sedimentology, 29, 897-901. https://doi.org/10.1111/j.1365-3091.1982.tb00093.x
Orvain, F., Sauriau, P.-G., Sygut, A., Joassard, L. and Le Hir, P. (2004) Interacting Effects of Hydrobia ulvae Bioturbation and Microphytobenthos on the Erodibility of Mudflat Sediments. Marine Ecology Progress Series, 278, 205-223. https://doi.org/10.3354/meps278205
Langer, M.R., Hottinger, L. and Huber, B. (1989) Functional Morphology in Low-Diverse Benthic Foraminiferal Assemblages from Tidal Flats of the North Sea. Senckenberg Maritima, 20, 81-99.
Wetmore, K.L. (1988) Burrowing and Sediment Movement by Benthic Foraminifera, as Shown by Time-Lapse Cinematography. Revue de Paléobiologie, 2, 921-927.
Linke, P. and Lutze, G.F. (1993) Microhabitat Preferences of Benthic Foraminifera a Static Concept or a Dynamic Adaptation to Optimize Food Acquisition? Marine Micropaleontology, 20, 215-234. https://doi.org/10.1016/0377-8398(93)90034-U
Hemleben, C. and Kitazato, H. (1995) Deep-Sea Foraminifera under Long Time Observation in the Laboratory. Deep-Sea Research, 42, 827-832. https://doi.org/10.1016/0967-0637(95)00024-Z
Gross, O. (2002) Sediment Interactions of Foraminifera: Implications for Food Degradation and Bioturbation Processes. Journal of Foraminiferal Research, 32, 414-424. https://doi.org/10.2113/0320414
Duport, E., Gilbert, F., Poggiale, J.-C., Dedieu, K., Rabouille, C. and Stora, G. (2007) Benthic Macrofauna and Sediment Reworking Quantification in Contrasted Environments in the Thau Lagoon. Estuarine, Coastal, and Shelf Science, 72, 522-533. https://doi.org/10.1016/j.ecss.2006.11.018
Hollertz, K. and Duchene, J.-C. (2001) Burrowing Behaviour and Sediment Reworking in the Heart Urchin Brissopsis lyrifera Forbes (Spatangoida). Marine Biology, 139, 951-957. https://doi.org/10.1007/s002270100629
Maire, O., Lecroart, P., Meysman, F.J.R., Rosenberg, R., Duchene, J.C. and Grémare, A. (2008) Methods of Sediment Reworking Assessment in Bioturbation Research: A Review. Aquatic Biology, 2, 219-238. https://doi.org/10.3354/ab00053
Bouchet, V.M.P., Debenay, J.-P., Sauriau, P.-G., Radford-Knoery, J. and Soletchnik, P. (2007) Effects of Short-Term Environmental Disturbances on Living Benthic Foraminifera during the Pacific Oyster Summer Mortality in the Marennes-Oléron Bay (France). Marine Environmental Research, 64, 358-383. https://doi.org/10.1016/j.marenvres.2007.02.007
Armynot du Chatelet, E., Francescangeli, F., Bouchet, V.M.P. and Frontalini, F. (2018) Benthic Foraminifera in Transitional Environments in the English Channel and the Southern North Sea: A Proxy for Regional-Scale Environmental and Paleo-Environmental Characterisations. Marine Environmental Research, 137, 37-48. https://doi.org/10.1016/j.marenvres.2018.02.021
Bouchet, V.M.P., Alve, E., Rygg, B. and Telford, R.J. (2012) Benthic Foraminifera Provide a Promising Tool for Ecological Quality Assessment of Marine Waters. Ecological Indicators, 23, 66-75. https://doi.org/10.1016/j.ecolind.2012.03.011
Rhoads, D.C. (1963) Rates of Sediment Reworking by Yoldia limatula in Buzzards Bay, Massachusetts, and Long Island Sound. Journal of Sedimentary Petrolology, 33, 723-727. https://doi.org/10.1306/74D70F0B-2B21-11D7-8648000102C1865D
Wheatcroft, R.A., Jumars, P.A., Smith, C.R. and Nowell, A.R.M. (1990) A Mechanistic View of the Particulate Biodiffusion Coefficient: Step Lengths, Rest Periods and Transport Directions. Journal of Marine Research, 48, 177-207. https://doi.org/10.1357/002224090784984560
Lohrer, A.M., Thrush, S.F., Hunt, L., Hancock, N. and Lundquist, C. (2005) Rapid Reworking of Subtidal Sediments by Burrowing Spangoid Urchins. Journal of Experimental Marine Biology and Ecology, 321, 155-169. https://doi.org/10.1016/j.jembe.2005.02.002
Andersen, T.J. (2001) Seasonal Variation in Erodibility of Two Temperate, Microtidal Mudflats. Estuarine Coastal and Shelf Science, 53, 1-12. https://doi.org/10.1006/ecss.2001.0790
Meysman, F.J.R., Middelburg, J.J. and Heip, C.H. (2006) Bioturbation: A Fresh Look at Darwin’s Last Idea. Trends in Ecology an Evolution, 12, 688-695. https://doi.org/10.1016/j.tree.2006.08.002
Massé, C., Garabétian, F., Deflandre, B., Maire, O., Costes, L., Mesmer-Dudons, N., Duchêne, J.-C., Bernard, G., Grémare, A. and Ciutat, A. (2019) Feeding Ethology and Surface Sediment Reworking by the Ampharetid Polychaete Melinna palmata Grube, 1870: Effects on Sediment Characteristics and Aerobic Bacterial Community Composition. Journal of Experimental Marine Biology and Ecology, 512, 63-77. https://doi.org/10.1016/j.jembe.2018.12.009
Maire, O., Duchêne, J.-C., Bigot, L. and Grémare, A. (2007) Linking Feeding Activity and Sediment Reworking in the Deposit-Feeding Bivalve Abra ovata with Image Analysis, Laser Telemetry, and Luminophore Tracers. Marine Ecology Progress Series, 351, 139-150. https://doi.org/10.3354/meps07147
Dauvin, J.-C., Ruellet, T., Thiébaut, E., Gentil, F., Desroy, N., Janson, A.-L., Duhamel, S., Jourde, J. and Simon, S. (2007) The Presence of Melinna palmata (Annelida: Polychaeta) and Ensis directus (Mollusca: Bivalvia) Related to Sedimentary Changes in the Bay of Seine (English Channel, France). Cahiers de Biologie Marine, 48, 391-401.
Mosbahi, N., Blanchet, H., Lavesque, N., de Montaudouin, X., Dauvin, J.-C. and Neifar, L. (2017) Main Ecological Features of Benthic Macrofauna in Mediterranean and Atlantic Intertidal Eelgrass Beds: A Comparative Study. Journal of Marine Biology and Oceanography, 6, 2. https://doi.org/10.4172/2324-8661.1000174
Mermillod-Blondin, F., Rosenberg, R., Francois-Carcaillet, F., Norling, K. and Mauclair, L. (2004) Influence of Bioturbation by Three Benthic Infaunal Species on Microbial Communities and Biogeochemical Processes in Marine Sediment. Aquatic Microbial Ecology, 36, 271-284. https://doi.org/10.3354/ame036271