Meiofauna Metabolism in Suboxic Sediments: Currently Overestimated

Oxygen is recognized as a structuring factor of metazoan communities in marine sediments. The importance of oxygen as a controlling factor on meiofauna (32 µm-1 mm in size) respiration rates is however less clear. Typically, respiration rates are measured under oxic conditions, after which these rates are used in food web studies to quantify the role of meiofauna in sediment carbon turnover. Sediment oxygen concentration ([O2]) is generally far from saturated, implying that (1) current estimates of the role of meiofauna in carbon cycling may be biased and (2) meiofaunal organisms need strategies to survive in oxygen-stressed environments. Two main survival strategies are often hypothesized: 1) frequent migration to oxic layers and 2) morphological adaptation. To evaluate these hypotheses, we (1) used a model of oxygen turnover in the meiofauna body as a function of ambient [O2], and (2) performed respiration measurements at a range of [O2] conditions. The oxygen turnover model predicts a tight coupling between ambient [O2] and meiofauna body [O2] with oxygen within the body being consumed in seconds. This fast turnover favors long and slender organisms in sediments with low ambient [O2] but even then frequent migration between suboxic and oxic layers is for most organisms not a viable strategy to alleviate oxygen limitation. Respiration rates of all measured meiofauna organisms slowed down in response to decreasing ambient [O2], with Nematoda displaying the highest metabolic sensitivity for declining [O2] followed by Foraminifera and juvenile Gastropoda. Ostracoda showed a behavioral stress response when ambient [O2] reached a critical level. Reduced respiration at low ambient [O2] implies that meiofauna in natural, i.e. suboxic, sediments must have a lower metabolism than inferred from earlier respiration rates conducted under oxic conditions. The implications of these findings are discussed for the contribution of meiofauna to carbon cycling in marine sediments.

[1]  D. Oevelen,et al.  Carbon processing at the deep-sea floor of the Arabian Sea oxygen minimum zone: A tracer approach , 2013 .

[2]  S. Powers,et al.  Effects of Hypoxia and Anoxia on Meiofauna: A Review with New Data from the Gulf of Mexico , 2013 .

[3]  A. Vanreusel,et al.  Feeding ecology of shallow water meiofauna: insights from a stable isotope tracer experiment in Potter Cove, King George Island, Antarctica , 2012, Polar Biology.

[4]  A. Vanreusel,et al.  Feeding ecology of shallow water meiofauna: insights from a stable isotope tracer experiment in Potter Cove, King George Island, Antarctica , 2012, Polar Biology.

[5]  K. Soetaert,et al.  Biological vs. Physical Mixing Effects on Benthic Food Web Dynamics , 2011, PloS one.

[6]  D. Oevelen,et al.  Nutritional importance of benthic bacteria for deep‐sea nematodes from the Arctic ice margin: Results of an isotope tracer experiment , 2010 .

[7]  K. Soetaert,et al.  Respiration partitioning in contrasting subtidal sediments: seasonality and response to a spring phytoplankton deposition , 2010 .

[8]  A. Vanreusel,et al.  Preferred use of bacteria over phytoplankton by deep-sea nematodes in polar regions , 2010 .

[9]  Karline Soetaert,et al.  A Practical Guide to Ecological Modelling: Using R as a Simulation Platform , 2008 .

[10]  R. Glud Oxygen dynamics of marine sediments , 2008 .

[11]  K. Soetaert,et al.  Uptake of phytodetritus by meiobenthos using 13C labelled diatoms and Phaeocystis in two contrasting sediments from the North Sea , 2008 .

[12]  P. H. Avesaath,et al.  Biomass-specific respiration rates of benthic meiofauna: Demonstrating a novel oxygen micro-respiration system , 2008 .

[13]  K. Soetaert,et al.  Responses of intertidal nematodes to short-term anoxic events , 2007 .

[14]  I. Boomer,et al.  The use of ostracods from marginal marine, brackish waters as bioindicators of modern and Quaternary environmental change , 2005 .

[15]  M. Vincx,et al.  Laboratory experiments on the infaunal activity of intertidal nematodes , 2005, Hydrobiologia.

[16]  Markus Huettel,et al.  Hydrodynamical impact on biogeochemical processes in aquatic sediments , 2003, Hydrobiologia.

[17]  C. Heip,et al.  Size and shape of ocean margin nematodes: morphological diversity and depth-related patterns , 2002 .

[18]  C. Heip,et al.  Bacteria and Foraminifera: key players in a short-term deep-sea benthic response to phytodetritus , 2002 .

[19]  R. Glud,et al.  Benthic carbon mineralization in the Atlantic: a synthesis based on in situ data from the last decade , 2002 .

[20]  P. Herman,et al.  Tidal migration of nematodes on an estuarine tidal flat (the Molenplaat, Schelde Estuary, SW Netherlands) , 2001 .

[21]  C. Heip,et al.  Vertical distribution of meiofauna in sediments from contrasting sites in the adriatic sea: Clues to the role of abiotic versus biotic control , 2000 .

[22]  P. Herman,et al.  Predation rates and prey selectivity in two predacious estuarine nematode species , 2000 .

[23]  M. Vincx,et al.  Linking estuarine nematodes to their suspected food. A case study from the Westerschelde Estuary (south-west Netherlands) , 1999, Journal of the Marine Biological Association of the United Kingdom.

[24]  M. Vincx,et al.  Feeding biology of a predatory and a facultatively predatory nematode (Enoploides longispiculosus and Adoncholaimus fuscus) , 1999 .

[25]  E. Ólafsson,et al.  Responses of Baltic benthic invertebrates to hypoxic events , 1998 .

[26]  M. Vincx,et al.  Observations on the Feeding Ecology of Estuarine Nematodes , 1997, Journal of the Marine Biological Association of the United Kingdom.

[27]  R. Kuhn,et al.  Microhabitats of salt marsh foraminifera: St. Catherines Island, Georgia, USA , 1995 .

[28]  Y. Shirayama,et al.  Weight-dependent respiration rates in deep-sea organisms , 1995 .

[29]  K. Soetaert,et al.  Spatial patterns of Westerschelde meiobenthos , 1994 .

[30]  J. Labat,et al.  A Simulation Model of a Deep Meiobenthic Compartment: A Preliminary Approach , 1993 .

[31]  P. Jensen,et al.  Vertical Distribution of the Nematode Fauna in a Coastal Sediment Influenced by Seasonal Hypoxia in the Bottom Water , 1993 .

[32]  L. Moodley,et al.  Tolerance of Infaunal Benthic Foraminifera for Low and High Oxygen Concentrations. , 1992, The Biological bulletin.

[33]  E. Powell Oxygen, sulfide and diffusion: Why thiobiotic meiofauna must be sulfide-insensitive first-order respirers , 1989 .

[34]  H. Thiel,et al.  Introduction to the study of meiofauna , 1989 .

[35]  K. Reise Tidal Flat Ecology: An Experimental Approach to Species Interactions , 1985 .

[36]  C. Heip,et al.  Problems in meiofauna energy-flow studies , 1984, Hydrobiologia.

[37]  K. Reise,et al.  A meiofaunal “thiobios” limited to the anaerobic sulfide system of marine sand does not exist , 1979 .

[38]  P. Calow,et al.  THE RELATIONSHIP BETWEEN RATION, REPRODUCTIVE EFFORT AND AGE-SPECIFIC MORTALITY IN THE EVOLUTION OF LIFE-HISTORY STRATEGIES-SOME OBSERVATIONS ON FRESHWATER TRICLADS , 1977 .

[39]  T. Fenchel Factors determining the distribution patterns of mud snails (Hydrobiidae) , 1975, Oecologia.

[40]  H. Atkinson The functional significance of the haemoglobin in a marine nematode, Enoplus brevis (Bastian). , 1975, The Journal of experimental biology.

[41]  W. Wieser,et al.  An ecophysiological study of some meiofauna species inhabiting a sandy beach at Bermuda , 1974 .

[42]  F. Schiemer,et al.  Respiration and anaerobiosis of free living nematodes from marine and limnic sediments , 1973 .

[43]  D. Cullen,et al.  Bioturbation of Superficial Marine Sediments by Interstitial Meiobenthos , 1973, Nature.

[44]  J. Nicol,et al.  The Biology of Marine Animals , 1968 .

[45]  W. Wieser,et al.  ECOLOGICAL AND PHYSIOLOGICAL STUDIES ON MARINE NEMATODES FROM A SMALL SALT MARSH NEAR WOODS HOLE, MASSACHUSETTS1 , 1961 .

[46]  W. Wieser BENTHIC STUDIES IN BUZZARDS BAY II. THE MEIOFAUNA1 , 1960 .

[47]  P. Herman,et al.  A Practical Guide to Ecological Modelling , 2009 .

[48]  Andreas ahn'l Physiological adaptations of Cyprideis torosa ( Crustacea , Ostracoda ) to hydrogen sulphide , 2006 .

[49]  S. Gerlach On the importance of marine meiofauna for benthos communities , 2004, Oecologia.

[50]  R. Warwick The influence of temperature and salinity on energy partitioning in the marine nematode Diplolaimelloides bruciei , 2004, Oecologia.

[51]  Karline Soetaert,et al.  On the oxidation and burial of organic carbon in sediments of the Iberian margin and Nazaré Canyon (NE Atlantic) , 2002 .

[52]  M. Vincx,et al.  Temperature, salinity and food thresholds in two brackish-water bacterivorous nematode species: assessing niches from food absorption and respiration experiments , 2000 .

[53]  S. Goldstein,et al.  Taphofacies implications of infaunal foraminiferal assemblages in a Georgia salt marsh, Sapelo Island , 1993 .

[54]  T. Blackburn,et al.  Nitrogen cycling in coastal marine environments , 1988 .

[55]  F. D. Bovee Biomasse et équivalents énergétiques des nématodes libres marins , 1987 .

[56]  K. Reise Macrofauna Promotes Meiofauna , 1985 .

[57]  Karsten Reise,et al.  Tidal Flat Ecology , 1985, Ecological Studies.

[58]  W. Wieser,et al.  The ecophysiology of some marine nematodes from Bermuda: Seasonal aspects , 1977 .

[59]  R. Newell,et al.  Biology of intertidal animals , 1970 .

[60]  M. Brzeski,et al.  The determination of volume and weight of nematodes. , 1967 .