In Situ Coral Reef Oxygen Metabolism: An Eddy Correlation Study

Quantitative studies of coral reefs are challenged by the three-dimensional hard structure of reefs and the high spatial variability and temporal dynamics of their metabolism. We used the non-invasive eddy correlation technique to examine respiration and photosynthesis rates, through O2 fluxes, from reef crests and reef slopes in the Florida Keys, USA. We assessed how the photosynthesis and respiration of different reef habitats is controlled by light and hydrodynamics. Numerous fluxes (over a 0.25 h period) were as high as 4500 mmol O2 m−2 d−1, which can only be explained by efficient light utilization by the phototrophic community and the complex canopy structure of the reef, having a many-fold larger surface area than its horizontal projection. Over diel cycles, the reef crest was net autotrophic, whereas on the reef slope oxygen production and respiration were balanced. The autotrophic nature of the shallow reef crests implies that the export of organics is an important source of primary production for the larger area. Net oxygen production on the reef crest was proportional to the light intensity, up to 1750 µmol photons m−2 s−1 and decreased thereafter as respiration was stimulated by high current velocities coincident with peak light levels. Nighttime respiration rates were also stimulated by the current velocity, through enhanced ventilation of the porous framework of the reef. Respiration rates were the highest directly after sunset, and then decreased during the night suggesting that highly labile photosynthates produced during the day fueled early-night respiration. The reef framework was also important to the acquisition of nutrients as the ambient nitrogen stock in the water had sufficient capacity to support these high production rates across the entire reef width. These direct measurements of complex reefs systems yielded high metabolic rates and dynamics that can only be determined through in situ, high temporal resolution measurements.

[1]  Alfred Wüest,et al.  Variable sediment oxygen uptake in response to dynamic forcing , 2010 .

[2]  P. Cook,et al.  Advective relief of CO2 limitation in microphytobenthos in highly productive sandy sediments , 2006 .

[3]  M. Kühl,et al.  MICROENVIRONMENTAL CONTROL OF PHOTOSYNTHESIS AND PHOTOSYNTHESIS‐COUPLED RESPIRATION IN AN EPILITHIC CYANOBACTERIAL BIOFILM 1 , 1996 .

[4]  P. Berg,et al.  A comparison and correction of light intensity loggers to photosynthetically active radiation sensors , 2012 .

[5]  B. Jørgensen,et al.  Oxygen uptake by aquatic sediments measured with a novel non-invasive eddy-correlation technique , 2003 .

[6]  P. Berg,et al.  Benthic O2 exchange across hard-bottom substrates quantified by eddy correlation in a sub-Arctic fjord , 2010 .

[7]  P. Glynn Ecology of a Caribbean coral reef. The Porites reef-flat biotope: Part II. Plankton community with evidence for depletion , 1973 .

[8]  R. Bak,et al.  Coral reef framework cavities: is functional similarity reflected in composition of the cryptic macrofaunal community , 2010 .

[9]  D. Tchernov,et al.  Flow enhances photosynthesis in marine benthic autotrophs by increasing the efflux of oxygen from the organism to the water , 2010, Proceedings of the National Academy of Sciences.

[10]  Stephen R. Carpenter,et al.  Persistence of net heterotrophy in lakes during nutrient addition and food web manipulations , 2000 .

[11]  R. R. Olson,et al.  In situ measurements of flow effects on primary production and dark respiration in reef corals , 1991 .

[12]  N. Revsbech,et al.  An oxygen microsensor with a guard cathode , 1989 .

[13]  P. Berg,et al.  Monitoring the Seafloor Using the Noninvasive Eddy Correlation Technique: Integrated Benthic Exchange Dynamics , 2008 .

[14]  R. Galzin Structure of fish communities of French Polynesian coral reefs . I . Spatial scales , 2006 .

[15]  J. Faganeli,et al.  Semi-annual carbon and nitrogen isotope variations in the water column of Lake Bled, NW Slovenia , 2012 .

[16]  P. Berg,et al.  Eddy correlation measurements of oxygen uptake in deep ocean sediments , 2009 .

[17]  Z. Dubinsky,et al.  PHOTOSYNTHESIS AND RESPIRATION OF THE ZOOXANTHELLAE IN HERMATYPIC CORALS HABITATED ON DIFFERENT DEPTHS OF THE GULF OF FILAT , 1996 .

[18]  D. Wethey,et al.  Intracolony variability in photosynthesis by corals is affected by water flow: role of oxygen flux , 2007 .

[19]  S. V. Smith,et al.  C:N:P ratios of benthic marine plants1 , 1983 .

[20]  J. Gattuso,et al.  Carbon fluxes in coral reefs. I. Lagrangian measurement of community metabolism and resulting air-sea CO2 disequilibrium , 1996 .

[21]  J. Gattuso,et al.  CARBON AND CARBONATE METABOLISM IN COASTAL AQUATIC ECOSYSTEMS , 1998 .

[22]  N. Gassman,et al.  The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis , 1990, Coral Reefs.

[23]  W. Dunlap,et al.  Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef, Australia. II. Light saturation curves for photosynthesis and respiration , 1983 .

[24]  W. McGillis,et al.  Productivity of a coral reef using boundary layer and enclosure methods , 2011 .

[25]  A. Dahl Surface area in ecological analysis: Quantification of benthic coral-reef algae , 1973 .

[26]  Ryan J. Lowe,et al.  Continuous measurements of net production over a shallow reef community using a modified Eulerian approach , 2008 .

[27]  H. Seim,et al.  Measurements of Reynolds stress in a wind-driven lagoonal estuary , 2006 .

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

[29]  M. Huettel,et al.  Advective pore‐water exchange driven by surface gravity waves and its ecological implications , 2003 .

[30]  R. Jovin,et al.  Estimation of the photosynthesis/irradiance (P/I) curve parameters from light and dark bottle experiments , 1997 .

[31]  D. Kinsey Metabolism, calcification and carbon production. I. System level studies , 1985 .

[32]  V. Kitidis,et al.  Impact of ocean acidification on benthic and water column ammonia oxidation , 2011 .

[33]  Hideo Yamasaki,et al.  Photoinhibition of photosynthesis is reduced by water flow in the reef-building coral Acropora digitifera , 2005 .

[34]  Michael P. Lesser,et al.  Diurnal and bathymetric changes in chlorophyll fluorescence yields of reef corals measured in situ with a fast repetition rate fluorometer , 2001 .

[35]  T. Ayukai Retention of phytoplankton and planktonic microbes on coral reefs within the Great Barrier Reef, Australia , 1995, Coral Reefs.

[36]  B. Law,et al.  Handbook of Micrometeorology , 2005 .

[37]  Mohammed Rasheed,et al.  Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges , 2001, Nature.

[38]  S. Monismith,et al.  Intense benthic grazing of phytoplankton in a coral reef , 2009 .

[39]  S. Monismith,et al.  Boundary layer turbulence and flow structure over a fringing coral reef , 2006 .

[40]  J. Trowbridge ON A TECHNIQUE FOR MEASUREMENT OF TURBULENT SHEAR STRESS IN THE PRESENCE OF SURFACE WAVES , 1998 .

[41]  K. Anthony,et al.  Energetic cost of photoinhibition in corals , 2006 .

[42]  M. Kühl,et al.  Light utilization efficiency in photosynthetic microbial mats. , 2012, Environmental microbiology.

[43]  B. Eyre,et al.  Breathing of a coral cay: tracing tidally driven seawater recirculation in permeable coral reef sediments , 2010 .

[44]  Ryan J. Lowe,et al.  Short-term coherency between gross primary production and community respiration in an algal-dominated reef flat , 2011, Coral Reefs.

[45]  Z. Dubinsky,et al.  Ratio of Energy and Nutrient Fluxes Regulates Symbiosis between Zooxanthellae and Corals , 1994 .

[46]  R. Galzin Structure of fish communities of French Polynesian coral reefs. II. Temporal scales , 1987 .

[47]  P. Berg,et al.  Dissolved oxygen fluxes and ecosystem metabolism in an eelgrass (Zostera marina) meadow measured with the eddy correlation technique , 2011 .

[48]  T. Binzer,et al.  Community photosynthesis of aquatic macrophytes , 2006 .

[49]  Zvy Dubinsky,et al.  Diurnal hysteresis in coral photosynthesis , 2004 .

[50]  O. Hoegh‐Guldberg,et al.  Variation in coral photosynthesis, respiration and growth characteristics in contrasting light microhabitats: an analogue to plants in forest gaps and understoreys? , 2003 .

[51]  Trevor Platt,et al.  Mathematical formulation of the relationship between photosynthesis and light for phytoplankton , 1976 .

[52]  A. Christopoulos,et al.  Fitting Models to Biological Data Using Linear and Nonlinear Regression: A Practical Guide to Curve Fitting , 2004 .

[53]  Johanna H. Rosman,et al.  Extracting Reynolds Stresses from Acoustic Doppler Current Profiler Measurements in Wave-Dominated Environments , 2008 .

[54]  J. Erez,et al.  In situ diel cycles of photosynthesis and calcification in hermatypic corals , 2009 .

[55]  S. V. Smith,et al.  Coral-reef area and the contributions of reefs to processes and resources of the world's oceans , 1978, Nature.

[56]  T. Binzer,et al.  Scaling of photosynthetic production of aquatic macrophytes – a review , 2007 .

[57]  C. Langdon,et al.  Production‐respiration relationships at different timescales within the Biosphere 2 coral reef biome , 2001 .

[58]  Ronald D. Jones,et al.  A rapid, precise and sensitive method for the determination of total nitrogen in natural waters , 1998 .

[59]  P. Berg,et al.  Benthic oxygen consumption rates during hypoxic conditions on the Oregon continental shelf: Evaluation of the eddy correlation method , 2012 .

[60]  S. G. Nelson,et al.  Effect of elevated CO2 on the community metabolism of an experimental coral reef , 2003 .

[61]  Steven B. Kraines,et al.  Separating biological and physical changes in dissolved oxygen concentration in a coral reef , 1996 .

[62]  P. Berg,et al.  Eddy correlation flux measurements: The sediment surface area that contributes to the flux , 2007 .

[63]  P. Berg,et al.  Oxygen exchange and ice melt measured at the ice-water interface by eddy correlation , 2011 .

[64]  John Finnigan,et al.  Coordinate Systems and Flux Bias Error , 2004 .