Technical note: Estimating light-use efficiency of benthic habitats using underwater O2 eddy covariance

Light-use efficiency defines the ability of primary producers to convert sunlight energy to primary production and is computed as the ratio between the gross primary production and the intercepted photosynthetic active radiation. While this measure has been applied broadly within terrestrial ecology to investigate habitat resource-use efficiency, it remains underused within the aquatic realm. This report provides a conceptual framework to compute hourly and daily light-use efficiency using underwater O-2 eddy covariance, a recent technological development that produces habitat-scale rates of primary production under unaltered in situ conditions. The analysis, tested on two benthic flux datasets, documents that hourly light-use efficiency may approach the theoretical limit of 0.125 O-2 per photon under low-light conditions, but it decreases rapidly towards the middle of the day and is typically 10-fold lower on a 24 h basis. Overall, light- use efficiency provides a useful measure of habitat functioning and facilitates site comparison in time and space.Peer reviewe

Fixed-Nitrogen Loss Associated with Sinking Zooplankton Carcasses in a Coastal Oxygen Minimum Zone (Golfo Dulce, Costa Rica)

Oxygen minimum zones (OMZs) in the ocean are of key importance for pelagic fixed-nitrogen loss (N-loss) through microbial denitrification and anaerobic ammonium oxidation (anammox). Recent studies document that zooplankton is surprisingly abundant in and around OMZs and that the microbial community associated with carcasses of a large copepod species mediates denitrification. Here, we investigate the complex N-cycling associated with sinking zooplankton carcasses exposed to the steep O2 gradient in a coastal OMZ (Golfo Dulce, Costa Rica). 15N-stable-isotope enrichment experiments revealed that the carcasses of abundant copepods and ostracods provide anoxic microbial hotspots in the pelagic zone by hosting intense anaerobic N-cycle activities even in the presence of ambient O2. Carcass-associated anaerobic N-cycling was clearly dominated by dissimilatory nitrate reduction to ammonium (DNRA) at up to 30.8 nmol NH4+ individual−1 d−1, followed by denitrification (up to 10.8 nmol N2-N individual−1 d−1), anammox (up to 1.6 nmol N2-N individual−1 d−1), and N2O production (up to 1.2 nmol N2O-N individual−1 d−1). In contrast, anaerobic N-cycling mediated by free-living bacteria proceeded mainly through anammox and denitrification in the anoxic bottom water, which underpins the distinctive microbial metabolism associated with zooplankton carcasses. Pelagic N-loss is potentially enhanced by zooplankton carcasses both directly through N2 and N2O production, and indirectly through NH4+ production that may fuel free-living anammox bacteria. We estimate that in the hypoxic water layer of Golfo Dulce, carcass-associated N2 and N2O production enhance N-loss as much as 1.4-fold at a relative carcass abundance of 36%. In the anoxic bottom water, however, N-loss is likely enhanced only marginally due to high ambient rates and low zooplankton abundance. Thus, zooplankton carcasses may enhance N-loss mainly at the hypoxic boundaries of OMZs which are usually more extensive in open-ocean than in coastal settings. Notably, these contributions by zooplankton carcasses to pelagic N-loss remain undetected by conventional, incubation-based rate measurements

Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater

Submergence during germination impedes aerobic metabolisms and limits the growth of most higher plants. However, some wetland plants including rice can germinate under submerged conditions. It has long been hypothesized that the first elongating shoot tissue, the coleoptile, acts as a snorkel to acquire atmospheric oxygen (O2) to initiate the first leaf elongation and seminal root emergence. Here, we obtained direct evidence for this hypothesis by visualizing the spatiotemporal O2 dynamics during submerged germination in rice using a planar O2 optode system. In parallel with the O2 imaging, we tracked the anatomical development of shoot and root tissues in real-time using an automated flatbed scanner. Three hours after the coleoptile tip reached the water surface, O2 levels around the embryo transiently increased. At this time, the activity of alcohol dehydrogenase (ADH), an enzyme critical for anaerobic metabolism, was significantly reduced, and the coleorhiza covering the seminal roots in the embryo was broken. Approximately 10 h after the transient burst in O2, seminal roots emerged. A transient O2 burst around the embryo was shown to be essential for seminal root emergence during submerged rice germination. The parallel application of a planar O2 optode system and automated scanning system can be a powerful tool for examining how environmental conditions affect germination in rice and other plants

Seasonal rates of benthic primary production in a Greenland fjord measured by aquatic eddy correlation

We present the first year-round estimates of benthic primary production at four contrasting shallow (3–22 m depth) benthic habitats in a southwest Greenland fjord. In situ measurements were performed using the noninvasive aquatic eddy-correlation (EC) oxygen (O2) flux method. A series of high-quality multiple-day EC data sets document the presence of a year-round productive benthic phototrophic community. The shallow-water sites were on average autotrophic during the spring and summer months, up to 43.6 mmol O2 m22 d21, and heterotrophic or close to metabolic balance during the autumn and winter. Substantial benthic gross primary production (GPP) was measured year-round. The highest GPP rates were measured during the spring, up to 5.7 mmol O2 m22 h21 (136.8 mmol O2 m22 d21), and even at low light levels (, 80 mmol quanta m22 s21) during late autumn and winter we measured rates of up to 1.8 mmol O2 m22 h21 (43.2 mmol O2 m22 d21) during peak irradiance. The benthic phototrophic communities responded seasonally to ambient light levels and exhibited year-round high photosynthetic efficiency. In situ downwelling irradiances as low as , 2 mmol quanta m22 s21 induced an autotrophic response and light saturation indices (Ik) were as low as 11 mmol quanta m22 s21 in the winter. On an annual timescale, the average areal rate of benthic GPP was 11.5 mol O2 m22 yr21, which is , 1.4 times higher than the integrated gross pelagic primary production of the , 30–50 m deep photic zone of the fjord. These results document the importance of benthic photosynthesis on an ecosystem level and indicate that the benthic phototrophic compartment should be accounted for when assessing carbon and nutrient budgets as well as responses of coastal Arctic ecosystems to climate change

Sediment oxygen consumption: Role in the global marine carbon cycle

The seabed plays a key role in the marine carbon cycle as a) the terminal location of aerobic oxidation of organic matter, b) the greatest anaerobic bioreactor, and c) the greatest repository for reactive organic carbon on Earth. We compiled data on the oxygen uptake of marine sediments with the objective to understand the constraints on mineralization rates of deposited organic matter and their relation to key environmental parameters. The compiled database includes nearly 4000 O 2 uptake data and is available as supplementary material. It includes also information on bottom water O 2 concentration, O 2 penetration depth, geographic position, water depth, and full information on the data sources. We present the different in situ and ex situ approaches to measure the total oxygen uptake (TOU) and the diffusive oxygen uptake (DOU) of sediments and discuss their robustness towards methodological errors and statistical uncertainty. We discuss O 2 transport through the benthic and diffusive boundary layers, the diffusion- and fauna-mediated O 2 uptake, and the coupling of aerobic respiration to anaerobic processes. Five regional examples are presented to illustrate the diversity of the seabed: Eutrophic seas, oxygen minimum zones, abyssal plains, mid-oceanic gyres, and hadal trenches. A multiple correlation analysis shows that seabed O 2 uptake is primarily controlled by ocean depth and sea surface primary productivity. The O2 penetration depth scales with the DOU according to a power law that breaks down under the abyssal ocean gyres. The developed multiple correlation model was used to draw a global map of seabed O2 uptake rates. Respiratory coefficients, differentiated for depth regions of the ocean, were used to convert the global O 2 uptake to organic carbon oxidation. The resulting global budget shows an oxidation of 212 Tmol C yr − 1 in marine sediments with a 5-95% confidence interval of 175-260 Tmol C yr − 1 . A comparison with the global flux of particulate organic carbon (POC) from photic surface waters to the deep sea, determined from multiple sediment trap studies, suggests a deficit in the sedimentation flux at 2000 m water depth of about 70% relative to the carbon turnover in the underlying seabed. At the ocean margins, the flux of organic carbon from rivers and from vegetated coastal ecosystems contributes greatly to the budget and may even exceed the phytoplankton production on the inner continental shelf

Benthic oxygen exchange in a live coralline algal bed and an adjacent sandy habitat: an eddy covariance study

Coralline algal (maerl) beds are widespread, slow-growing, structurally complex perennial habitats that support high biodiversity, yet are significantly understudied compared to seagrass beds or kelp forests. We present the first eddy covariance (EC) study on a live maerl bed, assessing the community benthic gross primary productivity (GPP), respiration (R), and net ecosystem metabolism (NEM) derived from diel EC time series collected during 5 seasonal measurement campaigns in temperate Loch Sween, Scotland. Measurements were also carried out at an adjacent (~20 m distant) permeable sandy habitat. The O2 exchange rate was highly dynamic, driven by light availability and the ambient tidally-driven flow velocity. Linear relationships between the EC O2 fluxes and available light indicate that the benthic phototrophic communities were lightlimited. Compensation irradiance (Ec) varied seasonally and was typically ~1.8-fold lower at the maerl bed compared to the sand. Substantial GPP was evident at both sites; however, the maerl bed and the sand habitat were net heterotrophic during each sampling campaign. Additional inputs of ~4 and ~7 mol m-2 yr-1 of carbon at the maerl bed and sand site, respectively, were required to sustain the benthic O2 demand. Thus, the 2 benthic habitats efficiently entrap organic carbon and are sinks of organic material in the coastal zone. Parallel deployment of 0.1 m2 benthic chambers during nighttime revealed O2 uptake rates that varied by up to ~8-fold between replicate chambers (from -0.4 to -3.0 mmol O2 m-2 h-1; n = 4). However, despite extensive O2 flux variability on meter horizontal scales, mean rates of O2 uptake as resolved in parallel by chambers and EC were typically within 20% of one another

Microbial degradation dynamics of farmed kelp deposits from Saccharina latissima and Alaria esculenta

Seaweed farming is a growing industry worldwide, and its sustainable management requires detailed knowledge about the environmental implications of detrital release. This study investigates benthic degradation of kelp detritus in defaunated mesocosms. The degradation dynamics were investigated over several weeks by resolving O2 and dissolved inorganic carbon (DIC) fluxes as a function of detritus amendments (0.15 g wet weight [WW] m-2 to 1 kg WW m-2), temperature (8 and 15°C), and presence of O2 for 2 commercially important kelp species: Saccharina latissima and Alaria esculenta. Kelp fragments were deposited in 2 different ways to simulate oxic and anoxic degradation: on the sediment surface (surface amendments) and just below the oxic surface sediment layer (subsurface amendments). All amendments resulted in high initial O2 consumption followed by an exponential decrease in O2 uptake over time. The degradation rates increased linearly with the amount of kelp added for both species and for both types of amendments. S. latissima expressed higher decay constants across all experiments and had a higher percentage turnover of carbon. In some instances, microbial priming apparently enabled enhanced degradation of pre-existing resilient sedimentary carbon. The absolute degradation rates of kelp were reduced in the absence of O2, and sulfate reduction resulted in gradual accumulation of iron sulfide. Lower ambient temperature reduced the benthic mineralization rate of both kelp species, particularly during the initial incubation stages. The current study demonstrates the importance of key variables for microbial kelp degradation in marine sediments and their dynamics—variables that should be carefully considered when assessing environmental implications of seaweed farming.publishedVersio

Intracellular nitrate of marine diatoms as a driver of anaerobic nitrogen cycling in sinking aggregates

Diatom-bacteria aggregates are key for the vertical transport of organic carbon in the ocean. Sinking aggregates also represent pelagic microniches with intensified microbial activity, oxygen depletion in the center, and anaerobic nitrogen cycling. Since some of the aggregate-forming diatom species store nitrate intracellularly, we explored the fate of intracellular nitrate and its availability for microbial metabolism within anoxic diatom-bacteria aggregates. The ubiquitous nitrate-storing diatom Skeletonema marinoi was studied as both axenic cultures and laboratory-produced diatom-bacteria aggregates. Stable 15N isotope incubations under dark and anoxic conditions revealed that axenic S. marinoi is able to reduce intracellular nitrate to ammonium that is immediately excreted by the cells. When exposed to a light:dark cycle and oxic conditions, S. marinoi stored nitrate intracellularly in concentrations > 60 mmol L-1 both as free-living cells and associated to aggregates. Intracellular nitrate concentrations exceeded extracellular concentrations by three orders of magnitude. Intracellular nitrate was used up within 2-3 days after shifting diatom-bacteria aggregates to dark and anoxic conditions. Thirty-one percent of the diatom-derived nitrate was converted to nitrogen gas, indicating that a substantial fraction of the intracellular nitrate pool of S. marinoi becomes available to the aggregate-associated bacterial community. Only 5% of the intracellular nitrate was reduced to ammonium, while 59% was recovered as nitrite. Hence, aggregate-associated diatoms accumulate nitrate from the surrounding water and sustain complex nitrogen transformations, including loss of fixed nitrogen, in anoxic, pelagic microniches. Additionally, it may be expected that intracellular nitrate not converted before the aggregates have settled onto the seafloor could fuel benthic nitrogen transformations