Anthony F. Michaels

Nitrogen fixation: Anthropogenic enhancement‐environmental response

In the absence of human activities, biotic fixation is the primary source of reactive N, providing about 90–130 Tg N yr−1 (Tg = 1012 g) on the continents. Human activities have resulted in the fixation of an additional ≈140 Tg N yr−1 by energy production (≈20 Tg N yr−1 ), fertilizer production (≈80 Tg N yr−1), and cultivation of crops (e.g., legumes, rice) (≈40 Tg N yr−1 ). We can only account for part of this anthropogenic N. N2O is accumulating in the atmosphere at a rate of 3 Tg N yr−1. Coastal oceans receive another 41 Tg N yr−1 via rivers, much of which is buried or denitrified. Open oceans receive 18 Tg N yr−1 by atmospheric deposition, which is incorporated into oceanic N pools (e.g., NO3−, N2). The remaining 80 Tg N yr−1 are either retained on continents in groundwater, soils, or vegetation or denitrified to N2. Field studies and calculations indicate that uncertainties about the size of each sink can account for the remaining anthropogenic N. Thus although anthropogenic N is clearly accumulating on continents, we do not know rates of individual processes. We predict the anthropogenic N-fixation rate will increase by about 60% by the year 2020, primarily due to increased fertilizer use and fossil-fuel combustion. About two-thirds of the increase will occur in Asia, which by 2020 will account for over half of the global anthropogenic N fixation.

Influence of mesoscale eddies on new production in the Sargasso Sea

It is problematic that geochemical estimates of new production — that fraction of total primary production in surface waters fuelled by externally supplied nutrients — in oligotrophic waters of the open ocean surpass that which can be sustained by the traditionally accepted mechanisms of nutrient supply., In the case of the Sargasso Sea, for example, these mechanisms account for less than half of the annual nutrient requirement indicated by new production estimates based on three independent transient-tracer techniques. Specifically, approximately one-quarter to one-third of the annual nutrient requirement can be supplied by entrainment into the mixed layer during wintertime convection, with minor contributions from mixing in the thermocline, and wind-driven transport (the potentially important role of nitrogen fixation — for which estimates vary by an order of magnitude in this region — is excluded from this budget). Here we present four lines of evidence — eddy-resolving model simulations, high-resolution observations from moored instrumentation, shipboard surveys and satellite data — which suggest that the vertical flux of nutrients induced by the dynamics of mesoscale eddies is sufficient to balance the nutrient budget in the Sargasso Sea.

Dinitrogen fixation in the world's oceans

The surface water of themarine environment has traditionally beenviewed as a nitrogen (N) limited habitat, andthis has guided the development of conceptualbiogeochemical models focusing largely on thereservoir of nitrate as the critical source ofN to sustain primary productivity. However,selected groups of Bacteria, includingcyanobacteria, and Archaea canutilize dinitrogen (N2) as an alternativeN source. In the marine environment, thesemicroorganisms can have profound effects on netcommunity production processes and can impactthe coupling of C-N-P cycles as well as the netoceanic sequestration of atmospheric carbondioxide. As one component of an integrated ‘Nitrogen Transport and Transformations’ project, we have begun to re-assess ourunderstanding of (1) the biotic sources andrates of N2 fixation in the worldsoceans, (2) the major controls on rates ofoceanic N2 fixation, (3) the significanceof this N2 fixation for the global carboncycle and (4) the role of human activities inthe alteration of oceanic N2 fixation. Preliminary results indicate that rates ofN2 fixation, especially in subtropical andtropical open ocean habitats, have a major rolein the global marine N budget. Iron (Fe)bioavailability appears to be an importantcontrol and is, therefore, critical inextrapolation to global rates of N2fixation. Anthropogenic perturbations mayalter N2 fixation in coastal environmentsthrough habitat destruction and eutrophication,and open ocean N2 fixation may be enhancedby warming and increased stratification of theupper water column. Global anthropogenic andclimatic changes may also affect N2fixation rates, for example by altering dustinputs (i.e. Fe) or by expansion ofsubtropical boundaries. Some recent estimatesof global ocean N2 fixation are in therange of 100–200 Tg N (1–2 × 1014 g N)yr−1, but have large uncertainties. Theseestimates are nearly an order of magnitudegreater than historical, pre-1980 estimates,but approach modern estimates of oceanicdenitrification.

Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry

The Bermuda Atlantic Time-series Study (BATS) commenced monthly sampling in October 1988 as part of the US Joint Global Ocean Flux Study (JGOFS) program. The goals of the US JGOFS time-series research are to better understand the basic processes that control ocean biogeochemistry on seasonal to decadal time-scales, determine the role of the oceans in the global carbon budget, and ultimately improve our ability to predict the effects of climate change on ecosystems. The BATS program samples the ocean on a biweekly to monthly basis, a strategy that resolves major seasonal patterns and interannual variability. The core cruises last 4-5 d during which hydrography, nutrients, particle flux, pigments and primary production, bacterioplankton abundance and production, and often complementary ancillary measurements are made. This overview focuses on patterns in ocean biology and biogeochemistry over a decade at the BATS site, concentrating on seasonal and interannual changes in community structure, and the physical forcing and other factors controlling the temporal dynamics. Significant seasonal and interannual variability in phytoplankton and bacterioplankton production, biomass, and community structure exists at BATS. No strong relationship exists between primary production and particle flux during the 10 yr record, with the relationship slightly improved by applying an artificial lag of 1 week between production and flux. The prokaryotic picoplankton regularly dominate the phytoplankton community; diatom blooms are rare but occur periodically in the BATS time series. The increase in Chi a concentrations during bloom periods is due to increases by most of the taxa present, rather than by any single group, and there is seasonal succession of phytoplankton. The bacterioplankton often dominate the living biomass, indicating the potential to consume large amounts of carbon and play a major ecological role within the microbial food web. Bacterial biomass, production, and specific growth rates are highest during summer. Size structure and composition of the plankton community may be an important factor controlling the quality of dissolved organic matter produced and could affect production of bacterioplankton biomass. Larger heterotrophic plankton play an integral role in the flux of material out of the euphotic zone at BATS. Protozoans are abundant and can constitute a sizable component of sinking flux. Zooplankton contribute significantly to flux via production of rapidly sinking fecal pellets, and vertically migrating zooplankton can actively transport a significant amount of dissolved organic and inorganic carbon and nitrogen to deep water. An important question that remains to be further addressed at BATS is how larger climatological events drive some of the interannual variability in the biogeochemistry

Primary production, sinking fluxes and the microbial food web

Abstract The size distribution of pelagic producers and the size and trophic position of consumers determine the composition and magnitude of sinking fluxes from the surface communities in a simple model of oceanic food webs. Picoplankton, the dominant producers in the model, contribute little to the sinking material, due primarily to the large number of trophic steps between picoplankton and the consumers that produce the sinking particles. Net phytoplankton are important contributors to the sinking materials, despite accounting for a small fraction of the total primary production. These net phytoplankton, especially those capable of nitrogen fixation, also dominate the fraction of the new production that is exported on its first pass through the food chain. The sinking flux is strongly determined by the community structure of the consumers and varies by an order of magnitude for different food webs. The model indicates that generalist grazers, zooplankton that consume a broad size spectrum of prey (including pico-and nanoplankton), play a critical role in exporting particles. The role of generalists that occasionally form swarms, such as thaliaceans (salps and doliolids), can be particularly difficult to assess. Short-term studies probably miss the relatively infrequent population blooms of these grazers, events that could control the average, long-term exports from surface oceanic communities.

An assessment of the use of sediment traps for estimating upper ocean particle fluxes

This review provides an assessment of sediment trap accuracy issues by gathering data to address trap hydrodynamics, the problem of zooplankton “swimmers,” and the solubilization of material after collection. For each topic, the problem is identified, its magnitude and causes reviewed using selected examples, and an update on methods to correct for the potential bias or minimize the problem using new technologies is presented. To minimize hydrodynamic biases due to flow over the trap mouth, the use of neutrally buoyant sediment traps is encouraged. The influence of swimmers is best minimized using traps that limit zooplankton access to the sample collection chamber. New data on the impact of different swimmer removal protocols at the US time-series sites HOT and BATS are compared and shown to be important. Recent data on solubilization are compiled and assessed suggesting selective losses from sinking particles to the trap supernatant after collection, which may alter both fluxes and ratios of elements in long term and typically deeper trap deployments. Different methods are needed to assess shallow and short- term trap solubilization effects, but thus far new incubation experiments suggest these impacts to be small for most elements. A discussion of trap calibration methods reviews independent assessments of flux, including elemental budgets, particle abundance and flux modeling, and emphasizes the utility of U-Th radionuclide calibration methods.

Zooplankton vertical migration and the active transport of dissolved organic and inorganic carbon in the Sargasso Sea

The least known component of the “biological pump” is the active transport of carbon and nutrients by diel vertical migration of zooplankton. We measured CO2 respiration and dissolved organic carbon (DOC) excretion by individual species of common vertically migrating zooplankton at the US JGOFS Bermuda Atlantic Time-series Study (BATS) station. The inclusion of DOC excretion in this study builds on published research on active transport by respiration of inorganic carbon and allows a direct assessment of the role of zooplankton in the production of dissolved organic matter used in midwater microbial processes. On average, excretion of DOC makes up 24% (range=5–42%) of the total C metabolized (excreted+respired) and could represent a significant augmentation to the vertical flux that has already been documented for respiratory CO2 flux by migrant zooplankton. Migratory fluxes were compared to other transport processes at BATS. Estimates of combined active transport of CO2 and DOC by migrators at BATS averaged 7.8% and reached 38.6% of mean sinking POC flux at 150 m, and reached 71.4% of mean sinking POC flux at 300 m. DOC export by migrator excretion averaged 1.9% and reached 13.3% of annual DOC export by physical mixing at this site. During most of the year when deep mixing does not occur, diel migration by zooplankton could provide a supply of DOC to the deeper layers that is available for use by the microbial community. A carbon budget comparing migrant zooplankton transport to the balance of fluxes in the 300–600 m depth strata at BATS shows on average that the total migrant flux supplies 37% of the organic carbon remineralized in this layer, and that migrant DOC flux is more than 3 times the DOC flux gradient by diapycnal mixing. New estimates of active transport of both organic and inorganic carbon by migrants may help resolve observed imbalances in the C budget at BATS, but the magnitude is highly dependent on the biomass of the migrating community.

Inputs, losses and transformations of nitrogen and phosphorus in the pelagic North Atlantic Ocean

The North Atlantic Ocean receives the largest allochthonous supplies of nitrogen of any ocean basin because of the close proximity of industrialized nations. In this paper, we describe the major standing stocks, fluxes and transformations of nitrogen (N) and phosphorus (P) in the pelagic regions of the North Atlantic, as one part of a larger effort to understand the entire N and P budgets in the North Atlantic Ocean, its watersheds and overlying atmosphere. The primary focus is on nitrogen, however, we consider both nitrogen and phosphorus because of the close inter-relationship between the N and P cycles in the ocean. The oceanic standing stocks of N and P are orders of magnitude larger than the annual amount transported off continents or deposited from the atmosphere. Atmospheric deposition can have an impact on oceanic nitrogen cycling at locations near the coasts where atmospheric sources are large, or in the centers of the highly stratified gyres where little nitrate is supplied to the surface by vertical mixing of the ocean. All of the reactive nitrogen transported to the coasts in rivers is denitrified or buried in the estuaries or on the continental shelves and an oceanic source of nitrate of 0.7–0.95 × 1012 moles NO3−1 y−1 is required to supply the remainder of the shelf denitrification (Nixon et al., this volume). The horizontal fluxes of nitrate caused by the ocean circulation are both large and uncertain. Even the sign of the transport across the equator is uncertain and this precludes a conclusion on whether the North Atlantic Ocean as a whole is a net source or sink of nitrate. We identify a source of nitrate of 3.7–6.4 × 1012 moles NO3− y−1 within the main thermocline of the Sargasso Sea that we infer is caused by nitrogen fixation. This nitrate source may explain the nitrate divergence observed by Rintoul & Wunsch (1991) in the mid-latitude gyre. The magnitude of nitrogen fixation inferred from this nitrate source would exceed previous estimates of global nitrogen fixation. Nitrogen fixation requires substantial quantities of iron as a micro-nutrient and the calculated iron requirement is comparable to the rates supplied by the deposition of iron associated with Saharan dust. Interannual variability in dust inputs is large and could cause comparable signals in the nitrogen fixation rate. The balance of the fluxes across the basin boundaries suggest that the total stocks of nitrate and phosphate in the North Atlantic may be increasing on time-scales of centuries. Some of the imbalance is related to the inferred nitrogen fixation in the gyre and the atmospheric deposition of nitrogen, both of which may be influenced by human activities. However, the fluxes of dissolved organic nutrients are almost completely unknown and they have the potential to alter our perception of the overall mass balance of the North Atlantic Ocean.

Overview of the U.S. JGOFS Bermuda Atlantic Time-series Study and the Hydrostation S program

Abstract In October 1988 the Bermuda Atlantic Time-series Study (BATS) commenced sampling the Sargasso Sea in an area 85 km south-east of Bermuda as part of the U.S. Joint Global Ocean Flux Study (JGOFS). The scientific goal of the BATS program is to understand the causes of seasonal and interannual variability in ocean biogeochemistry both at this site and as it may relate to biogeochemistry of the rest of the ocean. Bermuda is also the site of other continuing and historical oceanic and atmospheric time-series programs. The ongoing Hydrostation S time-series commenced in 1954 and the biweekly profiles of temperature, salinity and oxygen provide data to link the more recent biogeochemistry time-series studies to the decadal variability in this region. Data on midwater particle fluxes have been collected continuously since 1976, ongoing measurements of atmospheric chemistry and wet and dry deposition began in 1980 and a long-term study of benthic boundary fluxes began in 1986. These various time-series studies complement each other and combine to make this region one of the most heavily documented oceanic environments in the world. The BATS and Hydrostation S programs each sample the ocean on a biweekly-to-monthly basis, a strategy that resolves the major seasonal patterns, interannual variability and decadal patterns. The Sargasso Sea also has more episodic or local processes, such as fluctuations that occur on scales of days to weeks and mesoscale eddies, and potentially patterns from the net advection of water past the sampling sites; these processes are more difficult to resolve by the one-dimensional time-series sampling strategy. The BATS program has begun to provide a coherent picture of the oceanic carbon and nutrient cycles in this region and the linkage between these cycles and the biological, chemical, physical and optical processes that control them. The significant interannual and decadal variability in the physical environment near Bermuda also allows us to examine the longer-term relationships between the physical forcing and biogeochemical response. Finally, the BATS program has proved a valuable platform to support other ancillary oceanographic research and technology development. These studies all benefit from the existence of the core time-series studies to add context and value to their more specific research efforts and they, in turn, further enhance the diversity of co-located measurements in this area.

Seasonal patterns of ocean biogeochemistry at the U.S. JGOFS Bermuda Atlantic time-series study site

Seasonal patterns in hydrography, oxygen, nutrients, particulate carbon and nitrogen and pigments were measured on monthly cruises at the Bermuda Atlantic Time-series Study site, 80 km southeast of Bermuda. Between October 1988 and September 1990, the annual cycle was defined by the creation of 160–230 m-deep mixed layers in February of each year and a transition to strong thermal stratification in summer and fall. The 230 m mixed layer in February 1989 resulted in mixed-layer nitrate concentrations of 0.5–1.0 μmole kg−1, carbon fixation rates over 800 mg C m−2 day−1, and a phytoplankton bloom with chlorophyll concentrations over 0.4 mg m−3. Chlorophyll a, particulate organic matter, inorganic nutrients and primary production had returned to prebloom levels the following month with the exception of a chlorophyll maximum layer at 100 m. Particle fluxes at 150 m in February 1989 reached 56 mg C m−2 day−1 and 11 mg N m−2 day−1 (0.77 mmole N m−2 day−1). Estimates of new production during the bloom period calculated from changes in oxygen and nitrate profiles ranged from 100 to 240 mmoles N m−2, significantly higher than the sediment trap fluxes and approaching the measured total production rates. In spring of 1990, mixed layer depths did not exceed 160 m, nitrate was rarely detectable in the upper euphotic zone, chlorophyll a concentrations were similar to 1989, and particulate organic matter concentrations were lower. The period of elevated biomass lasted for 3 months in 1990, and phytoplankton pigment composition varied between cruises. The average rates of primary production and particle flux were higher in 1990 than those measured in the spring of 1989, despite the differences in mixed layer depth. Throughout both years, NO3 : PO4 ratios in the upper thermocline exceeded Redfield ratios. The maintenance of this pattern requires a net uptake of PO4 between 150 and 250 m, a depth range usually associated with net remineralization. The exact mechanism that maintains elevated PO4 uptake and its implication for the nutrient supply to the euphotic zone remain unknown.