A well-oxygenated eastern tropical Pacific during the warm Miocene.

The oxygen content of the oceans is susceptible to climate change and has declined in recent decades1, with the largest effect in oxygen-deficient zones (ODZs)2, that is, mid-depth ocean regions with oxygen concentrations <5 µmol kg-1 (ref. 3). Earth-system-model simulations of climate warming predict that ODZs will expand until at least 2100. The response on timescales of hundreds to thousands of years, however, remains uncertain3-5. Here we investigate changes in the response of ocean oxygenation during the warmer-than-present Miocene Climatic Optimum (MCO; 17.0-14.8 million years ago (Ma)). Our planktic foraminifera I/Ca and δ15N data, palaeoceanographic proxies sensitive to ODZ extent and intensity, indicate that dissolved-oxygen concentrations in the eastern tropical Pacific (ETP) exceeded 100 µmol kg-1 during the MCO. Paired Mg/Ca-derived temperature data suggest that an ODZ developed in response to an increased west-to-east temperature gradient and shoaling of the ETP thermocline. Our records align with model simulations of data from recent decades to centuries6,7, suggesting that weaker equatorial Pacific trade winds during warm periods may lead to decreased upwelling in the ETP, causing equatorial productivity and subsurface oxygen demand to be less concentrated in the east. These findings shed light on how warm-climate states such as during the MCO may affect ocean oxygenation. If the MCO is considered as a possible analogue for future warming, our findings seem to support models suggesting that the recent deoxygenation trend and expansion of the ETP ODZ may eventually reverse3,4.

Enhanced ocean oxygenation during Cenozoic warm periods.

Dissolved oxygen (O2) is essential for most ocean ecosystems, fuelling organisms' respiration and facilitating the cycling of carbon and nutrients. Oxygen measurements have been interpreted to indicate that the ocean's oxygen-deficient zones (ODZs) are expanding under global warming1,2. However, models provide an unclear picture of future ODZ change in both the near term and the long term3-6. The paleoclimate record can help explore the possible range of ODZ changes in warmer-than-modern periods. Here we use foraminifera-bound nitrogen (N) isotopes to show that water-column denitrification in the eastern tropical North Pacific was greatly reduced during the Middle Miocene Climatic Optimum (MMCO) and the Early Eocene Climatic Optimum (EECO). Because denitrification is restricted to oxygen-poor waters, our results indicate that, in these two Cenozoic periods of sustained warmth, ODZs were contracted, not expanded. ODZ contraction may have arisen from a decrease in upwelling-fuelled biological productivity in the tropical Pacific, which would have reduced oxygen demand in the subsurface. Alternatively, invigoration of deep-water ventilation by the Southern Ocean may have weakened the ocean's 'biological carbon pump', which would have increased deep-ocean oxygen. The mechanism at play would have determined whether the ODZ contractions occurred in step with the warming or took centuries or millennia to develop. Thus, although our results from the Cenozoic do not necessarily apply to the near-term future, they might imply that global warming may eventually cause ODZ contraction.

The Bering Strait was flooded 10,000 years before the Last Glacial Maximum.

The cyclic growth and decay of continental ice sheets can be reconstructed from the history of global sea level. Sea level is relatively well constrained for the Last Glacial Maximum (LGM, 26,500 to 19,000 y ago, 26.5 to 19 ka) and the ensuing deglaciation. However, sea-level estimates for the period of ice-sheet growth before the LGM vary by > 60 m, an uncertainty comparable to the sea-level equivalent of the contemporary Antarctic Ice Sheet. Here, we constrain sea level prior to the LGM by reconstructing the flooding history of the shallow Bering Strait since 46 ka. Using a geochemical proxy of Pacific nutrient input to the Arctic Ocean, we find that the Bering Strait was flooded from the beginning of our records at 46 ka until [Formula: see text] ka. To match this flooding history, our sea-level model requires an ice history in which over 50% of the LGM's global peak ice volume grew after 46 ka. This finding implies that global ice volume and climate were not linearly coupled during the last ice age, with implications for the controls on each. Moreover, our results shorten the time window between the opening of the Bering Land Bridge and the arrival of humans in the Americas.

Oceanic nutrient rise and the late Miocene inception of Pacific oxygen-deficient zones.

The modern Pacific Ocean hosts the largest oxygen-deficient zones (ODZs), where oxygen concentrations are so low that nitrate is used to respire organic matter. The history of the ODZs may offer key insights into ocean deoxygenation under future global warming. In a 12-My record from the southeastern Pacific, we observe a >10‰ increase in foraminifera-bound nitrogen isotopes (15N/14N) since the late Miocene (8 to 9 Mya), indicating large ODZs expansion. Coinciding with this change, we find a major increase in the nutrient content of the ocean, reconstructed from phosphorus and iron measurements of hydrothermal sediments at the same site. Whereas global warming studies cast seawater oxygen concentrations as mainly dependent on climate and ocean circulation, our findings indicate that modern ODZs are underpinned by historically high concentrations of seawater phosphate.

Analytical improvements and assessment of long-term performance of the oxidation-denitrifier method.

The analysis of the nitrogen (N) isotopic composition of organic matter bound to fossil biomineral structures (BB-δ15 N) using the oxidation-denitrifier (O-D) method provides a novel tool to study past changes in N cycling processes. METHODS: We report a set of methodological improvements to the O-D method, including (a) a method for sealing the reaction vials in which the oxidation of organic N to NO3 - takes place, (b) a recipe for bypassing the pH adjustment step before the bacterial conversion of NO3 - to N2 O, and (c) a method for storing recrystallized dipotassium peroxodisulfate (K2 S2 O8 ) under Ar atmosphere. RESULTS: The new sealing method eliminates the occasional contamination and vial breakage that occurred previously while increasing sample throughput. The protocol for bypassing pH adjustment does not affect BB-δ15 N, and it significantly reduces the processing time. Storage of K2 S2 O8 reagent under Ar atmosphere produces stable oxidation blanks over more than 3.5 years. We report analytical blanks, accuracy, and precision for this methodology from eight users over the course of ~3.5 years of analyses at the Max Planck Institute for Chemistry. Our method produces analytical blanks characterized by low N content (0.30 ± 0.13 nmol N, 1σ, n = 195) and stable δ15 N (-2.20 ± 3.13‰, n = 195). The analysis of reference amino acid standards USGS 40 and USGS 65 indicates an overall accuracy of -0.23 ± 0.35‰ (1σ, n = 891). The analysis of in-house fossil standards gives similar analytical precision (1σ) across a range of BB-δ15 N values and biominerals: zooxanthellate coral standard PO-1 (6.08 ± 0.21‰, n = 267), azooxanthellate coral standard LO-1 (10.20 ± 0.28‰, n = 258), foraminifera standard MF-1 (5.92 ± 0.28‰, n = 243), and tooth enamel AG-Lox (4.06 ± 0.49‰, n = 78). CONCLUSIONS: The methodological improvements significantly increase sample throughput without compromising analytical precision or accuracy down to 1 nmol of N.

Global Nitrogen Cycle: Critical Enzymes, Organisms, and Processes for Nitrogen Budgets and Dynamics.

Nitrogen (N) is used in many of life's fundamental biomolecules, and it is also a participant in environmental redox chemistry. Biogeochemical processes control the amount and form of N available to organisms ("fixed" N). These interacting processes result in N acting as the proximate limiting nutrient in most surface environments. Here, we review the global biogeochemical cycle of N and its anthropogenic perturbation. We introduce important reservoirs and processes affecting N in the environment, focusing on the ocean, in which N cycling is more generalizable than in terrestrial systems, which are more heterogeneous. Particular attention is given to processes that create and destroy fixed N because these comprise the fixed N input/output budget, the most universal control on environmental N availability. We discuss preindustrial N budgets for terrestrial and marine systems and their modern-day alteration by N inputs from human activities. We summarize evidence indicating that the simultaneous roles of N as a required biomass constituent and an environmental redox intermediate lead to stabilizing feedbacks that tend to blunt the impact of N cycle perturbations at larger spatiotemporal scales, particularly in marine systems. As a result of these feedbacks, the anthropogenic "N problem" is distinct from the "carbon dioxide problem" in being more local and less global, more immediate and less persistent.

Natural forcing of the North Atlantic nitrogen cycle in the Anthropocene.

Human alteration of the global nitrogen cycle intensified over the 1900s. Model simulations suggest that large swaths of the open ocean, including the North Atlantic and the western Pacific, have already been affected by anthropogenic nitrogen through atmospheric transport and deposition. Here we report an ∼130-year-long record of the 15N/14N of skeleton-bound organic matter in a coral from the outer reef of Bermuda, which provides a test of the hypothesis that anthropogenic atmospheric nitrogen has significantly augmented the nitrogen supply to the open North Atlantic surface ocean. The Bermuda 15N/14N record does not show a long-term decline in the Anthropocene of the amplitude predicted by model simulations or observed in a western Pacific coral 15N/14N record. Rather, the decadal variations in the Bermuda 15N/14N record appear to be driven by the North Atlantic Oscillation, most likely through changes in the formation rate of Subtropical Mode Water. Given that anthropogenic nitrogen emissions have been decreasing in North America since the 1990s, this study suggests that in the coming decades, the open North Atlantic will remain minimally affected by anthropogenic nitrogen deposition.

Megacity development and the demise of coastal coral communities: Evidence from coral skeleton δ15 N records in the Pearl River estuary.

Historical coral skeleton (CS) δ18 O and δ15 N records were produced from samples recovered from sedimentary deposits, held in natural history museum collections, and cored into modern coral heads. These records were used to assess the influence of global warming and regional eutrophication, respectively, on the decline of coastal coral communities following the development of the Pearl River Delta (PRD) megacity, China. We find that, until 2007, ocean warming was not a major threat to coral communities in the Pearl River estuary; instead, nitrogen (N) inputs dominated impacts. The high but stable CS-δ15 N values (9‰-12‰ vs. air) observed from the mid-Holocene until 1980 indicate that soil and stream denitrification reduced and modulated the hydrologic inputs of N, blunting the rise in coastal N sources during the early phase of the Pearl River estuary urbanization. However, an unprecedented CS-δ15 N peak was observed from 1987 to 1993 (>13‰ vs. air), concomitant to an increase of NH4+ concentration, consistent with the rapid Pearl River estuary urbanization as the main cause for this eutrophication event. We suggest that widespread discharge of domestic sewage entered directly into the estuary, preventing removal by natural denitrification hotspots. We argue that this event caused the dramatic decline of the Pearl River estuary coral communities reported from 1980 to 2000. Subsequently, the coral record shows that the implementation of improved wastewater management policies succeeded in bringing down both CS-δ15 N and NH4+ concentrations in the early 2000s. This study points to the potential importance of eutrophication over ocean warming in coral decline along urbanized coastlines and in particular in the vicinity of megacities.

Impact of glacial/interglacial sea level change on the ocean nitrogen cycle.

The continental shelves are the most biologically dynamic regions of the ocean, and they are extensive worldwide, especially in the western North Pacific. Their area has varied dramatically over the glacial/interglacial cycles of the last million years, but the effects of this variation on ocean biological and chemical processes remain poorly understood. Conversion of nitrate to N2 by denitrification in sediments accounts for half or more of the removal of biologically available nitrogen ("fixed N") from the ocean. The emergence of continental shelves during ice ages and their flooding during interglacials have been hypothesized to drive changes in sedimentary denitrification. Denitrification leads to the occurrence of phosphorus-bearing, N-depleted surface waters, which encourages N2 fixation, the dominant N input to the ocean. An 860,000-y record of foraminifera shell-bound N isotopes from the South China Sea indicates that N2 fixation covaried with sea level. The N2 fixation changes are best explained as a response to changes in regional excess phosphorus supply due to sea level-driven variations in shallow sediment denitrification associated with the cyclic drowning and emergence of the continental shelves. This hypothesis is consistent with a glacial ocean that hosted globally lower rates of fixed N input and loss and a longer residence time for oceanic fixed N-a "sluggish" ocean N budget during ice ages. In addition, this work provides a clear sign of sea level-driven glacial/interglacial oscillations in biogeochemical fluxes at and near the ocean margins, with implications for coastal organisms and ecosystems.

Deep-sea coral evidence for lower Southern Ocean surface nitrate concentrations during the last ice age.

The Southern Ocean regulates the ocean's biological sequestration of CO2 and is widely suspected to underpin much of the ice age decline in atmospheric CO2 concentration, but the specific changes in the region are debated. Although more complete drawdown of surface nutrients by phytoplankton during the ice ages is supported by some sediment core-based measurements, the use of different proxies in different regions has precluded a unified view of Southern Ocean biogeochemical change. Here, we report measurements of the 15N/14N of fossil-bound organic matter in the stony deep-sea coral Desmophyllum dianthus, a tool for reconstructing surface ocean nutrient conditions. The central robust observation is of higher 15N/14N across the Southern Ocean during the Last Glacial Maximum (LGM), 18-25 thousand years ago. These data suggest a reduced summer surface nitrate concentration in both the Antarctic and Subantarctic Zones during the LGM, with little surface nitrate transport between them. After the ice age, the increase in Antarctic surface nitrate occurred through the deglaciation and continued in the Holocene. The rise in Subantarctic surface nitrate appears to have had both early deglacial and late deglacial/Holocene components, preliminarily attributed to the end of Subantarctic iron fertilization and increasing nitrate input from the surface Antarctic Zone, respectively.

Changes in North Atlantic nitrogen fixation controlled by ocean circulation.

In the ocean, the chemical forms of nitrogen that are readily available for biological use (known collectively as 'fixed' nitrogen) fuel the global phytoplankton productivity that exports carbon to the deep ocean. Accordingly, variation in the oceanic fixed nitrogen reservoir has been proposed as a cause of glacial-interglacial changes in atmospheric carbon dioxide concentration. Marine nitrogen fixation, which produces most of the ocean's fixed nitrogen, is thought to be affected by multiple factors, including ocean temperature and the availability of iron and phosphorus. Here we reconstruct changes in North Atlantic nitrogen fixation over the past 160,000 years from the shell-bound nitrogen isotope ratio ((15)N/(14)N) of planktonic foraminifera in Caribbean Sea sediments. The observed changes cannot be explained by reconstructed changes in temperature, the supply of (iron-bearing) dust or water column denitrification. We identify a strong, roughly 23,000-year cycle in nitrogen fixation and suggest that it is a response to orbitally driven changes in equatorial Atlantic upwelling, which imports 'excess' phosphorus (phosphorus in stoichiometric excess of fixed nitrogen) into the tropical North Atlantic surface. In addition, we find that nitrogen fixation was reduced during glacial stages 6 and 4, when North Atlantic Deep Water had shoaled to become glacial North Atlantic intermediate water, which isolated the Atlantic thermocline from excess phosphorus-rich mid-depth waters that today enter from the Southern Ocean. Although modern studies have yielded diverse views of the controls on nitrogen fixation, our palaeobiogeochemical data suggest that excess phosphorus is the master variable in the North Atlantic Ocean and indicate that the variations in its supply over the most recent glacial cycle were dominated by the response of regional ocean circulation to the orbital cycles.

Marine biogenic source of atmospheric organic nitrogen in the subtropical North Atlantic.

Global models estimate that the anthropogenic component of atmospheric nitrogen (N) deposition to the ocean accounts for up to a third of the ocean's external N supply and 10% of anthropogenic CO2 uptake. However, there are few observational constraints from the marine atmospheric environment to validate these findings. Due to the paucity of atmospheric organic N data, the largest uncertainties related to atmospheric N deposition are the sources and cycling of organic N, which is 20-80% of total N deposition. We studied the concentration and chemical composition of rainwater and aerosol organic N collected on the island of Bermuda in the western North Atlantic Ocean over 18 mo. Here, we show that the water-soluble organic N concentration ([WSON]) in marine aerosol is strongly correlated with surface ocean primary productivity and wind speed, suggesting a marine biogenic source for aerosol WSON. The chemical composition of high-[WSON] aerosols also indicates a primary marine source. We find that the WSON in marine rain is compositionally different from that in concurrently collected aerosols, suggesting that in-cloud scavenging (as opposed to below-cloud "washout") is the main contributor to rain WSON. We conclude that anthropogenic activity is not a significant source of organic N to the marine atmosphere over the North Atlantic, despite downwind transport from large pollution sources in North America. This, in conjunction with previous work on ammonium and nitrate, leads to the conclusion that only 27% of total N deposition to the global ocean is anthropogenic, in contrast to the 80% estimated previously.

Southern Ocean dust-climate coupling over the past four million years.

Dust has the potential to modify global climate by influencing the radiative balance of the atmosphere and by supplying iron and other essential limiting micronutrients to the ocean. Indeed, dust supply to the Southern Ocean increases during ice ages, and 'iron fertilization' of the subantarctic zone may have contributed up to 40 parts per million by volume (p.p.m.v.) of the decrease (80-100 p.p.m.v.) in atmospheric carbon dioxide observed during late Pleistocene glacial cycles. So far, however, the magnitude of Southern Ocean dust deposition in earlier times and its role in the development and evolution of Pleistocene glacial cycles have remained unclear. Here we report a high-resolution record of dust and iron supply to the Southern Ocean over the past four million years, derived from the analysis of marine sediments from ODP Site 1090, located in the Atlantic sector of the subantarctic zone. The close correspondence of our dust and iron deposition records with Antarctic ice core reconstructions of dust flux covering the past 800,000 years (refs 8, 9) indicates that both of these archives record large-scale deposition changes that should apply to most of the Southern Ocean, validating previous interpretations of the ice core data. The extension of the record beyond the interval covered by the Antarctic ice cores reveals that, in contrast to the relatively gradual intensification of glacial cycles over the past three million years, Southern Ocean dust and iron flux rose sharply at the Mid-Pleistocene climatic transition around 1.25 million years ago. This finding complements previous observations over late Pleistocene glacial cycles, providing new evidence of a tight connection between high dust input to the Southern Ocean and the emergence of the deep glaciations that characterize the past one million years of Earth history.

Nitrogen isotope fractionation by alternative nitrogenases and past ocean anoxia.

Biological nitrogen fixation constitutes the main input of fixed nitrogen to Earth's ecosystems, and its isotope effect is a key parameter in isotope-based interpretations of the N cycle. The nitrogen isotopic composition (δ(15)N) of newly fixed N is currently believed to be ∼-1‰, based on measurements of organic matter from diazotrophs using molybdenum (Mo)-nitrogenases. We show that the vanadium (V)- and iron (Fe)-only "alternative" nitrogenases produce fixed N with significantly lower δ(15)N (-6 to -7‰). An important contribution of alternative nitrogenases to N2 fixation provides a simple explanation for the anomalously low δ(15)N (<-2‰) in sediments from the Cretaceous Oceanic Anoxic Events and the Archean Eon. A significant role for the alternative nitrogenases over Mo-nitrogenase is also consistent with evidence of Mo scarcity during these geologic periods, suggesting an additional dimension to the coupling between the global cycles of trace elements and nitrogen.

Updates to instrumentation and protocols for isotopic analysis of nitrate by the denitrifier method.

RATIONALE: The denitrifier method allows for highly sensitive measurement of the (15) N/(14) N (δ(15) N value) and (18) O/(16) O (δ(18) O value) of nitrate dissolved in natural waters and for highly sensitive δ(15) N measurement of other N forms (e.g., organic N) that can be converted into nitrate. Here, updates to instrumentation and protocols are described, and improvements in data quality are demonstrated. METHODS: A 'heart cut' of the N2 O was implemented in the extraction system to (1) minimize introduction of contaminants into the mass spectrometer, reducing isotopic drift and (2) decrease the fraction of sample lost at the open split to improve sensitivity. Referencing protocols were updated, including a correction scheme for a weak dependence of nitrate δ(18) O values on nitrate concentration. Analyses of samples from the US GEOTRACES North Atlantic Program and of reference solutions from the same analysis batches were used to characterize performance. RESULTS: The drift is typically <0.1‰ for both δ(15) N and δ(18) O values. Within-batch and inter-batch replication yields 1 standard deviation (SD) of ≤0.06‰ for δ(15) N values and ≤0.14‰ for δ(18) O values down to 5 µM nitrate and ≤0.08‰ and ≤0.23‰ at 2 and 1 µM. The blank is typically 0.06 nmol N, 0.3% of the N in a 20 nmol N sample. Differences between reference materials in seawater are indistinguishable from reported differences for δ(15) N values, with a contraction for δ(18) O values of ≤5%. CONCLUSIONS: The new instrumentation and protocols yield nitrate isotopic data with external precision of ≤0.1‰ for large sample sets such as those derived from oceanographic sections. Further study should investigate the causes of (1) the weak dependence of nitrate δ(18) O values on nitrate concentration and (2) the inter-batch variation in the δ(18) O contraction (due mostly to oxygen atom exchange with water). Nevertheless, comprehensive correction schemes are in place for the measurement of both the δ(15) N and δ(18) O values of nitrate. Copyright © 2016 John Wiley & Sons, Ltd.

The polar ocean and glacial cycles in atmospheric CO(2) concentration.

Global climate and the atmospheric partial pressure of carbon dioxide () are correlated over recent glacial cycles, with lower during ice ages, but the causes of the changes are unknown. The modern Southern Ocean releases deeply sequestered CO(2) to the atmosphere. Growing evidence suggests that the Southern Ocean CO(2) 'leak' was stemmed during ice ages, increasing ocean CO(2) storage. Such a change would also have made the global ocean more alkaline, driving additional ocean CO(2) uptake. This explanation for lower ice-age , if correct, has much to teach us about the controls on current ocean processes.

Enameloid-bound δ15 N reveals large trophic separation among Late Cretaceous sharks in the northern Gulf of Mexico.

The nitrogen isotopic composition (15 N/14 N ratio, or δ15 N) of enameloid-bound organic matter (δ15 NEB ) in shark teeth was recently developed to investigate the biogeochemistry and trophic structures (i.e., food webs) of the ancient ocean. Using δ15 NEB , we present the first nitrogen isotopic evidence for trophic differences between shark taxa from a single fossil locality. We analyze the teeth of four taxa (Meristodonoides, Ptychodus, Scapanorhynchus, and Squalicorax) from the Late Cretaceous (83-84 Ma) Trussells Creek site in Alabama, USA, and compare the N isotopic findings with predictions from tooth morphology, the traditional method for inferring shark paleo-diets. Our δ15 NEB data indicate two distinct trophic groups, with averages separated by 6.1 ± 2.1‰. The lower group consists of Meristodonoides and Ptychodus, and the higher group consists of Scapanorhynchus and Squalicorax (i.e., lamniforms). This δ15 NEB difference indicates a 1.5 ± 0.5 trophic-level separation between the two groups, a finding that is in line with paleontological predictions of a higher trophic level for these lamniforms over Meristodonoides and Ptychodus. However, the δ15 NEB of Meristodonoides is lower than suggested by tooth morphology, although consistent with mechanical tests suggesting that higher trophic-level bony fishes were not a major component of their diet. Further, δ15 NEB indicates that the two sampled lamniform taxa fed at similar trophic levels despite their different inferred tooth functions. These two findings suggest that tooth morphology alone may not always be a sufficient indicator of dietary niche. The large trophic separation revealed by the δ15 NEB offset leaves open the possibility that higher trophic-level lamniforms, such as those measured here, preyed upon smaller, lower trophic-level sharks like Meristodonoides.

Oxygen rise in the tropical upper ocean during the Paleocene-Eocene Thermal Maximum.

The global ocean's oxygen inventory is declining in response to global warming, but the future of the low-oxygen tropics is uncertain. We report new evidence for tropical oxygenation during the Paleocene-Eocene Thermal Maximum (PETM), a warming event that serves as a geologic analog to anthropogenic warming. Foraminifera-bound nitrogen isotopes indicate that the tropical North Pacific oxygen-deficient zone contracted during the PETM. A concomitant increase in foraminifera size implies that oxygen availability rose in the shallow subsurface throughout the tropical North Pacific. These changes are consistent with ocean model simulations of warming, in which a decline in biological productivity allows tropical subsurface oxygen to rise even as global ocean oxygen declines. The tropical oxygen increase may have helped avoid a mass extinction during the PETM.

Spatial coupling of nitrogen inputs and losses in the ocean.

Nitrogen fixation is crucial for maintaining biological productivity in the oceans, because it replaces the biologically available nitrogen that is lost through denitrification. But, owing to its temporal and spatial variability, the global distribution of marine nitrogen fixation is difficult to determine from direct shipboard measurements. This uncertainty limits our understanding of the factors that influence nitrogen fixation, which may include iron, nitrogen-to-phosphorus ratios, and physical conditions such as temperature. Here we determine nitrogen fixation rates in the world's oceans through their impact on nitrate and phosphate concentrations in surface waters, using an ocean circulation model. Our results indicate that nitrogen fixation rates are highest in the Pacific Ocean, where water column denitrification rates are high but the rate of atmospheric iron deposition is low. We conclude that oceanic nitrogen fixation is closely tied to the generation of nitrogen-deficient waters in denitrification zones, supporting the view that nitrogen fixation stabilizes the oceanic inventory of fixed nitrogen over time.