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Increasing subtropical North Pacific Ocean nitrogen fixation since the Little Ice Age

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Abstract

The North Pacific subtropical gyre (NPSG) plays a major part in the export of carbon and other nutrients to the deep ocean1. Primary production in the NPSG has increased in recent decades despite a reduction in nutrient supply to surface waters2,3. It is thought that this apparent paradox can be explained by a shift in plankton community structure from mostly eukaryotes to mostly nitrogen-fixing prokaryotes2,3,4. It remains uncertain, however, whether the plankton community domain shift can be linked to cyclical climate variability or a long-term global warming trend5. Here we analyse records of bulk and amino-acid-specific 15N/14N isotopic ratios (δ15N) preserved in the skeletons of long-lived deep-sea proteinaceous corals collected from the Hawaiian archipelago; these isotopic records serve as a proxy for the source of nitrogen-supported export production through time. We find that the recent increase in nitrogen fixation is the continuation of a much larger, centennial-scale trend. After a millennium of relatively minor fluctuation, δ15N decreases between 1850 and the present. The total shift in δ15N of −2 per mil over this period is comparable to the total change in global mean sedimentary δ15N across the Pleistocene–Holocene transition, but it is happening an order of magnitude faster6. We use a steady-state model and find that the isotopic mass balance between nitrate and nitrogen fixation implies a 17 to 27 per cent increase in nitrogen fixation over this time period. A comparison with independent records7,8 suggests that the increase in nitrogen fixation might be linked to Northern Hemisphere climate change since the end of the Little Ice Age.

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Figure 1: NPSG circulation and N* distribution with sample locations.
Figure 2: NPSG δ15N proxy records and their relationship to climate change.
Figure 3: Depth variations in water column δ15N confirm K. haumeaa δ15NPhe as a proxy for export production.

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Acknowledgements

We thank the captain and crew of the RV Ka‘imikai-o-Kanaloa and the pilots and engineers of the Hawaiian Undersea Research Laboratory’s Pisces V submersible for their assistance in collecting the specimens presented here. Funding for sample collection was from NOAA/NURP and the National Geographic Society (grant number 7717-04). Radiocarbon analyses were performed under the auspices of the US Department of Energy (grant number DE-AC52-07NA27344). The bulk of the work presented here was funded by the NSF (grant number OCE 1061689).

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Contributions

O.A.S. helped conceive the project, prepared samples, performed bulk and compound-specific δ15N analyses and wrote the paper. F.C.B. and J.T.S. assisted in sample preparation and analysis, and commented on the manuscript. T.P.G. and M.D.M. conceived and supervised this project, discussed the results and edited the manuscript.

Corresponding author

Correspondence to Owen A. Sherwood.

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The authors declare no competing financial interests.

Additional information

Data will be digitally archived with the National Oceanic and Atmospheric Adminstration paleoclimatology datasets (http://www.ncdc.noaa.gov/data-access/paleoclimatology-data/datasets) after publication.

Extended data figures and tables

Extended Data Figure 1 World Ocean Database 2009 instrumental records demonstrate physical and biological changes in the NPSG since 1950.

Increasing salinity and temperature is accompanied by a strong decrease in silicate and phosphate nutrient concentrations, and an increase in N*. These data are consistent with the previously observed shift from a dominantly eukaryotic to dominantly prokaryotic (N2-fixation) ecosystem in the NPSG2,3,42. Increasing rates of change with depth suggest large-scale changes in oceanographic circulation, consistent with expansion of the NPSG. Rates of change across separate depth bins are provided in Extended Data Table 1.

Extended Data Figure 2 Distribution of amino-acid concentration and δ15Naa in K. haumeaae.

a, Amino-acid mole per cent composition. b, δ15Naa data, showing two main groups: relatively δ15N-enriched ‘trophic’ amino acids (TrAA), and relatively lower-δ15N ‘source’ amino acids (SrcAA). These patterns are very close to those of heterotrophic fresh biomass18,19,21. Together with low ΣV values (Table 1), this supports the use of δ15NPhe as a proxy for the δ15N of exported production, and indicates that δ15N values have not undergone any significant diagenetic alteration. Extremely low values of threonine (Thr) are consistent with previous observations43,44, and this amino acid is now understood to be neither a trophic nor source amino acid45. Mean δ15Nbulk is shown for context. Error bars represent 1 s.d. (n = 20).

Extended Data Figure 3 Timeseries of δ15Naa parameters in comparison to δ15Nbulk from two K. haumeaae specimens from Makapuu.

Closed symbols, specimen Ger9701; open symbols, specimen Ger9702. Trophic position and ΣV parameters are defined in Table 1.

Extended Data Figure 4 Example K. haumeaae colony photographed in situ.

Photo credit: NOAA Hawaiian Undersea Research Laboratory, DSRV Pisces Pilots & Engineers, 2004.

Extended Data Figure 5 Example K. haumeaae skeletal cross-section.

Specimen Ger9701 from Makapuu. Red lines indicate micromill transect.

Extended Data Figure 6 Radiocarbon age models.

Blue-shaded areas represent conventional 14C calibrated age distributions. Green-shaded areas are post-bomb (post-1950) age distributions. Black curves and grey-shaded regions represent spline fits with 95% confidence intervals, respectively. The average age model error is 45 years. Outliers (indicated in red) were excluded from age models owing to age reversals. The shape of the curves reflects variable growth rates in the four coral samples illustrated.

Extended Data Figure 7 Relationship between δ15N and N* across different oceanographic regions.

The δ15NNO3 is driven by isotopic fractionation processes of denitrification, nitrate uptake and remineralization of diazotrophic organic nitrogen (ETNP, Eastern Tropical North Pacific; ETSP, Eastern Tropical South Pacific; redrawn from ref. 46). Existing deep-sea coral δ15NPhe data (red points) closely follow the same overall pattern. Data points are: (1) Hawaii K. haumeaae (2 specimens, 20 measurements; this paper); (2) Northwest Atlantic Primnoa resedaeformis (2 specimens, 8 measurements15); (3) Monterey Bay Isidella sp. (1 specimen, 10 measurements47); Error bars show the total range of measurements. Corresponding values of N* are obtained from the nearest surface water grid point of the World Ocean Atlas 2009 (http://www.nodc.noaa.gov/OC5/WOA09/woa09data.html).

Extended Data Table 1 World Ocean Database 2009 physical and chemical parameters
Extended Data Table 2 K. haumeaae radiocarbon data

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Sherwood, O., Guilderson, T., Batista, F. et al. Increasing subtropical North Pacific Ocean nitrogen fixation since the Little Ice Age. Nature 505, 78–81 (2014). https://doi.org/10.1038/nature12784

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