Millennial-scale plankton regime shifts in the subtropical North Pacific Ocean

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Science  26 Nov 2015:
DOI: 10.1126/science.aaa9942


Climate change is predicted to alter marine phytoplankton communities and affect productivity, biogeochemistry, and the efficacy of the biological pump. We reconstructed high-resolution records of changing plankton community composition in the North Pacific Ocean over the past millennium. Amino acid–specific δ13C records preserved in long-lived deep-sea corals revealed three major plankton regimes corresponding to northern hemisphere climate periods. Non-N2 fixing cyanobacteria dominated during the Medieval Climate Anomaly (950-1250C.E.) before giving way to a new regime where eukaryotic microalgae contributed nearly half of export production during the Little Ice Age (~1400-1850C.E.). The third regime, unprecedented in the last millennium, began in the industrial era and is supported by increasing N2-fixing cyanobacterial production. This picoplankton community shift may provide a negative feedback to rising atmospheric CO2.

Gone is the paradigm of the oligotrophic subtropical gyres as vast oceanic deserts. In the recent instrumental record a new picture has emerged of substantial dynamics in plankton community structure, biogeochemical cycling, and export production (14). Numerous lines of evidence suggest that shifts in phytoplankton community “regimes” are intimately connected to oceanographic conditions (2, 4, 5). For instance, the 1976 Pacific Decadal Oscillation (PDO) polarity reversal caused a shoaling of the mixed layer and subsequent declines in available nutrients to the North Pacific Subtropical Gyre (NPSG). These conditions likely promoted the food-web regime shift from a eukaryotic to a prokaryotic, cyanobacteria-dominated system (2). Such changes are superimposed on secular shifts associated with the areal increase of subtropical gyres that has been ongoing for at least 25 years (6). In the face of increasing climate change, it becomes imperative to understand recent changes at the base of the NPSG food-web in the context of longer-term trends. However, our understanding of how NPSG plankton communities have shifted on centennial time scales has been limited by available methods and paleo-archives of sufficient length and resolution.

Hawaiian gold corals (Kulamanamana haumeaae) are extraordinarily long-lived paleo-archives that record the biogeochemical signatures of recently exported production in their proteinaceous skeletons (7, 8). We generated millennial-length records of bulk stable carbon isotopes (δ13Cbulk) from specimens of K. haumeaae collected from the top of the mesopelagic zone at two sites in the Hawaiian archipelago (Fig. 1). The δ13Cbulk records showed remarkable congruence, characterized by a gradual increase of ~1.0‰ from ~1000C.E. to ~1850C.E., followed by a rapid decrease of -1.0‰ from ~1850 to the present after correcting for the Suess effect (Fig. 2A) (911). These changes in δ13Cbulk imply multi-centennial scale shifts in primary production δ13C values that we hypothesize reflect major changes in plankton community structure over the last 1000 years.

Fig. 1 NPSG productivity distribution with sample locations.

(A) Spatial extent of the oligotrophic gyre from spring 2012 remote sensing-derived chlorophyll a concentrations for the North Pacific from Aqua/MODIS (image courtesy of NASA Goddard’s Ocean Biology Processing Group). (B) K. haumeaae sampling locations at Makapuu and French Frigate Shoals relative to oceanographic station ALOHA (X) overlain on surface ocean nitrate concentration (National Oceanographic Data Center, 2013).

Fig. 2 1000 year bulk and essential amino acid δ13C records from deep-sea corals in the North Pacific Subtropical Gyre.

Records of K. haumeaae (A) δ13Cbulk (solid lines show 20 year average, analytical error 0.05‰) and (B) phenylalanine δ13CPhe (squares, analytical error (0.2‰) for Makapuu live coral (blue), Makapuu fossil coral (magenta), and French Frigate Shoals (brown). All records have been corrected for the oceanic Suess effect since 1860 (10, 11). Well-known northern hemisphere climate phenomena are overlaid for reference (18).

Bulk δ13C records integrate the combined influences of: the δ13C value of inorganic carbon utilized during carbon fixation, shifts in plankton community structure, trophic changes, and biochemical fractionation. To isolate plankton source signatures within this signal, we applied a powerful fingerprinting approach to these deep-sea corals, based on the normalized δ13C values of essential amino acids (δ13CEAA) in primary producers (11). These δ13CEAA fingerprints reflect the substantial metabolic diversity in EAA synthesis pathways and associated isotope effects among evolutionarily distinct primary producers (12, 13). We found diagnostic multivariate patterns in literature values of normalized δ13CEAA values among four key source end-members relevant to the NPSG (eukaryotic microalgae, non-dinitrogen utilizing and dinitrogen fixing cyanobacteria, and heterotrophic bacteria) (fig. S2). Because animals cannot synthesize the carbon skeletons of EAAs (14), these δ13CEAA fingerprints are incorporated, virtually unmodified, into upper trophic level consumers, including gorgonin corals (15). Furthermore, normalized δ13CEAA fingerprints are robust to the myriad factors affecting bulk δ13C values such as environmental and growth conditions (11, 13, 15, 16).

A subset of the deep-sea coral samples spanning the entire 1000-year record was analyzed for δ13CEAA at approximately 20-year resolution (table S1). δ13CEAA values were strongly correlated with δ13Cbulk (fig. S1), indicating that trends in δ13Cbulk can be attributed to changes in source carbon at the base of the food-web (15). For example, the δ13CEAA of phenylalanine (Fig. 2B) mirrored that of δ13Cbulk (Fig. 2A), however the magnitude of change was 10 times larger than in δ13Cbulk. This suggests that isotopic contribution from other macromolecules had a strong muting effect on δ13Cbulk values, and thus δ13CEAA is a more sensitive record of changes in primary producer δ13C than δ13Cbulk (15). Our results indicate that variability in primary producer export δ13C values was in fact much larger than would be inferred from coral δ13Cbulk records alone and strongly suggest broad changes in the sources of exported primary production through time.

To reconstruct past shifts in the relative contribution of major phytoplankton groups to export production in the NPSG, we applied a Bayesian stable isotope-mixing model to published source end-member δ13CEAA fingerprints (11) and the δ13CEAA records of K. haumeaae normalized to their respective means (fig. S2 and table S2). Over the entire 1000-yr record, photoautotrophic carbon dominated the coral’s sinking particulate organic matter (POM) food source (mean 87 ± 6%), with a relatively small heterotrophic bacterial contribution (13 ± 6%) (Fig. 3). Likewise, prokaryotic cyanobacterial sources dominated photoautrophic carbon (63 ± 14%), with a moderate mean contribution from eukaryotic microalgae (24 ± 10%) (Fig. 3). On centennial timescales, however, relative contributions from photoautotrophic end-members shifted dramatically. For example, between 1000-1850C.E cyanobacteria decreased from 80% to 50% of total exported productivity, offset by an equivalent increase in eukaryotic microalgae to a peak contribution of ~45% in the early 1800s. While previous studies have noted enhanced diatom abundance in the NPSG associated with mesoscale oceanographic features (17), such a sustained level of high eukaryotic microalgal production has never been observed in the modern instrumental record. The most parsimonious explanation of our data are that the changes in phylogenetic identity of sources contributing to export production reflect changes in the relative surface plankton community composition through time. An alternative, albeit highly unlikely, hypothesis is that surface plankton community composition has remained relatively constant through time, and instead the degree of decoupling between surface and export production has undergone dramatic changes as a function of climate shifts (11)

Fig. 3 Millennial record of relative contribution of primary producer carbon sources to deep-sea corals.

Relative contribution of carbon from nitrogen fixing cyanobacteria (black), non-nitrogen fixing cyanobacteria (yellow), eukaryotic microalgae (green), and heterotrophic bacteria (gray) to deep-sea corals collected at 450m in the Hawaiian Archipelago of the North Pacific Subtropical Gyre over the past 1000 years. Relative contributions were based on a compound-specific Bayesian stable isotope mixing model of normalized phytoplankton end-member and coral essential amino acid δ13C values. Well-known northern hemisphere climate phenomena are overlaid for reference (18).

To better constrain the patterns of changing plankton community composition, we applied hierarchical cluster analysis to the normalized δ13CEAA data (11). This approach identified three distinct plankton community regimes that corresponded to well-known northern hemisphere climate phenomena (Fig. 4). The first regime corresponded to the Medieval Climate Anomaly [MCA; 950-1250C.E. (18)], with δ13CEAA fingerprints indicative of export production dominated by nitrate (NO3-) utilizing cyanobacteria. There is general consensus that the putative MCA in the northern mid-latitudes was similar to the mid 20th century (18, 19), implying relatively warm sea surface temperatures, weak winds, shallow mixed layer depths, and resulting nutrient limitation, all favoring a microbial-loop dominated community (2). The second regime corresponded to the Little Ice Age [LIA; 1400-1850C.E. (18)]. Here the plankton assemblage contributing to export production transitioned from a cyanobacteria-dominated community to one far more strongly influenced by eukaryotic microalgae (Fig. 3). This shift likely reflected cooler sea surface temperatures, a reduction in stratification, an increase in mixed layer depth, and an inferred increase in the supply of inorganic nitrate from depth (4, 20).

Fig. 4 Phytoplankton regime shifts recorded in deep-sea corals.

A dendrogram of similarity in exported plankton carbon utilization by deep-sea corals over the past 1000 years based upon an average-link hierarchical cluster analysis. The dendrogram is separated into three significantly different clusters according to multiscale bootstrapping with approximately unbiased p values >0.95. Well-known northern hemisphere climate phenomena (Medieval Climate Anomaly = magenta; Little Ice Age = cyan; Industrial Age = orange) are overlaid for reference (18).

The third and current regime began at the end of the LIA and the onset of the modern-industrial age (~1850C.E) (Fig. 4). Here we see a transition back to a cyanobacteria-dominated system. However, unlike the MCA period, the current regime is characterized by a biogeochemically distinct group of cyanobacteria: the N2-fixing diazotrophs. Historically, the availability of inorganic nitrogen (N) and/or phosphorus (P) was thought to limit plankton production in the NPSG (21). Post ~1850C.E., however, sea surface temperatures have increased with a likely decrease in the tradewinds concomitant with gyre expansion as a result of Northern Hemisphere warming. The resulting increase in stratification and decrease in nutrient availability may have selected for a dinitrogen (N2)-fixing cyanobacterial community, as seen in the instrumental record over the last ~20 years (2, 22). Current declining P inventories and increasing N:P ratios in the mixed layer at HOT-ALOHA are thought to reflect this decades-long increase in N2 fixation (1, 2, 8), which is further supported by recent literature suggesting that canonical Redfield ratios in the NPSG may be more plastic than previously realized (23, 24).

Our δ13CEAA fingerprinting data showing an increase in N2-fixing cyanobacteria carbon in export production (47%) since the end of the LIA correspond well with recent evidence of a 17-27% increase in NPSG N2-fixation since ~1850C.E based on amino acid-specific nitrogen isotopes (δ15NAA) on the same suite of K. haumeaae specimens as this study (8). These studies represent fully independent lines of evidence supporting the hypothesis that recent decreases in δ15Nbulk values of exported POM in the NPSG are related to increases in diazotrophic plankton within a microbial-loop driven system (11).

By offering the first direct phylogenetic context for long-term shifts in isotopic records of exported POM, our data represent a major new constraint in understanding the evolution of NPSG biogeochemistry. For example, a recently proposed alternate hypothesis suggests that advection of 15N-depleted nitrate from the Eastern Tropical Pacific, associated with a reduction of denitrification (25), might also explain recent low NPSG δ15N values. Similarly, Kim et al. (26) suggested atmospheric N deposition as the dominant factor driving increases in N* values across the Pacific. Simply put, the δ15N value of N entrained into the mixed layer should not, by itself, impact planktonic community structure. In contrast, our new evidence for a profound phylogenetic community shift is fully consistent with increasing N2-fixation, likely linked to overall increased stratification and reductions in upwelled NO3-, over the past 100 years.

Taken together, our data show that phytoplankton community structure in the NSPG is subject to multi-centennial shifts broadly linked to climate state. They also reveal that today’s cyanobacterial community, characterized by strongly enhanced N2-fixation, is unique within at least the past 1000 years. The transition to the current cyanobacterial regime (<200 years) was significantly faster than the transition from cyanobacterial dominance during the MCA to the eukaryotic dominance during the LIA (>600 years). Both the nature and rate of change of the current dominant autotrophic assemblage strongly suggest continuing rapid changes in NPSG plankton community structure with anthropogenic climate change and are consistent with predicted expansion of N2-fixing cyanobacteria habitat (27).

Regime shifts in plankton community composition have far-reaching implications for productivity, food-web dynamics, biogeochemical cycling, and the efficacy of the biological pump (22, 28, 29). The fact that dominant cyanobacterial signatures were recorded in deep-sea corals from the mesopelagic strongly suggests that continuing shifts to an N2-fixing prokaryotic regime have fundamentally altered the main sources of exported POM. These observations also support recent evidence (3, 30) that small cell picoplankton production, free-living and/or through cyanobacteria-diatom symbioses (11, 22), may be a more important component of export production in oligotrophic gyres than traditionally recognized. Further, recent studies have shown that plankton elemental stoichiometry is more variable than previously assumed under the classical Redfield paradigm, with C:P ratios several times higher in the oligotrophic gyres compared with upwelling regions (23, 24). This suggests that carbon export could actually be more efficient (on a per mol of P basis) in the oligotrophic gyres, despite their lower overall productivity, and further suggests that increasing nutrient limitation in warmer and more stratified oceans over the past 100 years may have provided a major negative climate feedback (23, 24). Our results showing that the phylogenetic origin of export production in the NPSG has indeed trended toward greater N2-fixing prokaryotes over the last century strongly support this idea. If small cell export does in fact represent a more efficient C pump, our new records suggest this carbon cycle feedback has already been operating for the last 100 years. For this feedback loop to persist into the future, the system cannot become phosphate limited.


Materials and Methods

Figs. S1 and S2

Tables S1 and S2

References (3168)


  1. Materials and methods are available as supplementary materials on Science Online.
  2. ACKNOWLEDGMENTS All Methods, additional display items, and Source Data are available in the Supplementary Materials. K.W.M., T.P.G. and M.D.M conceived the project. K.W.M. prepared samples, performed bulk and compound-specific δ13C analyses, and wrote the manuscript. O.A.S. and T.L. assisted in data analysis and commented on the manuscript. T.P.G. and M.D.M. supervised this project, discussed the results, and commented on the manuscript. We would like to thank M. Hanson, S. Fauqué, and J. Liu for assistance in lab. This work would not have been possible without the captain and crew of the RV Ka‘imikai-o-Kanaloa and the pilots and engineers of the Hawaii Undersea Research Lab's Pisces IV and V. We would also like to thank three anonymous reviewers for valuable feedback on the manuscript. Funding for sample collection was from NOAA/NURP and the National Geographic Society (7717-04). A portion of this work was performed under the auspices of the U.S. Department of Energy (DE-AC52-07NA27344). The majority of the work presented here was funded by the NSF (OCE 1061689).
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