Changes in phytoplankton concentration now drive increased Arctic Ocean primary production

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Science  10 Jul 2020:
Vol. 369, Issue 6500, pp. 198-202
DOI: 10.1126/science.aay8380

Food for thought

Phytoplankton abundances in the Arctic Ocean have been increasing over recent decades as the region has warmed and sea ice has disappeared. The presumptive causes of this increase were expanding open water area and a longer growing season—at least until now. Lewis et al. show that although these factors may have driven the productivity trends before, over the past decade, phytoplankton primary production rose by more than half because of increased phytoplankton concentrations (see the Perspective by Babin). This finding means that there has been an influx of new nutrients into the region, suggesting that the Arctic Ocean could become more productive and export additional carbon in the future.

Science, this issue p. 198; see also p. 137


Historically, sea ice loss in the Arctic Ocean has promoted increased phytoplankton primary production because of the greater open water area and a longer growing season. However, debate remains about whether primary production will continue to rise should sea ice decline further. Using an ocean color algorithm parameterized for the Arctic Ocean, we show that primary production increased by 57% between 1998 and 2018. Surprisingly, whereas increases were due to widespread sea ice loss during the first decade, the subsequent rise in primary production was driven primarily by increased phytoplankton biomass, which was likely sustained by an influx of new nutrients. This suggests a future Arctic Ocean that can support higher trophic-level production and additional carbon export.

In response to anthropogenic climate change, the Arctic is warming faster than any other region, with the majority of the warming centered over the Arctic Ocean (AO) (1). Sea ice has radically decreased in concentration, volume, and duration, with summer sea ice predicted to disappear completely by mid-century (1). Correspondingly, annual phytoplankton net primary production (NPP) has significantly increased owing to a longer growing season and an expanded area of open water (OW) (25). However, scientists debate how continued sea ice declines will affect AO NPP in the future (6, 7). Greater freshwater flux through precipitation, ice melt, and river outflow could intensify surface ocean stratification and inhibit the mixing of deep nutrients into surface waters, thus reducing AO NPP (8, 9). Alternatively, greater OW area and more frequent storms (5) may increase NPP by promoting the upward delivery of new nutrients to the depleted euphotic zone through enhanced wind mixing (10), internal waves (11), and shelf break upwelling (12, 13). Here, we present a two-decade-long time series of NPP in the AO that we parameterized using the largest and most complete dataset of in situ optics and phytoplankton biomass and physiology ever assembled for these waters to assess the current trajectory of NPP in response to ongoing changes in Arctic climate.

Satellite-derived estimates of chlorophyll a (Chl a), sea surface temperature (SST), and sea ice concentration were used as input to an AO NPP algorithm (2, 3, 14) to evaluate trends from 1998 to 2018. We used a modified version of the standard empirical NASA–Chl a algorithm to better account for the distinct bio-optical properties of the AO, which differ notably from the global ocean because of higher pigment packaging and chromophoric dissolved organic matter (CDOM) concentrations (15, 16). The updated Chl a algorithm (17) was developed by using 501 coincident measurements of in situ remote sensing reflectance and Chl a from 25 different cruises that captured the spatial heterogeneity across the AO. Time series trends for mean surface phytoplankton biomass concentration (Chl a, milligrams per cubic meter), spatially integrated NPP (teragrams of carbon per year), SST (degrees Celsius), OW area (square kilometers), and OW duration (days) were statistically evaluated for the entire AO and 10 subregions (Fig. 1A) for the 21-year time period.

Fig. 1 Regions of interest and changes in phytoplankton biomass.

(A) The AO with its shelf seas and basin. Subregions are bounded by black lines by using the 1000-m isobath and categorized as inflow (green), interior (orange), or outflow (purple) shelves. The 200-m isobath is shown in gray. Inflow and outflow currents are depicted as green and purple arrows, respectively. (B) The rate of change in Chl a (milligrams per cubic meter per year) between 1998 and 2018. Subregions are delineated by gray lines. Black pixels indicate no data.

OW area (<50% sea ice cover) has increased by 27% in the AO between 1998 and 2018, with ~59,000 km2 of OW added each year (Table 1). Subregions that experienced significant increases in OW area (24 to 123%) included the Basin, Kara, Siberian, Barents, and Chukchi (Table 1). Increases in OW area in the Laptev and Beaufort subregions were nonsignificant, and changes in the outflow shelves of the Nordic, Canada, and Baffin subregions were negligible (Table 1). However, the rate of OW increase in the AO and all subregions, except the Nordic, has slowed considerably since 2009 (Fig. 2A and Table 1).

Table 1 Time series trends.

Regional time series trends for the AO and its subregions. Total percent change for the entire time series as well as slope of the regression (annual absolute change) for the entire time series (1998–2018), first decade (1998–2008), and the most recent decade (2009–2018) are shown. Values in parentheses for Chl a are rates of increase in the seasonal maximum Chl a concentrations, rather than the mean.

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Fig. 2 AO time series trends.

(A to C) Annual time series of AO (A) mean OW area, (B) mean Chl a, and (C) NPP. Results from regression analysis for the entire (1998–2018), early (1998–2008), and recent (2009–2018) parts of the time series are in black, red, and blue, respectively, with significant trends (P < 0.05) indicated by an asterisk.

At the same time, AO Chl a concentration increased significantly (22%) between 1998 and 2018 (Table 1), with almost all of the increase occurring since 2009 (Fig. 2B and Table 1). These changes were largely restricted to the Chukchi and Barents inflow shelves, where Chl a increased by 26 and 61%, respectively (Fig. 1B and Table 1). For both regions, three of the highest years of mean Chl a were measured in the past 4 years of the time series. Chl a also significantly increased in the smaller Baffin subregion (26%), with much of the increase occurring in recent years (Table 1). In all remaining subregions, Chl a showed no significant trend between 1998 and 2018 (Table 1). However, the slope of the Chl a trend in the shelf subregions shifted more positive between the first and second decades of the time series (Table 1). There were areas of intense increases in Chl a concentration along the shelf break of the interior seas, especially immediately north of the Beaufort, Laptev, and Barents shelf breaks (Fig. 1B).

Since 1998, satellite-based NPP in the AO has increased by 57% (Fig. 2C and Table 1), far outpacing previously estimated rates (24, 6). The most dramatic increases were on the eastern interior shelves (Siberian, Laptev, and Kara subregions), the inflow shelves (Chukchi and Barents subregions), and the Basin subregion (Table 1). The inflow shelves together contributed 70% of the AO NPP increase (Table 1), which is consistent with past studies that noted the importance of the Barents and Chukchi seas to AO NPP (2, 3, 18). A more modest yet statistically significant increase was seen on the western interior shelf (Beaufort subregion) (Table 1). The outflow shelves (Nordic, Canada, and Baffin subregions) exhibited the smallest percent increase in NPP, with the Nordic and Canada subregions showing no statistically significant trend (Table 1).

Historically, greater OW area and longer OW duration associated with sea ice decline have been the primary drivers of increased spatially integrated NPP across the AO (25). We found that although there were significant regional increases in OW duration (Table 1), there was no significant trend in OW duration across the entire AO, and OW duration was not a significant predictor of changes in AO NPP (Table 1). Although OW area significantly increased in the AO and most of its subregions (Table 1), these increases have slowed in recent years (Fig. 2A and Table 1). This recent deceleration in sea ice decline is likely due to internal climate variability temporarily masking human-induced changes (19). Regardless of the cause, although OW area explained 74% of the variance in AO NPP between 1998 and 2008 when sea ice was declining rapidly (Table 2), the relationship became less significant between 2009 and 2018, when rates of sea ice loss slowed, explaining only 20% of the variance in NPP (Table 2). This indicates that the recent increases in AO NPP were not driven by increases in OW area alone.

Table 2 Relative importance in predicting AO NPP.

Multiple linear regression parameter estimates (± standard error) for the intercept (teragrams of carbon per year), OW area (ratio of teragrams of carbon per year to square kilometer), and Chl a concentration (ratio of teragrams of carbon per year to milligrams Chl a per cubic meter) in explaining the variance in mean annual NPP (teragrams of carbon per year) across the AO for entire time series (1998–2018), first decade (1998–2008), and the most recent decade (2009–2018).

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We found that increased Chl a explained 80% of variance in AO NPP between 2009 and 2018 compared with only 26% during the previous decade, when changes in OW area controlled the trend in NPP (Table 2). Within the Barents subregion, which contributed more than any other region to AO NPP, significant increases in Chl a since 1998 sustained greater NPP despite the slowing of OW expansion (Table 1). Clearly, changes in phytoplankton biomass over the past decade were largely responsible for the sustained increase in NPP across the AO (Fig. 2C), particularly in the inflow shelves (Fig. 1B), despite the slowing of sea ice loss.

There are a few possible causes for the observed increase in phytoplankton Chl a over the past decade. Photoacclimation can lead to altered cellular Chl a concentrations, but incident light, mixed-layer depth, and light attenuation within the water column did not change sufficiently during our study period to significantly alter C:Chl a ratios in areas where Chl a increased (fig. S1), so this possibility can be eliminated. Earlier phytoplankton blooms (4) could intensify the mismatch between grazing and phytoplankton growth, resulting in higher Chl a concentrations in recent years. However, this possibility is diminished by annual changes in Chl a being the same in spring (April through June) as they were in summer (July through September) (fig. S2), when grazing rates would be expected to be highest. Interannual variability in atmospheric factors such as cloud cover (fig. S3), the state of the North Atlantic Oscillation and AO (fig. S4), wind speed (fig. S5), and the number of upwelling-favorable wind days per year (fig. S6) were also unrelated to the measured increases in Chl a.

In the AO, nitrogen availability limits maximum phytoplankton biomass (7), so the increases in Chl a being restricted to the inflow shelves and to the central Arctic, where sea ice had receded back from the shelf break, points to nutrients playing a role. This is supported by seasonal maximum Chl a concentrations, which would be especially sensitive to additional nutrient input, having increased at more than three times the rate of mean Chl a concentrations from 2009 to 2018 in the AO and the Barents and Chukchi seas (Table 1). Increased advection of Atlantic Ocean waters into the Barents Sea (20) and Pacific Ocean waters into the Chukchi Sea (21) may supply enough additional nutrients to sustain the higher biomass observed on these inflow shelves (Fig. 1B and Table 2). The Pacific inflow through the Bering Strait, which provides most of the nutrients that fuel Chukchi Sea summer blooms (22), has increased by ~50% from 1999 to 2015 (21). The “Atlantification” of the Barents Sea may be associated with increased advection of phytoplankton and nutrients (19, 2326). In addition, the incoming warm Atlantic water reduces stratification, which has not increased since 1979 (27), and promotes vertical mixing (28) that increases nutrient availability to sustain substantial increases of phytoplankton biomass and production (18). Last, decreased sea ice cover and increased frequency and intensity of storms at high latitudes (10) result in episodic nutrient injections from the historically inaccessible deep water beneath the pycnocline through increased internal wave mixing (11) and storm-induced upwelling (5, 28, 29) throughout the shallow shelves. Increased Chl a along the interior shelf break (Fig. 1B) may be fueled by upwelling events that pull “new” nutrients from deep basin reservoirs into the nutrient-depleted upper euphotic zone and that are increasingly common now that the ice edge regularly retreats north of the shelf break (12, 13, 30) and storms have become more frequent and intense (31).

Despite substantial sea ice loss, there are still regions of the AO, including much of the interior and outflow shelves, where there was either no change or a decline in Chl a concentration between 1998 and 2018. Apart from the few areas of the shelf break where Chl a was enhanced, Chl a generally declined across most of the interior shelves (Fig. 1B and Table 1). These waters receive large volumes of low-nutrient and highly turbid river runoff (30, 32), which suppresses NPP across the interior shelves (30). For example, the Kara subregion, which exhibited a significant 22% decline in Chl a (Fig. 1B and Table 1), has received an increasing amount of discharge from two of the three largest AO rivers (the Yenisey and the Ob) (32) that has been documented to suppress NPP on the Kara shelf (33). Similarly, the outflow and interior shelves may receive increasingly nutrient-depleted surface water from upstream consumption by phytoplankton on the productive inflow shelves, resulting in a decline in NPP downstream (2).

Previously, it was unclear whether NPP increases in the AO, which were linked only to increases in OW area and duration, were sustained by new or recycled nutrients (2, 3). Our study documents sustained increases in NPP between 1998 and 2018 that are no longer being driven by increased OW area and duration alone; increased phytoplankton concentration is playing an increasingly important role. These biomass increases must be sustained by a larger supply of new nutrients to the system. To the extent that increases in new nutrient availability are driven by processes associated with anthropogenic climate change, the future AO may become not only more productive but also more able to support additional higher trophic-level production and carbon export (34).

Supplementary Materials

Materials and Methods

Supplementary Text

Figs. S1 to S6

References (3644)

References and Notes

Acknowledgments: The authors thank M. Ardyna and M. M. Mills for their constructive comments on initial versions of the manuscript. Funding: This work is supported by NASA Earth and Space Science Fellowship grant NNX16AO08H awarded to K.M.L., NASA Earth and Space Science Fellowship grant RR175-257-4945576 awarded to K.R.A., and National Science Foundation grant 1304563 awarded to K.R.A. Author contributions: K.M.L. was responsible for formal analysis, funding acquisition, investigation, and writing (original draft). G.L.v.D. was responsible for data curation, investigation, software, formal analysis, and writing (reviewing and editing). K.R.A. was responsible for conceptualization, investigation, supervision, and writing (reviewing and editing). Competing interests: The authors have no competing interests. Data and materials availability: Bio-optical data used to develop the Arctic Chl a algorithm as well as time series data for Chl a, NPP, SST, OW area, and OW duration can be found on the Dryad data repository (35).

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