The effect of increasing levels of atmospheric carbon dioxide on carbon uptake in and export from the upper ocean is one of the big questions in environmental science. But it can be tackled experimentally.
Marine phytoplankton are major players in the carbon cycle, accounting for about 50% of the global biological uptake of carbon dioxide1. Near the ocean surface, these single-celled organisms use light energy to convert CO2 into organic molecules for building cellular structures and driving their metabolism. Some of this organic carbon eventually sinks into the deep ocean, where most of it is either converted back to CO2 or sequestered in sediments. This 'biological pump' effectively removes CO2, a greenhouse gas, from the atmosphere for hundreds to millions of years.
On page 545 of this issue, Riebesell et al.2 describe evidence that the biological pump may become stronger at elevated concentrations of CO2 in the atmosphere, and thus provide a negative feedback on increasing atmospheric CO2. According to their calculations, that feedback has accounted for about 10% of the extra CO2 pumped into the atmosphere since pre-industrial times (the past 200 years or so).
Since industrialization, atmospheric CO2 has risen from about 280 parts per million (p.p.m.) to more than 385 p.p.m., increasing by some 2 p.p.m. per year during the past decade. Each year, approximately 25–30% of anthropogenic CO2 enters the surface ocean, where it increases both the concentration of dissolved inorganic carbon (DIC) and acidity. The latter has potentially adverse consequences for phytoplankton that require calcium carbonate to build their shells. Although the oceans are Earth's largest reservoir for DIC, only about 1% is in the form of CO2, the molecule required by the photosynthetic enzyme rubisco. At the low CO2 concentrations typical of sea water, rubisco operates at rather low efficiency3. So increasing ambient concentrations of CO2 in sea water could boost photosynthetic efficiency and increase biological uptake of anthropogenic CO2, just as some marine phytoplankton use intracellular carbon-concentrating mechanisms to increase their photosynthetic capacity.
This is the context for Riebesell and colleagues' research2 into how phytoplankton might respond to increasing CO2 concentrations. They conducted CO2 manipulations in large cylindrical enclosures called mesocosms that were placed in a fjord in southern Norway and extended from the surface to a depth of approximately 9–10 metres. Although this approach is complex and logistically difficult, the advantage is that mesocosms are exposed to the same environmental influences as the surrounding waters, making them reasonable analogues for natural systems. And they can be manipulated experimentally. In Riebesell and colleagues' study, phytoplankton were grown in different mesocosms with the partial pressure of CO2 adjusted to simulate the present (350 µatm) or projected future (2 × present CO2, 700 µatm, and 3 × present CO2, 1,050 µatm) atmosphere.
What the authors found was intriguing. Uptake of CO2 by phytoplankton (mainly bloom-forming diatoms and coccolithophores) in the 2 × CO2 and 3 × CO2 treatments was 27% and 39% higher, respectively, than in the present-day CO2 treatment. But the additional CO2 removed from surface waters at elevated CO2 was not balanced by increases in particulate organic carbon (POC) in the surface layer. Furthermore, the loss of nitrate from the surface waters was the same in all three CO2 treatments, indicating that the ratio of carbon to nitrogen uptake increased at higher CO2 concentrations whereas the cellular carbon/nitrogen ratio of the phytoplankton remained unchanged.
This result suggests that, although higher ambient CO2 concentrations increased CO2 uptake by phytoplankton, the additional carbon incorporated into cells was rapidly lost as dissolved organic carbon (DOC). However, although DOC concentrations in the mesocosms increased, these were insufficient to balance the measured CO2 deficits. In nature, organic molecules excreted from phytoplankton (for example, as DOC), or otherwise lost as these organisms die or are grazed, can coalesce to form semi-solid structures called transparent exopolymer particles (TEPs). These structures are sticky and facilitate the aggregation and increased sinking speeds of other particulate matter. In the mesocosms, TEP concentrations increased fourfold during the experiment (the carbon content of these TEPs is not presented by Riebesell et al.).
The authors propose that accumulations of TEPs in the elevated-CO2 treatments facilitated aggregate formation, increasing the flux of particulate matter from the mesocosm surface. Coupled with higher DOC production, this may explain why POC did not increase in the elevated CO2 treatments. Thus, it seems that increased CO2 uptake fuelled by higher CO2 concentrations was rapidly converted to DOC and TEPs, and any additional carbon incorporated into POC was lost from the surface of the mesocosm owing to increased particle aggregation and sinking (Fig. 1). Assuming that their results are representative of the larger ocean, increased atmospheric CO2 may lead indirectly to increased particle fluxes from the surface ocean to depth, providing a negative feedback to increasing atmospheric CO2 concentrations. Unfortunately, the authors did not measure POC sinking fluxes in their mesocosms to confirm this link.
Nevertheless, there are some notable conclusions to be drawn from this study. First, although CO2 uptake by phytoplankton may be stimulated in a high-CO2 world, this negative feedback will only partly offset expected increases in atmospheric CO2. In fact, Riebesell et al. perform some clever calculations to show that the CO2-enhancement effect they identified has probably reduced the rise in atmospheric CO2 by only 11 µatm (about 10%) since the dawn of the industrial revolution.
More importantly, their study provides a vivid example of the fact that ocean biology is not in steady-state and that fundamental biological and biogeochemical processes are likely to respond to climate change, resulting in either positive or negative feedbacks that are difficult to predict. One positive feedback between biology and climate has already been identified, whereby future increases in stratification of the Southern Ocean could favour types of phytoplankton that have a reduced capacity to take up CO2 (ref. 4). Conversely, increased CO2 has been shown to enhance fixation of free nitrogen, thereby relaxing nutrient limitation by nitrogen availability and increasing CO2 uptake5. Riebesell and colleagues document another negative feedback whereby CO2 use by the dominant bloom-forming groups of phytoplankton could increase as atmospheric levels of CO2 rise. Neither these, nor other possible non-steady-state biological feedbacks, are currently accounted for in models of global climate — a potentially serious omission, given that the biological pump is responsible for much of the vertical CO2 gradient in the ocean.