Technical Comments

Regional Carbon Imbalances in the Oceans

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Science  11 Jun 1999:
Vol. 284, Issue 5421, pp. 1735
DOI: 10.1126/science.284.5421.1735b

Recent studies (1, 2) have suggested that respiration exceeds photosynthetic oxygen production in large areas of the oceans. If correct, the conclusion has profound implications for our understanding of the oceanic carbon cycle. C. M. Duarte and S. Augusti conclude that four-fifths of the ocean are net heterotrophic, with photosynthesis providing for only 75% of respiration (2). We estimate this shortfall as 0.5 petamole C year−1 (3), which is difficult to account for. Nonlocal sources such as river and aeolian input probably contribute no more than 0.015 petamole as a whole to the open oceans (4), that is, only 3% of the calculated shortfall. Major inputs from upwelling dissolved organic carbon (DOC) or from the net autotrophic areas are unlikely because they would be associated with concurrent input of nutrients and consequent eutrophication. Furthermore, they would also require massive water transport—perhaps 50 to 1500 sverdrups (5), which is a flow comparable to or many times greater than the Gulf Stream. Thus, there are major difficulties balancing the proposed regional deficits with nonlocal sources, even in combination. An alternative analysis based on depth integrations of individual productivity stations gave no evidence for major systematic imbalances (6). Because the data sets used in all three studies are similar (6), one comes to the conclusion that the discrepancy must lie in the form of analysis.

Duarte and Agusti (2) used an allometric equation in reaching their conclusion: R =aP b, where R is the community respiration rate, a and b are operational constants, andP is the gross primary production rate. This equation is an unsatisfactory model when extrapolating across ecosystems of widely differing productivities because the term “a” is not a constant, but dependent on the scale of local photosynthesis [table 1 in the report (2)]. The R =aP b relationship attempts to fit a single curve to a series of curves (parallel lines in the case of a log-log plot). This ascribes a single value for respiration to each value of photosynthesis, which effectively treats oligotrophic areas as the lower part of the water column of more productive ones. The result is that the critical value whereR = P is wrongly evaluated. As an illustration, we have examined a simple situation and show the general relationship betweenP and R for a balanced water column to beR = bP 0 (1 − b) P b(7). Even when all the water columns in the data set are in balance, if an intermediate relationship is used, there would be an overestimate of respiration for areas of low photosynthesis and the reverse at high photosynthesis, the degree of error depending on the distribution of photosynthetic observations in the data set (Fig. 1). Thus, the conclusion (2) that substantial areas of the ocean are in organic deficit is very likely to be a product of an oversimplistic analysis. We would conclude, rather, that there is (6, p. 57) “no evidence to suggest that the open oceans, either as a whole or regionally, are substantially out of organic balance.” Our analysis does not preclude the possibility that major imbalances exist, but such a conclusion would need to come from detailed studies of the areas of the ocean concerned, and not from generalized relations obtained across different systems.

Figure 1

Relation of photosynthesis and respiration based on the equation R =bP 0 (1 − b) P b (7). Dashed line indicates P = R. Two solid black lines showP versus R relation for two values ofP 0. Dots indicate the particular value whereP = R. Red line is from the equation given by Duarti and Agusti (2). Arrows show the movement of the line consequent to the simplifying assumption of a single relationship. Units are μmoles dm−3 day−1.


  1. We are indebted to S. Sathendraynath, S. Smith, and D. Kirchman for invaluable advice and guidance.

Response: Is the open ocean heterotrophic? Taken as an entire ecosystem, and at long time scales, the world's oceans respire more organic C than they produce by primary production. That is, the importation of terrestrial organic C from rivers exceeds burial in the sediments by on the order of 25 Tmol year−1(1). Most geochemists concur that this simple budget implies that biotic processes in the sea are supported, in part, by subsidy from land. Whether the pelagic surface waters exhibit the same net heterotrophic nature of the ocean as a whole remains controversial (2–5). This controversy may partially derive from different methods of analysis, although not in the way argued by Williams and Bowers (6). Rather, the conclusion that biological production (P) generally exceeds respiration (R) in the open ocean (5) appears to be a product of the choice of analysis (7). In addition, the data sets they use are not particularly well suited for examining the balance between Rand P in the open ocean, which was not the main goal of some of the studies (2, 3). In particular, the data set Williams used to specifically address this question (5) was biased towards highly productive waters (8), because the mean depth-integrated value of P in the data set [122 mmol O2 m−2 day−1 or 1500 mg C m−2 day−1, calculated with the use of a photosynthetic quotient of 1.0 (5)] is more than fourfold greater than the average primary production of the open ocean [approximately 350 mg C m−2 day−1(9)]. In Williams' data set (5), 97% of the data exceed this average oceanic value ofP.

Figure 1

Average depth-integrated planktonicP/R ratio in oceanic regions of different gross phytoplankton production (GPP). GPP and P/R values in the data set resulting from combining the data used by Duarte and Agustı́ (3) and Williams (5) were binned (13) for areas with comparable GPP's (< 30, 30 to 100, 100 to 300, 301 to 1000, 1001 to 3000, 3001 to 10,000, and > 10,000 mg C m−2 day−1) and then averaged (open circles). Regional averages of GPP and P/R reported by Williams in table 1 of (5) (black circles) show the same pattern of declining P/R ratios with declining GPP within a narrower range of GPP. Trend towards declining P/R with decreasing GPP is highly statistically significant (R2= 0.75, p < 0.001). All data were converted to mg C m−2 day−1 and assume PQ = 1 (5).

The conclusion that the surface waters of the open oceans are generally autotrophic and in metabolic balance (5) is, therefore, flawed by the extrapolation from unusually productive waters to the global open ocean with the underlying assumption that P/Rdoes not vary systematically with P. The bias towards highly productive systems in the relation between R andP results because observations on the balance between production and respiration in the oligotrophic ocean are still few. Unbiased analyses should, therefore, be derived from studies of the balance between R and P in individual areas of the ocean, which are best summarized by the resulting P/Rratios (3, 10), to then test for systematic variations in this balance across systems. The data set assembled by Williams shows a decline in the ratio P/R with declining primary production across regions (Fig. 1). It is not possible, with the use of Williams' data, to further extend this pattern because there are no data below 350 mg C m−2 day−1, but we combined the existing data sets (3, 5) to further compare theP/R ratios in unproductive (that is, below the average oceanic P of 350 mg C m−2 day−1) and productive regions of the sea. The P/R ratio of the unproductive communities tended to be (Wilcoxon sign ranked test,p < 0.05, z = −2.2) below the value of 1.0, indicating respiration to exceed production, whereas the reverse holds for productive ocean regions (Wilcoxon sign ranked test,p < 0.001, z = −6.4) and demonstrates that the declining pattern in P/R extends to the most oligotrophic areas (Fig. 1), where the biota tend to be a net source of CO2. This analysis confirms that the P/R ratio in the biogenic layer of the oligotrophic ocean tends to be below unity and that the biota is a net source of CO2.

The annual organic carbon input needed to support the excess organic carbon consumption in the unproductive areas of the open ocean has been estimated at 0.5 Pmol C by Williams and Bowers. This estimate of deficit is only indicative, for it is extrapolated from a comparative analysis (3), but it suggests the utilization of large amounts of allochthonous organic matter in these oligotrophic areas. Yet, it does not imply that the overall P/R ratio, which is driven by the highly productive oceanic areas, is less than 1. The carbon deficit in oligotrophic areas may be met by carbon surpluses from the most productive areas, which export about 0.46 Pmol C annually (11). The production of this excess carbon is not homogeneously distributed over the autotrophic 20% of the ocean's surface, but is concentrated in an area comprising at most 5% of the ocean surface (12). That the excess carbon produced in the coastal zone is exported to the unproductive open ocean follows from the consideration that only about 0.012 Pmol C are buried annually in the coastal zone (11), and that there is no evidence of a long-term increase in the organic carbon concentration of coastal waters. That the export from the coastal zone is a significant source of carbon to the open ocean, where it fuels heterotrophic metabolism (13), appears to be well established (14, 15).

The conclusion that allocthonous inputs of organic carbon are essential for the functioning of the oligotrophic ocean should promote research aimed at quantifying these inputs and their sources, and to expand the presently meager empirical basis on pelagic R andP estimates there, because extrapolation from highly productive situations can lead to misleading perceptions of the functioning of the open oceans. To dismiss the pattern towards heterotrophy in the oligotrophic ocean as artifactual or conceptually impossible does not account for the bulk of the available empirical evidence.


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