Institute of Marine Geology and Chemistry, National Sun Yat-Sen University, P.O. Box 59-60, Kaohsiung 804 24, Taiwan, ROC Received 5 July 2000; accepted 18 December 2002
Abstract
The uptake of atmospheric CO2by the oceans via the biological pump and the sustainability of fish catch are driven by new production of organic matter and its export into deep waters or its consumption by organisms of higher tropic level. The f-ratio based on15N measurements of discrete samples for continental shelf waters is around 0.4. However, the system-level constraints imposed by mass balance indicate that this f-ratio may be too high. Specifically, it is more than twice as the value determined on the basis of net export of organic carbon. Such a discrepancy is caused by the fact that, unlike the open-ocean system where remineralized nutrients below the euphotic zone do not return easily, the remineralized nutrients on the shelf reenter the euphotic zone quickly. Since new production based on direct 15N measurements on the shelf actually utilizes nutrients remineralized on the shelf as well, the value is higher than the net export of organic carbon sustained on external sources of nutrients. It is the net export of carbon, however, that sequesters CO2and sustains productivity on the shelf.
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1. Introduction
In light of the ongoing concern to evaluate future global environmental change, it is critical to understand the carbon cycle where the continental shelves play a major role because of their high biological productivity. Although, initially at least, the major international program aimed at studying the oceanic carbon cycles, the Joint Global Ocean Flux Study (JGOFS), focused mainly on vertical fluxes, it is increasingly being realized within the international research community that horizontal fluxes, especially those across the continental margins, are substantial (Chenet al., 1994;Smith et al., 1998). The land-ocean interaction in the
coastal zone program (LOICZ) was conceived to lead to a better understanding of these fluxes, and subsequently JGOFS teamed up with LOICZ to form a continental margins task team (CMTT).
The CMTT has concluded that the export of organic carbon from continental shelves (2 Pg C yr 1 to the intermediate and deep waters of the open oceans) accounts for some 20% of the global biological pump, and this is despite the fact that the shelves occupy less than10% of the global oceansurface. Inaddition, 0.15 Pg C yr 1 of organic carbon is buried in the sediments on shelves (Liu et al., 2000). Under the assumption of a steady state, these exports of organic carbon must be balanced by net horizontal inputs and by new production and are not directly related to primary production. In many papers referred to hereafter, it is not specified whether they report
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doi:10.1016/S0967-0645(03)00026-2
‘‘net’’ or ‘‘gross’’ primary production, but it is assumed here that ‘‘net’’ production was mea-sured.
The concept of partitioning net primary produc-tion into fracproduc-tions corresponding to new and remineralized production was originally developed for the open oceans based on the source and form of nitrogen (N) (Dugdale and Goering, 1967).
Essentially new production is that part of net primary productionthat relies uponallochthonous N sources, such as nitrate mixed in from the deeper oceanbelow, atmospheric deposits of various forms of N from above, and nitrogen fixation(Fig. 1a). New productionalso is consid-ered to be that portionof net primary production that canbe removed from the euphotic zone as dissolved and particulate organic matter (POM) are transported out of the mixed layer. Reminer-alized productionis the other part of net primary production and depends upon autochthonous N, principally NH3 and urea, derived from the metabolic end products of local biological pro-cesses.
The situationis more complicated onthe shelf in that riverine inputs of various forms of N contribute to the allochthonous N. Further more,
onshore advection of upwelled, subsurface water from offshore adds a major portionof ‘‘new’’ N to the shelf water (Wong et al., 1991; Chenet al., 1995; Nixonet al., 1996), which subsequently enters the euphotic zone (Fig. 1b) because of the shallow water depth combined with the effects of coastal upwelling, winds, tidal movements, not to mention cooling and vertical advection in winter.
These two sources, absent in the open ocean, contribute to new production in the shelf seas.
Further, unlike the open ocean, where particulate N transported out of the euphotic zone is slow in returning, on the shelf N is mostly remineralized in the relatively shallow water columnand inthe bottom sediments, and the physical movements mentioned above frequently transport the remi-neralized N back to the euphotic zone rather quickly.
Inorder to sustainthe ecosystem, new produc-tionmust be equal to the net export averaged over time. Data inthe literature have frequently provided an f-ratio (new production/net primary production; Eppley and Peterson, 1979; Knauer, 1993;Gorshkov et al., 2000) of around 0.4 based on the direct measurements of both new and primary productiononthe shelf (Harrisonet al.,
Fig. 1. Sketch of the main elements of (a) net primary production in the open ocean and (b) the export production on the continental shelf.
C.-T.A. Chen / Deep-Sea Research II 50 (2003) 1327–1333 1328
1987; Jiao et al., 1998; Chenet al., 1999, 2001).
Evenso, the f-ratio based on inputs of new nutrients or net exports of organic carbon is often more thana factor of 2 lower (Biscaye et al., 1994;
Li, 1995; Liu et al., 1995; Chen, 1996; Chenand Wang, 1999). This discrepancy may well be caused by any of a combination of the following factors:
(1) errors inprimary productionmeasurements;
(2) errors inthe Redfield ratios; (3) errors innet organic carbon export; (4) errors in new produc-tion; (5) a mismatch of definitions. What follows here is a case study mainly derived from data from three of the most detailed analyses (Chenand Wang, 1999;Chenet al., 1999, 2001) for the East China Sea (ECS) shelf to date.
2. Primary production
There are now numerous data sets vis-"a-vis primary productivity inthe ECS, and these are particularly valuable due to their extensive geo-graphic and temporal coverage. Chen and Wang (1999) chose to use a value of 438 mg org C m 2d 1(Zhang, 1991), based onvery extensive
14C and chlorophyll a assimilationdata collected from 173 stations in all four seasons. Ning et al.
(1995) obtained 448 mg org C m 2d 1 based on data from 64 stations, again in all four seasons, using the same method. These values are similar to the latest, albeit smaller scale, estimates of 549 mg org C m 2d 1for the southernECS byGong et al.
(2000)and 400 mg org C m 2d 1for the ECS, also based onthe 14C method (G.C. Gong, private communication, 2000). The14C method may have its shortcomings (e.g. Platt and Harrison, 1985), but it remains one of the most widely used methods (Parsons et al., 1990) and is precisely the one recommended by JGOFS. On the other hand, Chenet al. (1999) obtained an average primary productivity value of 530 mg org C m 2d 1, based onthe 13C method, for the mid-to-south ECS excluding the intensive upwel-ling region northeast of Taiwan.Chenet al. (2001) obtained similar values (except at the two coastal stations) in the ECS also based on the13C method.
Since these measured values are all similar, differences in primary productivity cannot account
for the factor-of-2 difference in the f-ratio. Finally, evenif all primary productivity data erred by a certain factor, it would still not account for the factor-of-2 difference since primary productivity is the denominator in the calculation of the f-ratio.
Simply put, systematic errors would cancel each other out.
3. Redfield ratios
Phytoplankton produces POM during photo-synthesis, which consumes dissolved inorganic carbon (DIC) and mainly nitrate (NO3) an d phosphate (PO4). The elemental ratios of carbon (C) and phosphorus (P) within freshly produced POM are found to be similar in oceans all over the world. The widely used Redfield ratio suggests that the concentration changes in DIC and nutrients during production and remineralization of POM are approximately inthe same ratio (Redfield et al., 1963). Making reference to Redfield’s concept of a coupling between DIC and nutrient concentrations and elemental ratios of POM, Dugdale and Goering (1967) deduced the descriptionof new production and its nutrient limitations. To be more exact, productionis defined as the amount of phytoplanktonproductionbased onnitrate uptake that can be converted to carbon units using the elemental ratios of POM.Chenet al. (1999, 2001), indeed, calculated new productivity based on the Redfield C/N ratio.
Following the same reasoning,Chen and Wang (1999)calculated new productivity and the f-ratio (0.12) based onthe Redfield C/P ratio. Well aware that the C/N/P ratio for both dissolved and particulate material may vary from place to place and that there may be some preferential recycling of nutrients (Doney et al., 1996; Thomas and Schneider, 1999;Thomas et al., 1999),Chenet al.
(1996) reported that the stoichiometry of the particulate matter inthe westernNorth Pacific marginal seas is consistent with the Redfield ratio.
New data (Chen, 1998) also have emerged for the ECS, such as the fact that the POC/PON ratios in the euphotic zone average 7.570.5. These ratios in the aphotic zone average only slightly higher at 8.470.6. A higher POC/PON ratio inthe aphotic
C.-T.A. Chen / Deep-Sea Research II 50 (2003) 1327–1333 1329
zone would mean a larger export of organic carbonout of the shelf compared with the 15 N-based new production values. Therefore, this cannot explain the lower f-ratio based on the net export of organic carbon.
Unfortunately, little information is available to allow for the estimationof DOC/DON/DOP ratios, but the preliminary data of Chen(1998) seem to indicate that the DOC/DON and DOC/
DOP ratios also must be higher inthe aphotic zone, meaning that they cannot explain the lower f-ratio on the basis of the net export of organic carbon. In view of the general consistency in the reported Redfield ratios all over the world, the use of either C/N or C/P for the calculationof new production should not be a matter of concern.
Another illustration of this is the independent estimate made by Chen and Wang (1999) of new productivity based onthe difference betweenthe total organic carbon outflux and influx. The corresponding f-ratio of 0.15 agrees very well with that from P. Such a good agreement, again, indicates that the Redfield ratios do not show any significant error.
4. Net export of organic carbon
Net export is takento be the difference between the total export and the total input. The former includes such factors as net burial in the sediments, offshore transport of sediments, and offshore transport of dissolved and POM by the offshore flow, whereas the latter includes riverine, aeolian, nitrogen fixation, and upwelling, as well as other onshore flows (Figs. 1b and 2b).
The end result is that there are now several estimations of net export of organic carbon from the ECS. As stated earlier,Chen and Wang (1999) calculated the net export of organic carbon and determined it to be 52716 mg org C m 2d 1 based onP budgets, and 64732 mg org C m 2d 1 based onC budgets. These values agree reasonably well with those of Li (1995), i.e. 80 mg org C m 2d 1 and Chen(1996), i.e. 73722 mg org C m 2d 1, all for the ECS. It is worth noting, however, that although the groundwater input of nutrients is taken into account in the budgets of
Chenand Wang (1999), the marine groundwater is not because there are no data available.
5. Newproduction
Despite the emergence of other methods (e.g.
Wong, 2001), one of the most widely used methods to estimate new production employs 15N. This method measures the new production of organic nitrogen, which is subsequently converted to the new production of organic carbon using the Redfield C/N ratio (Dugdale and Goering, 1967;
Chavez and Toggweiler, 1995). So far the only three comprehensive studies of new production in the ECS have all used the15N technique in discrete samples. Jiao et al. (1998) obtained data only in spring, and the values they obtained range between 15 and 1372 mg org C m 2d 1. Unfortunately, those authors did not provide any numerical data or the average value. They did, however, give an average f-ratio of 0.38.
Spring, summer and fall production values measured byChenet al. (1999) range between 70 and 340 mg org C m 2d 1, and average 170 mg org C m 2d 1outside the intensive upwelling zone northeast of Taiwan. This gives an f-ratio of 0.48 for the upwelling region (including the coastal zone near China) and 0.34 for the continental shelf at a considerable distance from the upwelling regions.Chenet al. (2001) recently repeated their measurements in the ECS in summer and winter, obtaining new production values that range between80 and 550 mg org C m 2d 1away from coastal areas. The average f-ratio of Chenet al.
(1999, 2001) is 0.38 inregions away from the coastal and intensive upwelling regions, in perfect agreement with the value ofJiao et al. (1998).
6. Mismatch of definitions
It seems hard to deny that there is somewhat a mismatch of definitions for new production. To illustrate this point, Li (1995), Chen(1996) and Chenand Wang (1999)calculated new production on the basis of the amount of nutrients from new sources that enter the shelf.Chenand Wang (1999)
C.-T.A. Chen / Deep-Sea Research II 50 (2003) 1327–1333 1330
also worked under the assumption that the net organic carbon exported out of the water column is equivalent to new production on the shelf.
MeanwhileLiu et al. (1995)considered the sinking flux of POC out of the euphotic zone as new production.
To demonstrate the inconsistencies in approach further, Jiao et al. (1998) and Chenet al. (1999, 2001) used the 15N technique to measure new productioninthe euphotic zone. Onthe basis of this, nitrate diffused or advected to the euphotic zone from the deep and bottom shelf waters, in addition to the nitrate advected onshore from offshelf waters, all fuel new production (Fig. 2a).
By contrast,Li (1995),Chen(1996)andChenand Wang (1999) considered only the portion of nutrients advected onshore or from riverine and aeoliansources as factors that trigger new production.Chenand Wang (1999)also presented a carbonbudget based onthe mass-balance of sources and sinks across the land-shelf, shelf-sediments and shelf-open ocean boundaries (Fig. 2b). What takes place withinthe euphotic and aphotic zones is strictly internal and does not affect the mass-balance. The difference between the total outflux and the total influx is the net export of organic carbon.
Previously, new productivity was interpreted as that part of total organic carbon fixed by phytoplankton that can be removed without destroying the long-term integrity of the pelagic ecosystem (Quinones and Platt, 1991). Integrated over some period of time, new production must be equal to the maximum amount of organic matter that the system canexport without losing biomass or having an external organic matter subsidy (Smith, 1988). Naturally, the
15N method gives higher values because the remineralized nitrate in the sediments and in the deep and bottom waters of the shelf is partly diffused or advected back to the euphotic zone, thus contributing to new productivity (Figs. 1b and 2a; Jickells et al., 1991). Whenthe shelf is considered as an ecological system, however, such nutrient supplies are still internal. In other words, although the euphotic zone may export about 40%
of net primary production, half of the export returns from the aphotic zone, with only the remainder buried in the sediments or transported offshore. As a result, shelves canonly sustaina smaller net export of organic carbon out of the water column. Net export represents only half of new production based on the 15N technique for the ECS.
Fig. 2. Sketch of (a) the main external sources of nitrate related to the 15N-based new production in the euphotic zone of the continental shelf, and (b) the main external sources and sinks of organic carbon related to the mass-balance export production of the continental shelf.
C.-T.A. Chen / Deep-Sea Research II 50 (2003) 1327–1333 1331
7. Conclusions
It canbe concluded that, based onthe 15N method, the f-ratio of the ECS shelf consists of remineralized nitrate transferred back to the euphotic zone. As a consequence, the value is higher thanthe f-ratio calculated solely onthe basis of the external supply of nutrients from outside of the shelf area, or from the mass balance of organic carbon. Since new production as originally defined was generally based on the 15N method, the present author suggests that the definition be maintained. Instead, the f-ratio calculated interms of the external supplies of nutrients or the mass-balance of organic carbon for the ECS is really related to the export of net organic carbon transported off the water column.
Accordingly, it should be termed the e-ratio (net export of organic carbon/net primary production).
The f- an d e-ratios inthe openoceanshould be approximately equal. Onthe other hand, the e-ratio should be smaller thanthe f-e-ratio onthe shelf since part of the organic carbon transported out of the euphotic zone, but not out of the shelf, is remineralized on the shelf. Subsequently, part of the remineralized nutrients are transported back to the euphotic zone to support the new production, thus making the f-ratio higher.
Acknowledgements
This work has beensupported by the National Science Council of the Republic of China (NSC 89-2611-M-110-001). Profs. S.V. Smith, G.T.F.
Wong, T. Platt, T. Parsons, K. Habbard and two anonymous reviewers have provided valuable comments.
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