Ocean margins as a signiﬁcant source of organic matter to the deep open ocean

Continental shelves and slopes comprise less than 20% of the world ocean area, yet they are proposed to be quantitatively important sources of the organic matter that fuels respiration in the open ocean's interior,. At least certain regions of the coastal ocean produce more organic carbon than they respire, suggesting that some fraction of this non-respired, unburied organic carbon is available for export from the coastal to the open ocean. Previous studies of carbon fluxes in ocean margins,, have not considered the potential roles of dissolved organic carbon (DOC) and suspended particulate organic carbon (POCsusp), even though both pools are quantitatively far larger than sinking POC. Here we report natural radiocarbon (14C) abundance measurements that reveal continental slope and rise waters to contain both DOC and POCsusp that are concurrently older and in higher concentrations than DOC and POCsusp from the adjacent North Atlantic and North Pacific central gyres. Mass-balance calculations suggest that DOC and POCsusp inputs from ocean margins to the open ocean interior may be more than an order of magnitude greater than inputs of recently produced organic carbon derived from the surface ocean. Inputs from ocean margins may thus be one of the factors contributing to the old apparent age of organic carbon observed in the deep North Atlantic and Pacific central gyres.

Continental shelves and slopes comprise less than 20% of the world ocean area, yet they are proposed to be quantitatively important sources of the organic matter that fuels respiration in the open ocean's interior 1,2 . At least certain regions of the coastal ocean produce more organic carbon than they respire 3 , suggesting that some fraction of this non-respired, unburied organic carbon is available for export from the coastal to the open ocean 4 . Previous studies of carbon fluxes in ocean margins 1,5,6 have not considered the potential roles of dissolved organic carbon (DOC) and suspended particulate organic carbon (POC susp ), even though both pools are quantitatively far larger than sinking POC. Here we report natural radiocarbon ( 14 C) abundance measurements that reveal continental slope and rise waters to contain both DOC and POC susp that are concurrently older and in higher concentrations than DOC and POC susp from the adjacent North Atlantic and North Pacific central gyres. Mass-balance calculations suggest that DOC and POC susp inputs from ocean margins to the open ocean interior may be more than an order of magnitude greater than inputs of recently produced organic carbon derived from the surface ocean. Inputs from ocean margins may thus be one of the factors contributing to the old apparent age of organic carbon observed in the deep North Atlantic and Pacific central gyres [7][8][9] .
The radioisotopic form of carbon, 14 C (half-life, 5,730 yr), can be used as an indicator of the average age of bulk marine organic carbon pools such as DOC and POC. In addition to natural cosomogenically produced 14 C, the increase in the global inventory of 14 C as a result of nuclear weapons testing during the late 1950s and early 1960s also allows us to use bomb-produced 14 C to constrain the age of more recently formed (over the past ϳ40 years) organic carbon pools 10 . The D 14 C (defined as the deviation in parts per thousand (‰) from the 14 C activity of nineteenth century wood) values of natural marine organic carbon have been found to range from as low as around −525‰ ( 14 C age of ϳ6,000 yr BP) for deep ocean DOC 8 to as high as about +140‰ for suspended POC samples containing bomb 14 C in the mid-to late 1980s (ref. 9).
Samples for 14 C isotope analysis of DOC and POC susp were collected from the western North Atlantic (WNA) and eastern North Pacific (ENP) continental margins. In April 1994, samples were collected from 4 depths at each of three WNA sites located over the continental slope in the Middle Atlantic Bight region between eastern Long Island, New York, and Cape Hatteras, North Carolina. The Bight is characterized by a permanent thermohaline front between continental shelf and slope waters and a net southwestward flow of slope water, of which ϳ50% is entrained across the front into slope waters and the remainder is advected offshore near Cape Hatteras 5 . The depth of the WNA mid-slope sites ranged from ϳ1,100-1,500 m. Samples were also collected from the eastern North Pacific from 1991 to 1993 at a time-series site located at the base of the continental rise (ϳ4,100 m depth) at 34Њ 50Ј N, 123Њ 00Ј W 11,12 , and previously in 1985 at a site in the Santa Monica basin of the California continental borderland 13 . The ENP site is located ϳ220 km off the coast of central California within the California current system and is influenced by spring-summer maxima in primary productivity and sinking POC fluxes as a result of seasonal upwelling 14 .
The D 14 C values of DOC from shallow surface waters (5 m depth) of the WNA continental slope were highly variable, ranging over ϳ200‰ (Fig. 1a). In mid-depth slope waters (ϳ300 m and 750 m; Fig. 1a), D 14 C-DOC values were significantly lower (that is, more negative in D 14 C) by 75 to 150‰ relative to DOC from similar depths in the central north Atlantic gyre (−276 to −260‰ in the Sargasso Sea (SS) 8,9 . By 1,000 m depth, the D 14 C-DOC profiles of WNA slope water and those of SS water converged towards similar values. These data indicate the presence of 14 C-depleted DOC at mesopelagic depths in WNA slope waters. On the basis of its ␦ 13 C values (␦ 13 C range: −21.3 to −22.4‰; J.E.B., unpublished data), this DOC appears to be predominantly marine in origin (fully marine DOC has ␦ 13 C values ranging from about −22 to −18‰).
The D 14 C values of POC susp from the WNA ranged from −190 to +80‰ and were significantly lower than D 14 C of POC susp from the SS 9 (Fig. 1b). D 14 C values more positive than about −70 to −40‰ are considered to be post-bomb (that is, later than early 1950s to early 1960s thermonuclear weapons testing) because the pre-bomb D 14 C of the temperate and tropical surface ocean was in this range 15 . The ␦ 13 C values in POC susp (range: −22.9 to −24.9‰; J.E.B., unpublished data) suggest that terrestrial carbon (with an assumed average ␦ 13 C Ϸ Ϫ 27‰) may have contributed slightly more to POC susp than to DOC in WNA slope waters. The similar offsets in D 14 C for both DOC and POC susp between the WNA and the SS (Fig. 1a, b) suggest that the same or related mechanisms may control inputs of 14 C-depleted DOC and POC susp to WNA slope waters.
Similar to the WNA, profiles from the ENP also indicate a net depletion in 14 C (that is, more negative D 14 C values) of both DOC and POC susp relative to the central North Pacific (CNP) gyre 7,9 (Fig.  1c, d). The lowest D 14 C-DOC values in the ENP occurred, also like the WNA, at shallow to intermediate depths (0-700 m), and D 14 C-DOC values in the ENP were lower than in the CNP at all depths samples (Fig. 1c). The D 14 C-DOC values in Santa Monica basin were also, with the exception of the single 850-m sample, lower than values in the CNP (Fig. 1c). Significantly lower D 14 C values of POC susp were likewise observed at all depths in both the ENP and Santa Monica Basin 13 relative to the CNP gyre (Fig. 1d). The average difference in D 14 C-DOC between WNA and SS waters was greater than the corresponding margin-central gyre difference in the North Pacific (compare Fig 1a, c); the margin-central gyre offset in D 14 C of POC susp was also greater overall in the North Atlantic (compare  Concentrations of DOC were greatest in shallow (0 to ϳ100 m) WNA (J.E.B., unpublished data) and ENP 12 slope and rise waters and decreased with increasing depth. With the exception of ϳ300 m depth in the WNA and 0 to 700 m depth in the ENP, DOC in slope and rise waters exceeded by 4-9 M those concentrations measured previously in North Atlantic and Pacific central gyre waters [7][8][9] (Table  1). Suspended POC concentrations were up to an order of magnitude higher in surface waters of the slope and rise than in surface waters of both the SS (J.E.B., unpublished data; ref. 9) and CNP 9 . At depths уϳ500 m, POC susp concentrations in slope and rise waters were in all cases ϳ2-3 times (2-3 g C l −1 ) greater than in the deep SS and CNP, where POC susp concentrations were ϳ0.6-1 g C l −1 ( Table 1).
The elevated DOC and POC susp concentrations in slope (in the WNA) and rise (in the ENP) waters, together with lower D 14 C values in both pools, indicate that organic matter older than that in the North Atlantic and Pacific central gyres is present in ocean margins and that it is potentially available for export to the open ocean. The origin(s) of this old, 14 C-depleted carbon to continental slope and rise waters is (are) not known, but several possibilities may be considered. In the WNA, the reintroduction to the water column of old sedimentary organic carbon (both as DOC and POC susp ) from weathered shelf and upper slope sediments 16,17 may contribute to the highly 14 C-depleted (D 14 C as low as about −700‰) colloidal and dissolved organic carbon observed in near-bottom waters in the Middle Atlantic Bight 18 as well as to the 14 C-depleted POC susp (Fig.  1b). The WNA may also at times be influenced by upwelled Antarctic Intermediate Water 19 which could contain a component of older, higher-concentration DOC. However, this mechanism is unlikely to account for the elevated concentrations of 14 C-depleted POC susp also found in the WNA (Fig. 1b). Finally, the presence of trace amounts of hydrocarbons (with D 14 C of about 1,000‰) from submarine seeps off California 20 could impart lower-than-average D 14 C values to the DOC pool (but less likely so to the POC susp pool) of the ENP compared with areas remote from seepage (such as the CNP). Thus, the older DOC and POC susp in these two ocean margin systems may arise from multiple system-specific sources or from a common source such as weathered shelf and slope sediments.
The DOC of surface open ocean waters can be shown conceptually to consist of a mixture of both old, conservative material that has aged in the deep ocean and of young labile material recently produced in the photic zone 9,21,22 . Using a mass-balance approach, it has been calculated 9 that surface seawater D 14 C-DOC values for the central North Pacific and North Atlantic Oceans are −155‰ and −214‰, respectively, which agree well with measured values of −153‰ and −210‰, respectively. A similar calculation is made here for surface (5 m) slope water of the central WNA, which has the highest D 14 C-DOC value (−107‰; Fig. 1a) of all WNA slope waters examined. The background DOC from deeper (300-1,000 m) waters of the central WNA slope has a mean concentration of 52 M (J.E.B., unpublished data) and a mean D 14 C of −421‰ (Fig.  1a). The DOC concentration of surface slope water is ϳ91 M (J.E.B., unpublished data), giving a calculated D 14 C of the 'excess' surface DOC component (with a concentration of 91 M minus 52 M, or 39 M) of +311‰. This D 14 C value is high and similar to previous measurements of humic substances in Amazon river water made in 1984 (D 14 C ¼ þ230‰) 23 and reflects the input of postbomb, terrestrial carbon to shallow central WNA slope waters which are influenced by inputs from rivers and estuaries.
The same calculation when applied to southern WNA waters yields a different conclusion. Using a deep, background mean DOC concentration of 51 M (J.E.B., unpublished data) and a D 14 C-DOC value of −435‰ (Fig. 1a) and a DOC concentration and D 14 C-DOC value in shallow slope waters of 83 M (J.E.B., unpublished data) and −306‰ (Fig. 1a) (Table  1). We can estimate by 14 C mass balance the relative potential contributions of each of these sources to the deep North Atlantic and Pacific using the following simplifying assumptions: (1) the deep central North Atlantic and Pacific are in steady state with respect to D 14 C values and concentrations of DOC and POC susp (refs 7-9); (2) the two dominant sources of DOC and POC susp to the deep central gyres are lateral inputs of 14 C-depleted material derived from the margins and vertical inputs of 'modern', 14 C-enriched material derived from surface ocean production 11 ; and (3) the margin-to-deep open ocean and surface-to-deep open ocean gradients observed in these studies are representative of the North Atlantic and Pacific as a whole. We find that in order to maintain the observed average DOC D 14 C values in the deep central gyres, the input of DOC from the margins is calculated to be as much as 25-100 times that of modern, surface ocean-derived carbon; for POC susp , the contribution from margins is smaller than that for DOC but still 5-19 times greater than the contribution of material from the surface ( Table 1). These estimates of margin and surface contributions to the deep open ocean have two principal implications: (1) inputs of 'aged' organic carbon from the margins to the deep open ocean may surpass inputs derived from recent surface ocean production, and (2) in view of the much larger surface-todeep than margin-to-deep concentration gradients, most young, surface-derived material must be degraded, allowing a smaller but more highly refractory margin component to contribute proportionally more to the deep central gyres.
Lateral transport of organic matter from margins to pelagic and abyssal environments has been invoked previously to help explain carbon and oxygen imbalances in the deep ocean 14,25 . Transport of 14 C-depleted DOC and even POC susp from ocean margins to the central gyres may be facilitated by isopycnal (that is, lateral) eddy diffusion, which can be 10 3 -10 7 times greater than vertical eddy diffusive transport 26 . Although vertical transport of recently produced surface material to the central gyres may also be enhanced by such processes as seasonal thermocline breakdown 27 and rapidly sinking organic particles 9,11,14 , we would expect this younger organic carbon to be relatively more susceptible to microbial remineralization 21,22,28 than older margin-derived material. Thus, although the open ocean undoubtedly receives inputs from both its margins and surface production, the D 14 C and concentration profiles of DOC and POC susp in the deep central gyres may be maintained by greater relative inputs from the margins than from recent surface production. k Mean observed gradients in concentrations of DOC and POC between surface (average of 0-20 m depth for DOC; average of particle maximum zone for POC susp , typically 20-85 m depth) and deep (Ͼ1,000 m depth) central gyre waters 9 . ¶ Excludes 0 to ϳ700 m depth interval. # Excludes shallowest depths sampled where concentrations were up to 30 times greater in margins.

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Shallow continental shelf and slope waters may also act as lowsalinity conduits of younger terrestrial organic matter (J.E.B., unpublished data, and ref. 18), where margins are affected significantly by rivers and estuaries. However, most of this material must also be degraded in nearshore waters or sequestered in sediments as it does not appear to comprise a significant component of open ocean DOC 29 and POC susp seaward of the shelf-slope front. The isotope signatures of DOC and POC susp at the coastal-open ocean boundaries (that is, slope and rise waters) here indicate that this carbon has mainly a non-recent marine origin and is older than organic carbon from the North Atlantic and Pacific central gyres. If this material propagates seaward, possibly along isopycnal surfaces, it may represent a source of old DOC and POC to intermediate and deep waters of the interior ocean 4 .