GEOPHYSICAL RESEARCH LETTERS, VOL. 36, L15607, doi:10.1029/2009gl038475, 2009

GEOPHYSICAL RESEARCH LETTERS, VOL. 36, L15607, doi:10.1029/2009gl038475, 2009 Reconciling the paradox that the heterotrophic waters of the East China Sea shelf act as a significant CO 2 sink during the summertime: Evidence and implications Wen-Chen Chou, 1 Gwo-Ching Gong, 1 David D. Sheu, 2 Sen Jan, 3 Chin-Chang Hung, 1 and Chung-Chi Chen 4 Received 2 April 2009; revised 30 May 2009; accepted 16 June 2009; published 6 August 2009. [1] To explore the paradox that the heterotrophic waters of the East China Sea (ECS) shelf act as a significant CO 2 sink in summer, vertical structures of carbon chemistry and hydrography were examined in July 2007. The results show that waters above the pycnocline (10 to 30 m) in the major CO 2 sink area are supersaturated with oxygen (110 ± 7%; autotrophic) but undersaturated with respect to atmospheric CO 2 (DfCO 2 = 130 ± 58 matm; sink). In contrast, waters below the pycnocline are undersaturated with respect to oxygen (61 ± 16%; heterotrophic) but supersaturated with CO 2 (DfCO 2 = 116 ± 115 matm; source). This demonstrates that summer stratification is the key factor maintaining the CO 2 sink status in the heterotrophic ECS shelf waters. Furthermore, the shallow pycnocline can easily be broken down when strong mixing occurs, potentially allowing the respired CO 2 stored in the subsurface waters to return to the atmosphere. Citation: Chou, W.-C., G.-C. Gong, D. D. Sheu, S. Jan, C.-C. Hung, and C.-C. Chen (2009), Reconciling the paradox that the heterotrophic waters of the East China Sea shelf act as a significant CO 2 sink during the summertime: Evidence and implications, Geophys. Res. Lett., 36, L15607, doi:10.1029/ 2009GL038475. 1. Introduction [2] There are two long-standing opposing views on the role of trophic states in regulating CO 2 uptake in marginal seas: heterotrophic-sources of atmospheric CO 2 [Smith and Hollibaugh, 1993; Mackenzie et al., 2000] vs. autotrophicsinks of atmospheric CO 2 [Gattuso et al., 1998; Chen, 2004]. The East China Sea (ECS) shelf has recently been found to present a paradox in this regard, being heterotrophic in summer but acting as a significant sink of atmospheric CO 2 [Chen et al., 2006]. To reconcile this paradox, Chen et al. [2006] suggested that during summer the high biological productivity may be restricted to the extremely shallow mixed layer in the strongly stratified water column, while large amounts of dissolved inorganic carbon (DIC) 1 Institute of Marine Environmental Chemistry and Ecology, National Taiwan Ocean University, Keelung, Taiwan. 2 Institute of Marine Geology and Chemistry, National Sun Yat-Sen University, Kaohsiung, Taiwan. 3 Institute of Hydrological and Oceanic Sciences, National Central University, Jungli, Taiwan. 4 Department of Life Science, National Taiwan Normal University, Taipei, Taiwan. are regenerated and stored in the subsurface layer through respiration of the planktonic community. The main objective of the present study was, therefore, to assess whether the ECS CO 2 system behaves as hypothesized by Chen et al. [2006]. Furthermore, the implications for carbon cycling in the ECS, drawn from the depth distribution of the CO 2 system, are also discussed. 2. Materials and Methods [3] A total of 30 stations along seven transects on the ECS shelf were investigated from 1 11 July, 2007 (Figure 1), aboard the R/V Ocean Researcher I. At each station, water samples were collected at various depths in 20 L Niskin bottles (X type) mounted on a rosette assembly. Temperature (T) and salinity (S) were recorded using a Seabird SBE 911plus conductivity temperature depth (CTD) profiler. Methods for total alkalinity (TA) and DIC analyses followed Chou et al. [2007], and these measurements had precisions of ±0.1% (±2 mmol kg 1 ) and ±0.15% (±3 mmol kg 1 ), respectively. The fugacity of CO 2 (fco 2 ) was calculated from the measured DIC and TA data using the program of Lewis and Wallace [1998]. Dissolved oxygen (DO) was determined by calibrated DO sensor (SBE43, Sea-Bird Electronics, Inc.) with a precision of ±1 mmol kg 1. Apparent oxygen utilization (AOU) was calculated using Benson and Krause s [1984] formula. Measurements of Chl a concentrations were made using a fluorometer (10-AU- 005; Turner Inc., USA), following Gong et al. [2003]. The depths of the pycnocline (P D ) and the euphotic zone (E Z ) were taken as the depths of the steepest vertical gradient in density and of 1% surface light penetration, respectively. 3. Description of the T, S, TA, DIC, fco 2 and AOU Transects [4] Cross shelf sections of T, S, TA, DIC, fco 2 and AOU along the six transects are shown in Figure S1 of the auxiliary material. 5 The steep temperature gradients in the water column indicate a strong stratification of ECS shelf waters during summer; the exception was station 6 on transect E, where the water column was well mixed. A low temperature water mass (T < 19 C) with high DIC, fco 2 and AOU was found only in the bottom waters at stations 21, 22 and 23 on transect A. The low salinity core Copyright 2009 by the American Geophysical Union. 0094-8276/09/2009GL038475 5 Auxiliary materials are available in the HTML. doi:10.1029/ 2009GL038475. L15607 1of5

Figure 1. Bathymetric map showing the sampling stations on the East China Sea shelf, with superimposed surface fco 2 contours. The major CO 2 sink area is defined as that zone where the surface fco 2 < 300 matm. (S < 32) in the surface waters at stations close to the mouth of the Changjiang River (stations 19 and 20 on transect A, station 29 on transect B, and station 18 on transect C; Figure S1b) suggests dilution by river outflow [Gong et al., 2006]. In contrast, the high salinity core (S > 34.5) found at deep water stations on the outer shelf is indicative of the intrusion of the Kuroshio Tropical Water [Gong et al., 1996]. The distribution of TA was generally correlated with salinity (Figures S1b and S1c); the lowest TA value corresponded to the low salinity stations affected by the Changjiang River, and the highest TA values corresponded to the higher salinity waters at stations affected by the Kuroshio Current. These data suggest that the variation in TA is controlled by the same factors affecting salinity. [5] DIC, fco 2 and AOU showed strong vertical stratification, and increased markedly with depth on all transects (Figures S1d S1f), notably at all stations on transect A, the near shore station 29 on transect B, and station 18 on transect C. At these stations, surface waters were well below saturation with respect to atmospheric CO 2 (fco 2 = 370 matm), but were supersaturated at quite shallow depth in the water column. In addition, surface waters at these stations were highly supersaturated (large negative AOU) with DO, but subsurface waters were well below saturation (large positive AOU). At station 18 on transect C, for example, fco 2 and AOU increased from 280 matm and 58 mmol kg 1 at the surface, respectively, to 712 matm and 103 mmol kg 1 at 10 m depth. These steep gradients of DIC, fco 2 and AOU suggest an intensification of the biological pump. 4. Reconciling the Paradox Between Heterotrophy and Function as a CO 2 Sink [6] As shown in Figure 1, the strongest CO 2 sink area (defined as surface fco 2 < 300 matm) was mainly confined to the northwestern part of the study area, where was also characterized by having the steepest DIC, fco 2 and AOU gradients (Figures S1d S1f). This situation provides a unique opportunity to investigate the paradox between heterotrophy and CO 2 sink in the ECS in summer, as reported by Chen et al. [2006]. [7] Figure 2 shows the depth profiles of Chl a, AOU, DIC and fco 2 at stations where surface fco 2 was less than 300 matm (depth profiles at other stations outside the major CO 2 sink area are given in Figure S2). As evidenced by the elevated surface Chl a concentrations (>2 mg m 3 ; Figures 2a 2d), a phytoplankton bloom above the pycnocline depth (P D ) occurred only at stations influenced by fresh water input from the Changjiang River (stations 18, 19, 20 and 29). The extremely negative AOU values (as low as 58 mmol kg 1 ) indicate that biological production overwhelmed community respiration, and that surface waters above the P D were autotrophic in the vicinity of these stations. High biological production consumes a large amount of DIC in drawing down the surface fco 2 below the saturation level. Consequently, the heterotrophy but acting as a CO 2 sink scenario did not apply in waters above the P D. However, the autotrophic condition only occurred above the P D, which is much shallower than the euphotic depth (E Z ) in the ECS during summer [Chen et al., 2007]. Chl a concentrations decreased in the lower part of the E Z (defined as the depth interval between the P D and the bottom of E Z ; the shadowed zone in Figure 2), but AOU values became positive, signifying that community respiration exceeded primary production, and the lower part of the E Z became heterotrophic. As a result of the heterotrophic activity a substantial amount of DIC could be released back to the water column, causing subsurface waters to become supersaturated with respect to atmospheric CO 2. In contrast, the E Z was generally deeper and Chl a concentrations were lower at other stations in the strongest CO 2 sink area (stations 21, 22, 23 and 24; Figures 2e 2h). However, at these stations the vertical distributions of AOU, DIC and fco 2 followed a similar trend to those at stations near the Changjiang River mouth. This included a generally negative AOU, a depleted DIC, and an undersaturated fco 2 in waters above the P D, but a positive AOU, an enriched DIC, and a supersaturated fco 2 in the lower part of the E Z. [8] As a whole, the E Z in the major CO 2 sink area of the ECS is composed of two distinctive layers (Figure 3). The upper portion of the E Z (i.e., waters above the P D ) is autotrophic (average AOU = 21 ± 15 mmol kg 1, corresponding to an oxygen saturation level of 110 ± 7%) and under saturated with respect to atmospheric CO 2 (average DfCO 2 = 130 ± 58 matm; DfCO 2 is sea-to-air fco 2 difference), whereas the lower portion of the E Z (i.e., the depth interval between the P D and the bottom of the E Z ) is heterotrophic (average AOU = 90 ± 38 mmol kg 1, corresponding to an oxygen saturation level of 61 ± 16%) and supersaturated with CO 2 (average DfCO 2 =116± 115 matm). Values for community respiration and primary production are usually integrated over the entire depth of the E Z, and on this basis the E Z zone in the major CO 2 sink area of the ECS would appear to be heterotrophic, despite the fact that the water overlaying the P D is autotrophic. This may explain the paradoxical phenomenon reported by Chen et al. [2006], that the ratio of the integrated primary production to community respiration (P/R ratio) within the 2of5

Figure 2. Depth distributions of Chl a, AOU, DIC and fco 2 at stations (a) 18, (b) 19, (c) 20, (d) 29, (e) 21, (f) 22, (g) 23 and (h) 24. These stations are located in the major CO 2 sink area of the East China Sea shelf. The horizontal dashed and solid lines indicate the depths of the pycnocline (P D ) and the euphotic zone (E Z ), respectively. E Z is less than 1 (i.e., heterotrophic), but the surface waters remain a significant sink for atmospheric CO 2. 5. Implications Drawn From the Depth Distribution of the CO 2 System on Carbon Cycling in the ECS [9] As shown in Figure 2, despite the surface waters were under saturated with respect to the atmospheric CO 2,the subsurface waters became strongly supersaturated at relatively shallow water depth. Accordingly, following fixation of atmospheric CO 2 through intensive biological production in the upper layer of the E Z, the accumulated DIC arising from the respiration/remineralization of POC in the subsurface layer could easily be returned to the surface in the event of extreme physical disturbance (such as cyclones/ typhoons) and diffuse back to the atmosphere. In this context, large scale upwelling and vertical mixing inducing by typhoon could be a mechanism potentially turning the surface waters of the ECS shelf from a CO 2 sink to a source. [10] Since severe weather conditions hamper any vesselbased investigations, we have applied the one-dimensional turbulence model of Mellor and Durbin [1975] and Mellor and Yamada [1982] to simulate the effect of the passage of a tropical storm on the sea-to-air CO 2 exchange flux. As shown in Figure S3, the mixed layer could deepen to 50 m in the major sink area of the ECS shelf within 24 hrs in the event of a tropical storm. The model result was further supported by a mooring observation Nemoto et al. [2008] in the ECS (28 10 0 N, 126 20 0 E), in which the temperatures at Figure 3. A plot of AOU versus fco 2 above the pycnocline depth (P D ) (upper E Z ; solid cycles) and within the depth region between the P D and the bottom of the E Z (lower E Z ; solid triangles). 3of5

Table 1. A Model Calculation Showing the fco 2 of Surface Seawater (fco 2sw ), the Sea-to-Air fco 2 Difference (DfCO 2 ), and the Sea-to-Air CO 2 Exchange Flux Before and After the Passage of a Hypothetical Tropical Depression Station no. fco 2sw a fco 2sw b matm DfCO 2 a DfCO 2 b Flux a Flux b mmol m 2 day 1 18 280 592 90 +242 5.3 +356.7 19 191 297 179 53 10.6 78.8 20 180 336 191 14 11.3 21.1 29 300 448 70 +98 4.1 +144.4 21 247 359 124 +9 7.2 +13.4 22 211 402 159 +52 9.3 +77.3 23 160 315 214 35 12.3 51.9 24 259 296 111 55 6.5 79.4 Average 228 381 142 +31 8.3 +45.1 a After the passage of a hypothetical tropical depression. b Before the passage of a hypothetical tropical depression. water depths of 1 and 50 m converged readily when typhoons passed the vicinity of the buoy site, suggesting that the mixed layer at least had deepened to 50 m. Accordingly, the values of T, S, TA and DIC for the top 50 m of water were calculated from data in the present study to derive the hypothetical fco 2 after such a strong mixing. The resulting data (Table 1) indicated that surface waters at stations 18, 21, 22 and 29 changed from being below saturation with respect to atmospheric CO 2 (DfCO 2 <0) to being supersaturated (DfCO 2 > 0), whereas undersaturation levels at the other stations declined, i.e., the absolute values of DfCO 2 decreased. The average value of DfCO 2 turned from a negative value of 142 to a positive value of 31 matm, respectively, before and after the mixing event. These results demonstrate that the major CO 2 sink area of the ECS shelf could become a CO 2 source area if physical forcing such as a tropical storm overturns the top 50 m of the water column. If the average wind speed during an extreme weather event is five times that under normal weather conditions (e.g., 25 vs. 5 m sec 1 ), and the wind speedtransfer velocity relationship is maintained at high wind speeds, then based on the formula of Wanninkhof [1992] the average CO 2 efflux would be 5.4 times greater than the CO 2 influx (45.1 vs. 8.3 mmol m 2 day 1 ; Table 1). Although uncertainty remains in the above calculations, these results demonstrate that episodic severe weather events indeed have the potential to transport regenerated CO 2 back to the atmosphere. [11] In addition to episodic severe weather events in summer, enhanced vertical mixing associated with the onset of the northeast monsoon and seasonal cooling in early autumn may be another mechanism returning respired CO 2 to the atmosphere. Although the ECS has long been considered a year-round CO 2 sink [Tsunogai et al., 1999; Wang et al., 2000], Shim et al. [2007] recently reported that the northern ECS acts as a CO 2 source in early autumn as a result of vertical mixing and/or upwelling of CO 2 -rich subsurface water from depth. Results from this study further imply that CO 2 photosynthetically fixed during summer might not be completely exported from the ECS shelf via the continental shelf pump, as suggested by Tsunogai et al. [1999]. Instead, it may be stored in the deep layer, but be readily returned to the atmosphere through strong vertical mixing event(s) that occur during the storm period in summer, and/or during the prevailing period of northeast monsoon and seasonal cooling in early autumn. [12] Acknowledgments. We are grateful to the crew of R/V Ocean Researcher I for shipboard operation and water sampling, and to T.F. Tseng and L.P. Chang for laboratory assistance. We also thank the two anonymous reviewers for constructive comments that helped to improve the paper significantly. 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