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Speciation of dissolved iodine: integrating nitrate uptake over time in the oceans
Continental Shelf Research 21 (2001) 113–128
Speciation of dissolved iodine: integrating nitrate uptake over time in the oceans George T.F. Wong*, Chin-Chang Hung1 Department of Ocean, Earth and Atmospheric Sciences, Old Dominion University, Norfolk, VA 23529, USA Received 30 November 1998; accepted 13 June 2000
Abstract The distributions of nitrate reductase activity (NRA), iodate and iodide were determined in May 1996 in the southern East China Sea in a transect that traversed across the upwelling center northeast of Taiwan where topographically induced upwelling occurred as the Kuroshio interacted with the shelf edge. ÿ Rationalized iodate (R-iodate or R-IOÿ 3 in nM) and iodide (R-iodide or R-I in nM), the concentrations of iodate and iodide normalized to a salinity of 35, were strongly correlated to each other so that ÿ ½R-IOÿ 3 ¼ ÿ1:06ð0:06Þ½R-I þ 424ð15Þ;
r2 ¼ 0:87:
ÿ1 ÿ Since the slope was indistinguishable from ÿ1 mol-IOÿ 3 mol -I , this implies that, if iodate is depleted in the surface oceans by biologically mediated uptake, it re-appears almost quantitatively as iodide so that little iodate is retained in the particulate phase. In the upwelling zone, R-iodate and R-iodide were also strongly correlated to NRA (in nM-N hÿ1) such that
½R-IOÿ 3 ¼ ÿ10:2ð1:0ÞNRA þ 392ð12Þ;
r2 ¼ 0:84;
½R-Iÿ ¼ 9:8ð1:1ÞNRA þ 27ð5Þ; r2 ¼ 0:76: Since NRA is an indicator of nitrate uptake and the source water to the upwelling zone, the Kuroshio Subsurface Water, is rich in iodate and almost devoid of iodide, these relationships are consistent with the conceptual model that iodate reduction and nitrate uptake occur in tandem through the activities of the ÿ enzyme nitrate reductase. Since NRA represents an instantaneous rate while [R-IOÿ 3 ] and [R-I ] are concentrations, these strong correlations also suggest that iodate reduction and hence nitrate uptake had operated at approximately constant rates during the residence time of the water in the upwelling zone. Thus, the depletion of iodate and the gain in iodide in the upwelled water relative to its source water were integrations of the uptake and reduction of iodate over this residence time. The slope of the relationship *Corresponding author. Tel.: +1-757-683-4932; fax: +1-757-683-5303. E-mail address: [email protected] (G.T.F. Wong). 1 Present address: Department of Oceanography, Texas A&M University at Galveston, 5007 Ave. U., Galveston, TX 77551, USA. 0278-4343/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S 0 2 7 8 - 4 3 4 3 ( 0 0 ) 0 0 0 8 6 - 8
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between R-iodate and NRA represented the product of this residence time and the biological discrimination of iodate reduction relative to nitrate uptake by the enzyme. Outside of the upwelling area, R-iodate and R-iodide did not correlate well with NRA, probably as a result of the masking effect of mixing among water masses with undefined concentrations of pre-existing iodate and iodide. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: East China Sea; New production; Nitrate uptake; Iodine; Trace element speciation
1. Introduction New production is the fraction of primary production in the oceans that is supported by nutrients originating from outside of the euphotic zone (Dugdale and Goering, 1967). An understanding of its governing processes and an accurate estimation of its global magnitude are crucial factors for deciphering the present apparent imbalance in the global budget of anthropogenic carbon (Platt et al., 1992; Siegenthaler and Sarmiento, 1993; Sarmiento and Le Quere, 1996) which has been linked to the green-house effect. While allochthonous nutrients to the euphotic zone may originate from various sources, such as the upwelling of deep water, atmospheric deposition, nitrogen fixation and riverine input, in the open oceans, away from the influence of land, the input of nutrients by the global upwelling of deep waters to the surface oceans is a major, if not the dominant, contributor. Since combined nitrogen exists almost exclusively as nitrate in the deep waters, new production has been represented by nitrate uptake (Eppley, 1989). Nonetheless, studying nitrate uptake through direct observations by using labeled nitrate suffers from significant limitations. Using a radioactive isotope is not feasible since there is no readily available radioactive nitrogen (Wada and Hattori, 1991). The sensitivity in measuring the uptake of 15N-labelled nitrate in incubation experiments (Eppley, 1989) is somewhat limited since 15N is also a naturally occurring isotope of nitrogen with relatively high abundance. In oligotrophic waters, when the nitrate concentration is low, the amount of added 15N-labelled nitrate may be larger than the natural reservoir and cause artificially stimulated nitrate uptake and unreliable results (Dugdale and Wilkerson, 1986; McCarthy et al., 1992, 1996; Allen et al., 1996). Thus, using chemical analogues is a valuable complementary experimental approach for gaining additional insights into the biogeochemical dynamics of the marine nitrogen system. Halates are attractive candidates as chemical analogues for studying nitrate uptake because of their similar ionic formula to nitrate. 36Cl-labelled chlorate has been used extensively to study nitrate transport (Balch, 1985, 1987; Balch et al., 1987) and the rate of transport of chlorate into the cells has been found to be linearly related to nitrate uptake rates in both laboratory cultures of marine phytoplankton and in the field although the biological affinity for chlorate relative to nitrate was about three orders of magnitude lower. However, unlike nitrate, chlorate is not a natural constituent of seawater. While nitrate uptake involves transport, reduction and assimilation, chlorate can only trace the first step in the process. Iodate, being a naturally occurring species of dissolved iodine in seawater, may be a more powerful natural analogue for studying nitrate uptake. Dissolved iodine is a bio-intermediate element which exists primarily as iodate and iodide in the oceans (Wong, 1991). Although iodide is thermodynamically unstable relative to iodate in oxic seawater and is virtually absent in the
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deep water, it co-exists ubiquitously with iodate in the surface oceans (Tsunogai and Henmi, 1971; Tsunogai, 1971; Wong and Brewer, 1974, 1977; Elderfield and Truesdale, 1980; Wong et al., 1985; Jickells et al., 1988; Wong and Zhang, 1992a; Tian and Nicolas, 1995; Wong, 1995; Campos et al., 1996; Tian et al., 1996). On the other hand, dissolved iodine exists almost exclusively as iodate in the deep water. Because of the chemical similarities between iodate and nitrate, it has been long suspected that the unstable iodide is formed by the biologically mediated reduction of iodate through the activity of the enzyme nitrate reductase (Tsunogai and Sase, 1969) which also is the essential enzyme that initiates nitrate uptake (Wada and Hattori, 1991). If this hypothesis is true, then, iodate reduction may be intertwined with nitrate uptake and iodate may be used as an analogue for studying nitrate uptake and new production (Wong, 1991). The relationship between chlorate transport and nitrate uptake reported by Balch and coworkers (Balch, 1985, 1987; Balch et al., 1987) is suggestive of this possibility. Recent laboratory studies (Udomkit and Dunstan, 1991; Moisan et al., 1994; Udomkit, 1994) have provided direct evidence that iodate can be taken up by marine phytoplankton and iodide is formed in the process. Hung (1999) found that nitrate reductase extracted from natural marine phytoplankton assemblages and from a culture of Skeletonema costatum can also reduce iodate to iodide. However, while the laboratory evidence points strongly to the possibility of a biologically mediated reduction of iodate to iodide which is linked to nitrate uptake, no field observations which relate the changes in speciation of dissolved iodine in the oceans to an indicator of nitrate uptake have been reported. Nitrate uptake by phytoplankton involves three enzymatically mediated steps: (1) the reduction of nitrate to nitrite by nitrate reductase, (2) the reduction of nitrite to ammonia by nitrite reductase, and (3) the assimilation of the ammonia formed (Wada and Hattori, 1991). The determination of nitrate reductase activity (NRA) measures the rate of the first step under a constant set of operationally defined conditions (Eppley et al., 1969, 1970; Packard et al., 1971, 1978; Slawyk and Collos, 1976; Eppley, 1978; Hochman et al., 1986; Berges and Harrison, 1995). If nitrate reduction is the rate-limiting step in nitrate uptake, NRA will be proportional to nitrate uptake (Eppley et al., 1970; Packard et al., 1971; Wheeler, 1983; Berges and Harrison, 1993). Indeed, Hung et al. (1998, 2000) reported that NRA is linearly and quantitatively related to 15 N-labelled nitrate uptake under nutrient- and light-replete conditions in the East China Sea. Here we present the first field evidence of the relationships between the concentrations of iodate and iodide, and, NRA in the oceans.
2. Environmental setting The East China Sea is consisted of the water on the East China Sea Shelf and the water in the deep Okinawa Trough. The East China Sea Shelf is one of the large and more productive marginal seas of the world. It extends from the Cheju Island, at about 338200 N, in the north to the northern coast of the island of Taiwan, at about 258N, in the south. It is bounded to the east by the Kuroshio and to the west by continental China from which it receives the outflow of Changjiang, one of the large rivers of the world (Milliman and Jin, 1985). In the southern East China Sea Shelf, the outflow of the Minjiang can also be locally significant. These freshwater inflows result in the presence of the fresh, cold and nutrient-rich Coastal Water along the Chinese coast (Wong et al., 1998). At the southeastern corner of the East China Sea, after the Kuroshio enters the Okinawa Trough from the
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western Philippine Sea through the Suao-Yonaguni Pass over the Ilan Ridge, this northward travelling current runs into the shelf edge of the southern East China Sea Shelf which stretches in a west to east direction. As a result, the Kuroshio turns eastward and flows along the shelf edge. At the point where the Kuroshio changes its direction, a year-round upwelling center is formed northeast of Taiwan where the cold nutrient-rich Kuroshio Subsurface Water enters the East China Sea Shelf and becomes a significant source of nutrient to the shelf (Wong et al., 1991, 2000a; Liu et al., 1992a, b). This upwelling is strong enough at times that its influence can become clearly evident even in the surface waters. Along the shelf edge, there is also extensive exchange between the East China Sea Shelf and the Kuroshio through frontal processes so that the warm, saline and nutrient-poor Kuroshio Surface Water may find its way onto the shelf (Chern and Wang, 1990; Chern et al., 1990; Su et al., 1990; Wong et al., 1991; Hsueh et al., 1992; Liu et al., 1992a, b; Chen et al., 1995; Gong and Liu, 1995; Chen, 1996). Another source of surface water to the shelf is the Taiwan Current Warm Water which enters the Sea through the Taiwan Strait from the south. This water is nutrient poor while its temperature and salinity are slightly lower than those of the Kuroshio Surface Water. Thus, the major surface water masses in the East China Sea Shelf are the Coastal Water, the Kuroshio Surface Water, the upwelled Kuroshio Subsurface Water and the Taiwan Current Warm Water (Liu et al., 1992a; Chen et al., 1995; Gong and Liu, 1995).
3. Methods Eight stations were occupied in a transect across the southern East China Sea between May 2 and 15, 1996 aboard the R/V Ocean Research I during Cruise ORI-449 of the Kuroshio Edge Exchange Processes (KEEP) Study (Wong et al., 2000b). The locations of the stations are shown in Fig. 1. At each station, the distributions of temperature and salinity were recorded with a SeaBird model SBE9/11 conductivity–temperature–depth (CTD) recorder. Discrete samples were collected with GO-FLO bottles mounted onto a Rosette Sampling assembly (General Oceanic). Sub-samples were then obtained for the determination of salinity, the dissolved iodine species, NRA, nitrite and (nitrate+nitrite). Salinity was determined in a shore-based laboratory with an Autosal salinometer with a precision of 0.003. Nitrite and (nitrate+nitrite) were determined onboard ship by the standard pink azo dye method which has been adapted for use with a flow injection analyzer (Morris and Riley, 1963; Strickland and Parsons, 1972; Pai et al., 1990; Gong, 1992). The precisions for the determination of nitrate and nitrite were 0.3 and 0.03 mM, respectively. The sub-samples for the determination of the dissolved iodine species were drawn and stored frozen in polyethylene bottles (Wong, 1973) and returned to the shore-based laboratory for analyses. Both iodate and iodide were determined by using an EG&G-PAR Model 384B-4 polarographic analyzer system with a Model 303A static mercury drop electrode. Iodate was determined directly by differential pulse polarography according to the method of Herring and Liss (1974) as modified by Wong and Zhang (1992b). At concentrations above 0.1 mM, the precision of the method was 0.006 mM. Iodide was determined directly by cathodic stripping square wave voltammetry by the method of Luther III et al. (1988) as modified by Wong and Zhang (1992b, c). The precision of the method was 0.005 mM. Sub-samples for the determination of NRA and the dissolved iodine species were obtained from the same sample at Stations 49–53. At Sta. 55, they were drawn from different casts. NRA was
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Fig. 1. The locations of the stations in a transect across the southern East China Sea.
determined onboard ship by a modified version of the method of Hochman et al. (1986). Seawater samples (20 l at Sta. 55 and 4–8 l at the other stations) were collected just after sunrise and filtered through a 47-mm Gelman type A/E glass fiber filter. The filter was transferred to a beaker together with 1 ml of a phosphate buffer (150 mM of K2HPO4 adjusted to a pH of 7.6), 50 ml of toluene, 0.2 ml of 6.5 mM NADH (Sigma Chemical Co.) and 0.2 ml of 0.1 M potassium nitrate. The beaker was placed on a vortex mixer and mixed for 5 min at room temperature. Then, the reaction was terminated by transferring 1 ml of the slurry from the beaker into a centrifuge tube containing 1.7 ml of 0.13 M ZnSO4 at 978C. After the solution was allowed to cool, 0.2 ml of 1 N NaOH was added and the mixture was centrifuged for 20 min at 4000 rpm. Two ml of the supernatant liquid was removed for the determination of nitrite by adding 0.1 ml of a 2% (w/v) sulfanilamide solution in 15% hydrochloric acid and 0.1 ml of a 0.3% (w/v) N-1-naphthylethylenediamine hydrochloride solution to the supernatant liquid and measuring the absorbance of the azo dye formed at 543 nm (Strickland and Parsons, 1972) with a Brinkman PC-800 Probe Colorimeter equipped with a probe tip with a 2-cm light path. The precision of the measurement was about 5%. 4. Results and discussions 4.1. Hydrography and the distributions of NRA and the dissolved iodine species The distributions of temperature, salinity, nitrate, rationalized iodate (R-iodate, R-IOÿ 3 ) and ÿ rationalized iodide (R-iodide, R-I ) in the surface waters at 10 m across the transect are shown in
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Figs. 2a and b. R-iodate and R-iodide are the concentrations of iodate and iodide normalized to a salinity of 35 (Fig. 2b, Truesdale, 1994). By normalizing concentrations to a constant salinity, changes in concentrations resulting from variation in salinity are removed. At least three of the four major surface water masses were clearly represented in the transect. The colder and fresher Coastal Water was found at Sta. 48 and 49. The upwelled Kuroshio Subsurface Water was represented as the cold and nitrate-rich water at Sta. 51–53. The Kuroshio Surface Water was found at Sta. 54 and 55 where nitrate was virtually absent and the temperatures were the highest. The water at Sta. 50, with its high temperature and low concentration of nitrate, might have represented Taiwan Strait Warm Water (Wong et al., 1991; Liu et al., 1992a, b). However, the present data set was too limited to make a definitive assignment. The upwelled water was clearly distinguished from the other surface water masses by its high concentrations of R-iodate and low concentrations of R-iodide (Fig. 2b). The vertical distributions of sigma-y, nitrate, NRA, R-iodate and R-iodide at Sta. 49, 53 and 55, representing the mesotrophic coastal zone, the upwelling zone and the oligotrophic Kuroshio, are shown in Figs. 3, 4 and 5, respectively. The thinnest mixed layer, about 10 m thick, and the shallowest nitrate-cline, which started almost at the sea surface, were found in the upwelling zone (Fig. 4) where vertical transport should have been the strongest. In contrast, the water column in the coastal zone (Fig. 3), which was also highly turbid, was well mixed down to about 35 m but nitrate was depleted only down to 20 m probably as a result of light limitation on phytoplankton activity. In the Kuroshio, the mixed layer was 25 m thick and nitrate was depleted at depths even below the mixed layer (Fig. 5). Similar levels of NRA were found in the coastal zone and the upwelling zone. In both cases, the highest level of NRA was found at the sea surface and it decreased rapidly with depth to background levels at about 25 m. In contrast, NRA in the Kuroshio was about one order of magnitude lower but it extended to greater depths. In fact, it increased with depth until it reached a sub-surface maximum in the pycnocline at 80 m. The distributions of R-iodate and R-iodide at these stations approximately followed the local hydrography. In the coastal zone (Fig. 3b), the concentration of R-iodide remained consistently
ÿ ÿ Fig. 2. The distributions of (a) temperature (*), salinity (*) and NOÿ 3 (m), and (b) R-IO3 (*) and R-I (*) at 10 m across the transect.
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ÿ ÿ Fig. 3. The vertical distributions of (a) sigma-t (*), NOÿ 3 (*) and NRA (&), and (b) R-IO3 (*) and R-I (*) at Sta. 49 in the coastal zone.
ÿ ÿ Fig. 4. The vertical distributions of (a) sigma-t (*), NOÿ 3 (*) and NRA (&), and (b) R-IO3 (*) and R-I (*) at Sta. 53 in the upwelling zone.
high, never below 100 nM, while that of R-iodate remained consistently low, never above 330 nM, through out the water column. The variations in the concentrations of R-iodate and R-iodide with depth were also small, being confined to within the ranges of about 75 and 50 nM respectively. Within the mixed layer in the top 35 m of the water column, there were weak indications of an increase in the concentration of R-iodate and a decrease in the concentration of R-iodide with
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ÿ Fig. 5. The vertical distributions of (a) sigma-t (*), NOÿ 3 (*) and NRA (&) at Sta. 55 Cast 3, and (b) R-IO3 (*) and ÿ R-I (*) at Sta. 55 Cast 1 in the Kuroshio.
depth. In the bottom water below 35 m, where both sigma-y and nitrate increased significantly, indicating that a different water mass might have been present, there were suggestions of a slight decrease in the concentration of R-iodate and an increase in the concentration of R-iodide. On the other hand, in the upwelling zone (Fig. 4b) and in the Kuroshio (Fig. 5b), the highest concentration of R-iodide and the lowest concentration of R-iodate were found in the mixed layer. The concentration of R-iodide decreased while that of R-iodate increased systematically with depth until the former became minimal at concentrations below 30 nM while the latter reached concentrations exceeding 380 nM. Thus, in both cases, as observed in other parts of the oceans (Wong, 1991), the vertical distributions of R-iodate and R-iodide were approximate mirror images. The highest concentration of R-iodate, >300 nM, and the lowest concentration of R-iodide, 5100 nM, in the mixed layer were found in the upwelling zone. The upwelling Kuroshio Subsurface Water originates from about 300 m in the Okinawa Trough with t (temperature)=13– 158C, S (salinity)=34.4–34.6, [NOÿ 3 ]=13–16 mM (Wong et al., 1991; Liu et al., 1992a, b). No sample was collected at this depth in the Okinawa Trough during this cruise. The deepest sample ÿ was collected at 203 m at Sta. 55 where t=18.48C, S=34.8, [NOÿ 3 ]=4 mM, [R-I ]=11 nM and ÿ [R-IO3 ]=408 nM. Even at this shallower depth, the concentrations of R-iodate and R-iodide had apparently reached their asymptotic concentrations and were not expected to change significantly any further with depth. In another cruise in May 1994, a sample was collected at 350 m in the ÿ Okinawa Trough and its properties were t=148C, S=34.6, [NOÿ 3 ]=11 mM, [R-I ]=8 nM, ÿ [R-IO3 ]=452 nM (Lin, 1995). Thus, dissolved iodine existed almost exclusively as iodate in the source water of the upwelling system.
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4.2. Relationships between iodate and iodide and a conceptual model for the cycling of dissolved inorganic iodine species in the surface oceans The linear relationship between R-iodide and R-iodate at all stations is shown in Fig. 6. A similar relationship was found in the South Atlantic Bight (Wong and Zhang, 1992c; Wong, 1995). Model II linear regression analysis (Laws and Archie, 1981) of the data from this study yields ÿ ½R-IOÿ 3 ¼ ÿ1:06ð0:06Þ½R-I þ 424ð15Þ;
r2 ¼ 0:87; n ¼ 50;
ÿ where [R-IOÿ 3 ] and [R-I ] are in nM and n is the number of observations. The slope of the line is indistinguishable from ÿ1 within statistical uncertainties. Thus, removal of iodate in the surface oceans was accompanied by an almost quantitative production of iodide. In other words, unlike nitrate which can be sequestered rather effectively in the particulate phase during nitrate uptake, if iodate is lost in the surface oceans through biologically mediated uptake, it is converted to iodide which is quantitatively exuded to the surrounding water by the organisms. Little of the iodate processed by the organisms is retained in the particulate phase and little of the iodide exuded is converted to a form other than iodate. Indeed, Udomkit and Dunstan (1991), Moisan et al. (1994) and Udomkit (1994) found uptake of iodate by phytoplankton and an associated appearance of iodide in laboratory cultures. Wong (1980) and Luther III et al. (1995) observed that iodide, though thermodynamically unstable relative to iodate, is metastable. Once it is formed, it cannot be readily oxidized back to iodate. Based on this information, the following conceptual model for cycling among the iodine species in the oceans may be constructed. Through global upwelling, virtually iodide-free and iodate-rich deep water is supplied to the surface oceans where nitrateand iodate-uptake may occur in tandem. The iodate taken up is exuded almost quantitatively to the surrounding water as iodide. Since iodide is not readily reconverted back to iodate once it is formed, the depletion of iodate and the enrichment of iodide in the surface oceans relative to the deep oceans represent an integration of the reduction of iodate over the residence times of the water of the surface oceans. If the reduction of iodate is coupled to nitrate uptake, the changes in
ÿ Fig. 6. The relationships between R-IOÿ 3 and R-I at all the stations: Sta. 48 } *; Sta. 49 } *; Sta. 50 } &; Sta. 51 } &; Sta. 52 } n; Sta. 53 } m; Sta. 54 } 5; Sta. 55 } .. The line represents the Model II linear regression line.
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the speciation of dissolved inorganic iodine in the surface oceans will also be an integrator of nitrate uptake over time. Since upwelling does not occur uniformly over the world’s oceans, the concentration of iodide and iodate at a given location in the surface oceans may reflect not only the effect of in situ biologically mediated reduction of iodate but also mixing with other surface water masses containing pre-existing concentrations of iodate and iodide. Thus, on a regional scale, this conceptual model is directly applicable only to upwelling centers where the source water is well defined and the input of iodide-free deep water dominates over mixing with other surface water masses. The linear relationship between R-iodide and R-iodate contained more variability moving from the oligotrophic Kuroshio water to the coastal water at Sta. 48–50 as the concentration of Riodate decreased and R-iodide increased (Fig. 6). Similar behavior was also observed previously in the South Atlantic Bight (Wong and Zhang, 1992a; Wong, 1995). In fact, the relationship broke down in the inner shelf of the South Atlantic Bight. This may be caused by the conversion of the dissolved inorganic iodine species to particulate iodine, gaseous iodine and/or organic iodine. Wong and Cheng (1998) have reported recently the occurrence of significant quantities of dissolved organic iodine in coastal waters. 4.3. Relationships between iodate and NRA, and, iodide and NRA The relationships between R-iodate and NRA, and R-iodide and NRA in the upwelling water ÿ are shown in Fig. 7. Both [R-IOÿ 3 ] and [R-I ] were strongly correlated to NRA. Based on Model II linear regression analyses (Laws and Archie, 1981), the following relationships were found: ½R-IOÿ 3 ¼ ÿ10:2ð1:0ÞNRA þ 392ð12Þ; ½R-Iÿ ¼ 9:8ð1:1ÞNRA þ 27ð5Þ;
r2 ¼ 0:84; n ¼ 18;
r2 ¼ 0:76; n ¼ 18;
ÿ ÿ1 and n is the number of samples where [R-IOÿ 3 ] and [R-I ] are in nM and NRA is in nM-N h with readily detectable concentrations of iodate, iodide and level of NRA. The intercepts of these
ÿ Fig. 7. The relationships between (a) R-IOÿ 3 and NRA, and (b) R-I and NRA in the upwelling zone at Sta. 51 (*), 52 (*) and 53 (&). The Model II linear regression lines are shown.
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relationships represent the composition of the source water. Since iodate and iodide are in the dissolved phase while NRA measures the instantaneous activity of an enzyme extracted from the particulate phase, the strong correlations suggest that there was no decoupling between the dissolved and particulate phases and that the processes that caused the disappearance of iodate and the appearance of iodide occurred at approximately constant rates during the lifetime of the water in the upwelling zone. The slopes of the two relationships were of opposite signs but their absolute values were indistinguishable from each other within their statistical uncertainties. Thus, the disappearance of iodate was approximately equal to the appearance of iodide so that these relationships were consistent with the conceptual model as described previously. According to this model, d½R-IOÿ 3 ¼ ðIRAÞ t; ÿ where d [R-IOÿ 3 ] is the deficit in [R-IO3 ] in the upwelling water relative to its source water, IRA is the iodate reduction activity and t is the residence time of the upwelling water which is controlled by the physical dynamics of the upwelling system. If
IRA ¼ NRAðIRR=NRRÞ; where IRR is the iodate reduction rate and NRR the nitrate reduction rate, IRR/NRR represents the biological discrimination factor of the enzyme nitrate reductase for selecting between iodate and nitrate for the reduction. Then, ðd½R ÿ IOÿ 3 =NRAÞ ¼ ðIRR=NRRÞt; ÿ where d [R-IOÿ 3 ]/NRA is the slope of the relationship between [R-IO3 ] and NRA. This slope is ÿ ÿ1 ÿ1 in the East China Sea. By considering the mass balance of oxygen, 10.2 nM-IOÿ 3 nM -NO3 h the upwelling rate at this upwelling zone of the East China Sea has been estimated to be 5 m dÿ1 (Liu et al., 1992b). Since the water depth at the shelf edge in the upwelling zone is about 100 m thick, the residence time of the upwelling water will be about 20 d. Thus, this model would yield an IRR/NRR of 1/50. The value of IRR/NRR is poorly known. The information on iodate uptake rates is limited to laboratory cultures of four species of phytoplankton which gave values ranging from 0.003 to ÿ1 ÿ1 and two field experiments with rates of 0.08 and 0.26 nmol0.24 nmol-IOÿ 3 mg -chl-a h ÿ1 ÿ1 ÿ giving an average of 0.1 0.1 nmol-IO3 mgÿ1-chl-a hÿ1 (Udomkit and IO3 mg -chl-a h Dunstan, 1991; Moisan et al., 1994; Udomkit, 1994). During this East China Sea cruise, nitrate uptake rates were estimated at some stations by measuring the uptake of 15N-labelled nitrate and/ or NRA. When both measurements were made simultaneously, they were strongly correlated with each other with an average ratio of approximately 1 when there were sufficient ambient light and nitrate (Hung et al., 1998, 2000). This indicates that NRA was approximately a quantitative indicator of nitrate uptake. At Sta. 52 in the upwelling zone, nitrate uptake was determined at various depths in the euphotic zone by measuring NRA and the uptake of 15N-labeled nitrate simultaneously in one cast and by measuring NRA only in another cast. The average of all the ÿ1 ÿ1 (Hung et al., 1998, 2000). If the average values measurements was 9 2 nmol-NOÿ 3 mg -chl-a h of the reported iodate uptake rates and the nitrate uptake rates at Sta. 52 are used, then, IRR/ NRR is about 1/90. More recently, Hung (1999) determined nitrate and iodate reduction activities in nitrate reductase extracted from four coastal phytoplankton assemblages and a culture of
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Skeletonema costatum and found IRR/NRR ranging between 1/39 and 1/99. Considering the uncertainties involved in each of these approaches for estimating IRR/NRR, the agreement between the model generated value, 1/50, and these other estimated values, 1/39–1/99, was quite reasonable and lends support to the conceptual model proposed here for cycling among the iodine species in the oceans. The relationships between R-iodate and NRA, and R-iodide and NRA outside of the upwelling zone in the East China Sea Shelf at Sta. 49 and 50 are shown in Fig. 8. (The data from Sta. 55 could not be treated in this manner because the sub-samples for the determinations of the dissolved iodine species and NRA were drawn from different casts.) The conceptual model suggests that mixing among surface water masses with different pre-existing concentrations of Riodate and R-iodide may have significant effects on their observed concentrations. Indeed, in contrast to the strong correlations found in the upwelling zone, there was weak to no correlation between R-iodate and NRA, and R-iodide and NRA in these waters. Thus, the in situ biologically mediated reduction of iodate to iodide could not be the primary control of their concentrations.
4.4. Iodate depletion in the surface oceans and global new production The plausibility of the proposed linkage between iodate reduction and nitrate uptake may be further examined by taking into account the reported estimates of global new production. The average deficit of iodate in the surface oceans relative to the deep oceans is about 0.15 mM (Wong, 1991, 1995). The average thickness of the surface mixed layer is 200 m. Hence, the iodate deficit in the mixed layer is 3 104 mmol mÿ2. Since the residence time of the surface waters in the oceans is about 30 yr, the annual disappearance of iodate by its reduction to iodide in the surface oceans is 1000 mmol mÿ2 yrÿ1. If IRR/NRR is between 1/39 and 1/100 as suggested previously, then, nitrate uptake, or nitrate-based production, is 4 104–1 105 mmol-N mÿ2 yrÿ1 or 3.2–8 g-C mÿ2 yrÿ1. At a global primary production of 125 g-C mÿ2 yrÿ1 (Falkowski et al., 1998), the ratio of nitratebased production to primary production is 0.03–0.06. In comparison, the global new production
ÿ Fig. 8. The relationships between (a) R-IOÿ 3 and NRA, and (b) R-I and NRA at Sta. 49 (*) and 50 (*) in the shelf outside of the upwelling zone. The lines represent the relationships in the upwelling zone.
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and the ratio of new production to primary production, or f-ratio, have been estimated to be 9–44 g-C mÿ2 yrÿ1 and 0.15–0.36 (Eppley, 1989; Falkowski et al., 1998). Obviously, there are large uncertainties associated with the values estimated from the dissolved iodine species. For example, the value of IRR/NRR is still poorly known. If there is any oxidation of iodide to iodate during the residence time of the surface oceans, the reduction of iodate, and thus the global nitrate-based production and its ratio to primary production would have been underestimated. Furthermore, nitrate-based production and its ratio to primary production do not correspond exactly with new production and the f-ratio. In fact, the former is likely to be lower than the latter since allochthonous combined nitrogen may not be supplied to the surface oceans in the form of nitrate only. Nonetheless, despite the preliminary nature in the approach for estimating nitrate uptake from iodate deficit in the surface oceans and the possible conceptual mismatch between nitratebased production and new production, the values estimated from these two approaches are of similar magnitude. This apparent agreement is notable and is consistent with a linkage between the iodine cycle and the nitrogen cycle in the oceans.
5. Conclusions The results from this study provide field evidence that supports the idea that the depletion of iodate in the surface oceans is caused by a biologically mediated reduction of iodate to iodide through the activity of the enzyme nitrate reductase. In the process, the iodate reappears in the dissolved phase as iodide almost quantitatively so that little of the iodate processed by the organisms is sequestered in the particulate phase. Thus, the depletion of iodate and the enrichment of iodide relative to the composition of the source water of a surface water mass represent an integration of NRA through the lifetime of the water mass. Acknowledgements This work was supported by the National Science Foundation through grant numbers OCE9301298 and INT-9515521 to Wong. The manuscript was prepared while Wong occupied a research chair at the National Center for Ocean Research (NCOR) of the National Science Council of Taiwan. We thank the captain and the crew of R/V Ocean Researcher I for their assistance in sample collection. This cruise, ORI-449 was funded by the National Science Council of Taiwan as part of the Kuroshio Edge Exchange Process (KEEP) program. Hydrographic data and data on nutrient distributions and 15NOÿ 3 uptake were provided by G.-C. Gong and F.-K. Shiah. This is contribution number 30 of NCOR.
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Tsunogai, S., Henmi, T., 1971. Iodine in the surface water of the ocean. Journal of the Oceanographic Society of Japan 27, 67–72. Tsunogai, S., Sase, T., 1969. Formation of iodide-iodine in the ocean. Deep-Sea Research 16, 489–496. Udomkit, A., 1994. Iodate transformation by marine phytoplankton. Ph.D. Thesis, Old Dominion University, Norfolk, VA, 124pp. Udomkit, A., Dunstan, W.M., 1991. Preliminary study on the influence of phytoplankton on iodine speciation. Journal of Phycology 27 (Suppl.), 73. Wada, E., Hattori, A., 1991. Nitrogen in the Sea: Forms, Abundances, and Rate Processes. CRC Press, Boca Raton, 208pp. Wheeler, P.A., 1983. Phytoplankton nitrogen metabolism. In: Carpenter, E.J., Capone, D.G. (Eds.), Nitrogen in the Marine Environment. Academic Press, New York, pp. 309–346. Wong, G.T.F., 1973. The marine chemistry of iodate. M.Sc. Thesis, Massachusetts Institute of Technology. Wong, G.T.F., 1980. The stability of dissolved inorganic species of iodine in seawater. Marine Chemistry 9, 13–24. Wong, G.T.F., 1991. The marine geochemistry of iodine. Critical Reviews in Aquatic Sciences 4, 45–73. Wong, G.T.F., 1995. Dissolved iodine across the Gulf Stream front and in the South Atlantic Bight. Deep-Sea Research I 42, 2005–2023. Wong, G.T.F., Brewer, P.G., 1974. The determination and distribution of iodate in South Atlantic waters. Journal of Marine Research 32, 25–36. Wong, G.T.F., Brewer, P.G., 1977. The marine chemistry of iodine in anoxic basins. Geochimica et Cosmochimica Acta 41, 151–159. Wong, G.T.F., Chao, S.-Y., Li, Y.-H., Shiah, F.-K., 2000a. The Kuroshio edge exchange processes (KEEP) study } an introduction to hypotheses and highlights. Continental Shelf Research 20, 335–347. Wong, G.T.F., Chao, S.-Y., Chung, Y.-C., Li, Y.-H., 2000b. Preface KEEP } exchange processes between the Kuroshio and the East China Sea Shelf. Continental Shelf Research 20, 331–334. Wong, G.T.F., Cheng, X.-H., 1998. Dissolved organic iodine in marine waters: determination, occurrence and analytical implications. Marine Chemistry 59, 271–281. Wong, G.T.F., Gong, G.-C., Liu, K.-K., Pai, S.-C., 1998. ‘Excess nitrate’ in the East China Sea. Estuarine, Coastal and Shelf Science 46, 411–418. Wong, G.T.F., Pai, S.-C., Liu, K.-K., Chen, C.-T.A., 1991. Variability of the chemical hydrography at the frontal region between the East China Sea and the Kuroshio northeast of Taiwan. Estuarine, Coastal and Shelf Science 33, 105–120. Wong, G.T.F., Takayanagi, K., Todd, J.F., 1985. Dissolved iodine in waters overlying and in the Orca Basin, Gulf of Mexico. Marine Chemistry 17, 177–183. Wong, G.T.F., Zhang, L., 1992a. Changes in iodine-speciation across coastal hydrographic fronts in southeastern United States continental shelf waters. Continental Shelf Research 12, 717–733. Wong, G.T.F., Zhang, L.-S., 1992b. Chemical removal of oxygen with sulfite for the polarographic or voltammetric determination of iodate and iodide in seawater. Marine Chemistry 38, 109–116. Wong, G.T.F., Zhang, L.-S., 1992c. The determination of total inorganic iodine in seawater by cathodic stripping square wave voltammetry. Talanta 39, 355–360.
Speciation of dissolved iodine: integrating nitrate uptake over time in the oceans George T.F. Wong*, Chin-Chang Hung1 Department of Ocean, Earth and Atmospheric Sciences, Old Dominion University, Norfolk, VA 23529, USA Received 30 November 1998; accepted 13 June 2000
Abstract The distributions of nitrate reductase activity (NRA), iodate and iodide were determined in May 1996 in the southern East China Sea in a transect that traversed across the upwelling center northeast of Taiwan where topographically induced upwelling occurred as the Kuroshio interacted with the shelf edge. ÿ Rationalized iodate (R-iodate or R-IOÿ 3 in nM) and iodide (R-iodide or R-I in nM), the concentrations of iodate and iodide normalized to a salinity of 35, were strongly correlated to each other so that ÿ ½R-IOÿ 3 ¼ ÿ1:06ð0:06Þ½R-I þ 424ð15Þ;
r2 ¼ 0:87:
ÿ1 ÿ Since the slope was indistinguishable from ÿ1 mol-IOÿ 3 mol -I , this implies that, if iodate is depleted in the surface oceans by biologically mediated uptake, it re-appears almost quantitatively as iodide so that little iodate is retained in the particulate phase. In the upwelling zone, R-iodate and R-iodide were also strongly correlated to NRA (in nM-N hÿ1) such that
½R-IOÿ 3 ¼ ÿ10:2ð1:0ÞNRA þ 392ð12Þ;
r2 ¼ 0:84;
½R-Iÿ ¼ 9:8ð1:1ÞNRA þ 27ð5Þ; r2 ¼ 0:76: Since NRA is an indicator of nitrate uptake and the source water to the upwelling zone, the Kuroshio Subsurface Water, is rich in iodate and almost devoid of iodide, these relationships are consistent with the conceptual model that iodate reduction and nitrate uptake occur in tandem through the activities of the ÿ enzyme nitrate reductase. Since NRA represents an instantaneous rate while [R-IOÿ 3 ] and [R-I ] are concentrations, these strong correlations also suggest that iodate reduction and hence nitrate uptake had operated at approximately constant rates during the residence time of the water in the upwelling zone. Thus, the depletion of iodate and the gain in iodide in the upwelled water relative to its source water were integrations of the uptake and reduction of iodate over this residence time. The slope of the relationship *Corresponding author. Tel.: +1-757-683-4932; fax: +1-757-683-5303. E-mail address: [email protected] (G.T.F. Wong). 1 Present address: Department of Oceanography, Texas A&M University at Galveston, 5007 Ave. U., Galveston, TX 77551, USA. 0278-4343/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S 0 2 7 8 - 4 3 4 3 ( 0 0 ) 0 0 0 8 6 - 8
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between R-iodate and NRA represented the product of this residence time and the biological discrimination of iodate reduction relative to nitrate uptake by the enzyme. Outside of the upwelling area, R-iodate and R-iodide did not correlate well with NRA, probably as a result of the masking effect of mixing among water masses with undefined concentrations of pre-existing iodate and iodide. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: East China Sea; New production; Nitrate uptake; Iodine; Trace element speciation
1. Introduction New production is the fraction of primary production in the oceans that is supported by nutrients originating from outside of the euphotic zone (Dugdale and Goering, 1967). An understanding of its governing processes and an accurate estimation of its global magnitude are crucial factors for deciphering the present apparent imbalance in the global budget of anthropogenic carbon (Platt et al., 1992; Siegenthaler and Sarmiento, 1993; Sarmiento and Le Quere, 1996) which has been linked to the green-house effect. While allochthonous nutrients to the euphotic zone may originate from various sources, such as the upwelling of deep water, atmospheric deposition, nitrogen fixation and riverine input, in the open oceans, away from the influence of land, the input of nutrients by the global upwelling of deep waters to the surface oceans is a major, if not the dominant, contributor. Since combined nitrogen exists almost exclusively as nitrate in the deep waters, new production has been represented by nitrate uptake (Eppley, 1989). Nonetheless, studying nitrate uptake through direct observations by using labeled nitrate suffers from significant limitations. Using a radioactive isotope is not feasible since there is no readily available radioactive nitrogen (Wada and Hattori, 1991). The sensitivity in measuring the uptake of 15N-labelled nitrate in incubation experiments (Eppley, 1989) is somewhat limited since 15N is also a naturally occurring isotope of nitrogen with relatively high abundance. In oligotrophic waters, when the nitrate concentration is low, the amount of added 15N-labelled nitrate may be larger than the natural reservoir and cause artificially stimulated nitrate uptake and unreliable results (Dugdale and Wilkerson, 1986; McCarthy et al., 1992, 1996; Allen et al., 1996). Thus, using chemical analogues is a valuable complementary experimental approach for gaining additional insights into the biogeochemical dynamics of the marine nitrogen system. Halates are attractive candidates as chemical analogues for studying nitrate uptake because of their similar ionic formula to nitrate. 36Cl-labelled chlorate has been used extensively to study nitrate transport (Balch, 1985, 1987; Balch et al., 1987) and the rate of transport of chlorate into the cells has been found to be linearly related to nitrate uptake rates in both laboratory cultures of marine phytoplankton and in the field although the biological affinity for chlorate relative to nitrate was about three orders of magnitude lower. However, unlike nitrate, chlorate is not a natural constituent of seawater. While nitrate uptake involves transport, reduction and assimilation, chlorate can only trace the first step in the process. Iodate, being a naturally occurring species of dissolved iodine in seawater, may be a more powerful natural analogue for studying nitrate uptake. Dissolved iodine is a bio-intermediate element which exists primarily as iodate and iodide in the oceans (Wong, 1991). Although iodide is thermodynamically unstable relative to iodate in oxic seawater and is virtually absent in the
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deep water, it co-exists ubiquitously with iodate in the surface oceans (Tsunogai and Henmi, 1971; Tsunogai, 1971; Wong and Brewer, 1974, 1977; Elderfield and Truesdale, 1980; Wong et al., 1985; Jickells et al., 1988; Wong and Zhang, 1992a; Tian and Nicolas, 1995; Wong, 1995; Campos et al., 1996; Tian et al., 1996). On the other hand, dissolved iodine exists almost exclusively as iodate in the deep water. Because of the chemical similarities between iodate and nitrate, it has been long suspected that the unstable iodide is formed by the biologically mediated reduction of iodate through the activity of the enzyme nitrate reductase (Tsunogai and Sase, 1969) which also is the essential enzyme that initiates nitrate uptake (Wada and Hattori, 1991). If this hypothesis is true, then, iodate reduction may be intertwined with nitrate uptake and iodate may be used as an analogue for studying nitrate uptake and new production (Wong, 1991). The relationship between chlorate transport and nitrate uptake reported by Balch and coworkers (Balch, 1985, 1987; Balch et al., 1987) is suggestive of this possibility. Recent laboratory studies (Udomkit and Dunstan, 1991; Moisan et al., 1994; Udomkit, 1994) have provided direct evidence that iodate can be taken up by marine phytoplankton and iodide is formed in the process. Hung (1999) found that nitrate reductase extracted from natural marine phytoplankton assemblages and from a culture of Skeletonema costatum can also reduce iodate to iodide. However, while the laboratory evidence points strongly to the possibility of a biologically mediated reduction of iodate to iodide which is linked to nitrate uptake, no field observations which relate the changes in speciation of dissolved iodine in the oceans to an indicator of nitrate uptake have been reported. Nitrate uptake by phytoplankton involves three enzymatically mediated steps: (1) the reduction of nitrate to nitrite by nitrate reductase, (2) the reduction of nitrite to ammonia by nitrite reductase, and (3) the assimilation of the ammonia formed (Wada and Hattori, 1991). The determination of nitrate reductase activity (NRA) measures the rate of the first step under a constant set of operationally defined conditions (Eppley et al., 1969, 1970; Packard et al., 1971, 1978; Slawyk and Collos, 1976; Eppley, 1978; Hochman et al., 1986; Berges and Harrison, 1995). If nitrate reduction is the rate-limiting step in nitrate uptake, NRA will be proportional to nitrate uptake (Eppley et al., 1970; Packard et al., 1971; Wheeler, 1983; Berges and Harrison, 1993). Indeed, Hung et al. (1998, 2000) reported that NRA is linearly and quantitatively related to 15 N-labelled nitrate uptake under nutrient- and light-replete conditions in the East China Sea. Here we present the first field evidence of the relationships between the concentrations of iodate and iodide, and, NRA in the oceans.
2. Environmental setting The East China Sea is consisted of the water on the East China Sea Shelf and the water in the deep Okinawa Trough. The East China Sea Shelf is one of the large and more productive marginal seas of the world. It extends from the Cheju Island, at about 338200 N, in the north to the northern coast of the island of Taiwan, at about 258N, in the south. It is bounded to the east by the Kuroshio and to the west by continental China from which it receives the outflow of Changjiang, one of the large rivers of the world (Milliman and Jin, 1985). In the southern East China Sea Shelf, the outflow of the Minjiang can also be locally significant. These freshwater inflows result in the presence of the fresh, cold and nutrient-rich Coastal Water along the Chinese coast (Wong et al., 1998). At the southeastern corner of the East China Sea, after the Kuroshio enters the Okinawa Trough from the
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western Philippine Sea through the Suao-Yonaguni Pass over the Ilan Ridge, this northward travelling current runs into the shelf edge of the southern East China Sea Shelf which stretches in a west to east direction. As a result, the Kuroshio turns eastward and flows along the shelf edge. At the point where the Kuroshio changes its direction, a year-round upwelling center is formed northeast of Taiwan where the cold nutrient-rich Kuroshio Subsurface Water enters the East China Sea Shelf and becomes a significant source of nutrient to the shelf (Wong et al., 1991, 2000a; Liu et al., 1992a, b). This upwelling is strong enough at times that its influence can become clearly evident even in the surface waters. Along the shelf edge, there is also extensive exchange between the East China Sea Shelf and the Kuroshio through frontal processes so that the warm, saline and nutrient-poor Kuroshio Surface Water may find its way onto the shelf (Chern and Wang, 1990; Chern et al., 1990; Su et al., 1990; Wong et al., 1991; Hsueh et al., 1992; Liu et al., 1992a, b; Chen et al., 1995; Gong and Liu, 1995; Chen, 1996). Another source of surface water to the shelf is the Taiwan Current Warm Water which enters the Sea through the Taiwan Strait from the south. This water is nutrient poor while its temperature and salinity are slightly lower than those of the Kuroshio Surface Water. Thus, the major surface water masses in the East China Sea Shelf are the Coastal Water, the Kuroshio Surface Water, the upwelled Kuroshio Subsurface Water and the Taiwan Current Warm Water (Liu et al., 1992a; Chen et al., 1995; Gong and Liu, 1995).
3. Methods Eight stations were occupied in a transect across the southern East China Sea between May 2 and 15, 1996 aboard the R/V Ocean Research I during Cruise ORI-449 of the Kuroshio Edge Exchange Processes (KEEP) Study (Wong et al., 2000b). The locations of the stations are shown in Fig. 1. At each station, the distributions of temperature and salinity were recorded with a SeaBird model SBE9/11 conductivity–temperature–depth (CTD) recorder. Discrete samples were collected with GO-FLO bottles mounted onto a Rosette Sampling assembly (General Oceanic). Sub-samples were then obtained for the determination of salinity, the dissolved iodine species, NRA, nitrite and (nitrate+nitrite). Salinity was determined in a shore-based laboratory with an Autosal salinometer with a precision of 0.003. Nitrite and (nitrate+nitrite) were determined onboard ship by the standard pink azo dye method which has been adapted for use with a flow injection analyzer (Morris and Riley, 1963; Strickland and Parsons, 1972; Pai et al., 1990; Gong, 1992). The precisions for the determination of nitrate and nitrite were 0.3 and 0.03 mM, respectively. The sub-samples for the determination of the dissolved iodine species were drawn and stored frozen in polyethylene bottles (Wong, 1973) and returned to the shore-based laboratory for analyses. Both iodate and iodide were determined by using an EG&G-PAR Model 384B-4 polarographic analyzer system with a Model 303A static mercury drop electrode. Iodate was determined directly by differential pulse polarography according to the method of Herring and Liss (1974) as modified by Wong and Zhang (1992b). At concentrations above 0.1 mM, the precision of the method was 0.006 mM. Iodide was determined directly by cathodic stripping square wave voltammetry by the method of Luther III et al. (1988) as modified by Wong and Zhang (1992b, c). The precision of the method was 0.005 mM. Sub-samples for the determination of NRA and the dissolved iodine species were obtained from the same sample at Stations 49–53. At Sta. 55, they were drawn from different casts. NRA was
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Fig. 1. The locations of the stations in a transect across the southern East China Sea.
determined onboard ship by a modified version of the method of Hochman et al. (1986). Seawater samples (20 l at Sta. 55 and 4–8 l at the other stations) were collected just after sunrise and filtered through a 47-mm Gelman type A/E glass fiber filter. The filter was transferred to a beaker together with 1 ml of a phosphate buffer (150 mM of K2HPO4 adjusted to a pH of 7.6), 50 ml of toluene, 0.2 ml of 6.5 mM NADH (Sigma Chemical Co.) and 0.2 ml of 0.1 M potassium nitrate. The beaker was placed on a vortex mixer and mixed for 5 min at room temperature. Then, the reaction was terminated by transferring 1 ml of the slurry from the beaker into a centrifuge tube containing 1.7 ml of 0.13 M ZnSO4 at 978C. After the solution was allowed to cool, 0.2 ml of 1 N NaOH was added and the mixture was centrifuged for 20 min at 4000 rpm. Two ml of the supernatant liquid was removed for the determination of nitrite by adding 0.1 ml of a 2% (w/v) sulfanilamide solution in 15% hydrochloric acid and 0.1 ml of a 0.3% (w/v) N-1-naphthylethylenediamine hydrochloride solution to the supernatant liquid and measuring the absorbance of the azo dye formed at 543 nm (Strickland and Parsons, 1972) with a Brinkman PC-800 Probe Colorimeter equipped with a probe tip with a 2-cm light path. The precision of the measurement was about 5%. 4. Results and discussions 4.1. Hydrography and the distributions of NRA and the dissolved iodine species The distributions of temperature, salinity, nitrate, rationalized iodate (R-iodate, R-IOÿ 3 ) and ÿ rationalized iodide (R-iodide, R-I ) in the surface waters at 10 m across the transect are shown in
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Figs. 2a and b. R-iodate and R-iodide are the concentrations of iodate and iodide normalized to a salinity of 35 (Fig. 2b, Truesdale, 1994). By normalizing concentrations to a constant salinity, changes in concentrations resulting from variation in salinity are removed. At least three of the four major surface water masses were clearly represented in the transect. The colder and fresher Coastal Water was found at Sta. 48 and 49. The upwelled Kuroshio Subsurface Water was represented as the cold and nitrate-rich water at Sta. 51–53. The Kuroshio Surface Water was found at Sta. 54 and 55 where nitrate was virtually absent and the temperatures were the highest. The water at Sta. 50, with its high temperature and low concentration of nitrate, might have represented Taiwan Strait Warm Water (Wong et al., 1991; Liu et al., 1992a, b). However, the present data set was too limited to make a definitive assignment. The upwelled water was clearly distinguished from the other surface water masses by its high concentrations of R-iodate and low concentrations of R-iodide (Fig. 2b). The vertical distributions of sigma-y, nitrate, NRA, R-iodate and R-iodide at Sta. 49, 53 and 55, representing the mesotrophic coastal zone, the upwelling zone and the oligotrophic Kuroshio, are shown in Figs. 3, 4 and 5, respectively. The thinnest mixed layer, about 10 m thick, and the shallowest nitrate-cline, which started almost at the sea surface, were found in the upwelling zone (Fig. 4) where vertical transport should have been the strongest. In contrast, the water column in the coastal zone (Fig. 3), which was also highly turbid, was well mixed down to about 35 m but nitrate was depleted only down to 20 m probably as a result of light limitation on phytoplankton activity. In the Kuroshio, the mixed layer was 25 m thick and nitrate was depleted at depths even below the mixed layer (Fig. 5). Similar levels of NRA were found in the coastal zone and the upwelling zone. In both cases, the highest level of NRA was found at the sea surface and it decreased rapidly with depth to background levels at about 25 m. In contrast, NRA in the Kuroshio was about one order of magnitude lower but it extended to greater depths. In fact, it increased with depth until it reached a sub-surface maximum in the pycnocline at 80 m. The distributions of R-iodate and R-iodide at these stations approximately followed the local hydrography. In the coastal zone (Fig. 3b), the concentration of R-iodide remained consistently
ÿ ÿ Fig. 2. The distributions of (a) temperature (*), salinity (*) and NOÿ 3 (m), and (b) R-IO3 (*) and R-I (*) at 10 m across the transect.
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ÿ ÿ Fig. 3. The vertical distributions of (a) sigma-t (*), NOÿ 3 (*) and NRA (&), and (b) R-IO3 (*) and R-I (*) at Sta. 49 in the coastal zone.
ÿ ÿ Fig. 4. The vertical distributions of (a) sigma-t (*), NOÿ 3 (*) and NRA (&), and (b) R-IO3 (*) and R-I (*) at Sta. 53 in the upwelling zone.
high, never below 100 nM, while that of R-iodate remained consistently low, never above 330 nM, through out the water column. The variations in the concentrations of R-iodate and R-iodide with depth were also small, being confined to within the ranges of about 75 and 50 nM respectively. Within the mixed layer in the top 35 m of the water column, there were weak indications of an increase in the concentration of R-iodate and a decrease in the concentration of R-iodide with
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ÿ Fig. 5. The vertical distributions of (a) sigma-t (*), NOÿ 3 (*) and NRA (&) at Sta. 55 Cast 3, and (b) R-IO3 (*) and ÿ R-I (*) at Sta. 55 Cast 1 in the Kuroshio.
depth. In the bottom water below 35 m, where both sigma-y and nitrate increased significantly, indicating that a different water mass might have been present, there were suggestions of a slight decrease in the concentration of R-iodate and an increase in the concentration of R-iodide. On the other hand, in the upwelling zone (Fig. 4b) and in the Kuroshio (Fig. 5b), the highest concentration of R-iodide and the lowest concentration of R-iodate were found in the mixed layer. The concentration of R-iodide decreased while that of R-iodate increased systematically with depth until the former became minimal at concentrations below 30 nM while the latter reached concentrations exceeding 380 nM. Thus, in both cases, as observed in other parts of the oceans (Wong, 1991), the vertical distributions of R-iodate and R-iodide were approximate mirror images. The highest concentration of R-iodate, >300 nM, and the lowest concentration of R-iodide, 5100 nM, in the mixed layer were found in the upwelling zone. The upwelling Kuroshio Subsurface Water originates from about 300 m in the Okinawa Trough with t (temperature)=13– 158C, S (salinity)=34.4–34.6, [NOÿ 3 ]=13–16 mM (Wong et al., 1991; Liu et al., 1992a, b). No sample was collected at this depth in the Okinawa Trough during this cruise. The deepest sample ÿ was collected at 203 m at Sta. 55 where t=18.48C, S=34.8, [NOÿ 3 ]=4 mM, [R-I ]=11 nM and ÿ [R-IO3 ]=408 nM. Even at this shallower depth, the concentrations of R-iodate and R-iodide had apparently reached their asymptotic concentrations and were not expected to change significantly any further with depth. In another cruise in May 1994, a sample was collected at 350 m in the ÿ Okinawa Trough and its properties were t=148C, S=34.6, [NOÿ 3 ]=11 mM, [R-I ]=8 nM, ÿ [R-IO3 ]=452 nM (Lin, 1995). Thus, dissolved iodine existed almost exclusively as iodate in the source water of the upwelling system.
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4.2. Relationships between iodate and iodide and a conceptual model for the cycling of dissolved inorganic iodine species in the surface oceans The linear relationship between R-iodide and R-iodate at all stations is shown in Fig. 6. A similar relationship was found in the South Atlantic Bight (Wong and Zhang, 1992c; Wong, 1995). Model II linear regression analysis (Laws and Archie, 1981) of the data from this study yields ÿ ½R-IOÿ 3 ¼ ÿ1:06ð0:06Þ½R-I þ 424ð15Þ;
r2 ¼ 0:87; n ¼ 50;
ÿ where [R-IOÿ 3 ] and [R-I ] are in nM and n is the number of observations. The slope of the line is indistinguishable from ÿ1 within statistical uncertainties. Thus, removal of iodate in the surface oceans was accompanied by an almost quantitative production of iodide. In other words, unlike nitrate which can be sequestered rather effectively in the particulate phase during nitrate uptake, if iodate is lost in the surface oceans through biologically mediated uptake, it is converted to iodide which is quantitatively exuded to the surrounding water by the organisms. Little of the iodate processed by the organisms is retained in the particulate phase and little of the iodide exuded is converted to a form other than iodate. Indeed, Udomkit and Dunstan (1991), Moisan et al. (1994) and Udomkit (1994) found uptake of iodate by phytoplankton and an associated appearance of iodide in laboratory cultures. Wong (1980) and Luther III et al. (1995) observed that iodide, though thermodynamically unstable relative to iodate, is metastable. Once it is formed, it cannot be readily oxidized back to iodate. Based on this information, the following conceptual model for cycling among the iodine species in the oceans may be constructed. Through global upwelling, virtually iodide-free and iodate-rich deep water is supplied to the surface oceans where nitrateand iodate-uptake may occur in tandem. The iodate taken up is exuded almost quantitatively to the surrounding water as iodide. Since iodide is not readily reconverted back to iodate once it is formed, the depletion of iodate and the enrichment of iodide in the surface oceans relative to the deep oceans represent an integration of the reduction of iodate over the residence times of the water of the surface oceans. If the reduction of iodate is coupled to nitrate uptake, the changes in
ÿ Fig. 6. The relationships between R-IOÿ 3 and R-I at all the stations: Sta. 48 } *; Sta. 49 } *; Sta. 50 } &; Sta. 51 } &; Sta. 52 } n; Sta. 53 } m; Sta. 54 } 5; Sta. 55 } .. The line represents the Model II linear regression line.
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the speciation of dissolved inorganic iodine in the surface oceans will also be an integrator of nitrate uptake over time. Since upwelling does not occur uniformly over the world’s oceans, the concentration of iodide and iodate at a given location in the surface oceans may reflect not only the effect of in situ biologically mediated reduction of iodate but also mixing with other surface water masses containing pre-existing concentrations of iodate and iodide. Thus, on a regional scale, this conceptual model is directly applicable only to upwelling centers where the source water is well defined and the input of iodide-free deep water dominates over mixing with other surface water masses. The linear relationship between R-iodide and R-iodate contained more variability moving from the oligotrophic Kuroshio water to the coastal water at Sta. 48–50 as the concentration of Riodate decreased and R-iodide increased (Fig. 6). Similar behavior was also observed previously in the South Atlantic Bight (Wong and Zhang, 1992a; Wong, 1995). In fact, the relationship broke down in the inner shelf of the South Atlantic Bight. This may be caused by the conversion of the dissolved inorganic iodine species to particulate iodine, gaseous iodine and/or organic iodine. Wong and Cheng (1998) have reported recently the occurrence of significant quantities of dissolved organic iodine in coastal waters. 4.3. Relationships between iodate and NRA, and, iodide and NRA The relationships between R-iodate and NRA, and R-iodide and NRA in the upwelling water ÿ are shown in Fig. 7. Both [R-IOÿ 3 ] and [R-I ] were strongly correlated to NRA. Based on Model II linear regression analyses (Laws and Archie, 1981), the following relationships were found: ½R-IOÿ 3 ¼ ÿ10:2ð1:0ÞNRA þ 392ð12Þ; ½R-Iÿ ¼ 9:8ð1:1ÞNRA þ 27ð5Þ;
r2 ¼ 0:84; n ¼ 18;
r2 ¼ 0:76; n ¼ 18;
ÿ ÿ1 and n is the number of samples where [R-IOÿ 3 ] and [R-I ] are in nM and NRA is in nM-N h with readily detectable concentrations of iodate, iodide and level of NRA. The intercepts of these
ÿ Fig. 7. The relationships between (a) R-IOÿ 3 and NRA, and (b) R-I and NRA in the upwelling zone at Sta. 51 (*), 52 (*) and 53 (&). The Model II linear regression lines are shown.
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relationships represent the composition of the source water. Since iodate and iodide are in the dissolved phase while NRA measures the instantaneous activity of an enzyme extracted from the particulate phase, the strong correlations suggest that there was no decoupling between the dissolved and particulate phases and that the processes that caused the disappearance of iodate and the appearance of iodide occurred at approximately constant rates during the lifetime of the water in the upwelling zone. The slopes of the two relationships were of opposite signs but their absolute values were indistinguishable from each other within their statistical uncertainties. Thus, the disappearance of iodate was approximately equal to the appearance of iodide so that these relationships were consistent with the conceptual model as described previously. According to this model, d½R-IOÿ 3 ¼ ðIRAÞ t; ÿ where d [R-IOÿ 3 ] is the deficit in [R-IO3 ] in the upwelling water relative to its source water, IRA is the iodate reduction activity and t is the residence time of the upwelling water which is controlled by the physical dynamics of the upwelling system. If
IRA ¼ NRAðIRR=NRRÞ; where IRR is the iodate reduction rate and NRR the nitrate reduction rate, IRR/NRR represents the biological discrimination factor of the enzyme nitrate reductase for selecting between iodate and nitrate for the reduction. Then, ðd½R ÿ IOÿ 3 =NRAÞ ¼ ðIRR=NRRÞt; ÿ where d [R-IOÿ 3 ]/NRA is the slope of the relationship between [R-IO3 ] and NRA. This slope is ÿ ÿ1 ÿ1 in the East China Sea. By considering the mass balance of oxygen, 10.2 nM-IOÿ 3 nM -NO3 h the upwelling rate at this upwelling zone of the East China Sea has been estimated to be 5 m dÿ1 (Liu et al., 1992b). Since the water depth at the shelf edge in the upwelling zone is about 100 m thick, the residence time of the upwelling water will be about 20 d. Thus, this model would yield an IRR/NRR of 1/50. The value of IRR/NRR is poorly known. The information on iodate uptake rates is limited to laboratory cultures of four species of phytoplankton which gave values ranging from 0.003 to ÿ1 ÿ1 and two field experiments with rates of 0.08 and 0.26 nmol0.24 nmol-IOÿ 3 mg -chl-a h ÿ1 ÿ1 ÿ giving an average of 0.1 0.1 nmol-IO3 mgÿ1-chl-a hÿ1 (Udomkit and IO3 mg -chl-a h Dunstan, 1991; Moisan et al., 1994; Udomkit, 1994). During this East China Sea cruise, nitrate uptake rates were estimated at some stations by measuring the uptake of 15N-labelled nitrate and/ or NRA. When both measurements were made simultaneously, they were strongly correlated with each other with an average ratio of approximately 1 when there were sufficient ambient light and nitrate (Hung et al., 1998, 2000). This indicates that NRA was approximately a quantitative indicator of nitrate uptake. At Sta. 52 in the upwelling zone, nitrate uptake was determined at various depths in the euphotic zone by measuring NRA and the uptake of 15N-labeled nitrate simultaneously in one cast and by measuring NRA only in another cast. The average of all the ÿ1 ÿ1 (Hung et al., 1998, 2000). If the average values measurements was 9 2 nmol-NOÿ 3 mg -chl-a h of the reported iodate uptake rates and the nitrate uptake rates at Sta. 52 are used, then, IRR/ NRR is about 1/90. More recently, Hung (1999) determined nitrate and iodate reduction activities in nitrate reductase extracted from four coastal phytoplankton assemblages and a culture of
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Skeletonema costatum and found IRR/NRR ranging between 1/39 and 1/99. Considering the uncertainties involved in each of these approaches for estimating IRR/NRR, the agreement between the model generated value, 1/50, and these other estimated values, 1/39–1/99, was quite reasonable and lends support to the conceptual model proposed here for cycling among the iodine species in the oceans. The relationships between R-iodate and NRA, and R-iodide and NRA outside of the upwelling zone in the East China Sea Shelf at Sta. 49 and 50 are shown in Fig. 8. (The data from Sta. 55 could not be treated in this manner because the sub-samples for the determinations of the dissolved iodine species and NRA were drawn from different casts.) The conceptual model suggests that mixing among surface water masses with different pre-existing concentrations of Riodate and R-iodide may have significant effects on their observed concentrations. Indeed, in contrast to the strong correlations found in the upwelling zone, there was weak to no correlation between R-iodate and NRA, and R-iodide and NRA in these waters. Thus, the in situ biologically mediated reduction of iodate to iodide could not be the primary control of their concentrations.
4.4. Iodate depletion in the surface oceans and global new production The plausibility of the proposed linkage between iodate reduction and nitrate uptake may be further examined by taking into account the reported estimates of global new production. The average deficit of iodate in the surface oceans relative to the deep oceans is about 0.15 mM (Wong, 1991, 1995). The average thickness of the surface mixed layer is 200 m. Hence, the iodate deficit in the mixed layer is 3 104 mmol mÿ2. Since the residence time of the surface waters in the oceans is about 30 yr, the annual disappearance of iodate by its reduction to iodide in the surface oceans is 1000 mmol mÿ2 yrÿ1. If IRR/NRR is between 1/39 and 1/100 as suggested previously, then, nitrate uptake, or nitrate-based production, is 4 104–1 105 mmol-N mÿ2 yrÿ1 or 3.2–8 g-C mÿ2 yrÿ1. At a global primary production of 125 g-C mÿ2 yrÿ1 (Falkowski et al., 1998), the ratio of nitratebased production to primary production is 0.03–0.06. In comparison, the global new production
ÿ Fig. 8. The relationships between (a) R-IOÿ 3 and NRA, and (b) R-I and NRA at Sta. 49 (*) and 50 (*) in the shelf outside of the upwelling zone. The lines represent the relationships in the upwelling zone.
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and the ratio of new production to primary production, or f-ratio, have been estimated to be 9–44 g-C mÿ2 yrÿ1 and 0.15–0.36 (Eppley, 1989; Falkowski et al., 1998). Obviously, there are large uncertainties associated with the values estimated from the dissolved iodine species. For example, the value of IRR/NRR is still poorly known. If there is any oxidation of iodide to iodate during the residence time of the surface oceans, the reduction of iodate, and thus the global nitrate-based production and its ratio to primary production would have been underestimated. Furthermore, nitrate-based production and its ratio to primary production do not correspond exactly with new production and the f-ratio. In fact, the former is likely to be lower than the latter since allochthonous combined nitrogen may not be supplied to the surface oceans in the form of nitrate only. Nonetheless, despite the preliminary nature in the approach for estimating nitrate uptake from iodate deficit in the surface oceans and the possible conceptual mismatch between nitratebased production and new production, the values estimated from these two approaches are of similar magnitude. This apparent agreement is notable and is consistent with a linkage between the iodine cycle and the nitrogen cycle in the oceans.
5. Conclusions The results from this study provide field evidence that supports the idea that the depletion of iodate in the surface oceans is caused by a biologically mediated reduction of iodate to iodide through the activity of the enzyme nitrate reductase. In the process, the iodate reappears in the dissolved phase as iodide almost quantitatively so that little of the iodate processed by the organisms is sequestered in the particulate phase. Thus, the depletion of iodate and the enrichment of iodide relative to the composition of the source water of a surface water mass represent an integration of NRA through the lifetime of the water mass. Acknowledgements This work was supported by the National Science Foundation through grant numbers OCE9301298 and INT-9515521 to Wong. The manuscript was prepared while Wong occupied a research chair at the National Center for Ocean Research (NCOR) of the National Science Council of Taiwan. We thank the captain and the crew of R/V Ocean Researcher I for their assistance in sample collection. This cruise, ORI-449 was funded by the National Science Council of Taiwan as part of the Kuroshio Edge Exchange Process (KEEP) program. Hydrographic data and data on nutrient distributions and 15NOÿ 3 uptake were provided by G.-C. Gong and F.-K. Shiah. This is contribution number 30 of NCOR.
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