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JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 111, C08016, doi:10.1029/2005JC003216, 2006
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Nitrogen isotope constraints on subantarctic biogeochemistry Peter J. DiFiore,1 Daniel M. Sigman,1 Thomas W. Trull,2 Martin J. Lourey,3 Kristen Karsh,1,2 Greg Cane,1 and Ruby Ho1 Received 10 August 2005; revised 29 January 2006; accepted 28 April 2006; published 11 August 2006.
[1] We report nitrate (NO 3 ) nitrogen isotope ratios for seawater samples collected in the
Subantarctic Zone of the Southern Ocean during both winter and summer as part of the Australian Antarctic CRC Subantarctic Zone (SAZ) Project. The concentration and 15 14 N/ N of the wintertime surface nitrate are very close to those of the subantarctic thermocline. The 15N/14N of nitrate in the surface increases sharply into the summer even though there is little seasonal change in nitrate concentration. There are two possible end-member explanations for this observation. First, there may be significant equatorward nitrate transport during the summer, including a supply from the Antarctic surface. Second, the isotope effect of algal nitrate assimilation may be higher than has been estimated elsewhere, for example, for the seasonal sea ice zone of the Antarctic. We use a simple geochemical box model of the SAZ surface mixed layer as it evolves over the course of the summer to simulate salinity, nitrate concentration, and the 15N/14N of nitrate and sinking N. Our results suggest that a significant portion (30%) of the summertime SAZ nitrate is supplied from south of the Subantarctic Front and that N export is 3.5 mmol N m2 d1. Our approach also identifies the necessity of an isotope effect for nitrate assimilation in the SAZ of 7% and probably 8–9%. Comparison to laboratory results suggests that this relatively high isotope effect may result from light limitation of algal growth in the SAZ. Citation: DiFiore, P. J., D. M. Sigman, T. W. Trull, M. J. Lourey, K. Karsh, G. Cane, and R. Ho (2006), Nitrogen isotope constraints on subantarctic biogeochemistry, J. Geophys. Res., 111, C08016, doi:10.1029/2005JC003216.
1. Introduction [2] The Southern Ocean represents a region of intense communication between the ocean and atmosphere as well as a critical junction in the exchange of waters between the cold, deep ocean and the warmer, low-latitude surface and thermocline. The combined effect of wind-driven surface water transport and geostrophy as well as the densification associated with surface cooling and sea ice formation result in the surfacing of deep CO2-charged, nutrient-rich water in the Antarctic. Despite intense export production in some parts of the Antarctic, the consumption of the major nutrients (N and P) is incomplete, so that excess CO2 in upwelled deep water escapes to the atmosphere. Westerly winds advect surface water northward across the Polar frontal zone and into the Subantarctic Zone (SAZ), where biological uptake draws nutrient concentrations to lower values northward and generates a sinking flux of organic matter that reinjects part of the escaped CO2 back into the ocean interior [Takahashi et al., 1997]. However, the major 1 Department of Geosciences, Princeton University, Princeton, New Jersey, USA. 2 Antarctic Climate and Ecosystem Cooperative Research Centre, CSIRO Marine and Atmospheric Research, Hobart, Tasmania, Australia. 3 CSIRO Marine and Atmospheric Research, Wembley, Western Australia, Australia.
Copyright 2006 by the American Geophysical Union. 0148-0227/06/2005JC003216$09.00
nutrients are not completely consumed in much of the Subantarctic, which may be due to limitation of phytoplankton growth by iron, silica, and/or light [Boyd et al., 1999, 2001; Debaar et al., 1995; Hutchins et al., 2001; Martin et al., 1990; Mitchell et al., 1991; Sedwick et al., 1999, 1997]. [3] The degree of SAZ nutrient drawdown affects not only atmospheric CO2 but also the nutrient content of the thermocline and thus the fertility and biogeochemistry of the low-latitude ocean. Nutrients are constantly being lost from the low-latitude surface ocean and thermocline by the rain of organic detritus that survives into the abyss. These nutrients may be dominantly resupplied to the upper ocean from the new middepth waters that form in the Subantarctic [Sarmiento et al., 2004]. If so, the nutrient supply to the subtropical, tropical, and equatorial surface ocean depends largely on the incomplete consumption of nutrients by algae in the Southern Ocean surface; if nutrients in the Southern Ocean surface were more efficiently depleted, the supply of nutrients to the low-latitude thermocline and surface ocean would be reduced [Keir, 1988; Matsumoto et al., 2001; Robinson et al., 2005; Sigman et al., 2003]. Increased nutrient drawdown could occur in either the Antarctic or the Subantarctic, but the nutrient concentration in the Subantarctic is the final determinant of the nutrient supply to the low-latitude thermocline. Thus the development of a quantitative and mechanistic understanding of subantarctic biogeochemistry is central to an understanding of global ocean biogeochemistry.
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[4] The integrated rates of net primary production and export production estimated from direct measures are plagued by the spatial and temporal variability of the surface ocean as well as artifacts associated with making these measurements (e.g., bottle effects and sediment trap artifacts). Dissolved geochemical tracers are useful because they integrate over heterogeneities and do not involve manipulation of the organisms responsible for the biogeochemical fluxes. Over the last forty years, there has been great progress in characterizing the spatial distribution of bioactive species in the ocean. The distributions of dissolved inorganic carbon, alkalinity, dissolved oxygen, and the nutrients nitrate, phosphate, and silicate are relatively well-defined, and the databases are being continuously improved [Conkright et al., 2002; Key et al., 2004]. The use of these distributions to quantify physical and biological fluxes is an area of active research. If the ocean circulation was known, then the nutrient fields could be overlain on the circulation field to quantify the uptake of nutrients and carbon throughout the surface ocean (‘‘nutrient restoring’’ [Deutsch et al., 2001; Dunne et al., 2005; Jin and Gruber, 2003; Najjar et al., 1992; Schlitzer, 2002]). However, uncertainties in the model-derived circulation compromise these estimates. In the surface ocean, where transport and mixing occur in complex patterns, it can be difficult to derive rates and patterns of nutrient assimilation from nutrient concentration fields because both assimilation and water exchange affect the nutrient concentration. Thus additional dissolved tracers with different sensitivities to physical and biological processes would be of great complementary use. [5] Nitrate assimilation by phytoplankton leaves a clear imprint on the isotopic composition of oceanic nitrate and on the products of phytoplankton growth. Field and laboratory studies have demonstrated isotopic fractionation associated with nitrate assimilation by phytoplankton, with the preferential incorporation of 14N into phytoplankton biomass [Altabet et al., 1991; Altabet and Francois, 1994; Altabet and McCarthy, 1985; Farrell et al., 1995; Francois et al., 1992; Montoya and McCarthy, 1995; Nakatsuka et al., 1992; Pennock et al., 1996; Wada, 1980; Wada and Hattori, 1978; Waser et al., 1998; Wu et al., 1997]. In the case of a finite nitrate pool, this pool becomes progressively enriched in 15N as nitrate is consumed, also leading to an increase in the d15N of newly formed biomass N (d15 N versus atmospheric N 2 = [[( 15 N/ 14 N) sample / (15N/14N)atm] 1]). [6] Because this anticorrelation between the degree of nitrate consumption and nitrate 15N/14N is propagated to the sinking flux out of the surface ocean and to deep sea sediments, the N isotopes have been used as an indicator of past changes in nutrient utilization (the ratio of nutrient uptake to gross nutrient supply) in Southern Ocean surface waters [Altabet and Francois, 1994; Francois et al., 1992, 1997; Robinson et al., 2004, 2005; Sigman et al., 1999b]. There are several processes and parameters that must be understood for the paleoceanographic application of the link between nitrate utilization and the N isotopes in the Southern Ocean. The d15N of the nitrate supply and the amplitude of isotope discrimination associated with nitrate assimilation are two key parameters relating nitrate utilization to the isotopic composition of nitrate in oceanic surface waters and
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of the sinking flux to the seafloor. Both parameters require quantification in the modern ocean, assessments of their variability, and the development of a mechanistic understanding of the parameters that control them. [7] As shown previously, the possible sources of nitrate to the subantarctic surface have distinct nitrate d15N-to 15 [NO 3 ] relationships (hereafter ‘‘d N/[NO3 ]’’) [Sigman et al., 1999a, 2000]. From the perspective of paleoceanographic studies, this largely represents an unwanted complexity. However, for modern ocean studies, it may prove useful in defining and quantifying the routes of nitrate supply to the subantarctic surface. Moreover, mixing of waters that have previously undergone nitrate assimilation has an effect on the d15N of nitrate that is very different from the effect of nitrate assimilation alone: while [NO 3] mixes conservatively, the d15N of nitrate of a volumetric mixture of waters is weighted toward the end-member with the higher [NO 3 ]. Thus assimilation and mixing in the upper ocean should be distinguishable when the concentration and isotope constraints are coupled. [8] Much as in paleoceanographic studies, the major limitation on nitrate d15N as a tool for modern upper ocean studies is uncertainty in the amplitude of N isotope discrimination associated with nitrate assimilation. This discrimination is quantified as the isotope effect, e, which is defined as (14k/15k 1), where 14k and 15k are the rate coefficients of nitrate assimilation for the 14N- and 15Nlabeled forms of nitrate, respectively. Currently, estimates of e from the ocean range between roughly 4 and 10% [Altabet and Francois, 2001; Karsh et al., 2003; Lourey et al., 2003; Sigman et al., 1999a], while the range observed in batch culture experiments is much greater, 0 to 20% [Granger et al., 2004; Montoya and McCarthy, 1995; Needoba et al., 2003; Waser et al., 1997]. The first Southern Ocean data yielded isotope effect estimates in the range of 4 to 6% [Sigman et al., 1999a]; however, subsequent estimates from the Southern Ocean near the polar frontal zone have yielded higher values (7 –10%) [Altabet and Francois, 2001; Karsh et al., 2003; Lourey et al., 2003]. There may be coherent spatial (i.e., environmentally driven) variation within the Southern Ocean and among nutrient-rich regions in general. For the degree of nitrate consumption to be derived from nitrate isotope data, a better understanding of the isotope effect and its controls must be developed. At the same time, evidence has arisen that the magnitude of the isotope effect is affected by the factors that limit phytoplankton growth [Needoba and Harrison, 2004; Needoba et al., 2004], so that reliable estimates of the isotope effect in the subantarctic ocean may have implications for what controls phytoplankton growth in this region. [9] Previous nitrate isotope measurements from subantarctic samples collected during the austral summer show clear signs of net northward transport of nitrate in the subantarctic surface layer, such that the underlying thermocline cannot be the sole source of nitrate to the surface layer [Sigman et al., 1999a]. The entire data set was consistent with nitrate being supplied from the Polar Frontal Zone and being assimilated with an isotope effect of 5%. However, this study included no samples collected during winter conditions, under which nitrate supply from the thermocline is most likely to occur.
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Figure 1. Orthographic projections of the Southern Ocean, south of Australia showing positions of cruises used in this study. The Subtropical Front (solid line) and Subantarctic Front (dashed line) are from Orsi et al. [1995]. (a) Hydrocast locations of AU9701, AU9706, AU9901, and SS9902 are shown as solid markers; sediment traps from Lourey et al. [2003] are shown as blue crosses. (b) Underway collections AU9701, AU9804, AU9901, SS9902 are shown as solid markers. Further cruise information is presented in Table 1.
[10] Here, we report new data for 15N/14N of nitrate from samples collected during both summer and winter conditions across the Subantarctic and Polar Frontal Zones south of Australia. While seasonal changes in surface nitrate concentration are unremarkable, we observe a dramatic summertime increase in nitrate 15N/14N across the entire Subantarctic. This indicates that the meridional gradient in nitrate concentration is purely a circulation feature during the winter, whereas it is strongly modified by assimilation during the summer. As in previous work [Sigman et al., 1999a], there is evidence for equatorward transport of
nitrate, especially close to the Subantarctic Front, the poleward border of the SAZ. However, the new seasonal information indicates that the high-nitrate 15N/14N in the SAZ surface is generated in the very short time interval associated with summertime stratification and nitrate drawdown. Over this short time interval, surface salinity has been used as a constraint on water transport [Lourey and Trull, 2001; Wang et al., 2001], as ocean/atmosphere exchanges of freshwater have been found to be insignificant during the spring/summer productive season [Rintoul and England, 2002]. The modest summertime decrease in sub-
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Table 1. Cruises and Sampling Season Winter Summer Winter Summer Winter
Cruise AU9701 AU9706 AU9804 SS9902 AU9901
Research Vessel a
R/V Aurora Australis R/V Aurora Australis R/V Aurora Australis R/V Southern Surveyorb R/V Aurora Australis
Start Date
End Date
Underway Stations
Casts
9 Sep 1997 28 Feb 1998 29 Oct 1998 9 Feb 1999 16 Jul 1999
22 Sep 1997 1 Apr 1998 23 Dec 1998 16 Feb 1999 6 Sep 1999
40 47 14 46
7 10 2 3
a
R/V Aurora Australis is operated by the Australian Antarctic Division. R/V Southern Surveyor is operated by the Australian Commonwealth Scientific and Industrial Research Organization (CSIRO). b
antarctic surface salinity essentially puts an upper bound on the quantity of Antarctic water imported into the Subantarctic during the summer. The data set reported here also benefits from sediment trap collections in this region and the constraint that they provide on the 15N/14N of sinking N [Lourey et al., 2003]. While uncertainties exist in the interpretation of these data, combining them with the seasonally resolved nitrate isotope data provides at least a rough constraint on the amplitude of the isotope effect of nitrate assimilation. We explore the constraints provided by the available data with a simple geochemical model of the SAZ surface mixed layer subsequent to the onset of warm season stratification, with emphasis placed on evaluating the magnitudes of Antarctic nitrate supply and N export during these periods and on developing a revised estimate of the isotope effect of nitrate assimilation in the SAZ.
2. Sample Sets [11] Water column depth profiles (‘‘hydrocasts’’) were collected from two companion sediment trap deployment/ retrieval cruises as a starting basis for comparison of winter and summer seasons in the Subantarctic Zone south of Tasmania (Figure 1 and Table 1). Meridional transects of hydrographic profiles were collected along 142E during September of 1997 (AU9701) and between 141 and 144.5E during March of 1998 (AU9706), both aboard the R/V Aurora Australis by the Antarctic Cooperative Research Centre (CRC). During AU9701, 7 profiles were collected for nitrate isotopes, augmented by 40 samples taken from 7 m depth by the ship’s underway system; during AU9706, 10 depth profiles were collected. Both cruises traverse the Subtropical front into the Subantarctic Zone and extend across the Subantarctic Front into the Polar Frontal Zone at 52S (Figure 1). [12] To improve our interseasonal comparison, our sample set was augmented by subsequent underway collections
from other SAZ transect cruises AU9804, AU9901, and SS9902 (Table 1 and Figure 1b). AU9804 and AU9901 transects were completed on the R/V Aurora Australis during 29 October to 23 December 1998 and 16 July to 6 September 1999, respectively. AU9804 included 47 underway surface samples, AU9901 included 46 underway samples and 3 hydrocasts. SS9902 completed on the R/V Southern Surveyor of the Australian Commonwealth Scientific and Industrial Research Organisation (CSIRO) during 9 – 16 February 1999, consisted of 14 underway collections and 2 hydrocasts at 44S and 54S. [13] Samples were collected in acid- and deionized water– washed 500 mL HDPE bottles. The bottles were rinsed twice with sample water before filling. The samples were preserved for nitrate concentration and 15N/14N analysis by acidification with the addition of 0.5 mL 50% HCl to each 500 mL seawater sample, bringing the sample pH to between 2 and 3.
3. Methods [14] Nitrate concentration ([NO 3 ]) was analyzed by standard colorimetric methods at the University of Tasmania – Antarctic CRC [Eriksen, 1997; Strickland and Parsons, 1972]. Some samples were reanalyzed at Princeton Univer sity by reduction of NO 3 (and NO2 ) to NO using a V(III) reagent followed by measurement of NO by chemiluminescence [Braman and Hendrix, 1989]. NO 2 was always scarce and is subsequently disregarded. The 15N/14N of nitrate was analyzed by the ‘‘denitrifier method’’ [Casciotti et al., 2002; Sigman et al., 2001]. Briefly, 10 or 20 nmol nitrate is quantitatively reduced to N2O by a strain of bacteria that lacks an active N2O reductase, and the product N2O is analyzed by continuous flow isotope ratio mass spectrometry. Referencing to the 15N/14N of N2 in air was through parallel measurement of the potassium nitrate reference material IAEA-N3, with a d15 N of +4.7%
Figure 2. Density characteristics of the study region. (a) Underway potential density versus latitude for cruises used in this study. Winter cruises (solid markers) tended to be 103 kg m3 (1 unit s) more dense. Density was calculated from temperature and salinity determined from shipboard thermosalinometer instruments (depth 7 m) (Mark Rosenberg, personal communication, 2004). Underway temperature and salinity data for R/V Auroura Australis cruises are from AADC. Underway temperature and salinity data for R/V Southern Surveyor were processed by CSIRO. (b) Depth profiles of potential density for summer cruise AU9706 (open circles) and winter cruise AU9701 (solid circles). The region attributed to the formation of SAMW is visible at s = 26.8. (c) Mixed layer depth climatology for SAZ (average for 138– 142E and 42 – 50S) from the model of Kara et al. [2003] plotted by month. Cruises are labeled according to date. The area is characterized by deep winter mixed layers in excess of 400 m that shoal to 3% higher than in the underlying thermocline, even though nitrate concentrations are rarely 30% lower than in the thermocline. This observation in itself could be explained in two ways: (1) equatorward nitrate transport across the SAZ, including nitrate input from the Antarctic and Polar Frontal Zones to the south, and/or (2) a large isotope effect for nitrate assimilation in the SAZ. Sigman et al. [1999a] noted 15N enrichment in SAZ surface nitrate even where [NO 3 ] was the same or higher than in the subsurface, pointing toward the former explanation. [51] The summertime nitrate isotope data reported here show the same indications of equatorward nitrate transport as noted previously. However, the wintertime data, which are the first of their kind, indicate that the 15N enrichment of SAZ nitrate observed during the summer is generated each summer starting from near-thermocline values. Over this short time period, it is impossible for enough AZ/PFZ nitrate to be transported into the SAZ surface layer to replace the wintertime surface nitrate pool across the entire latitude range of the SAZ, a point that is quantified here with salinity, which should provide an indication of the amount of water coming into the SAZ from the south. Thus, to explain the amplitude of the winter-to-summer increase in the d15N of nitrate requires a higher isotope effect than estimated by Sigman et al. [1999a]. At the same time, the comparison of the change in the d15N of nitrate with the d15N of sediment trap material for this region of the SAZ constrains how large that isotope effect can be, in this way maintaining the need for AZ/PFZ-sourced nitrate in the summertime SAZ. [52] The data and our numerical simulation of them yield several important conclusions regarding the SAZ south of Australia. First, following the shoaling of the SAZ mixed layer in spring, the supply of Antarctic nutrients across the PFZ accounts for 15% or more of nitrate assimilation and N export during the spring and summer blooms and 30% or more of the nitrate resident in the mixed layer by midsummer. Second, export production must be adequately high to produce the observed summertime nitrate drawdown in the face of a significant nitrate input from the AZ/PFZ through the warm season, which leads to higher N export than if this input were ignored (Table 6). Third, the isotope balance in our model suggests that the previous estimates of the isotope effect in the SAZ are too low, and we estimate an epsilon of 8 – 9%. [53] Without the N isotope constraints, our model simulation of the seasonal changes in salinity and nitrate concentration is in essence similar to the study of Lourey and Trull [2001], who estimated summertime nitrate assimilation from the winter-to-spring decrease in surface [NO 3 ], using the summertime decrease in SAZ surface salinity to correct for the amount of nitrate imported from the AZ/PFZ. Because our model is fit to match these two parameters perfectly, our estimate of summertime SAZ nitrate assimilation is similar to theirs (Table 6).
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[54] The unique aspect of this study is our use of the N isotope data to test this approach. While the d15N of nitrate data can be fit simply by adjusting the assumed isotope effect for nitrate assimilation, comparison of these data with a sediment trap – based estimate of sinking N d15N puts a constraint on the isotope effect, precluding arbitrarily high values for it. We did not carry out a model simulation that addressed this overconstrained system by trying to simultaneously fit all parameters. Instead, it proved most transparent to simply allow the model to fit the salinity, [NO 3 ], and d15N of nitrate data perfectly and then compare the predicted sinking flux d15N with the sediment trap observations, determining whether the fit to the sediment trap d15N data was good and in which direction any misfit to the data tended to be. [55] While the model simulation predicted a sinking N d15N that was arguably within 1% of the sediment trap constraint, the sense of misfit was clearly for the model to underestimate sinking N d15N. Far from being a detail or uncertainty, the observed sense of model misfit is a key warning that AZ/PFZ nitrate transport into the SAZ and nitrate assimilation within the SAZ may be underestimated by the approach of using seasonal nitrate concentration data and assuming that salinity is a conservative tracer of AZ water inputs to the SAZ. Two end-member alternative interpretations of the misfit are that: (1) salinity is not acting in a completely conservative manner, and there is somewhat more AZ/PFZ nitrate entering the summertime SAZ than we and Lourey and Trull [2001] allow, or (2) the sediment trap d15N is 1 – 2% higher than the true N export out of the surface ocean, so that the true isotope effect for nitrate assimilation can be somewhat greater than we accept on the basis of our data/model comparison for sinking flux d15N. [56] Coupled with recent progress in laboratory studies of the nitrate assimilation isotope effect, this study raises this isotope effect as a possible environmental tool to study the physiological state of phytoplankton in modern aquatic environments. That our estimate for the isotope effect in the SAZ is 2 – 3% higher than our estimates from the marginal ice zone of Antarctica [Sigman et al., 1999a; P. DiFiore et al., manuscript in preparation, 2006] suggests some difference in the constraints on algal growth between these two Southern Ocean environments. Given the available culture data and the characteristics of the SAZ, a role for light limitation in the SAZ is a natural hypothesis for our observations. Along with continued use of algal cultures to explore the mechanism of nitrate isotope discrimination, studies in the Southern Ocean that couple the isotope effect estimates extracted from regional tracer distributions (i.e., the approach taken here) with shipboard-board growth experiments should help to test this explanation and, more generally, illuminate the environmental controls on (and the physiological significance of) the isotope effect of nitrate assimilation. [57] A fundamental goal of this study was to develop an understanding of the constraints on subantarctic circulation and biogeochemistry that can be extracted from the coupling of N isotope measurements with standard oceanographic measurements. Beyond the proof of concept that we believe was achieved, there are key lessons for the future. In particular, if the N isotope budgetary approach is to be
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pursued further, the uncertainties on the d15N of exported N should be reduced. This includes not only improving our ability to measure the particulates sinking out of the surface ocean but also accounting for the N exported laterally, such as dissolved organic N. [58] Acknowledgments. Sample collection was supported by the Australian Commonwealth Cooperative Research Centre Program and Australian Antarctic Science Award 1156 (T.W.T.). This work was funded by U.S. NSF grant OCE – 0081686 (to D.M.S.) and by BP and Ford Motor Company through the Princeton Carbon Mitigation Initiative. We thank Michael Bender and Matt Reuer for discussions. This manuscript benefited from reviews by Niki Gruber and an anonymous reviewer.
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G. Cane, P. J. DiFiore, R. Ho, K. Karsh, and D. M. Sigman, Department of Geosciences, Princeton University, Guyot Hall, Princeton, NJ 08544, USA. (
[email protected]) M. J. Lourey, CSIRO Marine and Atmospheric Research, Private Bag 5, Wembley, WA 6913, Australia. T. W. Trull, Antarctic Climate and Ecosystem Cooperative Research Centre, CSIRO Marine and Atmospheric Research, Hobart, TAS 7001, Australia.
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