Article Cite This: Environ. Sci. Technol. 2019, 53, 6869−6876
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Potential of Nitrogen/Argon Analysis in Surface Waters in the Examination of Areal Nitrogen Deficits Caused by Nitrogen Fixation Oliver Schmale,* Mattis Karle, Michael Glockzin, and Bernd Schneider
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Leibniz Institute of Baltic Sea Research (IOW), Seestrasse 15, Rostock D-18119, Germany ABSTRACT: In marine systems, the loss of nitrogen caused by denitrification in oxygendeficient zones is balanced by nitrogen fixation mediated by cyanobacteria, which may form extensive blooms in surface waters. In this study, by determining the concentration ratio of nitrogen (N2) and argon (Ar) in air equilibrated with surface water, we were able to detect changes in the N2 concentration attributable to N2 fixation. For this purpose, surface water was pumped continuously into a spray-type equilibrator while the air in the equilibrator’s headspace was analyzed by mass spectrometry. After laboratory tests and model analysis to evaluate the sensitivity of our N2/Ar approach, feasibility studies were conducted in the central Baltic Sea in the summer of 2015 during the development of a cyanobacterial bloom. Our results showed that N2 deficits accumulated during periods of low wind and increasing surface water temperatures. A comparison of our results with the N2 deficits calculated from changes in the partial pressure of carbon dioxide in surface water indicated a similar trend. By demonstrating the ability of the N2/Ar approach to resolve N2 deficits in surface water caused by N2 fixation, our study contributes to assessments of the N2 fixation efficiency of cyanobacterial blooms.
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INTRODUCTION The concentrations of dissolved gases in seawater are controlled by physical and biological processes. The physical processes include temperature-, salinity-, and wind-driven gas exchange with the atmosphere, bubble injection, and the interaction between different water bodies through mixing. In marine biogeochemistry, the inert character of argon (Ar) is used to separate these physical effects from the biological activities that affect gas concentrations. Because oxygen (O2) and Ar have similar physicochemical properties, dissolved O2/ Ar ratios can be employed to estimate net community production and to resolve regional phenomena in the surface water linked to photosynthesis and respiration.1,2 Biological processes involved in the marine nitrogen cycle and associated with changes in the concentration of molecular nitrogen (N2) include denitrification, ammonium oxidation (anammox reaction), and N2 fixation.3 Analogous to oxygen-related processes, the molecular nitrogen (N2) excess resulting from water column denitrification and the anammox reaction in oxygen-deficient zones was estimated by measuring N2/Ar ratios.4,5 In the ocean, the loss of dissolved inorganic nitrogen (DIN) compounds due to denitrification and anammox reactions is mainly balanced by N2 fixation, i.e., the conversion of molecular into organic nitrogen, in reactions carried out by diazotrophic organisms. Most of the N2 fixation in the central Baltic Sea and Gulf of Finland can be attributed to the cyanobacteria Nodularia spumigena, Aphanizomenon spec., and Dolichospermum spec.,6 which form annually recurring blooms from July to the beginning of August. There is general concern that eutrophication and climate change will favor the proliferation of these harmful blooms.7 Consequently, an understanding of their development is essential for the © 2019 American Chemical Society
ecological management of the Baltic Sea and other coastal areas. Among the methods used to estimate the contribution of N2 fixation, and therefore the activity of bloom-forming cyanobacteria, to the nitrogen (DIN) budget of the Baltic Sea are (i) the incubation of discrete water samples with 15Nlabeled molecular nitrogen to obtain instantaneous fixation rates,6,8 (ii) the establishment of basin-wide mass balances for total nitrogen,9,10 and (iii) the deployment of measuring devices on voluntary observing ships (VOS) to obtain highresolution data on the carbon dioxide partial pressure (pCO2) in surface water, thus enabling determinations of net community production and estimates of the nitrogen demand.11,12 In this study, we demonstrate that the small changes in the N2 concentration arising from N2 fixation can be detected by a novel method based on mass spectroscopy of the N2/Ar ratio in air equilibrated with surface water. To this end, a continuous-mode equilibrator system coupled to a mass spectrometer (Equi-MS) was developed, and its performance was optimized and evaluated in laboratory experiments. Then, using a simple physicochemical model, we assessed the potential and limitations of the N2/Ar approach for studies of the biogeochemical processes that decrease or increase the N2 concentration. Finally, the feasibility of our N2/Ar approach in the detection of N2 deficits in surface water caused by N2 fixation was tested in a field study in the central Baltic Sea. The results were compared with those of an established approach for the quantification of N2 fixation capacities. Received: Revised: Accepted: Published: 6869
November 26, 2018 May 17, 2019 May 22, 2019 May 22, 2019 DOI: 10.1021/acs.est.8b06665 Environ. Sci. Technol. 2019, 53, 6869−6876
Article
Environmental Science & Technology
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MATERIALS AND METHODS Fundamentals and Limitations of the N2/Ar Method. The N2/Ar method was applied to estimate N2 fixation by measuring the surface water concentration of N2. As noted above, this same method is used to estimate the N2 excess caused by denitrification (e.g., ref 4). Given the similar physicochemical properties of N2 and Ar, the N2/Ar concentration ratios in seawater correspond within narrow limits to saturation with atmospheric N2 and Ar (denoted as (N2/Ar)sat) at the respective temperature and salinity as long as no N2 transformations occur.13 Hence, any biogeochemically induced changes in the N2 (ΔN2) concentration will be reflected in a shift of the N2/Ar ratio and can be determined by multiplying the difference in the N2/Ar ratio by the Ar concentration,14 as shown in eq 1: jii N y i N y yz ΔN2 = jjjjjj 2 zzz − jjj 2 zzz zzzAr jk Ar { k Ar { z sat { k
than N2 gas exchange because Ar has a higher diffusivity (lower Schmidt number). To estimate possible deviations between the N2/Ar ratios of the “real” abiotic concentrations and those of (N2/Ar)sat, N2/ Ar ratios were simulated by a simple model that takes into account different scenarios in the Baltic Sea. A sinus-shaped SST seasonality (0−20 °C) of the water column with a defined mixed layer depth (zmix) was considered. The initial concentrations of N2 and Ar at the start of the calculations were set to saturation values. SST was then changed at time (t) steps of 1 day, and the difference between the “new” csat t+1 and the previous ct was used to calculate the exchange with the atmosphere (F) of either N2 or Ar for each time step, as shown in eqs 2 and 3: i Sc yz zz F = k660jjj k 660 {
−0.5
(ct − ctsat + 1)
(2)
with
(1)
k660 = 0.24u 2
where the element symbols represent the concentrations of those elements. However, the use of (N2/Ar)sat as a nonbiotic reference for the actual measured N2/Ar ratio is an approximation and may be associated with considerable uncertainties if the N 2 concentration is expected to change by only a few percent, as in the case of N2 fixation. One reason for these problems is due to the seasonality of the surface water temperature in combination with the different temperature coefficients of the solubility constants for N2 and Ar. The solubility of N2 and Ar decreases by 1.99% and 2.16% per Kelvin, respectively.15 Consequently, (N2/Ar)sat values run through a minimum/ maximum corresponding to the seasonality of the sea surface temperature (SST, Figure 1). However, the seasonality of the real N2/Ar ratio lags behind that of (N2/Ar)sat because gas exchange and re-equilibration with atmospheric N2 and Ar do not occur spontaneously but are delayed with respect to the temperature change. Furthermore, Ar gas exchange is faster
(3)
where k660 is the gas exchange transfer velocity at a Schmidt number of 660 [cm h−1], Sc is the Schmidt number, which is reciprocally proportional to the diffusivity of the considered gas in seawater, and u is the wind speed [m s−1].16,17 Dividing the flux (F) by the mixed layer depth yields the changes in N2 and Ar concentrations in units of mmol m−3 from t to t + 1. For the determination of csat, we first calculated the solubility constant as a function of temperature and salinity,15 which was then multiplied with the atmospheric partial pressures of the respective gases. For the calculation of the latter, we used standard atmospheric pressure as well as the N2 and Ar mole fractions in dry air and assumed water vapor saturation at the sea−air interface. N2/Ar seasonality was simulated for a scenario in which conditions favor midsummer production fueled by N2 fixation: low wind speed (u = 4 m s−1), a shallow surface mixed layer (zmix = 5 m), and a temperature maximum by the end of July of 20 °C. Three seasonal cycles were simulated for a spin-up of the model calculations. Deviations from a steady state were already negligible after the second cycle. The seasonality of (N2/Ar)sat (Figure 1, red curve) showed minimum and maximum values of 36.9 and 38.1, respectively, coinciding with the minimum and maximum surface water temperature. In contrast, both the amplitude and the phase of the simulated “real” N2/Ar ((N2/ Ar)real; Figure 1, green curve) were slightly different. The difference (N2/Ar)real − (N2/Ar)sat corresponds to a bias in the calculated ΔN2 (δ(ΔN2), Figure 1, black curve). The asymmetric annual cycle of δ(ΔN2 ) was due to the superposition of the two effects: different temperature coefficients of the solubility constants and different transfer velocities (Schmidt numbers) for N2 and Ar. Positive δ(ΔN2), which cause an underestimate of ΔN2, was the largest during spring when the temperature increase was the strongest. For the period from mid-June to mid-August when cyanobacteria blooms are common in the central Baltic, δ(ΔN2) ranged between 0.2 and 1.1 μmol L−1. The simulations presented in Figure 1 for a whole year were based on a midsummer scenario regarding zmix and u. Nonetheless, the results for a typical winter scenario, i.e.,
Figure 1. Simulation of the N2/Ar ratios for a sinus-shaped seasonality of temperature: Spontaneous equilibration by gas exchange (red line) and delayed equilibration due to slow gas exchange (green line). The difference between the N2/Ar ratios at equilibrium (N2/Ar, saturation) and under simulated real conditions (N2/Ar, real) corresponds to a bias of the calculated ΔN2 (δ(ΔN2), black line) for the performed scenario (Tmax = 20 °C, zmix = 5 m, u = 4 m s−1). The blue dots in the third period of the simulations indicate the start (15.6) and termination (15.8) of the time period when the bloom of cyanobacteria (i.e., nitrogen fixation) is most common in the Baltic Sea. 6870
DOI: 10.1021/acs.est.8b06665 Environ. Sci. Technol. 2019, 53, 6869−6876
Article
Environmental Science & Technology higher wind speed and deeper mixing, showed a similar pattern for δ(ΔN2) but with somewhat larger amplitudes. Our exemplary and simplified simulations of the influence of seasonal surface water temperature variations on the N2/Ar ratios provided a sensitivity test of the N2/Ar method. The results are not intended for practical use; rather, they indicate the possibility of errors in the determination of N 2 concentration changes caused by biogeochemical processes such as N2 fixation and denitrification. In reality, the wind speed and mixed layer depth are subject to short-term fluctuations, and the seasonality of the surface water temperature is not a continuous function of time but frequently pulselike. To account for such conditions, repeated measurements on the basis of a few days may provide a realistic N2/Ar reference ratio for the start of the N2 fixation by cyanobacteria. This could be facilitated by the deployment of an automated equi-MS system on a VOS line (see section “Comparison with the pCO2 Approach”). Our simulations did not account for the impact of air bubble injection on the determination of ΔN2. Previous studies have demonstrated that the injection of air bubbles may generate a significant surface water N2 and Ar disequilibrium that, depending on the bubble size, may also affect the N2/Ar ratio (e.g., refs 18 and 19). Small bubbles (bubble diameter of
