Control of the Hydraulic Load on Nitrous Oxide Emissions fromCascade ReservoirsXia Liang,*,†,‡ Tao Xing,‡ Junxiong Li,‡ Baoli Wang,*,§ Fushun Wang,‡ Chiquan He,‡ Lijun Hou,†

and Siliang Li§

†State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai 200244, China‡School of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, China§Institute of Surface-Earth System Science, Tianjin University, Tianjin 300072, China

*S Supporting Information

ABSTRACT: Nitrous oxide (N2O) emissions show large variability among damreservoirs, which makes it difficult to estimate N2O contributions to globalgreenhouse gases (GHGs). Because river damming alters hydraulic residence timeand water depth, the hydraulic load (i.e., the ratio of the mean water depth to theresidence time) was hypothesized to control N2O emissions from dam reservoirs.To test this hypothesis, we investigated N2O fluxes and related parameters in thecascade reservoirs along the Wujiang River in Southwest China. The N2O fluxesshowed obvious temporal and spatial variations, ranging from −7.86 to 337.22μmol m−2 d−1, with an average of 12.76 μmol m−2 d−1. Nitrification was the mainpathway of N2O production in these reservoirs, and seasonal dissolved oxygen(DO) stratification played an important role in regulating the N2O production.The reservoir N2O flux had a significant negative logarithmic relationship with thehydraulic load, suggesting its control of the N2O emission. This was because thehydraulic load was a prerequisite for regulating the nitrification−denitrification and the DO stratification in the dam reservoirs.This empirical relationship will help to estimate the contribution of reservoir N2O emissions to global GHGs.

■ INTRODUCTION

Nitrous oxide (N2O) is one of the important trace greenhousegases (GHGs), and has gained much attention due to itssignificant contribution to global warming.1−4 Based on a recentestimation, the global biogenicN2O emission is more than 12 TgN yr−1 and the atmospheric N2O concentration shows a fastincrease with time.1,2 In recent decades, due to the rapiddevelopment of global hydropower construction, reservoirs asan important source of GHGs to the atmosphere have receivedmuch attention.5,6 Recent estimations indicate that reservoirN2O fluxes range from−2.02 to 131.09 μmol m−2 d−1, and N2Oevasion ranges from 0.03 to 0.07 Tg N yr−1.7,8 Nevertheless,N2O emissions from reservoirs have still received much lessattention. The lack of systematic data and a clear understandingof the control mechanism of N2O production make it difficult toaccurately estimate the N2O emissions from dam reservoirs andevaluate the importance of reservoirs in the global N2O budget.In general, N2O production is biologically driven by

nitrification and denitrification.9−11 N2O can also be formedthrough abiotic reactions under the condition of high hydroxyl-amine (NH2OH) and nitrite (NO2

−) concentrations.12,13 SinceNH2OH and NO2

− concentrations are very low in freshwatersystems, the contribution of an abiotic reaction to the N2Oproduction would be small. N2O production by nitrification anddenitrification is governed by a variety of hydrological,geochemical, and biological factors. First, dissolved inorganic

nitrogen (DIN) (e.g., NO3− and NH4

+) as the reactive Nsubstrate has shown a strong effect on N2O production.14

Second, organic carbon acts as an electron donor in thedenitrification process and also supports the growth ofdenitrifying bacteria and fungi.15,16 Thirdly, dissolved oxygen(DO) can regulate organic carbon and nitrogen (N) utilizationduring nitrification and denitrification, and ensure thecompletion of the two processes.17 Furthermore, the waterresidence time could govern the N processing time that isstrongly related to N2O production in reservoirs.5,8,18 Deepreservoirs in which the lacustrine zone has a long retention timeusually develop thermal stratification seasonally.19,20 Theperiodical stratification could create barriers to the nutrientand DO exchange between the epilimnion and the hypolimn-ion,5,21 resulting in a change of the main pathways of N2Oproduction in the water profile and accumulation of N2O in thehypoxic hypolimnion.22,23 The hydraulic load, derived from thequotient between the mean depth and the water residence time,has been reported in a global model of lentic N removal in lakesand reservoirs.24 However, comparatively little work has beendone to understand the effect of the hydraulic load on the N

Received: June 9, 2019Revised: September 7, 2019Accepted: September 17, 2019Published: September 17, 2019

Article

pubs.acs.org/estCite This: Environ. Sci. Technol. 2019, 53, 11745−11754

© 2019 American Chemical Society 11745 DOI: 10.1021/acs.est.9b03438Environ. Sci. Technol. 2019, 53, 11745−11754

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biogeochemical cycling in freshwater systems. Because river

damming substantially alters water depths and retention times,

we hypothesized that N2O emission from cascade reservoirs

would be controlled by the hydraulic load.The Wujiang River, located in southwest China, is an ideal

place to test this hypothesis since a series of reservoirs along this

river have been built with different hydraulic residence times and

mean water depths (Table 1). Therefore, we investigated the

N2O concentration, N2O fluxes, and related environmental

factors in the impounded Wujiang River to understand the

hydraulic control mechanism of the N2O emissions from the

cascade reservoirs. This study could be of great significance for

estimating the contribution of N2O emissions from dam

reservoirs at regional or global scales.

■ MATERIALS AND METHODS

Site Description and Sample Collection. The WujiangRiver (26°07′−30°22′N, 104°18′−109°22′E) is the largestsouthern tributary of the Yangtze River, and it mainly flowsthrough a karst area in Guizhou Province, Southwest China(Figure 1). The river has a length of 1037 km, with a fall of 2124m, and it takes drainage from an 8.03 × 104 km2 watershed. TheWujiang River Basin is subject to a subtropical monsoon humidclimate, and more than 80% of the annual runoff occurs in thesummer (May to September). The multiyear average annualrainfall and the temperature in the basin are about 1100 mm and14.8 °C, respectively. As the major power source for China’smassive West-to-East Power Transmission Project, a series ofhydroelectric reservoirs have been constructed along theWujiang River over the past five decades.25 In this study, eightcascade hydroelectric reservoirs along the Wujiang River werechosen, among which seven reservoirs were located at the

Table 1. Hydromorphological Characteristics of the Studied Reservoirs

reservoirselevation(m)

catchmentarea (km2)

averagedepth(m)

normal/deadwater level

(m)discharge(108 m3)

operationtime (yr)

waterretentiontime (d)

type ofregulation

type ofreservoirsa

drainagebasin

stratifiedstatus

HJD 1093 9900 61.18 1140/1076 155 39 368 pluriennial storage mainstream seasonalDF 965 18 161 45.28 970/936 345 24 29 seasonal storage mainstream seasonalSFY 850 21 862 42.43 835/813 427 16 4 daily run-of-river mainstream seasonalWJD 760 27 790 44.77 760/720 502 14 49 seasonal storage mainstream seasonalSL 457 48 558 31.42 440/431 844 11 17 seasonal run-of-river mainstream seasonalPS 336 69 000 81.05 293/278 1300 11 11 seasonal run-of-river mainstream noneYP 285 74 910 16.05 215/211.5 1390 10 1 daily run-of-river mainstream noneHF 1230 1596 13.16 1240/1227.5 29 60 300 incomplete

annualstorage Maotiao river seasonal

aThe reservoirs were classified according to their size and their designed purpose.5

Figure 1. Sampling locations and sites in the Wujiang River watershed. HJD, Hongjiadu reservoir; DF, Dongfeng reservoir; SFY, Suofengyingreservoir;WJD,Wujiangdu reservoir; SL, Siling reservoir; PS, Pengshui reservoir; YP, Yingpan reservoir; HF, Hongfeng reservoir. Among the samplingsites, the capital letters “W” and “T” indicate sites located at the Wujiang River mainstream and its tributaries, while “M” and “B” indicate sites at themainstream and the tributaries of the Maotiao River.

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mainstream and one (Hongfeng reservoir, HF) was located atthe major tributary (Maotiao River). In the river’s mainstream,the reservoirs of Hongjiadu (HJD), Dongfeng (DF), Suofengy-ing (SFY), and Wujiangdu (WJD) were located in the upstreamand midstream reaches, while the reservoirs of Siling (SL),Pengshui (PS), and Yingpan (YP) were located in thedownstream reaches (Figure 1). The eight reservoirs wereconstructed between 1958 and 2008, and all of them were usedfor hydroelectric power with bottom discharge. These reservoirsexhibit various hydrographic characteristics due to their differentgeomorphic forms and dam designs (Table 1). TheHF reservoirhas the longest residence time and operation times, and its majorfunction changed from hydropower to drinking water supply in2000. The HF, WJD, and SL reservoirs have all experiencedeutrophication due to the cage culture and dumping ofagricultural waste. More information about the reservoirs,including the operation plans and catalogs, is described inTable 1.Seasonal sampling was performed during 2017: winter

(January), spring (April), summer (June, July, and August),and autumn (October). In total, 44 sites were surveyed withinthe inflowing, reservoir, and released waters of the eightreservoirs (Figure 1). Surface water (upper 0.5 m) was collectedfrom all the sampling sites and the water profiles wereinvestigated at the reservoirs. Water sampling in the verticalprofiles was different among the reservoirs. The stratifiedsampling was conducted at depths of 0, 15, 30, 45, and 60 m atthe sampling sites of W2−W5 (HJD reservoir), W8−W10 (DFreservoir), W12 (SFY reservoir), W17 (WJD reservoir), W20−W21 (SL reservoir), and W24−W25 (PS reservoir). Stratifiedsampling was also conducted at depths of 0, 5, 10, 15, and 25 min the sampling sites of M2−M4 (HF reservoir) andW14−W16(WJD reservoir), and at depths of 0, 5, 10, 15, 30, and 45m in thesampling site of W28 (YP reservoir), respectively. The watertemperature, pH, DO, and chlorophyll were measured in situwith a calibrated automated multiparameter profiler (model:YSI 6600; YSI Inc., Yellow Springs, OH). The thermalstratification of each reservoir and the corresponding depthswere then determined according to the vertical temperatureprofile and the empirical models developed by Zhang et al.26

Triplicate water samples were collected for the DIN and gasanalyses. The water samples for the dissolved N2O analyses weresampled in 70 mL headspace bottles and preserved by addingsaturated HgCl2. The sampling bottles were then immediatelyclosed without headspace and hermetically sealed in the field.The water samples for the N2 analyses were sampled in 500 mLpolyethylene bottles, sealed, and stored at 4 °C. The DINmeasurements were filtered through 0.45 μm cellulose acetatemembranes (Millipore Corporation) within 12 h, stored in 100mL polyethylene bottles, and kept in the dark at 4 °C until theanalysis.Sample Analysis. The dissolved N2O concentrations were

determined in triplicate following the modified headspace-equilibrium method.27 In brief, 20 mL of highly purified N2 wasinjected into the headspace bottles and 20 mL of water wasdisplaced. The bottles were then shaken with an ultrasonicshaker for 30 min at 20 °C and equilibrated overnight. The N2Oconcentration in the headspace was analyzed using a gaschromatograph equipped with an electron capture detector(HP6890) and a 4.5 m × 3 mm packed Porapak Q (80/100mesh) column. The column and the ECD detector wereconditioned at 50 and 320 °C, respectively. The dissolved N2was determined following the method described by Yan et al.

and Chen et al.28,29 using a Membrane Inlet Mass Spectrometry(MIMS) system (HPR40, Hiden Analytical, UK) and measuredwith the N2:Ar method. The dissolved N2O concentrations werecalculated using the equation described by Wang et al. and Yu etal.27,30

β=

× + × ×C

C V C VVw

AI AI AI w

w (1)

where Cw is the measured N2O concentration (μmol L−1), CAI isthe concentration of N2O in the headspace during equilibration(μmol L−1),VAI andVw are the volumes of the headspace and thewater phase in the sampling bottle (L), and β is the Bunsensolubility coefficient of N2O.The flux of N2O was calculated using the equation described

by Liss et al. (1974)31

= −F k C C( )w A (2)

where F is the flux of N2O (μmol m−2 h−1), Cw is the measuredN2O concentration (μmol L−1), CA is the N2O concentration ofthe ambient air sample, and k is the gas-exchange coefficient (cmh−1).The gas-exchange coefficient took the wind speed and the

temperature into account and was calculated according to thefollowing equation:

=−i

kjjj

y{zzzk k

S600

x

600c

(3)

where x = 0.66 and 0.5 for wind speeds ≤3 and >3 m s−1,respectively, Sc is the Schmidt number for N2O and is dependenton the temperature (in °C), and k600 is the gas-exchangecoefficient expressed in cm h−1, normalized for N2O at 20 °C infreshwater with a Schmidt number of 600.The Sc and k600 were estimated by the following

equations:32,33

= − + −S t t t2055.6 137.11 4.3173 0.054350c2 3

(4)

= + ×k U1.68 (0.228 )600 102.2

(5)

where t is the temperature (°C) and U10 is the frictionless windspeed at 10 m expressed in m s−1. U10 is calculated based on therelationshipU10 = 1.22U1, whereU1 is the wind speed at a heightof 1 m (in m s−1) and was measured in situ in this study.The N2O emissions (in ton N2O-N yr−1) from the reservoirs

were calculated by the multiplication of the average emissionflux by the area covered by the reservoirs.34 The surface waterarea was calculated based on the GDEMDEM 30-M resolutiondigital elevation data and the normal water levels of thereservoirs. The concentrations of NH4

+ and NO2− in water

samples were determined using Nessler’s reagent and N-(1-naphthyl) ethylenediamine dihydrochloride spectrophotome-try, respectively, and the NO3

− concentrations were measuredusing ultraviolet spectrophotometry.35

The hydraulic load (Hl, m d−1) was calculated with thefollowing equation:36

= DT

Hl (6)

where D refers to the mean water depth of the reservoir (in m)and T is the water residence time of the reservoirs (in days).

Data Collection. Given the controlling of the hydrologicalfactors for N2O emissions that was observed in this study, arealdata from more than 200 global reservoirs were collected to

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further evaluate the relationship between the N2O flux andhydrological variables. Among the areal data, 13 reservoirs withN2O and hydrological data (i.e., the hydraulic residence timeand the mean water depth) that met the methodological criteriain our analyses were then further evaluated (Table S1).Statistical Analyses. The statistically significant differences

between different study sites were analyzed using one-wayanalysis of variance (ANOVA), least significant difference(LSD), and Duncan calculation at the 0.05 significance level.Pearson’s correlations were used to analyze the correlationbetween the N2O concentration and each environmentalparameter. A t-test approach was used to compare the linearregression slopes. Stepwise forward multiple regression was thenused to estimate the effect of the environmental variables on theN2O concentration, and only the variables that were significantlycorrelated with the N2O concentration were included based onthe t-test. Other assumptions that needed to meet thespecification of the multiple regression analysis, such as themulticollinearity or homogeneity of the error terms, werechecked. All of the statistical analyses were performed using theSPSS 19.0 statistical software package (SPSS Inc.).

■ RESULTSWater Temperature and Dissolved Oxygen. The water

temperature (WT) and dissolved oxygen (DO) were studied astwo important basic parameters. The WT ranged from 8.22 to31.17 °C, with an average of 18.71 °C, and the DOconcentration was in the range of 0.10−27.01 mg L−1, with anaverage of 3.73 mg L−1. The WT in the Wujiang River showedno significant variation among the reservoirs, and the reservoirWT varied seasonally, with the highest values recorded in thesummer and the lowest values recorded in the winter (Table 2and Figure 2). As a response, the change in the DOconcentration exhibited greater amplitude in the summer thanin the winter. Moreover, the variation of the DO concentrationin the water profile was different among the reservoirs (Figure3). The seasonal thermal and DO stratifications were obvious inthe HF, HJD, DF, WJD, and SL reservoirs with long residencetime, and were weak in the SFY reservoir and completely absentin the PS and YP reservoirs with a short residence time (Table1). For example, the DO concentration in the HF reservoirdecreased from 9.96mg L−1 of the water surface to less than 0.20mg L−1 at a 25 m depth during the summer stratification, whilethat in the YP reservoir was almost zero.Nitrate and Ammonium. The concentration of NO3

−

ranged from 0.35 to 136.22 μmol L−1, with an average of

40.42 μmol L−1, which was almost eight times higher than theNH4

+ concentration (5.53 μmol L−1) in the studied area (Table2). Although there were no significant spatial differences for theNO3

− and NH4+ concentrations between the inflowing,

reservoir, and released waters, significantly low and highconcentrations of NO3

− were observed in the HF (13.18 μmolL−1, P < 0.05) and HJD reservoirs (50.31 μmol L−1, P < 0.05),when compared to the other reservoirs (Table S2). Moreover,obvious NO3

− stratification was exhibited at water depths of 20m in the HJD reservoir (Figure 4).

Nitrous Oxide. The dissolved N2O concentration in theWujiang River ranged from 3.98 to 477.16 nmol L−1, with anaverage of 28.57 nmol L−1 (Table 2). N2O concentrations in thesurface water showed remarkable spatial variations. Thetributaries exhibited significantly higher N2O concentrationsthan the inflowing water, while the released waters showedsignificantly higher N2O concentrations than the reservoirs(two-ANOVA, P < 0.05; Figure 5). The HF reservoir had thehighest N2O concentration (51.76 nmol L−1) in the surfacewater, nearly more than 2.5 times higher than that of the others.Moreover, the average N2O concentration in the released waterof the HF reservoir was 61.50 nmol L−1, which was 2.21 and 1.19times higher than that from the inflowing and reservoir surfacewater, respectively. However, in the SFY, SL, and YP reservoirs,the N2O concentrations in the released water showed nosignificant difference or a slight decrease compared with thereservoir surface water (Figure 5). Additionally, there wasobvious summer N2O stratification in the reservoirs, whichcovaried with the DO stratification in the water profile (Figures

Table 2.Water Chemical Parameters, Gaseous Nitrogen Concentrations, andN2O Fluxes in the Reservoirs of theWujiang Rivera

inflowing + tributary reservoir released water

parameters value n value n value n

WT (°C) 19.40 ± 0.48 (2.16, 29.63) 95 18.50 ± 0.17 (0.98, 31.17) 629 18.33 ± 0.43 (10.73, 23.12) 47DO (mg L−1) 7.87 ± 0.20 (1.63, 13.92) 96 7.18 ± 0.11 (0.10, 27.01) 632 8.08 ± 0.26 (1.55, 13.21) 47Chl (μg L−1) 3.20 ± 0.56b (0.01, 32.10) 96 3.94 ± 0.28b (0.02, 54.27) 479 1.26 ± 0.21a (0.01, 7.78) 47pH 7.82 ± 0.03 (7.00, 8.79) 94 7.79 ± 0.01 (7.14, 9.30) 622 7.70 ± 0.04 (7.26, 8.55) 47NO3

− (μmol L−1) 40.24± 2.40 (0.96, 136.22) 89 40.21± 0.79 (0.35, 88.26) 561 43.26 ± 2.74 (11.43, 83.25) 46NH4

+ (μmol L−1) 9.41± 2.63 (0.85, 214.20) 88 4.75 ± 0.18 (0.28, 36.40) 549 7.42 ± 2.27 (1.35, 101.88) 44N2O (nmol L−1) 33.47 ± 4.79 (6.17, 380.60) 94 27.00 ± 1.36 (3.98, 477.16) 589 33.13 ± 4.11 (5.83, 172.74) 47N2 (mmol L−1) 0.58 ± 0.01 (0.42, 0.77) 93 0.59 ± 0.003 (0.42, 0.74) 582 0.59 ± 0.01 (0.52, 0.73) 44FN2O (μmol m−2 d−1) 12.35 ± 2.50 (−7.86, 131.32) 95 7.73 ± 1.29 (−5.33, 72.97) 113 18.24 ± 7.28 (−1.50, 337.22) 47

aThe data are presented as the mean ± standard error; n is the number of measurements and the minimum and maximum values of themeasurements are given within parentheses. Significant differences between the reservoirs are indicated by different lowercase letters (P < 0.05).Inflowing: the water that was from the stations in the reservoir sections that directly received river inflows.37

Figure 2. Temporal variation of water temperature (blue line) anddissolved oxygen (red line) in the reservoirs along the Wujiang River.The data are presented as mean ± standard error. The light yellowshaded section represents the summer periods of the studied sites.

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Figure 3.Variations in the water temperature and the dissolved oxygen in the water profile ahead of the dam of each reservoir along theWujiang River.The light yellow shaded section shows the thermocline layer of each reservoir in summer. The name abbreviations of each reservoir refer to Figure 1.

Figure 4. Variations in the NH4+, NO3

−, N2O, and N2 concentrations in the water profile ahead of the dam of each reservoir along the Wujiang River.The name abbreviations of each reservoir refer to Figure 1.

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3 and 4). In the HF reservoir, the maximum N2O concentrationoccurred in August at the oxycline, a water layer between the 10and 20m depths, where the DO concentration rapidly decreasedfrom more than 5 mg L−1 to below 0.5 mg L−1. As for the HJD,DF, WJD, and SL reservoirs, the maximum N2O concentrationsall occurred below the oxycline (30−45 m depths), and themaximum concentration was much less than that in the HFreservoir. Comparatively, in the SFY, PS, and YP reservoirs, N2Ostratification and the remarkable increase of the N2Oconcentration were not observed in the water profile.The N2O fluxes from the impounded Wujiang River ranged

from −7.86 to 337.22 μmol m−2 d−1, with an average of 12.76μmol m−2 d−1 (Table 2). The HF reservoir showed a significanthigh mean N2O flux of 17.15 μmol m−2 d−1, nearly 2 timeshigher than that of the other reservoirs (P < 0.05, two-wayANOVA) (Figure 6 and Table S1). Moreover, it was observedthat in the HJD reservoir, the N2O fluxes from the reservoirsurface were significantly lower than the N2O fluxes from theinflowing water, while the N2O fluxes from the released water ofthe PS reservoir were significantly higher than that from thereservoir surface (two-ANOVA, P < 0.05). The total N2Oemission from the studied reservoirs was 26.33 ton N2O-N yr−1.The HF, WJD, and SL reservoirs showed significantly high N2Oemissions, ranging from 5.19 ton N2O-N yr−1 to 10.02 ton N2O-N yr−1, which were nearly ten times higher than those from theDF, SFY, PS, and YP reservoirs (Figure 6).

■ DISCUSSIONEnvironmental Factors Influencing N2O Production in

the Impounded Wujiang River. Nitrous oxide is well knownto be created from biologically driven nitrification anddenitrification, and nitrogen availability and oxygen have beenreported to be important factors controlling the N2O-producingprocesses.38−40 In this study, the multiple regression analysissuggested that nitrate was the main determinant for the N2Oconcentration in the river water, while the main determinant forthe reservoirs was DO (Table 3). Denitrification was found to bethe main pathway of N2O production in the river water.14,41 Inthe Wujiang river waters, the high NO3

− concentrationsuggested that the reduction of NO3

− to N2O was not limitedby the available NO3

− substrate (Table 2), and the significantpositive correlation between the NO3

− and N2O concentrationsalso supported the fact that the N2O could be mainly producedby denitrification (Table 4). Although a high DO concentrationwas found in the river water, microbial respiration occurred inthe suboxic layer below the sediment−water interface, allowing

Figure 5. Variations in N2O concentrations in the surface water of the reservoirs along the Wujang River. The data are presented as mean ± standarderror. The name abbreviations of each reservoir refer to Figure 1.

Figure 6. Variations in the N2O fluxes and emissions in the reservoirs along the Wujiang River. The data for the N2O emissions are presented as mean± standard error. For the N2O flux data, the boxes and whiskers indicate the 25th to 75th and 10th and 90th percentiles, respectively. The central linesindicate the median and the outliers are not included. The name abbreviations of each reservoir refer to Figure 1.

Table 3. Results of the Stepwise Multiple Regression of N2OConcentrations with Environmental Parameters in theWujiang River

type regression model r P df

rivera N2O = −21.581 + 24.046 NO3− 0.545 <0.001 40

reservoir N2O = 104.789 − 4.083 DO −0.332 <0.001 507aData from the inflowing and released waters.

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the development of anaerobic conditions in this microenviron-ment (a few millimeters to centimeters), finally resulting in theoccupation of denitrification at the anoxic subsurface sedimentslayers.42,43 Then, N2O gas produced via the denitrification waseasily diffused into the river water under a lotic condition, henceincreasing the near-surface N2O production and emissions.44

Nitrification should have been co-occurring in the river water,

but it was less important for N2O production according to thestatistical analysis in this study.After river damming, with an increase of the water depth and a

decrease of the water flow, thermal and DO stratificationsoccurred seasonally in the reservoirs along the Wujiang River.45

Table 4. Relationships Between N2O Concentrations and the Concerned Environmental Parameters in the Eight CascadeReservoirsa

inflowing + tributary released water reservoir

r2 P n r2 P n r2 P n

WT (°C) −0.196 0.075 83 −0.028 0.867 38 0.064 0.147 508DO (mg L−1) 0.015 0.894 83 −0.088 0.599 38 −0.327b <0.001 508NO3

− (μmol L−1) 0.361b 0.001 83 0.228 0.168 38 −0.117b 0.008 508NH4

+ (μmol L−1) 0.266c 0.015 83 0.749b <0.001 38 0.134b 0.002 508N2 (mmol L−1) 0.342b 0.002 83 −0.082 0.624 38 −0.139b 0.002 508

an is the number of samples, while P is the significance level; the sampling sites were split into three categories: inflowing, released, and reservoirwater. bThe correlation was significant at the 0.01 level. cThe correlation was significant at the 0.05 level.

Figure 7. Relationship between the DO and N2O concentrations in theeight cascade reservoirs of the Wujiang River. The name abbreviationsof each reservoir refer to Figure 1. The power regressions when the DOconcentration was more than 0.24 mg L−1 (solid color circles) were asfollows: y = 21.815x−0.387, adjusted r2 = 0.397, P < 0.001, and when theDO concentration was less than 0.24 mg L−1 (red hollow circles): y =0.066x0.175, adjusted r2 = 0.768, P < 0.001.

Figure 8. (a) Dissolved oxygen versus the hydraulic load (Hl) and (b) N2O emission versus theHl in the eight cascade reservoirs of theWujiang River.The data consist of the mean of each reservoir and is symbolized by the solid color circles. The name abbreviations of each reservoir refer to Figure 1.The power regressions were as follows: (a) y = 7.018x0.060, adjusted r2 = 0.661, P < 0.001; (b) y = 2.805x−0.384, adjusted r2 = 0.625, P = 0.008.

Figure 9.N2O flux versus the hydrologic load (Hl). The data consist ofthe mean of each reservoir and is symbolized by the solid color circles.The reservoir N2O fluxes and the hydraulic load were Log10transformed. The correlation is described as a linear regression: y =0.947− 0.491x, adjusted r2 = 0.347, P = 0.003. The complete lists of thereservoir N2O fluxes and the hydrological parameters from other worksare given in Tables S1.

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The significant correlation between the DO and N2Oconcentrations and the multiple regression analysis suggestedthat DOwas a key driver of N2O production in the reservoirs. Asa result, the N2O synchronously varied with the DO in the waterprofiles, implying that DO stratification was probably a maindriving force. The reservoir N2O production depended on theDO concentration (Figure 7), and the N2O concentrationdecreased with the DOwhen the DO concentrations were above1.0 mg L−1, a threshold value above which nitrification occurs inlentic systems.22,46,47 Therefore, nitrification was the mainpathway of N2O production in the reservoirs.48−50 Moreover,the N2O concentration was significantly correlated to the NH4

+

and NO3− concentrations in the reservoirs (Table 4), suggesting

that the NH4+ was stepwise oxidized via nitrification to NO3

−

with N2O as a byproduct when there was a high DO level.8,22,51

In the HF reservoir, more complex N cycling was found in thewater profile. The dissolved N2O exhibited a remarkableincrease near the oxycline and a sharp decline in thehypolimnion, where an extremely low DO level (<0.2 mg L−1)was persistent (Figures 3 and 4). The co-occurrence ofnitrification and denitrification led to high yields of N2O inthe oxycline, a layer where the DO dramatically declined to thelimitation of the oxygen tolerance of the two N cyclingprocesses.52−55 Additionally, the persistent anaerobic conditionpromoted the reduction of N2O to N2 via denitrification,

56−59

resulting in a decrease of the N2O and an increase of N2 in thebottom of the water (Figure 4). Evidence from the δ15N andδ18O of NO3

− demonstrated that nitrification occurred from thesurface to a depth of 10 m during the summer stratification,while denitrification occurred in the bottom of the water of theHF reservoir.49 The characteristic isotopic signature of the N2O(15N-site preference, SP) also confirmed similar N cycling in thedownstream reservoir.50,60 Finally, based on the extents of theDO andN2O stratifications, the eight reservoirs could be dividedinto three groups: (1) a reservoir with strong stratification andmaximum N2O concentrations in the oxycline (the HFreservoir), (2) reservoirs with middle stratifications and N2Oconcentrations decreasing with water depth (the HJD, DF,WJD, and SL reservoirs), and (3) reservoirs with weak or nostratification (the SFY, PS, and YP reservoirs).Hydrologic Control of the N2O Flux in the Cascade

Reservoirs. The importance of hydrologic conditions incontrolling N removal and gaseous N emissions is well knownfor lakes and rivers.49,61,62 In this study, the hydraulic load wasfound to have a significant negative correlation with the N2Oemission in the Wujiang cascade reservoirs (Figure 8b), and theHF reservoir (Hl = 0.04 m d−1) showed remarkably higher N2Oemissions than the PS, SFY, and YP reservoirs (Hl > 7 m d−1)(Table S1). This may be attributed to the influence of thehydraulic load on the DO stratification (Figure 8a), animportant driving factor for N2O concentration as discussedabove. For deep reservoirs, long residence time andsubsequently developed thermal and DO stratifications intensifythe microbial O2 depletion in the hypolimnion, raising theopportunity and duration for denitrification and therebyimproving the production of gaseous N.59,63 In contrast, shortresidence times promote vertical mixing of DO in the waterprofile and they represent a disadvantage for DO stratificationand the development of anoxic deep water. The hydraulic loadcombines water residence time and water depth, and is thusconsidered the key factor for controlling the N2O emissions inthese cascade reservoirs. This process implies a coupling ofhydrological conditions and the N biogeochemical cycle. In

addition to hydrological factors, N2O emission from the watersurface is influenced by climate factors such as wind speed andwater temperature64 and these factors should be considered inthe calculation of N2O flux (eqs 2−5). There are severalmethods for calculating k600 values.33,64,65 Although the k600values from different calculations showed significant differencesin this study, the N2O fluxes based on these different k600 valueswere similar for the inflowing, reservoir, and released waters(Figures S1 and S2). This suggested that the difference in theN2O concentration between the water and the ambient air couldbe more important than the WT and the wind speed for thecalculation of the N2O flux.Given the control of the hydrological factors for the N2O

emissions observed in this study, the N2O fluxes and thehydraulic loads from the other reservoirs around the world werecollected from the references (Table S1). The reservoirhydraulic loads were found in a range of 0.016−6.25 m d−1,with an average of 1.21 ± 0.47 m d−1, and the reservoir N2Ofluxes were found in a range from −0.61 to 480 μmol m−2 d−1,with an average of 57.58 ± 28.83 μmol m−2 d−1. Both the valuesshowed a significant spatial variation, and the N2O flux wassignificantly negatively correlated with the hydraulic load(Figure 9), implying that the hydrologic control of N2O fluxwas common in the reservoirs. The empirical relationshipbetween theN2O flux and the hydraulic load will help to evaluatethe reservoir N2O flux in a large spatial scale since the reservoirhydraulic load is more easily obtained than its N2O flux. Ourstudy enriches the understanding of the regulation of thehydrologic regime for N2O production and emission in theimpounded rivers.

■ ASSOCIATED CONTENT*S Supporting InformationThe Supporting Information is available free of charge on theACS Publications website at DOI: 10.1021/acs.est.9b03438.

Supplementary Reservoir data proof; gaseous nitrogenconcentrations and water chemical parameters in thereservoirs of theWujiang River; relationships between thek600 values and the wind speeds (U10); and relationshipsbetween the N2O fluxes and the wind speeds (U10) underthe conditions of different k600 values that are referred toFigure S1 (PDF)

■ AUTHOR INFORMATIONCorresponding Authors*E-mail: xliang@sklec.ecnu.edu.cn (X.L.).*E-mail: baoli.wang@tju.edu.cn (B.W.).ORCIDXia Liang: 0000-0003-3882-5406Baoli Wang: 0000-0003-1437-6095Fushun Wang: 0000-0002-6433-6940Siliang Li: 0000-0002-0295-9675NotesThe authors declare no competing financial interest.

■ ACKNOWLEDGMENTSThis work was supported by the National Key R&DProgram ofChina (2016YFA0601003) and the National Science Founda-tion of China (41773076 and 41373097). The authorsacknowledge the kind help of our work team in the fieldwork

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and the sample analysis. The authors also thank the anonymousreviewers and the editors for their insightful comments.

■ REFERENCES(1) IPCC. In: Climate Change 2013: The Physical Science Basis.Contribution of Working Group I to the Fifth Assessment Report of theIntergovernmental Panel on Climate Change; Stocker, T. F., Qin, D.,Plattner, G. K., Tignor, M., Allen, S. K., Boschung, J., Nauels, A., Xia, Y.,Bex, V., Midgley, P. M., Eds.; Cambridge University Press: Cambridge,United Kingdom, 2013.(2) Tian, H.; Lu, C.; Ciais, P.; Michalak, A. M.; Canadell, J. G.;Saikawa, E.; Huntzinger, D. N.; Gurney, K. R.; Sitch, S.; Zhang, B.;Yang, J.; Bousquet, P.; Bruhwiler, L.; Chen, G.; Dlugokencky, E.;Friedlingstein, P.; Melillo, J.; Pan, S.; Poulter, B.; Prinn, R.; Saunois, M.;Schwalm, C. R.; Wofsy, S. C. The terrestrial biosphere as a net source ofgreenhouse gases to the atmosphere. Nature 2016, 531, 225−228.(3) Tian, H.; Yang, J.; Xu, R.; Lu, C.; Canadell, J. G.; Davidson, E. A.;Jackson, R. B.; Arneth, A.; Chang, J.; Ciais, P.; Gerber, S.; Ito, A.; Joos,F.; Lienert, S.; Messina, P.; Olin, S.; Pan, S.; Peng, C.; Saikawa, E.;Thompson, R. L.; Vuichard, N.; Winiwarter, W.; Zaehle, S.; Zhang, B.Global soil nitrous oxide emissions since the pre-industrial eraestimated by an ensemble of Terrestrial Biosphere Models: Magnitude,attribution and uncertainty. Global Change Biol. 2019, 25, 640−659.(4) Duffy, P. B.; Field, C. B.; Diffenbaugh, N. S.; Doney, S. C.; Dutton,Z.; Goodman, S.; Heinzerling, L.; Hsiang, S.; Lobell, D. B.; Mickley, L.J.; Myers, S.; Natali, S. M.; Parmesan, C.; Tierney, S.; Williams, A. P.Strengthened scientific support for the Endangerment Finding foratmospheric greenhouse gases. Science 2019, 363, No. eaat5982.(5) Hayes, N. M.; Deemer, B. R.; Corman, J. R.; Razavi, N. R.; Strock,K. E. Key differences between lakes and reservoirs modify climatesignals: A case for a new conceptual model. Limnol. Oceanogr. 2017, 2,47−62.(6) Prairie, Y. T.; Alm, J.; Beaulieu, J. J.; Barros, N.; Battin, T. J.; Cole,J. J.; Giorgio, P.; DelSontro, T.; Guerin, F.; Harby, A.; Harrison, J.;Mercier-Blais, S.; Dominique, S.; Sobek, S.; Vachon, D. GreenhouseGas Emissions from Freshwater Reservoirs: What Does theAtmosphere See? Ecosystems 2018, 21, 1058−1071.(7) Deemer, B. R.; Harrison, J. A.; Li, S.; Beaulieu, J. J.; Delsontro, T.;Barros, N.; Bezerra-Neto, J. F.; Powers, S. M.; Santos, M. A. D.; Vonk, J.A. Greenhouse gas emissions from reservoir water surfaces: a newglobal synthesis. BioScience 2016, 66, 949−964.(8) Maavara, T.; Lauerwald, R.; Laruelle, G. G.; Akbarzadeh, Z.;Bouskill, N. J.; Van Cappellen, P.; Regnier, P. Nitrous oxide emissionsfrom inland waters: Are IPCC estimates too high? Global Change Biol.2019, 25, 473−488.(9) Ni, B. J.; Yuan, Z. Recent advances in mathematical modeling ofnitrous oxides emissions from wastewater treatment processes. WaterRes. 2015, 87, 336−346.(10) Wenk, C. B.; Frame, C. H.; Koba, K.; Casciotti, K. L.; Veronesi,M.; Niemann, H.; Schubert, C. J.; Yoshida, N.; Toyoda, S.; Makabe, A.;Zopfi, J.; Lehmann, M. F. Differential N2O dynamics in two oxygen-deficient lake basins revealed by stable isotope and isotopomerdistributions. Limnol. Oceanogr. 2016, 61, 1735−1749.(11) Kuypers, M. M. M.; Marchant, H. K.; Kartal, B. The microbialnitrogen-cycling network. Nat. Rev. Microbiol. 2018, 16, 263−276.(12) Jones, C. M.; Spor, A.; Brennan, F.; Breuil, M.; Bru, D.;Lemanceau, P.; Gri-ths, B.; Hallin, S.; Philippot, L. Recently identifiedmicrobial guild mediates soil N2O sink capacity. Nat. Clim. Change2014, 4, 801−805.(13) Terada, A.; Sugawara, S.; Hojo, K.; Takeuchi, Y.; Riya, S.; Harper,W. F.; Yamamoto, T.; Kuroiwa, M.; Isobe, K.; Katsuyama, C.; Suwa, Y.;Koba, K.; Hosomi, M. Hybrid nitrous oxide production from a partialnitrifying bioreactor: hydroxylamine interactions with nitrite. Environ.Sci. Technol. 2017, 51, 2748−2756.(14) Beaulieu, J. J.; Tank, J. L.; Hamilton, S. K.; Wollheim, W. M.;Hall, R. O., Jr.; Mulholland, P. J.; Peterson, B. J.; Ashkenas, L. R.;Cooper, L. W.; Dahm, C. N.; Dodds, W. K.; Grimm, N. B.; Johnson, S.L.; McDowell, W. H.; Poole, G. C.; Valett, H.M.; Arango, C. P.; Bernot,M. J.; Burgin, A. J.; Crenshaw, C. L.; Helton, A. M.; Johnson, L. T.;

O’Brien, J. M.; Potter, J. D.; Sheibley, R. W.; Sobota, D. J.; Thomas, S.M. Nitrous oxide emission from denitrification in stream and rivernetworks. Proc. Natl. Acad. Sci. USA 2011, 108, 214−219.(15) Liu,W.; Liu, G.; Zhang, Q. Influence of vegetation characteristicson soil denitrification in shoreline wetlands of the DanjiangkouReservoir in China. Clean-Soil Air Water 2011, 39, 109−115.(16) Scaroni, A. E.; Lindau, C. W.; Nyman, J. A. Spatial variability ofsediment denitrification across the Atchafalaya River basin, Louisiana,USA. Wetlands 2010, 30, 949−955.(17) Massara, T. M.; Malamis, S.; Guisasola, A.; Baeza, J. A.;Noutsopoulos, C.; Katsou, E. A review on nitrous oxide (N2O)emissions during biological nutrient removal from municipal waste-water and sludge reject water. Sci. Total Environ. 2017, 596−597, 106−123.(18) Thompson, S. E.; Basu, N. B.; Lascurain, J., Jr.; Aubeneau, A.;Rao, P. S. C. Relative dominance of hydrologic versus biogeochemicalfactors on solute export across impact gradients. Water Resour. Res.2011, 47, W00J05.(19) Thornton, K. W. Sedimentary Processes. In: Reservoir Limnology:Ecological Perspectives; Thornton, K. W., Kimmel, B. L., Payne, F. E.,Eds.; John Wiley & Sons: New York, 1990; pp. 43−70.(20) Straskraba, M. Retention Time as Key Variable of ReservoirLimnology. InTheoretical Reservoir Ecology and its Applications; Tundisi,J. G., Straskraba,M., Eds.; Backhuys Publishers: Leiden, 1999; pp. 385−410.(21) Yu, Z.; Yang, J.; Amalfitano, S.; Yu, X.; Liu, L. Effects of waterstratification and mixing on microbial community structure in asubtropical deep reservoir. Sci. Rep. 2015, 4, No. 5821.(22) Beaulieu, J. J.; Nietch, C. T.; Young, J. L. Controls on nitrousoxide production and consumption in reservoirs of the Ohio RiverBasin. J. Geophys. Res. Biogeosci. 2015, 120, 1995−2010.(23) Salk, K. R.; Ostrom, P. H.; Biddanda, B. A.; Weinke, A. D.;Kendall, S. T.; Ostrom, N. E. Ecosystem metabolism and greenhousegas production in a mesotrophic northern temperate lake experiencingseasonal hypoxia. Biogeochemistry 2016, 131, 303−319.(24) Harrison, J. A.; Maranger, R. J.; Alexander, R. B.; Giblin, A. E.;Jacinthe, P. A.; Mayorga, E.; Seitzinger, S. P.; Sobota, D. J.; Wollheim,W. M. The regional and global significance of nitrogen removal in lakesand reservoirs. Biogeochemistry 2009, 93, 143−157.(25) Wang, B.; Liu, C.; Wang, F.; Liu, X.; Wang, Z. A decrease in pHdownstream from the hydroelectric dam in relation to the carbonbiogeochemical cycle. Environ. Earth Sci. 2015, 73, 5299−5306.(26) Zhang, Y.; Wu, Z.; Liu, M.; He, J.; Shi, K.; Zhou, Y.; Wang, M.;Liu, X. Dissolved oxygen stratification and response to thermalstructure and long-term climate change in a large and deep subtropicalreservoir (Lake Qiandaohu, China). Water Res. 2015, 75, 249−258.(27) Wang, S.; Liu, C.; Yeager, K. M.; Wan, G.; Li, J.; Tao, F.; Lu, Y.;Liu, F.; Fan, C. The spatial distribution and emission of nitrous oxide(N2O) in a large eutrophic lake in eastern China: anthropogenic effects.Sci. Total Environ. 2009, 407, 3330−3337.(28) Yan, W.; Yang, L.; Wang, F.; Wang, J.; Ma, P. Riverine N2Oconcentrations, exports to estuary and emissions to atmosphere fromthe Changjiang River in response to increasing nitrogen loads. GlobalBiogeochem. Cycles 2012, 26, GB4006.(29) Chen, N.; Chen, Z.; Wu, Y.; Hu, A. Understanding gaseousnitrogen removal through direct measurement of dissolved N2 andN2Oin a subtropical river-reservoir system. Ecol. Eng. 2014, 70, 56−67.(30) Yu, Z.; Deng, H.; Wang, D.; Ye, M.; Tan, Y.; Li, Y.; Chen, Z.; Xu,S. Nitrous oxide emissions in the Shanghai river network: implicationsfor the effects of urban sewage and IPCC methodology. Global ChangeBiol. 2013, 19, 2999−3010.(31) Liss, P. S.; Slater, P. G. Flux of gases across the air-sea interface.Nature 1974, 247, 181−184.(32) Wanninkhof, R. Relationship between wind speed and gasexchange over the ocean. J. Geophys. Res. 1992, 97, 7373−7382.(33) Crusius, J.; Wanninkhof, R. Gas transfer velocities measured atlow wind speed over a lake. Limnol. Oceanogr. 2003, 48, 1010−1017.(34) Barros, N.; Cole, J. J.; Tranvik, L. J.; Prairie, Y. T.; Bastviken, D.;Huszar, V. L. M.; del Giorgio, P.; Roland, F. Carbon emission from

Environmental Science & Technology Article

DOI: 10.1021/acs.est.9b03438Environ. Sci. Technol. 2019, 53, 11745−11754

11753

hydroelectric reservoirs linked to reservoir age and latitude.Nat. Geosci.2011, 4, 593−596.(35) China EPA. Environmental Quality Standards for Surface Water ofthe People’s Republic of China; Ministry of environmental protection ofthe people’s republic of China: Beijing, 2002.(36)Wollheim,W.M.; Vorosmarty, C. J.; Peterson, B. J.; Seitzinger, S.P.; Hopkinson, C. S. Relationship between river size and nutrientremoval. Geophys. Res. Lett. 2006, 33, L06410.(37) Musenze, R. S.; Grinham, A.; Werner, U.; Gale, D.; Sturm, K.;Udy, J.; Yuan, Z. Assessing the spatial and temporal variability ofdiffusive methane and nitrous oxide emissions from subtropicalfreshwater reservoirs. Environ. Sci. Technol. 2014, 48, 14499−14507.(38) Yoh, M.; Terai, H.; Saijo, Y. Accumulation of nitrous oxide in theoxygen deficient layer of freshwater lakes. Nature 1983, 301, 327−329.(39) Gruber, N.; Galloway, J. N. An Earth-system view of the globalnitrogen cycle. Nature 2008, 451, 293−296.(40) Saarenheimo, J.; Rissanen, A. J.; Arvola, L.; Nykanen, H.;Lehmann, M. F.; Tiirola, M. Genetic and environmental controls onnitrous oxide accumulation in lakes. PLoS ONE 2015, 10, e0121201.(41) Mulholland, P. J.; Helton, A.; Poole, G. C.; Hall, R. O., Jr.;Hamilton, S. K.; Peterson, B. J.; Tank, J. L.; Ashkenas, L. R.; Cooper, L.W.; Dahm, C. N.; Dodds, W. K.; Findlay, S. E. G.; Gregory, S. V.;Grimm, N. B.; Johnson, S. L.; McDowell, W. H.; Meyer, J. L.; Valett, H.M.;Webster, J. R.; Arango, C. P.; Beaulieu, J. J.; Bernot, M. J.; Burgin, A.J.; Crenshaw, C. L.; Johnson, L. T.; Niederlehner, B. R.; O’Brien, J. M.;Potter, J. D.; Sheibley, R. W.; Sobota, D. J.; Thomas, S. M. Streamdenitrification across biomes and its response to anthropogenic nitrateloading. Nature 2008, 452, 202−206.(42) Hinshaw, S. E.; Dahlgren, R. A. Dissolved nitrous oxideconcentrations and fluxes from the eutrophic San Joaquin River,California. Environ. Sci. Technol. 2013, 47, 1313−1322.(43) Xia, X.; Zhang, S.; Li, S.; Zhang, L.; Wang, G.; Zhang, L.; Wang,J.; Li, Z. The cycle of nitrogen in river systems: sources, transformation,and flux. Environ. Sci.: Processes Impacts 2018, 20, 863−891.(44) Dore, J. E.; Popp, B. N.; Karl, D. M.; Sansone, F. J. A large sourceof atmospheric nitrous oxide from subtropical North Pacific surfacewaters. Nature 1998, 396, 63−66.(45) Han, Q.; Wang, B.; Liu, C.; Wang, F.; Peng, X.; Liu, X. Carbonbiogeochemical cycle is enhanced by damming in a karst river. Sci. TotalEnviron. 2018, 616−617, 1181−1189.(46) CENR 2000; Integrated Assessment of Hypoxia in the NorthernGulf of Mexico; National Science and Technology Council Committeeon Environment and Natural Resources: Washington, DC, 2000.(47) Sasaki, Y.; Koba, K.; Yamamoto, M.; Makabe, A.; Ueno, Y.;Nakagawa, M.; Toyoda, S.; Yoshida, N.; Yoh, M. Biogeochemistry ofnitrous oxide in Lake Kizaki, Japan, elucidated by nitrous oxideisotopomer analysis. J. Geophys. Res. 2011, 116, G04030.(48) Liu, X.; Liu, C.; Li, S.; Wang, F.; Wang, B.; Wang, Z.Spatiotemporal variations of nitrous oxide (N2O) emissions from tworeservoirs in SW China. Atmos. Environ. 2011, 45, 5458−5468.(49) Wang, Z.; Yue, F.; Li, S.; Li, X.; Wang, S.; Li, C.; Tao, F. Nitratedynamics during impoundment and flood periods in a subtropical karstreservoir: Hongfeng Lake, Southwestern China. Environ. Sci.: ProcessesImpacts 2018, 20, 1736−1745.(50) Yue, F.; Li, S.; Liu, C.; Mostofa, K. M. G.; Yoshida, N.; Toyoda,S.; Wang, S.; Hattori, S.; Liu, X. Spatial variation of nitrogen cycling in asubtropical stratified impoundment in southwest China, elucidated bynitrous oxide isotopomer and nitrate isotopes. Inland Waters 2018, 8,186−195.(51) Rosamond, M. S.; Thuss, S. J.; Schiff, S. L.; Elgood, R. J. Coupledcycles of dissolved oxygen and nitrous oxide in rivers along a trophicgradient in Southern Ontario, Canada. J. Environ. Qual. 2011, 40, 256−270.(52) Firestone, M. K.; Firestone, R. B.; Tiedje, J. M. Nitrous-oxidefrom soil denitrification: Factors controlling its biological production.Science 1980, 208, 749−751.(53) Firestone, M. K.; Davidson, E. A. Microbiological Basis of NOand N2O Production and Consumption in Soil. In Exchange of Trace

Gases between Terrestrial Ecosystems and the Atmosphere; Andreae, M.O., Schimel, D. S., Eds.; Wiley: Chichester; 1989; pp 7−21.(54) Goreau, T. J.; Kaplan, W. A.; Wofsky, S. C.; McElroy, M. B.;Valois, F. W.; Watson, S. W. Production of NO2

− and N2O by nitrifyingbacteria at reduced concentrations of oxygen. Appl. Environ. Microbiol.1980, 40, 526−532.(55) Mengis, M.; Gachter, R.; Wehrli, B. Sources and sinks of nitrousoxide (N2O) in deep lakes. Biogeochemistry 1997, 38, 281−301.(56) Koike, I.; Hattori, A. Energy yield of denitrification: An estimatefor growth yield in continuous cultures of Pseudononas denitrificansunder nitrate, nitrite, and nitrous oxide limited conditions. J. Gen.Microbiol. 1975, 88, 11−19.(57) Richardson, D.; Felgate, H.;Watmough, N.; Thomson, A.; Baggs,E. Mitigating release of the potent greenhouse gas N2O from thenitrogen cycle-could enzymic regulation hold the key? TrendsBiotechnol. 2009, 27, 388−397.(58) Deemer, B. R.; Harrison, J. A.; Whitling, E. W. Microbialdinitrogen and nitrous oxide production in a small eutrophic reservoir:an in situ approach to quantifying hypolimnetic process rates. Limnol.Oceanogr. 2011, 56, 1189−1199.(59) Beaulieu, J. J.; Smolenski, R. L.; Nietch, C. T.; Townsend-Small,A.; Elovitz, M. S.; Schubauer-Berigan, J. P. Denitrification alternatesbetween a source and sink of nitrous oxide in the hypolimnion of athermally stratified reservoir. Limnol. Oceanogr. 2014, 59, 495−506.(60) Toyoda, S.; Yoshida, N. Determination of nitrogen isotopomersof nitrous oxide on a modified isotope ratio mass spectrometer. Anal.Chem. 1999, 71, 4711−4718.(61) Saunders, D. L.; Kalff, J. Nitrogen retention in wetlands, lakes andrivers. Hydrobiologia 2001, 443, 205−212.(62) Alexander, R. B.; Bohlke, J. K.; Boyer, E. W.; David, M. B.;Harvey, J. W.;Mulholland, P. J.; Seitzinger, S. P.; Tobias, C. R.; Tonitto,C.; Wollheim, W. M. Dynamic modeling of nitrogen losses in rivernetworks unravels the coupled effects of hydrological and biogeochem-ical processes. Biogeochemistry 2009, 93, 91−116.(63) Descloux, S.; Chanudet, V.; Serca, D.; Guerin, F. Methane andnitrous oxide annual emissions from an old eutrophic temperatereservoir. Sci. Total Environ. 2017, 598, 959−972.(64) MacIntyre, S.; Wanninkhof, R.; Chanton, J. Trace Gas ExchangeAcross the Air-Water Interface in Freshwater and Coastal MarineEnvironments. In: Biogenic Trace Gases: Measuring Emissions from SoilandWater; Matson, P., Harriss, R., Eds.; Blackwell: New York, 1995; pp52−97.(65) Cole, J. J.; Caraco, N. F. Atmospheric exchange of carbon dioxidein a low-wind oligotrophic lakemeasured by the addition of SF6. Limnol.Oceanogr. 1998, 43, 647−656.

Environmental Science & Technology Article

DOI: 10.1021/acs.est.9b03438Environ. Sci. Technol. 2019, 53, 11745−11754

11754