Desorption kinetics of ammonium and methylamines from estuarine sediments: Consequences for the cycling of nitrogen

Marine Chemistry 101 (2006) 12 – 26 www.elsevier.com/locate/marchem

Desorption kinetics of ammonium and methylamines from estuarine sediments: Consequences for the cycling of nitrogen Mark F. Fitzsimons a,⁎, Geoffrey E. Millward a , D. Michael Revitt b , Mekibib D. Dawit b a

School of Earth Ocean and Environmental Sciences, University of Plymouth, Drake Circus, Plymouth, Devon PL4 8AA, United Kingdom b Urban Pollution Research Centre, Middlesex University, Queensway, Enfield, Middlesex EN3 4SA, United Kingdom Received 11 April 2005; received in revised form 25 November 2005; accepted 6 December 2005 Available online 23 February 2006

Abstract Concentrations of dissolved and particulate NH+4 and mono-, di- and trimethylamines (MAs) were determined in surface sediments and pore-waters collected from the Thames Estuary, United Kingdom, during July and November 2001. Dissolved NH+4 was an order of magnitude more abundant than the MAs in the pore-waters, whereas in the solid phase each MA was more abundant than NH+4 . Sediments were also used in controlled, time-dependent, desorption experiments, using indigenous, filtered seawater. Desorption of NH+4 was more rapid than the MAs and the kinetics were interpreted using a reversible first-order mechanism. The mean response times (i.e. time taken to achieve 63% of the new equilibrium) of NH+4 and MAs were about 15 and 25 min, respectively. Increases in the concentrations of dissolved NH+4 and dissolved MAs, in the Thames Estuary over a tidal cycle, were coincident with the remobilisation of seabed sediments. Model calculations showed that desorption of NH+4 from the remobilised sediments accounted for approximately 50% of increase, whereas for MAs it was N 90%. The results are proposed as a predictor for the sorption behaviour of other organic nitrogen compounds, such as basic amino acids, and emphasise the importance of sediment resuspension as a mechanism for the release of ON to the water column. © 2006 Elsevier B.V. All rights reserved. Keywords: Ammonium; Methylamines; Sediment resuspension; Kinetics; Thames Estuary

1. Introduction The speciation and reactivity of organic nitrogen (ON) compounds in rivers and estuaries are unquantified, giving rise to major uncertainties in the factors controlling the flux of N from estuaries to coastal seas. The key to reducing the unknowns is an improved understanding of the kinetics and equilibria of sorption reactions involving estuarine sediments and suspended particulate material (SPM) (Komada and Reimers, 2001). ⁎ Corresponding author. Tel.: +44 1752 232971; fax: +44 1752 233035. E-mail address: [email protected] (M.F. Fitzsimons). 0304-4203/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.marchem.2005.12.006

Amino acids, in both free and combined form, comprise the most abundant group of compounds within the ON fraction (Burdige and Martens, 1988; Ittekot and Zhang, 1989). Analysis of sediments (Hedges et al., 1994; Aufdenkampe et al., 2001) and laboratory radiotracer studies have indicated that basic amino acids show a greater propensity to adsorb to particles than their acidic and neutral counterparts (Henrichs and Sugai, 1993; Montluçon and Lee, 2001). Benthic fluxes of dissolved ON (DON) from coastal and estuarine sediments are relatively small compared to the benthic dissolved inorganic nitrogen (DIN) flux (Enoksson, 1993; Cowan and Boynton, 1996). However, particulate N (PN) is organic, and desorption of this

M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

fraction will increase the estuarine benthic ON flux during sediment resuspension. Increases in the occurrence of harmful algal blooms in the United States midAtlantic region have been attributed to DON enrichment (Lewitus et al., 1999; Glibert et al., 2001). Furthermore, Middelburg and Nieuwenhuize (2000) measured biological uptake of spiked 15N substrates in the outer Thames Estuary and found that amino acids accounted for approximately 50% of the N taken up. The measured amino acid turnover times were rapid in comparison with inorganic N substrates, being in the range 4.8 to 46 h. This fits with the paradigm that DON compounds are preferentially utilised by marine bacteria (Jørgensen et al., 1993). Amino compounds can adsorb to particle exchange sites, usually as cations (Wang and Lee, 1990; Henrichs and Sugai, 1993). Adsorption of NH4+ to sediments is demonstrably reversible and increased benthic fluxes of NH4+ have been measured during flooding of inter-tidal sediments (Caetano et al., 1997; Rocha, 1998) and as a consequence of dredging (Morin and Morse, 1999). Assuming that the degree of adsorption of a compound is related to its basicity, those compounds with a lower pKb than NH4+ will desorb less readily. Cations in seawater can compete with NH4+ ions for particle exchange sites. Indeed, a relationship between NH4+ release from sediments and salinity was observed in a study of N dynamics in Texas estuaries (Gardner et al., 2006). This study also found that dissimilatory nitrate reduction to ammonium (DNRA) in sediments was stimulated by salinity, leading to increased regeneration of NH4+. Factors controlling the particle–water exchange of ON are key to the quantification of its role within the N cycle, while knowledge of the sorption mechanisms of ON compounds could explain the composition of sedimentary N. In this paper we quantify the sorption behaviour of NH4+ and a group of ON compounds, the methylamines (MAs), in samples from the Thames Estuary, UK. Monomethylamine (MMA), dimethylamine (DMA) and trimethylamine (TMA) are chemical analogues of NH4+ and are basic compounds within the ON fraction. Their pKbs (3.27–4.19) reflect the different chemical structures and behaviour in aqueous solution, and are all below that of NH4+ (4.75).

13

Greater London, finally discharging into the southern North Sea. The mean fluvial input is 82 m3 s− 1, the tidal range varies from 3 to 6 m and the flushing time varies from 20 to 40 days (Abril et al., 2002). The catchment area is 14,000 km2 supporting a population of 11 million. Sewage contamination of the estuary was an issue in the past (Kinneburgh, 1998) and some beaches (e.g. those near Southend; Fig. 1) have achieved only mandatory compliance with the EC Bathing Water Directive. The estuary is classed as nitrate-rich (Middelburg and Nieuwenhuize, 2000) and a fraction of the SPM is sewage-derived and undergoes carbon mineralization during its advection seawards (Abril et al., 2002). The sample transect comprised four sites (i.e. TE1 to TE4), extending from Southend to Benfleet Creek (Fig. 1), covering various inter-tidal ecosystems and sediment types. TE1 reflected the open estuary, TE2 was modified by inputs from Benfleet Creek and TE3 and TE4 were located in inner Benfleet Creek. 2.2. Sample collection and pre-treatment

2. Methods

Sediments and overlying water (OLW) were collected in July and November 2001 from exposed mudflats using acid-washed PVC core tubes (150 × 70 mm) and placed in a cool box. The tidal range during the three sampling campaigns was 4.1 m and the mean salinity was approximately 34 U. The top 5 mm of oxic sediment was removed from each core to determine concentrations of sediment-exchangeable and pore-water N species, and physico-chemical parameters. Pore-waters were separated from the sediment sections by centrifugation (3000 rpm, 5 min) followed by filtration of the supernatant (passing a Whatman 0.45 μm pore-size filter). The supernatant liquids were poured into acidwashed glass vials and they, and sediment, were stored in a freezer (− 20 °C). Water samples (0.5 L) were collected, at hourly intervals for 6 h, in acid-washed Nalgene bottles, from a bridge overlooking site TE3 during a flooding tide. The samples were transported to the laboratory and filtered, immediately, through pre-weighed glass fibre filters and the filtrate stored at 4 °C. The filters were weighed, after drying at 105 °C, and the SPM concentrations were estimated using the dry weight of SPM and volume of filtrate.

2.1. Site description and sample locations

2.3. Analysis

The Thames estuary is a turbid, macrotidal estuary on the east coast of the United Kingdom (Fig. 1a) extending from the tidal limit at Teddington Weir (Fig. 1b), through

2.3.1. Physico-chemical measurements Grain size measurements were measured using a Malvern Long-bed Mastersizer-X, according to ISO13320.

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M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

N

c

Benfleet

TE4

Southend

TE3 TE1 TE2

Canvey Island

o

56

a

THAMES ESTUARY

o

54

1 km

o

52

LONDON BRIDGE

TEDDINGTON WEIR

o

50

o

6

o

3

o

0

Canvey Island

b

Scale 10km

Fig. 1. Location of the sampling sites in the Thames Estuary, United Kingdom. 1a shows the location of the Thames Estuary in SE England. 1b shows the location of the sampling area within the Estuary, while 1c shows the precise location of the sampling sites. Sampling sites are marked (e.g. TE1).

Prior to analysis the samples were freeze-dried and the organic material removed through wet oxidation using 6% hydrogen peroxide (Smith, 1975). The water content of the sediments was estimated as weight loss after heating (105 °C, 48 h). Particulate organic carbon (POC) and PN were determined, in triplicate, on freeze-dried sediments placed in silver micro-cups, pre-extracted in a 1 : 1 mixture of acetone and hexane, followed by combustion in a muffle furnace (250 °C, 14 h). Samples of ∼5 mg were accurately weighed into the micro-cups and 2 mg of pure CaCO3 added to separate micro-cups as reference standards. One drop of Milli-Q water (18 MΩ cm− 1 resistivity) was added to each micro-cup, which were then placed in a desiccator containing a beaker of concentrated HCl (∼250 mL, 4 h) in order to de-carbonate the sediments (Yamamuro and Kayanne, 1995). The carbonatefree sediments were dried (60 °C, 5 h) and the CHN analyses carried out combustiometrically, in triplicate, on a Carlo Erba EA1110 elemental analyzer. The reproducibility was better than 10% for POC and 20% for PN, with the exception of TE1-July (47%). Analyses of the certified marine sediment reference material (BCSS-1; National Research Council Canada) gave a total carbon concen-

tration of 2.22 ± 0.03% compared to a certified value of 2.19 ± 0.09%. 2.3.2. Analysis of NH4+ and MAs The concentrations of all dissolved and particulate NH4+([NH4+]D and [NH4+]P , respectively) and each MA (e.g. [MMA]D and [MMA]P) were determined. NH4+ was determined by colorimetry (Dal Pont et al., 1974) and the MAs by microdiffusion-gas chromatography, with nitrogen–phosphorus detection, using a method described by Fitzsimons et al. (2001). Aqueous samples were transferred to acid-washed volumetric flasks and diluted to 50 mL in a solution of synthetic seawater, adjusted to pH 12 through addition of 2 mL NaOH (6 M). Cyclopropylamine (CPA) was added as an internal standard and the MAs were then pre-concentrated (24 h, 60 °C) in an oven. The pre-concentrated samples (i.e. MAs in 0.2 mL of 0.02 M HCl) were readjusted to pH 12 by adding 50 μL NaOH (0.5 M) and injected onto a Fisons 8000 Series, packed column, gas chromatograph equipped with a nitrogen-phosphorus detector (GC-NPD). The GC column (2 m) was packed with Carbopack B (60–80 mesh) coated with Carbowax 20 M (4%) and

M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

15

KOH (0.8%). Peak areas were recorded using a PC equipped with Chrom-card for Windows (Thermo Finnigan). Ultra-pure water for blanks and standard solutions was obtained from a SERADEST S600 system (b0.1 μS cm− 1 conductivity). Stock standard solutions of NH4+(100 mM) and the MAs (1 M) were prepared through dissolution of their chloride salts, with a small amount of concentrated HCl added as a preservative. The solutions were refrigerated and checked regularly for degradation. Working standard dilutions were prepared as required. The detection limit for NH4+ was estimated as 111 nmol L− 1 (4 × standard deviation of synthetic seawater blank). Detection limits for the MAs, using microdiffusion-GC-NPD, were 9, 12 and 22 nmol L− 1 for MMA, DMA and TMA, respectively (calculated using a synthetic seawater blank on the basis of a signal to noise ratio ≥ 2).

concentrations in the range 0.4 to 0.6 g L− 1. These SPM concentrations were higher than those measured during the tidal cycle but were similar to those used in comparable experiments (Morin and Morse, 1999). A subsample of water (10 mL) was taken, prior to addition of the sediment, to determine the background, dissolved concentrations of the analytes at t = 0. The reactors were then sealed and gently agitated on a mechanical shaker (48 h, 25 °C). Aliquots of the suspension (10 mL) were taken at selected time intervals and filtered through 0.45 μm poresize filters. The filtrates were analysed for [NH4+]D and [MA]D according to the methods described above. The measurement precision was 4% or less for dissolved NH4+, and b 10% for determinations of dissolved MAs, with one exception (12%). The contributions of [NH4+]D and [MA]D from the pore-waters of the unfiltered sediments were estimated to be b 1% of the final concentration in all of the experimental runs.

2.3.3. Determination of sediment-exchangeable NH4+ and MAs Multiple extractions of the sediments with a 2 M KCl solution were undertaken to obtain a measure of the sediment-exchangeable NH4+([NH4+]P) and MA ([MA]P) fractions. A sample of moist, filtered sediment (0.5–1.0 g) was placed in a clean, acid-washed Nalgene centrifuge tube and extracted with a volume of 2 M KCl (see below) for 24 h (Morin and Morse, 1999). The suspension was centrifuged (3000 rpm, 1 h) and filtered (0.45 μm poresize filter). The filter was washed several times with 2 M KCl to ensure that any decanted sediment was returned to the centrifuge tube for the next extraction. In all, six extractions (3 × 20 mL; then 3 × 40 mL) were performed on each sample and the filtrate from each extraction analysed separately according to the methods described above. All experiments were carried out in duplicate and the measurement precision was b 10% for NH4+, with one exception (18%) and b6% for the MAs.

3. Results

2.3.4. Desorption experiments These experiments were designed to evaluate the rate and extent of desorption of [NH4+]P and [MA]P during sediment resuspension. Duplicate incubations were carried out in acid-washed Nalgene reactors (1 L volume) using natural sediments and OLW (0.45 μm-filtered) from each site. Sodium azide (NaN3) was added to each OLW sample, as a biocide, at a concentration of 0.1% w/v (Morin and Morse, 1999). Amines can be produced from NaN3 under non-aqueous conditions (Clayden et al., 2001) but were not predicted to form in our suspensions of natural waters. Natural, unfiltered sediments were added to their respective OLW from each site to create SPM

3.1. Physico-chemical characteristics of the sediment The sediments at sites TE1 and TE2 had a high sand content (45–76%) in both July and November, since the sites were most exposed to the up-estuary migration of marine sediments (Table 1). TE3 had a greater proportion of finer material in both July and November when the combined silt and clay fractions were typically N60%. Site TE4 had a total of 60% silt and clay in July, whereas in November the major component was sand. The water content of the sediments varied over a range from 33% to 57%. POC concentrations ranged from 0.54% to 2.06% in July and from 0.24% to 1.71% in November (Table 1). PN values ranged from 0.02% to 0.20% in July and from 0.03% to 0.18% in November. The sediment POC concentrations for July and November were inversely related to the fraction of sand (R2 = 0.68; p b 0.05); a similar relationship existed for PN (R2 = 0.76; p b 0.05). 3.2. Concentrations of sediment-exchangeable NH4+ and MAs Fig. 2 shows the [NH4+]P and [MAs]P recovered from moist, filtered sediment using sequential volumes of 2 M KCl. Multi-volume extraction of sediment with 2 M KCl consistently released more of the sedimentexchangeable analyte than a single volume extraction of the same sample. The single-volume extraction efficiency (as a percentage of the total amount extracted via multi-volume extraction) for the July samples ranged from 37% to 44% for NH4+ and from 35% to 51% for the

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M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

Table 1 Summary of physical and chemical data for surface sediments (0–5 mm depth) sampled in the Thames Estuary Sample

Salinity

July TE1

36.5

TE2

37.0

TE3

34.9

TE4

40.1

November TE1 28.3

TE2

28.9

TE3

32.2

TE4

34.3

Grain size

Size fraction (%)

Water (%)

POC (%)

PN (%)

Sand Silt Clay Sand Silt Clay Sand Silt Clay Sand Silt Clay

45 45 10 76 20 4 6 77 17 40 48 12

49

0.54

0.05

42

0.26

37

Sand Silt Clay Sand Silt Clay Sand Silt Clay Sand Silt Clay

49 43 8 61 32 7 19 67 14 64 29 7

C/N (atomic)

Available particulate concentrations (μmol g− 1)

Dissolved porewater concentrations (μmol L− 1)

NH+4

MMA

DMA

TMA

NH+4

14.7

3.29

5.58

5.72

7.66

0.02

24.8

3.18

5.17

4.87

2.03

0.20

12.1

2.09

3.76

3.40

51

2.06

0.19

12.7

2.52

8.44

7.96

32

0.46

0.05

12.4

1.91

2.05

2.81

33

0.24

0.03

14.6

2.69

3.81

55

1.71

0.18

11.3

2.89

57

0.65

0.04

18.7

3.46

MAs. The single-volume extraction efficiencies were higher for the November sediments from all sampling sites and were in the range from 44% to 51% for NH4+ and from 45% to 58% for the MAs. The mean [NH4+]P in July (2.77 ± 0.57 μmol g− 1) was similar to that in November (2.74 ± 0.64 μmol g− 1) (Table 1). The sediment-exchangeable pool of [MA]P was greater than that of [NH4+]P in all the samples, and individual MAs were also consistently more abundant than NH4+ (Table 1). The mean concentrations of [MMA]P were highest in July (5.74 ± 1.96 μmol g− 1), where it was present at similar abundance to [DMA]P (5.49 ± 1.91 μmol g−1). TMA was the most abundant analyte in the July samples (7.27 ± 2.19 μmol g− 1). In November, the mean [MMA]P (2.86 ± 0.73 μmol g− 1), [DMA]P (3.78 ± 0.8 μmol g− 1) and [TMA]P (6.01 ± 1.2 μmol g− 1) were lower than the values for July. The sediment-exchangeable concentrations for July and November were compared for each analyte using ANOVA statistical tests (p b 0.05) and the sample sets were not significantly different between July and November in all cases.

MMA

DMA

TMA

61

0.08

0.31

0.03

6.72

39

0.11

0.32

0.06

4.72

54

0.09

0.35

0.06

25

0.13

0.37

0.06

4.37

77

0.98

1.20

1.40

4.66

7.15

82

1.10

1.42

1.56

2.65

3.51

6.63

92

1.31

1.60

1.75

2.93

4.14

5.90

113

1.44

1.85

2.23

10.0

Multi-volume extraction of sediment samples with 2 M KCl provided a better estimate of sediment-exchangeable NH4+ and MAs than a single-volume extraction. Previously, this has only been observed for NH4+(Laima, 1992; Morin and Morse, 1999) and we show that a singlevolume extraction of sediments considerably underestimated the sediment-exchangeable MA pool in these samples. The MAs remaining associated with the sediment solid phase after extraction with 1 M LiCl (2 h; sediment : water= 1 : 20 v/v) have been categorized as ‘fixed’ within the sediment matrix (Wang and Lee, 1990, 1994). However, the equilibrium concentrations of all MAs released during the desorption experiments were greater than the amount released by a single-volume extraction with 2 M KCl. In some cases, this also exceeded the amounts recovered by multi-volume extraction (Tables 2 and 3). These findings suggest that 2 M KCl may be an inappropriate reagent for the determination of total [NH4+]P and [MA]P and, by extrapolation for the estimation of sediment-exchangeable organic N. Nevertheless, 2 M KCl is in common use and we have used it as a basis for estimating the sediment-exchangeable [NH4+]P and [MA]P.

July

(d)

10

10

10

8

8

8

2

1

6 4 2

0

50

100

Cumulative volume 2M KCl, mL

November

200

Ammonia, µ mol g -1

2

1

50 100 150 Cumulative volume 2M KCl,mL

200

0

200

8

8

8

4

6 4

100

150

Cumulative volume 2M KCl, mL

200

200

6 4

0

0 50

150

2

2

0

100

(h)

10

6

50

Cumulative volume 2M KCl, mL

10

0 0

150

(g)

2

0

100

10

MMA, µ mol g-1

3

50

Cumulative volume 2M KCl, mL

(f)

4

4

0 0

DMA, µ mol g-1

(e)

50 100 150 Cumulative volume 2M KCl, mL

6

2

0

0

200

150

4 2

0

0

6

TMA, µ mol g -1

MMA, µmol g-1

3

TMA, µ mol g-1

(c)

M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

Ammonia, µmol g-1

4

(b)

DMA, µ mol g -1

(a)

0

50

100

150

Cumulative volume 2M KCl, mL

200

0

50

100

150

200

Cumulative volume 2M KCl, mL

Fig. 2. Concentrations of NH+4 and MAs from multiple extractions of Thames Estuary sediments using 2 M KCl. July 2001 (a) NH+4 , (b) MMA, (c) DMA and (d) TMA and November 2001 (e) NH+4, (f) MMA, (g) DMA and (h) TMA (Δ = TE1; = TE2; □ = TE3; ▴ = TE4).

▪

17

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M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

Table 2 Reaction constants for desorption experiments collected in July 2001, where (k1 + k− 1) = the sum of the forward and reverse rate constants; n = number of points used in kinetic analysis; R2 = regression coefficients for points in the kinetic analysis Available particulate concentration a [MA]P, μmol L− 1

Dissolved concentration at equilibrium [MA]eD, μmol L− 1

SPM concentration, mg L− 1

KD, L kg− 1

(k1 + k− 1), h− 1

n

R2

τresp, h

TE1 NH4 MMA DMA TMA

1.7 2.9 3.0 3.9

1.4 2.9 3.4 3.6

520 520 520 520

410 – – 160

ND 2.8 2.1 2.0

5 4 4

0.88 0.87 0.75

0.36 0.48 0.50

TE2 NH4 MMA DMA TMA

1.9 3.0 2.8 3.9

1.3 2.8 3.2 3.5

580 580 580 580

800 120 – 200

ND 2.5 2.2 2.0

5 5 5

0.83 0.98 0.97

0.40 0.46 0.49

TE3 NH4 MMA DMA TMA

1.3 2.4 2.1 3.0

1.1 2.5 2.5 2.8

630 630 630 630

290 – – 110

ND 2.4 2.5 2.3

5 5 4

0.89 0.99 0.85

0.42 0.40 0.44

TE4 NH4 MMA DMA TMA

1.2 4.1 3.9 4.9

0.84 2.0 2.1 2.4

490 490 490 490

870 2140 1750 2130

ND 2.4 1.9 1.7

5 5 5

0.91 0.87 0.96

0.41 0.53 0.57

Sample

a Available particulate ammonia or MA concentration (w/v) is estimated as the product of the ammonia or MA concentration (w/w) in Table 1 and the SPM concentration (w/v). ND = Not determined. In experiments where the equilibrium concentration exceeds the maximum extracted by 2 M KCl, determination of KD was not possible.

3.3. Concentrations of NH4+ and MAs in sediment pore-waters Pore-water NH4+ was more abundant in November (91 ± 16 μmol L− 1) than in July (45 ± 16 μmol L− 1). Porewater MA concentrations were significantly lower than for NH4+ in both months (Table 1). The range of dissolved concentrations for the three MAs was relatively low in July (0.03–0.37 μmol L− 1), but had increased significantly in the November samples (0.98–2.23 μmol L− 1). DMA was the most abundant MA in the pore-waters during July, when TMA was the least abundant, whereas in November, TMAwas the most abundant MA. ANOVA statistical tests were performed on the sample sets for each analyte and it was observed that the pore-water concentrations were significantly different between July and November for each analyte (p b 0.05). 3.4. Evolution of [NH4+]D and total [MA]D over a tidal cycle (TE3) Fig. 3 shows the time-dependent behaviour of [NH4+]D, total dissolved MAs (Σ[MA]D), and SPM

over part of a tidal cycle at site TE3. During the incursion of the flood tide resuspension of mobile bed sediment occurred and the SPM concentration increased from 55 to 250 mg L− 1. [NH4+]D increased steadily in parallel with the concentration of SPM. The Σ[MA]D began to increase, reaching a maximum after 4.5 h, then decreased. Concentrations of the individual MAs followed this trend, and their order of abundance was TMA N DMA N MMA. [NH4+]D was typically an order of magnitude more abundant than the dissolved MAs, which was similar to their relative concentrations in the pore-waters. 3.5. Desorption of NH4+ and MAs during sediment resuspension Representative results for the time-dependent desorption experiments are shown in Figs. 4 and 5 for TE1 and TE3, respectively. The reaction profiles show an initial fast rise, particularly for NH4+, followed by a slower approach to equilibrium. The NH4+ desorption profiles were characterised by a rapid initial desorption (b1 min), an overshoot after about 20 min, followed by

M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

19

Table 3 Reaction constants for desorption experiments collected in November 2001, where (k1 + k− 1) = the sum of the forward and reverse rate constants; n = number of points used in kinetic analysis; R2 = regression coefficients for points in the kinetic analysis Available particulate concentration a [MA]P, μmol L− 1

Dissolved concentration at equilibrium [MA]eD, μmol L− 1

SPM concentration, mg L− 1

KD, L kg− 1

(k1 + k− 1), h− 1

n

R2

τresp, h

TE1 NH4 MMA DMA TMA

1.3 1.4 1.9 3.0

0.52 0.93 1.2 2.0

680 680 680 680

2210 740 860 740

3.1 3.1 2.8 3.4

3 3 3 3

0.99 0.97 0.98 0.91

0.32 0.32 0.36 0.29

TE2 NH4 MMA DMA TMA

1.8 2.5 3.1 4.7

0.60 1.8 1.9 3.4

660 660 660 660

3030 590 960 580

5.2 1.9 1.8 2.1

3 3 3 3

0.98 0.99 0.99 0.98

0.19 0.52 0.55 0.48

TE3 NH4 MMA DMA TMA

1.3 1.2 1.6 3.0

0.64 1.3 1.6 2.0

450 450 450 450

2300 – – 1100

3.6 2.2 2.9 2.7

3 4 3 3

0.92 0.98 0.96 0.99

0.28 0.46 0.35 0.37

TE4 NH4 MMA DMA TMA

1.6 1.3 1.8 2.5

0.73 1.6 2.2 3.7

430 430 430 430

2770 – – –

4.2 3.1 2.9 3.6

3 3 3 3

0.94 0.97 0.97 0.88

0.24 0.32 0.35 0.28

Sample

a Available particulate ammonia or MA concentration (w/v) is estimated as the product of the ammonia or MA concentration (w/w) in Table 1 and the SPM concentration (w/v). In experiments where the dissolved equilibrium concentration exceeds the maximum extracted by 2 M KCl, determination of KD was not possible.

3.6. Theoretical treatment of the desorption profiles 3.6.1. Desorption kinetics It was assumed that the desorption of NH4+ and the MAs is described by a first-order reversible mechanism (Millward and Liu, 2003), with the particulate 300

2000

200 150

-1

1000

MAs, nmol L ; SPM, mg L

-1

250 1500

NH4+, nmol L-1

re-adsorption of NH4+, declining to a plateau; a general phenomena also observed by Morin and Morse (1999). Typically, the plateaus in dissolved NH4+ concentrations for the July samples were obtained within 30 min. The [NH4+]D at equilibrium were higher in July (0.84– 1.40 μM; Table 2) than in November (0.52–0.73 μM; Table 3), when they were also confined to a narrower concentration range. The desorption of the MAs was slower than that of NH4+, such that maximum concentrations were not observed until about 1 hour (November samples) and there was no overshoot. For the July samples, the plateau concentrations were reached after several hours of incubation. Micro molar concentrations of the MAs were desorbed in each sample set and dissolved TMA was consistently the most abundant MA, followed by DMA and MMA, all of which had higher concentrations than NH4+(Tables 2 and 3). This result mirrored the order of abundance of measured sediment-exchangeable analytes (Fig. 2). The maximum concentration of dissolved MAs desorbed were at least an order of magnitude higher than [MA]D in the water column at TE3 during the tidal cycle.

100 50

500

0 -50

0 0

1

2

4 3 Time (h)

5

6

7

Fig. 3. Concentrations of SPM, dissolved NH+4 and total dissolved MAs over a tidal cycle at site TE3 (O = SPM; = NH+4; Δ = total MAs).

▪

20

July

(b)

(d) 4

1.5

3

3

3

1.0

0.5

2

1 Time, h

10

0 0.01

100

2

0.1

1

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0 0.01

100

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1

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0 0.01

(f)

(g)

3

3

3

1

0.0 0.01

0.1

1 Time, h

10

100

0 0.01

TMA, µ mol L -1

1.5

DMA, µ mol L -1

4

MMA, µmol L-1

2.0

0.5

2

1 Time, h

10

100

0 0.01

100

2

1

1

0.1

10

(h) 4

2

1 Time, h

4

1.0

0.1

Time, h

Time, h

(e) November

2

1

1

1

0.1

TMA, µmol L -1

4

DMA, µ mol L -1

4

MMA, µ mol L -1

2.0

0.0 0.01

Ammonia, µmol L-1

(c)

0.1

1 Time, h

10

100

0 0.01

0.1

1

10

100

Time, h

Fig. 4. Time dependent desorption of NH+4and MAs from Thames Estuary sediments collected at site TE1. July 2001 (a) NH+4, (b) MMA, (c) DMA and (d) TMA and November 2001 (e) NH+4 , (f) MMA, (g) DMA and (h) TMA. The filled circles are the observations and the line is the predicted time course derived from a first-order reversible mechanism.

M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

Ammonia, µmol L-1

(a)

(b)

0.5

0.0 0.01

4

3

3

3

2

1

0.1

1

10

0 0.01

100

November

0.1

10

DMA, µmol L -1

MMA, µmol L 1 Time, h

10

100

2

0 0.01

1 Time, h

10

0 0.01

100

1 Time, h

10

100

1 Time, h

10

100

1

10

100

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3

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0 0.01

2

1

1

0.1

0.1

(h)

3

1

0.1

0.1

4

-1

-1

0.5

2

1

(g)

3

1.0

0.0 0.01

0 0.01

100

4

1.5 Ammonia, µmol L

1 Time, h

(f)

2.0

2

1

Time, h

(e)

TMA, µmol L -1

1.0

4

-1

MMA, µmol L-1

1.5

4

0.1

1 Time, h

10

100

0 0.01

0.1

M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

Ammonia, µmol L -1

2.0

(d)

(c)

TMA, µmol L

July

DMA, µmol L-1

(a)

Time, h

Fig. 5. Time dependent desorption of NH+4 and MAs from Thames Estuary sediments collected at site TE3. July 2001 (a) NH+4, (b) MMA, (c) DMA and (d) TMA and November 2001 (e) NH+4, (f) MMA, (g) DMA and (h) TMA. The filled circles are the observations and the line is the predicted time course derived from a first-order reversible mechanism.

21

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M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

constituents, MAP, exchanging reversibly with the dissolved constituent, MAD,: MAp X MAD

ð1Þ

The desorption and adsorption rate constants are k− 1, and k1, respectively. The time-dependent concentration t of the dissolved constituent is given by [MA]D and the e equilibrium concentrations, [MA]D, were normally taken as the 48 h determination. Integration of the differential equations for reaction (1) gives: ½MAtD ¼ ½MAeD ð1−e−ðk1 þk−1 Þ*t Þ

ð2Þ

The chemical response time, τresp, for a first-order reversible reaction (i.e. the time to achieve 63% of the new equilibrium) is: sresp ¼

1 ðk1 þ k−1 Þ

ð3Þ

Values for (k1 + k− 1) were obtained from the slope of the line obtained by re-arranging Eq. (2) and plotting ln e e t ([MA]D / ([MA]D − [MA]D )) versus time. The values of τresp, and their respective linear regression coefficients are given in Tables 2 and 3. The reaction constant, (k1 + k− 1), was used in Eq. (2) to predict desorption as a function of time (Figs. 4 and 5). The mean τresp for the desorption of NH4+ from the July sediments was 15 min, whereas in November the rate of desorption was too rapid for quantitative analysis. For the MAs the mean τresp for July and November was 25 ± 5 min. 3.6.2. Partition coefficients The partition coefficients, KD (L kg− 1), for NH4+ and each MA in the sediments were derived as follows: KD ¼

½MAP ½MAD

ð4Þ

where [MA]P is the concentration of sediment-exchangeable MA and [MA]D is the pore-water MA concentration. The KDs for NH4+, in July and November, covered the range 25 to 100 L kg− 1, whereas the MAs had values from 9.7 × 103 to 2.6 × 105 L kg− 1 in July and 2.0– 4.6 × 103 L kg− 1 in November. The two sample sets for the MAs were found to be significantly different using ANOVA statistical tests (p b 0.05). The KDs for the compounds in the desorption experiments were estimated according to: KD ¼

½MAeP ð½MAP −½MAeD Þ ¼ ½MAeD *½SPM ½MAeD *½SPM

ð5Þ

where [MA]P is the initial concentration of sedimente exchangeable MA (μmol L− 1), [MA]D is the equilibrium concentration of dissolved MA, or NH4+(in μmol L− 1), [SPM] is the concentration of SPM (kg L− 1), [MA]Pe is the equilibrium concentration of particulate MA, or NH4+ (in μmol L− 1) and is obtained from the e mass balance (i.e. [MA]P − [MA]D ). The KDs for NH4+ in July and November were in the range 0.3–0.9 × 103 L kg− 1, whereas in November they ranged from 2.2– 3.0 × 103 L kg− 1. The KDs for the MAs in July varied over an order of magnitude from 0.1 × 103 to 2.1 × 103 L kg− 1 and in November from 0.6–1.1 × 103 L kg− 1. 4. Discussion 4.1. Partitioning of NH4+ and MAs by sediments and SPM In the sediments, the KDs of NH4+ were relatively low and values were slightly higher in July, mainly due to differences in [NH4+]D in the pore-waters (Fig. 6a). The KDs for the MAs were at least an order of magnitude higher than those for NH4+ and the KDs for July were significantly higher than those for November. The numerical difference between the KDs for NH4+ and those for the MAs may be explained by the higher pKb for the former which confers a greater tendency for it to desorb into solution. Differences in pKb do not explain why the MAs have higher KDs in July. Neither do variations in the grain size of the sediments, as a proxy for their surface area, clarify why there should be a significant increase in KD in July. One possibility is that, in July, the MAs may have been associated with recently deposited planktonic or flocculated material which had not degraded and had not had time to release MAs into solution. This may explain why the pore-water concentrations are relatively low in July and why, in November, as a consequence of less biological activity (Wang and Lee, 1994) the KDs were much lower and relatively constant. Within the MAs there was no systematic trend between KD and the degree of methylation, of the sort obtained by Fitzsimons et al. (2001) for sediments from a pristine estuary in SE England. The KDs from the Thames followed the sequence TMA N MMA N DMA in July and TMA ≈ DMA ≈ MMA in November. There appears to be no apparent effect on KD from the differences of pKb between the MAs, which might be related to the MAs desorbing from different particle types, alluded to above. The KDs for NH4+ and MAs estimated from the desorption experiments were clustered about a narrower range of values than for the sediments (Fig. 6b). The

M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

(a)

decrease in KDs, particularly for the July sediments, is unclear but may be related to the behaviour of planktonic or flocculated particles during resuspension. This hypothesis is speculative and emphasises the requirement for further investigations of the seasonal variability of sedimentary MA content and its exchangeability.

1000000

100000

-1

10000

KD, L kg

23

4.2. Sources of NH4+ and MAs during a tidal cycle

1000

100

10 0

2

4

6

8

+

[NH4 ]P or [MA]P, µmol g

10

12

10

12

-1

(b) 10000

KD, L kg

-1

1000

100

10 0

2

6

4 +

8

[NH4 ]P or [MA]P, µmol g

-1

Fig. 6. Partition coefficients, KD, for NH+4(э; !) and MAs (Δ; ▴) as a function of [MA]P (i.e. MA available to multiple extractions with 2 M KCl), where the open symbols are for July 2001 and the closed symbols are for November 2001. The MA data comprise all MAs at all sites. (a) sediments, where KD is estimated using Eq. (4) and (b) resuspended solids, where KD is estimated using Eq. (5).

KDs for NH4+ were generally an order of magnitude higher, with November being greater, and more constant, than July. The increased KD for the desorption experiments suggests that the remnant fraction of NH4+ on the particles was bound to higher energy sites and was, therefore, less exchangeable. As a consequence, e the [NH4+]D was relatively small because most of the sediment-exchangeable fraction had already desorbed into the pore-waters. In comparison, the KDs for the MAs were more than an order of magnitude lower than in the sediments. The November KDs were relatively constant and those for the July experiments show four data points with KD ∼100 L kg− 1 and three, all for TMA, with KD N 1000 L kg− 1. The reason for the sharp

During the tidal cycle [NH4+]D and [SPM] increased simultaneously. The [MA]D also increased but was more variable (Fig. 3). These results suggest that the N compounds had a common source, which was linked to the resuspension process. The [NH4+]D was always an order of magnitude greater than [MA]D, which mirrored their relative abundances in the pore-waters (Table 1). Thus, dissolved NH4+ and MAs from pore-waters could have been injected into the water column during the tidal inundation of the sediments (Caetano et al., 1997; Rocha, 1998). Estimates of the potential input of [NH4+]D and [MA]D from the sediments into the water column were made assuming (a) a uniform texture in the sediment column, (b) tidal shear mixed the sediments to a depth of 0.1 m and (c) the water column was well mixed during the tidal incursion. Taking a mean water content of 45% for the sediments, a mean [NH4+]D in pore-waters of 68 μmol L− 1 and a mean Σ[MA]D in pore-waters of 0.82 μmol L− 1 (i.e. the means of values in Table 1) then, to a first approximation, the total amounts of [NH4+]D and [MA]D available for input into the water column were 3 mmol m− 2 and 37 μmol m− 2, respectively. Since the average depth of water during high spring tide was about 5 m, the [NH4+]D and the Σ[MA]D were predicted to increase by ∼700 and ∼7 nmol L− 1, respectively, as a result of sediment pore-waters remobilised into a well-mixed water column. Thus, approximately 50% of the observed increase in [NH4+]D (Fig. 3) was predicted to originate from sediment pore-waters at TE3, a similar conclusion to that observed by Morin and Morse (1999) for the Laguna Madre. Measurements of [NH4+]D and exchangeable [NH4+]p in inter-tidal sediments from the Sado Estuary (Portugal) showed that an estimated 75% of the combined [NH4+]D and sediment-exchangeable [NH4+]P was exported to the water column during sediment flooding (Rocha, 1998), while another study in the Ria Formosa (Portugal) revealed that 64% of the sediment-exchangeable [NH4+]P was exported (Caetano et al., 1997). These data compare well with our prediction of 50%. In contrast, the predicted pore-water contribution for ΣMAs was b 10% of the peak concentration in

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M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

Fig. 3, suggesting that pore-waters were not the major MA source. Since adsorption of MMA, DMA and TMA to sediments is reversible (Wang and Lee, 1993), transport of pore-water and, more significantly, sediment-exchangeable MAs could occur during tidal inundation. Field and laboratory data indicate that NH4+ has a shorter residence time in estuarine sediments compared with freshwater sediments (Seitzinger et al., 1991; Gardner et al., 1991), due to competition for exchange sites from seawater cations and ion pairing of NH4+. Fitzsimons (1993) measured MA concentrations in Priest Pot, a eutrophic lake in the Lake District, UK, and observed low recoveries of the internal standard, CPA, during the extraction process. This was attributed to a large number of sediment exchange sites and a high TOC content of the sediments (e.g. Wang and Lee, 1990). 4.3. Desorption from resuspended sediments A significant fraction of the sediment-exchangeable pool of each MA was desorbed at equilibrium in the desorption experiments. The τresp values measured in this study show that the MAs, which are more basic than NH4+, desorbed more slowly from the sediments than NH4+. This result is consistent with studies of SPM from the River Amazon and its tributaries (Hedges et al., 1994, 2000; Aufdenkampe et al., 2001), which showed that basic amino acids adsorbed most strongly to fine particles of b 63 μm diameter. Thus, the sorption behaviour of the MAs may be representative of other ON compounds associating with the sediments by this mechanism. Our τresp for individual MAs did not correlate with their relative basicities. DMA, the most basic MA in aqueous solution (pKb 3.27) had the longest τresp of the MAs in July in two of the three samples. TMA (the least basic of the three in aqueous solution, with a pKb of 4.19) had the longest τresp in all of the November samples. Wang and Lee (1990) determined partition coefficients for MMA and TMA by adding 14C-labelled analytes to sediment slurries (DMA was not tested) and found that TMA adsorbed more strongly than MMA, which they attributed to TMA having a less soluble trigonal planar structure. The dissolved concentrations of each MA at equilibrium in the desorption experiments reflected their exchangeable concentrations, but the reasons for their different τresp are not clear from our data and require further investigation. The MAs exist as cations in seawater and can compete for exchange sites on the particles. An increase in [MA]D was observed in both the results from the multi-volume

extraction and the (time-dependent) desorption experiments. NH4+ behaved in an identical fashion, suggesting that ion exchange is the main mechanism desorbing MAs from the solid-phase. This is consistent with evidence showing that adsorption of MAs to sediments was reduced when they were dissolved in seawater rather than freshwater or deionized water (Wang and Lee, 1990). Desorption from resuspended particles may be considered as an additional source of dissolved MAs. For a typical SPM concentration of 500 mg L− 1, 1– 3 μmol L− 1 of an MA will be desorbed at equilibrium. The SPM concentration varied between 55 and 250 mg L− 1 during the tidal observations at TE3. Given the extents of desorption measured here the contribution to the enhanced MA concentrations in the water column could be in the range 110 to 1500 nmol L− 1. This calculation does not take account of advection and dilution from mixing between waters of different MA concentrations (or NH4+), nor is it possible to consider the consequences of any particle concentration effects (Turner and Millward, 2002). Equilibrium [MA]D measured in the desorption experiments were typically an order of magnitude greater than [MA]D measured in the water column at TE3. This result indicates that the SPM sampled at TE3 was depleted in MAs, possibly due to the particles having undergone previous cycles of resuspension (Schoellhamer, 1996) or the MAs having a shorter turnover time than NH4+. 4.4. Relative importance of pore-water injection and desorption Although inputs of pore-water NH4+ appeared to contribute to the increases in water column [NH4+]D during tidal incursions (Fig. 3), desorption from SPM may provide additional NH4+. Using the rationale above, desorption contributes 0.25 to 0.80 μmol L− 1 of [NH4+]D. The range of [NH4+]D in the Thames Estuary at Southend between January 2000 and December 2001, which coincided with our sampling campaigns, was 0.47–4.59 μmol L− 1 (average 1.79 μmol L− 1; Environment Agency, pers. comm.). However, the equilibrium [NH4+]D from the desorption experiments (the range was 0.52–1.40 μmol L− 1) may underestimate the contribution of desorbed NH4+ to the water column in this region of the estuary. Dissolved NH4+ is enhanced in estuarine sediments by DNRA which is stimulated by increases in salinity. Although the contribution of DNRA was not considered in this study, it was shown to be an important control on N dynamics in Texas estuaries (Gardner et al., 2006).

M.F. Fitzsimons et al. / Marine Chemistry 101 (2006) 12–26

Following sediment resuspension, desorbed MAs constituted a larger fraction of total dissolved N than NH4+ , although this finding was not reflected in the data from TE3 tidal cycle. Interestingly, the increase in [NH4+ ]D was coincident with the trend in SPM (Fig. 3), whereas the MAs were out of phase with SPM. One possibility is that the MAs were taken up preferentially by bacteria (Jørgensen et al., 1993). In the outer Thames Estuary, amino acids accounted for approximately 50% of the N taken up by bacteria (Middelburg and Nieuwenhuize, 2000). The turnover of amino acids, in the range 4.8 to 46 h, was rapid in comparison with inorganic N substrates. The time-dependent MA concentrations at TE3 varied over a comparable period. A greater percentage of net NH4+ produced in aerobic freshwater sediments appears to be nitrified and denitrified (80–100%), relative to marine sediments (40–60%) because of NH4+ desorption from the latter (Seitzinger et al., 1991). Bioavailable MAs are degraded to NH4+ in marine sediments (Kim et al., 2003), which can be further mineralized as mentioned above, so desorption may be an important mechanism retaining this form of N within an estuary. Our experiments indicated that sediment resuspension reduced the residence time of both NH4+ and the MAs in estuarine sediments, through desorption. We hypothesize that the exchangeable fraction of other ON cations will undergo similar sorption behaviour under the same conditions, with varying chemical response times. 5. Conclusions This study has shown that pore-water injection and desorption from resuspending particles combine to release NH4+ and MAs to the dissolved phase, with the latter process being more important for MAs. Specifically, the amount of sediment-exchangeable MAs considerably outweighed concentrations of the inorganic nutrient, NH4+ , in our inter-tidal samples. This trend, if replicated by other ON fractions, will have major consequences for the local and, potentially, global N cycle. Assuming that the behaviour of the MAs is representative of other basic ON compounds, we predict that they will also undergo desorption at variable rates and to variable extents depending on the chemical properties of the particles and water column conditions. This conclusion points to the need for more sorption studies to be conducted in estuarine waters so that the influence of solid-solution interactions may be incorporated into models of organic N cycling.

25

Acknowledgements We are grateful to Martin Attrill and Alan Tappin for discussions on the manuscript which also benefited considerably from the comments of Wayne Gardner and another reviewer. This work was co-financed by grants from Middlesex University and the Environment Agency (Thames Region), and supported, in part, by a grant from the Leverhulme Trust (F/00568/H), whose support we gratefully acknowledge. References Abril, G., Nogueira, M., Etcheber, H., Cabecadas, G., Lemaire, E., Brogueira, M.J., 2002. Behaviour of organic carbon in nine contrasting European estuaries. Estuar. Coast. Shelf Sci. 54, 241–262. Aufdenkampe, A.K., Hedges, J.I., Richey, J.E., Krusche, A.V., Llerena, C.A., 2001. Sorptive fractionation of dissolved organic nitrogen and amino acids onto fine sediments within the Amazon Basin. Limnol. Ocenogr. 46, 1921–1935. Burdige, D.J., Martens, C.S., 1988. Biogeochemical cycling in an organic-rich coastal marine basis. 10. The role of amino acids in sedimentary carbon and nitrogen cycling. Geochim. Cosmochim. Acta 52, 1571–1584. Caetano, M., Falcão, M., Vale, C., Bebianno, M.J., 1997. Tidal flushing of ammonium, iron and manganese from inter-tidal sediment pore waters. Mar. Chem. 58, 203–211. Clayden, J., Greeves, N., Warren, S., Wothers, P., 2001. Organic Chemistry. Oxford University Press. 1512 pp. Cowan, J.L.W., Boynton, W.R., 1996. Sediment-water oxygen and nutrient exchanges across the longitudinal axis of Chesapeake Bay: seasonal patterns, controlling factors and ecological significance. Estuaries 19, 562–580. Dal Pont, G., Hogan, M., Newell, B., 1974. Laboratory techniques in marine chemistry. II. Determination of ammonia in seawater and the preservation of samples of nitrate analysis. Commonwealth Sci. Indust. Res. Org. Div. Fish. Oceanogr. Rep. 55, 8 pp. Enoksson, V., 1993. Nutrient cycling by coastal sediments: effects of added algal material. Mar. Ecol. Prog. Ser. 92, 245–254. Fitzsimons, M.F., 1993. The geochemistry of the methylamines in recent marine and lacustrine sediments. PhD Dissertation, University of Liverpool, UK. Fitzsimons, M.F., Kamhi-Danon, B., Dawit, M., 2001. Distributions and adsorption of the methylamines in the inter-tidal sediments of an East Anglian estuary. Environ. Exp. Bot. 46, 225–236. Gardner, W.S., Seitzinger, S.P., Malczyk, J.M., 1991. The effects of sea salts on the forms of nitrogen released from estuarine and freshwater sediments: does ion pairing affect ammonium flux? Estuaries 14, 157–166. Gardner, W.S., McCarthy, M.J., An, S., Sobolev, D., Sell, K.S., Brock, D., 2006. Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnol. Oceanogr. 51, 558–568. Glibert, P.M., Magnien, R., Lomas, M.W., Alexander, J., Fan, C.K., Haramoto, E., Trice, M., Kana, T.M., 2001. Harmful algal blooms in the Chesapeake and coastal bays of Maryland, USA: comparison of 1997, 1998, and 1999 events. Estuaries 24, 875–883. Hedges, J.I., Cowie, G.L., Richey, J.E., Quay, P.D., Benner, R., Strom, M., Forsberg, B.R., 1994. Origins and processing of organic matter

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