Sediment-Water Column Coupling and the Fate of the Spring Phytoplankton Bloom in Loch Linnhe, a Scottish Fjordic Sea-loch. Sediment Processes and Sediment-Water Fluxes

Estuarine, Coastal and Shelf Science (1995) 41, 1–19

Sediment–Water Column Coupling and the Fate of the Spring Phytoplankton Bloom in Loch Linnhe, a Scottish Fjordic Sea-loch. Sediment Processes and Sediment–Water Fluxes

J. Overnell, A. Edwards, B. E. Grantham, S. M. Harvey, K. J. Jones, J. W. Leftley and D. J. Smallman NERC Dunstaffnage Marine Laboratory, P.O. Box 3, Oban, Argyll PA34 4AD, Scotland, U.K. Received 26 March 1993 and in revised form 22 June 1994

Keywords: nutrient flux; oxygen flux; sulphate reduction; manganese Sediment–water fluxes of oxygen and nutrients before and after the impact of the spring phytoplankton bloom were measured by core incubation experiments. Less than 10 days after the bloom had settled, chlorophyll was found down to a depth of 2 cm in the sediment. This rapid burial was probably due to mixing during resuspension events. There was some increase in oxygen uptake by the sediment after settlement of the bloom and a concomitant increase in the apparent oxygen diffusion coefficient; this latter increase may indicate a stimulation of bio-irrigation. There was a nitrate influx after settlement of the bloom, but no measurable efflux of ammonium or phosphate from the sediment. There was no increase of sulphate reduction activity after the impact of the bloom nor was solid-phase extractable manganese used as an alternative terminal electron acceptor for oxidation of carbon. We conclude that much of the readily biodegradable organic components of the bloom was mineralized in the water column during sediment resuspension events. ? 1995 Academic Press Limited

Introduction An understanding of the quantitative importance of sediment processes in the degradation of organic carbon is necessary to assess the degree of coupling between water column productivity and sediment mineralization. For this, estimates must be made of the sediment–water fluxes of both particulate and dissolved phases. Particulate fluxes may be measured with sediment traps. Direct estimates of fluxes of oxygen and dissolved nutrients have usually been made by one of two methods. First, fluxes have been measured in situ with benthic flux chambers, which have relatively large surface areas (~1 m2). Second, fluxes have been measured with cored samples in tubes with relatively small surface areas (~3#10 "3 m2). Indirect methods have been used, based on the calculation of fluxes from porewater gradients of dissolved components at the sediment 0272–7714/95/010001+19 $12.00/0

? 1995 Academic Press Limited

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surface and from their diffusion constants. However, the activities of macrobenthic infauna can greatly increase the fluxes over those calculated using a simple onedimensional model. Calculations accounting for the infaunal activities are both complicated and require additional information concerning the animals and their burrows (Aller, 1980). Differences between the directly measured and the calculated fluxes are frequently used to give an insight into the activities of the benthic fauna. The choice between in situ benthic flux chambers and flux measurements in core tubes is usually made on practical grounds. Although a benthic flux chamber may be preferable, the cost of acquisition and deployment of one suitable for working below a depth at which it can be serviced by dividers, is large. Such chambers are scarce, hence incubations in core tubes remain popular. Subsequent chemical analysis of the cores also enables valuable additional measurements to be made of sediment components. Cores were used in this work. It must be remembered, however, that enclosing a sample of water for flux measurements, either in a flux chamber or in a core tube, represents a non-natural state because the sediment is shielded from large water movements. We wished to measure coupling between phytoplankton productivity and remineralization. We report here measurements of sediment–water fluxes of oxygen and nutrients by laboratory incubation of sediment cores from one station in Loch Linnhe before, during and after the spring phytoplankton bloom and chemical measurement on the same cores, during the period February–June 1990. Materials and methods Study site The location of the study site, Loch Linnhe, is shown in Figure 1. All sediment samples were taken from station L14. Sampling and analysis Sediment samples Sediment samples were obtained at approximately weekly intervals between 12 February and 12 June 1990, using a damped gravity corer (Craib, 1965) which recovered cores with an undisturbed sediment–water interface. The samples were obtained in clear acrylic core tubes 24 cm long#5·9 cm (id.). The undisturbed cores were approximately 15 cm in length; any cores showing signs of disturbance were rejected. Macrofauna were not visible in the cores before or after the flux measurements, but if the core tubes were left unstirred, brittle stars were often seen, driven from their sediment by the anoxic conditions which developed. Cores subsequently found to have contained macrofauna were not excluded from the data set because it was considered important that the effect of the whole benthic community be evaluated. To measure sulphate reduction rate, porewater sulphate and porosity, modified core tubes (called ‘ spiral ’ core tubes) were used: these tubes had 1·4 cm diameter holes vertically spaced 1·5 cm apart, arranged in a spiral pattern and sealed with adhesive tape, to allow subsampling down the core. To measure sulphate reduction rate, sediment subsamples were taken on board ship immediately after coring using the sampling protocols below. These subsamples were stored on ice or at 10 )C (see below). For oxygen uptake and nutrient flux experiments, standard core tubes were used. After sampling, the core tubes were sealed at both ends with rubber bungs, packed in ice

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Figure 1. Geographical location of the study site. Depths shown in metres.

and returned to the laboratory within a few hours of sampling. Cores were pre-incubated overnight in the dark without the top bung, submerged in a tank of recirculating aerated seawater at 10 )C. Additional stirring above each tube ensured equilibration with the circulating seawater down to the sediment surface. The seawater used in the tank was taken from about 10 m above the sea-bed at the same station as the cores. Cores to be analysed for porewater nutrients and solid-phase components were held overnight in a refrigerator at 4 )C in the dark. Cores were then extruded and sectioned into short cylinders to give samples from 0–0·5, 0·5–1, 1–1·5, 1·5–2, 2–3, 3–4 and 4–6 cm below the sediment surface. Sediment sectioning and porewater extraction were carried out under a stream of oxygen-free nitrogen. The porewater was separated by centrifugation of the appropriate section of sediment core at 3000 g for 10 min in tubes filled with nitrogen and the supernatant was filtered (Whatman GF/F). The sediment pellet was frozen and lyophilized and stored at room temperature. To determine sulphate reduction rate, porewater sulphate and porosity, subsamples of sediment were taken from the ‘ spiral ’ core tubes via the sampling ports using 5-ml syringes which had been cut off at the Luer end. This provided four samples taken from

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0·7–5·2 cm below the surface at 1·5 cm intervals. Samples for sulphate reduction determination were capped immediately with a butyl rubber Suba-seal and stored in an oxygen-free atmosphere at 10 )C. Determination of carbon and nitrogen Analysis of particulate carbon and nitrogen contents of the lyophilized samples was by the Dumas method using a Leco CHN 900 elemental analyser and acetanilide for calibration. Combustion was at 950 )C with 10 ml of oxygen in a helium carrier. Determination of nutrient concentrations from incubation experiments and in porewater Analysis of overlying water samples and samples from incubation experiments was carried out using a Technicon autoanalyser for phosphate and silicate (Grasshoff, 1976) and for nitrate+nitrite (Folkard, 1978). Insufficient volumes of porewater were available for analysis of nitrate on the autoanalyser, which also had insufficient sensitivity after dilution of the sample. Nitrate was therefore measured in porewater by means of ion chromatography (Dionex, with uv detection at 215 nm, Ionpac CS5 separating column, running buffer 40 mM NaCl, flow rate 2 ml min "1) after dilution of the seawater sample 1]10 with distilled water. The method used was a modification of Anonymous (1987). Porewater samples were measured after appropriate dilution with nutrient-free artificial seawater (autoanalyser) or distilled water (ion chromatography). Porewater sulphate Porewater samples were diluted 100# with distilled water and the sulphate concentration was measured by means of ion chromatography, using a Dionex System 14 ion chromatograph with conductivity detection, AS4A separating column, running buffer 0·75 mM NaHCO3, 2 mM Na2CO3 and flow rate 4 ml min "1 (Parkes & Buckingham, 1986). Sediment porosity and content of organic matter Porosity was determined by weight loss after lyophilization and organic matter content by weight loss after ashing at 450 )C for 24 h. Solid-phase manganese Extraction of lyophilized sediment for determination of manganese was carried out at room temperature with 1 M hydroxylamine HCl, 25% acetic acid (Chester & Hughes, 1967). Manganese concentrations were measured by flame atomic absorption after appropriate dilution against standards (BDH) diluted in 0·1 N HCl. There was no matrix effect at the minimum dilution. Oxygen concentrations Oxygen concentration was measured by Winkler titration with potentiometric detection of the end point (Parkes & Buckingham, 1986). Oxygen concentration in sediment porewater Interstitial water immediately below the sediment–water interface was squeezed from the sediment in its core tube with an apparatus constructed according to Bender et al. (1987). Effective depths of sampling were calculated by dividing the measured depth on the screw thread by the average porosity of the top 1·5 cm.

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Incubations for measurement of nutrients and oxygen Incubations for nutrient determinations were made initially in triplicate, and from 7 May (day 127) in quintuplicate. Incubations to determine oxygen uptake rates were only made in triplicate. Fluxes were determined by measuring the changes in concentration of stirred seawater in contact with sediment. At time zero, the core tubes were fitted with submersible stirrers, described by Parkes and Buckingham (1986), enclosing seawater about 12 cm high above the sediment. The stirring speed was adjusted so that fine material of the sediment surface was not just resuspended. Overlying water samples (~11 ml) were taken in glass syringes for measurement of oxygen at 6 and (for the first half of the experimental period) 24 h. After the last sample was taken for oxygen determination, 20 ml of air were introduced and incubation was continued for measurement of nutrient fluxes. The air was necessary to maintain the oxygen concentration in the water to avoid nutrient flux rate changes consequent on depletion of oxygen (Cerco, 1989; Koop et al., 1990). Samples for nutrient determinations (~20 ml) were taken at 1, 2 and 3 days, filtered through Whatman GF/F papers and stored at "20 )C for about 6 months before analysis. The height of the water column above the sediment was measured before each sample was taken. Although oxygen fluxes could readily be measured during a period of 6 h, fluxes of nutrients were often small and incubation had to be extended to days in order to observe measurable changes. The measured concentrations of nutrients were normalized to a water height of 10 cm thus: Cni =Cn(i"1) +(Ci "C(i"1)) #hi /10

(1)

where Cni is the normalized concentration after the ith sampling; Ci is the measured concentration at the ith sampling; and hi is the height of water before the ith sampling. Flux rates were determined from the slope of the best fit regression of nutrient concentration on time. Data sets where the points did not fall on a smooth curve were not used. Fluxes of both phosphate and nitrate were sometimes non-linear as a function of time and the concentrations in the water appeared to approach an asymptote. In these cases the initial rate was estimated by fitting the data to an equation of the form C=C0 +A (1"e "t/ô), where C is concentration at time t; C0, concentration at time 0; C0 +A, asymptomatic concentration; t, time; ô, time constant; and initial rate=1/ô.

Calculation of apparent oxygen diffusion coefficients and of oxygen fluxes from sediment porewater concentration profiles Apparent sediment diffusion coefficients for oxygen were calculated from the oxygen flux (measured with core incubations) and the oxygen gradient at the surface (calculated from the oxygen depth profile) using Fick’s first law of diffusion (Berner, 1980): J=ÖDs(äO2/ äz)z=0

(2)

where J is flux (mmol cm "2 day "1), Ö is porosity (dimensionless), Ds is sediment diffusion coefficient (cm2 day "1), (äO2/äz)z=0 is the oxygen gradient at the surface of the sediment (mmol cm "4) and z is the depth (cm). The oxygen gradient at the sediment surface was calculated from the depth profile as described in Results: oxygen penetration.

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1·5

–1

Chlorophyll (µg ml )

2·0

1·0

0·5

0·0

50

75

125 100 Julian day

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Figure 2. Sediment chlorophyll concentration as a function of time. -, 0–0·5 cm; /, 0·5–1·0 cm; ;, 1·0–1·5 cm; 4, 1·5–2·0 cm.

Calculations of theoretical oxygen fluxes were based on the bulk diffusion coefficient, D0, of oxygen in water at 10 )C of 1·57#10 "5 cm2 s "1 (Broecker & Peng, 1974) and the empirical expression Ds =D0 Ö2 (Ullman & Aller, 1982). Sulphate reduction rates Rates of sulphate reduction were determined by the method of Parkes and Buckingham (1986) in which rates of incorporation of 35S into acid volatile sulphide (AVS) were determined first, followed by determination of rates to pyrite volatile sulphide (PVS), with the following modifications: (1) after injection of 35SO42" the subsamples were incubated for 24 h at 11 )C, (2) deoxygenated distilled water was used instead of 50% seawater at the AVS releasing stage, (3) during PVS release the reaction vessel was heated to 100 )C and (4) during both stages the released H2S was trapped in 10 ml of 10% zinc acetate. Results Changes in the chemistry of the sediments with time Chlorophyll Chlorophyll sedimentation was measured using gimballed sediment traps with an aspect 10:1 ratio (Leftley & MacDougall, 1991) and chlorophyll extracted and measured as described by Tett (1982). Chlorophyll sedimentation peaked on 8 May at a rate of 7·7 mg m "2 day "1 at 60 m, with rates for the week before and the week after of only half this value. On 30 April the chlorophyll concentration in the top 0·5 cm of sediment (at 120 m depth) was still at the background winter value (Figure 2) but it peaked 7 days later. The total sedimentation of chlorophyll at 60 m depth in the water column over the period of the bloom (26 April–15 May) was 115 mg m "2. The sedimentation at 60 m,

Sediment–water column coupling

Manganese (mg 100 g–1)

120

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Figure 3. Extractable manganese concentration in 0–5 mm sediment depth interval as a function of time. Single measurements.

measured over 8 days in the traps recovered on 8 May was 62 mg m "2 and the weight of chlorophyll in the top 0·5 cm of sediment on 7 May was 97 mg m "2. Complete correspondence of these values is not expected for a variety of reasons, but the rough equivalence between the amounts of sedimenting chlorophyll measured in the traps and in the sediment constitutes a useful internal check. Within 10 days of the appearance of the chlorophyll in the 0–0·5 cm depth interval (Figure 2), substantial quantities had apparently been passed down through the sediment to 1·5–2·0 cm depth. This probably represents the effects of resuspension caused by the inflowing gravity currents that were renewing bottom water around this time. Vigorous tidally-induced resuspension was reported for this station in 1991 (Overnell & Young, 1995). Extractable solid-phase manganese Extractable manganese concentrations in the top 0·5 cm of sediment were relatively constant at c. 80 mg 100 g "1 (dry weight) (Figure 3). There was no change following the impact of phytoplankton chlorophyll on 7 May. Porewater silicate The concentration of porewater silicate in the top 0·5 cm of sediment was low at the end of February and beginning of March (Figure 4) and, thereafter, values fluctuated wildly. Low values at c. 20-day intervals did not correspond to the predicted spring tides at c. 15-day intervals. Porewater nitrate During March and April the concentration of porewater nitrate in the topmost 0·5 cm of the sediment was lower than that in the overlying water. The concentrations of porewater nitrate declined with depth during this period. (Since nitrate is an electron acceptor that is utilized by sediment bacteria after oxygen has been depleted; under

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400

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Silicate (µM)

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Figure 4. Porewater silicate concentration in 0–5-mm sediment depth interval as a function of time. Single determinations.

steady-state conditions its concentration in porewater declines with depth). On 30 April at the very start of the impact of the bloom of the sediment, the measured concentration of nitrate in porewater in the 0–0·5 cm depth interval had increased to a value of 13 ìM which was higher than that in the overlying water (9·5 ìM). On the next sampling date, 7 May, the nitrate had dropped below the level of detection. This corresponded to the time of arrival of the bulk of the phytoplankton debris. Three weeks later the concentration of nitrate in the 0·5–1·0 cm depth interval also decreased to a very low value (Figure 12). Sulphate reduction rate Total sulphate reduction rates (AVS+PVS) measured at an effective depth of 0·75 cm (Figure 5), showed no increase after the impact of the phytoplankton chlorophyll (7 May). A value of approximately 10 nmol ml "1 day "1 would be typical. All rates of sulphate reduction measured from 2·2 to 6·0 cm depth (not illustrated) were of similar magnitude and again showed no signal with time. Oxygen penetration The oxygen concentration in porewater at the top of the cores decreased approximately exponentially with effective depth for the first part of the squeeze (in most cases until oxygen had decreased to c. 80% of saturation, i.e. down to c. 5–9 mm before the impact of the bloom and 4–5 mm after). The data were fitted using a linear regression of the logarithmically transformed concentration data on effective depth. This regression yielded a 50% oxygen penetration depth and the oxygen gradient at the surface. This procedure maximized the number of data points used. Linear fitting of the topmost data points to determine oxygen gradient (Reimers & Smith, 1986), however, gave similar values. The 50% oxygen penetration depth values are presented in Figure 6. The oxygen penetration is less for the days following the impact of the spring bloom (7 May) compared with the measurements in the 4 weeks preceding the impact. The decrease,

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Sulphate reduction (nmol ml–1 day–1)

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Figure 5. Sulphate reduction rates to AVS+PVS as a function of time, measured using samples taken from an effective depth of 0·75 cm below the sediment surface. Points are means of three measurements and bars SD.

Oxygen depth (mm)

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Figure 6. Fifty percent oxygen penetration depths into sediment as a function of time, determined from oxygen depth profiles. Points are means of two determinations or single measurements.

from a mean value of 2·4 to 1·6 mm was significant at a 0·01 probability level on the basis of a two-tailed t-test (14 degrees of freedom).

Flux measurements Bottom water temperatures were 9·5 )C in February; they dropped to 8·0 )C at the end of April and rose to 10·0 )C at the beginning of June. All flux measurements were measured at constant temperature (10·0 )C).

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Figure 7. Sediment–water flux of oxygen as a function of time, determined by measurement of changes in oxygen concentration by Winkler titration of water sampled from incubation experiments. Points represent means of three measurements and bars represent SD. Negative values represent flux from water to sediment.

Oxygen The fluxes were measured at a single stirring speed and a linear uptake was assumed for the first 6 h, following Parkes and Buckingham (1986) who found little or no difference between oxygen uptake rates at fast and slow speeds using the same apparatus. Davies (1975) found little effect of stirring speed on oxygen uptake so long as the flocculent surface material was not resuspended; if it was, there was a notable increase. Oxygen uptake experiments in benthic flux chambers showed that oxygen uptake was linear with time and decreased exponentially only below c. 100 ìM oxygen (Hall et al., 1989). Over the first 6 h in our work the oxygen concentration decreased typically from 310 to 250 ìM and end-point concentrations as low as 100 ìM were only recorded after 24 h incubation. Oxygen flux showed an increase starting with samples recovered on 30 April (Figure 7). The mean flux measured from 26 February to 20 April was "10·3 mmol m "2 day "1 and from 30 April to 20 June was "18·4 mmol m "2 day "1. The increase was significant at a 0·01 probability level on the basis of a two-tailed t-test (40 degrees of freedom). Nutrients Ammonium fluxes (Figure 8) were small and showed much individual variation. There was no evidence of an increased efflux of ammonium following the impact of the phytoplankton (7 May). Nitrate (Figure 9) showed a period of efflux during March, followed by influx during April and May and again efflux during June. The highest influx measured occurred on 7 May, the date of the highest chlorophyll content of the sediment. Phosphate fluxes (Figure 10) displayed the same general behaviour with time as nitrate fluxes (efflux followed by influx followed by efflux). In this case, however, the individual variation between measurements was larger, and hence any conclusions are less secure.

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Ammonium flux (mmol m–2 day–1)

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Figure 8. Sediment–water flux of ammonium as a function of time, determined by measurement of changes in ammonium concentration of water sampled from incubation experiments. Points are means of three to five measurements and bars represent SD.

Nitrate flux (mmol m–2 day–1)

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Figure 9. Sediment–water flux of nitrate as a function of time, determined by measurement of changes in nitrate concentration of water sampled from incubation experiments. Points are means of three to five measurements and bars represent SD.

Silicate fluxes (Figure 11) showed a dramatic and significant change from a mean efflux before the bloom of 0·36 mmol m "2 day "1 to a mean efflux of 2·58 mmol m "2 day "1 after 30 April and the impact of the bloom. Discussion Sediment–water fluxes and estimation of expected values To interpret the values of the measured fluxes, some approximate predictive calculations have been made for Loch Linnhe. Since the aim of this paper was to study the coupling

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Phosphate flux (mmol m–2 day–1)

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Figure 10. Sediment–water flux of phosphate as a function of time, determined by measurement of changes in phosphate concentration of water sampled from incubation experiments. Data points are means of three to five measurements and bars represent SD.

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Figure 11. Sediment–water flux of silicate as a function of time, determined by measurement of changes in silicate concentration of water sampled from incubation experiments. Data points are means of three to five measurements and bars represent SD.

of primary production and sediment processes, estimates were needed of the input of phytoplankton carbon and other nutrients. Inputs of terriginous material have been ignored because they were assumed to be poor in nutrients and not readily biodegradable. The total phytoplankton chlorophyll settling out from 60 m (from 26 April–15 May) was 115 mg m "2. If assumed to have settled to the benthos, it may be used to estimate the carbon input. Sediment trap samples, even at 20 m, always contained non-algal particulates as a result of resuspension (Overnell & Young, 1995), so that measured ratios of carbon to chlorophyll were often very high. The minimum ratio obtained at the height of the bloom was 96. Therefore, published data were used on the composition of a diatom bloom after nitrate had become depleted (Antia et al., 1963).

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T 1. Sediment–water fluxes of oxygen. Negative values indicate flux into the sediment Flux (mmol m "2 day "1)

Temperature ()C)

"10·3 to "18·4 "13·6 to "17·8

10 10·5–11

"24·6 to "17·8

12–8·5

"4·7 to "18·7

7–11·5

"5·3 to "10·8

6–10

Location

Reference

Loch Linnhe Loch Etive (various stations) Loch Eil (various stations) Loch Thurnaig (annual cycle) Fanafjorden (annual cycle)

Present study Parkes and Buckingham, 1986 Parkes and Buckingham, 1986 Davies, 1975 Wassmann, 1984

Remineralization of phytoplankton carbon was assumed complete in 30 days at 10 )C (on the basis of other studies, e.g. Jensen et al., 1990) and the following chemical ratios assumed (Antia et al., 1953): carbon to chlorophyll weight ratio of 49, carbon to silicon molar ratio of 2·7, carbon to phosphorus molar ratio of 95·6. A respiratory quotient of 0·85 (Wassmann, 1984) was used to convert oxygen uptake to carbon consumed. On this basis the following fluxes might have been expected: an increase in the oxygen influx of c. "18·4 mmol m "2 day "1 in silicate efflux of c. 5·8 mmol m "2 day "1 and a phosphorus efflux of c. 0·16 mmol m "2 day "1 over a period of 30 days consequent on the remineralization of the bloom. The estimated phytoplankton input was 5·64 g C m "2 (469 mmol C m "2). This is somewhat less than the experimental loading rate (8·23 g C m "2) used by Hansen and Blackburn (1992). To interpret our results we ask: how do the fluxes measured in Loch Linnhe compare with these predicted fluxes and with those measured in incubation experiments (Hansen & Blackburn, 1992) and with field measurements at other sites? The measured oxygen flux increased from "10·3 to "18·4 mmol m "2 day "1 (Figure 7) following the bloom. The change was less than the predicted change ("18·4 mmol m "2 day "1) and was about half the increase measured by Hansen and Blackburn (1992) in laboratory experiments with the diatom Dithylum brightwelii, in which the transient oxygen uptake lasted only c. 10-days at 15 )C. The discrepancy could be due to a combination of two effects. First, there could be less biodegradable phytoplankton carbon in the sediment than assumed (see below). Second, chlorophyll and its associated carbon may have been rapidly buried below the depth of oxygen penetration (Figure 2), and hence the effect on fluxes could be delayed for longer than the assumed 30 days. The measured oxygen fluxes are compared with other measured fluxes in analogous locations in Table 1. Thus although lower than expected, the oxygen fluxes found here were in the general range found for sea-lochs/fjords. Oxygen fluxes calculated from the measured oxygen gradient and the bulk diffusivity of oxygen were "5·64 and "7·19 mmol m "2 day "1 before and after the impact of the bloom and the corresponding apparent oxygen sediment diffusion coefficients calculated from the measured fluxes and the measured oxygen gradient were 1·65 and 2·31 cm2 day "1. The calculated fluxes are less than those measured directly (Table 1). The difference between observed and calculated is probably attributable to irrigational water currents in the sediment induced by the benthic infauna. The apparent diffusion

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Porewater nitrate (µM)

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Figure 12. Porewater nitrate concentration as a function of time and at different depths. -, 0–0·5 cm; /, 0·5–1·0 cm; ;, 1·0–1·5 cm; 4, 1·5–2·0 cm.

coefficients are smaller than those found by Hofman et al. (1991) for some Dutch intertidal sediments (3·07–8·95 cm2 day "1) but higher than values of 0·89– 0·97 cm2 day "1 found for stations in the Laurentian Trough (Silverberg et al., 1987) and 0·85–1·07 cm2 day "1 in the deep ocean (Reiimers & Smith, 1986). The differences in apparent sediment diffusion constants are similarly a measure of bio-irrigation. Clearly, one of the effects of the impact of the bloom in Loch Linnhe on oxygen dynamics was an increase in bio-irrigation of the sediments. Ammonium fluxes (Figure 8) were small and there was no evidence of enhanced efflux of ammonium following settlement of the spring bloom. This is in contrast with Loch Thurnaig (Davies, 1975) and Aarhus Bight (Jensen et al., 1990) and with the laboratory experiments using Aarhus Bight sediments (Hansen & Blackburn, 1992) where transient ammonium effluxes of 1·2–2·2 mmol m "2 day "1 were observed. There was a large variation in ammonium fluxes between replicate cores in our incubations experiments. Large variation between replicates, particularly of ammonium, were also found by Pomroy et al. (1983). This variation could have been due to the random capture of large macrofauna in the core tubes. The flux of nitrate (Figure 9) changed from efflux to influx, roughly at the time of the phytoplankton bloom, then reverted to efflux, suggesting that outside the bloom period, efflux may prevail. This change in direction may be analogous to those found by Jensen et al. (1990) of 0·3 mmol m "2 day "1 before to "0·8 mmol m "2 day "1 after, and by Hansen and Blackburn (1992) of 1·0 mmol m "2 day "1 before to "0·4 mmol m "2 day "1 after the arrival of the phytoplankton. The change in direction of the nitrate flux coincided with the dramatic loss of all detectable nitrate in the top 0·5 cm of sediment on 7 May (Figure 12). Clearly, impact of chlorophyll in the sediment corresponded with a nitrate demand. In the Aarhus Bay study a good correlation between nitrate flux and overlying water nitrate concentration was found and ascribed to nitrate uptake and denitrification by the

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sediment. Sediment nitrification was concomitantly decreased due to reduced oxygen penetration, nitrate functioning as a terminal electron acceptor (oxidizing agent). Jensen et al. (1990) ascribed the ammonium efflux to rapid mineralization of a labile organic nitrogen pool, coupled with the reduced nitrification. In the Loch Linnhe sediments there appears to have been a small uptake of nitrate (Figure 9) without the release of ammonium (Figure 8). A possible explanation is the coupling of released ammonium with ammonium/nitrate denitrification. An alternative explanation may be that little available nitrogen reached the sediment (due to mineralization in the water column; see below) and what little was released from the labile organic nitrogen pool in phytoplankton was directly assimilated by the growing population of microorganisms. These growing microorganisms would also remove nitrate from the bottom water by assimilatory nitrate reduction, assuming that the feeding microorganisms have a greater nitrogen requirement than the phytoplankton debris can provide. This would generally be the case for bacteria. It also implies that the sediments represent a lesser sink for nitrogen than if the coupled denitrification were occurring. Clearly tight budgeting for nitrogen and direct measurement of denitrification are required. In a study of Carmarthen Bay, Pomroy et al. (1983) found release of both nitrate and ammonium with greatest release of ammonium in August and nitrate in October. At a 2-km deep station in the San Clemente Basin, Bender et al. (1989) found an influx of nitrate to the sediment and no net ammonium flux. A net nitrate uptake was calculated by Christensen et al. (1987) for continental shelf sediments and this was also found in shelf sediments by many authors cited therein. The phosphorus flux measured here (Figure 10) rises to only c. 0·02 mmol m "2 day "1 after the settlement of the bloom. The flux expected here from mineralization of the bloom over 30 days was 0·16 mmol m "2 day "1. However, Aller (1980) showed that mineralization of phosphorus is faster than that of nitrogen and so the predicted efflux maximum should have been sooner and greater. Balzer et al. (1987) measured porewater phosphate in the top 0–2 cm of sediment on a seasonal basis in the Kiel Bight and found a peak lasting less than a month at the end of May and beginning of June. The question then arises: why was a flux of phosphate of the expected magnitude not observed in Loch Linnhe? There are two possible (complementary) explanations. Either the assumed phosphorus may not have been present because of water column mineralization (see below), or that which was mineralized in the sediment may not have been released. In the presence of a surface oxidizing layer, the overlying phosphate appears to be in equilibrium with surficial sediment-bound phosphate (Einsele, 1938) and phosphate moves in or out of the sediments depending on its seawater concentration (Cerco, 1989). Caraco et al. (1989) have shown that for phytoplankton input into marine sediments the ratio of phosphate released to the water column to carbon consumed was very similar to the ratio of phosphorus to carbon in the original phytoplankton. We conclude that the apparent lack of a phosphate flux found here is probably not due to a high buffering capacity of the sediment, but rather that little easily degradable bound phosphate reached the sediment. In contrast to the other nutrients, silicate efflux increased dramatically after the impact of the bloom (Figure 11). The mean of 2·58 mmol m "2 day "1 after the bloom was less than the value of 5·8 mmol m "2 day "1 predicted on the basis of a 30-day mineralization, although predictions are a little uncertain since C:Si ratios are rather variable (Antia et al., 1963). In this case the assumption of 30 days for the mineralization is probably not well founded. Kamatani and Riley (1979) have measured dissolution rates

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of untreated cells of Thalassiosira in the dark in seawater at 30 )C. If we assume a Q10 of 2 then their decay rate would yield a time constant of 104 days. These authors estimated dissolution rates in sediment from porewater silica profiles in the Bering Sea assuming a range of sedimentation rates. These rates yielded time constants of 1·5–6#106 days. Time constants of between 55 and 110 days were calculated by Officer and Ryther (1980). Rates of silica dissolution from the diatom frustules could not be estimated from our data, but the process must be much slower than release of ammonium. Slow release of silicate implies that significant quantities of diatom frustules become permanently buried, thus further lowering the expected fluxes. Silicate concentrations in porewater from the 0–5 mm depth interval (Figure 4) show increasing oscillations with time, a feature which is not readily explainable, but which precluded calculation of fluxes from the diffusion constant. Comparison of sulphate reduction rates with expected values Interpretation of the small sulphate reduction rates measured at the 0·75 cm depth horizon (c. 10 nmol ml "1 day "1) and of the lack of seasonal signal associated with the settlement of the bloom (Figure 5), requires comparison with some estimate of the expected magnitude of the process. From Figure 2, the chlorophyll concentration at the 0·7 cm horizon was c. 12 ìg ml "1 on 14 May. Using a carbon to chlorophyll ratio of 49 and assuming that 50% of the associated carbon was mineralized via sulphate reduction in 1 month, then we might have expected an increase in sulphate reduction rate to 403 nmol ml "1 day "1 for a month. Such a predicted rate is not unreasonable and higher rates have been reported for surface sediments of Aarhus Bay during September, that is, well after the impact of a spring bloom (Troelsen & Jørgensen, 1981). Loch Linnhe sediments were anaerobic at the depth of measurement and the sulphate reduction rate was similar to that taking place at greater depths in the sediment, therefore inhibition of sulphate reduction by oxygen at the topmost horizon was not the reason for the discrepancy. One reason for the lack of a seasonal signal in the sulphate reduction rates might be that solid-phase manganese(IV) was the terminal electron acceptor for oxidation of carbon rather than sulphate. This role for solid-phase manganese has been deduced for sediments of the Panama Basin (Aller, 1990). The extractable solid-phase manganese found in Loch Linnhe in the top 0·5 cm of sediment [80 mg (100 g) "1), 1·45 mmol (100 g) "1] could, on stoichiometric grounds, oxidize c. 0·009%, 0·73 mmol (100 g) "1 carbon in the sediment (assuming Mn in valence state IV and carbon as carbohydrate). The chlorophyll concentration in the top 0·5 cm of the sediment column (19·4 ìg ml "1 on 7 May) would correspond to c. 0·20%, 16·8 mmol (100 g) "1 of phytoplankton carbon in the sediment. Clearly, extractable manganese had the potential to oxidize only a small fraction of the expected phytoplankton carbon and in any case extractable manganese did not diminish as a result of the impact of the bloom. It therefore cannot account for the lack of seasonality in sulphate reduction rate. We conclude either that solid-phase extractable manganese was not an alternative electron acceptor or that no biodegradable phytoplankton carbon had in fact reached the sediment (or both). We propose that the lack of a seasonal signal was due to vigorous resuspension that kept the topmost layer of sediment and the phytoplankton debris resuspended in the water column long enough for the most of the readily biodegradable carbon associated with the settled phytoplankton to be mineralized in the water column. Vigorous resuspension is known to occur in upper Loch Linnhe (Overnell & Young, 1995)

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although it was not possible in that work to estimate what depth of sediment the resuspension events affected. Thus the chlorophyll measured in the sediment would represent a marker not associated with readily biodegradable carbon. This marker might represent chlorophyll in diatom resting stages which are known to form at the end of a bloom during mass sinking (Smetacek, 1985). Resuspension events would ensure their rapid burial and explain why microscopical examination never showed diatoms on the sediment surface. Sedimenting chlorophyll is known to be relatively stable in reducing sediments, but less so in more oxidized sediments (Tett, 1982), thus giving rise to a modest increase in oxygen uptake at the sediment surface at the end of the bloom but no increase in sulphate reduction activity (which requires anaerobic conditions). Mineralization of the resting stages while resuspended in the water column by grazing or bacterial attack would lead to the observed decrease in sediment chlorophyll with time. Conclusions The key to understanding the impact of the bloom on the subsequent sediment processes in Upper Loch Linnhe is the lack of effect on the sulphate reduction rates in the top 1·4 cm of sediment even though ample phytoplankton carbon had settled from the water column and the concentration of chlorophyll in the sediment implied ample carbon. This means that the anaerobic heterotrophic bacteria associated with the sulphatereducing bacteria were not being provided with a pulse of biodegradable carbon that they were able to process. This carbon, together with fixed nitrogen and phosphorus, must have already been removed by aerobic bacteria while the plankton debris and resuspended sediment were together in the water column. The chlorophyll measured in the sediment may represent diatom resting stages from the bloom. Resuspension is a feature of this loch and it is due to bottom currents which are the result of both gravity currents of dense water associated with bottom water renewal and tidally-driven internal waves giving rise to seiching currents (Gade & Edwards, 1980; Overnell & Young, 1995). Since it is known that nitrogen and phosphorus are mineralized preferentially to carbon, these too would also have been largely lost in the water column and therefore they did not appear as ammonium and phosphate sediment–water fluxes. If a major part of the remineralization of phytoplankton debris in a sea-loch occurs in the water column during resuspension it is likely that a similar state of affairs occurs in many shelf sites where exposure is greater. Thus measurement of sediment–water fluxes under quiet conditions will give misleading indications of remineralization rates. Acknowledgements We thank the master, Mr G. Harries, and the crew of the RV Calanus for their assistance with the sample collection. We thank an anonymous referee for useful suggestions. References Aller, R. C. 1980 Diagenic processes near the sediment–water interface of Long Island Sound. I. Decomposition and nutrient element geochemistry (S, N, P). Advances in Geophysics 22, 237–350. Aller, R. C. 1990 Bioturbation and manganese cycling in hemipelagic sediments. Philosophical Transactions of the Royal Society of London Series A 331, 51–68. Anonymous 1987 Determination of nitrite, nitrate and ammonia in KCL soil extracts. Dionex Application Update AU118-A, 1–2.

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Antia, N. J., McAllister, C. D., Parsons, T. R., Stephens, K. & Strickland, J. D. H. 1963 Further measurements of primary production using a large-volume plastic sphere. Limnology and Oceanography 8, 166–183. Balzer, W., Erlenkeuser, M., Hartmann, M., Moller, P. J. & Pollehne, F. 1987 Diagenesis and exchange processes at the benthic boundary. In Seawater–Sediment Interactions in Coastal Waters: An Interdisciplinary Approach (Rumohr, J., Walger, E. & Zeitschel, B., eds). Springer-Verlag, Berlin, 111–161 pp. Bender, M., Martin, W., Hess, J., Sayles, F., Ball, L. & Lambert, C. 1987 A whole-core squeezer for interfacial pore-water sampling. Limnology & Oceanography 32, 1214–1225. Bender, M., Jahnke, R., Weiss, R. M., Martin, W. H., Heggie, D. T., Orchardo, J. & Sowers, T. 1989 Organic carbon oxidation and benthic nitrogen and silicate dynamics in San Clemente basin, a continental borderland site. Geochimica et Cosmochimica Acta 53, 685–697. Berner, R. 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Tett, P. 1982 The Loch Eil project: planktonic pigments in sediments from Loch Eil and the Firth of Lorne. Journal of Experimental Marine Biology and Ecology 56, 101–114. Troelsen, H. & Jørgensen, B. B. 1981 Seasonal dynamics of elemental sulfur in two coastal sediments. Estuarine, Coastal and Shelf Science 15, 255–266. Ullman, W. J. & Aller, R. C. 1982 Diffusion coefficients in nearshore marine sediments. Limnology and Oceanography 27, 552–556. Wassmann, P. 1984 Sedimentation and benthic mineralization of organic detritus in a Norwegian fjord. Marine Biology 83, 83–94.