Seston Dynamics and Food Availability on Mussel and Cockle Beds

Estuarine, Coastal and Shelf Science (1997) 45, 247–259

Seston Dynamics and Food Availability on Mussel and Cockle Beds A. C. Smaal and H. A. Haas National Institute for Coastal and Marine Management/RIKZ, P.O. Box 8039, 4330 EA Middelburg, The Netherlands Received 31 January 1996 and accepted in revised form 31 July 1996 To provide a better understanding of seston dynamics in relation to food supply to the benthos, a series of 13-h tidal cycle sampling programmes was executed in the Oosterschelde estuary (The Netherlands). Samples were taken near the surface and near the bottom on two subtidal mussel cultivation plots and on two intertidal cockle beds. Long-term annual variablity of seston concentrations was lower than coefficients of variance of the short-term tidal cycle seston data at the intertidal stations, and higher than at the subtidal stations. Near-bottom relative to surface concentrations were highest for suspended particulate matter (SPM), followed by particulate organic carbon (POC), and chlorophyll. There was no food depletion near the bottom but food quality was lower, presumably due to re-suspension of sediment, including low-quality biodeposits. Chlorophyll concentrations were lower in ebb than flood water at all stations, which was ascribed to feeding activity of the bivalves. At the subtidal stations, SPM and POC concentrations were also lower during low water, owing to sedimentation. There was a positive correlation at the intertidal stations of seston quantity with wind speed and wave action. At a wave length exceeding twice the water depth, re-suspension of low quality bottom material was observed and seston quality decreased. It was concluded that food availability for benthic suspension feeders was lower than suggested by routine monitoring data. At the intertidal stations, food quality was further reduced during periods of increased wind velocities and wave action. The low near-bottom food quality can partly be considered as an effect of the feeding activity of the benthic suspension feeders. ? 1997 Academic Press Limited Keywords: seston; chlorophyll; food composition; wind; erosion; vertical gradients; tidal cycle

Introduction Benthic suspension feeders, such as mussels (Mytilus edulis) and cockles (Cerastoderma edule), collect their food by filtering and sorting particles (seston) from the water column. Seston is composed of inorganic silt, refractory and labile detritus and living cells. In many estuaries, seston consists mainly of inorganic material and only a small fraction has food value. Seston concentration and composition on intertidal and subtidal beds of suspension feeders are influenced by many interacting factors, and are generally highly variable in time and space. Benthic suspension feeders in estuaries thus live in a highly dynamic environment with regard to their food supply, and many studies have dealt with physiological, behavioural and ecological adaptations of the populations to their food supply (see for review, Jørgensen, 1990; Hawkins & Bayne, 1992). Food supply depends on a number of factors of different temporal and spatial scales, such as season, (tidal) water flow, mixing of the water column, upwelling, wind speed and direction, sedimentation/ 0272–7714/97/020247+13 $25.00/0/ec960176

erosion characteristics, and depletion by benthic filtration. Various in situ measurements in estuaries of a broad geographical range have shown a large seasonal variation in seston concentration and composition, owing to seasonality of phytoplankton blooms (Widdows et al., 1979; Cade´e, 1982; Berg & Newell, 1989), ice coverage in winter (Anderson & Mayer, 1984) and wind effects (Shideler, 1984; Gabrielson & Lukatelich, 1985; Demers et al., 1987; De Jonge, 1992; Bock & Miller, 1995). Tidal motion is a major factor in the supply of seston to suspension feeder beds; mussel beds derive their food from production areas that are 11–16 times the size of the beds (Smaal & Prins, 1993). Current speed and vertical mixing determine the food supply to dense bivalve beds (Wildish & Kristmanson, 1984; Fre´chette et al., 1989). The uptake of particles by the bivalves may result in local seston depletion, which is reflected in small-scale concentration differences in the water column. Moreover, re-suspension of sediment may change the near-bottom seston composition and food value (Rhoads, 1974). This was also demonstrated by Fre´chette and Grant (1991) who showed that ? 1997 Academic Press Limited

248 A. C. Smaal & H. A. Haas

MW

CW

* 4°E

North Sea

* 52°N

CE The Netherlands

= Low water line

Oosterschelde

= Hydro-meteo station

*

= Routine monitoring station ME

0

5 km

F 1. Oosterschelde estuary with seston sampling stations. CW, intertidal cockle bank west; MW, subtidal mussel plot west; CE, intertidal cockle bank east; ME, subtidal mussel plot east.

mussels, suspended 1 m above the sediment, grew better than mussels in the bed. In contrast, Grant et al. (1990) showed that near-bottom oyster growth was not suppressed compared to suspended oysters, presumably because re-suspension of benthic microalgae had a positive effect on the food quality. These observations make clear that estimating food availability for benthic suspension feeders requires near-bottom seston measurements (Fegley et al., 1992). Wind-driven wave action is important for resuspension in shallow areas (Shideler, 1984; Anderson & Mayer, 1984; Demers et al., 1987; Fre´chette & Grant, 1991). Carper and Bachmann (1984) showed that wave-induced re-suspension was related to wind velocity in a shallow lake. The impact of wind speed, fetch and wave action was calculated for various subtidal areas (Demers et al., 1987; Arfi et al., 1993), and for intertidal mussel beds by Prins et al. (1996). It was shown by these authors that a critical wind velocity and fetch exist at which resuspension occurs, depending on the water depth. These studies indicate the need for short-term and small-scale measurements of seston concentration and composition, in order to examine the food availability to suspension-feeder beds.

This paper compares the near-bed and surface seston concentration and composition during a number of tidal cycles on two intertidal cockle beds and two subtidal mussel beds, as a function of tidal motion, wind velocity and season, in order to characterize the food supply at these sites.

Materials and methods Study area and sampling stations The Oosterschelde estuary is part of the Dutch delta area, formed by the rivers Rhine, Meuse and Scheldt (Figure 1). The freshwater load is restricted by dams and sluices, and salinity ranges from 28 to 32. On the tidal flats, extensive populations of (wild) cockles exist; in subtidal areas and on tidal flats, bottom culture of mussels is executed on cultivation lease sites. Mussels and cockles are dominant species in the Oosterschelde. In 1986, average biomass for the whole estuary was estimated as 22·8 and 10·0 g ashfree dry weight (AFDW) m "2 for cockles and mussels respectively (Smaal & Nienhuis, 1992). Routine seston sampling near the water surface occurred on a weekly basis in the framework of primary production measurements on locations in

Seston dynamics and food availability 249 T 1. Physical conditions during the seston sampling periods

Air

Wind velocity (m s "1) (min/max; avg)

Wind direction

Current velocity (max; cm s "1)

Tidal range (cm)

4·9 15·1 17·0 14·0 16·9 11·6 13·5 18·7 16·7 15·0 8·7 13·5 26·2 15·1 8·7 13·5 20·7 15·1

5·5–14·8 6·5–14·1 5·6–8·4 2·9–9·9 2·6–6·4 1·2–7·1 0·9–8·6 4·1–6·8 7·4–17·6 4·6–6·2 8·0 5·5 1·5 1·5 8·0 5·5 3·5 1·5

SSW WSW WNW SSW S SE NW WNW SSW NNE SSW W NW E SSW W WNW E

11 44 41 25 39 27 12 44 31 15 35 65 37 40 40 27 27 21

200 190 165 180 250 255 260 280 210 240 210 230 200 200 300 240 240 210

Temperature ()C) Station

Date (1986)

Water

CW CW CW CW CW CE CE CE CE CE MW MW MW MW ME ME ME ME

20 Mar 27 May 10 Jul 28 Aug 14 Oct 18 Mar 29 May 8 Jul 26 Aug 16 Oct 16 Apr 14 May 15 Jul 30 Sep 16 Apr 14 May 16 Jul 30 Sep

2·9 13·5 18·6 16·4 14·8 2·5 13·4 18·6 17·5 15·2 5·0 10·8 19·2 15·1 5·0 10·8 18·8 15·1

Min/max and mean wind velocity are presented for the C and M stations, respectively.

channels (Figure 1). In winter, the sampling frequency was on a monthly basis (Wetsteijn & Kromkamp, 1994). Sampling of seston in the framework of this study was executed during a number of tidal cycles on intertidal cockle beds at one location in the western (CW) and one in the eastern part (CE) of the estuary, and on subtidal mussel plots in the western (MW) and eastern part (ME) (Figure 1). Intertidal stations. At Station CW, average cockle density and biomass were 800 m "2 and 85 g dry flesh weight (DFW) m "2, respectively. At Station CE, density and biomass were 27 m "2 and 11 g m "2. Average growth rates of cockles during the growing season were 1·13 mg AFDW day "1 at CW and 1·30 mg day "1 at CE, which was not significantly different (R. Gols, pers. comm.). Depth of both stations was at Dutch Ordnance Level "1 m, with immersion for 75% of the time. Sediment characteristics were similar on both locations (median grain size=2·8 C; organic carbon=0·3%). Subtidal stations. The subtidal sampling stations were located on mussel cultivation plots, at a mid-tide depth at MW and ME of "5 and "6 m respectively. Average mussel densities and biomass on both mussel plots were approx 300 m "2 and 200 g DFW m "2. Growth rates of mussels of 45 mm standard size from June to October were 5 mg DFW day "1 and

0·07 mm day "1 at MW; at ME, growth rates were 2 mg DFW day "1 and 0·03 mm day "1 (van Stralen, 1988). Sampling programme Seston was sampled by pumping water from 5 cm above the bottom with a Masterflex tubing pump to a research vessel. The sampling tubes were mounted on a tripod, which was placed on the subtidal bottom by scuba divers. On the tripod, Ott current meters were mounted at 40 cm above the bottom. Samples were also taken near the water surface. Sampling was done for 13-h periods, from high water (HW) slack until next HW slack. At the intertidal stations, sampling was interrupted during low tide at a water level below 40 cm. Current velocity was recorded continuously during submersion; samples for suspended particulate matter (SPM) and particulate organic carbon (POC) were taken every 30 min, and particulate organic nitrogen (PON), chlorophyll a and phaeopigments were sampled every hour. Physical conditions during the measurements are given in Table 1. Estimation of wind influence Data on wind velocity and direction were available from routine monitoring stations (Figure 1). For the intertidal stations, seston data were compared with

250 A. C. Smaal & H. A. Haas

wind data collected with a 30* frequency. Wind direction was expressed as fetch length, and combined with water depth, according to the approach of Carper and Bachmann (1984), in order to estimate the wind conditions at which re-suspension of sediment may occur. When the base of a wave extends to the bottom of the water column, re-suspension is expected. As the wave base is supposed to be 0·5#wave length, resuspension will happen when wave length (L) exceeds the water depth (h) by a factor of 2 (L/h>2). L depends on wave period (T), which is calculated from wind velocity U and fetch F by an empirical relation (CERC, 1977): gT/2ðU=1·2 tanh (0·077 (gF/U2)0·25)

(1)

where g is gravitational constant (9·8 m s "2), T is wave period (s), U is wind velocity (m s "1), and F is fetch (m). The wave length is calculated as: L=gT2/2ð

(2)

L is wave length (m). For the purpose of presentation, graphs show the relation between seston concentration and log10(L/h).

Seston analysis Water samples were collected in polythene bottles, and transported to the laboratory for further processing. Suspended particulate matter was measured after filtering the samples on pre-weighed and pre-ashed Whatman GF/C filters, rinsing them with distilled water, drying for 48 h at 70 )C, and weighing again. Particulate organic carbon and nitrogen were determined on a Carlo-Erba analyser. Chlorophyll a (CHL) and phaeophytin a (PHAEO) were analysed by high performance liquid chromatography after filtration of a 1 l sample on Whatman GF/C filters. The fraction of particulate organic matter in seston (fPOM, in %) was calculated with a POM/POC ratio=1·9 (Smaal et al., 1986); the fraction phytoplankton in seston (fPHYTOPOM) was calculated with a carbon–chlorophyll ratio=40 (Vos, 1987): fPHYTOPOM=CHL#40#1·9#1000 "1 #SPM "1 #100%. Seston quantity is presented as concentrations of SPM, POC, CHL and PHAEO. Seston quality is expressed as C/N ratio (=POC/PON conc. by weight), fPOM, fPHYTOPOM and the pigment ratio PHAEO/CHL.

Data analysis Correlations were tested with non-parametric rank tests, and presented as box-and-whisker plots, because the concentrations of seston components do not show normal or lognormal distributions, owing to large variability and the frequent occurrence of outliers. Box-and-whisker plots show the median as the central horizontal line, splitting 50% of the values in two halves bordered by the hinges of the box. The whiskers show the range of values within 1·5#Hspread, whereby Hspread is defined as the differences between the two hinges. Values larger than 1·5#Hspread, but lower than 3#Hspread are outside values (*); values larger than 3#Hspread are far outside values (o). Differences between seston concentrations in the eastern and western part, and between surface and bottom samples, were tested by using the Wilcoxon test; the impact of ebb and flood tide was tested with the Kruskall–Wallis test; the impact of wind velocity, direction, L/h and current velocity were tested with Spearman’s rank correlation test; critical values of Spearman correlation coefficients (rs) were calculated according to Siegel (1956): t=rs #[(n"2)/(1"rs2)]0·5

(3)

Corresponding á values were taken for n>9 from a Student’s t-distribution table with v=n"2. All statistical tests were carried out with the SYSTAT Inc. statistical software package.

Results Seston dynamics in the Oosterschelde The seasonal variation of SPM, POC and CHL concentrations are shown in Figure 2. Suspended particulate matter values were higher in winter and lower in spring and summer; in July and August some peaks were observed in the eastern part due to strong wind conditions. Particulate organic carbon values were less variable; CHL concentrations showed maximum values of 27 mg m "3 in both areas. In both areas, a large spring peak was observed in March and a summer peak in July; in the western part a peak was also observed in May. The May and July peaks were caused by blooms of Phaeocystis sp. (B. Wetsteijn, pers. comm.). A pairwise test showed no significant difference between both areas for SPM and CHL concentrations; POC concentrations and fPOM were significantly higher in the eastern part (Wilcoxon test, P<0·005 and P<0·001, respectively). Fraction

Seston dynamics and food availability 251

Concentration (gm–3)

West

East

45

45

40

40

35

35 SPM

30

30

25

25

20

20

15

15

10

10

5

SPM

POC

5

Concentration (mgm–3)

POC 0

0

28

28

24

24

20

20

16

16

12

12

8

8 CHL

4 0

J

F M A M

J

J

A

S

O N D

CHL 4 0

J

F M A M

J

J

A

S

O N D

F 2. Suspended particulate matter (SPM), particulate organic carbon (POC) and chlorophyll a (CHL) concentrations in 1986 from routine measurements in the western and eastern part of the Oosterschelde estuary.

PHYTOPOM had a median value of 4 and 7% in east and west, respectively, which was not significantly different. Seston dynamics during a tidal cycle As an example of tidal variation, results from one 13-h sampling programme are presented for the Intertidal Station CW on 28 August (Figure 3). Increased concentrations of all seston parameters were observed before and after low water slack, indicating resuspension. Wind direction that day was SSW, so the sampling site was exposed to wind, with wind velocities up to 9·9 m s "1 (Table 1). Only SPM nearbottom concentrations were higher than near the surface. Chlorophyll concentrations were significantly lower in the ebb phase than in the flood phase. Average, minimum and maximum values of near-

surface seston parameters during all tidal cycle measurements are presented in Table 2. Suspended particulate matter concentration showed peaks up to 161 g m "3 in August at CE. Also in May, relatively high SPM concentrations were recorded at both intertidal stations; POC concentrations corresponded with the SPM peaks. These peaks coincided with increased wind velocities (Table 1). Chlorophyll concentrations were relatively high in March on both locations; on the other sampling dates, concentrations were higher at CE than CW. C/N ratios were relatively low (<8) during the phytoplankton spring blooms. At the subtidal stations, near-surface SPM concentrations did not exceed 33 and 8 g m "3 at MW and ME, respectively. Particulate organic carbon concentrations were not higher than 2·7 g m "3. Both at MW and ME a CHL peak was observed in July. C/N ratios were low in May at ME and in July at MW (Table 2).

252 A. C. Smaal & H. A. Haas 90 10

80 70

8 –3

CHL (mgm )

SPM (gm–3)

60 50 40 30 20

6

4

2

10 0

0

3.5 24 3 20

POC (gm–3)

2.5 16 2 12

1.5

8

1

4

0.5 0

10 11 12 13 14 15 16 17 18 19 20 21 22 Time (h)

0

10 11 12 13 14 15 16 17 18 19 20 21 22 Time (h)

F 3. Near-surface ( ) and bottom (———) suspended particulate matter (SPM), particulate organic matter (POC) and chlorophyll a (CHL) concentrations, water level (———, dm), current speed ( , cm s "1) and wind speed ( , m s "1) during a tidal cycle at Station CW in August 1986.

Comparison of annual and tidal variation Coefficients of variation (CVs) of the annual measurements are comparable or higher than the CVs of the subtidal stations, but lower than the CVs of the intertidal stations, except for CHL at CW (Table 3). Variability of seston concentration and composition is highest in the short-term at the intertidal stations. Tidal samples in deeper water showed lower or similar variability than the annual samples.

Surface/bottom comparison During all measurements, seston concentrations near the bottom were higher than near the surface (Table

4). Suspended particulate matter, POC, PON, CHL and PHAEO concentrations were significantly higher near the bottom at all locations. The ratio between bottom and surface concentrations was higher for SPM than for POC and CHL. The organic fraction, fPOM and fPHYTOPOM were higher near the surface in most cases. The C/N ratio, averaged over all measurements per location, showed significant differences between bottom and surface at MW only. The pigment ratio was not significantly different at any location (not shown). At the intertidal stations, the differences between surface and bottom concentrations were less than at the subtidal stations, presumably due to the smaller distance between surface and bottom at the intertidal stations.

Seston dynamics and food availability 253 T 2. Mean (min–max) concentrations of suspended particulate matter (SPM, mg l "1), particulate organic carbon (POC, mg l "1) and chlorophyll a (CHL, ìg l "11) and C/N ratio of near-surface samples of tidal measurements throughout the year at the four stations, and of the monitoring programme in West and East Loc.

Month

CW

MAR MAY JUL AUG OCT MAR MAY JUL AUG OCT APR MAY JUL SEP APR MAY JUL SEP YR YR

CE

MW

ME

W E

SPM 27 29 6 14 6 8 28 8 37 4 13 5 6 9 5 2 4 3 11 10

(6–55) (8–68) (2–19) (5–79) (3–8) (4–13) (5–63) (5–18) (3–161) (1–10) (3–25) (1–25) (2–19) (2–33) (3–7) (1–5) (2–7) (1–8) (2–42) (3–29)

POC 1·7 1·6 0·8 0·7 0·5 1·1 2·7 1·0 1·9 0·4 0·9 1·2 1·2 0·6 0·8 0·9 0·9 0·4 0·9 1·7

(0·7–2·7) (0·8–3·4) (0·4–1·4) (0·3–2·5) (0·2–0·7) (0·9–1·3) (1·5–5·2) (0·8–1·7) (0·4–7·1) (0·2–0·7) (0·3–1·9) (0·8–1·9) (0·3–2·7) (0·3–1·5) (0·6–1·5) (0·6–1·4) (0·6–1·1) (0·2–0·7) (0·3–1·6) (0·6–6·1)

CHL

C/N

14·5 (10·4–19·8) 3·5 (1·1–8·1) 7·6 (1·6–11·7) 3·4 (1·2–5·6) 3·9 (0·7–10·2) 23·0 (9·9–32·6) 13·8 (8·6–19·7) 5·9 (4·3–7·5) 13·0 (6·1–32·1) 2·7 (1·2–8·1) 5·2 (1·3–9·0) 6·5 (4·4–9·5) 15·3 (8·6–21·8) 5·2 (3·5–7·8) 5·2 (2·5–7·1) 5·3 (2·1–9·2) 10·4 (6·4–16·4) 5·5 (2·9–8·9) 7·7 (0·8–27) 7·5 (1·1–26·6)

9·1 (5·4–12·2) 7·7 (5·6–16·3) 7·0 (5·8–9·7) 9·8 (5·5–13·3) 13·2 (6·4–20) 6·7 (5·9–7·5) 6·9 (4·2–9·1) 7·0 (5·8–9·4) 9·4 (4·5–14·3) 11·3 (6–17·5) 10·6 (8·8–13·3) 7·8 (5–13·3) 6·8 (2·9–9·6) 12·4 (7–20) 9·9 (5·9–18·8) 5·4 (2·3–8·2) 9·2 (7·3–11·4) 9·4 (6·2–16·2) 9·6 (5·9–13·4) nd

nd, no data.

T 3. Comparison of annual and tidal coefficients of variation (CV, %) of seston concentrations Annual programme

Intertidal cockles

Subtidal mussels

CVtidal/CVannual intertidal

subtidal

Variable

W

E

n

W

E

n

W

E

n

W

E

W

E

SPM POC CHL

90 42 73

59 79 76

33 33 33

97 66 69

153 88 77

89 86 53

81 42 62

53 34 49

87 87 39

1·08 1·57 0·94

2·59 1·11 1·01

0·90 1·00 0·85

0·90 0·43 0·64

SPM, suspended particulate matter; POC, particulate organic carbon; CHL, chlorophyll a. W, west; E, east; n, number of observations.

Tidal motion Ebb/flood. Suspended particulate matter, POC and CHL concentrations in ebb and flood tide at the intertidal stations were not significantly different in most cases, when tested for the five tidal cycles (Table 5). The C/N ratio at the surface was lower in the flood tide at Stations CW and CE. These parameters were also tested per tidal cycle, and showed no significant differences in most cases. In contrast, CHL concentrations were significantly different in March, July, August (when the near bottom peak of 15.00h was ignored, see Figure 3) and October at CW, and in

March, May and August at CE. Chlorophyll concentrations were higher in the ebb phase in March, while on the other dates, flood tide values were higher (Figure 4). For the subtidal stations, seston concentrations were compared from mid tide in the flood phase till mid tide in the ebb phase (the high water period), and from mid tide in the ebb phase till next mid tide (the low water period). Significant differences were observed for SPM, POC and CHL concentrations (Table 5). In almost all cases, seston concentrations were higher in the high water period.

254 A. C. Smaal & H. A. Haas T 4. Ratio of bottom to surface seston concentrations (average bottom conc./average surface conc.) at the four sampling stations

SPM POC PON CHL PHAEO C/N fPOM fPHYTOPOM

CW

CE

MW

ME

1·83c 1·16b ns 1·07b 1·06a ns 0·79c ns

3·46c 1·17c 1·05a 1·28c 1·50c ns 0·81a ns

2·22c 1·40c 1·26c 1·30b 1·55b 1·18b 0·63c 0·49c

3·44c 1·64c 1·42b 1·41c nd ns 0·45c 0·46c

SPM, suspended particulate matter; POC, particulate organic carbon; PON, particulate organic nitrogen; CHL, chlorophyll a; PHAEO, phaeophytin a; fPOM, fraction of particulate organic matter in seston; fPHYTOPOM, fraction of phytoplankton in seston. Statistics based on Wilcoxon test; nd, no data; ns, not significant, a P<0·05, bP<0·01, cP<0·001.

T 5. Comparison of seston concentrations at ebb (e) and flood (f) tides at high (h) and low (l) water periods at the four sampling stations, near bottom (b) and surface (s) samples. Statistics based on the Kruskall-Wallis nonparametric test Location Variable SPM POC CHL PHAEO C/N fPOM fPHYTOPOM PHAEO/CHL

b s b s b s b s b s b s b s b s

CW

CE

MW

ME

ns ns ns ns ns ns ns ns ns ns ns ns ns f>ec f
ns f>ec ns ns ns ns ns ns ns f
h>ld h>ld h>ld h>ld h>lc h>la h>lc ns ns ns hla ns ns

h>ld h>lb h>lc h>la h>lc h>lb nd nd h>lc ns h
SPM, suspended particulate matter; POC, particulate organic carbon; CHL, chlorophyll a; PHAEO, phaeophytin a; fPOM, fraction of particulate organic matter in seston; fPHYTOPOM, fraction of phytoplankton in seston. nd, no data; ns, not significant; aP<0·1, bP<0·05, cP<0·01, d P<0·001.

Currents and depth. Spearman rank correlations (not shown) of concentrations of the various seston parameters with current velocity and water depth were not significant in almost all cases at the intertidal

stations. At the subtidal stations, significant positive correlations of SPM and POCb (near-bottom) with current velocity (P<0·05) were observed at MW only. Significant positive correlations with depth were observed of almost all seston parameters except SPM at MW. Wind and waves At both intertidal stations, there was a significant positive correlation of wind velocity and wave impact (L/h) with SPM and POC concentrations, and a negative correlation with fPOM (Table 6). A positive correlation of wind and waves with CHL and PHAEO concentrations was observed at CW only. At CE, there was a positive correlation with the C/N ratio, and a negative correlation with the fPHYTOPOM. In most cases, the observed correlations were similar for both bottom and surface samples. No significant correlation was found with the pigment ratio (Table 6). There was no significant relation at the subtidal stations of seston parameters with wind and wave influence. Suspended particulate matter and POC concentrations at CE and CW sharply increased at wind velocities >7 m s "1 (not shown); this wind velocity can therefore be considered as a re-suspension threshold for the conditions of the Oosterschelde estuary. A sharp increase is also demonstrated in Figure 5. Suspended particulate matter and POC concentrations are presented as a function of log(L/h); increased concentrations were observed at log(L/h) values >0·4 at CW and >0·3 at CE, which closely corresponds with L/h=2, a reference value for wind-induced re-suspension.

Discussion Annual and tidal variation The annual variation in seston quantity (SPM, POC, CHL) in 1986 in the Oosterschelde estuary is typical for estuaries and shallow coastal systems (Wetsteijn & Kromkamp, 1994). Suspended particulate matter concentrations were quite variable, with higher mean values in winter than in summer, probably caused by higher wind speeds and storm frequencies in winter. Chlorophyll concentrations represented the seasonality in phytoplankton development. Similar seasonal variability was found in the Lynher (Widdows et al., 1979), Lowes Cove (Anderson et al., 1981), the Wadden Sea (Cade´e, 1982) and Marennes-Ole´ron Bay (He´ral et al., 1987).

Seston dynamics and food availability 255 50

50

Near-bottom chlorophyll (mgm–3)

CW

CE

40

40

30

30

20

20

10

10

0

e

f

Mar†

e

f

May

e

f

Jul*

e

f

Aug*

e

0

f

e

f

Mar†

Oct*

e

f

e

May

f Jul

e

f

Aug*

e

f Oct

F 4. Box-and-whisker plots of near-bottom chlorophyll concentrations at Stations CW and CE during ebb and flood tide on the sampling dates. Significant differences per month are indicated: *=P<0·05; ,=P<0·01. T 6. Spearman rank correlation coefficients of the relation of wind velocity (WSP) and wave impact (L/h) with seston concentrations at the intertidal stations CW Variable SPM POC CHL PHAEO C/N fPOM fPHYTOPOM PHAEO/CHL

WSP b s b s b s b s b s b s b s b s

0·467c 0·605c 0·612c 0·722c 0·690c 0·584c 0·495c 0·463c "0·127 "0·082 "0·002 "0·254a 0·374a 0·048 "0·197 "0·110

CE L/h

0·466c 0·564c 0·484c 0·550c 0·393a 0·331a 0·505c 0·433b "0·055 "0·019 "0·167 "0·358b 0·033 "0·107 0·128 0·201

n 93 90 48 48 57 91 46 48

WSP 0·467c 0·405b 0·311b 0·128 0·194 0·182 0·228 0·196 0·627c 0·333a "0·565c "0·617c "0·658c "0·433c 0·090 0·174

L/h 0·539c 0·500c 0·441c 0·303c 0·196 0·152 0·178 0·093 0·628c 0·367a "0·505c "0·527c "0·524c "0·538c "0·019 0·076

n 84 84 43 50 43 48 48 48

SPM, suspended particulate matter; POC, particulate organic carbon; CHL, chlorophyll a; PHAEO, phaeophytin a; fPOM, fraction of particulate organic matter in seston; fPHYTOPOM, fraction of phytoplankton in seston. b, bottom; s, surface; n, number of observations. aP<0·05, bP<0·01, cP<0·001.

The food quality of seston for suspension feeders depends on the fraction of living material and labile detritus of total seston. Smaal and Van Stralen (1990) demonstrated a significant correlation of mussel growth and annual primary production in the Oosterschelde estuary, suggesting that phytoplankton

was the main food source. The fraction that phytoplankton comprise of total suspended matter in the Oosterschelde had a median value <7% on an annual basis. Food availability is therefore considered limited, or ‘ diluted ’ by the large inorganic fraction (Widdows et al., 1979).

256 A. C. Smaal & H. A. Haas CW

CE

80 160 70 140 SPM (gm–3)

50 40 30

120 100 80 60

20

40

10

20

0

0

3.4

8

3

7

2.6

6 POC (gm–3)

POC (gm–3)

SPM (gm–3)

60

2.2 1.8 1.4

5 4 3

1

2

0.6

1

0.2

0

0.2

0.4

0.8 0.6 log(L/h)

1

1.2

1.4

0 –0.8

–0.4

0

0.8 0.4 log(L/h)

1.2

1.6

F 5. Near-surface suspended particulate matter (SPM) and particulate organic matter (POC) concentrations as a function of wave action, expressed as log(L/h) at Stations CW and CE.

Coefficients of variation of seston concentrations on subtidal mussel beds were similar to, or lower than the CVs of the annual monitoring programme. At the intertidal stations, CVs of SPM and POC were higher than the annual CVs. Cade´e (1982) observed higher CVs for a number of seston parameters on an annual base, compared with tidal variation. In this case, the tidal samples were taken near the surface at stations in the channel. Berg and Newell (1989) found a significant increase of CVs with temporal and spatial scales. Other authors observed similarity in variation of seston concentrations of annual and tidal samples on subtidal stations (Fegley et al., 1992). For the intertidal stations, the present results showed higher variability in the short-term than in the long-term seston dynamics. The high variability at intertidal stations indicates the impact of factors as flood front (Anderson & Mayer, 1984) and wind-induced re-suspension, in addition to the effects of tide and season. Vertical mixing A comparison of surface and bottom samples clearly showed higher bottom concentrations for all seston

parameters. Higher bottom concentrations of SPM have been observed in many studies, and are explained by the existence of a benthic boundary layer, with strong vertical gradients of flow velocity and increased particle fluxes (Muschenheim, 1987). The bottom/surface ratio was in most cases different for the various seston components, in the order SPM>POC>CHL. This could be ascribed to: (1) re-suspension of low-quality sediment, in combination with hydrodynamic sorting (Muschenheim, 1987); (2) food depletion by the selective filtration activity of the suspension feeder bed (Fre´chette & Grant, 1991; Muschenheim & Newell, 1992); (3) filtration and selective ingestion of POC and chlorophyll by mussels and cockles and subsequent resuspension of low-quality biodeposits (Prins et al., 1997), or a combination of these processes. Food depletion is unlikely in the present case, because the near-bottom chlorophyll concentrations were higher than the surface concentrations; this also occurs at other locations (Smaal et al., 1986). Re-suspension and hydrodynamic sorting may explain the higher bottom/surface ratio of SPM compared to POC and

Seston dynamics and food availability 257

CHL, but not the difference between POC and CHL, assuming that the hydrodynamical behaviour of POC and CHL can be considered similar. Therefore the formation and re-suspension of biodeposits has to be taken into account. Prins et al. (1996) observed in situ selective uptake of higher quality seston components on an intertidal Oosterschelde mussel bed, resulting in a concentration decrease over a mussel bed in the sequence CHL>POC>SPM. This corresponds with the authors’ observations regarding the difference between surface and bottom for the various seston components. Near-bottom phytoplankton counts have shown higher concentrations than at the surface, but there was no difference in species composition, particularly with respect to benthic diatoms (Vos, 1987). Re-suspension of benthic diatoms was of minor importance, presumably due to the observed dominance of epipsammic diatoms in the Oosterschelde, which re-suspend less easily than epipelic diatoms (Vos, 1987). It is concluded, therefore, that there was no local depletion of seston or food near the bottom; the lower near-bottom quality of seston is regarded as an effect of the benthic boundary layer in combination with selective uptake of higher quality seston fractions by mussels and cockles, and subsequent re-suspension of sediment including low quality biodeposits. Ebb and flood tide At the intertidal stations, SPM and POC concentrations were not significantly different in flood and ebb phase in most cases. No net erosion or sedimentation were observed during the authors’ measurements. In contrast, chlorophyll concentrations were significantly lower in the ebb phase during most tidal cycles. This is ascribed to the filtration and selective ingestion of algae by the cockles. Only in March was the flood concentration lower; at that time, temperature was 2·9 )C and, consequently, the activity of the cockles was very low (Smaal et al., 1997). At the subtidal stations, significantly higher concentrations of SPM, POC and CHL during high water were observed in all cases. The mussel sampling stations were located in areas with mussel cultivation plots, and the water mass passed over dense mussel beds (Smaal & van Stralen, 1990). Therefore, reduction of chlorophyll concentrations during passage over mussel and cockle beds can be considered as an effect of the filtration and feeding activity of the animals. The impact of bivalve filter feeding on seston concentrations has been observed in many studies (Carlson et al., 1984; Fegley et al., 1992; Kamermans, 1994; Prins & Smaal, 1994). Potential

clearance time for the entire Oosterschelde estuary is 5 days, which is a normal value for areas with dense bivalve beds (Smaal & Prins, 1993), and this illustrates the potential impact of the bivalves on seston. The lower low water concentrations of SPM and POC at the subtidal stations are explained by biodeposition and net sedimentation of silt. In the Oosterschelde, sedimentation occurs mainly in the subtidal areas, including the mussel beds (Ten Brinke et al., 1995). Wind-induced re-suspension There was a significant increase of seston concentrations with wind velocity and wave action for all quantitative parameters in the western intertidal station, and for SPM and POC in the eastern intertidal station. The quality parameters showed an opposite pattern. Increased seston concentrations at the intertidal stations could be ascribed to wind-induced re-suspension of sediment, which had a lower quality than pelagic material. The positive correlation between wind and chlorophyll concentration suggests re-suspension of benthic chlorophyll, occurring at higher wind speeds. As discussed earlier, epipsammic diatoms were dominant, and these only re-suspend at higher wind velocities. Wind-induced re-suspension is described in many studies, and various approaches for estimation of re-suspension thresholds have been presented. According to Demers et al. (1987), wind velocities <4 m s "1 caused significantly higher POC concentrations, and they considered this value as a resuspension threshold in a shallow subtidal area; this is close to the value of 5 m s "1 (expressed as number of hours exceeding 5 m s "1) observed by Gabrielson and Lukatelich (1985) for an estuarine system. Arfi et al. (1993) observed particle re-suspension at wind velocities >3 m s "1. De Jonge (1992) showed windinduced re-suspension of SPM and benthic chlorophyll on a tidal flat at a wind velocity of 2 ms "1. He found a linear increase of SPM and CHL from 2 to 14 ms "1. In the present study, the wind velocity threshold for re-suspension of SPM and POC was 7 m s "1. Yet, in addition to wind velocity, wave action and wind fetch should be taken into account. This was done according to Carper and Bachmann (1984), Shideler (1984), Arfi et al.(1993) and Prins et al. (1996). Calculated wavelengths, based on empirical formulas from CERC (1977) were compared with water depth. When waves touch the bottom, presumably at L/h>2, re-suspension is to be expected. Indeed, in the present study, the observed resuspension threshold for SPM and POC on both intertidal stations were close to the predicted value.

258 A. C. Smaal & H. A. Haas

The mechanism of wind-induced re-suspension consists of increased wave action, rather than increased current velocities; this is reflected in the similarity of the correlation coefficients of seston parameters, with wave action (L/h), and wind velocity. It is concluded that wind-induced re-suspension affected seston concentration and composition, at wind velocities >7 m s "1, caused by waves of a certain length at a depth of twice the wavelength. Wind influence can be related to food availability of bivalve suspension feeders. Clearly, storm conditions result in high inorganic loads of the water column, and consequently decreased food quality (Bock & Miller, 1994, 1995). At moderate gales (<10 m s "1), Asmus et al. (1990) showed that outflow of particulate matter was higher than the uptake flux of material across mussel beds. This can be considered as beneficial, because silt accumulation of the beds was reduced. At lower wind velocities, the opposite was true (Asmus et al., 1990). This phenomenon was also described by Prins et al. (1996). Fre´chette and Grant (1991) showed that wind had a positive effect on resuspension of benthic diatoms, but it did not prevent food depletion. In the present study, food quality was, in most cases, negatively correlated with wind velocity and wave action, especially for the eastern location. Food conditions on tidal flats in the Oosterschelde were, therefore, negatively related with wind velocities. Interactions with the bivalves Seston quantity near mussel and cockle beds in the Oosterschelde showed higher values than at the surface, and quality was lower. Food availability for the bivalves was thus lower than suggested by the routine monitoring data. On the intertidal stations, food quality was further reduced during periods of increased wind velocities and wave action. These observations support the idea that the animals live in a highly dynamic environment with regard to their food, and that the uptake of the relatively small food fraction from the seston requires efficient selection mechanisms (Prins et al., 1991; Navarro et al., 1994). In fact, the low near-bottom food quality can partly be considered as an effect of selective ingestion, and rejection of low-quality material as pseudofaeces. The reduction of chlorophyll concentrations after passage of seston over the bivalve beds comprises further indications for the impact of the bivalves on seston quantity and quality. Acknowledgements The authors are grateful to the crews of the RVs Lodycke, Wijtvliet, Pluimpot, Molenvliet and Bokkegat

for their help in collecting the samples, R. Gols for assistance in collection and analysis of the data, to F. Colijn and K. Essink for comments on earlier drafts, T. C. Prins and W. J. Wolff for valuable suggestions to improve the manuscript, and H. Mulder and two anonymous referees for their constructive comments.

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