Primary Production in Estuaries

Primary Production in Estuaries

Nancy V.J. de Bakker

Groningen, April 1998

Primary production in Estuaries

Nancy V.J. de Bakker

Supervisors:

Dr. J. Kromkamp (NIOO-CEMO, Yerseke) Dr. W.W.C. Gieskes (RUG, Groningen)

Groningen, April 1998

£) 61b

Table of contents

1. Introduction

2. Factors influencing photosynthesis

2.1 nutrients

2.2

light

2.3 stratification and vertical mixing

2.4 interrelation

2.5 other

factors: salinity and temperature

3. Factors influencing biomass

3.1 grazing

3.2 wash-out as a factor influencing biomass

4. Antropogenic influences

4.1 human impact

4.2 a case study -

Oosterschelde

Interannual differences in primary production

Summary

Acknowledgements

References

1. Introduction

This essay will concentrate onprimary production of phytoplankton in estuaries, factors influencing this primary production and the interannual variability in primary

production.

There is no generally accepted definition of primary production in the literature.

Lawrence, in Henderson's dictionary of biological terms (1996), defined primary production as: assimilation of inorganic carbon and nutrients into organic matter by autotrophs. Primary producers can be both chemoautotrophs, which obtain energy from the oxidation of inorganic substances, and photoautotrophs, which use light, to

synthesise organic matter. One of the most important chemoautotrophic processes in eutrophic estuaries, due to high concentrations of ammonium, is nitrification, the process of conversion of ammonium to nitrate (Heip et al., 1995). Although the chemoautotrophic primary production can account for up to 32 % of the total primary production (Heip et al., 1995; Van Spaendonk, 1993), this essay is concentrated on primary production by photoautotrophs, especially phytoplankton.

The term primary production however, is used in the literature in several ways. Often photosynthesis irradiance relationships form the basis of primary production estimates.

Platt et al. (1984) defined gross primary production as the rate of photosynthetic energy conversion of light energy in chemical energy, while Williams (1993) defined it as the organic carbon produced by reduction of carbon as a consequence of the photosynthetic process over some specific period. Net production is defined by both as gross

production minus (autotrophic) respiration. Also other terms of primary production are used in the literature (Heip et a!., 1995), but they will not be mentioned in this essay.

Primary production can be seen from the point of view of the algal physiologist and theoretical ecologist, who see it as conversion of energy or as the community ecologists, modellers and biogeochemists, who interpret production in terms of nutrient flow (Heip et al., 1995).

Primary producers form the first trophic level in the pelagic food web (Lath and Parson, 1994). All heterotrophs are dependent of the primary production of the autotrophs.

During phytoplankton growth dissolved organic matter (DOM) is being released as part of the metabolic process. Bacteria can decompose this DOM and the inorganic nutrients become available again for autotrophic organisms (Lalli and Parson, 1994). In the sea organic matter is mainly of phytoplankton origin, as 5-50% of the fixed carbon during

photosynthesis is released as DOM (reference in Azam et a!., 1983; Lath and Parson, 1994). The regeneration of nutrients in the sea is a vital part of the interaction between higher and lower trophic levels. The bacteria are primarily grazed by heterotrophic nano-flagellates. These, together with autotrophic flagellates, are eaten by

microzooplankton. The microzooplankton is eaten by mesozooplankton. At this point the microbial foodweb is linked with the classical foodchain of phytoplankton-

zooplankton-fish (Azam et al, 1983).

In estuaries however, suspended organic matter originates from many sources, including riverine inputs or terrestrial plants, sewage, detritus from surrounding marshes, marine plankton, or primary production by vascular plants and algae (Cloern, 1996). In

estuaries bacterial biomass can be high (Heip et a!., 1995) and thus can be important for regeneration of nutrients available for primary production.

This essay deals with primary production in estuaries. Pritchard (1967) defined an estuary as a semi-enclosed coastal body of water which has a free connection with the open sea and within which seawater is measurable diluted with freshwater from land drainage. Boynton Ct a!. (1982) classified estuaries in four groups: fjords, lagoons, embayments and river dominated estuaries. Fjords, having a shallow sill and deep basin water with a slow exchange with the adjacent sea, will not be considered in this essay.

Lagoons are shallow, well mixed, slow flushed systems, slightly influenced by riverine inputs. Embayments are considered as deeper lagoons, often stratified, slightly

influenced by freshwater inputs and having a good exchange with the sea. The fourth category is the river dominated system, a diverse group, but all exhibit seasonally depressed salinities due to riverine inputs and variable degrees of stratification. Another classification can be made on tidal range: micro- meso- and macrotidal estuaries, in which the tidal range increases respectively (references in Monbet, 1992).

Estuaries are among of the most productive marine ecosystems of the world. Primary production in the water column ranges from 25 g C m2 yf' for the open ocean (Berger et at., 1989) up to 500 g C m2 yf' in estuaries (Heip et at., 1995). However, between estuaries there are large differences in primary production, ranging from 40-550 gC m2 yf' (table 1.1; Boynton et at., 1982; Heip et al., 1995). Although these differences_are partly due to differences in methods of the measurements, many different factors influence primary production. Phytoplankton primary production is mainly influenced by light and nutrient availability and grazing (Heip et al., 1995). Light and nutrients regulate primary production via bottom-up control. The biotic factor grazing controls primary production via top-down control (Alpine and Cloem, 1992); however, grazing

In the next chapter factors affecting photosynthesis, thus bottom-up control, will be discussed. The third chapter deals with factors influencing phytoplankton biomass (top- down control). The influences of man on an ecosystem will be shown in chapter 4, with a case study of the Oosterschelde, where a storm-surge barrier was built to protect the land. As different processes take place in estuaries, discussed in chapter 2 till 4, in the last chapter the focus is on interannual differences in primary production. Some attention will be paid to possible mechanisms of these differences.

stimulates the regeneration of nutrients (Sterner, 1986). Factors as light and nutrients_are affected by different processes such as stratification, vertical mixing, resuspension,_etc.

Table 1.1: Estimates of annual primary production (g C m 2)in several estuaries (adapted from Heip et al., 1995)

Estuary Production

USA

Estuary Production

Fourleague Bay Peconic Bay

Tomales Bay

Hudson River Hudson Estuary Delaware Bay

Chesapeake Bay

San Francisco Bay '

SanFrancisco Bay²⁾

upper inner inner

inner central outer average freshwater outer bay inner central outer average average 1985 average 1986 South Bay San Pablo Bay Suisan Bay South Bay North Bay San Pablo Bay Suisan Bay

322 514 317

70 420 420 400 70-240 200 105 296 344 307 569 324 27- 162 13-3 18 6-418 130 90 100 44

Neuse River Estuary

Europe Bristol Channel

Ems-Dollard

Westerschelde³⁾

Westerschelde⁴⁾

Oosterschelde

inner middle mouth

average 1988-91

inner central outer inner central outer inner central outer freshwater inner central outer inner central outer

213 177 251

7 49 165 70 91 283 122 197 212 388 122 184 230 301 312 382

' Coleand Cloem, 1984; ²⁾Jassbyet at., 1993;³⁾VanSpaendonck et al., 1993;⁴⁾ Kromkampand Peene, 1995; all references in Heip Ct al., 1995, except Mallin et at., 1993

2. Factors influencing photosynthesis

An estuary is a place where the sea meets freshwater from the land. Different processes, like stratificating, mixing, etc., take place by the influence of tides and freshwater run- off from the rivers. The wind can be another source of turbulence which mixes the water. Figure 2.1 shows the effects of wind, tides and freshwater run-off on

phytoplankton and the important factors that influence photosynthesis. These factors will be discussed below.

2.1 Nutrients

Phytoplankton needs nutrients and energy to synthesize new biomass. In marine and estuarine waters it is generally assumed that phytoplankton is nitrogen-limited, whereas freshwater phytoplankton is phosphorus-limited (Hecky and Kilham, 1988). However, P-limitation seems to occur in the North Sea (Riegman Ct a!., 1992) and the

Oosterschelde (Kromkamp and Peene, 1998), and the relationship between dissolved inorganic nitrogen (DIN) concentrations and primary production in Chesapeake Bay was, although significant, not very strong (r2= 0.38) (Boynton et a!., 1982).

Phytoplankton has a relative constant nutrient composition (except for silicon (Si), because not all phytoplankton species need Si) and this is often expressed in terms of the Redfleld ratio (P:N:Si (Si if necessary) is 1:16:16). Assuming this constant nutrient

N

+

Figure 2.1: Processes andfactorsinfluencing algal prodcution (modified after Heip et al., 1995); IC =toxiccomponents andTSM = total suspended matter.

composition, the limiting nutrient can be estimated from the water composition by comparing nutrient and ratios. The danger with looking at concentrations of limiting nutrients, however, is that although the concentration can be low, the flux of that particular nutrient can be high.

In estuaries nutrients are derived from the adjacent land, freshwater run-off, and from the sea, both as organic as inorganic nutrients (Postma, 1985; Malone et a!., 1988).

During strong vertical temperature or salinity stratification there is little exchange between the upper and lower water layer. Nutrients become depleted in the surface layer as they, due to uptake within algal cells or as aggregates, sediment out of the photic zone, precipitate, and accumulate on the bottom (Mann and Lazier, 1991). Via

mineralisation by micro-organisms, in the microbial loop, nutrients are transformed to inorganic nutrients, which can be used by primary producers (Lath and Parson, 1994).

Although parts of these nutrients may become available again, by (molecular) diffusion through the halo- or thermocline or by temporary entrainment due to more intense mixing, the bulk of these nutrients become available again when the stratification is turned over, resulting in a mixed water column (Mann and Lazier, 1991).

Import of dissolved organic matter (DOM) can be important in estuaries. Heip et al.

(1995) showed that there was a good correlation between the netto import of DOM and primary production. Where primary production was low, there was no such relation between DOM and primary production. Due to light limitation (in turbid estuaries), remineralised nutrients from organic import remain unused and do not contribute to the autochtonous production. If no light limitation occurs, nutrient remineralisation of the allochtonous organic matter is important for autochtonous primary production, which implies the importance of a microbial loop.

During the last decades, rivers became increasingly loaded with nutrients by wastes, agricultural practices etc. This anthropogenic enrichment of N and P has led to longterm declines in Si:N and Si:P ratios (Van Bennekom and Salomons, 1981). These higher nutrient levels stimulated annual primary production in estuaries and coastal areas (figure 2.2; Boynton et al., 1982; Cadee and Hegeman, 1986 & 1993, Smayda, 1990).

As diatoms need silicon for synthesis of their frustules, the decline in Si:P and Si:N ratio's favours non-diatom blooms, and thus can support a shift in phytoplankton species composition from diatoms to flagellates and cyanobacteria (Officer and Ryther,

1980; Smayda, 1990; Hallegraeff, 1993).

400

C

— — — — —

a

—

•

—

a

100 — — — — — —

Despite efforts to combat high N and P loadings, N loads have not decreased. However, the measures taken to decrease P loading were more successful. Nevertheless, despite

the fact that in some estuaries/coastal areas the loads of phosphate decreased since the early 1980's, no proportional decline in primary production was observed (Cadee and Hegeman, 1993; De Jonge, 1997), suggesting that there is still enough phosphate available for phytoplankton primary production, and that the loadings should be further decreased. Another explanation might be that sediments have been saturated with phosphate. This phosphate may be released during summer as sediments become

reduced (Cadee and Hegeman, 1993). As a consequence of this differential reduction of N and P the N:P ratio shifted considerably. It hence has been suggested that this might be a cause for increased occurrence of nuisance blooms (Hallegn.ff, 1993). Riegman et al. (1992) concluded this from competition experiments that showed that N:P and NH4:NOj ratio's influence species composition.

A

£

(pmol r') _{Total P} 8.0 firstquarter 7.0

6.0

5.0 Primaryproduction in Maradiep

4.0 (Waddenzee)

3.0 2.0 1.0 0

45 50 55 60 65 70 75 80 85 Year I

(tmoI1') Total N

4000 first quarter a

B -

3500

3000 _{1960 1970 1980 1990}

2500 Year

I000_

45 50 55 60 65 70 75 80 85

Year

Figure2.2: Concentrations of total P and N (A,B) for the Marsdiep (the Netherlands) from 1950-1985 (De Jonge and Van Raaphorst, 1995) and primary production (C) for the Marsdiep from 1960s-1992 (Cadee and Hegeman, 1993)

2.2 Light

The second resource that is essential for photosynthesis is light. In all aquatic

ecosystems the amount of light available for photosynthesis is dependent on the solar irradiance and the attenuation of light with depth in the water column. The solar radiation reaching the water surface is dependent on the latitude, cloud cover and time of the year. It is partly reflected by the surface, dependent of the sun angle. Roughening of the surface by wind stress lowers the reflectance at low solar elevations, which _means less reflectance at higher wind speeds. The effects of windspeed, reflection and solar angle on primary production is analysed by Waisby (1997). Penetration of light into aquatic ecosystems is greatly affected by the absorption and scattering (thus attenuation) processes that take place into the water colunm. Light that penetrates the water column is absorbed by the water itself, dissolved yellow pigments, photic biota and inanimate particulate matter. All of these factors contribute to the quality of the light spectrum, dependent of their amount present (Figure 2.3). Some wavelengths are absorbed _more than others, so light quality changes with depth of the water column (Kirk, 1996).

Among other things suspended matter (TSM in Figure 2.1) influences the amount of

25 availablelight. In estuaries these

particles enter both from the river and the sea (Soetaert et al., 1994; Cloern, 1996). Circulation of these particles, that absorb and scatter light, by tidal mixing can result in waters with high turbidity (Soetaert et al., 1994), which then can result in light limitation of

War; phytoplankton production (Van Spaendonk et al., 1993; Kromkamp et

I

• a!., 1995). Also wind can cause high turbidity as fine bottom sediments are

Figure2.3: Comparisonof spectral absorption

properties of the different fractions in an estuarine resuspended (De Jonge and Van

water from Southeast Australia -LakeKing

Victoria. Phytoplankton were present at a level of Beusekom, 1992). Tidally dnven

3.6 mg ChI a m3 water turbidity was 1.0 NTU resuspension and riverine sources of

(Kirk, 1996)

________________________________

sediments might be important mechanisms in influencing suspended matter concentrations in the water column (Cloern et aL, 1989). Semi-diurnal cycles of sediment erosion as a result of the ebb and flood currents are important in macrotidal estuaries (estuaries with a mean tidal range>

4 m). The suspended sediment concentrations in macrotidal estuaries is 5-100 times

20

'

::

00

higher than in microtidal estuaries (mean tidal range <2m) (Monbet, 1992).

Phytoplankton also contributes to the attenuation of light by absorption of light by the photosynthetic pigments. In productive waters they may increase attenuation to such a high level that by self-shading they become a significant factor limiting their own population growth (Kirk, 1996; Huisman, 1997). However, selfshading is seldom very

important in estuarine waters, as compared to eutrophic/hypertrophic freshwater

systems. In estuaries, most of the light limitation is caused by scatter and absorption of suspended matter; phytoplankton is important only rarely.

The water column can, in the context of photosynthesis, be divided into a photic zone and an aphotic zone. In the photic zone there is sufficient light to sustain photosynthesis and a positive net photosynthesis. This zone is bordered by the compensation depth, the depth where the amount of light required for photosynthetic production is balanced by respiration. In the lower, aphotic zone light intensity is too low for photosynthesis (Lalli and Parson, 1994; Cloern, 1996). Besides limiting, light can also be inhibitory. High light intensities in the surface layer of natural waters can result in photoinhibition. With increasing depth and diminishing light intensities, photoinhibition lessens and the maximum, light-saturated, but not inhibited photosynthetic rate is achieved. With further increase in depth, irradiance falls to the point at which light intensities become limiting (Kirk, 1996). However in the field this photoinhibition is of minor importance as phytoplankton is circulated over a range of depths by water movements.

The critical depth is the maximum depth of a mixed surface layer that still allows phytoplankton growth (Sverdrup, 1953; Tell, 1990). The depth of water circulation is limited through the depth of the bottom or through the presence of stratified layer. If water density is uniform over the whole water column, than tidal stirring and wind can move phytoplankton cells rapidly between the surface photic zone and the deeper aphotic zone (Cloern, 1996). However as long as the depth of mixing is above the critical depth, positive net photosynthesis can occur (Kirk, 1996). The critical depth is not a fixed depth, but varies through the season (influenced by daylength and

irradiance). In winter, the critical depth can be smaller than the mixing depth, preventing algal growth. However as days lengthen, the situation improves and the spring bloom is

initiated when the critical depth is not exceeded anymore. As diatoms have generally a low rate of respiration compared to other algal species (Langdon, 1993), it are mainly diatoms which initiate the spring bloom. As a rule of thumb, it is normally assumed that the critical depth is 5-6 times the photic depth (Tell, 1990), but evidence by Grobbelaar (1990) and Kromkamp and Peene (1995) suggest that the ratio may be even higher.

2.3 Stratjfication and Vertical mixing

As noticed in previous paragraphs, the stability of the water colunm influences light and nutrient availability. Variation in the stability of the water column result from the balance between buoyancy forces (solar heating, freshwater run-off) and mechanical energy inputs (from wind, tides and also freshwater run-off) (Mann and Lazier, 1991;

Monbet, 1992; Ragueneau et aL, 1996).

In estuaries freshwater from rivers and run-off from the land meet salt water from the sea. Freshwater with a low salinity is less dense than seawater. This freshwater tends to float on the denser seawater, which can result in a stratification of the water column, independent of temperature (Mann and Lazier, 1991). On the other hand tides, wind stress and freshwater run-off are source of turbulence. These inputs of mechanical energy drive vertical mixing in the water column (Demers Ct a!., 1986; Monbet, 1992), which can break down or prevent stratification. Vertical stratification varies with changes in the strength of the tidal stirring. Fluctuations in vertical stratification

coincide with the fort-night neap-spring tidal cycle, with variations between more mixed (spring tide) and more stratified (neap tide) conditions (Cloern, 1996; Ragueneau et aL,

1996). Macrotidal estuaries are more influenced by tides than microtidal estuaries in terms of suspended matter and water column stability (Monbet, 1992).

Thus, mixing processes influence primary production. Even if the critical depth is not exceeded, increases in mixing tend to reduce total photosynthesis (Kirk, 1996). This mixing process is important for non-motile phytoplankton species, as it keeps them in suspension. Especially large diatoms will sediment out of the photic zone rapidly under calm conditions or when stratification sets in. Motile phytoplankton can migrate

up/downward, provided the turbulence is low. But for the total phytoplankton population, circulation of water within the mixed layer is a major factor influencing primary production, by reducing the light climate, and frequently determines whether such production takes place at all (Kirk, 1996). Strong vertical stratification can

effectively isolate phytoplankton in a shallow surface layer in which the mean irradiance is much higher than the irradiance averaged over the full water column. As a result of this the net growth rate of phytoplankton in the surface layer increases after the

establishment of the vertical stratification (Cloern, 1996).

Intense vertical mixing can produce changes in light conditions that fluctuate faster than the rate at which the algae can adjust their physiology (Demers et al., 1986). Wether this

will have possitive or negative effects is not clear. The literature on this is small and confusing, and nothing is known of this in relation to estuaries, so this will not be discussed further.

2.4 Interrelation

The influence of tides, freshwater run-off and wind via light and nutrients _on

phytoplankton is summarized in figure 2.1. Hydrodynamical variability is transmitted to living organisms through the availability of light and/of nutrients, since stabilisation (which may lead to nutrient depletion) nor vertical mixing (which may lead to light limitation) alone favours biogenic matter production. Phytoplankton is therefore strongly dependent upon the frequency of stabilisation-destabilisation of the water column (Levasseur et al., 1984; Demers Ct al., 1986).

Freshwater run-off for example promotes stratification, and the light climate improves by this action. In situations of stratification, nutrients will be mainly available by diffusion through the thermo- or halocline and can become depleted. Mixing might

increase the nutrient concentration but decreases the light availability, leading to light limitation as the mixing depth exceeds the compensation depth. On the other hand freshwater also carries a lot of suspended matter and can cause high turbidity and by this influence the light climate unfavourably.

Primary production increases towards the mouth of an estuary, where better light

conditions prevail, but nutrient concentrations are lower (Colijn, 1983; Van Spaendonck et al. 1993; Kromkamp et al., 1995). This indicates that the decrease in available

nutrients is more than compensated for by the increased water transparency (Heip et al., 1995).

Not only light is important or not only nutrients; the ensemble of availability of these two are important for primary production.

2.5 Other factors influencing photosynthesis: salinity and temperature

It is important to mention that other factors also do influence primary production, like salinity or temperature. However, I will show some influences, but not discuss these factors in detail here.

Just as vertical mixing acts via light and nutrients on sucession of phytoplankton species (Demers et al., 1986), salinity can also act as important factor in species succession.

Phytoplankton species composition changes markedly along the estuarine gradient._All phytoplankton species have a range of survival concerning light, salinity and

temperature (Rijstenbil, 1989). The freshwater species dominate the upper (limnic) regions of the estuaries, and the main taxa can be very different (Heip et a!., 1995).

The freshwater species will, due to osmotic stress, die and be replaced by other_more salt tolerant species further down the estuary (Kromkamp and Peene, 1995).

Pennock and Sharp (1986) showed that photosynthesis per unit chlorophyll increased exponentially with increasing temperature. Temperature possitively influences

phytoplankton as enzymes are involved in the photosynthetic process. Gallegos and Jordan (1997) showed that the relationship between nutrient enhanced growth _rate (growth rates after addition of P) and water temperature was similar to that observed in phytoplankton monocultures under nutrient saturation and constant light. Temperature stimulates growth. Scatter in the observations is due to mixed species with species- dependent maximum growth rate and optimum temperature.

3. Factors influencing phytoplankton biomass

Important parameters to estimate phytoplankton primary production are phytoplankton biomass, light and nutrients (Help et al., 1995). The previous chapter dealt with the

factors light and nutrients. In this chapter some factors influencing biomass will be discussed.

3.1 Grazing

The predation on primary producers in aquatic ecosystems takes place by zooplankton and benthos. Zooplankton, commonly defined as the animals that float in the water column and have only limited swimming capacity, can be subdivided in several ways.

On size (micro-, meso- and macrozooplankton), on the duration of the planktonic stage (holoplankton: which spending the entire life in the water; meroplankton: which is temporary planktonic or tychoplankton: which is both benthic and planktonic), by their salinity tolerance (riverine, true estuarine or brackish, estuarine and marine, euryhaline marine and stenohaline marine) or by their origin (autochtonous versus allochtonous) (Heip et a!., 1995).

The microzooplankton (zooplankton between 20 and 200iM) mainly consists of heterotrophic protozoan, of which the heterotrophic flagellates and ciliates are the most abundant groups (Barnes, 1991; Heip et a!., 1995). Also juveniles of larger planktonic and benthic organisms can (temporarily) belong to the microzooplanktonic size (Heip et a!., 1995). Protozoa partly feed on bacteria and form a link between bacterial production in higher trophic levels. They also graze on picoplankton and nanoflagellaten (Lalli and Parson, 1994) and as their maximum growth rate is comparable with that of

phytoplankton, they can respond quickly to changes in primary production. The

abundance of microzooplankton is determined by the amount of available food and how much they are preyed themselves. This group of zooplankton can cause a high grazing pressure in estuaries, up to 100% day' of bacterial and algal production and biomass (Heip et a!., 1995, table 19). Gallegos and Jordan (1997) showed in Rhode River estuary that there was a correlation between phytoplankton growth rate and grazing rate by microzooplankton (r2=0.7).

The mesozooplankton (zooplankton between 200 and 2000tM) can be subdivided in autochtonous species, that develop and spend their entire life-history in estuaries, and allochtonous species, that are derived from either the river or the sea. The biggest group

of the mesozooplankton are the copepods. Copepods can feed on both living_{or dead} food particles, although for many copepods microphytoplankton is the major part of their food (Heip et al., 1995). All copepods have a similar pattern of development: from egg (70-150 tM) to adult (0.5-3mm) via 6 naupliar and 5 copepodite stages. Copepods winter in a copepodite stage. Phytoplankton can respond more rapidly to the improving light conditions in the spring (Nybakken, 1988) then the copepods can react by building up their population, because of longer generation times. Because of this, phytoplankton can temporarily escape grazing presure and build up a bloom.

Benthos can be defined as organisms living on top of or in the sediment. Also benthos can be subdivided on size: micro- , meio-and macrofauna, on feeding mechanism:

suspension feeding, deposit feeding, predation, scavenging and absorption (reference in Heip et a!., 1995).

The animals in the meiobenthos (metazoan between 50m and 1mm) belong to many different taxonomic groups. In temperate estuaries meiobenthos is dominated by nematodes. Other important groups are gastrotrichs, large ciliates and foraminiferans.

Also larvae of many macrobenthos species belong to the size-class of the meiobenthos in a part of the year. It is still unclear if the meiofauna biomass and abundance is regulated by food supply, by predation, by physicochemical factors from the

environment or a combination of these factors. The meiobenthos may feed on detritus, bacteria and diatoms.

The macrobenthos can be divided into two broad trophic categories: the benthic

suspension feeders (e.g. Mytilus, Cerastoderma) and the benthic deposit feeders, which are of minor importance for influencing phytoplankton biomass directly, as they feed on detritus and material that consists for more than 95% of inorganic matter. Suspension feeding benthic invertebrates, such as polychaete worms and bivalve molluscs (clams, mussels) actively remove phytoplankton biomass (detritus and bacteria) from just above the sediment water interface. Other benthic animals consume phytoplankton biomass

deposited on the sediment surface. The rate of benthic grazing can be limited by the vertical flux of phytoplankton biomass from the water colunm to the sediment-water

interface (Monismith, 1990). Stratification acts, via reduced exchange between the water layers, to decouple phytoplankton from the bottom grazers (Cloern, 1991).

In this chapter the importance of grazing on phytoplankton by different types of organisms in an estuary is pointed out, however, for a more extensive review about these groups in terms of the C balance in estuaries, I refer to Heip et al. (1995).

For San Francisco Bay it was suggested that the absence of the phytoplankton sunimer blooms in 1977 and from 1987-1990 resulted from the enhanced abundance of bivalve suspension feeders that reduced phytoplankton biomass. This enhanced abundance of the bivalves was either caused by upward migration of bivalves during drought (1977) or by the invasion of an introduced bivalve (1987-1990) (Alpine and Cloern, 1992).

Also bivalve beds influence primary production: 17-59% of the primary production_are taken up daily by the bivalve beds (Smaal and Prins, 1993). Phytoplankton biomass_can be high in absence of grazers, e.g. in the upstream part of the Westerschelde estuary, where grazers are absent due to low oxygen levels (Kromkamp and Peene, 1995;

Soetaert et a!., 1994). Low oxygen levels for example can be caused by the oxidation of organic matter by bacteria.

Besides reducing phytoplankton biomass, in situ measurements showed the uptake of particulate organic matter (including phytoplankton) and release of dissolved inorganic nutrients by bivalve beds, and consequently enhanced regeneration of inorganic

nutrients. This may result in a promotion of primary production as well _{as in} eutrophication control (Smaal and Prins, 1993). In Rhode river estuary

microzooplankton grazing delayed the nutrient limitation in the late spring, by regenerating nutrients and removing phytoplankton biomass (Gallegos and Jordan, 1997). However, in many estuaries total biomass (and potential grazing rate) of benthic organisms is higher that biomass of copepods and other zooplankton (Cloem, 1982).

Because of the relatively shallow depth, estuarine ecosystems are often characterised by very intense benthic-pelagic coupling. However, in times of stratification the impact of the benthic suspension feeders will be of more or less decoupled from phytoplankton primary production as there is less interaction between the water layers (Cloern, 1991).

3.2 wash-out as afactors influencing biomass

Besides grazing phytoplankton biomass can also be low due to wash-out of the estuary.

As the residence time of the water in the estuary is smaller than the doubling time of phytoplankton, more phytoplankton biomass is washed out per unit time (Wetsteyn _an Kromkamp, 1994; Cloern et al., 1983). Although only described for macro algae (as far as I know), the opposite also can occur. Due to the presence of weak circulation zones, some local patches of water are more or less isolated from others, and in these patches macro algal biomass can be high (Piriou and Menesguen, 1992).

4. Anthropogenic influences

4.1 human impact

Human activities influence the estuaries in several ways. Although much more can be said about impact of human activities in estuaries, I will mention some in this

paragraph.

First human activities led to eutrophication, already mentioned in paragraph 2.1 and not further discussed here. Besides nutrients also other waste products, like metals and pesticides might affect growth of primary producers. Lindane concentrations (a

pesticide) accumulates in phytoplankton towards the shore in the Southern ocean (there are no data of estuaries) (Knickmeyer and Steinhart, 1989); However, there is little known about the impact of toxic contaminants on phytoplankton species composition, primary production and population growth (Cloern, 1996). Jak and Michielsen (1996) showed that the effect of pesticides might be biggest on grazers, the microzooplankton and this effect might be underestimated in many places.

Another example of human impact is the introduction of 'new' species in a region by release of seawater ballast from cargo vessels (Canton et a!., 1990). In San Francisco Bay, California, an invasion of a till then unknown bivalve mollusk occured be the end of the 1 980s. This 'new' clam, the Asian species Potamocorbula amurensis, led to major disturbance at the ecosystem level: a reduction in annual production and diverse changes in the pelagic heterotrophic community (Cloern, 1996). The clam disrupted the

established benthic community and prevented dry-period communities to re-establish in dry periods (Nichols et al., 1990).

There are several other examples of human activities influencing estuarine ecosystems, like fishery, aquaculture, construction of dams etc. In the next paragraph I want to discuss effects of changes in an estuary, where construction of dams and a storm-surge barrner changed the Delta area in S. W. Netherlands.

4.2 a case study - TheOosterschelde

The storm flood disaster in 1953 in the south-west Netherlands, resulted in a large-scale engineering project in the Delta area, carried out between 1960 and 1987 (Nienhuis and

Smaal, 1994). This project comprehended the heightening of the dikes in this region and the construction of several dams to protect the land and people.

The original plan for the Oosterschelde was to build a 9 km dam across the mouth of the estuary (to be finished in 1978). Accumulating evidence however, showed that the estuary would change by this action into a stagnant lake, influenced by polluted and eutrophicated water from the rivers Rhine and Meuse. In 1960's and early 1970's conservationists provoked awareness of the need of natural resources and the unique tidal habitat, including an extensive shellfish industry (the only one in the Netherlands) (Smies and Huiskes, 1981).

In 1976 another plan for the Oosterschelde was accepted by the government: a storm- surge barrier at the mouth of the estuary. This barrier provided that tides could freely enter the estuary, and safety in flood threatened areas could be guaranteed by closing the barner. Besides this storm-surge barrier, the Oesterdam on the eastern side and the Philipsdam on the northern side enclosed the Oosterschelde (Figure 4.1), and the estuary changed in a tidal basin. This project took place between 1977 and 1987 (Nienhuis and Smaal, 1994).

The Delta project comprehended many changes in the ecosystems in this area: the Veerse meer changed into a brackish water lake; and the Grevelingenmeer into a saline lagoon. Also the construction of the storm-surge barrier and dams led to changes in the

Figure 4.1: Location of the Oosterschelde compartments (A: western part, B: central part, C: eastern part, D: nothern part) and sampling stations.

Oosterschelde ecosystem. This chapter will mainly focus on changes in natural communities directly relating to phytoplankton in the Oosterschelde. For changes in other levels of the ecosystem in the Oosterschelde I refer to Smaal and Nienhuis (1992) and Prins and Smaal (1994).

Table 4.1 summarises changes in hydrography of the Oosterschelde. A few of these parameters will be considered in more detail.

The water balance over the period 1980-1989 showed that the main freshwater load (50 m3 1) entered the Oosterschelde via Krammer-Volkerak, via sluices in de

Volkerakdam. This freshwater was mainly derived from the river Rhine and to a smaller extent of the

Table 4.1: Mainhydrodynamic characteristics of the Oosterschelde Estuary before and after the completion of the coastal engineering works (data Tidal Water Division, Middelburg) (Wetsteyn and

Pre-barrier Post-barrier

Total surface, km2 452 351

Water surface, (MWL) km2 362 304

Tidalflats,km2 183 118

Salt marshes, km2 17.2 6.4

Cross section, 80000 17900

barrier in open position, m2

Mean tidal range, Yerseke, m 3.70 3.25 Max. flow velocity, m s_I 1.5 1.0

Residence time, d 5-50 10-150

Mean tidal volume m3 x 106 1230 880

Total volume, m3 x 106 3050 2750

Mean freshwater load, m3 S1 70 25

river Meuse. By finishing the Philipsdam this load was reduced to 10 m3 s. The Grevelingenmeer showed increased water load during lowered tidal range due to

manipulations of the flood gates in the storm-surge barrier.

Furthermore the Oesterdam prevented freshwater from the Zoommeer to enter the

Oosterschelde freely. Rainfall and evaporation compensated each In total this meant a reduction of 64% of the This decrease in freshwater reduced the nutrient loads, especially to the northern

compartment as most freshwater entered the Oosterschelde via this compartment. As the water from the northern part enters the central part via ebb tide, and this water via flood tide goes to the eastern compartment, also these compartments are influenced by lower nutrients loads (Wetsteyn and Kromkamp, 1994).

From the average molar nutrient content in phytoplankton, P:N:Si = 1:16:16 (Si in case of diatoms; Gillbricht, 1988), and the half-saturation constants for nutrient-uptake (see Fisher et a!., 1988) one can estimate the growth limiting nutrient. Dissolved inorganic nitrogen and silicate concentrations were lower in the post-barrier period and reached growth-limited levels. However, phosphate concentrations did not change, perhaps due to release from the sediment, and was not limited. The Si/N ratio was, except in winter,

Kromkamp, 1994)

other roughly (Nienhuis fonner freshwater load.

and Smaal, 1994).

below 1. Finally, the diatom population will collapse and non-silicate containing species will take over, which is consistent with observations in this region (Bakker et a!., 1990) and in coastal waters (Cadee et a!., 1986; references in Wetsteyn and Kromkamp, 1994).

Furthermore there was a location dependent reduction of the maximum flow velocities during ebb and flood, varying from 25-86% (Wetsteyn and Bakker, 1991). This resulted in a decrease in suspended matter in the Oosterschelde, a decrease in the vertical

attenuation coefficient and thus the water became more transparent (especially at the eastern and northern part). (Wetsteyn and Kromkamp, 1994).

In all parts of the Oosterschelde residence time increased; fewest in the western part and increasing towards the eastern and northern parts of the Oosterschelde. Phytoplankton biomass is washed out in at lower rate (Wetsteyn and Kromkamp, 1994). The increased residence time resulted in a stronger benthic-pelagic coupling: grazing pressure (by both zooplankton and zoobenthos) increased, leading to a stronger control of phytoplankton in summer (Bakker and Vink, 1994). Biomass of one of the dominant suspension feeders, the blue mussel, is controlled by the mussel cultures. There is a strong correlation between mussel growth, stock size of mussels and cockles (the other dominant suspension feeder), and phytoplankton production and biomass (Van Stralen and Dijkema, 1994). The effect of the mussel population is the increase of the

mineralisation rate of nutrients that were stored in phytoplankton biomass. The nutrient turn-over rates, due to regeneration by the mussel beds, are much higher than the rates

of water renewal in the Oosterschelde (Prins and Smaal, 1994).

The phytoplankton species composition changed from a year-around diatom-dominated community with a summer peak of phytoplankton biomass and primary production in the pre-barrier period (Bakker, 1994) towards a flagellates and weakly silicified diatoms community, without a seasonal trend in the post-barrier period. The phytoplankton community changed from a typical tubid, estuarine community into a tidal bay or lagoonal community (Bakker et a!., 1994), although there was a large interannual variation in records of some diatom species, which didn't show a good relation with the changed environment.

annual primary production This change in species

composition and the increased grazing pressure result in lower annual primary production.

Table 4.2 shows that annual production in the pre-barrier period (1980-1984) showed a gradient with highest production values in the western part (P5) of the Oosterschelde. In the post- barrier period (1988-1990) production in the western part was lower than before. For station P3 and 021 the annual

production values fall in the same range

Table 4.2: Annual column production (g C m2) in the Oosterschelde.

Stations P5, P3, LGPK (1987-1990) and P6: particulate +dissolved production; station 021 and LGPK (1984) (for location see figure 4.1):

particulate production. nm: not measured; *: based on monthly measurements;^**: from20 may onwards;

(From Wetsteyn and Kromkamp, 1994)

measurements until July.

Year P5 P3 021 LGPK P6

1980 nm 327 345 nm nm

1981 280" 275 338 nm nm

1982 540 406 264 nm nm

1983 283 240 380 nm nm

1984 425 373 176 176 nm

1985 nm nm 198 nm nm

1986 1987

nm

260"

nm

233"

460 250

nm

169"

nm nm

1988 nm nm 230 nm nm

1989 277 319 229 294 550

1990 223 242 nm 237 502

than in the pre-barrier period. (One has to take into account that in 021 only particulate production is measured, while dissolved production (on extracellular release) can account for 10-15% of annual total primary production (references in Wetsteyn and Kromkamp, 1994). However all values in the post-barrier period fall in the same range (except station P6). In the eastern part the increment in water transparency seems to be of greater importance than the decrease in nutrients for increment in biomass (Wetsteyn and Kromkamp, 1994).

At least for the eastern and central compartment of the Oosterschelde annual primary production has not changed. However it is difficult to say if there is a decrease in primary production in the western part, because of the big natural interannual

differences. Latest results demonstrate that the production in the western compartment did not change significantly (Kromkamp, pers. comm.).

It is amazing that the overall primary production did not change as a result of the large changes to the ecosystem. This might indicate thate there is some sort of homeostasis in the system. This stabilization might be a result of the high grazing rates by mussels.

This would corroborate the hypothesis put forward by Herman and Scholten (1990) that suspension-feeders can stabilise estuarine ecosystems.

5. Interannual variation in primary production in estuaries

Annual primary production is not the same from year to year and can show big

differences (e.g.: 337 gCm2yf' to 782 gCm2yf' mid-Chesapeake Bay in respectively 1973 and 1977; Boynton eta!., 1982 and table 5.1). What causes this variation?

There is less information about interannual variation in primary production in estuaries, and there are not so much long time series of annual primary production measurements.

A few studies report long term primary production figures: North Sea/Marsdiep (Cadee and Hegeman, 1993), Ems-Dollard Estuary (Colijn, 1983), San Francisco Bay (Cloern,

1989), Delaware Estuary (Pennock and Sharp, 1986), Neuse River estuary (Mallin et a!., 1993), Rhode River Estuary (Gallegos and Jordan, 1997), Oosterschelde (Wetsteyn and Kromkamp, 1994). Not all however showed/searched for mechanisms that explain the interannual variation.

Table5.1: Overviewof annual primary production variation in different estuaries with suggested mechanisms of control of the primary production

Estuary years annual primary primary production (PP) Reference production stimulance / control

(mm-max range) 'mechanism' gC m2 yr'

Marsdiep 1964-1992 140-390 - eutrophication (increased

nutrients)

Cadee and Hegeman, 1993

Neuse River Estuary 1988-1991 202-320 - highwatershed run-off Mallin et al., 1993

Delaware Estuary 1981-1985 190-400 - -- Pennock & Sharp, 1986

Chesapeak Bay 1972-1977 337-782 - highriver run-off (increased nutrient inflow)

Boynton et al., 1982

San Francisco Bay ??? ??? ^- highriver run-off Cloern, 1989

- duringlow run-off, grazing Alpine and Cloern,

controls PP 1987

Eutrophication of the North Sea led to an increase in primary production in the late 1970s, which stabilised in the 1980s. A decrease in P-discharges from the river Rhine since 1981, did not lead to a decrease in primary production (Cadee and Hegeman,

1993).

In the Neuse River Estuary primary production is predominantly nitrogen limited (Rudek et a!., 1991). Primary production was studied from 1988 to 1991 and varied from 202.2 till 320.0 g C m2 yr'. Mallin et a!. (1993) correlate this interannual

variation in primary production to variation in forces controlling delivery of nitrogen to the estuary. Thus, the magnitude of the estuarine primary production and periodicity of

the algal blooms are related to the variation in the upper watershed rainfall and its subsequent regulation of downstream flow in this nutrient limited systems.

In Delaware Estuary, a nutrient rich system (Sharp et a!., 1982), light regulates the biomass (Pennock, 1985). Annual primary production was calculated from 1981 to 1985 and varied between 190 and 400 g C m2 yf'. This interannual variation could not be explained.

Boynton et al. (1982) reported for Chesapeake Bay that the timing and frequency of the events were similar, while the magnitude of the maximum production was different every year. It was speculated that this variation is related to the nutrients from watershed sources, which varied with river discharge.

Cloern (1989) found that in San Francisco Bay annual primary production was generally low, except during periods of high river run-off, which caused density stratification and hence a more transparent photic zone. This effect was modified by tidal activity and most pronounced during neap tides. Both Pennock and Sharp (1986) and Cloern (1989) stress that photo-adaptation is not important, because the mixing time is too rapid for photo-adaptation to occur during vertical transport through the water column. They found that temperature and species composition were more important in explaining variability in maximum photosynthesis.

Small et al. (1990) reported an increase in biomass (and hence production) for the Columbia River Estuary as a result of an enormous pulse of water and sediments due to the eruption of the Mount St Helens.

Alpine and Cloern (1992) reported that in some years with low river run-off trophic interactions, via the colonisation of large population of suspension feeders, control phytoplankton populations.

Primary production will change with biomass (light and grazing dependent), irradiance (climate dependent) and photic zone depth varying with river run-off (salinity

stratification) in light limiting estuaries (Heip et a!., 1995, chapter 2). Estuaries which are highly influenced by freshwater run-off, via light (as mentioned above) or nutrients (by supply of the river) seems to be dependent, for bloom formation and high

production rates, on the watershed. However, in times of low river run-off trophic interactions seems to be important. So both bottom-up and top-down control perhaps explain the year-to-year variability.

Sum mary

This essay is concentrated on phytoplankton primary production in estuaries. Factors controlling this primary production, bottom-up via photosynthesis or top-down via grazing are discussed. Herein first a general outline of the factors are given important in both estuaries and other aquatic ecosystems.

Light and nutrients are the most important factors controlling photosynthesis, however other factors can also be important. These factors are influenced by tides, freshwater run-off, which can be of great importance in estuaries as they influence stabilisation- destabilisation of the water column, and wind.

Grazing in estuaries occurs by zooplankton and benthic organisms, which influence phytoplankton dynamics in two ways: directly via consumption of phytoplankton biomass and indirectly through regeneration of nutrients.

Besides these 'natural' factors human activities might influence primary production through eutrophication, toxic components in waste waters, fishery, introduction of new species that replace natural communities etc. Through the construction of dams and a storm-surge barrier, the Delta area in the S.W. Netherlands changed enormously. The Oosterschelde estuary changed by this action into a tidal basin. Primary production however, did not change.

There are big differences in primary production between years in the same estuary.

Primary production will change with biomass (light and grazing dependent), irradiance (climate dependent) and photic zone depth varying with river run-off (salinity

stratification) in light limited estuaries. Watershed seems to be important for high production rates in estuaries influenced by river run-off both via light or nutrients.

However, in times of low river un-off trophic interaction might be important. Both bottom-up and top-down control might explain the interannual variation in primary production in estuaries.

Acknowledgements

I would like to thank Dr. Jacco Kromkamp from the NIOO-CEMO te Yerseke, who offered me this subject for my essay. He provided me with the articles (and even a book) I asked for, even though it had to go from Yerseke to Groningen. The

correspondence was OK, although e-mail is not always the easiest way of

cummunication. I also want to thank Dr. Winfried Gieskes from the University in Groningen, who also corrected the text of this essay.

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