Aquatic Ecology31: 349–359, 1998. 349c 1998Kluwer Academic Publishers. Printed in the Netherlands.

A review of the feedbacks between bivalve grazing and ecosystem processes

Theo C. Prins1;3, Aad C. Smaal2 and Richard F. Dame3

1Netherlands Institute of Ecology, Centre for Estuarine and Coastal Ecology, PO Box 140, 4400 AC Yerseke, TheNetherlands;2National Institute for Coastal and Marine Management/RIKZ, PO Box 8039, 4330 EA Middelburg,The Netherlands;3Coastal Carolina University, Marine Science Department, Conway, SC 29256, USA

Accepted 23 September 1997

Key words:suspension-feeding bivalves, phytoplankton, nutrient cycling, primary production, carrying capacity

Abstract

This paper gives an overview of interactions between bivalve grazing and ecosystem processes, that may affect thecarrying capacity of ecosystems for bivalve suspension feeders. These interactions consist of a number of positiveand negative feedbacks. Bivalve grazing can result in local food depletion, which may negatively influence bivalvegrowth. On a larger scale, it may induce a top-down control of phytoplankton biomasss, and structural shifts inphytoplankton composition. In the case of harmful algal blooms, phytoplankton may negatively affect bivalvegrazing rates. The processing of large amounts of particulate matter may change nutrient cycling on the scale ofestuaries, and can result in changes in the inorganic nutrient pool available for phytoplankton, through regenerationand reduced storage of nutrients in algal biomass. This can reduce nutrient limitation of the phytoplankton andstimulate algal growth rates. Observations from mesocosm studies suggest that a positive feedback from bivalvegrazing on phytoplankton growth may also change the physiological state of the algae and improve food quality.

Introduction

For a valid evaluation of the carrying capacity of anecosystem for bivalve growth and production, it isnecessary to include processes relating to the eco-physiology of the bivalves, processes involved withthe supply of food to the bivalve populations, and pro-cesses at the ecosystem scale describing the productionand consumption of food.

One of the methods to evaluate relations betweenshellfish growth and production and their environmentis the use of simulation models. In these simulationmodels, the ecosystem is viewed as distinct compart-ments or state variables (e.g. shellfish, phytoplankton),and flows of energy or material between the compart-ments are quantified (Grant et al., 1993). Simulationmodels can have various levels of complexity, andthe focus of the models can be oriented more on theecophysiology of the bivalves concerned, on physicaltransport processes in the environment, or on ecosys-tem scale processes. The models may therefore widelydiffer in the temporal and spatial scales of the processes

that are described by the model. In many physiolo-gical models, the supply and composition of food isdescribed as a forcing function (e.g. Willows, 1992)and these models typically depict processes at timescales of minutes to hours. On the other hand, manywhole ecosystem models are simulating processes attime scales of days to years, and do not actually modelbivalve suspension feeders as state variables, mainlybecause of the difference in time scales between eco-system processes and factors that are relevant to bivalvephysiology (see Herman, 1993 for a more elaboratediscussion on this topic). Furthermore, the physicaltransport processes that are described in some models,may work on the spatial scale of an entire bivalve bed,or may focus on boundary layer transport processes(Frechette et al., 1993; Wildish & Kristmanson, 1993).Coupling physiological, physical and ecosystem pro-cesses presents technical modeling problems becauseof the differences in spatial and temporal scales, thatcan be solved, at least in part, by parameterization ofsome of the functional relationships (see Grant et al.,1993; Herman, 1993). In this paper, we focus on the

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links between bivalve physiology, the physical envir-onment and ecosystem level processes. We will identi-fy a number of positive and negative feedbacks betweenthese three levels, that may be of quantitative signific-ance for the outcome of a carrying capacity model. Theexamples that we will discuss to a large extent comefrom ecosystem studies in the Oosterschelde estuary,SW Netherlands (Smaal & Nienhuis, 1992; Nienhuis& Smaal, 1994), and in North Inlet, South Carolina(Dame et al., 1989; Dame & Libes, 1993), and frommesocosm studies (Prins et al., 1995a,b and unpub-lished results).

Food depletion

Bivalves live in a highly dynamic physical environ-ment, and abiotic forcing results in large variabilityin the quantity and quality of the suspended matterthat serves as their food. Variability occurs on the timescales of minutes to hours, and the tidal changes in ses-ton concentrations and composition can be as large asseasonal changes. This variability is related to advect-ive processes, resuspension induced by tidal currentsand wind-induced wave action (Berg & Newell, 1986;Smaal et al., 1986; Frechette et al., 1989; Asmus etal., 1990; Grant et al., 1990; Frechette & Grant, 1991;Fegley et al., 1992; Prins et al., 1996; Smaal & Haas,1997).

In addition to this temporal variability, there maybe significant spatial variation in food supply as a con-sequence of the filtration activity of the bivalves. Fil-tration of phytoplankton from the water flowing acrossbivalve communities often leads to a depletion of thebenthic boundary layer, and consequently, lower foodconcentrations for the bivalves downstream. This pro-cess has been observed in a number of flume studies(Wildish & Kristmanson, 1984; Butman et al., 1994),but also underin situ conditions (Frechette & Bour-get, 1985b). This depletion of food can result in lowergrowth rates for the bivalves in the inner patches of abed (Newell, 1990). Obviously, seston depletion is notlimited to the benthic boundary layer. In raft culturesin Northwest Spain phytoplankton concentrations atthe downstream end of the raft are significantly lowerthan at the upstream end (Navarro et al., 1991). Like-wise, depletion of chorophyll was observed in an areaof extensive mussel culture in the Wadden Sea (Cadee& Hegeman, 1974).

Local depletion of food in an area with high bivalvesuspension feeder biomass is not the rule, however.

Studies in the Oosterschelde estuary failed to showdepletion of chlorophyll-a in the near bottom layerabove a mussel bed. In contrast, seston concentrationsand chlorophyll-a levels near the bottom are generallyhigher than surface values, showing the importance ofresuspension (Smaal & Haas, 1997). On a larger scale,it appears that there is no decrease in chlorophyll-ain the water after passing across a mussel lot (Prins,1996), indicating that advection may be the dominantprocess in a system with strong tidal currents.

Local depletion of food can set serious constraintson the growth of bivalves and the feasibility of shell-fish culture. As argued by Grant (1996), the relationof bivalve production to their food supply is scale-dependent, varying from competition between indi-viduals on a local scale to system-wide interactionsbetween culture sites. There may be a large poten-tial for the management of the local food competition,requiring knowledge of the interactions between thephysical environment and food supply to local bivalvepopulations.

Harmful algal blooms

Phytoplankton is generally assumed to be the mostimportant food source for bivalves in many estuaries,although microphytobenthosor detritus (e.g. kelp frag-ments; Grant & Cranford, 1991) may be an additionalfood source in some systems. A number of empiricalstudies show that bivalve growth is related to phyto-plankton biomass or production (Beukema & Cadee,1986; Blanton et al., 1987; Smaal & Van Stralen,1990).

Not all phytoplankton species may be equal in foodquality, however, and there is increasing evidence thatsome phytoplankton species may be harmful becausethey are inedible or even toxic to bivalves. A casein point is the haptophytePhaeocystissp., that mayform blooms of large colonies of cells embedded inmucus. In dense blooms, depression of clearance ratesof the musselMytilus edulisand the tellinidMacomabalthica can occur (Kamermans, 1994; Prins et al.,1994; Smaal & Twisk, 1997) and retarded growth ofbivalves in the western Wadden Sea was related toblooms ofPhaeocystissp. (Pieters et al., 1980; Beuk-ema & Cadee, 1991). There are similar observationsof toxic effects on physiological rates of bivalves inrelation to blooms of several species of dinoflagellates(Widdows et al., 1979; Lesser & Shumway, 1993;Luckenbach et al., 1993) and the chrysophyceanAure-

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ococcus anophegerens(Tracey, 1988). In North Caro-lina, massive kills of shellfish have been caused by thetoxic ambush-predator dinoflagellatePfiesteria pisci-cida (Burkholder et al., 1995).

Eutrophication is assumed to be one of the causesfor the increase in blooms of harmful algal species(Smayda, 1990), and excessive eutrophication maytherefore result in an uncouplingof primary productionand bivalve growth.

Nutrient retention and sediment biogeochemistry

Bivalve beds process large amounts of particulate mat-ter that is partly stored in the sediment as biodeposits.The high production of biodeposits can result in anenrichment of the sediment with organic matter. Thebiodeposits accumulate in the sediment, especially inthe case of epibenthic bivalves that form extensive bedsor reefs, like the blue mussel or the Eastern oyster.Some of this material may be resuspended, anotherfraction is mineralized and may be released into thewater column as inorganic nutrients. These processesdo not necessarily affect all nutrients in a similar fash-ion.

Resuspension of biodeposits, as a consequence oftidal currents or wave action, can result in a largerelease of POC and phaeopigments (Frechette & Bour-get, 1985a; Asmus et al., 1990; Prins et al., 1996). As aconsequence of pre-ingestive selection of phytoplank-ton and digestive processes, faeces and pseudofaeceshave a relatively low content of phytoplankton-derivedorganic matter, compared to the seston. Therefore,resuspension of part of the biodeposits will result ina flux of detritus to the water column, with a compos-ition that differs from the flux of seston to the bivalvebed.In situ studies in the Oosterschelde estuary showthat, as a net effect of filtration and resuspension, thebivalve population mainly acts as a selective filter forphytoplankton (Prins et al., 1996).

Benthic mineralization rates may also affect thestoichiometry of the sediment-water fluxes of inorganicnutrients. Several studies show that phosphate fluxesmay be more strongly affected by adsorption processesin the sediment than nitrogen fluxes.

Calculations of total P fluxes in and out of a musselbed suggest that a part of the P is retained, whereasthe inorganic N release approximately balances par-ticulate organic N uptake (Prins & Smaal, 1994). Amore extensive annual budget study of an oyster reefin North Inlet showed that oyster reefs are a major sink

of P, and only a small fraction of the total P uptake isreleased again as phosphate (Dame et al., 1989).

In the case of suspended cultures of bivalves, thesediments under the rafts or long lines often accumu-late large quantities of organic matter. This may leadto increased levels of oxygen demand and nitrogenregeneration compared to reference sites. The sed-iment under suspended bivalve cultures has a largeammonium pool, and ammonium release rates fromthe sediment are high (Kaspar et al., 1985; Baud-inet et al., 1990; Grant et al., 1995). Kaspar et al.(1985) argued that the prevailing anaerobic conditionsin the sediment, induced by the high organic loading,may promote denitrification.Bivalve culture could thusfunction as a sink of nitrogen, removing nitrogen fromthe aquatic environment not only by the harvesting ofthe bivalves, but also due to a loss of nitrogen to theatmosphere.

Increased nutrient availability

As the sediment surrounding bivalve populations tendsto be enriched with organic matter, nutrient regenera-tion rates from the substrate are among the highestobserved in the marine environment (Prins & Smaal,1994). Bivalve populations may, thus, form a majorfeedback loop by translocating particulate nutrientsfrom the water column to the sediment, indirectly stim-ulating benthic mineralization and inorganic nutrientfluxes from the sediment to the water column (Dameet al., 1984). Bivalves also directly excrete inorgan-ic nutrients, although excretion is less important thanmineralization in most cases (Dame et al., 1989; Asmuset al., 1990, 1995; Prins & Smaal, 1994). On thescale of entire ecosystems, the amounts of inorgan-ic nutrients released from bivalve populations and theadjacent sediment may be a major source of nutrientsfor primary producers. For example, estimates for theOosterschelde estuary, based onin situmeasured fluxesfrom mussel beds and estimates of total nitrogen min-eralization, showed that fluxes from mussel beds canaccount for a major part of total nitrogen mineraliza-tion in summer (Figure 1). A comprehensive study ofmaterial fluxes in a marsh-estuarine basin within NorthInlet showed that the oyster reefs are the main sourceof ammonium (Dame et al., 1991). It has been arguedthat, under nutrient limiting conditions, this enhancednutrient recycling may stimulate primary production(Asmus & Asmus, 1991; Dame, 1993).

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Figure 1. The amount of nitrogen regenerated by mussel beds inthe central part of the Oosterschelde estuary, compared to estimatesof total nitrogen mineralization (benthic+ pelagic). The amountof nitrogen regenerated by mussel beds was estimated fromin situmeasured fluxes of DIN between mussel beds and the water column,and data on total mussel biomass. Total nitrogen mineralizationrates were derived from the results of the Oosterschelde ecosystemsimulation model SMOES (Klepper et al., 1994). The vertical barsrepresent the 10–90% percentiles of model estimates, the horizontalbars indicate the median value. From: Prins & Smaal (1994).

Sterner (1986) argued that increased inorganicnutrient availability not only comes from nutrientregeneration by the grazers, but also from reductionsin algal concentrations and consequently lower storageof nutrients in algal biomass. In a mesocosm experi-ment conducted in spring 1993, the effect of bivalves onnutrient cycling was studied by adding different densit-ies of the blue musselMytilus edulisto each of four sys-tems. Mussel densities were chosen to represent a rangeof environments, from estuarine systems with a domin-ant bivalve biomass (>3 g ADW m�3) to systems witha predominantly pelagic food web (<0.5 g ADW m�3).

Figure 2. The amounts of P in the pools of particulate P and phos-phate in the water column of four mesocosms with different musselbiomass. Mussel biomass in the mesocosms is indicated (in g ADWm�3). The curves were fitted by a LOWESS regression (Wilkinson,1992).

The mesocosms were designed to reproduce conditionsin the Dutch coastal zone with respect to light, turbu-lence and nutrient loading (Prins et al., 1995b). Eachexperimental system received a similar external nutri-ent loading, and primary production was phosphatelimited. Grazing by the bivalves effectively controlledalgal biomass in the mesocosms with high mussel dens-ities, and this resulted in a low storage of particulate Pin pelagic biomass, and an increase of the inorganic Ppool, with the largest pool of inorganic nutrients in themesocosms with the highest mussel density (Figure 2).A tentative phosphorus balance indicated that pelagicregeneration was high in the mesocosms with low mus-sel density, and total P-regeneration (benthic+ pela-gic) was actually the highest in the mesocosm with lowmussel density (Prins et al., 1995b). This illustrates thepoint made by Sterner (1986), that reduced storage ofnutrients in phytoplankton due to grazing, rather thanenhanced nutrient regeneration, can increase inorganicnutrient availability.

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An in situ experimental manipulation of bivalvedensity, to study the effects on system level, was car-ried out by Dame & Libes (1993). They manipulatedoyster biomass in a number of replicated marsh creeks,and observed higher ammonium concentrations in thecreeks with oysters when compared to creeks withoutoysters. Chlorophyll-a concentrations were not signi-ficantly altered by the manipulation, and the authorssuggest that the effect of the bivalves on the inorganicnutrient pool in the water column was mainly due tonutrient excretion.

The examples from mesocosm research and fromNorth Inlet show that bivalves can affect inorganicnutrient levels on a system scale. This can happenthrough the process of enhanced nutrient regenerationand through reduced storage of nutrients in phyto-plankton. Enhanced nutrient availability can stimulateprimary production under conditions of nutrient limit-ation, as will be discussed below.

Effects of bivalve grazing on phytoplanktonbiomass

Bivalves are often the most abundant suspension feed-ers in estuarine systems, even when densities are notenhanced by mariculture activities (e.g. North Inlet;Dame, 1996). Low phytoplankton densities have beenattributed to high grazing rates by the bivalves. Thefirst inference about control of phytoplankton biomasson the scale of an entire estuary was made for San Fran-cisco Bay (Cloern, 1982; Officer et al., 1982). Sincethen, there has been a proliferation of studies indic-ating that bivalve grazing may control phytoplanktonbiomass in a range of estuarine systems (for reviews,see Smaal & Prins, 1993; Dame, 1996). A significantimpact of bivalve grazing can be expected when bivalveclearance time is approximately equal to phytoplank-ton turnover time and shorter than water residence time(Dame & Prins, 1997).

The top-down control of phytoplankton biomassby bivalve grazing implies that bottom-up controlof phytoplankton development (e.g. nutrient loading)becomes less important. As was pointed out by Her-man & Scholten (1990) this means that an ecosys-tem is more resilient to changes in external nutrientloading, and consequently, bivalve grazing can act asan eutrophication control. Results from a series ofmesocosm experiments, carried out in summer 1993and spring and summer 1994, clearly depict this phe-nomenon. In these experiments, silicate was the limit-

Figure 3. Average chlorophyll-a concentrations in a series of meso-cosm experiments with different mussel densities and differentexternal Si-loading. L: low mussel biomass (< 1 g ADW m�3); M:intermediate mussel biomass (1–2.7 g ADW m�3); H: high musselbiomass (>2.7 g ADW m�3). In all mesocosms, initial chlorophyll-a concentrations were identical, irradiance was comparable and Siwas the limiting nutrient.

ing factor for phytoplanktonproduction, and both silic-ate loading and mussel biomass were varied. The res-ults (Figure 3) showed that at low mussel biomass aver-age phytoplankton biomass shows a positive responseto increased nutrient loading (bottom-up control). Inthe systems with high mussel biomass phytoplanktonbiomass was low and independent of external nutrientloading (top-down control). Essentially the same phe-nomena are observed in freshwater lakes, where phyto-plankton biomass shows a strong response to externalnutrient loading in the absence of large zooplanktongrazers, but no or a weak response to nutrient load-ing in the presence of large zooplankton (Mazumder &Lean, 1994). An essential difference between bivalvesand zooplankton is the much lower metabolic rate ofmost bivalve species, enabling them to survive periodswith low food concentrations. Therefore, bivalve pop-ulations will already be present when a phytoplanktonbloom develops, whereas zooplankton developmentlags behind the phytoplankton bloom. Accordingly,top-down control by bivalve suspension-feeders willbe more efficient than control by zooplankton.

Phytoplankton biomass is determined by bottom-up (i.e. nutrients, light) and top-down (i.e. grazing)forces. In systems with abundant bivalve populations,top-down control will prevail in most cases, and thismeans that increasing the nutrient load may result inan only limited response of phytoplankton biomass.From an aquaculture point of view, this also meansthat the effect of fertilization of estuaries will be lim-ited. From a water management point of view, thisimplies that bivalves could be used for eutrophicationcontrol (Officer et al., 1982; Takeda & Kurihara,1994).

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However, the surplus of nutrients increases the prob-ability of blooms of ungrazable algae likePhaeocystissp., or an increasing dominance of macrophytes, andthis would result in a breakdown of the top-down con-trol of algal biomass by bivalve suspension feeders.

Grazing-induced structural changes in the pelagicsystem

Bivalve grazing induces a strong coupling between thepelagic and the benthic subsystems. As a consequence,the pelagic system is strongly affected by the largeexport of organic matter from the water column tothe benthic system. This effect may be illustrated bysome of the changes in the pelagic system of Ches-apeake Bay, that have been ascribed to the reductionof the oyster stock due to pollution, overexploitationand disease. Newell (1988) argued that the decline inoysters has resulted in an increase in planktonic sus-pension feeders and a predominantly pelagic food web.It has been hypothesized that the cascading effect oftop-down control of mesozooplankton by ctenophoreand fish results in high algal concentrations, and a res-toration of oyster stocks could lead to reduced phyto-plankton biomass through grazing and reduced stocksof gelatinous zooplankton through competition. Anincrease in oyster biomass might even have positiveeffects on fish stocks (Ulanowicz & Tuttle, 1992).

Mesocosm experiments have also shown thatbivalve grazing may result in shifts in phytoplanktoncomposition. Grazing in general may favor faster grow-ing algal species, or algal species that are less suscept-ible to grazing (Furnas, 1990). Enclosure experimentswith high mussel grazing rates (clearance times of lessthan 1 day) resulted in a predominance of algal cellsin the picoplankton size range (Riemann et al., 1988;Olsson et al., 1992; Graneli et al., 1993). Experimentsin mesocosms with a more environmentally realisticmussel biomass, showed that mussel grazing inducedshifts in phytoplankton species composition (Prins etal., 1995b). There is also evidence that bivalve grazingmay have an effect on the abundance of heterotroph-ic plankton organisms, either through competition forfood or through filtration of microzooplankton species(Horsted et al., 1988; Prins et al., 1995b) and possiblyeven filtration of copepod nauplii (Kimmerer et al.,1994).

Positive feedback on phytoplankton growth

Field and laboratory observations suggest that grazing,while reducing plant biomass, may have a stimulat-ory effect on plant growth rates (McNaughton, 1979;Sterner, 1986). In aquatic systems, the mechanismsinvolved in this positive feedback, can be (Dame,1996): increased light in the water column; the crop-ping of large algal cells, leading to a more logarithmicgrowth rate; shifts to faster growing species; highernutrient recycling rates and higher nutrient availab-ility due to reduced storage in algal biomass. Someof the mechanisms are a result of reductions in algalbiomass, or changes in plankton structure, as a con-sequence of grazing, as discussed earlier. Other mech-anisms are the result of the effects of grazers on theinorganic nutrient pools, as discussed above. Effectsof bivalve grazing on phytoplankton growth rates aredifficult to establish on the scale of an ecosystem, butresults from experimental ecosystems show a positivefeedback of bivalve grazing on phytoplankton growthrates. In experiments in the MERL mesocosms withthe Northern quahogMercenaria mercenaria, phyto-plankton growth rates were higher in mesocosms withclams compared to mesocosms without clams (Doer-ing et al., 1986). The higher primary production in thepresence of clams was attributed in part to the high-er flux of inorganic nitrogen from the benthos to thewater column. In the spring of 1993, experiments withfour land-based mesocosms with varying biomass ofmussels showed that chlorophyll-a concentrations andprimary production were negatively correlated withmussel biomass. However, the specific growth rates ofthe phytoplankton showed a positive correlation withmussel biomass because primary production showed aproportionallyweaker negative response to mussel bio-mass than chlorophyll-a did (Figure 4). The increasedgrowth rate of the algae was attributed to increasednutrient availability and shifts in phytoplankton com-position (Prins et al., 1995b).

Positive feedback of bivalve density on bivalvegrowth

There is increasing evidence from freshwater literat-ure, that the quality of phytoplankton as a food forzooplankton depends on the physiological state ofthe algae. The elemental composition of the algaeis affected by nutrient limitation, and P-limitation infreshwater systems causes a decline in the food quality

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Figure 4. Average chlorophyll-a concentration and primary produc-tion (panel A), and specific growth rate of the phytoplankton (panelB) as a function of mussel biomass in a mesocosm experiment.Adapted from: Prins et al. (1995a), Tables 2 and 3.

of the algae, whereas N-limitation has a relatively lim-ited effect (Sommer, 1992; Sterner et al., 1993). Thedecline in food quality may also be associated withmorphological changes of the algae (Sterner & Hessen,1994). We are not aware of any conclusive evidenceof similar phenomena in marine systems. However,in the spring 1993 mesocosm experiments, describedabove (Prins et al., 1995b), it was observed that mus-sel growth rates were highest at intermediate musseldensities (Figure 5). Low mussel growth rates at thehighest mussel density were presumably the effect ofinterspecific competion. The mesocosm with the low-est mussel biomass also showed low mussel growthrates, whereas it had the highest phytoplankton bio-mass, suggesting that food concentration apparentlywas not the cause of the low mussel growth in thissystem. As was discussed above, inorganic nutrientavailability was positively related to mussel biomass,and hence nutrient limitation (in this case: phosphate)of the phytoplankton was strongest in the mesocosms

Figure 5. Average concentrations of chlorophyll-a, average N:Pratio of the seston, and instantaneous growth rates of the mussels(mean� s.e.) as a function of mussel biomass in four mesocosms.Adapted from: Prins et al. (1995a), and unpublished results.

with low mussel biomass. This was illustrated by theN:P ratios of the particulate organic matter in the ses-ton, that increased with increasing P-limitation.

With exception of the mesocosm with the highestmussel biomass, growth rates of the mussels decreasedas the N:P ratios of the seston increased. This mightindicate that nutrient limitation of the phytoplanktonaffects food quality. Mussel growth rates may havereflected the combination of a negative and a posit-ive feedback between mussel density and food supply:a negative feedback at high mussel density caused byfood depletion, and a positive feedback at lower musseldensities caused by a weakening of the nutrient lim-itation of the phytoplankton. Although the latter dataare too restricted for final conclusions, in combination

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Table 1. Summary of relevant feedbacks in bivalve dominated ecosystems

Process involved Direct effect Consequences

Filtration (local scale) Local depletion of food Bivalve growth reduction

Blooming of Reduced filtration Reduced top-down control

harmful/unedible algae of algal blooms

id. Changes in physiological Bivalve growth reduction

rates

Biodeposition Retention of nutrients Changes in stoichiometry of

pelagic inorganic nutrient pool

Mineralization of Release of inorganic Increase of pelagic

biodeposits nutrients to water column inorganic nutrient pool

Filtration (system scale) Reduced storage of Increase of pelagic

nutrients in algal biomass inorganic nutrient pool

id. Top-down control of Reduced bottom-up effect

phytoplankton biomass of nutrient loading on

phytoplankton

id. Exclusion of slow-growing Change in phytoplankton

phytoplankton species composition

id. Increased mortality of Changes in trophic structure

zooplankton of pelagic food web

Change in phytoplankton Change in primary Change in carrying capacity

composition production

Change in inorganic Change in primary Change in carrying capacity

nutrient pool production

Change in primary Change in carrying capacity Change in nutrient growth

limitation phytoplankton

with the freshwater literature they suggest that this is afield of research that needs further exploration.

Final remarks

Decision making with respect to sustainable exploita-tion of areas for shellfish culture requires knowledge ofthe complex relations between the bivalve species andtheir environment. These relations depend on a numberof factors, i.e. physiology and population dynamics ofthe species involved, environmental conditions, spatialand temporal scales of the culture, and managementstrategies. Simulation models often are a useful tool tointegrate these relationships and evaluate managementstrategies. The modeling should include physiologic-al characteristics of the bivalve, and ecosystem pro-cesses, e.g. hydrodynamics, primary productivity, andcompetition with other species. The models should beable to predict responses in terms of bivalve growth,in relation to different management strategies. Of par-ticular interest are the interactions between the speciesand ecosystem level processes, which may influence

the carrying capacity of the system through a set ofpositive and negative feedbacks.

In this paper, we have tried to identify a numberof feedbacks that we consider relevant in terms ofcarrying capacity (Table 1). These feedbacks includeboth effects from ecosystem level processes on thephysiology and growth of the individual bivalve, andpotential feedback mechanisms as a result of bivalveactivity that affect phytoplankton biomass and primaryproductivity or the quality of the main food source,phytoplankton. In this review, we have mainly con-sidered the feedbacks between bivalve populations andecosystem processes as a function of bivalve density. Itshould be realized that the structure of the bivalve com-munity may significantly modulate these relationships.For example, natural mussel beds are often covered byepiphytic algae (e.g.Fucusspp.), that can form an effi-cient barrier for inorganic nutrient transfer from thebenthic system to the water column (Asmus & Asmus,1991). Similarly, oyster reefs are three-dimensionalstructures that provide numerousmicrohabitats for oth-er species (Dame, 1996). It is obvious, that materialfluxes between the bivalve community and the water

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column will be influenced by the co-occurring floraand fauna in the reef.

The negative feedbacks on phytoplankton biomassby grazing may be partly counteracted by positive feed-backs on phytoplankton growth rates, and this canhave a significant impact on the carrying capacity ofan ecosystem. The combination of positive and neg-ative feedbacks potentially stabilizes the productivityof the system, and increases the functional and struc-tural sustainability of the ecosystems (Dame, 1996).In our view, an evaluation of the carrying capacity ofan ecosystem for bivalve culture, either through thedevelopment of a simulation model or through someother type of analysis, needs to take these factors intoconsideration.

Acknowledgements

This work was supported by the European UnionTROPHEE project (contract FAR AQ 2500). TP wassupported by grants from KNAW (Royal NetherlandsAcademy of Arts and Sciences), NWO (NetherlandsOrganization for Scientific Research), and Award no.DEB-950957 from the National Science Foundation.TP wishes to thank the colleagues from the B.W.Baruch Institute for their hospitality. This is Public-ation no. 2349 of the Netherlands Institute of Ecology,Centre for Estuarine and Coastal Ecology.

References

Asmus, H, Asmus R and Reise K (1990) Exchange processes in anintertidal mussel bed: a Sylt-flume study in the Wadden Sea. BerBiol Anst Helgoland 6: 1–79

Asmus H, Asmus RM and Frances Zubillaga G (1995) Do musselbeds intensify the phosphorus exchange between sediment andtidal waters? Ophelia 41: 37–55

Asmus RM and Asmus H (1991) Mussel beds: limiting or promotingphytoplankton? J Exp Mar Biol Ecol 148: 215–232

Baudinet D, Alliot E, Berland B, Grenz C, Plante-Cuny M-R, PlanteR and Salen-Picard C (1990) Incidence of mussel culture onbiogeochemical fluxes at the sediment-water interface. Hydrobi-ologia 207: 187–196

Berg JA and Newell RIE (1986) Temporal and spatial variationsin the composition of seston available to the suspension feederCrassostrea virginica. Estuar Coast Shelf Sci 23: 375–386

Beukema JJ and Cadee GC (1986) Zoobenthos response to eutroph-ication of the Dutch Wadden Sea. Ophelia 26: 55–64

Beukema JJ and Cadee GC (1991) Growth rates of the bivalveMacoma balthicain the Wadden Sea during a period of eutroph-ication: relationships with concentrations of pelagic diatoms andflagellates. Mar Ecol Prog Ser 68: 249–256

Blanton JO, Tenore KR, Castillejo F, Atkinson LP, Schwing FBand Lavin A (1987) The relationship of upwelling to musselproduction in the rias on the western coast of Spain. J Mar Res45: 497–511

Burkholder JM, Glasgow HB Jr. and Hobbs CW (1995) Fish killslinked to a toxic ambush-predator dinoflagellate: distribution andenvironmental conditions. Mar Ecol Prog Ser 124: 43–61

Butman CA, Frechette M, Geyer WR and Starczak VR (1994) Flumeexperiments on food supply to the blue musselMytilus edulisL.as a function of boundary layer flow. Limnol Oceanogr 39: 1755–1768

Cadee GC and Hegeman J (1974) Primary production of phytoplank-ton in the Wadden Sea. Neth J Sea Res 8: 240–259

Cloern JE (1982) Does the benthos control phytoplankton biomassin South San Francisco Bay? Mar Ecol Prog Ser 9: 191–202

Dame RF (1993) Bivalve filter feeders in estuarine and coastal eco-system processes. Springer-Verlag, Berlin, 579 pp.

Dame RF (1996) Ecology of marine bivalves: an ecosystemapproach. CRC Press, Boca Raton, 254 pp.

Dame RF and Libes S (1993) Oyster reefs and nutrient retention intidal creeks. J Exp Mar Biol Ecol 171: 251–258

Dame RF and Prins TC (1998) Bivalve carrying capacity in coastalecosystems. Aquat Ecol 31: 409–421

Dame RF, Zingmark RG and Haskin E (1984) Oyster reefs as pro-cessors of estuarine materials. J. exp. mar. Biol. Ecol. 83: 239–247

Dame RF, Spurrier JD and Wolaver TG (1989) Carbon, nitrogen andphosphorus processing by an oyster reef. Mar Ecol Prog Ser 54:249–256

Dame RF, Spurrier JD, Williams TM, Kjerfve B, Zingmark RG,Wolaver TG, Chrzanowski TH, McKellar HN and Vernberg FJ(1991) Annual material processing by a salt marsh-estuarine basinin South Carolina, USA. Mar Ecol Prog Ser 72: 153–166

Doering PH, Oviatt CA and Kelly JR (1986). The effects of thefilter-feeding clamMercenaria mercenariaon carbon cycling inexperimental marine mesocosms. J Mar Res 44: 839–861

Fegley SR, MacDonald BA and Jacobsen TR (1992) Short-termvariation in the quantity and quality of seston available to benthicsuspension feeders. Estuar Coast Shelf Sci 34: 393–412

Frechette M. and Bourget E (1985a) Energy flow between the pelagicand benthic zones: factors controlling particulate organic matteravailable to an intertidal mussel bed. Can J Fish Aquat Sci 42:1158–1165

Frechette M. and Bourget E (1985b) Food-limited growth ofMytilusedulis L. in relation to the benthic boundary layer. Can. J FishAquat Sci 42: 1166–1170

Frechette, M. and Grant J (1991) An in situ estimation of the effectof wind-driven resuspension on the growth of the musselMytilusedulisL. J Exp Mar Biol Ecol 148: 201–213

Frechette M, Butman CA and Geyer WR (1989) The importance ofboundary-layer flows in supplying phytoplankton to the benthicsuspension feeder,Mytilus edulisL. Limnol Oceanogr 34: 19–36

Frechette M, Lefaivre D and Butman CA (1993) Bivalve feedingand the benthic boundary layer. In: Dame RF (ed.), Bivalve filterfeeders in estuarine and coastal ecosystem processes. Springer-Verlag, Berlin, pp. 325–370

Furnas, MJ (1990) In situ growth rates of marine phytoplankton:approaches to measurement, community and species growthrates. J Plankton Res 12: 1117–1151

Graneli E, Olsson P, Carlsson P, Graneli W and Nylander C (1993).Weak ‘top-down’ control of dinoflagelate growth in the coastalSkagerrak. J Plankton Res 15: 213–237

Grant J (1996) The relationship of bioenergetics and the environmentto the field growth of cultured bivalves. J Exp Mar Biol Ecol 200:239–256

358

Grant J. and Cranford PJ (1991) Carbon and nitrogen scope forgrowth as a function of diet in the sea scallopPlacopecten magel-lanicus. J Mar Biol Ass UK 71: 437–450

Grant J, Enright CT and Griswold A (1990) Resuspension and growthof Ostrea edulis: a field experiment. Mar Biol 104: 51–59

Grant J, Dowd M, Thompson K, Emerson C and Hatcher A(1993) Perspectives on field studies and related biological mod-els of bivalve growth and carrying capacity. In: Dame RF (ed.),Bivalve filter feeders in estuarine and coastal ecosystem pro-cesses. Springer-Verlag, Berlin, pp. 371–420

Grant J, Hatcher A, Scott DB, Pocklington P, Schafer CT and WintersGV (1995) A multidisciplinary approach to evaluating impactsof shellfish aquaculture on benthic communities. Estuaries 18:124–144

Herman PMJ (1993) A set of models to investigate the role of benthicsuspension feeders in estuarine ecosystems. In: Dame RF (ed.),Bivalve filter feeders in estuarine and coastal ecosystem pro-cesses. Springer-Verlag, Berlin, pp. 421–454.

Herman PMJ and Scholten H (1990) Can suspension-feeders sta-bilize estuarine ecosystems? In: Barnes M and Gibson R (eds.),Trophic relationships in the marine environment. Aberdeen Uni-versity Press, Aberdeen, pp. 104–116

Horsted SJ, Nielsen TG, Riemann B, Pock-Steen J and Bjørnsen PK(1988) Regulation of zooplankton by suspension-feeding bivalvesand fish in estuarine enclosures. Mar Ecol Prog Ser 48: 217–224

Kamermans P (1994) Nutritional value of solitary cells and coloniesof Phaeocystissp. for the bivalveMacoma balthica(L). Ophelia39: 35–44

Kaspar HF, Gillespie PA, Boyer IC and McKenzie AL (1985) Effectsof mussel aquaculture on the nitrogen cycle and benthic com-munities in Kenepuru Sound, Marlborough Sounds, New Zeal-and. Mar Biol 85: 127–136

Kimmerer WJ, Gartside E and Orsi JJ (1994) Predation by an intro-duced clam as the likely cause of substantial declines in zooplank-ton of San Francisco Bay. Mar Ecol Prog Ser 113: 81–93

Klepper O, Van der Tol MWM, Scholten H and Herman PMJ (1994)SMOES: a simulation model for the Oosterschelde ecosystem.I. Description and uncertainty analysis. Hydrobiologia 282/283:437–451

Lesser MP and Shumway SE (1993) Effects of toxic dinoflagellateson clearance rates and survival in juvenile bivalve molluscs. JShellfish Res 12: 377–381

Luckenbach MW, Sellner KG, Shumway SE and Greene K (1993)Effects of 2 bloom-forming dinoflagellates,Prorocentrum min-imum and Gyrodinium uncatenum, on the growth and survivalof the Eastern oyster,Crassostrea virginica(Gmelin 1791). JShellfish Res 12: 411–415

Mazumder A and Lean DRS (1994) Consumer-dependent responsesof lake ecosystems to nutrient loading. J Plankton Res 16: 1567–1580

McNaughton SJ (1979) Grazing as an optimization process: grass-ungulate relationships in the Serengeti. Amer Nat 113: 691–703

Navarro E, Iglesias JIP, Perez Camacho A, Labarta U and Beiras R(1991) The physiological energetics of mussels (Mytilus gallo-provincialis Lmk) from different cultivation rafts in the Ria deArosa (Galicia, N.W. Spain). Aquaculture 94: 197–212

Newell CR (1990) The effects of mussel (Mytilus edulis, Linnaeus,1758) position in seeded bottom patches on growth at subtidallease sites in Maine. J Shellfish Res 9: 113–118

Newell RIE (1988) Ecological changes in Chesapeake Bay: Are theythe result of overharvesting the American oyster,Crassostreavirginica? In: Lynch MP and Krome EC (eds.), Understandingthe estuary: advances in Chesapeake Bay research. ChesapeakeResearch Consortium, Solomon, pp. 536–546

Nienhuis PH and Smaal AC (1994) The Oosterschelde estuary (TheNetherlands). A case-study of a changing ecosystem. KluwerAcademic Publishers, Dordrecht, The Netherlands, 597 pp.

Officer CB, Smayda TJ and Mann R (1982) Benthic filter feeding: anatural eutrophication control. Mar Ecol Prog Ser 9: 203–210

Olsson P, Graneli E, Carlsson P and Abreu P (1992) Structuring of apostspring phytoplankton community by manipulation of trophicinteractions. J Exp Mar Biol Ecol 158: 249–266

Pieters H, Kluytmans JH, Zandee DI and Cadee GC (1980) Tissuecomposition and reproduction ofMytilus edulisin relation to foodavailability. Neth J Sea Res 14: 349–361

Prins TC (1996) Bivalve grazing, nutrient cycling and phytoplanktondynamics in an estuarine ecosystem. Ph.D. Thesis, University ofWageningen, 151 pp.

Prins TC and Smaal AC (1994) The role of the blue musselMytilusedulis in the cycling of nutrients in the Oosterschelde estuary(The Netherlands). Hydrobiologia 282/283: 413–429

Prins TC, Dankers N and Smaal AC (1994) Seasonal variation in thefiltration rates of a semi-natural mussel bed in relation to sestoncomposition. J Exp Mar Biol Ecol 176: 69–86

Prins TC, Escaravage V, Smaal AC and Peeters JCH (1995a) Func-tional and structural changes in the pelagic system induced bybivalve grazing in marine mesocosms. Wat Sci Tech 32: 183–185

Prins TC, Escaravage V, Smaal AC and Peeters JCH (1995b) Nutrientcycling and phytoplankton dynamics in relation to mussel grazingin a mesocosm experiment. Ophelia 41: 289–315

Prins TC, Smaal AC, Dankers N and Pouwer AJ (1996) Filtration andresuspension of particulate matter and phytoplankton on an inter-tidal mussel bed in the Oosterschelde estuary (SW Netherlands).Mar Ecol Prog Ser 142: 121–134

Riemann B, Nielsen TG, Horsted SJ, Bjørnsen PK and Pock-Steen J(1988) Regulation of phytoplankton biomass in estuarine enclos-ures. Mar Ecol Prog Ser 48: 205–215

Smaal AC and Haas HA (1997) Seston dynamics and food avail-ability on mussel and cockle beds. Estuar Coast Shelf Sci, inpress.

Smaal AC and Nienhuis PH (1992) The Eastern Scheldt (The Neth-erlands), from an estuary to a tidal bay – A review of responsesat the ecosystem level. Neth J Sea Res 30: 161–173

Smaal AC and Prins TC (1993) The uptake of organic matter and therelease of inorganic nutrients by bivalve suspension feeder beds.In: Dame RF (ed.), Bivalve filter feeders in estuarine and coastalecosystem processes. Springer-Verlag, Berlin, pp. 271–298

Smaal AC and Twisk F (1997) Filtration and absorption ofPhaeo-cystiscf globosaby the musselMytilus edulisL. J Exp Mar BiolEcol 209: 33–46

Smaal AC and Van Stralen M (1990) Average annual growth andcondition of mussels as a function of food source. Hydrobiologia195: 179–188

Smaal AC, Verhagen JHG, Coosen J and Haas HA (1986). Interac-tions between seston quantity and quality and benthic suspensionfeeders in the Oosterschelde, The Netherlands. Ophelia 26: 385–399

Smayda TJ (1990) Novel and nuisance phytoplankton blooms in thesea: Evidence for a global epidemic. In: Graneli E, Sundstrom B,Edler L and Anderson DM (eds.), Toxic marine phytoplankton.Elsevier, New York, pp. 29–40

Sommer U (1992) Phosphorus-limitedDaphnia: Intraspecific facil-itation instead of competition. Limnol Oceanogr 37: 966–973

Sterner RW (1986) Herbivores’ direct and indirect effects on algalpopulations. Science 231: 605–607

Sterner RW and Hessen DO (1994) Algal nutrient limitation and thenutrition of aquatic herbivores. Annu Rev Ecol Syst 25: 1–29

359

Sterner RW, Hagemeier DD, Smith WL and Smith RF (1993) Phyto-plankton nutrient limitation and food quality for Daphnia. LimnolOceanogr 38: 857–871

Takeda S and Kurihara Y (1994) Preliminary study of management ofred tide water by the filter feederMytilus edulis galloprovincialisMar Poll Bull 28: 662–667

Tracey GA (1988) Feeding reduction, reproductive failure, and mor-tality in Mytilus edulisduring the 1985 ‘brown tide’ in Nar-ragansett Bay, Rhode Island. Mar Ecol Prog Ser 50: 73–81

Ulanowicz RE and Tuttle JH (1992) The trophic consequences ofoyster stock rehabilitation in Chesapeake Bay. Estuaries 15: 298–306

Widdows J, Moore MN, Lowe DM and Salkeld PN (1979) Someeffects of a dinoflagellate bloom (Gyrodinium aureolum) on themussel,Mytilus edulis. J Mar Biol Ass UK 59: 522–524

Wildish DJ and Kristmanson DD (1984) Importance to mussels ofthe benthic boundary layer. Can J Fish aquat Sci 41: 1618–1625

Wildish DJ and DD Kristmanson, 1993. Hydrodynamic control ofbivalve filter feeders: a conceptual view. In: Dame RF (ed.),Bivalve filter feeders in estuarine and coastal ecosystem pro-cesses. Springer-Verlag, Berlin, pp. 299–324

Wilkinson L (1992) Systat for Windows. Systat, Inc., Evanston, Il.Willows RI (1992) Optimal digestive investment: A model for filter

feeders experiencing variable diets. Limnol Oceanogr 37: 829–847