A Scientific Review of the Potential Environmental Effects of Aquaculture in Aquatic Ecosystems - Volume 1

Ecosystem Level Effects of Marine Bivalve Aquaculture

P. Cranford
Fisheries and Oceans Canada, Bedford Institute of Oceanography, Dartmouth, Nova Scotia

M. Dowd
Fisheries and Oceans Canada, St. Andrews Biological Station, St. Andrews, New Brunswick

J. Grant
Dalhousie University, Oceanography Department, Halifax, Nova Scotia

B. Hargrave
Fisheries and Oceans Canada, Bedford Institute of Oceanography, Dartmouth, Nova Scotia

S. McGladdery
Fisheries and Oceans Canada, Gulf Fisheries Centre, Moncton, New Brunswick

Executive Summary

This paper reviews the present state of knowledge on environmental issues related to bivalve aquaculture, with emphasis on suspended mussel culture. Material reviewed includes Canadian and international studies on the role of wild and cultured bivalve populations in controlling ecosystem-level dynamics. The focus is on identifying potential changes in ecosystem processes (material and energy fluxes, and nutrient cycling) at the coastal ecosystem scale. Potential mechanisms for ecosystem-level effects include the utilization of particulate food resources by cultured bivalves and associated fauna, the subsequent release of unutilized materials in dissolved (urine) and particulate (feces and pseudofeces) form, and the removal of minerals from the system in the bivalve harvest. The potential consequences to coastal ecosystems from intensive bivalve aquaculture are summarized in the following sections.

Control of Suspended Particle Dynamics

Dense bivalve populations may exert a strong influence on suspended particulate matter (including phytoplankton, detritus, and some auto- and heterotrophic picoplankton and microzooplankton) in some coastal systems through their huge capacity to clear particles from the surrounding water (Dame 1996). Grant (2000) studied 15 embayments in Prince Edward Island (PEI) and concluded that the mussel biomass under culture in 12 of these embayments was potentially capable of removing food particles much faster than tidal exchange could replace them. Similarly, Meeuwig et al. (1998) concluded that mussel culture operations in many PEI embayments significantly reduce phytoplankton biomass through grazing. Similar conclusions have been reached for numerous international coastal regions (reviewed by Dame 1996). These relatively simple calculations of the time required for bivalve populations to clear the water column of particles indicate that intensive bivalve aquaculture has the capacity to alter matter and energy flow at the coastal ecosystem scale. However, gaps in knowledge exist regarding a number of important processes that could potentially mitigate the suspected impact of bivalve feeding. These include the following:

1. the effects of physical processes such as water column stratification, mixing and flow velocity, and spatially dependent tidal flushing;
2. the replenishment of food particles through primary production within the embayment; (3) bivalve-mediated optimization of primary production (Prins et al. 1995);
3. and the large flexibility of bivalve feeding responses to environmental variations (Cranford and Hill 1999).

A strong indication that bivalve filter-feeders are able to control suspended particulate matter in some coastal systems comes from documented ecosystem changes that occurred after large biomass variations in natural and cultured bivalve populations. Population explosions of introduced bivalve species in San Francisco Bay and dramatic reductions in oyster populations in Chesapeake Bay have been implicated as the cause of large changes in phytoplankton biomass and production experienced in these systems (Nichols 1985; Newell 1988; Nichols et al. 1990; Alpine and Cloern 1992; Ulanowicz and Tuttle 1992). Research on the whole-basin environmental effects of bivalve aquaculture in France and Japan indicate that intense bivalve culture in these regions led to changes in particulate food abundance and quality, resulting in large-scale growth reduction and high mortalities in the cultured bivalves (Héral et al. 1986; Aoyama 1989; Héral 1993). Speculation that intense bivalve culture can affect coastal ecosystems by reducing excess phytoplankton associated with eutrophication have been supported by some laboratory and field observations, but have not been rigorously proven.

Diversion of Materials to Benthic Food Webs

The feeding activity of bivalve filter-feeders results in the packaging of fine suspended material into larger feces and pseudofeces that rapidly settle to the seabed, especially under conditions with slow or poor water flushing and exchange. These activities divert primary production and energy flow from planktonic to benthic food webs. While the dynamics of bivalve feces deposition (settling velocity, disaggregation rate and resuspension) are poorly understood, enhanced sedimentation under shellfish culture is well documented. Mortality and fall-off of cultured bivalves, induced by seasonal colonization by fouling organisms, can result in additional acute benthic organic loading.

The spatial scale and degree of seabed organic enrichment effects caused by the increased vertical flux of naturally occurring particles is dependant on the biomass of cultured bivalves, local hydrographic conditions, and the presence of additional organic inputs from other natural and anthropogenic activities. The recycling of organic biodeposits under suspended mussel culture operations in PEI, and at several other international regions, has been shown to have local to inlet-wide benthic impacts (Dahlback and Gunnarsson 1981; Tenore et al. 1982; Mattsson and Linden 1983; Kaspar et al. 1985; Shaw 1998; Stenton-Dozey et al. 1999; Mirto et al. 2000; Chamberlain et al. 2001). The increased oxygen demand in sediments from mussel biodeposits can, under certain conditions, result in the generation of an anaerobic environment that promotes ammonification and sulfate reduction, increased sediment bacterial abundance, and changes in benthic community structure and biomass. Aquaculture is not solely responsible for such impacts in PEI, as many basins are also stressed by nutrient enrichment from agricultural run-off. Observations of seabed impacts under mussel lines in PEI are, therefore, not directly transferable to bivalve culture sites in many other regions of Canada. Biodeposition patterns and the dispersion of bivalve biodeposits are also controlled by water depth and local water movement. Slight differences in these physical properties can result in marked differences in the degree of impact observed on seabed geochemistry and communities under different suspended mussel culture sites (Chamberlain et al. 2001). Further research is needed to assess the ability of different coastal regions to resist or assimilate the effects of increased organic enrichment through a variety of physical and biogeochemical processes.

The increased coupling of planktonic and benthic food webs by cultured bivalves has the potential to change energy flow patterns in coastal ecosystems, including altering food availability to zooplankton and larval fish (Horsted et al. 1988; Newell 1988; Doering et al. 1989). Bivalve filter-feeders have a competitive advantage over zooplankton for food resources because they are able to respond immediately to increased food availability, while zooplankton must go through a complete life cycle before being able to fully exploit increased food resources. Direct ingestion of zooplankton by bivalves may also reduce zooplankton abundance (Horsted et al. 1988; Davenport et al. 2000). However, effects of bivalve culture on zooplankton communities are largely speculative owing to the limited research conducted.

Altered Coastal Nutrient Dynamics

The consumption and deposition of suspended particulate matter by bivalves, as well as the excretion of dissolved nutrients, can play a significant role in controlling the amounts and forms of nitrogen in coastal systems and the rate of nitrogen cycling (reviewed by Dame 1996). This transformation and translocation of matter by bivalves appears to exert a controlling influence on nitrogen concentrations in some coastal regions (Dame et al. 1991) and can provide a means of retaining nutrients in coastal areas, where they are recycled within detrital food chains, rather than being more rapidly exported (Jordan and Valiela 1982). Benthic nutrient mineralization can increase at culture sites as a result of the increased organic matter sedimentation, greatly speeding up the rate of nitrogen cycling (Dahlback and Gunnarsson 1981; Kaspar et al. 1985; Feuillet-Girard et al. 1988; Barranguet et al. 1994; Grant et al. 1995). The high flux of ammonia excreted from dense bivalve populations may have a major effect on phytoplankton production (Maestrini et al. 1986; Dame 1996) and may potentially contribute to more frequent algal blooms, including those of the domoic-acid-producing diatom Pseudo-nitzschia multiseries (Bates 1998; Bates et al. 1998). Aquaculture-induced changes in the relative concentrations of silica, phosphorus and nitrogen (e.g. Hatcher 1994) may also favor the growth of other harmful phytoplankton classes (Smayda 1990), but this has yet to be observed in nature. Bivalve aquaculture may also play a significant role in nutrient cycling in coastal systems, as nutrients stored in the cultured biomass are removed by farmers and the nutrients are no longer available to the marine food web. Kaspar et al. (1985) suggested that the harvesting of cultured mussels may lead to nitrogen depletion and increased nutrient limitation of primary production, but there is little direct evidence of environmental effects. The retention and remineralization of limiting nutrients in coastal systems is necessary to sustain system productivity, but the potential impacts of bivalve cultures on coastal nutrient dynamics is poorly understood.

Cumulative Environmental Effects

Any attempt to assess ecosystem-level effects of bivalve aquaculture must consider the complexity of natural and human actions in estuarine and coastal systems. Infectious diseases associated with intense bivalve culture, as well as exposure of cultured organisms to 'exotic' pathogens introduced with seed or broodstock, can have a significant and perhaps more permanent impact on ecosystems than the direct impact of the bivalves themselves (Banning 1982; ICES 1995; Bower and McGladdery 1996; Hine 1996; Renault 1996; Minchin 1999; Miyazaki et al. 1999). The presence of additional ecosystem stressors can also influence the capacity of bivalves to impact the ecosystem. The effects of chemical contaminants and habitat degradation are complex, but are well documented as having the potential to adversely affect bivalve health. Bivalve neoplasias show strong correlations to heavily contaminated environments (Elston et al. 1992), and the severity of infection is related to sub-optimal growing conditions (Elston 1989). Dissolved contaminants are frequently scavenged onto particulate matter, a mechanism which increases their availability for wild and cultured filter-feeders to ingest. Weakened bivalves with impeded feeding activity, along with spawning failure or poor quality spawn, can all contribute to morbidity, mortality and fall-off.

Land-use practices that transport sediments into estuaries can impact coastal water quality. Cultured bivalves and their support structures could alter sedimentation patterns within embayments, resulting in accelerated deposition of fine-grained sediment. Presently, there is no consensus on whether dense bivalve populations cause a net increase or decrease in sedimentation rates in coastal regions. However, if bivalve cultures influence the natural equilibrium among the major factors controlling sediment aggregation rate, sedimentary conditions within coastal regions may be altered.

Integration of Ecosystem Effects

The available literature has shown that extensive bivalve culture has the potential, under certain conditions, to cause cascading effects through estuarine and coastal foodwebs, altering habitat structure, species composition at various trophic levels, energy flow and nutrient cycling. Simulation modelling has been one of the more focused approaches to assessing the net ecosystem impact of bivalve interactions with ecosystem components. Modelling can quantitatively and objectively integrate the potential negative ecosystem effects of the impact of mussel grazing on phytoplankton, zooplankton and the benthos, with the potentially positive effects of increased recycling of primary production and retention of nutrients in coastal systems (Fréchette and Bacher 1998). For example, such an integrative approach can help to assess whether or not the severity of ecosystem effects in different coastal areas are regulated by water motion and mixing. Numerical models can also be directed toward assessment of system productive capacity, fish/land-use interactions, farm management and ecosystem health. Past work has provided an excellent means of identifying gaps in knowledge.

A variety of methods has been applied to assessing the environmental interactions of bivalve aquaculture operations (Grant et al. 1993; Dowd 1997; Grant and Bacher 1998; Smaal et al. 1998; Meeuwig 1999), but there is no standard assessment approach. Fully coupled biological-physical models may be envisioned (e.g. Prandle et al. 1996; Dowd 1997) that predict ecosystem changes in chlorophyll, nutrients and other variables of interest as a function of culture density and location. To do this, shellfish ecosystem models must be integrated with information on water circulation, mixing and exchange to account for transport and spatial redistribution of particulate and dissolved matter. Box models (Raillard and Menesguen 1994; Dowd 1997; Chapelle et al. 2000) offer a practical means to couple coastal ecosystem models with physical oceanographic processes. The bulk parameterizations of mixing required for these box models can be derived directly from complex hydrodynamic models (Dowd et al. 2002). Another promising avenue for improving ecosystem models is the use of inverse, or data assimilation, methods (Vallino 2000). These systematically integrate available observations and models, thereby combining empirical and simulation approaches, and improve predictive skill. Simulation models that focus on estimating mussel carrying capacity and related ecosystem impacts provide powerful tools for quantitative descriptions of how food is captured and utilized by mussels, as well as site-specific information on ecosystem variables and processes (Carver and Mallet 1990; Brylinsky and Sephton 1991; Grant 1996).

Research Needs

Few studies have assessed the potential environmental interactions of the bivalve aquaculture industry, and few quantitative measures presently exist to measure the ecosystem-level effects of this industry. Research on the ecosystem-level impacts of bivalve aquaculture is currently at a relatively early stage of development compared with finfish culture and for many other anthropogenic activities. As a result, ecologically relevant studies are needed on many topics, particularly the long-term responses of major ecosystem components (phytoplankton, zooplankton, fish, benthos, as well as the cultured bivalves) to bivalve-induced changes in system energy flow and nutrient cycling. The following general research areas have been identified to address gaps in knowledge:

• Ecological role of bivalve filter-feeders: accurately quantify the density-dependant role of bivalves in controlling phytoplankton and seston concentrations, including studies of hydrodynamics, bivalve ecophysiology, and phytoplankton community and productivity responses to grazing pressure.
• Organic loading: identify important processes controlling the severity of seabed organic enrichment impacts caused by bivalve biodeposits and determine the capacity of different coastal ecosystems to assimilate or recover from the effects of aquaculture-related organic loading.
• Nutrient dynamics: develop a predictive understanding of the potential effects of bivalve aquaculture on nutrient concentrations, elemental ratios and rate of cycling in coastal systems, and study the consequences of altered nutrient dynamics to phytoplankton communities and blooms, including harmful algal blooms.
• Ecosystem structure: investigate the effects of bivalve culture on ecosystem structure resulting from direct competition between bivalves, zooplankton and epibionts for trophic resources, and the transfer of energy and nutrients to benthic food webs.
• Numerical modelling: integrate knowledge obtained on the consequences of bivalve culture on ecosystem structure and function through the use of ecosystem modelling to assess the net impact of aquaculture activities on major system components and to address issues of aquaculture productive capacity and sustainability.
• Ecosystem status: develop a scheme for classifying and assessing the state of ecosystem functioning for regions supporting bivalve aquaculture. Integrate multiple ecosystem stressors from anthropogenic land- and marine-use in ecosystem studies of culture systems.

The complete papers can be found in the following document:

Fisheries and Oceans Canada. 2003. A scientific review of the potential environmental effects of aquaculture in aquatic ecosystems. Volume 1. Far-field environmental effects of marine finfish aquaculture (B.T. Hargrave); Ecosystem level effects of marine bivalve aquaculture (P. Cranford, M. Dowd, J. Grant, B. Hargrave and S. McGladdery); Chemical use in marine finfish aquaculture in Canada: a review of current practices and possible environmental effects (L.E. Burridge). Can. Tech. Rep. Fish. Aquat. Sci. 2450: ix + 131 p.

References

• Alpine, S.E. and J.E. Cloern. 1992. Trophic interactions and direct physical effects control phytoplankton biomass and production in an estuary. Limnol. Oceanogr. 37: 946-955.
• Aoyama, S. 1989. The Mutsu Bay scallop fisheries: scallop culture, stock enhancement, and resource management, p. 525-539. In J.F. Caddy [ed.]. Marine invertebrate fisheries: their assessment and management. John Wiley & Sons, New York, NY.
• Barranguet, C., E. Alliot and M.-R. Plante-Cuny. 1994. Benthic microphytic activity at two Mediterranean shellfish cultivation sites with reference to benthic fluxes. Oceanol. Acta 17: 211-221.
• Bates, S.S. 1998. Ecophysiology and metabolism of ASP toxin production, p. 405-426. In D.M. Anderson, A.D. Cembella and G.M. Hallegraeff [eds.]. Physiological ecology of harmful algal blooms. Springer-Verlag, Heidelberg.
• Bates, S.S., D.L. Garrison and R.A. Horner. 1998. Bloom dynamics and physiology of domoic-acid-producing Pseudo-nitzschia species, p. 267-292. In D.M. Anderson, A.D. Cembella and G.M. Hallegraeff [eds.]. Physiological ecology of harmful algal blooms. Springer-Verlag, Heidelberg.
• Bower, S.M and S.E. McGladdery. 1996. Synopsis of infectious diseases and parasites of commercially exploited shellfish. (www.pac.dfo-mpo.gc.ca/sci/sealane/aquac/ pages/title.htm.)
• Brylinsky, M. and T.W. Sephton. 1991. Development of a computer simulation model of a cultured blue mussel (Mytilus edulis) population. Can. Tech. Rep. Fish. Aquat. Sci. 1805. 81 p.
• Carver, C.E.A. and A.L. Mallet. 1990. Estimating the carrying capacity of a coastal inlet for mussel culture. Aquaculture 88: 39-53.
• Chamberlain, J., T.F. Fernandes, P. Read, T.D. Nickell and I.M. Davies. 2001. Impacts of deposits from suspended mussel (Mytilus edulis L.) culture on the surrounding surficial sediments. ICES J. Mar. Sci. 58: 411-416.
• Chapelle, A., A. Menesguen, J.-M. Deslous-Paoli, P. Souchu, N. Mazouni, A. Vaquer and B. Millet. 2000. Modelling nitrogen, primary production and oxygen in a Mediterranean lagoon. Impact of oyster farming and inputs from the watershed. Ecol. Model. 127: 161-181.
• Cranford, P.J. and P.S. Hill. 1999. Seasonal variation in food utilization by the suspension-feeding bivalve molluscs Mytilus edulis and Placopeten magellanicus. Mar. Ecol. Prog. Ser. 190: 223-239.
• Dahlback, B. and L.A.H. Gunnarsson. 1981. Sedimentation and sulfate reduction under a mussel culture. Mar. Biol. 63: 269-275.
• Dame, R.F. 1996. Ecology of marine bivalves: an ecosystem approach. CRC Press, Boca Raton, FL.
• Dame, R.F., N. Dankers, T. Prins, H. Jongsma and A. Smaal. 1991. The influence of mussel beds on nutrients in the Western Wadden Sea and Eastern Scheldt estuaries. Estuaries 14: 130-138.
• Davenport, J., R.J.J.W. Smith and M. Packer. 2000. Mussels Mytilus edulis: significant consumers and destroyers of mesozooplankton. Mar. Ecol. Prog. Ser. 198: 131-137.
• Doering, P.H., C.A. Oviatt, LL. Beatty, V.F. Banzon, R. Rice, S.P. Kelly, B.K. Sullivan and J.B. Frithsen. 1989. Structure and function in a model coastal ecosystem: silicon, the benthos and eutrophication. Mar. Ecol. Prog. Ser. 52: 287-299.
• Dowd, M. 1997. On predicting the growth of cultured bivalves. Ecol. Model. 104: 113-31.
• Dowd, M., K.R. Thompson, Y. Shen and D.A. Greenberg. 2002. Probabilisitic characterization of tidal mixing in a coastal embayment. Cont. Shelf Res. 22: 1603-1614.
• Elston, R.A. 1989. Bacteriological methods for diseased shellfish, p. 187-215. In B. Austin and D.A. Austin [eds.]. Methods for microbiological examination of fish and shellfish. Ellis Horwood Series in Aquaculture and Fisheries Support, John Wiley & Sons, Chichester, U.K.
• Elston, R.A., J.D. Moore and K. Brooks. 1992. Disseminated neoplasia in bivalve molluscs. Rev. Aquat. Sci. 6: 405-466.
• Feuillet-Girard, M., M. Héral, J.-M. Sornin, J.-M. Deslous-Paoli, J.-M. Robert, F. Mornet and D. Razet. 1988. Nitrogenous compounds in the water column and at the sediment-water interface in the estuarine bay Marennes-Oléron: influence of oyster farming. Aquat. Living Resour. 1: 251-265.
• Fréchette, M. and C. Bacher. 1998. A modelling study of optimal stocking density of mussel populations kept in experimental tanks. J. Exp. Mar. Biol. Ecol. 219: 241-255.
• Grant, J. 1996. The relationship of bioenergetics and the environment to the field growth of cultured bivalves. J. Exp. Mar. Biol. Ecol. 200: 239-256.
• Grant, J. 2000. Method of assessing mussel culture impacts for multiple estuaries (15) and associated culture sites for PEI. Unpublished report prepared for Habitat Management Division, Fisheries and Oceans Canada, 34 p.
• Grant, J. and C. Bacher. 1998. Comparative models of mussel bioenergetics and their validation at field culture sites. J. Exp. Mar. Biol. Ecol. 219(1-2): 21-44.
• Grant, J., M. Dowd, K. Thompson, C. Emerson and A. Hatcher. 1993. Perspectives on field studies and related biological models of bivalve growth, p. 371-420. In R. Dame [ed.]. Bivalve filter feeders and marine ecosystem processes. Springer Verlag, New York, NY.
• Grant, J., A. Hatcher, D. B. Scott, P. Pocklington, C.T. Schafer and C. Honig. 1995. A multidisciplinary approach to evaluating benthic impacts of shellfish aquaculture. Estuaries 18: 124-144.
• Hatcher, A., J. Grant and B. Schofield. 1994. Effects of suspended mussel culture (Mytilus spp) on sedimentation, benthic respiration and sediment nutrient dynamics in a coastal bay. Mar. Ecol. Prog. Ser. 115: 219-235.
• Héral, M. 1993. Why carrying capacity models are useful tools for management of bivalve molluscs culture, p. 455-477. In R.F. Dame [ed.]. Bivalve filter feeders in estuarine and coastal ecosystem processes. NATO ASI Series. Springer-Verlag, Heidelberg.
• Héral, M., J.-M. Deslous-Paoli and J. Prou. 1986. Dynamiques des productions et des biomasses des huitres creises cultivées (Crassostrea angulata et Crassostrea gigas) dans le bassin de Marennes-Oléron depuis un siecle. ICES CM86/F:14.
• Hine, P.M. 1996. Southern hemisphere mollusc diseases and an overview of associated risk assessment problems. Rev. Sci. Tech. Off. Int. Epiz. 15(2): 563-577.
• Horsted, S.J., T.G. Nielsen, B. Reimann, J. Pock-Steen and P.K. Bjornsen. 1988. Regulation of zooplankton by suspension-feeding bivalves and fish in estuarine enclosures. Mar. Ecol. Prog. Ser. 48: 217-224.
• ICES. 1995. ICES Code of practice on the introductions and transfers of marine organisms - 1994. ICES Coop. Res. Rep. No. 204.
• Jordan, T.E. and I. Valiela. 1982. A nitrogen budget of the ribbed mussel, Geukensis demissa, and its significance in the nitrogen flow in a New England salt marsh. Limnol. Oceanogr. 27: 75-90.
• Kaspar, H.F., P.A. Gillespie, I.C. Boyer and A.L. MacKenzie. 1985. Effects of mussel aquaculture on the nitrogen cycle and benthic communities in Kenepuru Sound, Marlborough Sound, New Zealand. Mar. Biol. 85: 127-136.
• Maestrini, S.Y., J.-M. Robert, J.W. Lefley and Y. Collos. 1986. Ammonium thresholds for simultaneous uptake of ammonium and nitrate by oyster-pond algae. J. Exp. Mar. Biol. Ecol. 102: 75-98.
• Mattsson, J. and O. Linden. 1983. Benthic macrofauna succession under mussels, Mytilus edulis L. cultured on hanging long-lines. Sarsia 68: 97-102.
• Meeuwig, J.J. 1999. Predicting coastal eutrophication from land-use: an empirical approach to small non-stratified estuaries. Mar. Ecol. Prog. Ser. 176: 231-241.
• Meeuwig, J.J., J.B. Rasmussen and R.H. Peters. 1998. Turbid waters and clarifying mussels: their moderation of empirical chl:nutrient relations in estuaries in Prince Edward Island, Canada. Mar. Ecol. Prog. Ser. 171: 139-150.
• Minchin, D. 1999. Exotic species: implications for coastal shellfish resources. J. Shellfish Res. 18(2): 722-723.
• Mirto, S., T. La Rosa, R. Danovaro and A. Mazzola. 2000. Microbial and meofaunal response to intensive mussel-farm biodeposition in coastal sediments of the Western Mediterranean. Mar. Pollut. Bull. 40: 244-252.
• Miyazaki, T., K. Goto, T. Kobayashi and M. Miyata. 1999. Mass mortalities associated with a virus disease in Japanese pearl oysters Pinctada fucata martensii. Dis. Mar. Org. 37(1): 1-12.
• Newell, R.I.E. 1988. Ecological changes in Chesapeake Bay: are they the results of overharvesting the American oyster, Crassostrea virginica? Chesapeake Res. Consor. Pub. 129: 536-546.
• Nichols, F.H. 1985. Increased benthic grazing: an alternative explanation for low phytoplankton biomass in northern San Francisco Bay during the 1976-1977 drought. Est. Coastal Shelf Sci. 21: 379-388.
• Nichols, F.H., J.K. Thompson and L.E. Schemel. 1990. Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. II. Displacement of a former community. Mar. Ecol. Prog. Ser. 66: 95-101.
• Prandle, D., G. Ballard, D. Flatt, A.J. Harrison, S.E. Jones, P.J. Knight, S. Loch, J. Mcmanus, R. Player and A. Tappin. 1996. Combining modeling and monitoring to determine fluxes of water, dissolved and particulate metals through the Dover Strait. Cont. Shelf Res. 16: 237-257.
• Prins, T.C., V. Escaravage, A.C. Smaal and J.C.H. Peters. 1995. Nutrient cycling and phytoplankton dynamics in relation to mussel grazing in a mesocosm experiment. Ophelia 41: 289-315.
• Raillard, O. and A. Menesguen. 1994. An ecosystem box model for estimating the carrying capacity of a macrotidal shellfish system. Mar. Ecol. Prog. Ser. 115: 117-130.
• Renault, T. 1996. Appearance and spread of diseases among bivalve molluscs in the northern hemisphere in relation to international trade. Rev. Sci. Tech. Off. Int. Epiz. 15(2): 551-561.
• Shaw, K.R. 1998. PEI benthic survey. Tech. Rep. Environ. Sci. No. 4, Dept of Environment and Dept. of Fisheries and Environment, 75 p.
• Smaal, A.C., T.C. Prins, N. Dankers and B. Ball. 1998. Minimum requirements for modelling bivalve carrying capacity. Aquat. Ecol. 31: 423-428.
• Smayda, T.J. 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic, p. 29-40. In E. Granéli, B. Sundström, L. Edler and D.M. Anderson [eds.]. Toxic marine phytoplankton. Elsevier, New York, NY.
• Stenton-Dozey, J.M.E., L.F. Jackson and A.J. Busby. 1999. Impact of mussel culture on macrobenthic community structure in Saldahana Bay, South Africa. Mar. Pollut. Bull. 39: 357-366.
• Tenore, K.R., L.F. Boyer, R.M. Cal, J. Corral, C. Garcia-Fernandez, N. Gonzalez, E. Gonzalez-Gurriaran, R.B. Hanso, J. Oglesias, M. Krom, E. Lopez-Jamar, J. McClain, M.M. Pamarmat, A. Perez, D.C. Rhoads, G. De Santiago, J. Tietjen, J. Westrich and H.L. Windom. 1982. Coastal upwelling in the Rias Bajas, NW Spain: contrasting the benthic regimes of the Rias de Arosa and de Muros. J. Mar. Res. 40: 701-772.
• Ulanowicz, R.E. and J.H. Tuttle. 1992. The trophic consequences of oyster stock rehabilitation in Chesapeake Bay. Estuaries 15: 298-306.
• Vallino, J.J. 2000. Improving marine ecosystem models: use of data assimilation and mesocosm experiments. J. Mar. Res. 58: 117-164.