shellfish aquaculture and the environment (shumway/shellfish aquaculture and the environment) ||...

Chapter 5

Trophic interactions between phytoplankton and bivalve aquaculture Gary H. Wikfors

The i nterdependence of b ivalves and p hytoplankton

The term “ trophic interactions ” used here is purposely broader than the concept of one thing feeding on another. In the case of the bivalve molluscs that are suspension - feeders and the microalgae — chiefl y phytoplankton — that constitute a large fraction of the living component of the suspended seston upon which molluscs feed, the most obvious interac-tion is bivalves eating algae. Increasingly, however, the reverse trophic interaction is being recognized; dissolved inorganic and organic waste compounds released by meta-bolically active bivalves can supply microalgae with nutrient and energy requirements for their growth (Offi cer et al. 1982 ; Boucher and

Boucher - Rodoni 1988 ; Smaal and Prins 1993 ; Prins et al. 1998 ; Newell 2004 ). This two - way interaction can be viewed as a type of com-munity symbiosis developed over long evolu-tionary timescales (Fig. 5.1 ).

How does aquaculture of molluscan shell-fi sh fi t into this long - established symbiosis between molluscs and phytoplankton? One could assume that, as in most monoculture cultivation scenarios, farming of suspension - feeding molluscs should intensify the interac-tions in time and space, possibly upsetting critical environmental equilibria. I argue, to the contrary, that natural populations of most molluscan species that are farmed inten-sively tend to be highly gregarious, naturally forming dense assemblages akin to those created through aquaculture practices. Further,

Shellfi sh Aquaculture and the Environment, First Edition. Edited by Sandra E. Shumway.© 2011 John Wiley & Sons, Inc. Published 2011 by John Wiley & Sons, Inc.

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126 Shellfi sh Aquaculture and the Environment

both eutrophication (see Chapter 7 in this book) and food web disruption (Ulanowicz and Tuttle 1992 ; Cerco and Noel 2007 ).

The main challenge in the harmonization of bivalve aquaculture and coastal ecosystem - based management of water quality involves scaling. In development of a natural system, the highly adaptive reproductive strategy of most bivalves, that is, high fecundity but low investment in offspring, allows bivalve popula-tions to respond on decadal timescales to changes in the quantity and quality of trophic resources available from phytoplankton primary productivity, as well as other ecologi-cal changes (Dekshenieks et al. 2000 ). In siting and scaling of shellfi sh aquaculture, one does not often have the benefi t of knowing past carrying capacity. Even if such knowledge was available, it is likely that bottom - up forcing functions of nutrient inputs, as well as competition for primary production from

reef - building characteristics of some species, such as oysters, have served under natural con-ditions to transfer benthic organisms into the pelagic realm where they are within the primary productivity maximum near the water surface and less vulnerable to stress from silt-ation and hypoxia (Lenihan 1999 ).

I argue that bivalve aquaculture can restore trophic balance between the bivalves and phytoplankton communities that may have existed before habitat modifi cations caused by other human activities, such as harvesting (dragging former reefs fl at), channel dredging for boat transportation, and bulkheading (Rothschild et al. 1994 ; Hargis and Haven 1999 ). Restoring bivalve – phytoplankton trophic interactions through shellfi sh aquacul-ture has the potential to mitigate ecosystem imbalances attributed to nutrient overenrich-ment and to help reverse the cycle of ecosystem degradation in coastal waters resulting from

Figure 5.1 “ Box model ” of a suspension - culture, oyster nursery, with arrows depicting exchanges of carbon, nitrogen, and phosphorus between the oyster nursery and environmental compartments. Of particular note are the arrows indicat-ing return of respiratory carbon (CO 2 ) and excreted nitrogen (NH 4 + ) to the phytoplankton community, thereby recycling resources not assimilated immediately by the oysters. (Figure original, S.L. Meseck and G.H. Wikfors.)

CO2

O2

N2 NO3–

NO3–

NO2–

NH4+

NH4+

Phytoplankton(pOrg. N,pOrg. C)

Advective/ diffusive exchange

Bioticuptake

Fecalmatterdeposition

Tidalflow

dOrg. N pOrg. N

pOrg. N, pOrg. C

pOrg. N

dOrg. N

Burial

Toxicsediments

Water column

Oyster nursery(pOrg. N, pOrg. C)

Harvested

(pOrg. N, pOrg. C)

Phytoplankton and bivalve aquaculture 127

environment and then to each other, forming three - dimensional aggregations that change shape as byssal threads are formed and broken by waves and tidal currents (Dolmer 2000 ; Lawrie and McQuaid 2001 ). Clams are the main infaunal bivalve group farmed. Subsurface aggregations of clams have been hypothesized to result from water current infl uences upon larval settlement and provision of food to the benthic boundary layer (Wells 1957 ), as well as from substrate refugia from predation, for example, under shell hash or between rocks. With scallops, it is more diffi cult to conform to the “ shellfi sh are gregarious ” generaliza-tion. Most scallop species farmed are at least somewhat motile, able to adjust their location vertically and spatially according to changes in conditions. In intensive culture, some scallop species appear to attempt to adjust their spatial density to minimize intraspecifi c com-petition for food (Rhodes and Widman 1984 ). Accordingly, scallop aquaculture tends to occur at somewhat lower intensity, employing ear - hanging or lantern - net methods to achieve spatial distribution in three dimensions. In general, though, the argument that bivalve aquaculture is analogous to “ monoculture agriculture ” ignores the natural distribution patterns of bivalve species farmed.

Bivalves as c onsumers and c ultivators of p hytoplankton

When bivalves feed, they remove suspended particulate matter from the water as the fi rst step in the process by which they acquire the energy and materials they need to live and to grow. The elemental composition of suspended organic material in the sea often is estimated by the “ Redfi eld ratio ” or the “ extended Redfi eld ratio ” (Twining et al. 2004 ). Two important points that limit the accuracy of these ratios to represent seston or phytoplank-ton composition are as follows: (1) these ratios are based on, and averaged for, samples of

zooplankton, have changed as a result of other environmental changes (Peterson and Lipcius 2003 ). Thus, quantitative knowledge of bivalve – phytoplankton trophic interactions in coastal waters will inform bivalve aquaculture development to effectively serve the needs of both seafood production and ecosystem restoration.

Bivalve p opulation d ensity: f armed b ivalves are n aturally g regarious

The characteristics of bivalves that make phys-ical proximity of individuals necessary are external fertilization of gametes coupled with effective nonmotility. If spawning is to lead to offspring, individuals contributing gametes must be close enough to each other for fertil-ization to occur before gametes are lost to physical dilution or consumption by grazers (Andre and Lindegarth 1995 ). Populations of bivalves often, therefore, are referred to as “ reefs ” or “ beds, ” depending on vertical struc-ture of the aggregation (Korringa 1946 ; Wells 1957 ; Hargis and Haven 1999 ; Lawrie and McQuaid 2001 ). Impaired spawning success has been attributed to shellfi sh overharvest or depletion of natural populations below “ criti-cal densities ” (Kraeuter et al. 2005 ). Particle clearance, excretion, and biodeposition inten-sities of dense, farmed populations of bivalves, therefore, cannot be considered as “ unnatu-ral, ” as bivalve species farmed are not typically distributed widely at low density; they occur by biological necessity as concen-trated aggregations.

Oysters have long been considered to be “ ecosystem engineers, ” more for their reef - building activities modifying benthic habitat than for their trophic interactions (Lenihan and Peterson 1998 ). Only recently are the par-ticle clearance and nutrient recycling activities of oysters being considered in oyster restora-tion efforts (Coen et al. 2007 ). Similarly, mussels attach to any hard substrate in the


primary productivity (Cloern 2001 ). Negative ecosystem consequences of high planktonic primary productivity are attributed to shading of submerged aquatic vegetation and espe-cially to benthic hypoxia and anoxia resulting from bacterial respiration of unassimilated phytoplankton biomass. Although water quality criteria may value “ clear ” water devoid of phytoplankton, fi lter - feeding bivalves will starve in the absence of suspended food par-ticles. Thus, bivalves exploit as a resource the phytoplankton production viewed by water quality managers as a nuisance (Lindahl et al. 2005 ). Indeed, phytoplankton standing stock is defi ned as the difference between primary production and consumption; therefore, coastal waters discolored by phytoplankton can be considered a consequence of both increased fertilization with nutrients (bottom - up) and reduced grazing pressure (top - down) if historic bivalve populations have been depleted. In this respect, implementing bivalve aquaculture in eutrophic coastal waters can be considered as “ restoration ” of the particle - clearing function to the impacted ecosystem (Nelson et al. 2004 ).

As with any ecological interaction, too much of a good thing is still too much. It is generally agreed that the so - called “ pseudofe-ces threshold ” for bivalves is in the range of 2 – 10 mg L − 1 suspended particles (Bayne and Newell 1983 ). Above this threshold, a portion of the particles captured is rejected before ingestion because the respiratory activities of the gills take precedence over food capture.

In the opposite direction of this trophic interaction, “ too much ” bivalve fi ltration has been considered as a possible risk to pelagic food webs that support fi sheries. Thus, the concept of “ carrying capacity ” for bivalves must be considered at several levels (see Chapter 6 in this book). First, the physical carrying capacity within the spatial domain must be considered — how many shellfi sh will fi t in a defi ned area (Smaal et al. 2001 )? Using

suspended solids collected from the sea, not based on an internal, chemical stoichiometry imposed by the living organisms in the samples (Falkowski 2000 ); and (2) average values reported mainly are from open - ocean samples, not from coastal, estuarine, or brackish waters where most molluscan aquaculture is practiced (Arrigo 2005 ). A large amount of variance, often on diurnal timescales, in the relative carbon content of seston results from assimila-tion of this element into microalgal sugars by photosynthesis during daylight and subse-quent catabolism of these sugars and release of carbon dioxide in darkness (Paerl and Mackenzie 1977 ). As the dietary energy avail-able to a feeding bivalve is modifi ed by the carbon status of the phytoplankton, feeding over the course of the day will present bivalves with a range of energy contents within ingested food. Similarly, the protein, hence nitrogen, content of phytoplankton is dependent on the availability of this nutrient and suffi cient energy for anabolic protein synthesis. Under conditions of energy limitation, phytoplank-ton will assimilate more nitrogen than needed for cell division (Geider and La Roche 2002 ) — a process referred to as “ luxury consump-tion. ” Thus, the two most important nutritional inputs for bivalves, energy and protein, can be expected to vary considerably over diurnal and seasonal cycles. Whether or not this variation averages over annual timescales to the Redfi eld ratio is not certain and probably very different from place to place. Less attention is paid to the phosphorus content in seston consumed by bivalves, as this element generally is thought to be in excess supply in coastal waters — an assumption that may not be valid in coastal waters used for shellfi sh cultivation (Howarth and Marino 2006 ).

Many coastal waters are considered to be negatively impacted by eutrophication (see Chapter 7 in this book) — an overabundance of nutrients (chiefl y biologically available nitro-gen) leading to “ excess ” phytoplankton


their energy content (Delaporte et al. 2005 ). Dietary PUFAs and sterols are dependent on both the energy status and the taxonomic com-position of the phytoplankton community (Sargent et al. 1985 ), with some microalgal classes being devoid of these compounds (e.g., chlorophytes have no PUFAs longer than 18 carbons, but 20 - and 22 - carbon PUFAs are considered to be essential). Despite this knowl-edge concerning qualitative nutritional needs of bivalves derived from laboratory feeding studies (Knauer and Southgate 1999 ), there is no evidence yet that biodeposits — the rejected portion of seston fi ltered but not assimilated — is selectively stripped of PUFAs or biologically useful sterols. Indeed, evidence from analysis of shellfi sh tissues indicates that some lipids not used in construction of new cell mem-branes are accumulated in the tissues, in a way like parts that do not fi t in the construction (Goad 1981 ). Thus, although much evidence exists for selective retention and ingestion of particles based on both physical and chemical properties (Ward and Shumway 2004 ), it is not clear that selection is based on nutritional criteria (see Chapter 4 in this book). This area of research needs further work to clarify selec-tivity in bivalve feeding and how this may impact planktonic communities and nutrient cycling (Ward et al. 1994 ).

One clear change in nutrient chemistry that can occur as a consequence of bivalve feeding and elimination processes involves the nutrient silica (Si). Silica is a macronutrient for one microalgal class, the Bacillariophyceae, or the diatoms. When a bivalve consumes diatom biomass, portions of the nitrogen and phos-phorus components are assimilated into bivalve tissues, and remaining portions are returned to the environment in relatively labile forms. Complex, organic molecules in biode-posits can be recycled rapidly by bacterial decomposition, and nitrogenous wastes in the form of ammonia and urea are available immediately for phytoplankton reuse. Silica in

suspension culture, physical carrying capacity often can be increased to a point where other considerations become limiting (Fr é chette and Bacher 1998 ). Next, production carrying capacity is defi ned as the density above which production is limited by lack of resources such as food or oxygen. Production carrying capac-ity has been exceeded in some shellfi sh cultiva-tion situations, such as raft culture of mussels in Spain (Blanton et al. 1987 ). It can be argued, though, that natural recruitment sometimes exceeds production carrying capacity, leading to mortality of individuals in populations (Peterson and Black 1988 ). Ecological carrying capacity next considers the overall impact of the shellfi sh cultivation activity upon the other living components of the ecosystem (Dame and Prins 1998 ; Grant et al. 2007 ). It seems unrealistic to defi ne this limit as the density at which any ecosystem effects are apparent, although it often is. Instead, I would argue that ecosystem carrying capacity should be defi ned as the point at which the positive con-sequences are balanced by the negatives. Agreeing on a defi nition of ecosystem carrying capacity overlaps, thus, with the highest - order determination — social carrying capacity. This can be defi ned as the level of activity that will be tolerated by human societies interested in the ecosystems. One cannot posit a scientifi c defi nition for this beyond what has been stated.

Moving from gross measures of food quan-tity to food quality, there is a general consen-sus that high protein contents in phytoplankton cells, and consequently in seston of coastal waters, generally are able to provide nutri-tional needs of bivalves for dietary protein (Brown et al. 1997 ). In contrast, specifi c lipids, especially long - chain, polyunsaturated fatty acid s ( PUFA s) and certain sterols, may be lim-iting in phytoplankton and seston food sources of bivalves (Trider and Castell 1980 ). These lipids are required as structural membrane components in bivalve cells, rather than for


where historical bivalve populations have been reduced by fi shing and other human activities, restoration of bivalve feeding and nutrient recycling activities could serve to restore or “ rebalance ” trophic structure. Fundamentally, though, assimilation of nitrogen and phospho-rus into shellfi sh tissues provides an opportu-nity to remove these nutrients from the environment during harvest. Only recently has this environmental benefi t been recognized (Offi cer et al. 1982 ; Rice 1999 ; Lindahl et al. 2005 ). The implementation of nitrogen trading mechanisms to manage coastal eutrophication is providing an opportunity for shellfi sh farmers to realize a portion of the ecosystem service value of their harvests (Ferreira et al. 2007 ) (see Chapters 1 and 8 of in this book).

Finally, to project into the future, the fi lter - feeding activities of cultivated bivalve mol-luscs can be viewed as a natural solution to a current problem in microalgal technology. Large investments are being made into devel-opment of technologies to mass - culture micro-algae for the purpose of producing biofuels (Chisti 2007 ). One of the main technical and economic challenges in this technology is removing the microalgal biomass from the water in which it is suspended. Bivalve mol-luscs do this very effi ciently, and eutrophic estuaries are already growing more phyto-plankton than the largest planned bioreactor of pond - based microalgal farms. Even if con-verting bivalve biomass into biodiesel is not practical, harvest of cultivated bivalves from eutrophic estuaries, planted for the purpose of eutrophication mitigation, is also a way to extract marine protein and lipids from micro-algae in a form with other possible uses. In one ongoing project in Sweden, mussel meal and oils are being used in poultry feeds as replace-ments for fi sh meal (Lindahl et al. 2005 ). A major controversy stalling development of carnivorous fi sh aquaculture expansion is the concern that “ feeding fi sh to fi sh ” will further deplete the forage base for natural fi sh stocks and cause a global imbalance in fi sher-

diatom frustules, however, can be returned to the environment in a form, the mineral opal, that is only slowly remineralized under condi-tions found within biodeposits (Nelson et al. 1995 ). Thus, molluscan shellfi sh can be con-sidered effi cient recyclers of nitrogen and phosphorus in the environment (Smaal and Zurburg 1997 ; Souchu et al. 2001 ; Newell et al. 2005 ), but they may represent a sink for silica. Thus, intense feeding by bivalves can be considered an activity that encourages the growth of nondiatom microalgae on recycled nitrogen and phosphorus. This is the process characterized as the “ cultivation ” of a fl agel-late food source by bivalve populations (Prins et al. 1998 ). Nondiatom taxa do include fl agel-lates in several taxonomic groups that are useful nutritionally, for example, prasino-phytes, prymnesiophytes, and cryptophytes. Harmful dinofl agellate and cyanobacterial taxa, however, may also benefi t from bivalve selective recycling of nitrogen and phosphorus. The possible contribution of intensive bivalve aquaculture to increases in harmful algal blooms can be theorized, but there is no evi-dence, even circumstantial, that this has occurred. Indeed, bivalves tend to fi lter and partially degrade many harmful algal species (Cerrato et al. 2004 ; H é garet et al. 2007, 2008 ) and seem to serve mainly as a vector transporting possibly viable cells from pelagic to benthic compartments in the environment.

Summary and p rospects

Trophic interactions between shellfi sh aqua-culture and phytoplankton fundamentally involve feeding and nutrient recycling activi-ties of bivalve molluscs, which tend to sustain primary production locally, but favor nondia-tom taxa. This sustained primary productivity during summer may benefi t other planktivo-rous animals, for example, micro - and meio-zooplankton that can contribute to the fi nfi sh food chain. In shallow, coastal ecosystems


ies trophic structure (Naylor et al. 2000 ). Rather than “ microalgal biomass - to - biofuel ” technologies, one can envision development of “ coastal eutrophication - to - fi sh feed ” tech-nologies that solve two problems simultane-ously using trophic interactions between phytoplankton and aquacultured bivalve mol-luscs as the functional “ clutch. ”

Acknowledgments

Many thanks to the following colleagues for discussions stimulating the thoughts expressed in this paper: Sandra Shumway, Chris Brown, Mark Tedesco, Robert Rheault, Odd Lindahl, Michael Rubino, Arthur Glowka, Loy Wilkinson, and Frank Trainor.

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shellfish aquaculture and the environment (shumway/shellfish aquaculture and the environment) ||...

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