Ecosystem Services of Bivalves: Implications for Restoration
OVERVIEW OF ECOSYSTEM SERVICES PROVIDED BY BIVALVE MOLLUSCS
Over the past quarter century, collaborations among mollusc biologists, biological oceanographers, fluid dynamicists, ecosystems ecologists, and natural resource economists have developed an appreciation of the many roles that suspension-feeding bivalves play in organizing estuarine and, to a lesser degree, coastal marine ecosystems. Following publication of the seminal book Nature’s Services (Daily, 1996), ecologists and natural resource economists have collaborated extensively to identify and partially quantify important services provided by organisms and natural habitats. This research has important applications to natural resource management. Traditional approaches to managing environmental resources often failed to recognize the costs of taking those services for granted and allowed development to degrade natural ecosystems and processes in ways that reduce the often substantial value of ecosystem services (Costanza et al., 1997). Appreciation of ecosystem services also helps prioritize and direct ecological restoration to enhance those resources that provide high levels of ecosystem services, for example, by targeting species that have declined from levels that prevailed before intense human modifications of the environment. This line of research has transformed perceptions about the value of oysters in particular, indicating that oysters and the reefs that they form can provide valuable ecosystem services (Lenihan and Peterson, 1998; Coen et al., 2007) that probably greatly exceed the value of oysters as an exploited commodity (Grabowski and Peterson, 2007). Many of the impacts
of suspension-feeding bivalves on the estuarine and marine ecosystem are potentially beneficial. This chapter acknowledges the potential ecosystem services that can be provided by suspension-feeding bivalves—as long as negative influences are effectively avoided or mitigated.
Although oysters have been the dominant target of these evaluations of bivalve ecosystem services, the beneficial biogeochemical functions provided by oysters are also provided by other suspension-feeding bivalves (Herman and Scholten, 1990; Dame, 1996; Dame and Olenin, 2005). All suspension-feeding bivalves filter particles, including phytoplankton, particulate organic matter, inorganic particles, and planktonic larvae of some marine invertebrates, from the water column and discharge biodeposits, a process that removes phytoplankton and biotic and abiotic particulates from suspension, clarifies the water column, may reduce settlement of some native marine invertebrates, and transfers organic- and nutrient-rich particulates to the bottom (Dame, 1996; Newell, 2004; Dumbauld et al., 2009). Oysters are physiologically capable of maintaining their active filtering function at higher concentrations of particulates, in large part because of their ability to reject particles before actual ingestion and eliminate them as pseudofecal biodeposits, whereas clams, cockles, and scallops lower their clearance rates as particle concentrations increase (Vahl, 1980; Prins et al., 1991; Hawkins et al., 1998a, b). The wide range of environmental conditions over which oysters can reduce turbidity and deposit organic material onto the bottom potentially renders their filtering services most valuable among suspension-feeding bivalves, especially when they exist as reefs of densely concentrated individuals. Pacific oysters (Crassostrea gigas) build structural reefs that project up into the water column in areas otherwise characterized by relatively flat sedimentary bottom, providing important habitat for other organisms (Coen et al., 2007; Grabowski and Peterson, 2007). This habitat provision service is less pronounced in infaunal and non-reef forming bivalves (e.g., native Olympia oysters [Ostrea lurida]). Blue mussels (Mytilus edulis) occupying soft-sediment habitats do not project up into the water column to any substantial degree, and the structures that they provide do not benefit from the vertical relief so important to oyster reefs (Lenihan and Peterson, 1998; Lenihan, 1999; Schulte et al., 2009). Nevertheless, they provide complex interstitial and outward-projecting structural habitat for many marine invertebrates and modify the community composition (Buschbaum et al., 2009). Mytilus californianus and other mussels occupying rocky habitats do provide structural habitat used by many small crustaceans and other invertebrates and fish (Paine and Suchanek, 1983). The shared biogeochemical functions of water clarification and biodeposition make all suspension-feeding bivalves a valued provider of ecological services to shallow-water ecosystems (detailed for oysters in Grabowski and Peterson ).
BIVALVE ECOSYSTEM SERVICES
Turbidity Reduction by Filtration
Oysters and other suspension-feeding bivalves help buffer shallow waters of estuaries and coastal oceans against developing and sustaining excessive phytoplankton blooms in response to anthropogenic loading of nitrogen (Officer et al., 1982). These bivalves also remove inorganic sediments from suspension, thereby counteracting sedimentation from soil erosion (Landry, 2002). Chlorophyll concentration and turbidity are fundamental indicators of water quality. The filtration exerted by suspension-feeding bivalves can remove inorganic particles from the water column and the phytoplankton from suspension and can counteract a negative symptom of eutrophication (Haamer, 1996). This effect of suspension-feeding bivalves is most dramatically illustrated (see Box 1.1) by studies of the invasive clam Potamocorbula in San Francisco Bay (Alpine and Cloern, 1992; Thompson, 2005) and the zebra mussel after its invasion of and proliferation in the Great Lakes (MacIsaac, 1996; Strayer, 2009). Coupled biology–fluid dynamics studies have demonstrated how mussels also reduce phytoplankton concentration (Frechette et al., 1989) and how model clams in sediments (Monismith et al., 1990; Newell and Koch, 2004) affect particulate concentrations in the water column, consistent with field measurements on various real clams (Peterson and Black, 1991). The resulting enhancement of water clarity allows deeper light penetration, which has been shown to increase growth of submerged aquatic vegetation (SAV) (Everett et al., 1995; Carroll et al., 2008; Wall et al., 2008). SAV habitat has declined dramatically in many lagoons and estuaries around the world (Lotze et al., 2006; Orth et al., 2006; Waycott et al., 2009). Because of the importance of SAVs as a nursery habitat for many commercially important fish, crustaceans, and molluscs, the ecosystem services attributable to turbidity reduction by suspension-feeding bivalves include enhancement of an estuarine nursery habitat that itself serves valuable functions in the estuary. Growing use of remote sensing with ocean color from satellite images has important potential for assessing the magnitude and spatial and landscape scales of bivalve filtration on turbidity and phytoplankton concentrations (International Ocean Colour Coordinating Group, 2009).
Biodeposition of Organics Containing Plant Nutrients
The process of bivalve depositing nutrients and organic carbon and nitrogen to the bottom helps to fertilize benthic micro- and macroalgae and SAVs. Modeling and empirical studies have demonstrated that this fertilization process contributes to higher SAV production, a second
mechanism by which bivalves serve the estuarine ecosystem by promoting growth and development of SAV habitat (Reusch et al., 1994; Everett et al., 1995; Peterson and Heck, 1999; 2001a, b; Carroll et al., 2008). Organic deposition presumably also promotes the growth of deposit-feeding and herbivorous benthic invertebrates, which serve as prey for crabs and demersal fish, so the value of soft-sediment habitats to demersal predators on higher trophic levels may be enhanced by organic deposition from suspension-feeding bivalves. Oysters probably generate greater per capita organic deposition than other bivalve types because of their high filtration rate and capacity to discharge pseudofeces and thereby continue filtration under conditions of high turbidity. In areas of limited flow and long water residence times, biodeposition by dense concentrations of bivalves can be detrimental, causing oxygen depletion in the sediments.
Induction of Denitrification Associated with Organic Deposition
Several researchers have demonstrated that the biodeposits created by mussels and oysters induce denitrification, a process that helps counter-act eutrophication by returning nitrogen into the atmosphere as inert nitrogen gas (Hatcher et al., 1994; Newell et al., 2002, 2005; Nizzoli et al., 2007). This function depends upon the capacity of the biodeposits to create anoxic microzones in the surface sediments where denitrifying bacteria are promoted. It seems likely that this ecosystem service is also associated with biodeposition by bivalves in general.
Sequestration of Carbon
Suspension-feeding bivalves produce external shells constructed of calcium carbonate. These shells thereby sequester carbon for long periods of time, dependent on the depositional environment in which the shells come to rest post mortem. Shells remaining in contact with brackish waters of estuaries or seawater in the coastal ocean will be subject to relatively rapid bioerosion by sponges and chemical dissolution as a function of acidity of the waters (e.g., Peterson, 1976). Shells incorporated deep into the sedimentary strata beneath the seafloor and shells buried in soils on land will remain intact indefinitely, allowing the molluscs to provide a long-lasting service of preventing the carbon from re-entering the atmosphere. Since molluscs are brought to land after harvest and their empty shells often discarded or buried terrestrially, mariculture probably increases the net long-term carbon sequestration in shells, as many of them are permanently removed from the growing waters. Removal of shell from the estuary or coastal ocean, however, inhibits the
degree to which the calcium carbonate can act as a buffer to acidification and as a promoter of recruitment and survival of those recruits by adding structural complexity to the sediments.
Provision of Structural Habitat That Promotes Epibiotic Diversity and Fish and Crustacean Production
Bivalve molluscs differ greatly in the habitat they provide, depending on whether they are completely infaunal in life position or whether they occupy sedimentary or hard bottoms. Among all molluscs, oysters are the most important providers of biogenic habitat because some can construct hard-bottom reef habitat that can rise well above the bottom in areas otherwise characterized by sediment. Eastern oysters (Crassostrea virginica) construct the most substantial reefs, although elevations of natural subtidal reefs have been substantially reduced by repeated habitat damage by dredges and other harvest gear (DeAlteris et al., 2004; Lenihan and Peterson, 1998). The presence of this hard substrate enhances biodiversity of macroalgae and benthic invertebrates that require stable hard substratum for attachment (Wells, 1961; Bahr and Lanier, 1981; Bruno and Bertness, 2001). The benthic invertebrate production together with the provision of structural habitat enhances use of the area by fish and mobile crustaceans by increasing prey availability and providing protection from higher-order predators amid the reef structure (Coen et al., 1999; Lenihan et al., 2001; Peterson et al., 2003; Coen and Grizzle, 2007). Empty shells of semi-infaunal bivalve, like pen shells (Pinna and Atrina spp.) and gaper clams (Tresus spp.), which remain in place after death of the molluscs, offer this habitat service to a lesser degree (Palacios et al., 2000; Gutierrez et al., 2003). Some mussels, such as the blue mussel, can form extensive beds on sedimentary habitats increasing habitat heterogeneity and harboring significantly different species assemblages from the surrounding sediments (Buschbaum et al., 2009). On hard substrata, shells of bivalve molluscs (e.g., mussels) do not represent the only local hard-bottom habitat. Nevertheless, the multiple layering of mussels in beds creates unique habitat occupied by at least 300 species of invertebrates (Paine and Suchanek, 1983; Beadman et al., 2004). Habitat provision is trivial to absent for completely infaunal clams (e.g., quahogs, soft-shell clams, cockles, surf clams). Some infaunal bivalves do serve as anchors for holdfasts of macroalgae, like Katelysia rhinophera hosting Hormosira banksii in Princess Royal Harbor, Western Australia (Black and Peterson, 1987), and such macroalgal growth is habitat for many smaller crustaceans and fish.
Not only do suspension-feeding bivalves influence the ecosystem through providing hard surfaces and interstitial spaces that offer habitat
for epibiota and fish and mobile crustaceans, but dense assemblages of these species also affect near-bottom flow regimes by emergent structure baffling water flows (Lenihan, 1999) and by creating strong current flows from exhalent siphons (O’Riordan et al., 1993). Changing flow patterns have significant direct and indirect effects on the geology, chemistry, and biology of the bottom habitats.
Habitat and Shoreline Stabilization
Some bivalve molluscs play important roles in stabilizing the bottom or protecting the shoreline from erosion by waves and currents. Oyster reefs rising up from the sedimentary bottom and positioned in linear arrays along marsh shorelines serve as natural living breakwaters that trip wave energy before it can strike and erode the marsh shoreline (Myer et al., 1997; Piazza et al., 2005). The giant clam (Tridacna gigas) helps cement and stabilize the calcium carbonate sediments and thereby promote recruitment of corals and recovery of coral reefs (Edgardo Gomez, personal communication). Mussels on rocky shores are not likely to play any role in stabilizing the rock substrate, and infaunal bivalves and scallops play only a modest role in stabilizing sediments.
USE OF MOLLUSCS TO PROMOTE ESTUARINE RESTORATION
Wild stocks of bivalve molluscs are susceptible to overexploitation by fishermen and have generally been depleted from estuaries and coastal oceans worldwide. Bivalve molluscs in soft sediments occupy an essentially two-dimensional bottom habitat; are largely sessile; can often be visually located by some surface clues, such as siphon openings, if not directly in the line of sight of fishermen; and, along with epifaunal bivalves like mussels, are readily accessed by fishermen because of their occupation of shallow or intertidal depths. All these characteristics combined with failures of fisheries management help to explain widespread depletion of bivalve molluscs.
The bivalve molluscs of estuarine sedimentary habitats are generally the most seriously depleted, whereas mussels are so abundant on rocky shores that they can sustain current fishing mortality in many locations (although see Lasiak  for concerns and examples). Eastern oysters have declined in the Chesapeake Bay, Pamlico Sound, and other western Atlantic estuaries and coastal lagoons to perhaps only 1–2% of historic abundance prior to 1900 (Newell, 1988; Rothschild et al, 1994; Kirby, 2004). Worldwide, oysters have been grossly depleted from estuaries by overfishing, sedimentation, pollution, habitat damage, and disease (Lotze et al., 2006; Beck et al., 2009). Quahogs (Mercenaria mercenaria) are greatly
depleted by overfishing in eastern states (Peterson, 2002; Kraeuter et al., 2005; Myers et al., 2007). Soft-shell clam (Mya arenaria) populations are much depressed in many states by overfishing, predation by the invasive green crab, and perhaps also disease, and bay scallop fisheries have nearly disappeared for lack of scallops (Peterson et al., 2001; Myers et al., 2007). With the exception of less-accessible areas like Alaska and subtidal areas (e.g., geoducks in Washington), native hard-shell clam and oyster fisheries on the Pacific coast of the United States have declined and/or sometimes been replaced by introduced species like the manila clam (Venerupis phillipinarum) and Pacific oyster (Lindsay and Simons, 1997; Robinson, 1997; Shaw, 1997).
Because of growing recognition of the ecosystem services provided by suspension-feeding bivalves, environmental advocates have increasingly pursued bivalve restoration as a component of restoring historical baseline conditions and functioning of estuaries (Rice, 2000). This remediation has been especially strong for oysters, in part because of their exceptional capacity for biogeochemical services associated with filtration under high turbidities but also because of the importance of habitat services provided by oyster reefs. Restoration of oyster filtration and deposition can restore water clarity, buffer against excess phytoplankton blooms induced by anthropogenic nutrient loading, filter out inorganic sediments, and lower turbidity (Everett et al., 1995; Carroll et al., 2008). Restoring native oysters can not only bring back an important species toward historical baseline levels but may also restore the filtration functions that improve water quality and enhance resilience of the estuarine ecosystem to eutrophication (Jackson et al., 2001a; Lotze et al., 2006). Oyster restoration also helps re-establish the biogenic habitat functions played by oyster reefs. Restoration of Eastern oyster reefs has been slow, in part because the less costly, shallowly constructed reefs tend to sink and become covered with silt, therefore reducing their habitat value (Stokstad, 2009). Indirectly, oyster restoration can also aid recovery of a critical nursery habitat, SAV, by improving light penetration to the bottom and by fertilizing the grasses via biodeposits (Carroll et al., 2008; Wall et al., 2008). This may lead to further enhancement of fish and crustacean production of species supported by SAV habitat.
Although most environmental advocacy of bivalve restoration has focused on oysters, other suspension-feeding bivalves play similar biogeochemical roles in the ecosystem. For example, restoring quahogs into existing SAV beds has been proposed by environmental organizations because of this biogeochemical function, and many species of bivalves could eventually be incorporated into ecological remediation and restoration plans.
A ROLE FOR MOLLUSCAN MARICULTURE IN ESTUARINE AND COASTAL OCEAN RESTORATION
If enhancing the abundance of suspension-feeding bivalves in estuarine and coastal ocean ecosystems helps restore beneficial functions and conditions that characterized the ecosystems prior to extensive human intervention, then to the degree that it replicates those functions, mariculture of these same or functionally analogous suspension-feeding bivalves to some degree holds the same promise (Haamer, 1996; Rice, 2000; Smaal et al., 2001; Landry, 2002; Newell, 2004). Consequently, bivalve mariculture deserves consideration as an estuarine, and perhaps also a coastal, ocean ecosystem restoration tool. Oysters may represent the most desirable type of bivalve for restoration of estuarine ecosystems because of their wide tolerance of turbidity, but other bivalve species can provide the same beneficial biogeochemical functions. Bivalve mariculture could serve to mitigate certain water-quality challenges, like excess chlorophyll or turbidity. In principle, culturists could receive appropriate compensation for mitigation based upon the level of environmental improvement achieved, and they could also sell their product, providing economic support to grow the industry and to enhance locally grown seafood production.
Mariculture of bivalve molluscs differs from restoration of native bivalves in the wild in several ways. Most culture methods for bivalves involve introduction of artificial materials to hold or protect the molluscs during grow-out. Although the structure provided by mariculture gear does not match the structure created by the corresponding wild molluscs, the structures associated with mariculture gear can themselves provide structural habitat for benthic epibiota, mobile crustaceans, and fish (DeAlteris et al., 2004; Powers et al., 2007). Because so much Eastern oyster reef habitat was lost to shell mining and oyster dredging, some mariculture structures that occupy a wide range of the water column may provide more functional hard-substrate habitat than degraded natural reefs. Natural populations of other oysters do not construct nearly as substantial vertical reefs, in which case mariculture gear may provide more high-relief, structural habitat. However, the introduction of artificial hard substrates often leads to colonization by invasive tunicates and other nonnative clonal invertebrates, clearly not members of the historical baseline ecosystems. Thus, regular removal and responsible disposal of nonnative epifauna from racks, bags, nets, lines, cages, and other mariculture gear should be included in managing any bivalve mariculture used for restoration. In addition, some of this gear has the potential to entangle water birds, marine mammals, and turtles so site-specific testing of alternative gears and appropriate adaptive management to avoid gear impacts on vertebrates is in order. Management concerns include potential degradation of bottom habitat by overloading bivalve molluscs in shallow
areas without sufficient physical flushing to disperse organic loading and resultant sediment anoxia and by other processes, such as application of bottom-disturbing harvest gear. Most bivalve mariculture requires active management and maintenance of the gear, which involves direct human visitation, on foot or by boat. This activity can disturb sensitive or protected species, implying a need to manage human activity so as to avoid disturbance of valued species. In addition, mariculture of molluscs can introduce nonnative hitchhikers and disease microbes so protocols for transport, isolation, quarantine, breeding, and introduction of first-generation molluscs need to be followed to minimize risks of unintended introductions (International Council for the Exploration of the Sea, 2005). Furthermore, hatchery health and inspection protocols need to be followed to insure that eyed larvae for importation are free of any diseases not already present in the recipient location.
Because harvest for human consumption of suspension-feeding bivalves requires growing waters that are low in pathogens and pass the standard fecal coliform bacterial assays, it is often tempting to locate mollusc farms near parks, sanctuaries, reserves, and other locations where pollution from stormwater and industrial contamination is minimal. Such locations often coincide with the most valuable wildlife habitats so conflicts between bivalve mariculture and wildlife protection can arise (Würsig and Gailey, 2002). Resolution of these conflicts is usually feasible, but a proper set of siting and operations protocols that avoids unacceptable negative consequences of human disturbance and gear entanglements is required in and around parks, sanctuaries, and reserves. Furthermore, the social considerations associated with protection of natural areas, especially Wilderness Areas within national parks, could lead to exclusion of mariculture operations as a policy decision because of incompatibility with the concept and goals of a wilderness.
FINDINGS AND RECOMMENDATIONS
Finding: There is a need for improved quantifying of ecosystem service values so that markets for these ecosystem services could be further explored. Through a market-based approach, the present practice of externalizing the lost value could be changed to a system that assesses the true costs to those who contribute to the deterioration of natural estuarine and coastal marine ecosystems services.
Recommendation: Research at the interface of biology and natural resource economics should be aggressively supported to explore the various proposed ecosystem services of bivalve molluscs and to develop rigorous economic methods of putting values on those services. This could include methods that specify market values for those
services that yield to this approach and methods involving “willingness to pay” and other public preference approaches where markets do not exist. This research should then be utilized by policy makers to achieve social equity in putting costs of service losses on those responsible and using fees paid for lost services to restore those ecosystem services and thereby preserve them for the general public trust.
Finding: Many estuaries suffer from eutrophication and potentially could benefit from increasing the biomass of suspension-feeding bivalves to provide resilience to eutrophication and reduce the symptoms of excessive nutrient and sediment loading. In addition to limiting effects of eutrophication and sedimentation, restoring the beneficial biogeochemical functioning of suspension-feeding bivalves, especially oysters, could provide additional ecosystem services associated with filtration of phytoplankton and inorganic particles from the water column and deposition of organic biodeposits. These effects will be greatest in shallow and well-mixed water bodies, such as those typically found in estuaries, coastal bays, and lagoons.
Recommendation: Policies should be developed to encourage restoration of the biogeochemical filtration functions associated with suspension-feeding bivalves in estuaries. Such policies should consider both recovery of wild stocks and mariculture of (preferably native) suspension-feeding bivalves to restore the filtration functions and associated ecosystem services. For restoration purposes, particular attention should be given to (1) establishing genetic husbandry guidelines to prevent loss of genetic diversity; (2) avoiding negative effects of disturbance of vertebrates and other valued species; (3) controlling spread of nonnative fouling organisms, especially certain tunicates; (4) regulating bivalve stocking to require use of eyed larvae from certified hatcheries with an effective and comprehensive disease inspection or to first-generation seed spawned from adult bivalves under quarantine conditions in order to minimize species introductions and disease spread; (5) insuring that bivalve shellfish loading does not exceed levels that have unacceptable negative impacts on the benthos through excessive organic loading or on other components of the ecosystem through clearance of planktonic foods and organic particles from the water column; (6) preventing unacceptable damage to bottom habitat by harvest gear; and (7) assessing the social tolerance for mariculture on a site-specific basis.