Comparative Evaluation of Native Bivalve Species Restoration for Water Quality Improvement in the Chesapeake Bay and Other Mid-Atlantic Watersheds

A review in support of:

Executive Order 13508—“Chesapeake Bay Protection and Restoration” FW20 White paper: “Evaluate native bivalve restoration for water quality improvement”

Action 1: “Complete literature review of relevant studies on the ability of tidal and non- tidal (freshwater and estuarine) bivalves to enhance water quality. Where the literature review finds gaps, identify topic areas and funding needed to support new studies to evaluate the effect of native bivalves on Bay water quality.”

Danielle A. Kreeger1, Catherine M. Gatenby2and Peter W. Bergstrom3

1 Partnership for the Delaware Estuary, Wilmington, DE 2 Lower Great Lakes Fish and Wildlife Conservation Office, Basom NY 3 NOAA Chesapeake Bay Office, Annapolis, MD

Match 31, 2017

Note: this document is a DRAFT that is intended for publication. Appendices comprise supplemental documents in separate files. Please contact the first author with questions or if current versions are sought. Until publication, the document can be sited as follows:

Kreeger, D. A., C. M. Gatenby and P. W. Bergstrom. 2015. Comparative evaluation of native bivalve species restoration for water quality improvement in the Chesapeake Bay and other Mid-Atlantic watersheds. Partnership for the Delaware Estuary, Wilmington, DE. PDE Report No. 17-05. 96 p.

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TABLE of CONTENTS TABLE of CONTENTS ...... 1 EXECUTIVE SUMMARY ...... 5 BACKGROUND ...... 11 GOALS ...... 13 BIVALVE FILTRATION ...... 15 Definitions ...... 15 Measuring comparable clearance rates...... 15 Measuring bivalve density and biomass ...... 16 Tidal Bivalve Filtration ...... 16 Non-tidal Bivalve Filtration ...... 21 SPECIES INVENTORY OF CLEARANCE RATES: FILTER FEEDERS THAT COULD IMPROVE WATER QUALITY AND PROVIDE OTHER SERVICES IN CHESAPEAKE BAY AND TRIBUTARIES ...... 23 Non-tidal (freshwater) bivalves ...... 33 Asian clam (Corbicula sp.) ...... 33 Zebra and quagga mussel (Dreissena polymorpha and D. rostriformis bugensis) ...... 33 Eastern elliptio (Elliptio complanata) ...... 34 Other freshwater mussels ...... 35 Estuarine (tidal) bivalves ...... 36 Brackish water clam (Rangia cuneata) ...... 36 Dark false mussel (Mytilopsis leucophaeata) ...... 37 Baltic macoma clam (Macoma balthica) ...... 38 Soft-shell clam (Mya arenaria)...... 38 Hooked or bent mussel (Ischadium recurvum) ...... 39 Atlantic ribbed mussel (Geukensia demissa) ...... 40 Stout razor clam (Tagelus plebeius) ...... 42 Eastern oyster (Crassostrea virginica) ...... 42 Hard clam (Mercenaria mercenaria) ...... 42 Blue mussel (Mytilus edulis) ...... 43 RECENT, CURRENT, AND PLANNED RESTORATION OF BIVALVES FOR ECOSYSTEM SERVICES ...... 43 Open waters of estuaries (subtidal) ...... 43 Recommended subtidal estuarine species for restoration in the Chesapeake watershed ...... 44

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Fringing waters of estuaries (Intertidal) ...... 46 Freshwater streams and rivers (non-tidal and freshwater tidal) ...... 47 Recommended freshwater species for restoration in the Chesapeake watershed ...... 50 DEVELOPING A BIVALVE RESTORATION STRATEGY AND ESTIMATING ECOSYSTEM SERVICES ...... 57 First step: obtain empirical data on weight-specific clearance and filtration rates by target species ... 57 Second step: appraisal of current population abundance and size distribution ...... 58 Third step: model the movement of water and associated pollutants ...... 58 Fourth step: develop a quantitative understanding of the fate of filtered matter ...... 59 Fifth step: develop a model of the current system’s carrying capacity for the target species of bivalves ...... 59 Sixth step: find sources for the target bivalve species, or determine propagation methods if no sources are available ...... 60 Seventh step: optional test to gauge restoration suitability ...... 60 Eighth step: Restoration ...... 60 POSSIBLE IMPEDIMENTS TO THE IMPLEMENTATION OF BIVALVE RESTORATION FOR ECOSYSTEM SERVICES ...... 61 Science Needs ...... 61 Human Health /Competition with Commercial Aquaculture ...... 62 Public Perception/Education ...... 63 Funding ...... 63 RECOMMENDATIONS ...... 64 ACKNOWLEDGMENTS ...... 65 REFERENCES ...... 66 GLOSSARY...... 81 (see separate appendix file) ...... 85 Appendix A. Maps of recent distribution of selected bivalve species in Chesapeake Bay...... 85 A.1. Brackish water clam (Rangia cuneata), soft bottom (all years with random data)...... 85 A-2. Soft‐shell clam (Mya arenaria), soft bottom (1990 onward)...... 85 A-3. Ribbed mussel (Geukensia demissa), soft bottom (1990 onward)...... 85 A-4.Hooked (bent) mussel (Ischadium recurvum), hard bottom, 2009 (most recent data). From MD fall oyster survey...... 85 A-5. Dark false mussel (Mytilopsis leucophaeata), hard bottom, 2009 (most recent data). From MD fall oyster survey...... 85

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A-6. Stout razor clam (Tagelus plebeius), soft bottom (1990 onward)...... 85 Appendix B. Box plots of density and line graphs of % occurrence by species by year (CBP benthic data)...... 85 B-1. Asian clam (Corbicula fluminea) ...... 90 B-2. Brackish water clam (Rangia cuneata) ...... 91 B-3. Dark false mussel (Mytilopsis leucophaeata) ...... 92 B-4. Baltic macoma clam (Macoma balthica) ...... 93 B-5. Soft-shell clam (Mya arenaria) ...... 94 B-6. Ribbed mussel (Geukensia demissa) ...... 85 B-7. Stout razor clam (Tagelus plebeius) ...... 85

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EXECUTIVE SUMMARY Bivalve mollusks provide water quality benefits throughout the Chesapeake Bay and its tributaries. While most of the attention on those benefits has focused on the role of the eastern oyster, Crassostrea virginica, in estuarine ecosystems, there are a number of other bivalves, both estuarine and freshwater, that provide similar benefits. The water quality benefits of other bivalves are much more poorly known, so one of the actions under Executive Order 13508, “Chesapeake Bay Protection and Restoration” was to produce a white paper summarizing what was known about the filtration ability of those other bivalves. This white paper was written in response to that action.

Bivalve mollusks furnish diverse ecosystem services, including providing complex habitats for other biota and stabilizing bottoms. Some species in some habitats also serve as commercial resources and build reefs that help protect coastlines. With few exceptions, bivalves are perhaps most heralded for their benefits to water quality because of their filter-feeding lifestyle. Most of the water quality benefits from bivalves come directly or indirectly from how they feed, by filtering the water in which they live. Bivalves pump water across their enlarged gills which function both in gas exchange as well as feeding. The volume of water cleared of particles per unit time is referred to as the “clearance rate,” whereas the biomass of particles that is removed per unit time is referred to as the “filtration rate.” Filtration rate is relevant to ecological impacts as is clearance rate, but it is much harder to measure. Thus, we found fewer studies of filtration across all marine and freshwater bivalves than clearance rate.

The removal of suspended matter from the water column can improve water clarity. Nutrients are often associated with these suspended particles, either adsorbed to particle surfaces or within particles such as algae, and bacteria. Some of those nutrients are then incorporated into the tissues of the bivalves, some are added to the sediments in biodeposits, and some are returned to the water column as dissolved byproducts. Thus, nutrients are not all removed from the aquatic ecosystem by bivalves over the long term, but they are removed from the water column in the short term, thus improving water quality. Furthermore, dissolved nutrients that are returned to the environment may be transformed by the animals into compounds that are more usable by other biota. Particulate matter in biodeposits may get buried or used by deposit-feeders or bacteria, including denitrifying bacteria.

This review had three main goals:

1. Evaluate whether native bivalves other than C. virginica provide similar ecosystem services for improving water quality and habitat quality. 2. Review whether the species with high clearance rates could be considered for use in restoration projects to improve water quality, potentially diversifying the places and habitats for bivalve- mediated improvements. 3. Assess what we know about limiting factors for populations of each promising species, to determine if we can realistically overcome those limiting factors through restoration.

The ability of filter-feeding bivalves to improve water quality has been the subject of intense research for the past 30 years or more, with the most focus on commercial species such as oysters. But the

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 5 restoration of bivalves for the principal purposes of sustaining and improving water quality has only recently garnered widespread attention and support. This “Biofiltration” approach (using bivalves or other animals to improve water quality) has not been widely tested in the Chesapeake Bay, but we believe it could enhance the array of choices available for improving water quality and habitats within the Chesapeake Bay and its tributaries, especially if the fuller array of species is considered.

In our review, we found four native species of bivalves that occur in estuarine systems and have water clearance rates similar to C. virginica (names in bold in Table E-1). It is plausible that the effects of some of the four native estuarine species on water quality could be equal to and possibly greater than those of C. virginica, depending on total biomass and other factors. Also, the cumulative effects of restoring multiple species of native bivalves within a range of habitats could be significantly greater than any single-species restoration project because different species occupy different niches and areas. We also identified three non-native estuarine bivalves that had high clearance rates (those without their names in bold in Table E-1), but we decided, after consulting with invasive species experts, these should not be considered for restoration projects.

The four native estuarine (tidal) bivalves with clearance rates similar to those of C. virginica are as follows, in decreasing order of clearance rates (Table E-1):

• Ribbed mussels (Geukensia demissa) which were used in a recent biofiltration pilot study in the Bronx River; • Hooked mussels (Ischadium recurvum) can reach very high density, but have not been tested for biofiltration potential; • Soft-shell clams (Mya arenaria) were planned for a pilot biofiltration study in the West River in 2012, but most of the animals died before the study started; and • Dark false mussels (Mytilopsis leucophaeata) were part of a natural experiment in 2004, when hundreds of millions of them appeared in several low mesohaline Chesapeake tributaries, and some of those tributaries had documented improvements in water quality and submerged aquatic vegetation (SAV) area when they were present (but most of the mussels were gone by 2005).

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Table E-1. Clearance rates for C. virginica and other estuarine (tidal) Chesapeake bivalves, arranged from highest to lowest maximum rates in two groups (native and non-native). The seven other bivalves listed all had maximum clearance rates that were at least 30% of the minimum rate for C. virginica. Three native species are recommended for use in restoration in different habitats (last column).

Species Clearance rate (l h-1 Salinity range from Best for restoration g−1 of dry tissue) literature in: Native species Eastern oyster, 6.4- 11.5 7-30 Subtidal Crassostrea virginica Ribbed mussel, 5.1-6.8 10-30 Intertidal & subtidal Geukensia demissa Soft-shell clam, Mya 3.5-4.8 5-30 arenaria Hooked mussel, 4.3 – 4.6 5-30 Subtidal Ischadium recurvum Dark false mussel, 1.7-2.4 0-10 Mytilopsis leucophaeata Non-native species Zebra mussel, 2.7-16.2 0-5 Dreissena polymorpha Asian clam, 2.9 0-2 Corbicula sp. Brackish water clam, 2.1 0.5-10 Rangia cuneata

Based on what we know about the limiting factors for each of the four highlighted species, we are recommending two of them, ribbed and hooked mussels, for consideration for restoration projects designed to increase biofiltration in subtidal areas (Table E-1). One species, G. demissa, is also recommended for intertidal restoration. See “Recommended subtidal estuarine species for restoration in the Chesapeake watershed” below for details.

Twenty-eight species of native freshwater mussels occur in the Chesapeake watershed, but researchers are only beginning to quantify their clearance rates and data are not yet available for all species. Judging from limited studies of freshwater bivalves from outside the Chesapeake, clearance rates of freshwater mussels are generally about 10-50% of those of C. virginica (per unit body mass); however, freshwater mussels are often long-lived (upwards of 30 years for some species in the Chesapeake watershed), and they can be found in extremely high density. Indeed, these studies have shown that mussels often dominate benthic biomass, playing an integral role in ecosystems by linking benthic and pelagic food webs. Thus, restoration of dense beds of freshwater mussels could help intercept

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 7 suspended particles prior to entering the estuary. Based upon an evaluation of interest by natural resource agencies, of species in hatchery production, of likely investment of dollars for hatchery production, and knowledge of species clearance rates, we identified thirteen species of freshwater mussels, including Elliptio complanata, which would be good candidates for a restoration program in targeted tributary streams to the Chesapeake Bay (Table E-2). We also included the endangered James spinymussel (Pleurobema collina) as a species for consideration in a restoration project because it formerly occupied extensive habitats throughout the James River drainage, and because an active propagation program is in place with the US Fish and Wildlife Service’s Harrison Lake National Fish Hatchery and the Virginia Department of Game and Inland Fisheries. Additional scientific collecting permits would be required in order to work with this species.

None of the native bivalves discussed above have a commercial fishery, except the soft-shell clam. This could be a problem, in that larvae and seed are not yet readily available from hatcheries. Any large-scale restoration effort would probably use seed from hatcheries, unless newly settled juveniles could be collected in one area and moved to another, as is often done in the aquaculture of blue mussels, Mytilus edulis. Another restoration option for freshwater mussels is to relocate salvaged mussels expected to be harmed by dredging or other operations.

Restoring noncommercial species can be easier than restoring commercial species because it is easier to get permits to raise them in waters that are closed to shellfish harvest. For example, the use of a noncommercial species was a condition of the permit in two recent bivalve restoration projects: the Bronx River study of ribbed mussels on a raft, and the Delaware Estuary Living Shoreline Initiative with ribbed mussels. There also is generally no pressure of illegal harvest for species that have no commercial fishery, and their cumulative impact is greater when combined with their longevity.

Before trying to restore any species, a review of what is limiting its current abundance will be necessary in order to be fairly confident that populations can be increased through carefully planned restoration. For example, oyster populations are limited by such factors as loss of hard substrate from harvest and sedimentation, low recruitment from falling salinity and dispersed relic beds, disease, hypoxia, parasites, and predators. Thus, if we plant oysters in mud or in a hypoxic dead zone, they will probably die. We also know that oyster recruitment will be poor in low salinity areas and survival of adults will be poor in high salinity areas prone to disease. Intertidal species such as ribbed mussels are generally constrained to shoreline areas such as salt marshes which are themselves rapidly eroding. Much less is known on specific water quality and environmental factors limiting native freshwater mussel populations than is known for oysters or other commercially-valuable tidal bivalves. In general, habitat degradation and dams are the primary causes for declines in freshwater mussels, followed by poor water quality from toxic spills and discharges. Managed restoration of these species through culture and propagation or translocation, however, is possible. Because all bivalve species have constraints on their distribution and abundance, a diversified, watershed-wide restoration strategy is likely to be more successful than a monospecific focus because it can address issues in a broader array of habitat types and areas via the preferred niches of different species.

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Of course, filtration is only one of many ecosystem services provided by bivalves. For example, they also provide food, habitat, and stabilization of bottom sediment, thus benefitting recreational and commercial fisheries. There has been increasing interest recently on another bivalve ecosystem service related to water quality: the tendency for biodeposits from bivalves to increase denitrification rates near the bivalves, compared to areas that lack them. To date this research has focused mainly on C. virginica, but any bivalve can promote denitrification through its biodeposits. In addition, larger populations of freshwater and estuarine bivalves are now thought to help buffer against ocean acidification. Any bivalve restoration project designed to increase biofiltration should also consider these other ecosystem services, and measure them to the extent this is practical.

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Table E-2. Thirteen species of native freshwater mussels found in the Chesapeake Bay Watershed that are good candidates for restoration projects. See Table 5 for more details on each species.

Species Common name In Developing Potential Investment Best use Production Technology Hatchery needed3 (Freshwater Production2 or Tidal Fresh) Alasmidonta triangle floater X high low FW undulata

Alasmidonta brook floater x X high med FW varicosa

Anodonta alewife floater x X high low TF implicata

Elliptio eastern elliptio X high low FW complanata1

Elliptio yellow lance x high low FW lanceolata

Lampsilis yellow lampmussel x high low FW cariosa Lampsilis eastern x high low FW radiata lampmussel Lasmigona green floater x high low FW subviridis Leptodea tidewater mucket x high low TF ochracea Ligumia eastern x high low Both nasuta pondmussel Pleurobema James spinymussel x high low FW collina Pyganodon eastern floater x high low FW cataracta Utterbackia1 paper pondshell X high low FW imbecillis

1 Clearance rates have been measured for this species; see Tables 2 and 3.

2. Potential Hatchery Production Assumptions: Interest level refers to interest by natural resource agencies. high = high interest, high knowledge and expertise; med = medium to low interest, high to medium knowledge, high to medium expertise; and low = low interest, medium to low knowledge, high to low expertise

3. Investment Assumptions: Infrastructure is in place for hatchery production. Costs are estimated for labor (broodstock and host species collection, and hatchery production) and specialty equipment that could be incurred in year one to develop propagation and/or implement production. Annual costs would decline as knowledge and capability increased for production of a species, and could be less per species, if multiple species are in production. High = >$100,000; Med = $50,000-100,000; Low = < $50,000.

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BACKGROUND Executive Order (EO) 13508, “Chesapeake Bay Protection and Restoration” from 2009, included a number of actions to restore water quality and living resources in the Chesapeake Bay. A number of those actions focused on oyster restoration, which has tens of millions of dollars spent on it annually, with funding from federal, state, and private sources. A great deal of research is being done on C. virginica, and their water quality benefits have been measured and modeled. However, there are a number of other bivalves, both estuarine and freshwater, that provide similar water quality benefits. Some of those species co-exist with C. virginica, such as G. demissa, while others live in lower salinity and non-tidal parts of the Chesapeake watershed, such as freshwater mussels. To assess those benefits by other bivalves, the Federal Leadership Council of the EO adopted an EO action to conduct a literature review of those benefits. This white paper was written in response to that action.

Bivalve mollusks live throughout the Chesapeake Bay and the various watersheds that drain into it. The indigenous assemblage includes native species of marine, saltwater, and freshwater tidal and non-tidal bivalves extending from the headwaters to the mouth of the Bay. Generally, the same species exist in the Chesapeake that characterize the Atlantic slope throughout the mid-Atlantic region. Kreeger and Kraeuter (2010) recently tallied more than 60 species of bivalves in the adjacent Delaware River Basin. A few introduced species of bivalves are also sufficiently abundant to be considered ecologically significant in the region (Kreeger and Kraeuter 2010).

Bivalve mollusks in the Chesapeake Bay watershed furnish a variety of important ecosystem services (Table 1). Although the relative importance of specific services varies among species, all species with high population biomass provide many different benefits. For example, a qualitative comparison of the American oyster (Crassostrea virginica), Atlantic ribbed mussels (Geukensia demissa), and a freshwater unionid mussel (Elliptio complanata) indicates that C. virginica are valued for both commercial and ecological reasons, whereas noncommercial G. demissa and freshwater mussels may have comparable or greater ecological value than C. virginica in their respective habitats.

The main ecological benefits of healthy bivalve communities are water quality and habitat improvement, and bottom stabilization. Furthermore, nutrient cycling by bivalves enhances food-web efficiencies and decomposition processes, which leads to improved habitat. Some tidal and non-tidal bivalve species also are known for providing essential fish habitat and stabilizing eroding shorelines. Bivalves have great utility for bioassessment as well. Marine species have long been used for monitoring coastal conditions; e.g. National Status and Trends Mussel Watch (Bushek 2011). Due to their long lifespan and sensitivity to degradation, freshwater mussels are also increasingly valued for tracking status and trends of the health of inland waters (PDE 2008, 2012).

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The focus of this review is on the water quality benefits furnished by bivalve species that live in Chesapeake Bay and its watershed. By filtering vast quantities of water to satisfy their nutritional demands, suspension-feeding bivalves remove suspended particles that include nutrients, various pollutants, and pathogens. By removing particles and either precipitating them in biodeposits or transforming them into less harmful forms, bivalves also increase light availability within the water column which benefits benthic producers such as submerged aquatic vegetation and benthic algae. Although we focus here on bivalve filtration services for water quality improvement, it is important to recognize that the fate of filtered material is highly variable in space and time and that some filtered Table 1. Summary of various ecosystem services furnished by oysters, Atlantic ribbed mussels and freshwater mussels categorized according to the Millennium Ecosystem Assessment (Kreeger and Kraeuter 2010).

pollutants will be recycled to the environment. For example, some nutrients removed by bivalves are transformed from particulate to dissolved forms (remineralization), which can then fuel algal production anew. Biodeposited material can fuel multi-celled benthic organisms as well as enter the microbial loop, leading to complex biogeochemical conversions that can lead to net losses of pollutants (e.g., via burial, denitrification) or recycling of pollutants (e.g., via particle resuspension, nutrient re-release). Burial and denitrification can both improve water quality by retaining or removing nitrogen. Examples of these processes are shown in Figure 1.

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For these reasons, it is important to recognize that the net removal of pollutants will usually be lower than gross capture via filtration. Despite these considerations, the literature is replete with clear examples of water quality improvements rendered by natural bivalve populations, and bulk particle filtration represents a quantifiable metric for estimating these water quality benefits.

Figure 1. Example of ecological processes mediated by suspension-feeding bivalves (from Dan Spooner, USGS).

GOALS This review had three main goals:

1. Evaluate whether native bivalves other than C. virginica provide similar ecosystem services for improving water quality and habitat quality. 2. Review whether the species with high clearance rates could be considered for use in restoration projects to improve water quality, potentially diversifying the places and habitats for bivalve- mediated improvements.

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3. Assess what we know about limiting factors for populations of each promising species, to determine if we can realistically overcome those limiting factors through restoration.

Oyster restoration can and should continue to be investigated as a tactic for water quality remediation in the portion of the system where they are sustainable. However, oyster restoration is challenging as a tool to improve water quality because of very limited shell substrate, high cost, disease susceptibility, their relatively high lower salinity limits (5-10), and other reasons. Diversification of target species may provide new opportunities to achieve greater outcomes for water quality, while also providing tangential benefits to aquatic ecosystems and coastal communities. Restoration of freshwater mussels in non-tidal waterways, for example, could potentially intercept pollutants before they reach the tidal estuary, and restoration of tidal species could potentially help to remediate pollution within the estuary.

Although more surveys are needed to appropriately assess status and trends of noncommercial bivalves, best scientific judgment suggests that all of the dozens of native bivalve species are currently far below their historic abundance. Freshwater mussels are the most imperiled of all animals in North America (about 75% of 300 native species). Of the twenty-eight native freshwater mussel species in the Chesapeake Bay and Delaware River Basins, only one (E. complanata) is considered stable by the States of Pennsylvania, Maryland and Virginia (B. Watson, VDGIF and N. Welte, PAFBC, pers. comm., M. Ashton, pers. comm.). The distribution and abundance of that species, however, is greatly reduced compared to historic reports. Among estuarine species, the Atlantic ribbed mussel (G. demissa) does not appear to be as reduced as other bivalves; however, it is increasingly threatened by the loss of its preferred habitat, tidal marshes (Kreeger et al. 2010, 2011, PDE 2012). Another estuarine bivalve, the soft-shell clam (Mya arenaria), once had a commercial harvest in the Chesapeake Bay, but their numbers have fallen so much that recent Chesapeake harvests average less than 1% by weight of the peak harvest in 1969, with no harvest reported in several recent years (NMFS 2012). Considering today’s reduced population abundances for most if not all native bivalves, significant potential exists to improve water quality from headwater streams to the lower bay by rebuilding stocks back toward the system’s carrying capacity, similar to the current interest in returning oyster stocks to past levels where they apparently filtered more of the bay’s volume (Newell 1988).

Of course, this focus on filtration capacity and water quality benefits is oversimplified. The actual net effects of bivalve populations on water quality depend on complex hydrodynamic, biogeochemical, and ecological interactions as discussed earlier, and more studies are needed. Populations of bivalves are naturally patchy, and the water quality benefits depend in part on the degree to which they interact with water bodies. The physiological rate functions of bivalves also vary with organismal health and seasonal changes in nutritional status, which are governed by the interplay between shifting nutritional demands and available food quantity and quality. On the other hand, water quality improvement via filtration is only one of many services provided by bivalves (Table 1). More research and analysis will be needed to improve our understanding of potential outcomes from non-oyster bivalve restoration investments. We list some recommendations for next steps at the end of this review.

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BIVALVE FILTRATION

Definitions Most of the water quality benefits from bivalves come directly or indirectly from how they feed, by filtering the water in which they live. Bivalves pump water across their enlarged gills which function both in gas exchange as well as feeding. The volume of water cleared of particles per unit time is referred to as the “clearance rate,” whereas the biomass of particles that is removed over unit time is referred to as the “filtration rate.” Filtration rate is more relevant to ecological impacts, but it is much harder to measure, so most bivalve “filtration” studies measure clearance rate.

The removal of suspended matter from the water column can improve water clarity. Nutrients are often associated with these suspended particles, either adsorbed to particle surfaces or within particles such as algae and bacteria. Some of those nutrients are then incorporated into the tissues of the bivalves, some are added to the sediments in biodeposits, and some are returned to the water column as dissolved byproducts. Thus, nutrients are not all removed from the aquatic ecosystem by bivalves over the long term, but they are removed from the water column in the short term, thus improving water quality. Furthermore, dissolved nutrients that are returned to the environment may be transformed by the animals into compounds that are more usable by other biota. Particulate matter in biodeposits may get buried or used by deposit-feeders or bacteria, including denitrifying bacteria. To assess and compare the ability of different bivalves to filter water, we reviewed studies that measured their “clearance rate,” which measures the volume of water cleared of particles by the bivalves per unit of time.

Measuring comparable clearance rates There are numerous methods for measuring bivalve clearance rates at the individual and population level, which are not reviewed here. For inter-comparability among studies and taxa, it is important to normalize measured rates to body size. For example, there are at least four different ways that clearance rates are reported in the literature: rates per individual and weight-specific rates using three different measures of body (or tissue) weight. The three different measures of tissue weight are: (1) dry tissue weight (dtw), (2) ash-free dry tissue weight (afdw), and (3) grams of tissue carbon (g C). Dry tissue weights (dtw) are determined by dissecting tissues from the shell and drying them to constant weight at 60 oC. Tissue weight is used since the shells vary widely in weight among species and they are generally inconsequential for routine maintenance metabolism. Ash-free dry tissue weights (afdw) require an added step of combusting the organic matter in the dried and weighed tissues for >4 hours at 450-500 oC and weighing what is left as the ash weight, and subtracting this from dtw to get ash-free dry weight, which is for organic matter only. The purpose of assessing afdw instead of just dtw is to ensure that inorganic elements do not complicate measurement of energy budgets or bias measurement of rate functions, which are best normalized to actual organic tissue mass. Typically, in healthy animals the values for dtw and afdw are within 15% of each other. Since the carbon content (g C) is generally about 50% of tissue organic weight (or afdw), rates reported per gram carbon will generally be twice the rates reported per gram of ash-free dry tissue and more than twice the rates reported per gram of dry tissue.

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Either dry tissue weight or ash-free dry tissue weight is preferred for interspecific standardization of clearance rates, whereas carbon units are more useful for constructing energy and carbon budgets.

Measuring bivalve density and biomass Clearance rates are typically determined at the organismal level, but for assessing ecosystem services these rates need to be related to the in situ population density and population biomass to calculate a population-wide clearance or filtration rate for a geographic area. Some survey techniques are tailored for hard bottoms, some for soft bottoms, and some can be used on both – from oyster dredge to ponar grab to benthic sled. Survey techniques also can be very different between marine and freshwater systems. The physical apparatus or method used to collect bivalves depends on the question, and a detailed analysis of the pros and cons of each survey method is beyond the scope of this paper. Regardless of how bivalves are collected, quantitative, statistically robust sampling methods are preferred to capture diversity, abundance, biomass and demographics within the community. Quantitative population data are essential for estimating overall ecological function and ecosystem services.

In freshwater (non-tidal) systems, biologists generally use SCUBA or snorkeling techniques to hand collect freshwater mussels buried in bottom sediments. In large freshwater rivers, brailing - as was used in the 1890s by the pearl-button industry - is often used. However, an oyster dredge can also be helpful for exploratory surveying of large rivers with soft bottoms. Strayer and Smith (2003) published a guide to sampling freshwater mussels that included both survey techniques and sampling methodology for estimating diversity within the community and estimating abundance at the species level and community level. Smith (2006) also recommended a unique sampling design for detecting rare species; and Dryer et al (2012) recently provided useful designs for sampling communities with “hot spots” of information (i.e. cluster sampling).

In marine systems, bivalve sampling is generally done with an oyster dredge, oyster tongs (either hand tongs or power-assisted patent tongs), or a ponar grab on soft bottom. For example, the Chesapeake Bay Benthic Survey (Versar 2011) uses a ponar grab on soft bottom. Fishery- independent oyster sampling in Chesapeake Bay is done with two methods: an oyster dredge in Maryland, supplemented by patent tongs at some sites, and patent tongs in Virginia (VIMS 2015). The Chesapeake Bay Program (NOAA 2009, 2012) provides a thorough assessment of oyster restoration in the Chesapeake Bay along with evaluation of restoration techniques and sampling methods and sampling designs.

Tidal1 Bivalve Filtration Chesapeake Bay is a textbook example of the decline of an estuary from human impacts that resulted in eutrophication. Eutrophication results when excess inputs of nutrients lead to phytoplankton blooms,

1 For the purposes of this section, bivalve filtration literature is reviewed separately for tidal and non-tidal species, which generally correspond to saltwater and freshwater species, respectively. However, it should be noted that some species are uniquely adapted to tidal freshwater or brackish areas.

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 16 which in turn have two harmful impacts: (1) they cloud the water and contribute to a decline in submerged macrophytes such as wild celery and eelgrass, and (2) they cause low dissolved oxygen after they die and decompose, especially in deeper water in the summer, which in turn can kill fish, shellfish and other aquatic life. In addition, increased sediment runoff resulting from human actions such as urbanization and some agriculture practices also clouds the water.

The traditional management method to reverse these impacts is “bottom-up” control, which is contrasted to “top-down” control observed in food webs (Dyer and Letourneau 2003). Bottom-up control involves reducing nutrient and sediment inputs by a variety of methods, such as upgrades to wastewater treatment plants, reducing the use of manure and other fertilizers, sediment runoff controls such as silt fences, and planting cover crops. However, the success of this method at reversing eutrophication has been limited, so the possibility of enhancing top-down control by using filter feeding organisms to control phytoplankton and excess sediment in estuaries has been explored for a number of years. Its feasibility was suggested by Kuenzler (1961) in a study of Atlantic ribbed mussels (Geukensia demissa) in a Georgia salt marsh. It was identified by Jordan and Valiela (1982) and Cloern (1982) as an important factor in controlling eutrophication in two different estuaries, and elaborated with clearance time calculations for Chesapeake Bay by Newell (1988) for C. virginica, and Gerritsen et al. (1994) for other bivalves.

Kuenzler (1961) studied phosphorus budgets of Atlantic ribbed mussels (now called Geukensia demissa) in a Georgia salt marsh. He measured their clearance rates to estimate their phosphorus intake, and about 99% of that was taken up in particulate form. Kuenzler stressed the mussels’ role in biogeochemical cycling, in contrast to the energy flow theories of HT Odum (Odum and Odum 1953) that dominated ecology at the time: The major effect of the population on the ecosystem was the removal of particulate matter from sea water; the turnover time of the particulate phosphorus in the water was 2.6 days under the supposition that the mussel population was the only agent involved. Mussels are more important as biogeochemical agents than as energy consumers. (Kuenzler 1961)

Jordan and Valiela (1982) similarly examined the importance of G. demissa for biogeochemical cycling of nitrogen in a New England salt marsh. G. demissa were shown to be sufficiently abundant to collectively filter, perhaps more than once, the entire volume of water overlying the marsh per tidal cycle (Jordan and Valiela 1982). Since much of the material removed from suspension gets deposited as feces and pseudofeces, mussels were described as important agents for the retention of nitrogen within the marsh.

Since G. demissa is considered a functional dominant animal of the eastern U.S. salt marsh, the system- level importance of ribbed mussels hinges on the abundance of healthy marsh acreage. For example, in the Delaware Estuary which is has more than 140,000 acres of coastal marsh, the combined water clearance by G. demissa has been estimated at 60 billion liters per hour compared with 10 billion liters per hour by C. virginica (Kreeger and Bushek 2008). But the Delaware Estuary is losing about an acre per day of salt marsh due to erosion (PDE 2012), thus representing an estimated loss of daily biofiltration

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 17 capacity of more than 400,000 liters per hour due to declining G. demissa habitat. This scenario demonstrates the importance of conservation to stem continued losses of filtration services, along with discussions of potential bivalve restoration.

Cloern (1982) was trying to understand how South San Francisco Bay could have both (1) high nutrient inputs and phytoplankton growth rates and (2) very low chlorophyll concentrations for an estuary with high nutrient inputs; usually less than 5 µg l-1 in summer. After concluding that local zooplankton biomass could not consume enough phytoplankton to keep chlorophyll that low, he suggested that three suspension feeding bivalve species were providing the “missing” filtration capacity. He calculated that the known biomass of those bivalves could filter all of the water in South Bay roughly once or twice a day.

Officer et al. (1982) further explored phytoplankton control by filter feeders in estuaries, trying to identify the conditions under which control was the most likely. After re-examining the processes in South San Francisco Bay, they discussed two North Carolina estuaries in which this control may be occurring. The factor that they identified as making phytoplankton control more likely include shallow water in partially enclosed regions with poor hydrodynamic exchange. They did not discuss how this control might be exerted in Chesapeake Bay, although parts of that estuary fit that description (Cerco and Noel 2007).

Newell (1988) extended this concept of top-down control by bivalves to Chesapeake Bay, which has the symptoms of eutrophication that seemed to be missing in South San Francisco Bay. He proposed that the standing stocks of C. virginica were once high enough to do what other bivalves were doing now in South San Francisco Bay: controlling phytoplankton populations by filter feeding. He calculated that historic oyster populations could “potentially” filter a volume of water equivalent to the entire water column in Chesapeake Bay in the summer in 3-6 days. He also calculated that at their depleted 1988 population levels, C. virginica would take almost a year to filter the same amount of water. Both water clearance times (3 days then, 1 year now) are now cited broadly to explain why the health of the Bay has declined.

Newell (1988) did not explore the possibility that other filter feeders in the watershed may have partly assumed the role once filled by C. virginica, other than to mention that two non-native clams had recently become much more abundant. However, both of these species, the brackish water clam (Rangia cuneata) and the Asian clam (Corbicula sp.) have much lower salinity tolerances than C. virginica, so their ranges, especially for the Corbicula sp., have little or no overlap with that of C. virginica.

Gerritsen et al. (1994) built on Newell’s (1988) study by using a model to calculate what proportion of 1987-1989 phytoplankton production in Chesapeake Bay was potentially consumed by populations of benthic filter feeders in those years, including C. virginica and a number of other species. One interesting question the authors asked was, if we could increase oyster populations to near historic levels, how much food would be available for them? Their model output also led to some surprising recommendations:

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Model results indicated that existing suspension-feeding bivalves could consume more than 50% of annual primary production in shallow freshwater and oligohaline reaches of the upper Chesapeake Bay and Potomac River. In deep mesohaline portions of the Chesapeake Bay and Potomac River, suspension-feeding bivalves could consume only 10% of primary production. . . . Our results suggest that the proposed use of suspension-feeding bivalves to improve water quality of large estuaries will be limited by the depth and width of the estuary, unless the bivalves are suspended in the water column by artificial means. (Gerritsen et al. 1994)

Cerco and Noel (2007) came to a similar conclusion about the need to have filter feeders in or near most of the water column to improve water quality, based on a modeling study. Their predicted effects of C. virginica on water quality in deeper water were minimal. Cerco and Noel (2010) extended their modeling of Chesapeake Bay filter feeders to include two of the dominant bivalves in tidal fresh and oligohaline reaches (salinity 0-5), Corbicula sp. and R. cuneata, both non-native in Chesapeake Bay. They concluded that:

. . . bivalves may reduce phytoplankton concentrations in oligohaline and tidal fresh waters throughout the system but the most significant effects were noted in the Potomac and Patuxent tributaries. Bivalve impacts were related to hydraulic residence time. (Cerco and Noel 2010)

The upper mainstem Bay had the highest R. cuneata biomass, but the upper Potomac had a higher combined bivalve biomass when R. cuneata biomass was added. Since the upper mainstem Bay had a much lower residence time than the upper Patuxent, due to higher flow from the Susquehanna River, the Potomac and Patuxent rivers had the largest predicted impacts on water quality by filter feeders (Cerco and Noel 2010).

Other studies have shown how introduced non-native bivalves can increase water clarity and/or reduce phytoplankton by increasing filtration. For example, effects on San Francisco Bay by introduced clams (Officer et al. 1982, Alpine and Cloern 1992, Thompson 2005), on the Great Lakes and the Hudson River by the introduced zebra mussel, Dreissena polymorpha (Fahnenstiel et al. 1995, Klerks et al. 1996, Baker and Levinton, 1999; Budd et al. 2001, Caraco et al. 2006), and on the Potomac River by Corbicula sp. (Cohen et al. 1984, Phelps 1994). While improved water clarity sometimes led to increases in submerged aquatic vegetation in the same water bodies, which is generally considered a positive change, negative impacts of introduced zebra mussels also have been well documented (Fahnenstiel et al. 1995).

One study documented the effects of the opposite change, from more to less filtration, namely the removal of oysters from a eutrophic coastal lagoon in Taiwan (Huang et al. 2008). The lagoon once had very dense oyster aquaculture in racks, but the racks had to be removed when it was designated as a “National Scenic Area,” so the study was done to document the effects of removal. The lagoon has inner (poorly flushed) and outer (well flushed) regions. After oyster removal, mean light attenuation increased over 50% and mean Chl a concentrations and phytoplankton production rate increased 4-fold in the inner region, but all three parameters remained unchanged in the outer region and at the control site. There were also changes in the fish community. After rack removal, lagoon reef fish declined by 23%

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(probably due to reduced physical structure) and pelagic or planktivorous fish increased by 268%, suggesting that a reverse shift (compared to what usually happens when oysters are added to a lagoon) from periphyton-grazing to phytoplankton-grazing organisms likely occurred in the lagoon after rack removal (Huang et al. 2008).

One example is known of an irruption of a small native mussel that led to dramatic (but short-lived) improvements in water quality. An irruption of dark false mussels (Mytilopsis leucophaeata) occurred in low mesohaline tidal regions of Chesapeake Bay in 2003-2005. For details see the section on this species below. Several of these papers mention “resistance to eutrophication” and how it can vary among estuaries (Cloern 1982, Carpenter et al. 1985, Cloern 2001, and Caraco et al. 2006). This resistance can be physical, for example when short residence time in flowing waters makes it hard for nutrients to stimulate algae blooms (Caraco et al. 2006), or it can be biological, which can be either the presence of abundant bivalves (as Cloern 1982 suggested for South San Francisco Bay) or abundant zooplankton (as Carpenter et al. 1985 suggested for lakes as a result of a trophic cascade). Cloern (2001) asked “Why are some coastal ecosystems highly sensitive to inputs of additional nutrients while others appear to be more resistant (at least to the primary responses)?” and then described four main “filters” (which might be more accurately called buffers or mitigating factors) to which he attributed this resistance, by determining how the ecosystem responds to stressors. The four filters from Cloern (2001) are:

1. Tidal magnitude: macrotidal estuaries such as San Francisco Bay appear to be more resistant to eutrophication than microtidal estuaries such as Chesapeake Bay. 2. Residence time, discussed above: shorter residence times seem to confer more resistance, since the excess nutrients are mostly exported quickly. 3. Inherent optical properties of water that control the light available to submerged plants, including phytoplankton and rooted plants (submerged aquatic vegetation): High suspended sediment concentrations, usually associated with poor water quality, can confer resistance to phytoplankton blooms by shading the plants; this explains some of the resistance of San Francisco Bay compared to Chesapeake Bay. The Delaware Estuary neighboring Chesapeake Bay is also an example of a system that is regarded as largely light shaded by high natural turbidity, perhaps explaining the general lack of harmful phytoplankton blooms there despite some of the highest nutrient loadings in the nation (EPA 2006). Color in the water (such as that from tannins in blackwater estuaries, such as the Nanticoke and Pocomoke rivers in Maryland) can have a similar shading effect (Bortone 2004). 4. Suspension feeders as a biological component of the filter: The dominant taxa tend to be zooplankton in lakes (as discussed below) and benthic suspension feeders (including bivalves) in estuaries.

Three of these four filters (or buffers) were considered in a recent review of the ecological role of bivalve aquaculture in US West coast estuaries (Dumbauld et al. 2009). The only filter not considered was the inherent optical properties of water. Residence time, along with phytoplankton population growth rates, were seen as key factors in determining the extent to which bivalves produced measurable effects on water quality (Dumbauld et al. 2009). More site-specific factors may also be important; for example, a mismatch in the timing of phytoplankton blooms and annual peak clearance

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 20 rates by bivalves can limit the responses of water quality to bivalve biomass. This was seen in South San Francisco Bay after an introduced clam arrived there, even though the same species had improved water quality in North San Francisco Bay (Thompson 2005).

A recent mesocosm study by Wall et al. (2011) examined how bivalve filtration (by adult C. virginica, bay scallops Argopecten irradians and hard clams Mecenaria mercenaria) could offset the effects of eutrophication, and how that affected the growth of eelgrass (Zostera marina) as well as the growth of juvenile bivalves of those species and one juvenile fish (sheepshead minnow, Cyprinodon variegatus). The authors found that while bivalve filtration had a positive effect on eelgrass (in 1 of 3 experiments), by increasing light penetration, it also had a negative effect on the juveniles of those same bivalve species, as well as the juvenile fish tested (in 2 of 3 experiments). Increased nutrient loading, normally viewed as harmful to estuaries, led to increased growth rates of juvenile bivalves compared to control mesocosms with lower loading rates in 2 of 3 experiments, presumably by increasing the food supply (Wall et al. 2011).

Non-tidal Bivalve Filtration Eutrophication occurs in non-tidal rivers, streams, lakes and ponds as well as in estuaries, and the ability of filter feeders (including freshwater bivalves) to ameliorate its negative effects is beginning to be explored. One reason fewer studies have been undertaken with freshwater bivalves is that they are not as commercially important as tidal bivalves, which have been the focus of intense study by marine biologists and commercial growers for more than 100 years. Ecological studies of non-tidal systems have been dominated by stream ecologists studying macroinvertebrates (not usually including bivalves) or lake ecologists studying zooplankton. Many of these lake studies were based on the trophic cascade theory of Carpenter et al. (1985). The ecological effects of the trophic cascade theory are similar to those of increased filtration by bivalves, but achieved a different way by enhancing filtration by zooplankton.

There are about 300 native species of freshwater bivalves in North America. Over 70% of these species are in decline nationwide and considered the most imperiled animals on the continent (Williams et al. 1993). Most of the scientific interest and restoration effort to date has been driven by biodiversity conservation interests. There has also been a large effort to study the effects of invasive freshwater species (e.g. zebra mussels, D. rostriformis bugensis, Corbicula sp.) on ecosystem dynamics. Only in the past 10 to 15 years has attention begun to focus on the environmental implications of widespread declines in population biomass of native freshwater mussels, regardless of whether species are imperiled or stable.

Although not as well researched as invasive and tidal species, an emerging literature suggests that native freshwater mussels furnish many of the same filtration benefits and other ecosystem services in freshwater tributaries as their marine counterparts (Atkinson et al. 2013, Atkinson and Vaughn 2015). For example, freshwater mussels are abundant enough in parts of the Delaware River basin to improve water clarity by their filtration. Kreeger (2005b) measured the abundance of E. complanata (eastern elliptio) in the Brandywine River and combined these data with survey information for the mainstem Delaware River by Dr. W. Lellis (USGS Wellsboro), yielding an estimate of 4 billion adult mussels of this

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 21 species across the basin. Based on these numbers and clearance rates for Brandywine mussels (3.4 l.h.g- 1dtw, Table 3) during summer, Kreeger and Gatenby (2008) estimated that E. complanata currently filter more than 9.7 billion liters of water per hour across the basin, which is comparable to the potential volume processed by C. virginica still living in Delaware Bay. A more recent study surveyed the abundance of six species of freshwater mussels in four beds within the tidal freshwater zone of the Delaware River and estimated their combined water clearance to exceed 25 million liters per day for a combined area of just under 4 hectares (Kreeger et al. 2013), therefore showing that tidal freshwater areas of estuaries can be important habitats for freshwater mussels and associated filtration services (Kreeger et al. 2013).

These estuary-wide estimates of mussel filtration capacity are especially notable since the current status of freshwater mussels in the Delaware River basin is greatly reduced relative to historic conditions (PDE 2008, 2012), suggesting that the carrying capacity exists to boost water processing by restoring mussel assemblages. Filtration potential estimates require robust information of the relative abundance of freshwater mussels, and to our knowledge such data are not widely available for most of the Chesapeake watershed; however, there is a large body of anecdotal evidence to suggest that mussel populations in the Chesapeake are also well below their habitats’ historic carrying capacity, similar to the situation in the Delaware Estuary watershed. Thus, the potential to boost water processing by restoring freshwater mussel assemblages in the Chesapeake watershed also exists.

One of the primary causes for the decline of native freshwater mussels has been impediments to fish passage in lotic systems since fish serve as hosts for freshwater mussel larvae (Neves 1993). The eastern elliptio is one of the most common freshwater mussels in the Chesapeake watershed (Ashton 2010). However, it is much more abundant in the Delaware River than the Susquehanna River, probably because the Susquehanna has been blocked to the passage of the only known host of its larvae, the American eel (Anguilla rostrata) since Conowingo Dam was built in 1928. Indeed, most of the eastern elliptios in the Susquehanna River are large and may have been there since before or shortly after 1928- -this species can live for 100 years or more (Bogan and Proch 1997). Successful reproduction and dispersal of mussels depends on species-specific relationships with fish. Thus, restoring eel passage to the Susquehanna may also restore eastern elliptios to the river. Indeed, the Pennsylvania Fish and Boat Commission had an extensive eel stocking program into the 1980s. Anecdotally, many of the streams that received eels support the “best” or “youngest” Elliptio populations.

As discussed for tidal bivalve species above, a narrow focus on filtration capacity and its water quality benefits from freshwater bivalves is greatly oversimplified. The actual net effects of mussel beds on water quality depend on complex hydrodynamic, biogeochemical, and ecological interactions, and more studies are needed. For example, water passing over mussel beds can become depleted in small particles and enriched in large particles (Kreeger 2011), and much of the filtered material can end up in biodeposits in the sediment which can be more than 50% enriched in nutrients and organic content compared to control areas without mussels (Kreeger, unpublished). Indeed, freshwater mussels provide many ecological functions in addition to filtering suspended particles from the water column (Vaughn et al. 2008; e.g., see Table 1). Interactions among different mussel species living in the same area may also

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 22 affect processing and ecological fate of suspended material (Spooner and Vaughn 2006, Vaughn et al. 2008).

Invasive and introduced bivalves in non-tidal Chesapeake tributaries include Asian clams (Corbicula sp.) and zebra mussels (Dreissena polymorpha). These non-native species can furnish some ecosystem services such as increased visibility and improved water quality through removal of nutrients from open water, diverting nutrients to bottom sediments. These services, however, disrupt natural ecological relationships and can be inherently unstable. Additionally, these invasive bivalves create biofouling problems which can be very costly for water treatment facilities, users of water intake pipes, and the boating industry. See species inventory for more detail on these species.

SPECIES INVENTORY OF CLEARANCE RATES: FILTER FEEDERS THAT COULD IMPROVE WATER QUALITY AND PROVIDE OTHER SERVICES IN CHESAPEAKE BAY AND TRIBUTARIES

Table 2 summarizes what is known about habitat preference, salinity and clearance rates of native and introduced bivalves in the Chesapeake Bay drainage that have improved or could improve water quality (via filtration), as well as provide other services. Both tidal and non-tidal species are included. Information on clearance rates of freshwater mussels that occur in the Chesapeake Bay drainage is scarce, with published clearance rate data for just two species (E. complanata and U. imbecilis). Clearance rates for species of freshwater mussels found in Europe or in the Mississippi drainage, however, are more prevalent. Table 3, therefore, provides information on known clearance rates of freshwater mussels which could be useful in assessing the potential benefits of restoring freshwater mussels in the Chesapeake Bay drainage.

Note that there are two columns for salinity ranges for in Table 2: the first of these are literature values and the second are ranges of measured salinity where that species was found in Chesapeake Bay. No salinity ranges were included for freshwater species. The measured ranges are from the Maryland fall oyster survey (Tarnowski 2010) for two hard bottom species, C. virginica and I. recurvum, using means of 2005-2009 data (N=1484-1791). Since salinity tends to be highest in the fall in Chesapeake Bay, these values are probably higher than annual average values would be for the same locations. The other ranges listed are from the Chesapeake Bay Benthic Survey database (Versar 2011) using means for 1994- 2004 (N=18-1023), for most of the other species, which tend to be found on soft bottom and rarely on oyster bars.

A limitation on data comparability is that some studies report clearance rates per animal (l h-1) and others report weight-specific clearance rates (often as l h-1 g-1 dtw). Bivalves vary widely in size and clearance rates are size-dependent, therefore, comparisons among species or populations are best made using dry tissue adjusted data (no shell). Here, we applied a simple weight adjustment for species where rates were reported per individual, or where only an allometric equation was provided.

Where rates were reported per individual, we converted this to a rate per gram by dividing that rate by a value for dtw or afdw for that species which was determined in one of two ways:

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1. Weight of a clam or mussel of the same length as the ones used to make the water clearance measurements -- used for D. polymorpha (Reeders and Bij de Vaate 1990) and M. leucophaeata, or 2. Mean weight of all the individuals of that species collected by the Chesapeake Bay Benthic Survey (Versar 2011) or similar survey -- used for Corbicula sp. (Kramer and Hübner 2000), M. balthica (Absil et al. 1996), and G. demissa (Kreeger and Newell 2001 using Delaware Bay weights). We did not have the data needed to make this adjustment allometrically, as described by Newell and Koch (2004).

Where only an allometric equation was given, with the clearance rate depending on dry tissue weight, we assumed that weight was 1 g, so the resulting rate was the coefficient. This was done for soft-shell clam (Riisgard and Seerup 2004, F = 4.76 W0.71), and three bivalves with rates reported by Riisgard (1988): C. virginica (F = 6.79 W0.73), G. demissa (F = 6.15 W0.83), and M. mercenaria (F = 1.24 W0.80).

We did not include published clearance rates for two species from one study (Corbicula sp. and R. cuneata, from Cerco and Noel 2010) because they were not species-specific, but were derived from the generic bivalve equation in Gerritsen et al. (1994). We did include the maximum clearance rate for C. virginica from Cerco and Noel 2007, since it was based on C. virginica data, converted from their form (0.55 m3 g-1 oyster C d-1) by converting to liters and hours, and dividing the rate by 2 since they assumed that 1 g dry weight was 0.5 g C, yielding the rate in Table 2, 11.5 l h-1 g-1 dtw. In future studies, we recommend that physiological processing rates be standardized to a typical standard-sized animal for a given species using allometric relationships and yielding clearance or filtration rates per gram of dry tissue mass (e.g., Kreeger 2011, Kreeger et al., 2013). It will be important to consider relative body size of adults for different species due to typical allometric scaling. Smaller (and younger) bivalves have greater weight-specific rates of filtration (and metabolism), and so an adult freshwater mussel or clam of approximately 1-2 cm should have a higher filtration rate per gram of body weight than an adult mussel or oyster of approximately 6-10 cm, whereas the absolute rate per animal would be lower in the smaller clam. Generally, the preferred standard-sized animal is the mean of a representative population. Not only do weight-adjusted rate data facilitate comparisons, they are also essential for enabling modelers to combine the rate data with population-level biomass and demographic size estimates (as g C or g dry tissue per unit size class and area of bottom) to calculate population-level filtration rates. Therefore, in quantitative surveys of natural populations for assessing bulk filtration services (or other ecosystem services), it is important to measure the overall biomass of tissues and size class demographics rather than just the numerical abundance of bivalves.

To better understand the ecology of natural systems, it also is important that future studies of bivalve physiological rate functions attempt to mimic natural conditions, especially food quantity and quality. Natural diets are filtered and processed differently than ideal diets of lab-cultured algae, which most published studies have used (Table 2). For example, Kreeger (1993) found that lab algae diets were cleared from suspension (and digested) better by tidal mussels than natural seston. Clearance rates (and digestion efficiencies) by freshwater mussels fed lab algae were similarly higher than those fed on seston in natural river water (Gatenby et al. 2002, Gatenby et al. 2003,). Natural seston typically includes particles of diverse sizes and qualities whereas nutritious lab diets have ideal sizes and composition.

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Table 2. Reported habitat preference, salinity and clearance rate for native and introduced bivalves found in Chesapeake Bay and its non-tidal tributaries that have the potential to improve water quality. See text above for details on measured salinity ranges.

Salinity, Clearance rates (l h-1 g−1 of dtw, n Max Salinity , measured Native unless listed as afdw) Species length Bottom type Issues literature to Bay? (cm) Lab Diets Natural Diets

Asian clam Corbicula Not Not 5 t Soft: silt, sand, No 2.9 afdw (x) Invasive in US sp. included included pebbles

Zebra mussel Dreissena Not Not 2.4 w Hard: pebble, No 8.3 (gg) 16.2 afdw (c), Invasive in US polymorpha included included cobble 2.70 afdw (bb), 1.43 afdw (w), 1.9 13.98 afdw (z)

Eastern elliptio, Elliptio Not Not 12 t Both: silt, Yes 0.337 (dd), 3.4 (l) Larval hosts (fish) may be limiting in complanata (See Table included included sand, pebble, 0.048 (ee) some areas 3 for details) cobble

Utterbackia imbecilis Not Not Both: silt, Yes 0.036 (ff) (See Table 3 for details) included included sand, pebble, cobble

Other freshwater Not Not Both: silt, Yes 0.0012-2.75 (see Harrison Lake National Fish mussels not native to included included sand, pebble, Table 3) Hatchery has capability to rear Ches Bay (See Table 3 cobble freshwater mussels for details)

Brackish water clam 0.5-10 s 0.4-11.5 5 s Soft No 2.06 (d) Probably from Gulf of Mexico; some Rangia cuneata think it is native

Dark false mussel 0-10 t, 0- 2.9-13.6 2.2 e Hard Yes 1.66 (bb), 1.94 Boom-bust cycles, rarely common Mytilopsis (e), 2.37 (cc) where native 26 u leucophaeata

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Salinity, Clearance rates (l h-1 g−1 of dtw, n Max Salinity , measured Native unless listed as afdw) Species length Bottom type Issues literature to Bay? (cm) Lab Diets Natural Diets

Baltic macoma clam 5-30 s 6.8-18.4 3.8 t Soft Yes 0.45-1.33 afdw 0.4 afdw (v) Some deposit feeding also Macoma balthica (o)

Soft-shell clam Mya 5-30 s 9.5-20.1 10 t Soft Yes Max 3.5 (f), Die-back started 1992 in arenaria 4.76 afdw (q) Chesapeake Bay

Hooked mussel 5-30 s 7.8-15.8 6i Hard Yes Max 4.3 – 4.6 Little research, no larvae raised in Ischadium recurvum (ff) hatcheries

Atlantic ribbed mussel 10-30 s 5.7-16.9 10 t Both Yes 6.8 (g), 6.2 [r] 5.1 (k) Trials in Bronx River on raft, 2012, Geukensia demissa and Del Bay

Stout razor clam 10-30 s 13.5-23.7 9 t Soft Yes No rates found Die-back in Chesapeake Bay started Tagelus plebeius in 1994

Eastern oyster 7-30 s 10.8-18.9 14 p Hard (shell) Yes 11.5 (h), 9.6 (j) 6.8 [r], 6.4 (y) Disease, shell supply, predation, Crassostrea virginica poaching

Hard clam Mercenaria 15-30 s 15.5-28.0 10 s Soft Yes 1.24 [r], 1.52 0.5 (y) High salinity only afdw (b)

a CBP benthic data survey base (Versar 2011) k Kreeger and Newell 2001, using 1.11 g dtw from Del. Bay t Lippson and Lippson 1984 b Echevarria et al. 2012 l Kreeger 2005a, Kreeger and Gatenby 2008 u Verween et al. 2010 c Fanslow et al. 1995 (mean rate) m Gatenby et al. 2002; Gatenby et al. 2003 v Hummel 1985 cited in Cugier et al. 2010 d w Wong et al. 2010 n Reeders and Bij de Vaate 1990, using calc afdw e x Rajagopal et al. 2005a, calc wt for 20 mm mussel from o Absil et al. 1996; mean afdw (0.0035 g) from (a) Kramer and Hübner 2000; mean afdw (0.047 g) from (a) (w) y p Tarnowski 2010 Newell and Koch 2004 f Bacon et al. 1998 z q Riisgard and Seerup 2004, assuming 1 g weight in Roditi et al 1996, calc wt from (w) g Kuenzler 1961 (mean rate) aa equation Walton 1996 h bb Cerco and Noel 2007 r Riisgard 1988, assuming 1 g weight in equation Rajagopal et al. 2003 I cc Lipcius and Burke 2006 s White 1989 Rajagopal et al. 2005b J Newell et al 2005 (Table 2, maximum monthly value)

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 27 dd Paterson 1984 ff Gedan, unpub. data, @ salinity 10 and 27 C gg Baker and Levinton (2003), report 125 ml h-1 15mg-1 dtw ee Leff et al. 1990, from graph @ 25 C ff Silverman et al. (1995 and 1997)

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Table 3. Comparison of clearance rates (CR) from unionid freshwater mussels. Species Food Source Ration CR (l h-1) CR (l h-1 Mussel Size Citation g−1 dtw) (g dtw or cm)

Anodonta Chlorella vulgaris 1.2 x 104 c ml-1 2.6-2.9 0.827- 3.141g 1 anatina 0.923

Unio crassus Chlorella vulgaris 1.2 x 104 c ml-1 3.3-4.1 1.233- 2.676 g 1 1.532

Unio pictorum Chlorella vulgaris 1.2 x 104 c ml-1 3.2-4.6 1.060- 3.017 g 1 1.525

Unio tumidus Chlorella vulgaris 1.2 x 104 c ml-1 2.1-2.4 0.875 2.424 g 1

Anodonta seston 8-19 mg l-1 0.59 - 0.170- 3.5 g 2 anatina 2.17 0.620

Unio tumidus seston 8-19 mg l-1 0.38- 0.150- 2.5 g 2 1.45 0.581

Villosa iris N. oleoabundans 5.0 x 104 c ml-1 0.053 0.181 0.29 g 3

Villosa iris N. oleoabundans 1.5 x 105 c ml-1 0.042 0.143 0.29 g 3

Villosa iris N. oleoabundans 5.0 x 105 c ml-1 0.016 0.056 0.29 g, 5 cm 3

Utterbackia bacteria (E. coli) 1-2 x 107 c ml-1 0.043 0.036 1.203 g 4 imbecilis

Toxolasma bacteria 1-2 x 107 c ml-1 0.017 0.038 0.454 g 4 texasensis

Ligumia bacteria 1-2 x 107 c ml-1 0.122 0.061 0.1.997 g 4 subrostrata

Cyclonaias bacteria 1-2 x 107 c ml-1 0.771 1.15 0.67 g 4 tuberculata

Fusconaia bacteria 1-2 x 107 c ml-1 0.358 0.299 1.195 g 4 flava

Lampsilis bacteria 1-2 x 107 c ml-1 0.418 0.354 1.18 g 4 ovata Elliptio bacteria 1-2 x 107c ml-1 0.496 0.4596 1.08 g 4 dilatata

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 29

Species Food Source Ration CR (l h-1) CR (l h-1 Mussel Size Citation g−1 dtw) (g dtw or cm)

Villosa lienosa bacteria 1-2 x 107c ml-1 0.360 0.394 0.913 g 4

Ptychobranch bacteria 1-2 x 107c ml-1 0.904 0.484 1.870 g 4 us fasciolaris

Elliptio 2-5 µm beads, 1 x 103c ml-1 nd 0.337 6-7 cm 5+ complanata lake water

Elliptio 2 µm beads, 45 No data 0.0109 0.048 4.4 g 6# complanata µm filtered stream water Lampsilis Chlamydomonas 2.5 mm3 l-1 1.5 1.450 1.5-2.1 g 7 siliquoidea sp.

Actinonaias seston 7.02 mg l-1, 1.53 0.288 5.31 g 8 ligamentina 1.2 x 104c ml-1

Elliptio seston 7.02 mg l-1, 1 1.12 0.580 1.93 g 8 dilatata .2 x 104c ml-1

Lasmigona seston 7.02 mg l-1, 1.10 0.375 2.93 g 8 costata 1.2 x 104c ml-1

Elliptio seston 2 x 104c ml-1 2.6 nd 7.5-9.5 cm 8 complanata

Elliptio algae 2 x 103c ml-1 3.1 nd 7.5-9.5 cm 8 complanata

Elliptio algae <2 x 103c ml-1 1.9 nd 7.5-9.5 cm 8 complanata

Elliptio seston ca. 2.4 mg l-1 3.4 7.5-9.5 cm 9 complanata

Margaratifera seston 0.8-7.4 mg l-1 0.5 0.45* 1.06 g (0.32-2.99g, 10 falcata 0.52 s 3.7-9.3 cm) Gonidea sp. seston 0.8-7.4 mg l-1 0.5 0.31* 1.13 g (0.4-2.5 g; 10 0.40s, 4.3-8.2 cm) Anodonta seston 0.8-7.4 mg l-1 0.8 0.9* 0.58 g (0.19- 1.9g, 10 californianus 1.1 s 3.4-8.6 cm)

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Species Food Source Ration CR (l h-1) CR (l h-1 Mussel Size Citation g−1 dtw) (g dtw or cm)

Actinonaias green and 89.7 mg C l-1 nd 0.0032 24.5±0.92 cm 11# ligamentina diatom algae

Lampsilis green and 89.7 mg C l-1 nd 0.0047 14.0±0.84 cm 11# cardium diatom algae

Truncilla green and 89.7 mg C l-1 nd 0.0076 4.3±0.19 cm 11# truncata diatom algae

Quadrula green and 89.7 mg C l-1 nd 0.0050 5.7±0.39 cm 11# pustulosa diatom algae

Amblema green and 89.7 mg C l-1 nd 0.0014 20.3±0.99 cm 11# plicata diatom algal

Fusconaia green and 89.7 mg C l-1 nd 0.0035 7.6±0.44 cm 11# flava diatom algae

Megalonaias green and 89.7 mg C l-1 nd 0.0012 40.6±3.1 cm 11# nervosa diatom algal

Obliquaria green and 89.7 mg C l-1 nd 0.0040 4.5±0.25 cm 11# reflexa diatom algae Amblema Typhus (cattail 1.0 x 105 c ml-1 1.0 0.500 1.0 g dtw (198- 12* plicata detritus) 364 g wet+shell)

Pyganadon Microcystis 1.0 x 105 c ml-1 1.5 0.75 2.0 g dtw 12** grandis (bluegreen) Margaritifera Crucigenia 1.0 x 105 c ml-1 5.5 2.75 2.0 g dtw 12** margaratifera tetrapedia. (green alga)

Italicized clearance rate data are estimated from reported data in order to tabulate data both l h-1and l h-1 g-1 dtw for this comparison of CR by taxa by study. c ml-1 = cells of algae per milliliter mg C l-1 = milligrams of carbon per liter, in the algae used seston = naturally occurring suspended material, including algae; ration may be reported as milligrams per liter, cells of algae per milliliter, or both nd = no data ca = approximately + = Paterson (1984) reported length (cm) but did not report actual dry tissue weight; thus we did not calculate CR in l h-1. Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 31

* = Annual clearance rates from pooled seasonal clearance rate data; s = summer clearance rate. # = Clearance rates of mussels acclimated to 25oC were reported in bar graphs (as l h-1 g-1 dtw). We approximated CR values based on unit scales in the graphs. We did not estimate clearance rate as l h- 1 from the data reported. ** = Clearance rates of mussels were reported in bar graphs as l h-1 standard animal -1 (2 g dtw). We approximated CR for 1 g dtw, from the data reported. Citations: 1. Kryger and Riisgard (1988) 2. Pusch et al. (2001) 3. Gatenby (2000) 4. Silverman et al. (1995 and 1997) 5. Paterson (1984) 6. Leff et al. (1990) 7. Vanderploeg et al. (1995) 8. Gatenby et al. (2002, 2003) 9. Kreeger (2005a), Kreeger and Gatenby (2008) 10. Kreeger (2011) 11. Spooner and Vaughn (2008) 12. Baker and Levinton (2003)

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Non-tidal (freshwater) bivalves

Asian clam (Corbicula sp.) Corbicula sp. first became abundant in the Potomac River in 1980 and has since spread to many tidal and non-tidal tributaries (MBSS 2011, Versar 2011). The mean clearance rate for Corbicula fed an artificial diet was 2.9 l h-1 g-1 afdw (Table 2, Kramer and Huebner 2000). See Appendix B for a box plot of Corbicula sp. density by year and a line graph of percent occurrence by year from benthic survey data (Versar 2011). The percent occurrence was very low except in 2004-2006 when it rose to near 10%. In the neighboring Delaware Estuary, Asian clams (and other less numerous bivalves) comprised >75% of the benthic biomass between Trenton NJ and the Chesapeake and Delaware Canal in DE in a survey during 1992 and 1993 (Environmental Consulting Services, 1993). Some authors (Cohen et al. 1984, Phelps 1994) give Corbicula credit for facilitating the resurgence of SAV in the Potomac River in the mid‐ 1980’s by increasing water clarity. It is an invasive non-native species, however, and would not be used in most restoration.

Zebra and quagga mussel (Dreissena polymorpha and D. rostriformis bugensis) Zebra mussels are gradually spreading down the Susquehanna from New York, with a few individuals found in Maryland above Conowingo Dam in 2008 and below the dam in 2010 (Chesapeake Bay Journal 2010). In 2011, one zebra mussel was found in the tidal Sassafras River (Chesapeake Bay Journal 2011). Most recently, 20 individuals were found attached to the anchors of three navigational buoys located on the Susquehanna Flats in 2012 (Wheeler 2012).

Zebra mussels have had profound effects on the Great Lakes and the Hudson River after they invaded. Shifts in ecosystem dynamics with changes in food web structure and changes in productivity at higher trophic levels have been observed (Baker and Levinton, 1999; Nalepa et al. 2000; 2005; 2006; Madenjian et al. 2005; 2006). For example, zebra mussels significantly reduced the biomass of phytoplankton which increased transparency by 100% in Lake Erie and in Saginaw Bay, Lake Huron (Holland 1993; Fahnenstiel et al. 1993; Klerks et al. 1996). Phytoplankton biomass also declined 85% following invasion in the Hudson River (Caraco et al. 1997). The invasion of the zebra mussels into the Great Lakes also led to significant changes in diversity, distribution, and abundance of both native mussels (Nalepa et al. 1996) and fish species as a result of declines in prey organisms that were outcompeted by the zebra mussel. Indeed, drastic declines in lake trout, alewife, and whitefish populations were attributed to declines in food prey items which were out competed by zebra mussels for planktonic food items (MacIsaac 1996; Nalepa et al. 2000; 2005; 2006; Madenjian et al. 2005; 2006). Changes in habitat occurred over time as a result of changes in visibility. Additionally, increased light penetration may cause water temperatures to rise and thermoclines to become deeper, but these effects have not yet been documented (USGS, 2015).

We found several studies of clearance rates, but have reported only a few of the highest published clearance rates in Table 2. One study that included a weight-specific filtration rate for D. polymorpha was the highest rate for this species (Table 2, from Fanslow et al. 1995). Three studies reported D. polymorpha filtration rates on a “per mussel” rather than a weight-specific basis (Reeders and Bij de

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 33

Vaate 1990, Roditi et al 1996, and Rajagopal et al. 2003). In all three cases, we converted these “per mussel” rates to the weight-specific filtration rates in Table 2 by (1) calculating the mean weight of the mussels used to measure the filtration rates from their reported mean length and the length-weight equation in each paper, and (2) using that weight in the equations in each paper to calculate a weight- specific filtration rate from that study. Baker and Levinton (2003) estimated clearance rate for a standard 15 mg dtw zebra mussel fed cultured unicellular cyanobacteria, Microcycstis at 125 mL.h-1. We scaled this rate up to a standard 1 g dtw bivalve for comparison with other bivalves in Table 2.

McLaughlan and Aldridge (2013) offer a thorough review of the potential for zebra mussels to improve water quality in reservoirs, but caution about risks associated with encouraging an invasive species, even within sites where it has already established. Zebra mussel is a prominent biofouler of unionid mussels and water control structures. It changes the physical characteristics of the habitat and can be responsible for toxic cyanobacterial blooms. At a 90% efficiency rate, zebra mussels are much more efficient at filtration of small particles than are unionids and Asian clams (Cotner et al. 1995, Silverman et al. 1997). Indeed, inland lakes with zebra mussels have been found to have lower concentrations of dissolved organic carbon (Raikow 2002). It has also been speculated that biodeposition of feces and pseudofeces might cause observed increases in benthic macroinvertebrate populations (Stewart and Haynes 1994).

We did not find any studies of D. rostriformis bugensis filtration rates. As noted for R. cuneata and Corbicula, these Dreissenid mussels are non-native and highly invasive in US waters, so neither would be used in restoration projects. Culture methods for both Dreissenid mussels were reported by Wright et al. (1996).

Eastern elliptio (Elliptio complanata) Recent information indicates that clearance rates for the eastern elliptio are significantly higher than those published earlier (Paterson 1984). Gatenby et al. (2003) estimated summer clearance rates of E. complanata at 2.6-3.1 l h-1 individual-1 (Table 3), slightly higher for mussels fed lab diets than for mussels fed natural seston diets. Kreeger (2005a) found summer clearance rates of 3.4 l h-1 g-1 dtw during stream-side studies of E. complanata fed natural seston from the Brandywine River near Chadd’s Ford. PA. A comparison of seasonal clearance rates for three western mussel species showed that rates dropped quickly when water temperatures fell below 5-8oC (Kreeger 2011). Indeed, Kreeger (2011) found that spring and fall clearance rates are typically about 75-90% of summer rates. When the summer clearance rates of 3.4 l h-1 g-1 dtw are applied to the population of eastern elliptio and seston concentrations found in non-tidal Brandywine River in southeast PA (6 river miles, 500,000 animals), approximately 26 metric tons of dry total suspended solids (TSS) is removed by this bed of elliptios per year (Kreeger 2005b). In a later survey, scientists and partners surveyed 3.8 hectares of mussel habitat in the tidal Delaware River and found 682,000 mussels (6 species) that clear 25 million liters per day and over 1000 kg of dry TSS per year (Kreeger et al. 2013). The current distribution of eastern elliptio is greatly reduced relative to their historic distribution (Thomas et al. 2011), suggesting that they did more filtration in the past.

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 34

Other freshwater mussels Information on clearance rates of freshwater mussels that occur in the Chesapeake Bay drainage is scarce, with published clearance rate data for just two species (E. complanata and U. imbecilis, Table 2). Clearance rates for species of freshwater mussels found in Europe or in the Mississippi drainage, however, are more prevalent. Table 3 summarizes know clearance rates for freshwater mussels, including E. complanata and U. imbecilis.

As discussed above, diet quality, seasonal physiological demands, size of the animal, and environmental conditions affect filtration and clearance rates of freshwater mussels. Indeed, many bivalves compensate for reductions in food quality, and thereby maintain energy intake, by altering clearance rate, ingestion rate, sorting efficiency, or absorption efficiency (Iglesias et al., 1992; Hawkins et al., 1996; Navarro & Iglesias, 1993). Bivalves differ, however, in their abilities to regulate these responses (Hawkins et al., 1990; Navarro & Iglesias, 1993). Kreeger (2011) found that western species of freshwater mussels fed on natural seston differed widely in their post-ingestive processing of diets, and their clearance rates were significantly different among genera, season and body size. Annual pooled CRs ranged 0.37-0.90 l h-1 g-1 dtw (Gonidea sp., Margaritifera falcata, and Anodonta californianus, respectively). Indeed, body size was a better predictor of clearance rate than species, demonstrating the critical importance of allometric scaling in experimental studies (Fig. 3).

The highest freshwater mussel clearance rates reported in Table 3 are for E. complanata fed natural seston during summer (ref. 9, 3.4.l.h.gdtw-) and for Margaratifera margaritifera fed a green cultured algae (ref. 12, 2.75 l h-1 g-1 . The lowest freshwater mussel clearance rates (ref 10, range 0.0012-0.0076 l h-1 g-1) were from mussels fed very high concentrations of cultured algae which could have supersaturated their needs and led to cessation of feeding. Clearance rates for Utterbackia (0.036 l h-1 g-1, ref. 4) also appear unusually low for a species that is fast growing and with large gills. This is likely because they Figure 3. Relationship between clearance were fed a lab-cultured diet of only E. coli bacteria, as the rate and dry tissue weight for three investigators were specifically interested in freshwater species of freshwater mussels living in mussel’s capacity to filter bacteria. Smaller sized mussels various streams of eastern Oregon had lower clearance rates than larger sized mussels, and (Kreeger 2011). rates appear to vary among species (Table 3). Freshwater mussels fed a high quality algal diet had higher clearance rates than species fed natural seston or fed only bacteria. Species adapted to turbid environments also had lower clearance rates than animals adapted to less productive waters (Silverman et al. 1997).

Gatenby et al. (2003) estimated summer clearance rates for 3 large-sized species of freshwater mussels in the Allegheny River and fed on natural seston ranged from 1.1 – 1.5 l h-1 individual -1 or 0.288-0.580 l

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 35 h-1 g-1 dtw. Baker and Levinton (2003) reported clearance rates ranging 0.5-2.75 l h-1 g-1 dtw for three fairly large species of mussels (Amblema plicata, Pyganodon grandis and Margaratifera margaritifera) found in the Mississippi, Great Lakes and Atlantic drainages. Kreeger (2011) found summer clearance rates for three western species of freshwater mussels ranged (0.40-1.1 l h-1 g-1 dtw; Gonidea sp., Margaritifera falcalta and Anodonta californianus, respectively). Clearance rates of over 2 l h-1 g-1 dtw for both Anodonta sp. and Margaritifera falcalta, however, were observed for smaller individuals less than 40 mm in length. The freshwater mussels of the Chesapeake Bay drainage range in size similar to several of the species reported in Table 3. Assuming that size is a better predictor of clearance rate, we estimate that clearance rates for native freshwater mussels in the Chesapeake Bay drainage fed natural seston will also range between 0.5 and 3.4 l h-1 g-1 dtw during the growing season (April to November). Winter clearance rate, while not zero unless systems are frozen, will be greatly reduced.

A comparison of clearance rates between freshwater mussels and similarly sized marine species suggests that marine species clear water slightly faster than their freshwater counterparts, perhaps because their metabolic and growth rates are faster than the more long-lived freshwater mussels (Kreeger, unpublished). We do not know, however, whether grazing pressure by freshwater mussel species affects plankton and periphyton communities differently compared to marine species. It's well documented that marine bivalves exhibit great plasticity in their post-filtration handling of captured material (Ward et al. 1993; Ward, 1996; Ward et a. 1998a and 1988b; Milke and Ward 2003; Rosa et al. 2013). For example, the ribbed mussel can adjust gill spacing to capture very small bacteria (Wright et al. 1982). Limited data suggest that freshwater mussels also can adjust the spacing of their gill filaments to capture different types and sizes of particles to best match their nutritional demands, potentially altering the trophic cascade within planktonic food chains (Gatenby et al. 2003; Baker and Levinton. 2003, Kreeger 2011). The fate of captured seston, therefore, likely varies among species even if clearance rates are similar. This could lead to important interspecific differences in the retention of material, remineralization of dissolved nutrients, and effects on sediment biogeochemistry (e.g., Kreeger 2011).

Estuarine (tidal) bivalves

Brackish water clam (Rangia cuneata) Details of their biology and ecology are in LaSalle and de la Cruz (1982). Clearance rates (Table 2) were reported as 2.06 l h-1 g-1 dtw (Wong et al. 2010). This species is probably non-native, but is not generally considered invasive in Chesapeake Bay since it is naturalized here. However, it is unlikely to be used in restoration projects since it may be non-native. We also know very little about its limiting factors in Chesapeake Bay.

Spawning in the lab and raising the larvae to settlement has been done for settlement experiments (Sundberg and Kennedy 1992 and 1993).

See map of the distribution of this species Chesapeake Bay in Appendix A; it can be very abundant in tidal fresh and oligohaline regions. See Appendix B for a box plot of density by year and a line graph of percent occurrence by year from benthic survey data (Versar 2011). Both the density and the percent

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 36 occurrence varied little by year; this species had the second highest percent occurrence after Baltic clams, Macoma. Poirrier et al. (2009) reported the maximum density of this species in Lake Ponchartrain, LA (before Hurricane Katrina) as 350 clams m-2 for clams 21 mm or larger, with a maximum biomass of 20-25 g m-2.

Dark false mussel (Mytilopsis leucophaeata) This species is fairly small (length to almost 3 cm) and is an uncommon inhabitant of low salinity oyster bars (unpublished data from Tarnowski 2011). They also occur on soft bottom in the CBP benthic surveys, but they are uncommon in those as well and found in only 1-13% (mean 3%) of samples by year from 1989-2008. The measured salinity ranges for this species in Table 2 (above) are from the CBP benthic surveys, because that survey samples at salinities lower than those at which C. virginica can grow.

Spawning in the lab has been done, followed by raising the resulting larvae to settlement and beyond, for up to 49 days for one brood (Kennedy 2011a, 2011b). Most larvae had undergone metamorphosis by 9 days.

Populations of this species appear to be so small and scattered (except during irruptions) that Kennedy (2011a, 2011b) wondered how they persist, since fertilization of their gametes seems unlikely. However, their tendency to have large and small irruptions (see below) suggests that there may be unknown populations of this species that can produce large numbers of gametes under the right conditions. Where these populations might live, and why they have not been sampled in various surveys, is not known. This sparse and patchy distribution was not mentioned in a review of this species where it has been introduced in Europe (Verween et al. 2010) or the Hudson River (Walton 1996), so the distribution of its introduced populations may be more uniform than where it is native. Given the many questions about its limiting factors, plus its small size, it is not a promising candidate for restoration projects.

Their maximum clearance rate (at the optimum temperature, 20-28 oC) was reported by Rajagopal et al. (2005a) as 0.055 l ind.-1 h-1 (per mussel) for the largest size class they tested (20 mm long). Their tissue weights were not given, and none could be found for a mussel of that size to convert this rate to a weight basis. Thus, we assumed that a published length-afdw relationship for D. polymorpha (Reeders and Bij de Vaate 1990) applied to M. leucophaeata. Using that equation, the afdw of a 20 mm M. leucophaeata would be 0.028 g, yielding a clearance rate based on that weight to 1.96 l h-1 g-1 afdw (Table 2), very close to the rate for 22 mm zebra mussels reported by Reeders and Bij de Vaate (1990). A similar approach was used to calculate the other clearance rates in the table, from Rajagopal et al. (2003), 1.66 l h-1 g-1 afdw, and from Rajagopal et al. (2005b), 2.37 l h-1 g-1 afdw. The last and highest rate was for detached mussels, which filtered 42% more than the attached mussels in the same study; that attached rate was almost identical to the rate from Rajagopal et al. (2003). The detached mussels gaped more often, and thus filtered more, in an effort to re-attach themselves (Rajagopal et al. 2005b). Since many clearance rate studies use detached mussels, this introduces another source of variability in measured clearance rates.

An irruption of M. leucophaeata occurred in low mesohaline regions of Chesapeake Bay (especially in the Patapsco and Magothy rivers) in 2003-2005 (Carey and Hornor 2005, Goldman 2007a, Bergstrom et Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 37 al. 2009, Kennedy 2011b). The irruption started during two wet years (2003-2004) that followed three dry years and one normal year (USGS 2012), and spawning can be triggered by a sudden drop in salinity in this species (Kennedy 2011a, 2011b). This normally uncommon inhabitant of low salinity oyster bars became abundant in these and some nearby rivers in the spring and summer of 2004, growing in thick layers on pilings, rocks, ropes, boats, and other hard substrates. Both the frequency of occurrence and estimated abundance of M. leucophaeata on oyster bars were slightly higher in 2004 than in 2005-2009, (unpublished data from oyster surveys in Tarnowski 2011). The fact that the dark false mussels were only slightly more common on C. virginica in 2004 suggests that during irruptions, most of the population increase occurs on substrates other than C. virginica. In that sense they resemble an invasive species during an irruption, growing on novel surfaces for this species.

See map in Appendix A from the MD oyster survey (hard bottom), and Appendix B for a box plot of density by year and a line graph of percent occurrence by year from benthic survey data (soft bottom, Versar 2011). In the box plots, note the peaks in density in wet years (1996, 2003, and 2004), but the highest percent occurrence was in a dry year, 1995. The M. leucophaeata found in the benthic survey on soft bottom may be attached to other, larger bivalves (such as Rangia shells, Poirrier et al. 2009) or other hard objects.

Baltic macoma clam (Macoma balthica) Two published clearance rates were found, and they were fairly low, 0.4-1.33 l h−1 g−1 afdw (Table 2). This species can also be a deposit feeder using an extendable siphon, but they are thought to use suspension feeding when adequate phytoplankton are available, as they usually are in Chesapeake Bay (Gerritsen et al. 1994, Lin and Hines 1994). They appear to be fairly tolerant of low dissolved oxygen or DO (< 2 mg l-1) with no mortality for the first 2 days of exposure, they can extend their incurrent siphon up in the water column in search of water with more DO in it, and they can detoxify sediment sulfide (Seitz et al. 2003). These clams are an important winter food of diving ducks, including canvasbacks, buffleheads, and ruddy ducks, and are eaten by other waterfowl as well (Perry et al. 2007). They are also important food for juvenile blue crabs, which may migrate from seagrass beds near the mouths of rivers quite a distance upriver to near the turbidity maximum, where these clams can be abundant due to a good food supply for them in the suspended particles (Seitz et al. 2005).

Spawning in the lab has been done (Caddy 1967), but no attempts to raise the resulting larvae are known.

See map in Appendix A from CBP benthic survey data (Versar 2011). See Appendix B for a box plot of density by year and a line graph of percent occurrence by year, also from CBP benthic survey data; note the drop in density in 1994. The box plot shows that density declined a bit after the first few years of data. The line graph shows that except for one peak in 1989 with about 75% occurrence, the percent occurrence was the highest of the species shown here and fairly consistent, ranging from 25-45% of samples.

Soft-shell clam (Mya arenaria) Riisgard and Seerup 2004 reported a clearance rate of 4.8 l h-1 g-1 afdw, and Bacon et al. (1998) measured clearance rates, but as a function of seston (total suspended solids) and particulate organic Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 38 matter concentration, so only a maximum rate from their study (from their Fig. 5) is listed in Table 2, 3.5 l h-1 g-1 dtw.

This is a commercial species, and seed of various sizes are available from hatcheries. The hatching and rearing process is well established (Downeast Institute 2013).

See map in Appendix A from CBP benthic survey data (Versar 2011). See Appendix B for a box plot of density by year and a line graph of percent occurrence by year, also from CBP benthic survey data. In the box plot, note the drop in density in 1994, and in the line graph, note the sharp drop in percent occurrence from near 20% in 1989 to 0% in 1995, remaining very low after that. For a discussion of limiting factors, primarily predation by crabs and disease, see Abraham and Dillon (1986) and Dungan et al. (2002). Thus, these are not a promising candidate for enhancing filtration in Chesapeake Bay, especially since seed clams bought from New England died in the Rhode River in summer 2011 (see below).

Hooked or bent mussel (Ischadium recurvum) The hooked or bent mussel (Ischadium recurvum) is much smaller than G. demissa, growing to only 4-6 cm long, and much less research has been done on it. No published clearance rates have been found. A study to measure rates in Chesapeake Bay is almost complete (L. Kellogg, pers. comm.), and we included unpublished rates from another study (K. Gedan, pers. comm) in Table 2, with a maximum rate of 4.3 – 4.6 l h-1 g-1 dtw.

Ischadium recurvum also was recently confirmed as native to Chesapeake Bay (Ruiz, pers. comm.), so it could be cultured to enhance filtration (see below) without raising issues of promoting non-native invasive species. It is more restricted than G. demissa to hard substrates, and is often found growing on C. virginica and associated hard substrates, being found on 75-92% of the oyster bars sampled in 2004- 2009 in the MD fall oyster survey (unpublished data from Tarnowski 2011), much more often than M. leucophaeata . Like M. leucophaeata, they were most common (essentially tied with 2007, 91% and 92%) and most abundant in the year (with the lowest salinity in that period, which was 2004 (unpublished data from Tarnowski 2011). This suggests that their spawning may be triggered by sudden drops in salinity, as it is for M. leucophaeata (Kennedy 2011a), since 2003-2004 were wet years after three dry years and one normal rainfall year (USGS 2012). It appears that I. recurvum reach peak abundances in higher salinity waters than M. leucophaeata; on oyster bars in MD Chesapeake Bay they were found at a salinity of about 8-16 (Table 2), and in SW Florida the peak abundance for I. recurvum was at 12, with a minimum salinity of 6 (Montagna et al. 2008).

Lipcius and Burke (2006) documented I. recurvum density and biomass where they grew with C. virginica on artificial reefs in the York River, estimating maximum mussel density as about 2,750 mussels m-2 of reef, and mean mussel biomass as 670 g m-2 of river bottom in five stacked layers of concrete reef (or 134 g m-2 of reef surface). Bahr and Lanier (1981) reported I. recurvum density and biomass on intertidal oyster reefs in Georgia, and their mean biomass was 24 g m-2. In Lake Pontchartrain, Louisiana, I. recurvum grow on dead R. cuneata shells on soft bottom, forming small spherical “reefs” about 30 cm in diameter (Poirrier et al. 2009), so I. recurvum may also grow on dead Rangia clam shells in Chesapeake Bay. I. recurvum had a mean lake-wide density up to 2,284 mussels m-2 when salinity in the lake was Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 39 high (up to 10) during a drought in 2000-2001 (Poirrier et al. 2009), very similar to the maximum density reported by Lipcius and Burke (2006) on artificial reefs. Since a shortage of hard substrate appears to be one of the main limiting factors for this species in Chesapeake Bay, and we can add hard substrate, and it has fairly high clearance rate, it is one of two native estuarine subtidal species we are recommending for restoration projects (see below).

Spawning in the lab has been done, raising the larvae to settlement (Chanley 1970). If I. recurvum were to be grown for their biofiltration benefits, they would probably attach strongly enough to suspended ropes to grow on those, just as many blue mussels (M. edulis) are grown in on ropes aquaculture (Lesser et al. 1992). Kennedy (2011b) measured the byssal thread strength of a 20 mm I. recurvum as 8.7 N, which is similar to literature values for M. edulis, which ranged from 4.9-16.7 N. The recent tests of G. demissa in the Bronx River tried to grow them on ropes but found their byssal threads could not support their weight, so they had to be held in place with synthetic socking that did not degrade over time (Rose, pers. Comm.). Socking, if left in place, would restrict both water flow and growth of the mussels. To culture blue mussels, culturists use biodegradable socking to give the mussels time to attach to the rope, and by the time the socking decays, they are firmly attached to the rope and can grow outwards.

See map in Appendix A for their distribution and estimated abundance from the MD oyster survey (hard bottom). The map shows that two areas, in the Chester River near the Corsica River and in the Choptank River near Cambridge, had the highest estimated abundances in most years. Being a hard bottom species, I. recurvum occur so rarely in the CBP soft bottom benthic survey that there is no box plot or line graph for them in Appendix B.

Atlantic ribbed mussel (Geukensia demissa) The Atlantic ribbed mussel (Geukensia demissa) grows up to 10 cm long, lives up to 15 years, and has weight-specific clearance rates similar to those of C. virginica (Table 2; Jordan and Valiela 1982, Riisgard 1988). It is omnivorous, feeding on a wide array of particle types (Kreeger et al. 1988, Kreeger and Newell 2001). Of special note, G. demissa have an exceptional ability to filter (and digest) free bacteria even less than 1 µm in size (Wright et al. 1982, Langdon and Newell 1990, Kreeger and Newell 1996), and they appear to possess their own endogenous cellulases for digesting refractory plant matter (Kreeger and Newell 2001). G. demissa filter and digest large celled benthic algae as well, with assimilation efficiencies >90%. These traits are thought to be adaptations for life in detritus-rich salt marshes (Kreeger and Newell 2000, Valiela et al. 1997), where they live primarily in mutualism with wetland vegetation (Bertness 1984). Of special relevance for water quality remediation is their bacteria removal ability since G. demissa might potentially help to remove and metabolize pathogenic bacteria (Kreeger and Bushek 2011). Filtered bacteria can be assimilated with >80% efficiency (Kreeger and Newell 1996, 2001). The exceptional bacteria filtration and digestion capacity of G. demissa could mean that they are especially useful for pathogen removal services.

The salinity tolerance of G. demissa is slightly broader than that of oysters (Table 2): from 5 (or lower) to >30 (Lent 1969, Puglisi 2008, Nestlerode and Toman 2009) or about 6-17 in Chesapeake Bay (Table 2), vs. about 11-19 for C. virginica in Chesapeake Bay (Table 2). Lent (1969) reported that mussels can tolerate salinities up to 70 and temperatures up to 56oC at least for limited times. They are uniquely

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 40 adapted for intertidal conditions, being able to respire aerobically through air-gaping when the tide is out (Lent 1967), tolerating ice freezing in winter (Kreeger, pers. comm.), and actually growing faster intertidally than subtidally (Gillmor 1982, Kreeger et al. 1990). Kuenzler (1961) reported its mean clearance rate was 6.8 l h-1 g-1 (Table 2) but the paper does not say if the tissue weight (g) was ash-free or not (presumably it was not ash-free). Kreeger and Newell (2001) measured seasonal clearance rates for G. demissa and contrasted those among particle types, finding average summer clearance rates of 5.1 l h-1 g-1 dtw for bulk seston.

G. demissa can be found intertidally on almost any firm surface. However, their natural habitat is in salt marshes where they attach to the rhizomes of marsh plants, particularly smooth cordgrass, Spartina alterniflora. Although they can live subtidally, their distribution appears confined mainly to intertidal areas due to predation from blue crabs (Bertness and Grosholz 1985, Lin 1989). Average densities of G. demissa in salt marshes vary with proximity to the edge. Along low marsh edges in the Delaware Estuary, G. demissa densities average 147 m-2 and 187 g dtw m-2; whereas, high marsh flats contain 10 mussels m-2 and 5.6 g dtw m-2 (Kreeger, unpublished). Despite the much greater area of high marsh compared with low marsh edge, 60% of the numerical abundance and 77% of population biomass of G. demissa was in the edge habitat. Summed across both habitats, each hectare of salt marsh was estimated to contain 208,000 mussels (>1 cm shell height) and weighing 205 kg dry tissue. These are consistent with findings of Jordan and Valiela (1982) who reported that G. demissa are the functional dominant animal of the salt marsh because they tend to outweigh all other animals combined. Their biodeposits act like fertilizer, helping to sustain high primary productivity in marshes with healthy mussel communities (Jordan and Valiela 1982, Bertness 1984). Although G. demissa populations are vulnerable to loss of salt marsh from increased rates of sea level rise and other factors (Kreeger et al. 2010), they nevertheless are estimated to currently filter more water per year than any other bivalve within the Delaware River Basin (60 billion l h-1, which is approximately 6 times greater than C. virginica at today’s populations (Kreeger and Gatenby 2008). Since the Delaware Estuary is losing an acre per day of ribbed mussel habitat (PDE 2012), it is important to consider ways to stem losses of ecosystem services (e.g. with living shorelines tactics) in addition to restoration investments.

In Chesapeake Bay, G. demissa are not routinely sampled where they tend to be most abundant, in tidal marsh edges. They have been found in soft-bottom benthic surveys in fairly deep water at low abundance (maximum density was 1000 m-2 but usually only 20-45 m-2), and found in only 1-3% of benthic samples by year from 1989-2008 (Versar 2011). They were found as far north as the Elk River and in the mainstem near Pooles and Hart-Miller islands, both oligohaline, and in the mouth of the Patapsco River (low mesohaline), so they probably have growth potential in low mesohaline rivers as well as in higher salinity. G. demissa sometimes also attach to subtidal C. virginica, but in the five years of MD fall oyster survey data available (2005-2009), this species was rare. They were found on C. virginica in 1-4 bars in three of those years, all at low abundance, and none were found in two years. Since this survey samples close to 400 oyster bars (Tarnowski 2010), these represent 1% or less of the bars sampled.

They have been stimulated to spawn in the lab, but the process is more difficult than in most of the other bivalves considered in this review (Kennedy, pers. Comm.). Despite that difficulty, since a

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 41 shortage of salt marsh edges appears to be one of the main limiting factors for this species in Chesapeake Bay, and we can restore those, it holds promise for restoration projects. Since it also has a high clearance rate, it is one of two estuarine subtidal species we are recommending for restoration projects, and the only species we recommend for intertidal restoration (see below).

See map in Appendix A from the Versar benthic data. See Appendix B for a box plot of density by year and a line graph of percent occurrence by year, also from benthic survey data (Versar 2011). Note the drop in density in 1994, and the percent occurrence (line graph) was very low in every year except 1995 when it rose above 20% for one year. Taken together, these findings indicate that the bulk of the Atlantic ribbed mussel population in the Chesapeake is likely to exist in the less studied fringing tidal marshes, which is thought to be their natural habitat.

Stout razor clam (Tagelus plebeius) No published clearance rates have been found. One study (Arruda et al. 2003) confirmed that they are suspension feeders, and that they could be the most abundant species in that group in the study area in Brazil, but it did not measure clearance rates.

Spawning in the lab has been done, raising the larvae to settlement (Chanley and Castagna 1971).

See map in Appendix A, and box plots of density by year in Appendix B, both from the CBP benthic survey (Versar 2011); note the drop in density in 1994 (box plot), and the percent occurrence (line graph) was very low, especially from 1998 onward.

Eastern oyster (Crassostrea virginica) Four published clearance rates were found (Table 2), ranging from about 6-11 l h-1 g-1 dtw. These were some of the highest rates in the table, and help explain why C. virginica are valued for their ecosystem benefits.

Their salinity range in Chesapeake Bay is from about 7-30 and they are usually limited to hard substrates. Their current populations in Chesapeake Bay are limited by a number of factors, primarily habitat loss (mainly from sedimentation and low dissolved oxygen), overutilization, variable recruitment and survival of larvae, predation, disease, introduced species, and harmful algal blooms (White 1989, Kennedy et al. 1996, and Eastern Oyster Review Team 2007).

Hard clam (Mercenaria mercenaria) Three published clearance rates were found (Table 2), and all were several times lower than the rate for C. virginica. Riisgard (1988) suggested that the hard clam rate might be twice as high for clams tested in natural substrates, but Newell and Koch (2004) measured clearance rates using clams in sediment and found lower clearance rates than Riisgard (1988), while the rate measured by Echevarria et al. (2012), for clams not in sediment, was slightly higher, but still low (Table 2). These low weight-specific rates suggest that hard clams are not a promising alternative to C. virginica for improving water quality. Research has shown that large numbers of hard clams grown in a small creek (Cherrystone Creek on Virginia’s Eastern Shore) can improve water clarity, but the macroalgae that grows on the nets that keep predators away from the clams may use up oxygen when they die (Goldman 2007b).

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Culture methods for hard clams are well known, and seed of various sizes is commercially available, for example from BayFarm in New Jersey (BayFarm 2013; Castagna and Kraeuter, 1981).

Blue mussel (Mytilus edulis) Blue mussels usually live attached to hard surfaces in rocky intertidal areas or attached to piers, but can also live in deeper ocean waters to 100 m or more (Newell 1989). They occur on the east coast of North America as far south as Cape Hatteras, NC, in shallow water, and are prevented from living farther south in shallow water by an upper temperature limit of about 27 oC. They have been found as far south as Charleston, SC in deeper, cooler water (Newell 1989). They are limited in Chesapeake Bay to the cooler, saltier waters near the mouth of the Bay (Lippson and Lippson 1984). As a result of their limited occurrence, they are not considered in this review, and are not listed in Table 2. Larvae that settle farther up the Bay may grow for a while, but usually die over the summer (Lippson and Lippson 1984). Thus, high summer temperatures, more than low salinity, limit their distribution in Chesapeake Bay, since blue mussels can tolerate salinity as low as the mesohaline range (5-18) in cooler estuaries (Newell 1989). They have been grown in coastal waters in Sweden for nitrogen removal, with mixed results (see next section).

RECENT, CURRENT, AND PLANNED RESTORATION OF BIVALVES FOR ECOSYSTEM SERVICES There are numerous potential opportunities to either conserve or enhance the water quality benefits of bivalves throughout the Chesapeake Bay and its watershed. Here, we review the literature and discuss these opportunities in three different parts of the watershed continuum: open waters of the tidal estuary (subtidal), fringing habitats along the tidal estuary (intertidal), and freshwater streams and rivers (non-tidal). Freshwater tidal habitats are not abundant in the Chesapeake and opportunities therein will be similar to freshwater non-tidal habitats.

Open waters of estuaries (subtidal) Mussels are often grown in aquaculture by suspending them on ropes in the water column, increasing their food availability, as suggested by Gerritsen et al. (1994). In addition to rearing mussels for their direct market value as a human food, mussel aquaculture is increasingly being studied as a tactic to remediate water quality. Mussel biomass is removed periodically, thereby removing sequestered nutrients and contaminants as a “bioextraction” process. For example, mussel culture on suspended ropes was funded in coastal Sweden for nitrogen removal, at a cost of about $200,000 US, which was promoted as a cheaper alternative to upgrading a wastewater treatment plant for the town of Lysekil (Lindahl et al. 2005). Unfortunately, the market for the mussels was not as good as had been projected, so it was not cost-effective to harvest them, and the nitrogen removal that was planned did not occur. As a result, the wastewater treatment plant upgrades had to be made later (Lindahl, pers. comm.). Other bivalves can also be used for bioextraction. Rhode Island is investigating whether nutrient removal credits might be issued to scallop farmers who routinely harvest product from the estuary (D. Alves, pers. comm.). The Long Island Sound Study is exploring ways to incorporate shellfish aquaculture into the Total Maximum Daily Load for Nitrogen that is currently under revision in Long Island Sound (J.

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Rose, personal communication). The Piscataqua Region Estuaries Partnership is investigating the potential use of shellfish aquaculture and restoration for nutrient removal in New Hampshire (Grizzle 2011, Grizzle and Ward 2011)

One group has explored possible ways to enhance the populations of bivalves other than C. virginica in low mesohaline estuaries in Chesapeake Bay. In the West and Rhode rivers, a postdoctoral student at the Smithsonian Environmental research Center (SERC) studied the feasibility of using soft-shell clam (Mya arenaria) seed (salinity range 5-30) bought from hatcheries in New England in 2011, grown under nets to provide predator protection, based on modeling done by engineering students at George Mason University (Askvig et al. 2011). However, most of the seed clams died in summer 2011, probably from high water temperatures, so the project will focus on oysters instead.

Recommended subtidal estuarine species for restoration in the Chesapeake watershed In our review, we found four native species of bivalves that occur in estuarine systems and have clearance rates similar to C. virginica (highlighted in Table 4). We also identified three non-native estuarine bivalves that had high clearance rates, but these should not be considered for any restoration projects. It is plausible that the effects of some of the four native estuarine species on water quality could be equal to and possibly greater than those of C. virginica, depending on total biomass and other factors. Also, the cumulative effects of restoring multiple species of native bivalves within a range of habitats could be significantly greater than any single-species restoration project.

Planning for restoration (see below) should include a consideration of what factors are limiting populations now, to assess whether restoration is feasible (if we can overcome those limitations), and if it is feasible, to assist with site selection and increase the chances that restoration will increase populations. For the native estuarine species we are recommending for restoration, we included what we know about limiting factors in Table 4.

The four native estuarine bivalves with clearance rates similar to those of C. virginica are as follows; the first two should be considered for subtidal estuarine restoration projects, since we can overcome their main limiting factors with restoration. However, as noted above, blue crab predation mainly limits G. demissa to intertidal habitats, so they are probably more promising for restoration in intertidal than subtidal habitats. We don’t know enough about the factors limiting populations of the last two species, or our ability to control them, to recommend them for restoration at this time (Table 4).

• Ribbed mussels (Geukensia demissa) which were used in a recent biofiltration pilot study in the Bronx River;

• Hooked mussels (Ischadium recurvum) can reach very high density, but have not been tested for biofiltration potential;

• Soft-shell clams (Mya arenaria) were planned for a pilot biofiltration study in the West River in 2012, but most of the animals died before the study started; and

• Dark false mussels (Mytilopsis leucophaeata) were part of a natural experiment in 2004, when hundreds of millions of them appeared in several low mesohaline Chesapeake tributaries, and some of Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 44 those tributaries had documented improvements in water quality and submerged aquatic vegetation (SAV) area when they were present (but most of the mussels were gone by 2005).

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Table 4. Clearance rates for C. virginica and other estuarine (tidal) Chesapeake bivalves, arranged from highest to lowest maximum rates in two groups (native and non-native). The seven other bivalves listed all had maximum clearance rates that were at least 30% of the minimum rate for C. virginica. Three native species are recommended for use in restoration in different habitats (last column).

Species Clearance rate (l h- Salinity range from Main limiting Best for 1 g−1 of dry tissue) literature factors restoration in: Native species Eastern oyster, 6.4- 11.5 7-30 Hard substrate, Subtidal Crassostrea low virginica recruitment1 Ribbed mussel, 5.1-6.8 10-30 Loss of marsh Intertidal & Geukensia demissa edges2 subtidal Hooked mussel, 4.3 – 4.6 5-30 Hard substrate3 Ischadium recurvum Soft-shell clam, Mya 3.5-4.8 5-30 Disease, crab Subtidal arenaria predation 4 Dark false mussel, 1.7-2.4 0-10 Not sure (not Mytilopsis common leucophaeata anywhere) 5 Non-native species Zebra mussel, 2.7-16.2 0-5 Dreissena polymorpha Asian clam, 2.9 0-2 Corbicula sp. Brackish water 2.1 0.5-10 clam, Rangia cuneata 1 Eastern Oyster Biological Review Team 2007 2 Kreeger et al. 2010 3 Lipcius and Burke 2006 4 Abraham and Dillon 1986, Dungan et al. 2002 5 Kennedy 2011a, 2011b

Fringing waters of estuaries (Intertidal) M. edulis are found intertidally in this region in many estuaries, but they are too scarce in Chesapeake Bay to be considered in this review (see above). However, G. demissa are an abundant intertidal bivalve in salt marshes of Chesapeake Bay (Lippson and Lippson 1984). The conservation and restoration of G. demissa appears to have promise for assisting in water quality management and improvement in intertidal Chesapeake Bay where the salinities are within its range, down to about 6 (Table 2). There are no other intertidal bivalves in Chesapeake Bay (other than oysters) that are candidates for restoration.

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Pilot projects are underway in two nearby estuaries to test the feasibility of culturing G. demissa to enhance water quality. In the Bronx River (LaSalle 2010, Galimany et al. 2011, Newell 2011, Newell 2013, Emspak 2012) and Delaware Bay (see below), projects are planned or underway to either conserve or enhance G. demissa populations for water quality benefits. The Bronx River project was funded in part through a settlement that resulted from discharges of raw sewage into the Bronx River from local storm sewers. The project attempted to collect and grow G. demissa larvae on subtidal aquaculture ropes hanging from a raft that was installed in August 2011, and on intertidal coir logs simultaneously placed in a local salt marsh. However, no G. demissa larvae attached to the ropes, and low numbers were observed on coir logs by April 2012 (Carter and Newell 2011), and the raft had to be removed by December 2012 as a permit condition, so the ropes were stocked with mussels from Jamaica Bay, NY during April 2012 and were harvested from the ropes in October 2012 (J. Rose, pers. comm.). The Partnership for the Delaware Estuary (PDE) is including intertidal G. demissa in living shoreline projects designed to stabilize eroding marsh edges (Bushek and Kreeger 2010, Whalen et al. 2011) and is strategizing ways to perhaps also capitalize on potential nutrient and pathogen removal for water quality remediation. Facing a projected loss of 25-95% of salt marshes by 2100, PDE is also making the case that a concomitant loss of G. demissa (from lost habitat) may have important ramifications for the maintenance of water quality in Delaware Bay. Efforts to sustain and expand salt marshes therefore represent an indirect but important tactic for sustaining or expanding filtration services provided by bivalves, especially considering that G. demissa can be the dominant filter-feeding bivalve in wetland- rich estuaries such as the Delaware system (Kreeger and Bushek 2008, Kreeger and Gatenby 2008, Kreeger et al. 2011).

Freshwater streams and rivers (non-tidal and freshwater tidal) With the creation of the Endangered Species Act in 1973 and the listing of 72 freshwater mussel species over subsequent years, research facilities began to investigate in earnest the life histories of individual species. The eventual goal of these investigations was the development of propagation techniques for restoring imperiled species (National Native Mussel Conservation Committee 1998). Since the late 1990’s, several propagation programs throughout the Midwest, Mid-Atlantic and Southeastern United States have been successful in propagating juvenile mussels and stocking progeny in the wild to augment dwindling populations of endangered freshwater mussels. Staff at the White Sulphur Springs National Fish Hatchery (WSSNFH) and Virginia Tech conducted research between 1991 and 2004 to develop culture and propagation technology, to identify feeding regimes for culturing freshwater mussels and to develop protocols for holding adult broodstock at the WSSNFH.

This information, coupled with advances in propagation techniques and advances in our understanding of the biology and ecology of freshwater mussels made by others at the U. S. Forest Service Southern Research Station in Oxford, MS, Missouri State University, North Carolina State University, Ohio State University, and Tennessee Tech, led to the development of freshwater mussel propagation programs at the WSSNFH, the Virginia’s Fisheries and Aquatic Wildlife Center (VFAWC) at the Harrison Lake National Fish Hatchery (HLNFH)and North Carolina’s State Fish Hatchery in Marion, NC. Other facilities exist

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 47 throughout the United States, but the aforementioned three facilities are culturing and stocking Chesapeake Bay drainage freshwater mussel species.

Although most of the interest in restoring freshwater mussels has been driven by species conservation, many in the academic and governmental community are beginning to also press for preservation and restoration of ecosystem services provided by more ubiquitous species. Still, the majority of freshwater mussel programs in the United States have a common goal, which is the recovery of endangered species of mussels through stock enhancement of dwindling populations and reintroduction into restored historical habitat. The goals of the WSSNFH and HLNFH also include working to restore the ecological function of our nation’s rivers by restoring beds of freshwater mussels and the ecosystem services they provide, and providing shelter for mussels threatened by pollution or other instream construction projects. Indeed, the US Fish and Wildlife Service (USFWS) with other state, federal, academic and non- governmental agencies is monitoring the status of freshwater mussels within the Chesapeake Bay basin, is working to identify areas for restoration and recovery of freshwater mussels and their habitats, and is working to restore population size and demographics to achieve recovery for generations to come, and to boost populations such that they can survive stochastic events. Thus, in addition to developing technology for culturing a suite of species of freshwater mussels, the USFWS and their partners are working to remove barriers to fish passage, are enhancing riparian zone habitat for fish and other aquatic organisms, and are restoring in-stream channel habitat for fish and mussels in the Chesapeake Bay drainage. The following are examples of restoration and recovery activities conducted by the USFWS’ WSSNFH, and there numerous others that could be referenced from around the country. From 2004 to 2008, the WSSNFH provided refuge to endangered northern riffleshell (Epioblasma rangiana) and clubshell (Pleurobema clava) while a new bridge was constructed at East Brady, PA. While in captivity adult northern riffleshell spawned and progeny were reared for 2 years, then stocked back into the Allegheny River. Additional northern riffleshell broodstock were collected for 3 years, larvae were extracted from gravid females, cultured at the WSSNFH for 2 years, and juvenile mussels were stocked in the Allegheny River to mitigate effects of bridge construction. During the summer of 2006, 38,000 juvenile freshwater mussels from 4 species were propagated at the WSSNFH and stocked in the Kanawha River, WV in cooperation with the West Virginia Division of Natural Resources, U.S. Army Corps of Engineers, and the USFWS’ West Virginia Field Office. More recently, the WSSNFH has been working with the WVDNR and the USFWS’ Ohio River Islands National Wildlife Refuge to restore freshwater mussel populations destroyed by a toxic chemical spill that occurred (in 1999) in the Ohio River near Marietta, OH. The spill killed over 1,000,000 freshwater mussels in a 20-mile reach of river. Adult mussels of several large-sized species of mussels were translocated from the Allegheny River (major tributary to the Ohio River) to help establish a mussel bed 900 meters in length. The restoration effort continues with stocking of cultured mussels from over 10 species of mussels into this managed mussel bed in the Ohio River. Annual monitoring of the bed shows high survival for adult translocatees and stocked juvenile mussels (Morrison 2012). The restoration effort is in year 4, and is expected to continue for a full 10 years to ensure the bed contains a wide distribution of age classes among species.

Virginia’s Fisheries and Aquatic Wildlife Center at the HL NFH has been developing technology and producing Atlantic slope freshwater mussels since 2006 for augmentation of depressed populations of state listed freshwater mussels (B. Watson, pers. comm) (Table 5). North Carolina’s Conservation Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 48

Aquaculture Center has over 12 years’ experience developing technology and rearing Atlantic slope freshwater mussels for restoration of endangered and threatened species. Other partners engaged in freshwater mussel restoration on the Atlantic slope include the Partnership for the Delaware Estuary, which launched a watershed-wide bivalve shellfish restoration strategy in 2005 that includes the restoration of native freshwater mussels in the tributaries to the Delaware River, along with oyster and G. demissa restoration in and along Delaware Bay (Kreeger 2005a, Kreeger and Padeletti 2011, Adkins 2011, PDE 2013). Their main goal in restoring freshwater mussels is to promote improved water quality, and their Freshwater Mussel Recovery Program (PDE 2013) aims to fill vital gaps in species range information, test the restoration readiness for streams that historically held mussels but no longer do, propagate mussels in a hatchery for river reseeding, relocate and track gravid adults using electronic tags, and build conservation awareness through education and outreach programs.

The USFWS Fishery Resource Office in Annapolis, MD also is working with partners on American eel restoration in the Susquehanna River basin, which will help restore the eastern elliptios that use them as larval hosts (Lellis et al. 2013).

Strategic planning for improving water quality in the Chesapeake Bay drainage by restoring native freshwater mussels in tributaries that feed the bay will likely begin with or at least place priority on restoring the Elliptio complanata (the eastern elliptio) for the following reasons: 1) filtration capacity, 2) it remains the most stable and abundant of Chesapeake Bay basin freshwater mussels, 3) because it was historically widespread, and very abundant and 4) propagation technology exists for this species. Table 5 provides a list of all freshwater mussels that occur throughout the Chesapeake Bay drainage, and identifies the potential interest, costs and capability for producing these species of freshwater mussels to restore ecosystem services in the Chesapeake Bay drainage. The information contained in this table was collected through conversations with state malacologists, State Wildlife Action Plans, and professional knowledge of propagation technology. For each species, the table summarizes the State(s) in which they occur, whether they are in hatchery production, whether hatchery technology is being developed, the potential for producing the species, and an estimated level of investment that will be needed to propagate and stock a species. The latter two metrics are estimated as high, medium or low. The potential for producing a species incorporated knowledge of life history, expertise among facilities rearing freshwater mussels, and interest level of states and federal partners. High knowledge, high expertise, and high interest by a state equaled high potential for propagation. Medium potential was assigned if interest level by States was medium to low, and either knowledge of life history or expertise was high to medium level (i.e. technology needed some development or further development). A Low potential (for producing a mussel) was assigned if interest was low among state partners, knowledge of the life history was medium to low and expertise was high to low. Thus, interest level really influences the potential for producing a species. This is because in general, propagation technology for rearing freshwater mussels is becoming well known. In estimating the potential for propagation, we tried to balance relative interest by decision makers at state and federal level with knowledge of technology and knowledge of the life history and biology of the species. Certain species may be more difficult to work with because they are extremely rare, or knowledge of host-fish may be still be lacking. The estimate of Investment considered knowledge of the species life history and biology, ability to locate adequate broodstock and host-fish, technological knowledge of how to produce the species, and associated costs Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 49 to develop the technology. In all cases, these costs assume the basic infrastructure is in place (i.e. building, greenhouse, and plumbing). Limited knowledge of the species and technology would translate into higher investment costs.

Recommended freshwater species for restoration in the Chesapeake watershed Freshwater mussels that would be most useful in restoration efforts in non-tidal freshwater systems of the Chesapeake Bay drainage include the following 13 species: Utterbackia imbecillis, Pyganodon cataracta, Ligumia nasuta, Lasmigona subviridis, Lampsilis radiata, Lampsilis cariosa, Elliptio complanata, Elliptio lanceolata, Alasmidonta undulata and Alasmidonta varicose. An eleventh non-tidal species (Pleurobema collina, the James spinymussel) might be considered in the non-tidal areas of the James River drainage because an active propagation program is in place with the Virginia Department of Game and Inland Fisheries and the US Fish and Wildlife Service to recover this federally endangered species. Additional permitting is required to work with federally listed species. See Tables 5 and 6 for more details.

Species that would be most useful in restoration efforts in tidal freshwater systems of the Chesapeake Bay drainage include three species: Ligumia nasuta (which is on both non-tidal and tidal fresh lists), Anodonta implicata, and Leptodea ochracea (Tables 5 and 6). The recent discovery of very large and apparently healthy populations of the latter two species in the tidal Delaware River (Kreeger et al. 2013, Kreeger and Padeletti 2011) offers promise that broodstock could be used to propagate and reintroduce these species into other areas of its historic range. Table 6 lists the subset of species in Table 5 that we are recommending for restoration projects.

Pyganadon cataracta and Utterbackia imbecillis would be useful in restoration efforts because they are lentic-tolerant species, thrive in slow moving or back-channel riverine habitats, and have high potential to process large volumes of water because they are fast-growing species with large gills. In the urban areas of the tidal Delaware River, large sized P. cataracta exist in abundant, healthy beds and may contribute substantially to water filtering capacity. And with clearance rates as high as 3.4 l h-1 g−1 dtw, about half of the published rates of oysters, E. complanata is also a very good candidate for restoration.

Nearly all of the aforementioned 13 species of freshwater mussels are medium to large-sized as adults and therefore would be capable of filtering larger volumes of water (e.g. at least 1 – 3 l h-1 per individual during the growing season).Historically, these species were some of the ecological dominants of natural mussel communities (and some still are), indicating that their potential role as ecosystem engineers of aquatic (Atlantic slope) habitats was high. Indeed, freshwater mussels still occur in the mainstem rivers of the Chesapeake Bay such as the Potomac, Patuxent, Rappahannock, James, Shenandoah, Chester, Choptank, and Susquehanna, although not in large numbers nor widespread. As well, mussels occur in many of the lower order tributaries to these mainstem rivers. Stocking hatchery-reared mussels from brood stock collected in the Chesapeake Bay or translocating individuals from healthy populations of mussels such as those recently observed in the Delaware River may be viable management strategies to boost ecosystem services and restore riverine habitat directly within the Chesapeake Bay drainage.

Although not very large in size, the Alasmidonta species of freshwater mussels are of interest in restoration efforts in the Chesapeake Bay basin because they once were abundant throughout eastern Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 50

West Virginia, throughout the Piedmont of Virginia and much of Maryland (M. Ashton, MDDNR and B. Watson, VDGIF, pers. comm.). These mussels may have lower (per animal) clearance rates in comparison to larger-sized freshwater mussels; however, if one considers potential biomass and published clearance rates for similar sized freshwater mussels (0.5-1 l h-1 g−1 dtw), then their contribution to the benthic community would be significant.

As noted above in the section on choosing subtidal estuarine bivalves for restoration, planning for restoration (see below) should include a consideration of what factors are limiting populations now. Since these limiting factors are very similar for all freshwater mussel species, we did not list them in Tables 5 or 6 as we did in Table 4 for subtidal species, but we describe them here.

Within the Chesapeake Bay watershed, loss of habitat and degradation of habitat from urbanization, agriculture, damming and channelization of rivers, sedimentation, and toxic pollutant discharges into rivers reduced freshwater mussel populations to such low numbers that recruitment became limited. Populations became disconnected, and in some cases, relic populations (not recruiting) can be found above dams because dams prevented suitable fish hosts from migrating upstream. However, over the past decade, water quality and management practices have improved in many areas throughout the Atlantic slope and Chesapeake Bay watershed. We also are seeing support for removal of dams that no longer serve the needs of the community. Thus, suitable habitat is available for freshwater mussel populations to recolonize within the Chesapeake watershed. Freshwater mussels delay sexual maturity for 4 to 8 years, however, so these species can be slow to recolonize historic habitats and are at risk to a stochastic event that could eliminate local population entirely. Restoration of freshwater mussels, therefore, will likely be most successful following a population management approach involving propagation and stocking and/or translocation of individuals from dense beds within the watershed to reestablish or boost other populations. These population management actions presume, however, that mandated habitat and water quality protections are continued, and that best management practices are employed by public and private entities to conserve the health of freshwater habitats.

For current information on propagation and restoration technology, consult Mair (2013) and Morrison et al. (2013). For stream habitat quality assessments, see the National Fish Habitat Partnership (NFHP) GIS database (with maps) that contains “scores” for most streams/HUCs in the U.S. (NFHP 2014).

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Table 5. Native freshwater mussels found in the Chesapeake Bay Watershed and their potential for propagation.

Potential Facilities In Developing Hatchery Capable of Species PA NY VA WV MD DE Production Technology Production Investment Production Comments 1,2,3 Technology needs further development; Alasmidonta broodstock difficult to heterodon x x x x high high find 1,2,3 Alasmidonta Technology not marginata x x low high developed 1,2,3 Alasmidonta Technology needs 1 undulata x x x x x x high low some development 1,2,3 Technology needs some development; Alasmidonta broodstock difficult to varicosa1 x x x x x x x x high med find 1,3 Anodonta 1 implicata x x x x x high low In production 1,2,3 Anodontoides Technology not ferussacianus x x low high developed 1,2,3 Technology not developed; developing Elliptio technology for other angustata x low med species within genus 1,2,3 Elliptio Technology developed 1 complanata x x x x x x high low recently 1,2,3 Technology not developed; developing Elliptio technology for other congaraea x low med species within genus

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Potential Facilities In Developing Hatchery Capable of Species PA NY VA WV MD DE Production Technology Production Investment Production Comments 1,2,3 Technology not developed; producing Elliptio similar species (E. fisheriana x x x x x high med lanceolata) 1,2,3 Technology not developed ; producing similar species (E. Elliptio icterina x med med lanceolata) 1,2,3 Elliptio 1 lanceolata x x high low In production 1,2,3 Technology not developed; producing Elliptio similar species (E. producta x x x high med lanceolata) Elliptio 1,2 Technology not roanokensis x x low high developed 1, 2 Technology needs some development; Fusconaia broodstock difficult to masoni x x high med find Lampsilis 1,2,3 2 cardium x x x x high low In production Lampsilis 1,2,3 1 cariosa x x x x x x x high low In production Lampsilis 1,2,3 1 radiata x x x x x x x high low In production Lasmigona 2 Technology not compressa x low high developed Lasmigona 1,2 Technology needs 1 subviridis x x x x x x high low some development Leptodea 1,2,3 1 ochracea x x x x high low In production

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Potential Facilities In Developing Hatchery Capable of Species PA NY VA WV MD DE Production Technology Production Investment Production Comments Ligumia 1,2,3 1 nasuta x x x x x high low In production Margaritifera 1,2,3 Technology not margaritifera x high high developed Pleurobema 2 Technology recently 1 collina x high low developed Pyganodon 1,2,3 1 cataracta x x x x x x high low In production Pyganodon 1,2,3 Technology needs grandis x x x med med further development Strophitus 1,2,3 Technology needs undulatus x x x x x x x med med further development Utterbackia 1 1 imbecillis x x x x high low In production

1These 13 species are also listed in Table 6 as species we are recommending for consideration for restoration projects. 2Lampsilis cardium is not native to Chesapeake watershed, and was likely introduced as result of recreational fish stocking in rivers in the 1980s. This species has become well established in certain tributaries to the Chesapeake Bay. State biologists are not in agreement whether to consider this species for any bivalve restoration effort. We include the species in this table only to provide a comprehensive list of freshwater mussels present in the Chesapeake watershed, and for which we have some working knowledge of propagation and ecology of the species.

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I. Potential Hatchery Production Assumptions: Interest level refers to interest by natural resource agencies. high = high interest, high knowledge and expertise; med = medium to low interest, high to medium knowledge, high to medium expertise; and low = low interest, medium to low knowledge, high to low expertise

II. Investment Assumptions: Infrastructure is in place for hatchery production. Costs are estimated for labor (broodstock and host species collection, and hatchery production) and specialty equipment that could be incurred in year one to develop propagation and/or implement production. Annual costs would decline as knowledge and capability increased for production of a species, and could be less per species, if multiple species are in production. High = >$100,000; Med = $50,000-100,000; Low = < $50,000.

III. Capability Assumptions: Expertise available, infrastructure available, proximity to broodstock and host fish, strength of partnerships. The facilities are: 1) Fisheries and Aquatic Wildlife Center of the Virginia Department of Game and Inland Fisheries, located at the Harrison Lake National Fish Hatchery, Charles City, VA 2) Aquatic Resource Recovery Center at the White Sulphur Springs National Fish Hatchery, White Sulphur Springs, WV 3) Conservation Aquaculture Center of the North Carolina State University and North Carolina Wildlife Resource Commission

Table 6. Thirteen species of freshwater mussels found in the Chesapeake Bay Watershed that are good candidates for restoration projects. See Table 5 for more details on potential for propagation of each species.

Species Common name In Developing Potential Investment Best use Production Technology Hatchery needed (Freshwater Production or Tidal Fresh) Alasmidonta triangle floater x high low FW undulata

Alasmidonta brook floater x x high med FW varicosa

Anodonta alewife floater x x high low TF implicata

Elliptio eastern elliptio x high low FW complanata1

Elliptio yellow lance x high low FW lanceolata

Lampsilis yellow lampmussel x high low FW cariosa Lampsilis eastern x high low FW radiata lampmussel Lasmigona green floater x high low FW subviridis Leptodea tidewater mucket x high low TF ochracea

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Species Common name In Developing Potential Investment Best use Production Technology Hatchery needed (Freshwater Production or Tidal Fresh) Ligumia eastern x high low Both nasuta pondmussel Pleurobema James spinymussel x high low FW collina Pyganodon eastern floater x high low FW cataracta Utterbackia paper pondshell x high low FW imbecillis

1 Clearance rates have been measured for this species; see Tables 2 and 3.

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DEVELOPING A BIVALVE RESTORATION STRATEGY AND ESTIMATING ECOSYSTEM SERVICES A holistic, watershed-wide strategy is recommended for restoring bivalve populations to in turn help maintain and enhance water quality. Each candidate restoration species has unique habitat requirements and environmental tolerance limits for conditions such as salinity, dissolved oxygen, and substrate. The different niches occupied by the species reviewed here, from headwaters to mouth of the bay, represent opportunities to build a diversified approach to restored water quality along the river to bay continuum. The initial selection of suitable species to target for restoration should therefore consider additional information not fully reviewed here, such as the nexus between current and potential species ranges and spatial variation in water quality remediation needs.

Ideally, five basic pieces of scientific information are required to develop a rigorous predictive understanding of the net water quality outcomes from bivalve restoration, which are summarized as the following steps. Once those five steps are in place, the sixth step in bivalve restoration to improve water quality is to find sources for the target bivalve species, or determine propagation methods if no sources are available. In areas that are impaired, an interim step (#7) might be warranted to test and prioritize streams/tributaries for their “restoration readiness.” The final step (#8) is to stock juvenile bivalves or relocate adult bivalves to target streams or tidal waters.

These steps are listed here, with further descriptions below:

1. Obtain empirical data on weight-specific clearance rates by target species (this review) 2. Obtain a quantitative appraisal of current population abundance, size distribution and geographic distribution of target species 3. Develop an understanding and model of the hydrodynamics and movement of pollutants of interest through the system in relation to the geospatial distribution of bivalve populations 4. Develop a quantitative understanding of the fate of filtered matter 5. Develop a model of the current system’s carrying capacity for the target species of bivalves 6. Find sources for targeted bivalve species, or determine propagation methods if no sources are available 7. For impaired waters, use relocation or caging studies to test and rank restoration suitability 8. Start restoration, by propagating and stocking juvenile bivalves and/or relocated adult bivalves to target streams or tidal waters.

First step: obtain empirical data on weight-specific clearance and filtration rates by target species To estimate whether bivalve restoration can help remediate water quality at the ecosystem level, the first step is to obtain empirical data on weight-specific filtration and clearance rates by target species. This assumes that the most promising target species have already been chosen. In early stages, the target species list should include all reasonable candidates, since it’s much easier to drop than to add them later. Getting filtration and clearance rate data requires an understanding of their physiological ecology because physiological processing rates vary among species, seasons, and with nutritional and

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 57 environmental conditions. As discussed in the preceding sections, there are various methods for measuring filtration and clearance rates that can bias or thwart inter-comparability of results (e.g., use of laboratory versus natural diets ), and for estimating ecosystem services we recommend that future studies deliver natural diets at ambient temperatures and simulating natural conditions expected in targeted restoration areas (tidal regime, substrate, etc.). Since filtration and clearance rates also vary with age and body size, measurements should be weight-adjusted using allometric relationships for standard-sized animals that best represent the wild population.

Second step: appraisal of current population abundance and size distribution The second step for scaling up ecosystem service estimates is to obtain a quantitative appraisal of current population abundance and size distribution, and factors that limit its abundance and distribution. Populations of most noncommercial species are not routinely monitored, and recent survey data can be difficult to obtain. For example, the last comprehensive survey of freshwater mussel distribution in Pennsylvania (for which data can be obtained freely) was conducted about 100 years ago (Ortmann 1919). Populations of freshwater mussels are patchy and logistically challenging to assess quantitatively, and their restoration will require a better understanding of the habitat, water and food conditions needed (Strayer 2008). Indeed, it is critical that up to date survey data be readily available via GIS or other means for scientists and managers to develop best management plans and strategies to meet the goals of restoring populations and ecosystems.

In Chesapeake Bay, which has decades of monitoring data collected by the Chesapeake Bay Program, there are reasonably complete data on soft-bottom benthos (including bivalves) in deeper tidal waters from the Chesapeake Bay Benthic Monitoring Program (Versar 2011), but abundance and distribution data are much more limited for bivalves on hard bottom (limited to annual oyster surveys) and almost no data exist for bivalves living in shallow water or intertidal marsh edges. Non-tidal bivalves are sampled at sites in Maryland by the MD Biological Stream Survey (MBSS 2011), but non-tidal benthic sampling in other states in the watershed (WV, VA, PA, NY, and DE) is more limited. After population demographics are assessed, these data can be paired with allometric and seasonal estimates of bivalve filtration (and other rate functions, from step 1) to obtain first order mass balance estimates for water processing potential at today’s populations.

Third step: model the movement of water and associated pollutants To develop more advanced estimates of actual water processing by bivalve populations, the third step is to develop an understanding and model of the hydrodynamics and movement of water and associated pollutants of interest (including food for the bivalves) through the system in relation to the geospatial distribution of bivalve populations (Dame 1996, Wildish and Kristmanson 1997). Systems that have greater residence times of water over bivalve populations allow more time for water to be filtered (and re-filtered), resulting in comparatively higher net pollutant removal efficiency. In contrast, high flows, short residence times, and patchy bivalve populations might limit the interception of pollutants via bivalve filtration.

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Fourth step: develop a quantitative understanding of the fate of filtered matter The capture of suspended matter through bivalve filtration is not necessarily a pollutant sink, and so the fourth step in assessing water quality services by bivalves is to develop a quantitative understanding of the fate of filtered matter. Much of the filtered material is of poor nutritional value and will be bound in mucous and rejected as either feces or pseudofeces – collectively referred to as biodeposits. Since these biodeposits tend to sink, bivalve filtration does tend to result in clearer water with direct light availability enhancement to benefit bottom producers. The biodeposits can get buried, resulting in a net ecological sink; however, as discussed in the background section above they can also be ingested or degraded by benthic and microbial organisms or be returned to the ecosystem via remineralizers (Newell et al. 2005). The bivalves themselves also remineralize nutrients by excreting dissolved ammonium and phosphate ions. Additionally, bivalves feed and digest adaptively, leading to variable physiological processing rates (filtration, absorption, assimilation, respiration, excretion) with changes in seasonal or ontogenetic nutritional demands and diet composition, leading to varying rates of biodeposition and nutrient excretion. For example, tidal mussels can increase nitrogen assimilation 8- fold and curtail ammonia excretion when protein demands are not being met (Kreeger et al. 1995).

Developing a better understanding the ecological fate of ingested matter under differing conditions would therefore strengthen our understanding of the net environmental benefits of bivalve feeding for water quality. Use of stable isotopic tracers and other new methods can also boost our understanding of how much anthropogenic, allochthonous sources of pollutants can be accumulated in both non-tidal and tidal bivalve populations (e.g., for nutrient retention, see Valiela et al. 1997, McKinney et al. 2001, 2002).

Fifth step: develop a model of the current system’s carrying capacity for the target species of bivalves The fifth step is to develop a model of the current system’s carrying capacity for the target species of bivalves. In some cases, this might be best estimated from data on historic ranges and population abundances. However, in most cases changing conditions have curtailed or shifted the location and extent of suitable habitats. For example, some streams and rivers may no longer be suitable for freshwater mussels due to degraded water and habitat quality. Some cold-adapted species may shift northward with warming climate. Increasing rates of sea level rise threaten tidal marshes that are home to intertidal G. demissa. To ensure that resources are invested strategically in sustainable places and species, predicted trajectories of climate change and continued watershed development should be considered in developing best possible estimates of future carrying capacity, which is likely to be different than current carrying capacity. In some cases (e.g. freshwater mussels), assisted migration might be needed for southern species to move northward if ecological services are to be sustained.

Development of a GIS database of likely current and future suitable habitat for various bivalve species will provide a first order framework for considering carrying capacity. This habitat layer should then be tempered by geospatial information on impediments or constraints on natural populations. Examples of potential density-dependent factors to be considered in carrying capacity estimates are disease prevalence (e.g. C. virginica), dams that impede fish hosts, suboptimal water quality, susceptibility to

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 59 predators, vulnerability to frequent disturbances (e.g. spills), and the presence of toxic levels of contaminants. In addition to ecological carrying capacity, this is also the step where logistical and political considerations should be weighed. These could include habitat tradeoff concerns by fisheries groups, aesthetic concerns by homeowners, and development restriction concerns if protected species are restored.

Sixth step: find sources for the target bivalve species, or determine propagation methods if no sources are available The sixth step is to find sources for the target bivalve species, or determine propagation methods if no sources are available (mainly needed for freshwater mussels). Some who prefer action will be tempted to skip right to Step 6, but doing so may lead to unsuccessful projects that could in turn jeopardize support for future bivalve restoration efforts, such as if the wrong species, growing locations, and/or number of individuals is used. An understanding of the whole ecological and political context, laid out in steps 1-5 above, would significantly boost outcomes by providing for strategic planning and targeting in the restoration design as well as facilitating post-restoration analysis and understanding of why any restoration attempts succeeded or failed. If no suitable source for a target species can be found in the drainage areas, it might be necessary to (re)introduce the species from the nearest possible source; however the consensus scientific view is that this should be a last resort due to potential genetic concerns. Interstate transfer of most native tidal bivalves are allowed with a permit. Interstate and interbasin transfers of freshwater mussel species are strictly regulated. Some transfers are allowed with a permit, which involved close collaboration with States, good communication on goals and objectives, and justifiable explanation of projected outcomes.

Seventh step: optional test to gauge restoration suitability If there is uncertainty of whether a candidate restoration species will survive and prosper in a specific habitat, due perhaps to past impairment, the seventh step represents an optional test to gauge restoration suitability. There are many case studies showing the effectiveness of relocating caged or tagged bivalves into prospective restoration areas and then monitoring their fitness for a period of time relative to control (source) locations. Waters that support the greatest fitness or growth are then prioritized for restoration, thereby strengthening the chances for successful restoration leading to self- sustaining populations. Comparative studies of suitable bottom habitat are also helpful for the same reason.

Eighth step: Restoration Lastly, the eighth step consists of actual restoration. There are myriad ways to both conserve and restore bivalve populations, and this review does not attempt to review these tactics. In general, however, one of the simplest approaches is to manage and restore the habitat needed by bivalves, including such activities as shell planting for oysters, salt marsh erosion control for G. demissa, and dam removals and stormwater controls for freshwater mussels. In cases where new habitat is created or past disturbances are removed, bivalves can be reintroduced through straightforward transplanting, and this is especially important where natural dispersal is impeded. Finally, we now have the technology to propagate almost all native species in hatcheries, and so we can reintroduce species, expand species

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 60 ranges, and boost natural populations by seeding juvenile bivalves that are bred and raised in hatcheries, with appropriate genetic conservation protocols.

POSSIBLE IMPEDIMENTS TO THE IMPLEMENTATION OF BIVALVE RESTORATION FOR ECOSYSTEM SERVICES

Science Needs There are a number of reasons why efforts to restore bivalves to enhance ecosystem services are just getting started. Despite the clear evidence that oscillations in bivalve populations elicit dramatic changes in water quality at the system scale (reviewed above), there remains some skepticism that the benefits of bivalve restoration will outweigh the costs. Furthermore, funding for environmental restoration is getting tighter and funders are increasingly requesting scientifically rigorous, quantitative predictions for the expected ecosystem benefits.

To do this well, we need to develop a more comprehensive understanding of the current range, physiological ecology, carrying capacity, and predicted functional benefits of noncommercial bivalves (steps 1-5 above) to make the case that investments are warranted. However, funding to fill these knowledge gaps has been nearly impossible to obtain by the research community because these species have not been valued as much as commercial species. Despite more than 100 years of scientific study of bivalves (particularly commercial species), this understanding is not yet mature because most physiological studies have used non-natural diets and culture systems because the intent was to optimize aquaculture or shellfishery outcomes rather than environmental benefits. The field of marine physiological ecology advanced in the 1960s-90s, followed by increasing attention to ecosystem-level effects in the 1990s-2000s. For freshwater and non-commercial species, research funding for physiological ecology and ecosystem effects remains difficult to this day. There is also considerable inconsistency in methods and units due to the varied research purposes. Therefore, much of the essential empirical information on organism-level and ecosystem-level processing has yet to be fully discovered in order to develop a rigorous and predictive understanding of ecosystem services by bivalves

As a result, a fundamental barrier to development of projects to enhance water quality with these noncommercial species is getting funding to perform scientific studies and to initiate and monitor pilot restoration projects. For example, it will be important to develop a more predictive understanding of post-capture physiological processing rates and net ecological fates of matter that is filtered by noncommercial species. Factoring these post-capture processes into calculations of services can become complicated. For example, Galimany et al. (2011) measured filtration rates in the Mediterranean mussel Mytilus galloprovincialis in Spain, and found that several feeding parameters (including clearance rate and absorption rate) varied greatly both among days and among seasons, with lower summer rates possibly caused by high temperatures. The literature is full of similar observations (e.g. Bayne and Newell 1983 [tidal mussels], Kreeger and Newell 2001 [G. demissa], Langdon and Newell 1996 [C.

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 61 virginica], Kreeger 2011 [freshwater mussels]. Bivalves are extremely adaptable organisms that need to satisfy changing nutritional demands from an ever-changing diet. Despite this complexity, rigorous predictive models can easily be developed for each target species if sufficient empirical evidence is obtained to parameterize the models. The main variables are season (temperature), natural diet quantity, natural diet quality, and general estuary/stream location (salinity zones, etc.). With this information, seasonal and nutritional effects can be captured, thus developing an annual estimate of ecosystem services for a particular species in a general river or estuary location.

Human Health /Competition with Commercial Aquaculture Impediments to quantifying bivalve ecosystem services also include usage and management conflicts. In 2010, the State of New Jersey enacted a ban on restoration of commercial (edible) species of shellfish, forcing some restored oysters reefs to be eradicated (New Jersey Baykeeper 2011). This policy is designed to protect both the public health and the oyster shellfishery by ensuring that no one gets sick from eating tainted animals from restoration sites or from oyster gardening projects. However, similar public health concerns over elevated bacteria and/or toxin levels extend to the species of bivalves not usually harvested or grown for human consumption that are raised in restricted waters. The public health problem is that some people will eat almost any free shellfish regardless of the species or where they got it, as long as it looks more or less like an edible species. For example, R. cuneata are eaten in Mexico and other areas and look quite similar to the hard clams sold as food, and Corbicula sp. are used in some Asian cooking. . Having an odd, musky, or dirt-like flavor does not seem to deter some consumers of wild-caught shellfish. In a sense, the main issue here is the limits of the responsibility of public health agencies to protect consumers from themselves. However, freshwater mussels are not a typical food source for humans (and should never be because of risks from parasites and pathogens).

Potential conflicts with raising shellfish for food could occur when the same hatcheries, cultch materials, and/or grow-out facilities are used for bivalves grown primarily for food and those grown primarily for ecosystem services. There are also potential conflicts if bivalves that are considered a harmful fouling species on C. virginica, such as I. recurvum, were cultured for their water quality and habitat benefits. Harmful fouling on C. virginica from such bivalve restoration could be minimized by growing out the I. recurvum in areas which currently have few C. virginica or I. recurvum (see below).

While bivalves raised in aquaculture provide interim services while they are growing, they are usually harvested as soon as this is profitable, which limits how long they can provide services. The two goals can be compatible in some situations, for example if growers are paid to leave their bivalves in the water for another year after they could be harvested to enhance the ecosystem services they provide, such as habitat, filtration, and spat for nearby wild populations. This is being considered for scallops in Rhode Island (D. Alves, pers. comm.)

Some aquaculture experts have argued that only bivalves that are raised in commercial aquaculture (and thus for food) can be raised in enough quantity to provide significant ecological services, so this conflict may be hard to avoid. Since most efforts to propagate and raise bivalves are to supply seed for aquaculture or to augment stocks for harvest, there is also a need for more research and development to grow “restoration aquaculture” of both commercial (edible) and noncommercial species.

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Public Perception/Education Traditional management paradigms and policies at federal, state and local levels generally fail to recognize the habitat and water quality benefits of restored bivalve populations (and the risk to water quality of continuing to lose natural stocks). Public interest in noncommercial species is also currently low, but only because of lack of awareness. Once educated about the importance of these animals, the public tends to quickly become interested and supportive. Bivalves offer a wealth of outreach opportunities due to the sessile nature of the animals (e.g., they can be tended in “gardens”) and the clear water quality benefits that are conveyed by simple aquarium demonstrations.

Funding Finally, perhaps the most important impediment to advancing bivalve restoration for ecosystem services is the difficulty obtaining funding for projects, including basic physiological and ecological research and pilot projects to monitor outcomes (see above). Being able to quantify ecosystems services from bivalve restoration is important both to justify the money spent on it, and also to calculate any payments that may result from it.

Despite these challenges and impediments, most are solvable and the methods and scientific prowess currently exists in the mid-Atlantic region to quantify bivalve services. Propagation technology is well understood for oysters, clams, tidal mussels, and even freshwater mussels, which grow slowly and have a convoluted life history strategy. The only major hurdle is funding to optimize culture and reintroduction methodologies (e.g. G. demissa and freshwater mussels) and to more directly quantify core ecosystem services with ecophysiological and modeling studies. Formation of an interdisciplinary technical workgroup comprised of culture specialists, physiological ecologists, economists, and hydrodynamics specialists could tackle these needs efficiently.

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RECOMMENDATIONS Some resource managers view the use of top-down controls on nutrients, such as bivalve enhancement, as an admission that traditional source control methods have failed. We do not advocate abandoning traditional management methods in favor of a program focused on top-down approaches. Bivalve restoration is an ideal complement to existing nutrient reduction programs, providing water quality benefits with the bonus of additional ecosystem services such as habitat and species restoration.

The restoration of bivalves provides diverse ecosystem services. They can help to stabilize erosion of stream bottoms and vulnerable marshes and enrich habitat for other fauna and flora (especially fish). A watershed-wide approach to restoring bivalves could also provide synergistic positive feedbacks because the restoration of freshwater mussel beds in non-tidal areas can benefit tidal shellfish through water quality enhancement, whereas restored shellfish reefs and mussel beds in estuaries might aid diadromous fish which might later serve as hosts for freshwater mussels.

The current ecosystem management relies on older restoration methods that can limit the acceptance of bivalve restoration as a restoration practice that is worth funding. In some cases, outdated management paradigms (e.g. restoration only to historic conditions or on historic reefs) may also hinder our ability to adapt to the changing climate due to shifting species ranges with temperature and salinity rise. In addition, nutrient trading credits, which could help to fund restoration, are usually limited to treatments that are done before wastes are discharged into a receiving water body, not after discharge, which often rules out traditional credits for bivalves. Therefore, it will be necessary for management policies and practices to evolve to best capitalize on ecosystem service based restoration.

Recommendations:

1. Develop a watershed-wide restoration strategy for noncommercial bivalve species to augment oyster restoration efforts for water quality remediation.  Prioritize ecologically significant, native species with high promise for restoration (see recommendations above)  Include representative freshwater, brackish, and saltwater species  Select pilot project sites in non-tidal, intertidal, and subtidal tidal waters of each state  Coordinate between Chesapeake and Delaware Estuaries to maximize efficiency (same species and challenges, synergistic expertise, for example see PDE 2013)

2. Fund research and development to fill vital knowledge gaps (as per steps 1-6 above) and standardize methods.  Deduce current species ranges and potential carrying capacity for target species  Quantify core physiological rate functions for target species and ecological fates of filtered matter under expected natural conditions  Model potential water quality benefits of target species at pilot restoration project sites  Fund research and development to fill vital knowledge gaps (as per steps 1-6 above) and standardize methods.

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3. Form a noncommercial bivalve restoration task force consisting of scientists and managers to prepare and guide implementation of the strategy.  A task force policy subgroup should identify and work to overcome operational impediments, such as permitting.  A task force technical subgroup consisting of experts should identify and fill knowledge gaps, provide pilot project specifications, and oversee implementation and monitoring of pilot projects  A task force outreach subgroup should work to educate the public about the importance of noncommercial bivalves and build awareness for their conservation and restoration.  The task force should include representatives from both the Chesapeake and Delaware River Basins, which share most of the same challenges, opportunities and Atlantic slope bivalve species.

4. Adaptively manage the strategy.  Work swiftly to implement pilot projects in small areas using best scientific judgment, and include rigorous monitoring  Modify strategy every two years to make adjustments for lessons learned from monitoring of pilot projects and the broader scientific literature.

ACKNOWLEDGMENTS Thanks to people who reviewed most of the document in earlier drafts: Vic Kennedy (UMCES Horn Point Lab) and Julie Rose (Milford Science Center, NOAA NMFS) for reviewing the sections on estuarine species, Matt Ashton (MD DNR) for reviewing the sections on freshwater mussels, and two anonymous reviewers. Thanks also to Rachel Mair (USFWS) and Brian Watson (Virginia Department of Game and Inland Fisheries) for providing valuable input on Table 5, and reviewing sections on freshwater mussel conservation. Thanks to Keryn Gedan (formerly at SERC, now at the University of MD) for providing unpublished estimates of clearance rates for hooked mussels that we used in Table 2. Thanks to Mitch Tarnowski and Frank Marenghi, MD DNR Shellfish Program, for providing and explaining the original oyster survey data sheets that we used for the occurrence maps in Appendix A for hard bottom species, and to Eric May, University of Maryland Eastern Shore, for arranging for his summer interns to enter most of the data we used from those data sheets. Thanks to Jackie Johnson, formerly with ICPRB at the Chesapeake Bay Program, for making the occurrence maps in Appendix A, including the maps of soft bottom species in the same Appendix, with data provided by Bergstrom. Thanks to LeeAnn Haaf (Partnership for the Delaware Estuary) for enhancing the graphics in Appendix A. Finally, we are grateful to Sally Hornor (Anne Arundel Community College) and Dick Carey and Paul Spadaro (Magothy River Association) for doing dark false mussel surveys in 2004 and 2005 during the Magothy River irruption of that species.

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GLOSSARY afdw: Ash free dry weight, measured by weight loss on ignition, using temperatures high enough to burn any organic carbon. allochthonous: Materials that originated in a different ecosystem. allometric: pertaining to the change in proportion of different parts of an animal as it grows. In this review, it refers to how clearance or filtration rates change with body size. bioassessment: Short for biological assessment. It involves using biota (plants or animals) to assess the prevalence of pollution, or the condition of a water body or other habitat. biodeposits: material moved from the water column to the bottom. For bivalves these may include feces and pseudofeces. bioextraction: A method of pollution reduction in which plants (often algae) or animals (often bivalves) are grown and periodically removed from the ecosystem to remove pollutants that they contain, such as nutrients. biofiltration: using biota to reduce pollution; in this review, the potential for bivalve filtration to improve water quality. biofouling: Plants or animals growing on surfaces where they are detrimental, usually to human uses. Examples include zebra mussels clogging water intake pipes, or barnacles growing on ship hulls, slowing the ship down. bivalves: a class of marine and freshwater mollusks with two shells (valves), most of which are filter feeders. blackwater estuaries: Estuaries with water stained dark by tannins from decaying plant material. byssal thread: Used by some bivalves, such as blue mussels, to attach their shells to hard substrates. They are excreted by the byssal gland. cellulases: enzymes for digesting cellulose.

Chl a: Chlorophyll a concentration in water, a measure of the amount of algae in the water. clearance rate: volume of water cleared of particles per unit time. Easier to measure than filtration rate, but less relevant to the ecological impacts of bivalves. denitrifying bacteria: bacteria that can metabolize nitrate compounds and release nitrogen gas, under anaerobic conditions in sediments. diadromous: refers to all fish that migrate between fresh and salt water to spawn, thus including both anadromous and catadromous fish.

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 81 dtw: Dry tissue weight. The body of the organism is usually dissected out of its shell, then dried at 60 C to constant weight. This is usually the basis of weight-specific clearance rates, unless “afdw” is noted. Dtw will be higher than afdw.

EO: Executive Order, by a US president to one or more agencies. This review was written in response to EO 13508, “Chesapeake Bay Protection and Restoration” from 2009. eutrophication: A harmful condition in water bodies caused by adding too many nutrients, especially phosphate. The nutrients trigger algae blooms, which cause hypoxia when the algae die and decompose, and the algae also cloud the water, reducing light for submerged plants. filtration rate: biomass of particles that is removed per unit time. Filtration rate is more relevant to ecological impacts, but it is much harder to measure. hypoxia: condition of a water body that does not contain enough dissolved oxygen to fully support its usual aquatic life. Usually defined as having from between 1 and 30% saturation of oxygen; waters with < 1% saturation are called anoxic. intertidal: living in the zone between low and high tide. See subtidal. irruption: a relatively fast but short-lived increase in the local population of an animal species. macroalgae: Multicellular algae, such as kelp. macroinvertebrates: The larger invertebrates living in non-tidal streams, generally not including bivalves. Used as an indicator of stream health (an example of bioassessment). macrophytes: multi-cellular aquatic plants, including submerged aquatic vegetation, for example wild celery, Vallisneria americana. macrotidal: estuaries or coasts with high tidal ranges (generally over 4 m);. Tidal currents are generally more important than waves on macrotidal coasts or estuaries. The Bay of Fundy is an example. malacologist: biologist who studies mollusks. mesocosm: An experimental aquatic chamber of medium size, larger than a microcosm and smaller than a macrocosm. It is generally small enough to allow room for enough replicates for all of the experimental conditions, while being large enough to mimic natural conditions. mesohaline: estuarine salinity zone of medium salinity, usually from 5-18. mesotidal: estuaries or coasts with medium tidal ranges (generally 2-4 m). Most of the other estuaries on the east coast of the US are mesotidal, for example in New Jersey, South Carolina, and Georgia.. microtidal: estuaries or coasts with low tidal ranges (generally less than 2 m). Their intertidal zones are thus smaller in area than those along macrotidal or mesotidal coasts, and they tend to be wave dominated. Most of Chesapeake Bay is microtidal, except near the heads of tide in major rivers.

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NMFS: National Marine Fisheries Service, also known as NOAA Fisheries.

NOAA: National Oceanic and Atmospheric Administration, part of the Department of Commerce.

Non-tidal: waters with no tidal variation in water level. oligohaline: estuarine salinity zone of the second lowest salinity, usually from 0.5 to 5. periphyton: benthic algae that grow on submerged surfaces; it may also contain bacteria and other microbes. It is an important food source for small consumers. piscivorous: animals that eat fish. plankton: small plants (phytoplankton) and animals (zooplankton) that float in water with limited mobility. planktivorous: Animals that eat plankton. polyhaline: estuarine salinity zone of high salinity, usually over 18.protists: eukaryotic microorganisms; most are unicellular. Some resemble plants (algae), some fungi, and some animals (protozoans). Some authors classify them by how they obtain energy. pseudofeces: particles ejected from bivalve gills, either because they were rejected as food while eating, or because the bivalve is filtering water for gas exchange, but not eating. remineralization: process by which nutrients are transformed from particulate to dissolved forms. salinity: describes the salt content of water; expressed in Practical Salinity Units (PSU) which are a ratio, so they have no units. seagrass: submerged macrophytes living in higher salinity, generally at the upper end of the mesohaline zone, and in the polyhaline zone (salinity over 18). seston: Solids suspended in the water column, which usually have both inorganic and organic components. subtidal: Living below the low tide line. See intertidal. tidal fresh: estuarine salinity zone of the lowest salinity, usually from 0 to 0.5.

USFWS: United States Fish and Wildlife Service, part of the Department of the Interior.

Unionid: refers to freshwater mussels in the family Unionidae.

Kreeger, Gatenby and Bergstrom, PDE Report No. 17-05 Page 83 water clarity: one of the aspects of water quality that can be improved by bivalve filtration. Organic and inorganic particles suspended in water reduce water clarity, and they may be removed by filtration.

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(see separate appendix file)

Appendix A. Maps of recent distribution of selected bivalve species in Chesapeake Bay.

A.1. Brackish water clam (Rangia cuneata), soft bottom (all years with random data).

A-2. Soft‐shell clam (Mya arenaria), soft bottom (1990 onward).

A-3. Ribbed mussel (Geukensia demissa), soft bottom (1990 onward).

A-4.Hooked (bent) mussel (Ischadium recurvum), hard bottom, 2009 (most recent data). From MD fall oyster survey.

A-5. Dark false mussel (Mytilopsis leucophaeata), hard bottom, 2009 (most recent data). From MD fall oyster survey.

A-6. Stout razor clam (Tagelus plebeius), soft bottom (1990 onward).

Appendix B. Box plots of density and line graphs of % occurrence by species by year (CBP benthic data).

B-1. Asian clam (Corbicula fluminea)

B-2. Brackish water clam (Rangia cuneata)

B-3. Dark false mussel (Mytilopsis leucophaeata)

B-4. Baltic macoma clam (Macoma balthica)

B-5. Soft-shell clam (Mya arenaria)

B-6. Ribbed mussel (Geukensia demissa)

B-7. Stout razor clam (Tagelus plebeius)

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