Council of Governments Meeting August 3, 2021

SUBJECT PRESENTATION ON BIVALVE INITIATIVE: “ALL CLAMS ON DECK - RESTORING ESTUARIES AND GROWING COASTAL ECONOMIES”

Category AGENDA ITEMS

Briefings None

Contact and/or Presenter Information Mayor John Chappie, City of Bradenton Beach Ed Chiles, Chiles Group

Presenter: Jeff Sedacca

Action Requested None

Enabling/Regulating Authority

Background Discussion A presentation will be made on the Gulfcoast Restoration Initiative, All Clams on Deck - Restoring Estuaries and Growing Coastal Economies.

Attorney Review Not Reviewed (No apparent legal issues)

Instructions to Board Records None

Cost and Funds Source Account Number and Name N/A

Amount and Frequency of Recurring Costs N/A GULF COAST RESTORATION INITIATIVE

Ed Chiles

Affiliates: Gulf Shellfish Institute, Sea & Shoreline Aquatic Restoration, Solutions to Avoid Red Tide (START), Sunnyvale Seafood Company (SSC) ALL CLAMS ON DECK: GETTING ON BOARD TO RESTORE FLORIDA'S ESTUARIES • Paradise under pressure: • Development, Pollution, Runoff • Storms & Hurricanes • Harmful Algal Blooms • Economic consequences • Coastal communities • Commercial and Recreational Fisheries • Florida tourism

Photo credit: Capt. Scott Moore BIOLOGICAL MITIGATION STRATEGIES: USING NATURE’S TOOLBOXAquacultured Seagrass & Hard Clams

FEDERAL FUNDING & FLORIDA LEGISLATION

• $15 M will support proof of concept to research and promote large-scale restoration efforts in 3 National Estuaries • Seagrass restoration & Hard clam deployment • Tampa Bay, Sarasota Bay, Charlotte Harbor

• Florida Governor and Legislative Ask • Certify bivalves for mitigation credits and create legislation that provides avenue to proceed • Increase mitigation tools available • Increase capacity of Florida’s shellfish aquaculture industry IT’S TIME TO ACT.

Website coming soon: AllClamsOnDeck.org Diatom Initiative Seagrass and Bivalve Restoration Florida has the largest coastal environment in the continental . This coastline hosts the majority of our population, jobs, wealth, recreation and tourism. One of, perhaps the greatest threat to our coastal environment, and all it supports, are excessive nutrients, primarily nitrogen.

Nitrogen nourishes microalgae blooms which we all see in the form of green and brown water as we drive boats or step into the ocean. Excessive nitrogen loads can, and do cause excessive blooms, disturbing the natural balance of the estuarine, and ocean biomes. One of the potential effects of excessive nutrients may be prolonged and larger algal blooms, which may include Red Tide events. Most of the microalgae species are necessary components of a healthy marine environment, as long as they are in balance. However, excessive blooms of all kinds of algae are an existential threat. These microalgae, when in excess, shade our coastal environments, stunting our fish nursery/seagrass beds. Excessive algae and nutrients create dead or crippled marine environments and cause marine mammal and fish mortalities. In proper balance, microalgae are the cleaners of the ocean and they exist everywhere, in every corner, temperature and salinity. Once they get too thick in the water column, they shade not only the seagrasses, and corals, but they also shade themselves. Overly shaded algal biomasses do not receive sufficient sunlight to survive. They stagnate and die, fouling the marine environment, and no longer filtering and cleaning the water.

The simple solution is to remove the excess microalgae, which will allow it to grow at a balanced, sustainable rate, and do what it does best, consume and sequester excess nutrients, which it does better than anything else. Just as microalgae are the best cleaners of the ocean, bivalves are the best at filtering, and consuming, microalgae and consequently and sequestering the excess nutrients. Bivalves deposit the nutrients into the marine substrate, where they become a nutritional source for marine grasses, and mangroves. The Chesapeake Bay is leading with this strategy, in which oyster aquaculture and restoration activities are applied as BMPs for reducing the Chesapeake Bay Total Maximum Daily Loads (TMDL).

Preservation and restoration of our coastal environment, our greatest natural asset, development of sustainable aquaculture businesses and jobs, saving commercial and recreational fisheries for the future, controlling and reducing algal blooms including possibly red tide, preserving the basis of our tourism industry (the key to keeping us from implementing a State income tax) can be addressed in large part by restoring bivalve populations to our estuaries and inshore waters. Naming bivalves, clams and oysters, as mitigation products, just like mangroves and seagrasses, would be instrumental in the development of a comprehensive restoration project.

Sustainable bivalve aquaculture and restoration are not a zero sum game, as is so much development. Bivalve aquaculture is unique in that not only does it not require expensive mitigation to prevent negative environmental impact, it has an immediate, quantifiable positive impact by its very nature.

Notes:

High densities of filter feeding organisms (like clams and oysters) enhance water quality by: -removing nutrients (like Nitrogen), -eating over abundant phytoplankton (algae) -increasing water clarity, and -enhancing seagrass growth

The ecosystem services provided by these organisms make them ideal candidates for use in restoration and water quality mitigation projects.

The goal would be to establish a legal framework in Florida that would use sound science to make it legally feasible for clams, oysters (and potentially other filtering organisms) to be utilized for environmental mitigation and/or nutrient trading and management.

This would invigorate existing aquaculture and restoration efforts that are ongoing in Florida, providing incentive for these industries to expand.

Increased capacity and market for these products, which are produced by small business owners throughout the state, would stimulate coastal economies and working waterfronts. brief compiled by Jeff from notes, and comments provided by: Angela Collins/Florida SeaGrant Curtis Hemmel/ Bay Shellfish AU Abo1at Florida I

2021 Policy Proposals •BROADBAND SUPPORT increased efforts to promote access to broadband and provide resources to support accessibility, speed and affordability of broadband in Florida. SUPPORT improving service mapping accurately by requiring more granular data from service providers, allowing crowd sourced data to be used to inform the map, and creating an appeal process to challenge demonstrable inaccuracies.

•AQUACULTURE Encourage state regulatory relief designed to encourage increased commercial production and harvest of aquacultured bivalve shellfish (e.g., clams, oysters) in state waters through review of submerged land leasing requirements and revision of restrictive or outdated regulatory policies. Direct the Florida Department of Agriculture and Consumer Services and/or Farm Service Agency to evaluate the reestablishment of a viable crop insurance program for shellfish aquaculture producers, specifically designed to cover crop and market losses due to mortality or extended harvest moratoriums and disrupted ability to sell product after environmental perturbations (hurricanes and harmful algal blooms). Direct FDEP to evaluate the potential for regulatory reform which considers the use of live clams to enhance the success of seagrass impact mitigation requirements Direct FDEP to evaluate implementation of a nutrient credit program to incentivize production of commercial shellfish aquaculture. Encourage FDEP, FWC and other relevant state agencies to advance additional grant opportunities for the scientific research required to promulgate regulatory standards for deployment of bivalve shellfish for large scale water quality improvement and nearshore habitat creation.

• ADDED TO GUIDING PRINCIPLES: FOOD INSECURITY SUPPORTS increased state funding and policies that reduce food insecurity among Floridians, in order to · 1) increase the health and productivity of those currently without consistent access to healthy food, 2) consequently reduce the demand for public health and human services, 3) improve the financial security of those in need, and 4) accelerate the recovery and increase the resiliency of Florida's economy in the aftermath of the COVI D19 pandemic.

FAC Contact Need additional information or want to know more about FAC's Agriculture & Rural Affairs program? Contact Jeff Scala, Deputy Director. at [email protected]. GULF COAST RESTORATION INITIATIVE

Affiliates: Gulf Shellfish Institute, Sea & Shoreline Aquatic Restoration, Solutions to Avoid Red Tide (START), Sunnyvale Seafood Company (SSC) RESTORING ESTUARIES AND GROWING COASTAL ECONOMIES ALL CLAMS ON DECK: GETTING ON BOARD TO RESTORE FLORIDA'S ESTUARIES

• Paradise under pressure: • Development, Pollution, Runoff • Storms & Hurricanes • Harmful Algal Blooms • Economic consequences • Coastal communities • Commercial and Recreational Fisheries • Florida tourism fwd &nd Diffuv.na IRBDI showing "C titive ftuorcscence fr'OIT h gh (n:dl to ow (v iole!). A -necl1on fi!t:ar w.as apphC to remo.,.• speckle . Winds 'ro'TI NOAA NO BC station VEN Fl. BIOLOGICAL MITIGATION STRATEGIES: USING NATURE'S TOOLBOX Aquacultured Seagrass & Hard Clams ECOSYSTEl\1 E C O l\:" O ,l\ll C SERVICES GRO\ YTH

> $20 BILLION 992 LBS GDP DEPENDS o::-,.: NITROGEN HEALTHY BAY INCORPORATED INTO CL\.\lS no <)\, JOBS 22,.500,000 RELY ON GALLONS \YATER HEALTHY ESTCARY FILTERED D .-\ILY

H0.\11: VALUES

2 - 4 X GREATER SHELi.FISH AQC:\CL"LTURE ESTUARIES FEDERAL FUNDING & FLORIDA LEGISLATION

• $15 M will support proof of concept to research and promote large-scale restoration efforts in 3 National Estuaries • Seagrass restoration & Hard clam deployment • Tampa Bay, Sarasota Bay, Charlotte Harbor

• Florida Governor and Legislative Ask • Certify bivalves for mitigation credits and create legislation that provides avenue to proceed • Increase mitigation tools available • Increase capacity of Florida's shellfish aquaculture industry IT'S TIME TO ACT.

RESTORING ESTUARIES AND GROWING COASTAL ECONOMIES Website coming soon: AllClamsOnDeck.org Gulf Coast Restoration Initiative

Project Overview

This initiative will support ecosystem sustainability and resilience. Restoring clam populations and seagrass meadows will result in improved water quality, reduced algal blooms, and heathier habitats for commercial and recreational fisheries in the Tampa Bay, Sarasota Bay, and Charlotte Harbor estuaries. Project Background

This novel project aims to enhance estuarine resiliency by implementing large-scale restoration initiatives for seagrass and clam populations in three of Florida's most valuable estuaries: Tampa Bay, Sarasota Bay, and Charlotte Harbor. These estuaries are currently at risk of unprecedented, rapid declines in seagrass andielam,p9pulatio_ns 9-ue to_~acro?-J_ga_l .--···{ Commented [C1J: Replace with shellfish? blooms, red-tide events, urban runoff, and industrial point source pollution (most recently, the event at Piney Point). Thriving seagrass meadows and healthy clam populations provide valuable fisheries habitat and contribute distinct and numerous ecological services including water filtration, nutrient reduction, and carbon sequestration. Seagrass habitats support a diverse community of organisms, including numerous sportfish species (e.g., juvenile grouper, spotted seatrout), and clams are an asset to commercial and recreational fisheries.

Millions of visitors spend billions of dollars every year to experience the splendor of our pristine, nationally recognized estuaries. The health of these habitats is critical - not only for the ecosystem services they provide, but for the economic impact that results from Florida's coastal tourism. Seagrassr.§.: There are seven species of seagrass that are native to Florida waters. These true flowering marine plants are dependent on adequate sunlight for photosynthesis, nutrients, and stable sediment in which to grow. Factors that inhibit seagrass growth include impaired water quality, coastal development, increased urban runoff, and erosion. Seagrass meadows are critical nurseries for juvenile fish, and manatees are dependent on seagrass as a food source. Hard Clams: Native southern hard clams, previously abundant on Florida's southwest coast, are one of the most prolific marine filter feeders within the region. This species grows well throughout the region because of its ability to withstand warmer temperatures and fluctuations in salinity that are common within estuarine environments. Filter feeding.Jn: clams play§ two primary roles in the marine ecosystem~c The first is that their F!RJJ3le aet of filter feeding removes particles from elurifies the water, which in turn promotes sunlight penetration and enhances photosynthesis within seagrasses; the second is that clams-Hiey physically consume and bind phytoplankton (microalgae). which are eventually expelled into the sediment as feces and pseudo-feces. This process allows water-soluble nitrogen (within the microalgae), to be reduced and assimilated into the marine substrate where it will continue to be broken down by microorganisms and bacteria.

'.Numerous precedents exist that demonstrate this proposal's capacity for success_. Multiple J Commented [MOU2]: Perhaps it would be good to list a ',I initiatives are currently underway throughout the US related to bivalve and seagrass couple of these efforts in parenthesis? ____ J restoration for economic and environmental benefit. These Pxam ple~7_-t:tttt!-indicate that with adequate funding and support, bivalves and seagrasses can be successfully restored to historic levels0 t-h-a+-t h u~ enhanci.nge the resiliency and vigor of coastal environments. Project Objective

This project will restore 650 acres of seagrass by strategically planting nursery-grown seagrass into areas that have sufficient water quality conditions to support them, create 30 high-density clam restoration sites {capable of producing 86.4-- 13 fertilized eggs every year for up to 50 years}, and monitor the primary and secondary benefits of the initiative. Clams would be recorded for genetics, ~l)_q~ing_f9r future !J.SS!!ssment of population exp!J.nsion and Commented (C3]: What about the seagrass genetics? Just restoration design improvements. wpndering how to simply state this - Perhaps, "Restored seagrass and clam populations will be sampled periodically !secondly, this project aims to create avenues for traditionally commercial fishing to monitor genetic composition, allowing for assessment of population expansion and refinement of future restoration communities to become more involved with environmental restoration. !sE!a_gr!).SSE!S are design efforts." known as nursery grounds to a multitude offish species, and providea key habitat§ Wfttffi Commented (C4] : This is a weird sentence since you don' t fH"O\·ides food to that s upport many other organisms such as seabirds, manatees and turtles. mention how they'll be involved wjth the restoralicm effort Clam~ (at both larval and adult stages) larvae are aoffer Q_primary source of food for many anywhere in the nartative. I would rephrase to say something fish and &tber-benthic organisms. Not only do they provide food, but as the larvae mature like, " This project will involve co=ercial aquaculture into adults, they ~!ear particles from the water and reduce nitrogen in the water operations, including shellfish and seagrass farmers, and will enhance habitats that are critical to both connnercial and column, which enhances the water quality. recteational wild marine fisheries."

!Methods and Timeline' - add estimate of costs for year (1) .. -· ·{ Commented [CS]: inc Year 1 -:: Distribute RFP and ,\eqeire acquire necessary permits for restoration activities.1.fil, and cultivate/purchase seagrass (amount, cost$) and clams_(fil Year 2 and 3 - Install hatchery-raised clams and seagrass Year 3 thru 6 - Maiate.iB Research and monitor rest oration sites to evaluate su ccess Year 5 - Present a-peer-reviewed publication~ of results

SCOPE OF SERVICES

• GSI distributes Request for Proposals (RFP stipulates JDC is capped at 10°.)

• Acquire necessary permits for restoration activities

An 1advisorv panel ~ f ~ -~rjn~ ~<;iEl!'lctU!Hl, natural resource managers and regulatorv __ •• . -< Commented [C6]: NEPs, NGOs, state and federal staff will guide the idrntify identification aAEI sun·ey and establishment of potential management agencies, county governments restoration sites that have the highest likelihood for success while J3ro,·idiAg the most eeosysteA~ sen-ices. Permits will be acquired from required entities, including the Florida Department of Environmental Protection (PEP). US Army Corps of Engineers (USAGE), National Oceanographic Atmospheric Administration (NOAA), Florida Fish & Wildlife Conservation Commission (FFWC{;), US Fish and Wildlife Service (USFWS), and US Coast Guard (USCG) to conduct restoration activities in pre-determined areas. • Install hatchery raised clams and seagrass

Areas of historic seagrass meadows will be planted with up to 3,250,000 nursery grown seagrass planting units for a total anticipated area of 650 acres across three estuanes. The species used will be selected ~hased on their suicahilit,· to the environmental conditions of the project site~. Restoration sites will be selected based on a low likelihood of natural recruitment, reduction in seagrass meadow integrity without preventive plantings, and where-as water quality and regula torv infrastructure allows. Approximately 5,000,000 clams will be raised to a 10mm size, then planted within permitted areas into 30 populations of high density l(Pohd~.':V~th4!Jh_e _th_r:E!!l. ~~t.l!~li.~s,.'J'l.i~ -~p~ciE!,s_ best ~uited for this region is tqe _.. { Commented [C7): What does this mean? Southern hard clam, Mercenaria campechiensis. • Maintain and monitor restoration sites

Seagrass and clam restoration areas will be monitored for a three-year period to document the -survival and success of the plantings. A time-zero and annual report will be generated from monitoring events. During each monitoring event, a biologist will measure density/cover and expansion rates of the seagrass restoration areas. The 10mm size clam populations, once planted, will be cover-netted, a proven technique to reduce predation, with the nets being changed out 4-10 times per year for purposes of controlling biofouling and net mesh size adaptation.

• Present a peer-reviewed publication of results

This project will provide an invaluable research opportunity to evaluate multiple parameters during a multi-species, large-scale restoration effort. An existing team of partners, including management agencies, academic researchers, and non-profit conservation organizations, will be encouraged to participate in the process and provide input to research design and progress. Results from any research that stems from this work will be disseminated in the form of scientific publications, formal presentations, and educational outreach to the public.

PROJECT BUDGET

The estimated cost for this project is $ 15 million. ~ F~ FLORIDA o\ -.C:)(lo\110\01 COUNTIES

All About Florida

ARA-PP-2: AQUACULTURE

COMMITTEE RECOMMENDATION: ADOPT

PROPOSED POLICY: • Encourage state regulatory relief designed to encourage increased commercial production and harvest of aquacultured bivalve shellfish (e .g., clams, oysters) in state waters through review of submerged land leasing requirements and revision of restrictive or outdated regulatory policies. • Direct the Florida Department of Agriculture and Consumer Services and/or Farm Service Agency to evaluate the reestablishment of a viable crop insurance program for shellfish aquaculture producers, specifically designed to cover crop and market losses due to mortality or extended harvest moratoriums and disrupted ability to sell product after environmental perturbations (hurricanes and harmful algal blooms). • Direct FDEP to evaluate the potential for regulatory reform which considers the use of live clams to enhance the success of seagrass impact mitigation requirements. • Direct FDEP to evaluate implementation of a nutrient credit program to incentivize production of commercial shellfish aquaculture. • Encourage FDEP, FWC and other relevant state agencies to advance additional grant opportunities for the scientific research required to promulgate regulatory standards for deployment of bivalve shellfish for large scale water quality improvement and nearshore habitat creation.

BACKGROUND: Bivalve shellfish aquaculture is a rapidly growing sector of the seafood industry, and Florida currently ranks 4th in domestic production of farmed shellfish (clams and oysters). The industry provides economic value to the state of Florida, and shellfish aquaculture is estimated to support at least 550 jobs and contribute $39 million annually to Florida's economy. In addition, this green agricultural enterprise is unique in its capacity to provide significant environmental benefit. Shellfish filter water to feed, thus improving water clarity, sequestering carbon, and perhaps most importantly, absorbing nutrients including nitrogen and phosphorous. This is especially relevant for bodies of water that must abide to Total Maximum Daily Load (TMDL) nutrient criteria (examples of regulated estuaries include Apalachicola Bay, Tampa Bay, Charlotte Harbor, Indian River Lagoon). Shellfish are being promoted in multiple US states (New York, Maryland, Virginia) as well as a large number of Florida counties making up the Indian River Lagoon, Panhandle, Cedar Key, Tampa Bay; Charlotte Harbor regional areas among others as water quality enhancers and restoration tools. A growing aquaculture industry benefits production for local consumption as well as a supply for these regional environmental efforts. However, the state of Florida consumer currently lacks the regulatory framework to compensate shellfish growers for the environmental benefits that their crops provide, nor the ability to incentivize shellfish farmers to produce additional product for restoration initiatives. This mitigation framework, combined with enhanced lease availability, updates to overly restrictive or ~ F~ FLORIDA .. ,\,(.)(l'\IIO,OI COUNTIES All About florida outdated regulations for harvest, and a viable crop insurance program would support existing farmers and provide incentive for the industry to expand in Florida .

ANALYSIS: Regulatory reform which incorporates live clams as part of a nutrient credit or seagrass impact mitigation strategy and development of additional grant opportunities for related supporting research provides an expanded market niche beyond production for table consumption for bivalve shellfish farmers across the state. One impediment to entering the shellfish aquaculture industry is the uncertainty inherit in loss of crop due to naturally occurring events such as hurricanes, red tide or other harmful algal blooms and the regulatory harvest closures which result. Extended harvest closures often result in a crop that has grown too large for profitable marketing to wholesalers and restaurants, resulting in devastating economic loss to farmers. Incorporating large clams into restoration efforts or mitigation strategies aimed to enhance water quality or habitat development would provide a secondary market and another level of profitability for the clam shellfish industry. Creation of a crop insurance program that accommodates for loss of marketability due to harvest restrictions because of hurricanes and harmful algal blooms would increase the commercial viability of locally grown and harvested clams and oysters and provide a level of protection that would encourage expansion of the industry.

FISCAL IMPACT: Bivalve shellfish aquaculture production in Florida ranks 4th in the nation. The industry supports over 550 jobs and contributes at least $39 Million in gross revenue to the state economy. Highlights from a University of Florida study on environmentally beneficial ecosystem services provided by hard clam production in 2012: Almost 550 million gallons of seawater were filtered by the statewide production farmed clams in 2012. Through Florida's aquacultured hard clams harvested in 2012, over 25 thousand pounds of nitrogen were removed, and 760 thousand pounds of carbon were stored from the coastal environment. The economic value of these benefits was estimated at $99,680, which represents the public good value that the industry generates to Florida citizens at no cost. This estimate was about 1% of the farm gate value of clam sales ($11.9 million) in that year.

SUBMITTING COUNTY AND CONTACT: Manatee; [email protected], 941-737-4765

ASSIGNED COMMITTEE: ARA

BOARD SUPPORT: Yes

UNFUNDED MANDATE: No

PROTECTIVE OF HOME RULE: N/A • • • • • Find us on social media TNC: Restorative aquaculture can improve marine habitats, biodiversity

Friday, 25 June 2021 James Wright Conservation group touts bivalve and seaweed farms as critical components of beneficial food systems

A new study from The Nature Conservancy touts the biodiversity benefits of mussel, oyster, clam and seaweed farms. Pictured: Tim Henry, owner of Bay Point Oyster Company, readies an oyster cage to be placed back in the water at his farm in Little Bay in Durham, New Hampshire. Photo by Jerry Monkman, courtesy of The Nature Conservancy. U.S . conservation group The Nature Conservancy (TNC) today released a meta­ analysis of existing research literature that has determined that restorative or regenerative aquaculture - seaweeds and bivalves - not only improves surrounding ecosystems but also contributes to healthier marine animal habitats and biodiversity.

Titled "Habitat value of bivalve shellfish and seaweed aquacultu re for fish and invertebrates: Pathways, synthesis and next steps," the study was published in the journal Reviews in Aquaculture. Robert Jones, globa l aquaculture lead at TNC and one of the study's authors, told the Advocate that the review of 65 published sources - which he called a form of "global synthesis science" - is the first of its kind to review and consolidate data around the idea of restorative aquaculture.

"Can we show that these farmers are having a positive benefit on the environment? That was the objective," said Jones. "I t seems somewhat counterintuitive, because in land-based systems, it'd be rare to find an example of placing a farm somewhere and improving wildlife habitat. But people familiar with the ocean understand that structure in the ocean can generate a habitat effect, like with artificial reefs. But aquaculture is a living system, and there can be more benefits than just the stru cture itself."

A lot of the findings in these studies had been "buried in the literature," he said , so TNC set out to centralize the information. TNC collaborated with its partners at the University of Melbourne, the University of Adelaide (both in Australia) and the University of New England (Maine, USA) to assess the biodiversity benefits of mussel, oyster, clam and seaweed farms. In each case, a greater number of fish and invertebrates were observed on the farm sites in comparison to nearby locations, with mussel farms showing the greatest ability to act as an aggregator of marine life. In fact, mussel farms attract about 3.6 times more fish and invertebrates than nearby locations.

"Earlier on, our research was focused on mapping out potential ecosystem benefits of aquaculture, making a high-level case for it. Then upon digging in, we found issue areas and three really strong cases for restorative aquaculture," said Jones . "One is water quality and [excess] nutrient removal - that's the one we have the best handle on . There's another body of emerging information around climate and carbon sequestration. That's an area we're digging into too and will have more on later this year. The third is habitat. The benefits of biodiversity [surrounding aquaculture farms] is not as well understood."

lnfographic provided by The Nature Conservancy. The TNC report also shows that oyster farms proved effective at increasing biodiversity, as 30 percent more species were found to inhabit oyster farms than surrounding areas. Marine farms, Jones said , are good at providing reproductive and foraging grounds as well as shelter from predators.

"Food production has had a significant negative impact on the natural world, including 80 percent of habitat loss, and aquaculture alone accounts for up to 30 percent of mangrove loss in some parts of Asia, which are vital nursery grounds for fish and marine life," said Dr. Heidi Alleway, global aquaculture scientist at TNC. "As a result, conservation efforts have been increasingly focused on how to curb the detrimental effects of food production practices. The benefits identified in this study open an exciting conversation about how we might be able to better design - to best design - a food system that not only addresses the environmental impacts, but perhaps even supports the repair and recovery of degraded ecosystems or areas." marine life," Jones said , stressing that not every farm examined in the literature met the criteria as a net environmental benefit. "Biodiversity is the essence of ocean health. If animals living in it are healthy, there's an inherent benefit for a functional ocean ecosystem but there are implications for humans as well if we utilize these animals as food sources."

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Author

• JAMES WRIGHT

Ed itorial Manager Global Aquaculture Alliance Portsmouth, NH, USA

[email protected] How Much Habitat Benefit do Shellfish and Seaweed Farms

REFERENCE SITE This research reviewed 65 Mussels In this study Oysters in this study were global studies that were exdusively grOWh grown majority on rack compared shellfish and on longfines. and bag.$)"$tems,- but seaweed aquaculture gear to so used longlines or nearby reference sites on-bottom methods. without aquaculture gear.

1 X 3.6x 1.7 X 1.5 X Abundance Abundance Abundance Abunda1 Multiplier

1 X 1.1 X 1.3 X 1.0 X Diversity Diversity Diversity Diversit) Multiplier .. ~ .... _..,.> . . ~ . .• : .:. ..

lnfographic provided by The Nature Conservancy. The authors want policymakers at local, regional and global levels to recognize the potential of aquaculture and to incorporate it into regulatory systems. They hope shellfish and seaweed farming systems can inspire application and development of aquaculture and agriculture that is "nature-positive" and assisting food security efforts.

"We were able to show for the first time, conclusively, that [seaweed and shellfish farms] do tend to have a positive impact on the abundance of marine life and the diversity of 1131 Bivalve-enhanced nitrogen removal from coastal estuaries

Ruth H. Carmichael, William Walton, and Heidi Clark

Abstract: Interest in use of bivalves to remediate estuarine eutrophication has increased in recent years. High variation among data sets, substantial focus on particle removal, and insufficient links to anthropogenic nitrogen (N) sources encour­ aged this empirical examination of N removal by bivalves from estuaries receiving different N loads. We determined the ca­ pacity of the oyster Crassostrea virginica to remove N by comparing N assimilated into tissues with anthropogenic N from land or available in phytoplankton. Oyster growth yielded 0.2-0.4 g N in tissues and depended on estuary-specific condi­ tions. 11 15N values confirmed that N in oyster tissues derived from local anthropogenic sources. At representative restoration and aquaculture conditions (5400 oysters·m-2 at 0.5 %-1.0% of estuary area), estimated N removal was 515% of land­ derived loads and

[Traduit par la Redaction]

Introduction and using different spatial and time scales, which makes comparison among systems problematic. Overall, a careful Increased awareness of the pervasive and often negative ef­ review of the data indicates that while bivalves may remove fects of eutrophication has prompted considerable interest in 30%~5% of local particle concentrations, and in one case bivalves as a natural solution to remove particles from the possibly as much as 90% of local chlorophyll a (chi a) con­ water column or remediate nitrogen (N) loads to coastal centration, N removal is lower, ranging from less than 1%- waters (e.g., Gifford et al. 2007; Cereo and Noel 2007; Gren 15% of total annual N loads to 25% of daily N load (Table 1). et al. 2009). At least 30 studies worldwide since 1980 have Although the available data are fragmentary and do not con­ attempted to quantify some aspect of bioremediation by bi­ vey comprehensive results with respect to N removal, they do valves, with more than half of these studies in the last decade suggest that bivalves remediate some symptoms of eutrophi­ (Table 1) . Nearly unanimously, these studies concluded that cation. bivalves were potentially important bioremediators. Specific Emphasis on particle removal as a primary means to assess results, however, are not entirely consistent with this optimis­ bioremediation among previous studies is a concern. In the tic notion. Only ~40% of studies quantified some form of N past 30 years, shellfish bioremediation research has largely removal, and results were typically reported in different units focused on reduction of particle loads, turbidity in the water

Received I October 2011. Accepted 18 May 2012. Published at www.nrcresearchpress.com/cjfas on 28 June 2012. J201 I-0413 Paper handled by Associate Editor Charles Ramcharan. R.H. Carmichael. Dauphin Island Sea Lab, Dauphin Island, AL 36528, USA. W. Walton. Auburn University Shellfish Laboratory, 150 Agassiz Street, Dauphin Island, AL 36528, USA. H. Clark. Woods Hole Group, I Technology Park Drive, East Falmouth, MA 02536, USA. Corresponding author: Ruth H. Carmichael (e-mail: [email protected]).

Can. J. Fish. Aquat. Sci. 69: 1131-1149 (2012) doi: I 0.1 I 39/F2012-057 Published by NRC Research Press Table 1. Comparison of bivalve bioremediation-related studies, including study locations, methods of remediation studied, density and shell height of bivalves, and primary conclusions. (;) I\) Method of remediation N N stored Particle Biogeo- Height 2 '

.s;:I Crassostrea virginica Chesapeake Bay, USA (+) 76 May remove 0.07%-1.4% of Fulford et al. 2007 ~ phytoplankton-day-' (modeled) ...: Crassostrea virginica Chesapeake Bay, USA (+) (+) Reduced total N concentration 10%- 15% Cereo and Noel 0 2007 :>. (modeled) .D Pinctada imbricata Port Stephens, Australia + Removed 7.5 kg N-tonne-1 oyster; ~2% of Gifford et al. 2005 wastewater N load-year-• 0s u Crassostrea virginica Chesapeake Bay, USA (+) (+) Denitrification-burial removed 7 .5 XI 0-4 kg Newell et al. 2005 ~ ~ N-g- 1 oyster; 0.6% of annual N load e~p.O (modeled) ...C:o U<1> Crassostrea virgi11ica Chesapeake Bay, USA + Denitrification by simulated biodeposits Newell et al. 2002 1,j;::l o- removed 20% of local N load (lab) 0 i:: Crassostrea gigas Thau Lagoon, France + + 40 Reduced chlorophyll a but increased N in Souchu et al. 200 I "'"'.... 0 0<1) water column at Pinctada imbricata Port Stephens, Au stralia (+) (+) (+) May remove 19 kg N·tonne-' oysters Gifford et al. 2004 Crassostrea virgi11ica North Carolina creek, + 125 48 Some reduction of chlorophyll a and Nelson et al. 2004 li USA suspended solids Crassostrea gigas Hiroshima Bay, Japan + (+) (+) Raft culture Removed ~ I 0% of N load-day-• Songsangjinda et 0s < ::r .0 ..ci "a. Myti/11 s galloprovi11cialis Dokai Bay, Japan + + Long lines 15- 41 Removed ~25% of dissolved inorganic Kohama et al. 2002 C CT ~ "' '< nitrogen (DIN) in I day (lab) ~ Yamamuro et al. (/) .....; :;oz Musc11/ista se11housia Lake Nakaumi, Japan + 0-46712 Shell burial removed 0.7%--4.9% of annual p . 2000 d n N load < :;o Mytilus edulis Omst- Tji:irn system, Sweden 100 kg, Removed 8.5- 12 g N-kg-• live mussel; Haamer 1996 Q_ u"' !). + + long lines removed 20% of DIN CJ) R" 50 ::r Myti/11s spp. Upper South Cove, Canada (+) + 400, Jong lines Increased sedimentation, released NH4 + Hatcher et al. 1994 I\) "" s ~ I\) 0 Table 1 (concluded). Ill 3o· Method of remediation :::, Ill N N stored Particle Biogeo- Height ~ 2 Species ) Source '<:f"- Location in tissues removal chemistry Density (m- (mm) Conclusion ~ ---0 ~ t-- Mytilus edulis North Sea, Netherlands + (+) Field flume Removed chlorophyll a and seston, released Dame et al. 1991 ---0 NH.,+ (possible denitrification) i:: 0 Mytilus edulis Northern Baltic Sea, + 535- 1693 g Increased annual N, C, P sedimentation by Kautsky and Evans v Sweden chambers 10% 1987 ..r:::: Perna ca11a/ic11/11s Kenepuru Sound, NZ Long lines Harvest and denitrification removed 68% Kaspar et al. 1985 "'0 + + .§ more N than reference sites Geukensia demissa Cape Cod, USA + + (+) 34-365 10-100 Mussels retained and recycled N within the Jordan and Valiela u"' marsh system 1982 ::r: -s::, Clams ~ Tapes philippina,rum Goro lagoon, Italy + I00-3000 Increased sedimentation with net removal of Nizzoli et al. 2006 ,_; N from sediments Cl >, Corbicu/a japonica Lake Shinji, Japan + (+) 0-1000 Removed chlorophyll a, released NH,' Nakamura and Ker- .0 ciku 2000 Loo and Rosenberg 0s Mya are11aria Laholm Bay, Sweden + + 0-2000 1- 25 Removed up to 27% of new local produc- 0 tion 1989 ~ ~ Doering et al. 1986, ~t:: Mercenaria 111erce11aria Narragansett Bay, USA + + 16 mesocosm 32- 107 Increased C sedimentation; models may p..O overestimate particle removal 1987 ..C:o 0CI) Corbicu/a fluminea Potomac River, USA 1.2- 1467 l - >25 Removed 30% of chlorophyll a in 2 h Cohen et al. I 984 &l ::, + o ~ 0 i:: Scallops "'"''"'0 0~ Ch/amys farreri Sishili Bay, China + (+) 0-40 32±4 Removed up to 45 % of particles-day-' Zhou et al. 2006 ~o

Cockles li Cardium edule Laholm Bay, Sweden + + 0-8000 4-21 Removed up to 27% of new local produc- Loo and Rosenberg s 1989 .g tion "O 0 Various "O Various (+) (+) 25- 500 Bioremediaiton was location- and condition- Ferreira et al. 2007 "'0 specific (modeled) San Francisco Bay, USA (+) (+) (+) 200 Defined conditions for remediation (model) Officer et al. 1982 10 Cl Note: Methods of remediation include nitrogen removal by assimilation into shell or soft tissues, particle removal (measured in terms of suspended particulates, chlorophyll a concentration, or filtration ·u rate), and stimulation of biogeochemical processes via biodeposits. Parentheses indicate studies for which results were calculated from literature values, estimated, or modeled and not directly measured. A (/) long dash (- ) indicates not reported. <;;j ~ & ~ ::r~ <> ..d C. Cl) er ~ '< ....; :,,z () d :,, I:. u"' n !; r. ::r '"O ol w ~ w 1134 Can. J. Fish. Aquat. Sci. Vol. 69, 2012

column, and biogeochemical processes, with fewer studies Fig. 1. Mean (± standard error) bivalve growth rates (a) and %N (~20%) directly quantifying N removal by assimilation into content in tissues (b) compared with N loading rates to four estu­ tissues (Table I). Focus on particle removal and associated aries in Cape Cod, Massachusetts. Clams include combined data for processes, however, may not be adequate to quantify N re­ softshell (Mya arenaria) and northern hard clams (Mercenaria mer­ moval. Phytoplankton particles are subject to hydrodynamic cenaria), which differed between seasons (2000, 2001 ), but not be­ forces, and it is difficult to assess consumption by bivalves tween species. Mussels refer to Geukensia demissa, and scallops relative to export down-estuary or consumption by other sus­ refer to Argopectin irradians. Data are from Evgenidou and Valiela pension feeders (Nelson et al. 2004; Grizzle et al. 2008). (2002), Weiss et al. (2002), Shriver et al. (2002), and Carmichael et Similarly, measurement of particle or N removal using filtra­ al. (2004a). Nitrogen (%) in scallops was determined by Shriver et tion rates may be inaccurate (Pomeroy et al. 2006; Grizzle et al . (2002), but not previously published. Shell length: y = 0.29 ln(x) 2 al. 2008), requiring careful consideration of environmental + 0.12, R = 0.96, F regrcssion 3 = 48.62, P = 0.02 (clams 2001); y = 2 conditions that affect shellfish metabolism and likely overes­ 0.21 ln(x) - 0. 15 , R = 0.93, Fregrcssion 5 = 55.80, P = 0.002 (clams 2 timating N removal when bivalve condition or growth de­ 2000); y = 0.02 ln(x) + 0.11 , R = 0.56, Fregression 8 = 9 .02, P = 0.02 clines (J¢rgensen 1966; Bayne and Newell 1983; Rice 1999). (mussels). Nitrogen (%): y = 0.56 ln(x) + 6.31 , R2 = 0.61, Consideration of N removal by tissue assimilation, however, Frcgrcssion 7 = 9.31 , P = 0.02 (hard clams); y = 0.86 ln (x) + 6.58, reflects net potential N removal regardless of variation in en­ R 2 = 0.69, Frcgrcssion 7 = 13.13, P = 0.01 (softshell clams). vironmental factors that alter filtration rates or physiological (a) •Clams 2001 condition. Since many species used for bioremediation are 2.1 oClams2000 commercially valuable, these species directly remove N in 0 0 0 •Mussels tissues when they are harvested as well as producing biode­ -'.!I::: OScallops posits that potentially alter downstream biogeochemical proc­ Q) 0 Q) esses (Rice 1999; Newell 2004). Bivalve biodeposition has 3: . 1.4 been credited with stimulating N removal as well as N addi­ E tion to estuaries worldwide (Table 1), and the effects appear E to be location-specific and inconclusive (Souchu et al . 2001; -.c Zhou et al . 2006; Coen et al. 2007). These findings encour­ 0) -C: age a more comprehensive empirical examination of N re­ 0.7 moval by tissue assimilation along with the potential for ~ biogeochemical processes to complement this mechanism of Q) .c N removal. CJ) Estimates of bioremediation also need to be made at rele­ • • • vant spatial scales, preferably considering entire estuaries. Previous studies reported largely local effects often based on generalized data or literature values, with the assumption that local effects and general conditions will broadly scale up 13 (Pomeroy et al. 2006; Grizzle et al. 2008; Dumbauld et al. 2009). The large variation in findings reported in Table 1 suggests that local controls on N removal may also vary 11 greatly. Location-specific factors such as salinity, tempera­ -0~ ture, dissolved oxygen (DO), hydrology, bivalve density and -(/) species composition, and total N load can affect estimates of Q) ::I bioremediation by affecting the quantity and quality of par­ (/) 9 (/) ticle loads or bivalve responses (e.g., Officer et al. 1982; Car­ :.= michael et al. 2004a; Grizzle et al. 2008), rendering C: generalized data unreliable. Studies across a range of N­ z 7 enriched estuaries show that the influence of N loads on bi­ + eHard clams valve growth and N content depended on species and o Softshell clams location-specific attributes (Fig. 1: data from Evgenidou and escallops Valiela 2002; Weiss et al. 2002; Shriver et al. 2002; and Car­ 5 michael et al. 2004a). Space available for cultivating shellfish 10 100 1000 may also strictly limit bioremediation relative to estuary size 1 1 (Ferreira et al. 2007) but has rarely been considered in biore­ N load (Kg N•ha- •year- ) mediation assessments (Table I). Calculations of N removal by tissue assimilation can avoid some of these potential hur­ remediation, restoration, or management efforts, it is also im­ dles by using location-specific measures of growth and N portant to demonstrate that bivalves remove N from land­ content in tissues relative to local planting areas, N loads, derived sources. Although most studies claim to test bivalve _and particle supply. These caveats highlight the need for capacity to remediate cultural eutrophication or anthropo­ location-specific data and the potential utility of tissue assim­ genic N loads (e.g., Officer et al. I 982; Zhou et al. 2006; ilation to define N removal capacity of bivalves across loca­ Cereo and Noel 2007), they have not demonstrated that bi­ tions and through time. valves actually removed land-derived or autochthonous N, To collect data that are meaningful for assessment of bio- rather than N in particles conveyed from adjacent waters.

Published by NRC Research Press Carmichael et al. 1135

Fortunately, the specific combination of N sources on a Materials and methods watershed confers unique N stable isotope signatures to nu­ trients delivered to a water body (McClelland et al. 1997; Study sites Carmichael et al. 2004b; Fertig et al. 2009). Producers may This study was conducted in five estuaries on Cape Cod, assimilate these nutrients and become food for consumers Massachusetts, USA (Fig. 2), characterized by different land such as bivalves, which subsequently acquire the location­ uses on their watersheds (Table 2) . N loads to these shallow, specific N stable isotope ratio (Evgenidou and Valiela 2002; well-mixed estuaries (Sage Lot Pond, Wild Harbor, Green Weiss et al. 2002; Shriver et al. 2002). Hence, N stable iso­ Pond, Snug Harbor, Childs River) do not vary substantially topes provide a tool to link estuary-specific N sources to bi­ among seasons because land-derived loads are delivered pri­ valves and determine the efficacy of bioremediation. marily through groundwater (Valiela et al. 1992; Jay et al. Although the full complement of bivalves in a system may 1997). The N loads have been estimated and span most of contribute to N removal at some level (if harvested and pos­ the range of land-derived N loads to coastal estuaries in the sibly via biogeochemistry), oysters or other commercially United States (e.g., Valiela et al. 1992, 2000; Kroeger et al. harvested species with similar feeding behavior and physio­ 1999). Several studies on the effects of eutrophication on logical capacity will likely have the greatest potential for use habitat and food supply for a variety of bivalve species have as a management or N bioremediation tool. Oysters are well been conducted in these estuaries; site conditions are well documented to maintain high feeding rates at high food con­ documented, and this previous work (e.g., Evgenidou and centrations by coupling high particle capture rates with an ef­ Valiela 2002; Shriver et al. 2002; Carmichael et al . 2004a) ficient pre-ingestion and sorting mechanism (Newell and provided context for the current study. Langdon 1996). Higher growth rates combined with resulting greater dry mass to height ratios compared with other species Field measurements (Shumway 1996; Carmichael et al. 2004a) and higher volume Oyster transplants of ejecta production (Tenore and Dunstan 1973; Newell and To quantify estuary-specific growth and N content in oys­ Langdon 1996) render oysters potentially more effective at ters, juvenile hatchery-reared oysters (8.2 ± 0.2 mm longest assimilating N into tissues or removing N via biogeochemical dimension) were transplanted at two sites in five Cape Cod processing than some other species. Oysters are also abun­ estuaries (Fig. 2) during the primary growing season (June­ dantly harvested throughout the world and frequently targeted October, starting on 29 June 2003), when bivalves in the es­ for aquaculture, restoration, and ecosystem assessment activ­ tuaries are most actively assimilating particle and N loads ities, making them of high interest for bioremediation study (Shriver et al. 2002; Carmichael et al. 2004a). We used (Table 1; Fulford et al. 2010; Beck et al. 2011). hatchery-reared oysters to ensure common stock was trans­ Given the paucity of comprehensive empirical assessments planted into each estuary and to most accurately reflect bi­ of bivalve bioremediation relative to estuary-specific N loads valves planted for culture or management purposes. Oysters and the likelihood that oysters are a most effective bioremedia­ were obtained from the Aquaculture Research Corporation in tor species, in this paper we directly measured N removal ca­ Dennis, Massachusetts. Oysters (n = 67 ± 2) were placed in pacity of the oyster Crassostrea virginica. To test N removal plastic-coated wire mesh aquaculture cages measuring 30 cm under different N loading regimes, we quantified N assimilated wide x 52 cm long x 8 cm deep. Cages were lined on the into tissues and removed at harvest by oysters transplanted into inside with 3 mm plastic mesh and elevated 6 cm above the five Cape Cod estuaries that receive different land-derived N sediment surface in approximately 1 m of water (at low tide). loads. Estuary-specific growth rates and N content in oyster Cages were placed at this height to mimic typical natural set­ tissues were measured to determine total N stored in oyster tis­ tlement elevations for oysters in the area and allow access for sues. To determine whether oysters assimilated (and therefore sampling and cleaning with minimal disturbance while main­ had potential to remove) anthropogenic N, we measured taining access to natural food sources. Four replicate cages estuary-specific N stable isotope ratios in suspended particles were transplanted at each site (eight per estuary), and one and oyster tissues and compared them with the percent waste­ randomly selected cage was removed from each site on days water contribution to each estuary. To roughly estimate the po­ 28 , 56, 84, and 112. This sampling scheme was chosen to tential N removal stimulated by oyster biodeposition associated capture spatial and temporal variation in growth, survival, with our empirical growth measurements, we applied literature and N content during the growing season . ..; estimates of N removal by denitrification and burial. Data on d N removal by tissue assimilation were further compared with Oyster growth and survival u"' estuary-specific, land-derived N loads and N in phytoplankton To measure growth during the experimental period, we re­ to calculate the number of oysters required to completely re­ corded shell dimensions of 50 randomly selected oysters mediate N loads and the approximate percent N (%N) removed from initial hatchery stock and from each cage at each re­ by oysters at typical restoration and aquaculture densities if moval date. Of the 50 oysters, 10 were further processed to planted over different percentages of embayment area. We determine mean soft tissue dry mass. Soft tissues from the used both land-derived and phytoplankton N to account for remaining 40 oysters were reserved for N content and stable dissolved inorganic N loaded to the estuary from external sour­ isotope analyses. In two cases (Snug Harbor and Green ces as well as to roughly account for additional N regenerated Pond), mortality limited the number of oysters measured to within or othetwise conveyed to the estuary, including from 33 and 49, respectively. Shell dimensions were recorded as biodeposits by oysters, which may contribute to algal produc­ the longest height (umbo to margin), width, and length of tion and symptoms of eutrophication (Kemp and Boynton each oyster to the nearest 0.1 mm using vernier calipers. To 1984; Mayer et al. 1998; York et al. 2007). measure soft tissue dry mass, whole tissues were separated

Published by NRC Research Press 1136 Can. J . Fish . Aquat. Sci. Vol. 69, 2012

Fig. 2. Study sites in five northeastern USA (a) estuaries on Cape Cod, Massachusetts (b). WH, Wild Harbor; and SN, Snug Harbor (c); GP, Green Pond; CR, Childs River; and SLP, Sage Lot Pond (d).

(a) Northeastern United States

0

41.63° -z -Q) "C :J :.:; (d) -ct! ....I 41.61 °

41.57°

70.67°

41.56°

10.ss0 10.so0 Longitude (W) from shell and dried to a constant mass at 60 °C. Whole tis­ we collected whole water at 10 cm from the sediment surface sues, except gut, were collected to reflect total N assimilated at each site (Fig. 2) every 2 weeks. Two 1 L samples without including unassimilated foods. Growth rates were de­ (200 µm prefiltered) were passed through pre-ashed 0.7 µm termined from the slope of the regression line comparing Whatman GF/F filters. We identified components of available mean shell height and dry mass of oysters in each estuary to foods by measuringchl a concentration and total suspended date of collection. To determine percent survival, we counted and organic particulate matter. Chi a was determined by 90% the number of living oysters in each transplant cage at collec­ acetone extraction and analyzed by spectrophotometry (Lor­ tion, divided by the total number planted, and multiplied by enzen 1967). Total suspended and organic particulate matter 100. were determined from the mass of dried filters (at 60 °C to a constant mass) before and after ashing at 490 °C for 4 h. Suspended particles To determine the quantity and quality of suspended par­ Environmental attributes ticles available as food for oysters during the growing season, Salinity was measured using a handheld salinity refractom-

Published by NRC Research Press Carmichael et al. 1137

eter with automatic temperature correction (Fisher Scientific). Temperature was measured using a Carolina armored water thermometer (N1ST certified, 0.5 °C accuracy). Parameters were measured adjacent to cages at each transplant site prior to collecting water samples.

Stable isotope analysis and N content in oysters To determine whether N assimilated into oysters was de­ rived from anthropogenic sources, we measured the N stable isotope ratios in suspended particulate matter (available foods) and oyster tissues. Soft tissues were aggregated from IO randomly selected oysters on each removal date to yield four replicate aggregate samples for each site (because of mortality, two replicates were processed for Snug Harbor on day 84). Samples were dried to a constant mass at 60 °C and ground to a powder with a mortar and pestle. Tissues and dried filters containing suspended particulate matter were an­ alyzed by continuous flow isotope ratio mass spectrometry (IRMS) at the University of California Davis Stable Isotope Facility (Davis, California). All samples were analyzed on a PDZ Europa 20-20 mass spectrometer after combustion in a PDZ Europa Automatic Nitrogen and Carbon Analyzer-Gas Solid Liquid. Gases were separated on a Supelco Carbosieve G column before IRMS. Machine reproducibility was 50.02%0 and was determined by analyzing randomly selected subsamples for 10% of the samples. N content in oyster soft tissues was determined by com­ 'b '°0 bustion during stable isotope analysis. To ensure N content X X 00 se:t reflected ambient rather than residual hatchery conditions, N 0 0 content data were used only from oysters sampled on day 112.

'°000 '° J 'b 'b N removal and bioremediation calculations X X 00 N To calculate the capacity of oysters to remove N and re­ 0 0 mediate eutrophication, we used a two-step process. First, we applied empirical estuary-specific growth and N content data from transplanted oysters to estimate estuary-specific times to reach harvestable size (Th) and used regression anal­ ysis to extrapolate the corresponding soft tissue N content °'00 when oysters did not reach harvestable size within the study season. We opted to define harvestable size as 76.2 mm shell height because it is representative of practices of the USA oyster fisheries (T. Getchis, East Coast Shellfish Growers As­ sociation, 1623 Whitesville Road, Toms River, NJ 08755, USA, personal communication, 2010; MacKenzie 1996; Hig­ 1 1 gins et al. 2011 ). X X \D Second, we estimated the number of oysters required to as­ C") 0 ·= N v::, similate and store the N in each estuary during the time pe­ riod between planting and harvest (Th) based on (i) land­ derived N load to each estuary and (ii) N in phytoplankton available in each estuary. We used these approaches to ac­ count for dissolved inorganic N loaded to the estuary from external sources (land-derived N loads) as well as to roughly account for additional N regenerated within or otherwise con­ veyed to the estuary, including from biodeposits by oysters, which may contribute to algal production (phytoplankton N) 4... 0 and symptoms of eutrophication (Kemp and Boynton 1984; Mayer et al . 1998; Souchu et al. 2001). We used phytoplank­ ~ ton N rather than N content in suspended particulate matter 32"' "°:::, = :.a for this calculation because it is likely most reflective of con­ r.l) u sumed diet and is consistent with estuary-specific phyto-

Published by NRC Research Press 1138 Can. J. Fish . Aquat. Sci. Vol. 69, 2012 plankton dynamics and bivalve growth responses measured phytoplankton N to the whole estuary volume provides only during this and other studies (Riera et al. 1999; Carmichael a rough estimate of the possible N in phytoplankton that may et al. 2004a; York et al. 2007). be available to oysters in these estuaries (Shaffer and Onuf 1985). Our approach composites data from a variety of spa­ Determining Th tial and temporal scales, including values generally represen­ The number of growing seasons required to reach harvest­ tative of si milar shallow water bodies, to generate an estimate able size (Th) was defined as the time period between plant­ based on the suite of best available data (e.g., Shaffer and ing and when oysters reach a length of 76.2 mm. Th was Onuf 1985). These estimates, however, may not capture calculated from estuary-specific growth rates, assuming short-term horizontal or vertical patchiness in biomass that growth occurred only during the growing season (mid-May - may occur in response to environmental variation or grazing, mid-October) in Cape Cod. Th was estimated by first deter­ despite the shallow, well-mixed attributes of the estuaries mining the number of days to reach harvest size by extrapo­ (Cloem et al. 1985; Monbet 1992). These values also do not lating from the equation for the lines best fit to the regression account for the potentially greater compensatory responses of of shell height compared with sampling day for each estuary. phytoplankton to the presence of oysters as estimates are We divided the number of days to reach 76.2 mm by the scaled up to higher densities. While approximate, this number of days estimated for a typical growing season scaling-up effort in terms of phytoplankton N is grounded in (~ 153 days) to determine the number of seasons (Th) to reach empirical site-specific data and important given that both 76.2 mm. This estimate of growing season length was consis­ land-derived and regenerated N sources may contribute to eu­ tent with conditions during this study and previous observa­ trophic conditions and available food supply for bivalves in tions for the mid to northern Atlantic region (Loosanoff and the estuary (Malone et al. 1988; Underwood and Kromkamp Nomejko 1949; Rheault and Rice 1996; Soniat et al. 1998). 1999; York et al. 2007). Hence, phytoplankton N load is con­ This estimate is also reasonable given the relatively short pe­ sidered a rough estimate of maximum N available in foods riod of growth to harvestable size for these estuaries, and be­ for oysters in our study estuaries. cause the smaller amount of growth that may occur during the remainder of the year (colder periods) is likely balanced N removal by tissue assimilation by a reduction in growth with age as bivalves approach legal To determine the amount of N assimilated into oyster soft size and not accounted for in a linear model (Askew 1972). tissues and potentially removed at harvest, we used estuary­ specific dry mass to shell height relationships (Table 3) to Land-derived and phytoplankton N loads extrapolate dry mass at legal size. We multiplied the resulting To calculate land-derived N loads and phytoplankton N in value by the mean %N content measured in soft tissues at the each estuary during oyster growth to harvestable size, we end of the study (day 112). For simplicity and because oys­ multiplied Th by total annual land-derived N load (Table 2) ters were planted at a small size (~8 mm), we assumed N and by estimated seasonal phytoplankton N in the estuary. content in oysters was negligible at the start of this study Seasonal phytoplankton N load was calculated by multiply­ and did not subtract initial N content from our N removal es­ ing the empirical mean chi a concentrations measured in timates. N assimilated into shell (estimated at 0.08%-0.8%; each estuary by estuary volume at mean tide height (Table 2) derived from Carriker 1996; Lee et al. 2011 ; R.H. Carmi­ and assuming a N:chl a ratio of 12.8 ± 1.5 (MacIntyre et al. chael, unpublished data) was not included in these calcula­ 2002). Although the N:chl a ratio will necessarily vary with tions because of the questionable ability to accurately the composition of phytoplankton in a given area, we opted estimate organic N content in shell at the time of study (Car­ to use this value because it is comparable to values previ­ riker 1996). ously applied to make similar calculations (Newell et al. 2005) but was refined based on raw data from a long-term N removal by denitrification and burial data set (MacIntyre et al. 2002). To roughly capture interan­ To include rough estimates of potential biogeochemical N nual and spatial variation in production, we used mean chi a removal (Nd) stimulated by bivalve biodeposits, we combined concentrations measured during this study and in two pre­ our field data with estimates of N removal by denitrification vious studies, including measurements throughout the estuary and burial (0.75 g N per gram of oyster dry mass per year) and along a salinity gradient (Weiss et al. 2002; Shriver et al. predicted by ·Newell et al. (2005). Since oysters were actively 2002; Carmichael et al. 2004a). Because the concentration of growing and changing size during the study, we extrapolated chl a will also vary with tidal flow and season, we opted to this additional N removed during Th by plotting estuary­ use a mean seasonal value based on samples collected across specific mean dry mass at each sampling day compared with different tidal cycles during the period of greatest bivalve calculated Nd for I day at that mass (assuming 0.002 g N re­ growth in our region. The resulting values were also within moved per gram of oyster dry mass per day). We used the the range of median seasonal chi a concentrations in estuaries slope of the resulting best-fit regression line for each estuary worldwide (Cebrian and Valiela 1999). Previous work indi­ as a rate of estuary-specific N removal (mg N-day- 1) via de­ cates this approach is appropriate to the physical and biolog­ nitrification and burial for oysters in this study. To determine ical dynamics of these estuaries (Jay et al. 1997; Shriver et total Nd during time to harvest, we then multiplied each rate al. 2002; York et al . 2007). by the estuary-specific number of days required for oysters to Because of the spatial and temporal heterogeneity inherent reach harvest size. We determined the percent enhancement in making estimates of primary production and biomass in of N removal provided by denitrification and burial by divid­ estuaries (Malone et al. 1988; Underwood and K.romkamp ing Nd at harvest by N in tissues at harvest and multiplying 1999), we emphasize that this effort to scale-up estimates of by 100. To roughly estimate N removal by oysters if not har-

Published by NRC Research Press Carmichael et al. 1139

Table 3. Equations and regression statistics describing the change in shell height through time and corresponding soft ti ssue dry mass and shell height relationships shown in Fig. 3.

Shell height Dry mass Estuary y R2 df F p y R2 df F p Sage Lot Pond 0.25x + 6.85 0.94 4 50.13 0.01 Wild Harbor O.3Ox + 10.77 0.97 4 109.75 0.002 O_OO5o.os9., 0.85 38 202.40 <0.0001 Green Pond O.39x + 11.06 0.95 4 61.37 0.004 O_OO80.os2 x 0.88 38 259.16 <0.0001 Snug Harbor 0.26x + 11.07 0.93 4 38.37 O.QI 0_0070.oss x 0.91 39 390.20 <0.0001 Childs River 0.31 x + 12.26 0.91 4 31.53 0.01 0.0100.072, 0.84 34 171.54 <0.0001

Table 4. Mean (± standard error) oyster shell and soft tissue growth rates, number of growing seasons to reach typical harvestable size of 76.2 mm (Th), and soft tissue dry mass (DW) and N content at harvestable size in Cape Cod estuaries.

Oyster growth rates Shell height Soft tissue DW at harvest Tissue N at harvest 1 Estuary (mrn·day- 1) (mg-day- 1) Th (g-oyster- 1) (g·oyste, ) Sage Lot Pond 0.25±0.04 1.7±0.5 1.8±0.3 Wild Harbor 0.30±0.03 1.8±0.1 1.4±0.2 4.1±1.3 0.35±0.11 Green Pond 0.39±0.05 6.8±2.0 1.1±0.2 4.2±1.2 0.36±0.10 Snug Harbor 0.26±0.04 2.3±0.4 1.7±0.3 4.4±1.1 0.38±0.09 Childs River 0.31±0.06 2. 1±0.5 1.4±0.3 2.4±1 .2 0.20±0.11 Note: Oysters in Sage Lot Pond did not grow sufficiently to reliably determine dry mass at harvest size. Tissue N at harvest was based on a mean of 8.6% ± 0.2% N in oyster tissues on day 112.

vested, we calculated Nd after I year at legal size by assum­ except for Sage Lot Pond (SLP) and Wild Harbor (WH), in ing no further growth, multiplying dry mass at harvest which cages were lost after day 28 and data were collected (Table 4) by 0.75 g N (Newell et al. 2005), and adding this from only one site. To compare the rate and magnitude of number to Nct during Th . growth among estuaries, regression analyses of shell height and dry mass through time were followed by a test for homo­ Quantifying capacity for bioremediation geneity of slopes (Sokal and Rohlf l 981) and analysis of cova­ Given the estuary-specific N removal per oyster at harvest riance (ANCOVA). Data were log-transformed, as needed, size, the actual capacity for bioremediation depends on the before testing for significance of regression and higher-order density and area on which bivalves are planted. Because den­ statistics. Type II regression was used when error was present sity and area planted can vary, we opted to first determine in the independent variable (comparison between growth rate the number of oysters needed to remove 100% of N loads in and chl a concentration, &15N in tissue, and suspended particu­ each estuary. We then determined the density of oysters re­ late matter). A one-way ANCOVA was used to compare sur­ quired to support this N removal if the entire bottom area of vival, suspended and organic particulate matter concentrations, each embayment were available and suitable for oyster and environmental attributes among estuaries. Since sample growth. The number of oysters required to remediate 100% sizes were not equivalent among estuaries (owing to cage loss of land-derived and phytoplankton N loads was determined from two sites), we averaged site values for each sampling date by dividing each N load during Th (the cumulative load dur­ to obtain estuary means for each variable on each sampling ing growth to harvest size) by the quantity of N in each oys­ day. Regression analyses, including F tests, were performed in ter at harvest size. Microsoft Excel 11.3.7. All other analyses were performed in To estimate more realistic N removal capacities at lower Stat View 5.0.1 (SAS Institute Inc., Cary, North Carolina). A coverage areas, we calculated N removal by oysters if planted significance value of P < 0.05 was used for all tests. at typical restoration and aquaculture grow-out densities of Each N stable isotope ratio data point represents the mean varying intensity (which also may account for different gear of data from two sites in each estuary from which aggregates types) at 0.5%-5.0% bottom area coverage. We multiplied of 10 individuals were replicated two to four times per site, the Nin each oyster at harvest size by 75 and 15O-m-2 (resto­ depending on the number of individuals available from each ration) and 400, 550, and 1650-m-2 (aquaculture) densities estuary (indicated above). Error reported for calculated values and by the appropriate surface area of each estuary (calcu­ were propagated from empirical field measurements (Valiela lated from values in Table 2). The resulting N removal esti­ 2001). All error is reported as standard error unless otherwise mates were compared to land-derived and phytoplankton N noted. For higher-order extrapolations (cumulative N loads, loads during the time to reach harvest size (Th). numbers of oysters, and area required for remediation), error is reported as coefficient of variation (CV) to most accurately Statistical analysis reflect the scale of relative variation in these data among es­ All growth and environmental data are reported as the mean tuaries. Where error bars are not visible in figures, error was of data from two replicate cages at two sites in each estuary, smaller than the symbol.

Published by NRC Research Press 1140 Can . J . Fish. Aquat. Sci. Vol. 69, 2012

Fig. 3. Mean (± standard error) shell height (a) of oysters trans­ Fig. 4. &15N in oyster ti ssues on days 28, 56, 84, and 112 compared planted into five Cape Cod estuaries on day 0 and removed on with percent contribution of wastewater to N load (from Table 2) days 28, 56, 84, and 112 and the corresponding soft tissue dry received by five Cape Cod estuaries (a) and on day 112 compared mass (b). Regression statistics are shown in Table 3. with &15N in suspended particulate matter (SPM; b). Dashed grey 15 (a) oSage Lot Pond lines show mean & N in oyster tissues at day 0 (a) and the I : 1 line 54 O Wild Harbor where points would fall if there were no isotope fractionation from eGreen Pond food sources (SPM) to oyster tissues (b). Data points in panel (a) -E • Snug Harbor show the mean (± standard error) of four samples for each date. E 42 .t, Childs River Where no error bars are present, error is smaller than the symbol. Panel (b) shows all four data points for day 112. Wastewater: y = -.c - 2 0, 1.46 ln(x) + 2.77, R = 0.88, Frcgrcssion 4 = 23.34, P = 0.02; SPM ·a5 2 .c 30 (type II regression): y = 1.18 x + 0.88, R = 0.94, F regression 19 = 267.85 , P < 0.001. Q) .c (a) 9.5 U) 18

6 7.5 0 20 40 60 80 100 120 Days 5.5 028 (b) 1.5 056 0 e84 -~ • e112 -z 3.5 ID 0 20 40 60 80 100 § 1.0 ~ Wastewater(%) 3: (J) 0 • Q) Q) :::, ::, (J) (b) o Sage Lot Pond (/) (J) OWild Harbor (/) 0.5 8.5 t= i= eGreen Pond • Snug Harbor .t,Childs River 6.5 ...... 0.0 ...... ,.,.,,,, ...... 12 26 40 54 68 ...... 4.5 ...... Shell height (mm) -...... Results 2.5 +-----.---.--...,,....----r----..---- ...... - ...... 2.5 3.5 4.5 5.5 6.5 Field measurements SPM 015 N (%0) Oyster growth and survival Oyster shell and soft tissue growth rates were in the range dry mass of tissues increased exponentially with sheJI height in all estuaries (Fig. 3b). Relative dry mass content during of 0.25--0.39 and 1.7-6.8 mg-day-1, respectively (Fig. 3; Ta­ the time to reach harvest size, however, differed by estuary bles 3 and 4). Morphometric ratios between shell height, (Table 4; test for homogeneity of slopes: F[u, 1.37, P length, and width were similar among estuaries (one-way 31 = = 0.26; ANCOVA: Ft1•31 = 5.80, P < 0.001), with the larger analysis of variance (ANOVA) for each ratio L:W, L:H, W:H oysters in Green Pond having greater corresponding dry compared among estuaries, Ft4•151 < 2.04, P > 0.14; data not mass (Fisher's partial least-squares difference for dry mass, shown). Hence, shell height (shown in Fig. 3a) was a suitable P < 0.0001 for all comparisons with Green Pond). Survival measure of relative shell growth for this study. SheJI growth ranged from 82% to 97% and did not differ among estuaries was generally highest among oysters in Green Pond and low­ (Table 2; one-way ANOVA: F ll.4J = 2.40, P = 0.12). est in Sage Lot Pond (Fig. 3; test for homogeneity of slopes: Fll.4,41 = 1.65, P = 0.21 ; ANCOVA: Fll.4J = 5.93, P = Environmental attributes 0.003). On average, oysters achieved 61 % ± 4% of harvest Chl a concentrations at oyster transplant sites increased size (76.2 mm height) within the study period, with the fast­ with increasing land-derived N load to estuaries (Supplemen­ est growing oysters exceeding 80% of harvest size (Fig. 3a). tal Fig. S la 1) . Oyster growth rates, in tum, increased with in­ Data for Sage Lot Pond were excluded from subsequent cal­ creasing chi a concentration among estuaries, but were culations because oysters in this estuary did not grow suffi­ stratified by salinity (Supplemental Fig. S Ib1) . In higher N­ ciently to achieve at least 50% of harvest size (Fig. 3a). The loaded estuaries in which salinity measured at or below 23

1Supplementary data are available with the article through the journal Web site at http://nrcresearchpress.com/doi/suppl/l0.11 39/f2012-057.

Published by NRC Research Press Carmichael et al. 1141

on 10%-30% of sampling dates (Snug Harbor and Childs River), oyster growth was depressed despite higher chi a con­ 1 centrations (>14 mg·m-3; Supplemental Fig. Slb ). Sus­ pended and organic particulate matter and water temperature did not vary significantly among estuaries and showed no re­ lationship to oyster growth (Table 2).

N stable isotope ratios &15N values in tissues confirmed that transplanted oysters assimilated N from local anthropogenic sources. Through time, &15N values in oysters moved away from hatchery val­ ues (Fig. 4a, grey dashed line) toward estuary-specific N sta­ ble isotope ratios that increased with increasing percent wastewater inputs to the adjacent watersheds. Oyster tissues also showed an approximately 2%o-4%o enrichment com­ pared with suspended particulate matter in each estuary, typi­ cal of a single trophic step from the estuary-specific food source to consumer (Fig. 4b).

Land-derived and phytoplankton N loads ..,.'.:"' > ' Total land-derived N loads to study estuaries during Th -~~ObOO (roughly one to two seasons) ranged from 4 500 to =E:zxxxx 12 000 kg N (Table 5). The estimated N available in phyto­ ::, oil °'• • \0 • 0 . ~ 0000..\0 U '-' N plankton standing stock during the same period was up to 24 times higher than land-derived N loads and ranged from 60 000 to 281 000 kg N-Th- 1 (Table 5). The greatest cumula­ tive N loads were estimated in Green Pond, owing to the high annual land-derived N load and larger embayment area and volume of this estuary (Tables 2 and 5).

N removal and estimated bioremediation In this section, we quantified oyster capacity for N removal via harvest and estimated theoretical N removal by denitrifi­ cation and burial. We then compared the empirical estimates of N removal by tissue assimilation with land-derived N .,., \0 .,., r- N <""i <""i r--i loads and N in phytoplankton to evaluate embayment-scale § ct' r±1 ~ j} remediation of eutrophication. ~N~~~ N removal by assimilation into tissues N content in oyster tissues averaged 8.6% ± 0.2% and did not differ among estuaries. Hence, the mean value was used for subsequent N removal calculations in all estuaries. Based on estuary-specific oyster growth rates (Tables 3 and 4) and %N content, N assimilation and potential removal was esti­ mated at 0.3-0.5 g N per oyster, if harvested at 76.2 mm (Ta­ ble 4). The estimated time for oysters to reach harvest size was less than two growing seasons (Th = 1.1-1.8 years) and resulted in mean dry mass of 2-4 g per oyster (Table 4). Although the %N content in tissues was similar among estua­ ries, the significant differences in relative dry mass at harvest size (Fig. 3 and Table 4) resulted in different N content per :a § oyster and therefore different N removal capacities via tissue u N assimilation (Table 4).

Estimated N removal by denitrification and burial Assuming the potential for increased denitrification due to biodeposit production by oysters was equivalent to 0.75 g N removed per gram of oyster dry mass annually (Newell et al. 2005), we estimated that denitrification and burial could the­ oretically enhance N removal by 1% -2% during growth to harvestable size (Table 6) . Hence, N removal by biogeochem-

Published by NRC Research Press 1142 Can. J. Fish . Aquat. Sci. Vol. 69, 2012

Table 6. Equations and regression statistics for estimated N removal (mg) through burial or denitrification per oyster compared with sampling day (0, 28, 56, 84, 112), based on estuary-specific dry mass measured in this study and N removal rates reported by Newell et al. (2005).

Th Nd during Th Additional N Nd I year after Th 1 1 Estuary y R2 df F p (days) (g N-oyster- ) removed (%) (g N-oyster ) Wild Harbor 0.03x- 1.49 0.84 5 20.79 0.01 217 0.007±0.002 2. 1± 1.0 3. 11±0,99 Green Pond 0.04x - 1.19 0.83 5 19.98 0.01 167 0.006±0.001 1.7±0.7 3.19±0.92 Snug Harbor 0.03 X - 1.52 0.89 5 33.24 <0.01 255 0.009±0.002 2.3±0.8 3.34±0.86 Childs River 0.02x - 0.73 0.86 5 25.11 <0.01 208 0.004±0.001 2.1±1.5 1.78±0.93 Note: These relationships and T, (reported in days) were used to estimate N removal due to burial or denitrification (N.) during growth to harvest size, the %N removed by these processes in addition to N assimi lation into tissues, and potential N removal by denitrification and burial if oysters are retained in the estuary for I year after reaching harvest size (assuming no further growth ).

Table 7. The number and density of harvest size (76.2 mm) oysters needed to assimilate 100% of land­ derived and phytoplankton N (Ph N), assuming the entire bottom area was available for rearing oysters in four Cape Cod estuaries.

To assimilate land-derived N To assimilate Ph N 2 No. Density (m-2) CV(%) No. Density (m- ) CV (%) Wild Harbor l.3xl01 26 26 3.lxl08 632 28 Green Pond 3.2xl07 54 34 7.7xl08 1287 49 Snug Harbor l.9xl07 104 42 2.5x!08 1396 54 Childs River 5.5x107 405 48 3.0xl08 2206 54

Note: Estimates do not include potential N removal by denitrification or burial. CV, coefficient of variation. ical processes appeared to be small compared with N assimi­ coverage in lower N loaded estuaries or where oyster growth lated into tissues during the first one to two seasons of was highest (Wild Harbor and Green Pond; Figs. Sa and Sb). growth (compare Tables 4 and 6). This same approach sug­ Under restoration and aquaculture conditions that seem most gests that retaining harvest-sized oysters (76.2 mm) in the es­ common in the USA at present (oyster densities ~ 400 m-2 tuary for up to 1 year after reaching harvest size could and when planting area is relatively small compared with total produce sufficient biodeposits to increase N removal by estuary area), estimated N removal capacity decreased to nearly an order of magnitude beyond N assimilation in tis­ ~15% of land-derived loads and <1 % of phytoplankton N sues (when immediately harvested) (Table 6). (Fig. 5). We considered only N removal via soft tissue assimi­ lation for these comparisons because we empirically quantified Determining the relevance and scale of N removal estimates this metric, and tissue assimilation was estimated to be the N removal by assimilation into tissues or by stimulation of dominant N removal process during growth to harvest size. biogeochemical processes depends on N removal per oyster as well as the density and area on which bivalves are grown. Discussion As a point of departure, we calculated how many oysters were needed to remove 100% of the land-derived or phyto­ In this study, as in many others, land-derived N loads fed plankton N loads to each estuary and determined the density local production and contributed to high local phytoplankton of planting that this level of remediation would require. We biomass, in turn providing useful endpoints for the range of do not suggest 100% N removal as a remediation goal, but potential N loads to be remediated in receiving estuaries. rather use this value as an endpoint to further evaluate the While land-derived N loads to our estuaries are typical of es­ scale of potential N removal. We estimated that 13-55 mil­ tuarine systems in the USA, our estimates of phytoplankton lion oysters would be required to assimilate and remove all N were high relative to N contributed by phytoplankton re­ embayment-wide land-derived N loads and at least 250 mil­ ported elsewhere (Malone et al. 1988). These high estimates lion to assimilate all of the estimated phytoplankton N load are likely due to heterogeneity in phytoplankton biomass (Table 7). Assuming the entire estuary were available and throughout the estuary, which cannot be systematically ac­ suitable for planting, these numbers of oysters correspond to counted for with the available data. These values, therefore, densities of roughly 30--400 m-2 to remediate 100% of the are considered a maximum value for N potentially available land-derived N load and 600-2200 m-2 to remediate 100% in foods for oysters within the estuary during the time to of phytoplankton N (Table 7). reach harvest size (roughly two growing seasons), and atten­ To give our findings a more biologically relevant context, tion should be given to the error associated with these values. we also determined %N removal capacity under different These values are important, however, because phytoplankton planting densities and at more realistic bottom coverage areas biomass directly relates to water turbidity and low dissolved of 0.5%-5% of the estuary (corresponding to approximately oxygen concentrations that are important management con­ 0.1-3.0 ha coverage in these estuaries; Fig. 5). Under the vari­ cerns (Cloern 2001; Valiela 2006). Hence, phytoplankton N ous N removal scenarios we tested, maximum N removal ca­ may be the form most important to assessing remediation of pacity was estimated at 20%-100% of land-derived N loads the symptoms or negative effects of eutrophication. We as­ and 4%-13% of phytoplankton N and occurred at 5% bottom sessed N removal capacity by oysters in these estuaries rela-

Published by NRC Research Press Carmichael et al. 1143

Fig. 5. Estimated removal of land-derived or phytoplankton N (%) by assimilation into oyster tissues if planted at typical restoration and aquaculture densities (75, 150, 400, 550, 1650-m-2) over different areas of percent bottom coverage (0.5, 1.0, 5.0) in four Cape Cod estuaries. Land-derived Phytoplankton

100 (a) Wild Harbor 2 Density (m- ) 12 80 • 75 • 150 60 8 400 40 0 550 4 0 1650 20

0 ~-11;.:;..JL_II-

100 (b) Green Pond 80 60 -~0 -co 40 > 0 20 E 0 --'-'---L...1._..,. ...IL...I _. ~ z 100 ( c) Snug Harbor "'C $ 80 E 60 ':,i:j en 40 UJ 20 0 -+--~--4----IIIIL::J.---

100 (d) Childs River 80 60 40 20 0 -+---~-----...... ~~ 0.5 1.0 5.0 0.5 1.0 5.0 Coverage (%)

Published by NRC Research Press 1144 Can . J . Fish. Aquat. Sci. Vol. 69, 2012

tive to both the land-derived N load (external N sources classes may vary if younger, smaller oysters are planted at alone, reflecting the minimum N load to be remediated) and higher densities than larger counterparts and if juvenile oys­ the phytoplankton N load (total N theoretically available in ters produce more biodeposits than we predicted based on lit­ food for bivalves, representing a possible maximum N load erature estimates from larger-sized oysters (Newell et al. to be remediated). 2005). It is also important to consider the practical limita­ tions to grow-out practices that may be required to encourage N removal via tissue assimilation bivalve-stimulated denitrification. The N removal benefits of Oysters assimilated anthropogenic N but showed the great­ retaining oysters in the estuary after harvest size, particularly est potential to remediate N loads in estuaries that were not for commercial growers, may not outweigh the increased pro­ highly eutrophied. Our estimates indicated that lower N­ duction costs, heightened risk of Joss, and greater exposure to loaded estuaries or those in which oyster growth rates were diseases (Ewart and Ford 1993; Lafferty et al . 2004). N re­ particularly high could support enough oysters to assimilate moval by biogeochemical processes through time, therefore, land-derived N when planting area and density were rela­ may be more important to restoration projects focused on tively high. Even at high densities, however, phytoplankton ecosystem services as opposed to fishery yields. N removal of more than a few percent required planting over The extent to which these estimates are relevant to the nat­ large areas of bottom that may make remediation impractical ural environment and can be scaled up to an estuary is not relative to estuary size. It is important to consider that a vari­ clear. In particular, the effect of estuary-specific variation in ety of factors limit the area available for planting shellfish in sediment type and composition, hydrology, microbial com­ suburban estuaries like those we studied, including variability munity composition, benthic consumers, and other factors in habitat quality, structures (e.g., docks, revetments, piers, may affect rates of N removal via burial or denitrification jetties, bottom debris), zoning and regulations protecting pub­ and other biogeochemical processes (Newell et al. 2005; Seit­ lic rights for commercial and recreational capture fisheries zinger et al. 2006; Ferguson and Eyre 2007). For example, and swimming, national shellfish sanitation program classifi­ variation in local tidal or current flow may dilute and redis­ cations, and aesthetic preferences. When you consider that tribute biodeposits to remote locations so that effects may be only 1.0% of bottom area in our study sites represented as diminished or difficult to detect and relate to grow-out efforts much as 0.5 ha (an area larger than a standard football or (Tenore et al. 1985; Chamberlain et al. 200 I; Forrest et al. soccer field), it is easy to perceive why N removal may be 2007). In some cases, high intensity aquaculture activities spatially impractical in some water bodies. Application of bi­ may change local environmental conditions in ways that me­ valve remediation measures should consider the potential for diate capacity for denitrification (Newell 2004), such as by enhanced N removal at high oyster densities to be mitigated reducing dissolved oxygen and enhancing sulfide concentra­ by overcrowding or changes in habitat quality such as re­ tions (Chamberlain et al. 2001 ; Christensen et al. 2003; Forr­ duced dissolved oxygen concentrations that can impair the est and Creese 2006). Measurements in Cape Cod estuaries growth and sustainability of shellfish stocks and ultimately (i.e., Sage Lot Pond and Childs River) indicate naturally oc­ diminish the capacity for bioremediation (Rheault and Rice curring denitrification could account for 32%-37% dissolved 1996; Ferreira et al . 2007). Overall, our data suggest N re­ inorganic N loss in the estuaries we studied (Lamontagne and moval capacity of 1% -15% is most realistic given the condi­ Valiela 1995; Lamontagne et al. 2002). Denitrification rates tions typical to restoration and aquaculture activities in USA in other estuaries reportedly range from 7% to nearly 60% of estuaries and depending on available space. This finding is total dissolved inorganic nitrogen load, depending on location consistent with previous estimates across a range of different (Nowicki et al. 1997). If N removal by denitrification stimu­ estuaries (e.g., Haamer 1996; Songsangjinda et al. 2000; Hig­ lated by oyster biodeposits equals or dominates N assimilated gins et al. 2011). We conclude that the capacity for N re­ into soft tissues by the time oysters reach harvestable size, moval by oyster harvest is likely to be modest relative to our data suggest total N removal by oysters would be compa­ total N load and limited by the area of available habitat in rable to these previously reported naturally occurring rates. A many estuaries where remediation efforts are most needed: recent field study that measured denitrification in sediments those with active, urbanized watersheds and high particle adjacent to oyster reefs found somewhat lower denitrification loads. rates than predicted by the literature values we applied, but corroborated that rates were highest in summer during peak N removal by biogeochemical processes feeding and growth and strongly correlated with sediment Inclusion of rough literature estimates for N removal oxygen demand (Piehler and Smyth 2011 ). Denitrification ca­ stimulated by biodeposition suggests that biogeochemical pacity, therefore, is likely to be location-specific, and varia­ processes have potential to enhance capacity for N removal tion with intensity and type of bivalve aquaculture or by oysters. Our findings indicate that during the first one to restoration activity needs to be determined. two seasons of growth, tissue assimilation was the dominant Further empirical and estuary-specific study is needed to form of N removal for individual oysters, but after reaching refine and corroborate N removal estimates via stimulation harvestable size, denitrification could become the dominant of biogeochemical processes. These data, in turn, will help process. These estimates should be taken with caution be­ quantify ecosystem services provided by bivalves and guide cause the rates of biogeochemical N removal applied in this how oysters may best function as a N management or resto­ study were based on a lab study (using the Ni:Ar method ap­ ration tool (Pomeroy et al. 2007; Coen et al. 2007; Grizzle et plied to simulated biodeposits in cores) and a subsequent al. 2008). A number of shellfish-related denitrification studies modeling effort (Newell et al. 2005). The differences we esti­ have been performed on large scale, deepwater mussel farms mated in N removal by denitrification among oyster age in Europe and Japan (e.g., Haamer 1996; Kohama et al.

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0 Cite this: Environ. Sci. Technol. 2020, 54, 24, 16156-16165

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Coastal Nitrogen Management

Eutrophication is a global environmental challenge, and diverse watershed nitrogen sources require multifaceted management approaches. Shellfish aquaculture removes nitrogen, but the extent and value of this ecosystem service have not been well-characterized at the local scale. A novel approach was employed to quantify and value nitrogen reduction services provided by the shellfish aquaculture industry to a municipality. Cultivated hard clam and eastern oyster nitrogen removal in Greenwich Bay, Connecticut, was valued using the replacement cost methodology and allocated by municipal nitrogen source. Using the preferred analysis allocating replacement costs by nitrogen source, aquaculture-based 1 removal of 14 006 kg nitrogen was valued at $2.3-5.8 (2.3-6.4€) million year- • This nitrogen removal represents 9% of the total annual Greenwich-specific nitrogen load, 16% of the combined nonpoint sources, 38% of the fertilizer sources, 51% of the septic sources, 98% of the atmospheric deposition to the watershed, or 184% of the atmospheric deposition to the embayments that discharge to Greenwich Bay. Our approach is transferable to other coastal watersheds pursuing nitrogen reduction goals, both with and without established shellfish aquaculture. It provides context for decisions related to watershed nitrogen management expenditures ~nd suggests a strategy to comprehensively evaluate mechanisms to achieve nitrogen reduction targets.

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The primary target of most coastal nutrient reduction programs has been nitrogen, which frequently limits primary production.(g,Z). (but also see ref .(B).) . Nitrogen management programs to date largely have focused on restricting land-based sources ..(9 - 71). Point sources of nitrogen, which have a well-defined waste stream, are well-characterized in many locations and have been a priority for nitrogen reduction. These include wastewater treatment plants (WWTPs) and large animal feeding operations. In contrast, nonpoint sources of nutrients, such as stormwater, car emissions, and fertilizer, are much more challenging to quantify and require multifaceted management approaches ..(7 2).

There has been growing interest in the potential contributions of shellfish aquaculture to nitrogen management in the Un ited States and Europe ..(7 3-15). Two programs in the Un ited States have incorporated shellfish aquaculture formally within overall nitrogen reduction planning at scales both local.(]..Q). and regional. .(7 7). Shellfish naturally remove plankton and detritus from the water through suspension-feeding activities and incorporate nutrients from ingested food into tissues, shell proteins, and other organic constituents during growth. When shellfish are harvested, nitrogen contained within the tissue and shell is removed from the local environment. There is some evidence that additional nitrogen reduction may be realized through enhancement of sediment denitriflcation by shellfish aquaculture activities,.(7 8). but to date, this pathway has not been incorporated into nitrogen management programs.

The nitrogen reduction services provided by shellfish aquaculture can be considered within a broader ecosystem service framework. Ecosystem services have been defined as the benefits that people receive from ecosystems ..( 12). These benefits may be quantified according to indicators of physical flows, such as tons of carbon sequestered or tons of fish provided, or using estimation of monetary flows with the assignment of dollar values ..( 20 ). Efforts are underway to develop accounting systems that rigorously catalog ecosystem services and associated ecosystem assets to better support the incorporation of ecosystem services into governmental planning decisions ..( 27 ). A key function performed by ecosystems is nitrogen cycling ..(22). We use the term "function" here though some ecosystem service categori zation approaches would refer to nitrogen cycling as an ecosystem "service" . When the balance of that cycle is disrupted through excess nitrogen inputs, a range of ecosystem services that directly benefit the public, such as clear water for boating, swimming, and water views and fish and ~hPllf1~h fnr r.nn~11mntinn m:=iv hP rli~n 1ntPrl (?11 M1 iltinlP fiplrl :=inrl l:=ihnr:=itnrv ~t11rliP~ h:=ivP

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sequestration by the value of a nitrogen nutrient credit within existing, relevant trading programs. By comparing the removal rates of nitrogen by an oyster reef versus soft bottom habitat and then multiplying by the trading price per kilogram in North Carolina in 2011 ($28.23; 37 .33€), Grabowski et al..(32). estimated the benefits of nitrogen removal by an oyster reef to be in the range of $7 385-6716 (7 537-7454€) hectare-1 year-1. Two studies (Kim et al.,.(33,34).) used experimental data to estimate nitrogen removal by kelp farm systems, then multiplied this by the value of a nutrient credit in Connecticut (CT) to arrive at annual values of between $147 and 1226 (7 63-1360€) hectare-1, depending on the species and location of the farm.

Additional research in Long Island Sound, the Mission-Aransas Estuary in Texas, and the Chesapeake Bay in Maryland estimated the replacement cost for services associated with nitrogen sequestration by oysters. Replacement cost is an economic valuation approach for ecosystem services that uses the costs of the required substitute capital investments (e.g ., wastewater treatment plant (WWTP) upgrades) that provide equivalent services to the ecosystem. In the Mission-Aransas Estuary, Beseres Pollack et al. .(30). used field-based estimates of nitrogen removal rates by the existing oyster population to determine the necessary specifications (and cost) for equivalent implementation of biological nitrogen removal at a WWTP This analysis resulted in an estimated value for the nitrogen removal services of oysters in the Estuary of $713 477 (7 25 953€) year- 1. Bricker et al. .(31). evaluated oyster aquaculture in Long Island Sound as a nitrogen removal service by applying costs that would be associated with WWTP and agricultural or urban best management practices (BMPs). That study arrived at a value of between $8.5 and 230 (9.4-255€) million year- 1, depending upon the replacement technology and acreage covered. Using the average cost of alternative abatement technologies in the Chesapeake Bay at the time, Newell et al..(35). estimated the value of nitrogen removal by oysters in the upper Choptank to be approximately $37 5 000 (349 650€) year-1.

Researchers have also explored the economics of shellfish as a nutrient reduction strategy using optimization models that project the best mix of nutrient management approaches for meeting a specified target and the cost savings generated by including shellfish farming as part of that mix. For example, Gren et al..(3 6). provided an optimized cost-effectiveness model that includes mussel farming as an abatement measure for meeting Baltic Sea nutrient targets, finding cost reductions of up to approximately 0.37 billion euros with the inclusion of mussel

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This paper describes a novel and transferable approach to quantifying and valuing the nitrogen redu ction services provided by the shellfish aquaculture industry at a local scale. The novelty of the approach is its use of local-scale data on nitrogen sources as a means of allocating replacement abatement technologies (and their associated costs) based on locally calibrated values for nitrogen sequestration by clams and oysters in Greenwich Bay, CT. Recent literature reviews have highlighted the stability of percent nitrogen content within tissues and shells of bivalve shellfish across time and space, but also identified tissue dry weight per individual as much more variable,.(17). highlighting the need for local shellfish dry weight data. We demonstrate the application to a well-established industry, as well as the use of an aquaculture model to predict industry potential where limited or no industry currently exists. Leveraging the local-scale data on nitrogen sources within our target watershed from nitrogen load modeling performed by Vaudrey et al.,.(38). our valuation methodology better assigns potential replacement costs for lost clam and oyster nitrogen sequestration and removal services by constraining the analysis to the rea l-world options available to watershed resource managers. These improvements to the replacement cost methodology should provide a more detailed understanding of the potential tradeoffs associated with gains or losses of shellfish populations for consideration by natural resource managers and the public.

Materials and Methods Jump Tov

Study Location

Greenwich Bay is located on the northwestern shore of Long Island Sound on the Northeastern coast of the United States (Figure Sl ). The Town of Greenwich has devoted 6945 total seafloor 2 acres (28 km ) to three categories of shellfish use, including commercial shellfish aquaculture 2 of hard clams (Mercenaria mercenaria; 4173 acres (16.9 km )) and eastern oysters 2 ( Crassostrea virginica; 6.3 acres (0.03 km )), recreational shellfishing (primarily hard clams; 920 2 2 acres (3.7 km )), and seed oystering (7 835 acres (7.4 km )) on areas designated by the State of Connecticut as "natural beds" (K. DeRosia-Banick, State of Connecticut Department of Agriculture, Bureau of Aquaculture (CT DA/BA), personal communication). Commercial shellfish aquaculture leases are managed jointly by the CT DA/BA and the Greenwich Shellfish Commission, although leases are officially classified as "town" or "state" based upon distance

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CONTINUE https://pubs.acs.org/doi/10.1021 /acs.est.0c03066 5/28 7/29/2021 Quantification and Valuation of Nitrogen Removal Services Provided by Commercial Shellfish Aquaculture at the Subwatershed Scale IE. ..

ACS Publications Most Trusted. Most Cited. Most Read . Q. = SI1 ). Loads were obtained for five categories of nitrogen sources: (1) atmospheric deposition to the embayment; (2) atmospheric deposition to the watershed; (3) fertilizer; (4) sewer; and (5) septic. Fertilizer sources in the Greenwich subwatersheds were exclusively suburban lawns and golf courses, with crop agriculture contributions functionally zero. These authors modeled six subwatersheds that discharge directly into Greenwich Bay (Figu re Sl; Captain Harbor, Greenwich Harbor, Smith Cove, Indian Harbor, Mianus River, and Greenwich Cove) and a seventh subwatershed whose discharge at times likely influences Greenwich Bay (Byram River; see Supporting Information, Sl1 and Table S2 for more details). Nitrogen loads from the local Grass Island WWTP (47 million liters treated effluent day-1) were obtained for 2015 from the CT Department of Energy and Environmental Protection (CTDEEP; K. Streich, personal communication). Maps of effluent pipes suggest that the discharge is directly to Greenwich Bay (J. Vaudrey, personal communication), and it was included here as a separate load located outside of the seven subwatersheds.

Calculation of Nitrogen Removal by the Greenwich Shellfish Aquaculture Industry

The ecological component of this study estimated nitrogen removed from Greenwich Bay by sequestration in the tissue and shell of clams and oysters and subsequent removal from Greenwich Bay by shellfish harvest. The same general approach was applied to both species, combining the number of animals harvested with the expected nitrogen content of those harvested animals, to yield nitrogen removal achieved by harvest. Two versions of this approach are presented in Figure 1, one that was applied to a large and established industry in Greenwich Bay (hard clam, M. mercenaria), and a second that was applied to a new and relatively small industry (eastern oyster, C. virginica) . Methodological details of each step in Figure 1 are provided in Supporting Information, Sl2.

Figure 1

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Nitrogen Removed ~ ·ssue aod~II Annually by i:,,-•daH Greenwich Clam Harvest

itssue and'Shef~ dry weigntsbv~ct.ss ( ls.study} .

b. Predictive approach for small or no aquaculture industry

Avenge tissue and -sheftdry.wel8'tt-per ~'9'f5tel' { ~cty) Gram$ Nitrogen Removed Annually by Gre-enwfch Oyster Harvest Harvestnembers ·w id'atectby indusby .· ~l'tMI" Smlla Mir 9Yffli' COMpa,w

Figure 1. Approach for estimating nitrogen removal from cultivated shellfish in Greenwich Bay, Connecticut, based on the size of the local aquaculture in dustry. The blue box indicates steps to calculate animals harvested, the orange box indicates steps to calculate nitrogen removed by that harvest. (a) M. mercenaria harvest information, combined with direct measurements of local clams, and literature values for percent nitrogen content of the tissue and shell; (b) FARM model calibration and validation for C. virginica, combined with direct measurements of local oysters, and literature values for percent nitrogen content of the tissue and shell.

Economic Analysis

Two approaches were used to value oyster and clam nitrogen removal services within Greenwich: (7) valuation based upon the cost of nutrient credits traded in Connecticut and (2) estimation of the cost of replacing clam and oyster nitrogen sequestration services with engineered approaches.

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CONTINUE https://pubs.acs.org/doi/1 0.1021 /acs.est.0c03066 7/28 7/29/2021 Quantification and Valuation of Nitrogen Removal Services Provided by Commercial Shellfish Aquaculture at the Subwatershed Scale I E .. .

ACS Publications .. Most Trusted. Most Cited. Most Read. Q = bottom cultivation and Tis the trading system credit value estimated annually by CTDEEP. For 2016, the value of a one-pound nitrogen credit was $6.70 (7.44€).

Replacement Cost Estimation

The second approach calculated the value of nitrogen removal services using the estimated cost of replacing the clam and oyster nitrogen removal with a human-engineered approach (e.g., stormwater best management practices (BMPs), septic system upgrades). Similar approaches for cost estimation have been used previously ..(30 ,40). In essence, this assumes that the town or state could invest in engineered treatment that would provide equivalent effectiveness to the annual nitrogen sequestration services provided by clams and oysters.

The basic formula is C = N x Er, where C is the estimated total replacement cost, N is the number of annual pounds of nitrogen removed by clams and oysters, and Eis the cost per pound of nitrogen removal by engineered removal process r. The value for C was calculated in two ways: (1) under the assumption that wastewater treatment is the sole engineered removal approach used (therefore only one value of Er) and (2) with nitrogen removal allocated across sources and, subsequently, engineered approaches.

The cost of wastewater treatment per pound of nitrogen assumed capital upgrades for nutrient removal equivalent to the services provided by clams and oysters. Importantly, these costs do not include costs for connecting new households that currently are on septic systems or cesspools. To estimate the cost per pound nitrogen removal for wastewater upgrades, the average cost of nutrient removal upgrade per million gallons per day (mgd) capacity ($ mgd- 1) was first calculated using EPA data for upgrade costs at WWTPs in Connecticut (EPA 2006). Existing daily nitrogen removal at the Grass Island Treatment plant was estimated using its design capacity of 12.5 mgd in combination with its approximate removal efficiency of 75% (K. Streich, CTDEEP, personal communication). These values were compared with the nitrogen removal capabilities of current clam and oyster cultivation practices to estimate the total capital costs of equivalent engineered wastewater investments. Capital costs were annualized using straight-line depreciation, assuming a 15-year time period. Operating and maintenance (O&M) costs were assumed to be 5% of annualized capital costs, which is between conservative estimates for O&M used in previous work.(30 ). and reports provided to municipal authorities in New England considering wastewater treatment..( 41,42).

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CONTINUE https://pubs.acs.org/doi/10.1021 /acs.est.0c03066 8/28 7/29/2021 Quantification and Valuation of Nitrogen Removal Services Provided by Commercial She llfish Aquaculture at the Subwatershed Scale I E ...

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Septic upgrade costs were estimated based upon a report from investigations into improved septic technologies in West Falmouth, MA..(43). The average, annual cost per pound of nitrogen removal($ lb-1) was calculated based upon three test cases described (blackwater systems, eliminite systems, and hoot systems). Straight-line depreciation assuming a 30-year life span for the system was used to estimate annualized installation costs.

As cost data came from different time periods, all dollar values were inflated to 2016 using consumer price index data ..(44). All USO to Euro conversions were calculated based on a 2016 conversion of 1.11 € = $1.

Results and Discussion Jump Tov

Calculation of Nitrogen Removal by the Greenwich Shellfish Aquaculture Industry

Shellfish aquaculture has been practiced in the United States for over a century, but in many locations, it remains a new and growing industry. We have demonstrated two versions of our approach for calculating nitrogen removal to broaden its potential for application beyond the relatively few municipalities that have a large and well-established industry. The first version, based on a well-established industry, enables calculation of nitrogen removal from annual harvest reports. The second version, for municipalities with limited or no shellfish aquaculture, enables predictions of harvest-based nitrogen removal for a new or growing industry. Quantile regression analysis yielded equations for the 50th quantile of tissue dry weight as a function of 27 shell length (y= 0.0000037 x x3· ) and shell dry weight as a function of shell length (y= 70 0.00011 x x3· ) for Greenwich clams (Figure S4). Annual municipal-scale clam aquaculture nitrogen removal of 13 766 kg was converted to per-acre basis us ing information from CT DA/BA on leased acreage, which yielded an estimated 3.3 kg acre-1 (Table 1).

Table 1. Clam and Oyster Annual Nitrogen Removal by Commercial Size Class in Greenwich Bay, Connecticutg

species limited industry: modeled oyster harvest based on i

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clams (chowder: 100.8 mm, 197 g) N/A

oysters (mean 82.1 mm, 56.5 g) 8.96 x 1 o5 I I

8 Morphometrics listed represent mean shell length and tissue+ shell dry weight for clams and mean shell height and tissue+ shell dry weight for oysters. Clam harvest was provided by Atlantic Clam Farms, oyster harvest model outputs were validated by Stella Mar Oyster Company (SMOC).

Monitored environmental data generated in this study were combined with cultivation practices from industry partner Stella Mar Oyster Company (SMOC) to run the FARM model. Environmental data are provided as Supporting Information (Figure S5). Modeled total production was 69 metric tons fresh weight, which was converted to 896 000 individuals based upon measurements of SMOC oysters (77 g fresh weight per oyster), a count very similar to the reported harvest of 856 000 oysters (Table 1) . Per-acre annual nitrogen removal for oyster aquaculture was 38.1 kg, and total annual nitrogen removed by SMOC was 240 kg .

1 Per-acre nitrogen removal rates for oyster aquaculture (38.1 kg year- ) were an order of 1 magnitude higher than those observed for hard clam aquaculture (3 .3 kg year- ) . Th is difference can be attributed primarily to differences in cultivation styles between the two industries. Hard clam aquaculture in Greenwich Bay, and Long Island Sound in general, is extensive in nature, relying on natural set within a large leased acreage, without external population enhancement through seeding activity, and without protection from predation through the use of clam nets or mesh bags ..(4 5). Oyster aquaculture in Greenwich Bay is more intensive, and leased acres are stocked with spat on shell seed oysters in spring. Additionally, oyster growers reduce mortality losses by seeding with larger oysters from an upweller nursery system (SMOC, personal communication).

FARM model results for oysters' close al ignment with actual harvest numbers reinforces the benefits and gives confidence in the use of this model to project potential harvest from a given farm area . Model outputs for the eight locations around Greenwich Bay were very similar and

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CONTINUE https://pubs.acs.org/doi/10.1021 /acs.est.0c03066 10/28 7/29/2021 Quantification and Valuation of Nitrogen Removal Services Provided by Commercial Shellfish Aquaculture at the Subwatershed Scale IE ...

ACS Publications Most Trusted. Most Cited. Most Read. Q = model studies in the Northeastern United States.(37,46). have not been available. Although the focus of this study was on actual bottom cultivation practices used in Greenwich, consideration of the sensitivity of the results to alternate cultivation approaches (e.g., cages for oysters) was warranted, as gear-based practices are common in other parts of the Northeast. We conducted a sensitivity analysis that suggested areal nitrogen removal rates were similar for the two cultivation practices; details are provided in Supporting In formation, Sl3. The success of the FARM model in estimating harvest under both cultivation practices gives us a high level of confidence that the model accurately represents harvest in this bay under these cultivation practices and can be confidently used to estimate oyster production in other waterbodies.

Nitrogen Removal Relative to Loads

The total annual nitrogen load from Greenwich sources, based upon the Vaudrey et al. _( 38). model output, was 7 62 237 kg (Sup porting Information, Sil ). Annual nitrogen removal by Greenwich clam and oyster aquaculture was 74006 kg, which represents 9% of the total annual Greenwich-specific combined nitrogen load. Modeled nitrogen loads included five categories of nitrogen sources, including atmospheric deposition directly to an embayment, atmospheric deposition to the watershed, fertilizer, sewer, and septic. Nitrogen from two of those categories, atmospheric deposition to the watershed and fertilizer, is delivered to the embayments, and on to Greenwich Bay, via stormwater runoff. Nonpoint sources of nitrogen (i.e., nonsewer) were greater than point sources of nitrogen to Greenwich Bay, contributing 86 7 4 7 kg (53%) of the total load. Annual nitrogen removal by Greenwich clam and oyster aquaculture represented 16% of the combined annual non point sources. Within the non point source categories, fertilizer was the single largest contributor, with 37 327 kg (43%) of the nonpoint source load. Septic was the second largest contributor, with 27 577 kg (32%) of the non point source load. Atmospheric deposition to the watershed contributed 14 228 kg (16%) . Atmospheric deposition to the Greenwich embayments was 7615 kg (9%), although it is worth noting that this does not represent the total atmospheric deposition directly to Greenwich Bay. Vaudrey's study was focused on the embayments, which feed into Greenwich Bay (Figure S2), and did not measure the direct deposition to our entire study area. When compared sequentially to the load from each individual nitrogen source, annual nitrogen removal by Greenwich clam and oyster aquaculture represented 38% of the annual fertilizer sources, 57 % of the septic sources, 98% of the atmospheric deposition to the watershed, or 784% of the atmospheric deposition to the

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most likely to reduce nitrogen derived from septic sources, whereas stormwater best management practices (BMPs) would be needed to address nitrogen derived from fertilizer or deposition to the watershed. The allocative approach required distribution of the current estimated N removal by clams and oysters (30 813 lbs year-1) to each of these various engineered removal solutions, which was accomplished using the percentage allocation of nitrogen sources from Vaudrey et al..(38 ). within Greenwich. For example, as fertilizer and atmospheric deposition to the watershed contribute 32% of the total loadings, it is assumed that 32% of the oyster and clam sequestration services would be replaced with stormwater BMPs.

Table 2. Proposed Linkages among Nitrogen Sources, Matched Engineered Approach, Cost Estimates for Engineered Approaches, and Allocation of Replacement Sequestration Services to these Engineered Approaches Based on Relative Proportion of Greenwich Bay Nitrogen Load

' nitrogen source engineered solution ' I I sewer WWTP capital upgrade I

septic septic system upgrade i I atmospheric deposition to watershed bioretention areas, wet ponds, or constructed wetl1

I fertilizer bioretention areas, wet ponds, or constructed wetlc:'

aProportion nitrogen removal does not sum to 100% as no engineered solution is proposed for an additional nitrogen source to the watershed-direct deposition to the embayment.

Table 3 summarizes the results from the economic analysis. The lowest value ($7 00 871; 111 967€) obtained assumes that wastewater treatment upgrades alone could replace the nitrogen sequestration services provided by clams and oysters; the next lowest value ($206 448; 229157€) uses existing nitrogen credit costs as a proxy for the value of services, and the

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li:IUlt: .,_ C~Ullli:11.t:U •~nruyt:11 ->t:\fUt:~Ui:ILIUII I-\IIIIUi:11 Vi:IIUt:~ uy 1-\ILt:rlli:ILIVt: Vi:IIUi:ILIUII Approaches

I valuation approach estimate (2016 dollars) (euro) i I nitrogen credit valuation $206 448 (229157€) I I WWTP upgrades alone $100 871 (111 967€) I ! I allocated replacement solutions ! I WWTP upgrades . $46 940 (52103€) l septic upgrades $292 949 (325173€) I I BMPs $1975941-5455561 (2193295-6055673€) I I total of allocated solutions $2315 829-5795449 (2 570 570-6432 948€)

The results of this study highlight the substantial contribution of nitrogen sequestration services from oyster and clam aquaculture in Greenwich Bay, Connecticut. Although WWTP upgrades and nitrogen credit valuation approaches indicate an annual value of $100 871 (111 967€) or $206448 (229157€), respectively, the allocated solution approach suggests a substantially higher value of between $2 315 829 and $5 795 449 (2 570 570-6 432 948€; Table 3). These higher values, in our opinion, are likely more representative of the actual benefits as it is unlikely that WWTP upgrades alone (which already assume cost-free connection of properties currently using septic) would be able to address the substantial nonpoint sources of pollution within this watershed. And given that Long Island Sound continues to experience seasonal hypoxia after a 20+ year successful campaign to upgrade wastewater treatment plants, it is highly likely that further nutrient reductions will be mandated for coastal states and municipalities that may require addressing those nonpoint sources ..(47). Furthermore, the credit values are essentially based upon the pricing of wastewater treatment upgrades; the determined credit price is based upon documented costs by WWTPs to perform upgrades.

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1 ($383-653 (425-725€) lb N-· ) as a replacement, engineered approach also drive the results obtained here; the lower the proportion of wet ponds actually used in the watershed as a mitigation strategy, the lower the replacement costs for the clam and oyster services would be. Differences across biological populations considered in these studies (oysters alone versus oysters and clams versus kelp) will also change the estimated replacement value for the services; more productive species or populations (whether driven by species physiological characteristics or combinations of characteristics with ambient environmental conditions) will have a higher replacement cost.

Shellfish Aquaculture and Nitrogen Management

Nitrogen management is highly variable across watersheds because of inherent differences in source contributions to total nitrogen load from different land use profiles. Accordingly, there is no standardized approach to nitrogen management that can be applied un iversally across rural, urban, or suburban watersheds. Watersheds dominated by large point sources, such as sewage in urban areas or large animal feeding operations in rural areas, have well-defined effluent streams that can be targeted for nitrogen reduction through the National Pollution Discharge Elimination System ..(48). This type of watershed is generally the exception, and resource managers will more commonly face a variety of point and nonpoint sources of nitrogen contributin g to the total load. A portfolio approach can be effective in this situation, matching sources of nitrogen with relatively large contributions to the total load with technologies and/or policies to manage these sources (e.g., the Watershed Implementation Plan approach used by the Chesapeake Bay Program.(49).). In practice, the wide range of price differences across technologies, willingness of communities to enact available nitrogen reduction policies (e.g., point-of-sale restrictions on fertilizer purchases), and availability of space to implement source reduction projects affect nitrogen management planning as much as the relative contribution of different nitrogen sources to total loads.

Greenwich is an excellent example of a suburban watershed with a variety of nitrogen sources and challenges to implementing a portfolio approach to nitrogen management. Less than half of the total nitrogen load comes from point sources, of which nearly 7 00% is from local WWTP effluent. $7.7 (7.9€) million was invested in 207 4 in WWTP upgrades ..(50). Some additional nitrogen reductions could be achieved through the implementation of biological nutrient romrnt-:::ll torhnAlrv,ioc h, ,t thoco n-:::linc 111/f"\ 1 ilrl nAt ho onf"\1 ,nh tf"I h-:::ll-:::lnro inn, ,tc frf"lm nf"\nnf"lint

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to connect septic systems to the municipal sewer system and/or upgrade septic systems with nitrogen reduction technology would be a logical approach. But again, the potential of these options to sequester the bulk of the nitrogen reaching Greenwich Bay is limited by the 32% total contribution of septic sources to the overall nonpoint source load (Fig ure S3).

Our results indicate that shellfish aquaculture makes an important annual contribution to nitrogen management in Greenwich, and we argue that these results are more broadly relevant to suburban coastal watersheds throughout the country. Municipalities increasingly face difficult and expensive paths to implement nitrogen reductions necessary to achieve water quality goals. One recent local economic assessment of the capital costs associated with a traditional sewering approach to nitrogen reduction in a small municipality in Massachusetts calculated that the projects necessary to meet nutrient reduction goals would be $250 000 000 (278 000 000€) for a town with a year-round population of 14842. .( 1.Q). Municipalities with diverse and diffuse nitrogen sources could benefit from the inclusion of shellfish aquaculture as one part·of a broader nutrient management plan.

The approach taken here is novel in its consideration of not just total nitrogen loads but the division of these loads into point versus nonpoint categories and the further division of non point loads into five source categories. This allowed the assessment of nitrogen removal services provided by shellfish aquaculture within a more realistic management context at the municipal scale. It is clear that shellfish aquaculture alone is not going to enable a municipality to meet all nitrogen reduction goals. Moreover, no single management strategy will achieve this end, because most municipalities face a diverse range of sources that cannot be simply "turned off' (e.g., Figure S3). The categorization of nitrogen inputs from various sources raises important considerations for planning investments in nutrient removal for a watershed. Point sources represent a relatively small contribution of nitrogen loading to the watershed and also are the least expensive to mitigate from a treatment perspective. Further point source upgrades are not likely to have much of an effect on the nitrogen loading into this system. The expense of alternative terrestrial best management practices for nonpoint sources highlights the need to consider alternative approaches for more cost-effective options. Some nitrogen sources are more technologically difficult to address, such as atmospheric deposition to an embayment, which comprised approximately 50% of the total loads to two of the Greenwich Bay subwatersheds. Shellfish, and other in-water best management practices, offer additional value

0 I . • . J . I ..•• • . . . II . . . • . • . r . 1 • • • •• I • • • I • • I . .. I ' .. I . I" .. I I • . • . I . .• I I .• . I • I . I . 1 • • • 1 ..... 1

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ACS Pu bl icat ions Q - Most Trusted . Most Cited. Most Read. - total seafloor acreage of the town. In some U.S. coastal communities (and even within other parts of Connecticut), shellfish aquaculture leasing has become a controversial topic, with the siting of new or expanding operations getting pushback at the local level; e.g., Connecticut,.(52). Maryland,.(53 ). Mississippi,.( 54). Washington State ..( 55). Greenwich, and in particular its Town Shellfish Commission,.(56 ). serves as an important example of how a robust shellfish aquaculture industry can thrive in a town with many other nearshore user groups and a highly developed suburban waterfront.

Study Considerations

It should be noted that the current study focused on an area with existing harvest and estimated the benefits of that harvest for nitrogen remova l; it did not estimate the costs associated with either establishing a clam and oyster population or subsequently harvesting that population. In this way, these dollar value estimates should be viewed as gross benefits of the oyster and clam nitrogen removal rather than net benefits, which would account for the costs associated with the farming and harvesting process. At the same time, the economic analysis also did not include the value associated with the sale of the harvested product, which would offset these costs, assuming a profitable harvesting firm. From society's perspective, since it is only paying for the harvested product and not for the nitrogen sequestration and removal benefits, these benefits are "free" (a positive externality of the growing and harvesting activity).

Our study is limited in its focus on the harvest of clams and oysters and the sequestration of nitrogen in their tissues and shells; denitrification and deposition benefits are not included, and neither are the benefits from nonharvested clam and oyster populations. We determined that adequate data do not yet exist to assess whether burial in sediments was a major loss process for nitrogen in shellfish aquaculture and natural shellfish beds in Greenwich. This pathway was thus not included in removal estimates but does represent a possible additional avenue of nitrogen reduction. Denitrification losses associated with restored oyster reefs and oyster aquaculture operations have been measured and shown to represent appreciable losses in some places ..(7 8,30,57). A recent literature review by an expert panel in the Chesapeake Bay region resulted in denitrification enhancement associated with restored oyster reefs being recommended to the Chesapeake Bay Program as a nutrient best management practice, with rom(")\1~1 r~nriinr, fr(")m ')f; ti'") 7'). l,,r, ~0n:,-1 \to~r- 1 /t::;Q '\ 1--J/'")\A/O\/or thic ovnort n~nol ro\/io1A1

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CONTINUE https://pubs.acs.org/doi/10.1021 /acs.est.0c03066 16/28 7/29/2021 Quantification and Valuation of Nitrogen Removal Services Provided by Commercial Shellfish Aquaculture at the Subwatershed Scale I E ...

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UUI I efJldL;el I ,e, IL L;U::iL 11 ,eu ,uuu,uyy I ld::i ::;eve, di 111 Ii-JUI Ldl IL 111111 LdLIUI l::i. r11 ::iL, WI Ille I efJldL;el I ,e, IL cost approaches ideally assume implementation of the least-cost approach (or combination of approaches) to replace the lost service, our intent in creating a replacement scenario based on the localized sources of nitrogen does not ensure the lowest cost mix of alternatives. Instead, we base our analysis on data on sources of nitrogen and ways that decision-makers may respond with appropriate abatement technologies. In effect, our model is forcing certain technologies to be used up to the percentage that matches the loading of nitrogen from an associated source. By including the range of costs from the literature, we intend to highlight the broad range of values that are possible given the uncertainty in cost estimates. Second, as with all replacement cost approaches, we assume that the affected municipality would take action to replace the lost nitrogen removal services should the clam and oyster harvest disappear. The actual decision to replace those services will be the result of a complex mix of social, economic, and political decisions. Finally, limited information is available on the septic upgrade and stormwater BMPs; more information in this regard could narrow the wide range of replacement costs associated with the terrestrial BMP approaches for mitigating nonpoint source pollution.

The focus here on nitrogen removal also does not account for other ecosystem services provided by clam and oyster assemblages (e.g., food production, habitat, shoreline protection) and the support of that habitat for the provision of additional ecosystem services and associated benefits (e.g., fish for recreation and food). For example, Grabowski et al..(32). found that nitrogen removal was, on average, only approximately 40% of the total nonharvest ecosystem service value generated by oyster reefs. Shellfish aquaculture also provides a sustainable source of local seafood, which is increasingly valued by consumers ..( 60 ).

Future Directions

Future work related to the incorporation of shellfish aquaculture into nutrient management should continue to investigate the tradeoffs between alternative nutrient management approaches as data continue to be compiled from the various geographies facing this issue and experimenting with solutions. A significant need remains to investigate how crediting systems, both in Long Island Sound and more broadly, can incorporate nitrogen management approaches that use in-water solutions. The Chesapeake Bay Program has recently made progress in advancing this issue ..( lZ).

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CONTINUE https://pubs.acs.org/doi/10.1021 /acs.est.0c03066 17/28 7/29/2021 Quantification and Valuation of Nitrogen Removal Services Provided by Commercial Shellfish Aquaculture at the Subwatershed Scale I E .. .

ACS Publications Most Trusted. Most Cited. Most Read. Q. = year across the Long Island Sound region ..(62). Such approaches, however, require significant funding for survey development and administration and in-depth data on the beneficiaries themselves. Johnston et al.,.(63). for example, reported shellfish water quality benefits for recreationists (fishers, boaters, and swimmers) to the Peconic Estuary System (PES) of over $55 (61 €) million (2016 dollars) year-1 based upon approximately 3 million beach, boating, or fishing trips taken there per year. This dollar estimate is approximately 10 times what we observed in Greenwich coastal waters using the maximum for the allocated replacement costs ($5.8 (6.4€) million). Although it is uncertain if Greenwich waters experience the same level of visitation (3 million beach, boating, or fishing trips) as the PES given the smaller geographic scale of Greenwich waters and more limited access points, estimated visitation to Greenwich Point Park (only one of several parks with beaches in Greenwich) totaled over 400 000 people in 2016 (M . Long, Town of Greenwich, personal communication).

The project process and results obtained demonstrate the benefits of interdisciplinary work across ecology and economics. Municipalities anticipating nutrient and other environmental management decisions benefit from quantitative monetary estimates and realistic performance expectations associated with implementation of best management practices. Moreover, the coupled ecological-economic approach provides a model for future interdisciplinary work that could be applied within any coastal watershed in the United States. The biological model is necessary to form a reasonable expectation of the harvest that could be obtained over a given acreage, and the economic model helps contextualize investments in terms of the typically "unpriced" economic benefits produced.

Supporting Information Jump Tov

The Supporting Information is available free of charge at https://pubs.acs.org/ doi/10.1021 / ac s.est.0c03066.

• Selected previous US studies on values of nutrient bioextraction services (Table S1 ); Map of Greenwich CT, USA, including location of subwatersheds, recreational harvest areas, commercial shellfish aquaculture leases, designated natural shellfish beds, Grass Island WWTP, and water sampling stations for FARM model calibration (Figure S1 ); details of modeled nitrogen loads from Vaudrey et al.;.(38). approach to estimate the CT portion of

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CONTINUE https://pubs.acs.org/doi/10.1021 /acs.est0c03066 18/28 7/29/2021 Quantification and Valuation of Nitrogen Removal Services Provided by Commercial Shellfish Aquaculture at the Subwatershed Scale IE .. .

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Quantification and Valuation of Nitrogen Removal Services 14 37 0 Provided by Commercial Shellfish Aquaculture at the views shares downloa Subwatershed Scale

Supporting Information

Quantification and valuation ofnitrogen remm-al sen-ices provided by commercial shellfuh aquaculture at the subwatershed scale

Anthony Dvarskas, Suzanne B. Bricker, Gary H. Wikfors, John Bohorquez, )..iark S. Dixon, Julie )..1. Rose

I otal number of pages: 19

Kumber of figures: 5

Kumber of tables: 3

1 / 2 < > "" < Share .J Downloac

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CONTINUE https://pubs.acs.org/doi/10.1021 /acs.est.0c03066 19/28 7/29/2021 Quantification and Valuation of Nitrogen Removal Services Provided by Commercial Shellfish Aquaculture at the Subwatershed Scale I E ...

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Quantification and Valuation of Nitrogen Removal Services 14 37 0 Provided by Commercial Shellfish Aquaculture at the views shares downloa Subwatershed Scale

Supporting Information

Quantification and ,·aluation ofnitrogen removal sen -ices provided by commercial shellfish aquaculture at the subwatershed scale

Anthony Dnrskas, Suzanne B. Bricker, Gary R Wikfors, John Bohor .uez,. fark S. Dixon, Julie )..!. Ros.e

Total number of pages: 19

• ·umber offigurecs: 5

!\umber of tables: 3

1 / 2 < > "" «! Share f Downloac

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CONTINUE https://pubs.acs.org/doi/10.1021 /acs.est.0c03066 19/28 7/29/2021 Quantification and Valuation of Nitrogen Removal Services Provided by Commercial Shellfish Aquaculture at the Subwatershed Scale I E ...

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Julie M. Rose - NOAA Fisheries NEFSC Milford Laboratory, 272 Rogers Avenue, Milford Connecticut 06460, United States; G http://orcid.org/ 0000-0001 -9796-997 4; Email: julie.ro se@n oaa.gov Authors

Anthony Dvarskas - School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York 7 7794, United States Suzanne B. Bricker - NOAA NOS NCCOS Cooperative Oxford Laboratory, Oxford Maryland 2 7654, United States, G http:// orcid.org/ 0000-0002-2960-2318 Gary H. Wikfors - NOAA Fisheries NEFSC Milford Laboratory, 27 2 Rogers Avenue, Milford Connecticut 06460, United States John J. Bohorquez - School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York 7 7794, United States Mark S. Dixon - NOAA Fisheries NEFSC Milford Laboratory, 272 Rogers Avenue, Milford Connecticut 06460, United States Notes

The authors declare no competing financial interest.

Acknowledgments Jump Tov

We thank Roger Bowgen, Sue Baker, Joan Seguin, and the Greenwich Shellfish Commission for providing boat access and information on municipal shellfish management. Steve Schafer and Jardar Nygaard (Stella Mar Oysters) provided cultivation practices, FARM model production validation, and oysters for morphometrics. Ed Stilwagen (Atlantic Clam Farms) provided harvest information and clams for morphometrics. Jamie Vaudrey (University of Connecticut) aided in interpretation of her model outputs. Denise Savageau (former Director of the Greenwich Conservation Commission) provided information on municipal nitrogen management and knowledge of local water dynamics. Funding was provided by the NOAA Office of Aquaculture.

References Jump Tov

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CONTINUE https://pubs.acs.org/doi/10.1021 /acs.est.0c03066 20/28 DAILY SCIENCE

Researchers calculate the value of bivalves' appetite for pollution. It's huge. If coastal cities planted clam beds along the urban edge, they could save millions in nitrogen clean-up costs

By Emma Bryce March 5, 2021

Oysters and clams are some of nature's most efficient feeders: these shellfish slurp up gallons of water, sieving out food and nutrients as they go, and repurposing some of those raw materials to make their shells.

Now researchers have calculated that if coastal cities and towns planted beds of these industrious bivalves along the urban edge, they could save councils several million dollars in clean-up costs associated with nitrogen pollution - all thanks to the water­ purifying power of shellfish gills.

Filter-feeding shellfish have long been celebrated for their cleansing abilities, especially when it comes to nitrogen pollution, which wends its way down to the coast from sources like farms when nitrogen fertilizer is overapplied. This can cause eutrophication and dead zones in oceans and lakes. But bivalves are hungry for these nutrients and can successfully cleanse them from inflowing water - so they represent an obvious nature-based solution to this threat.

However, the economic value of their pollution-fighting appetite hasn't been widely quantified at local scales, which is what the researchers on the new study wanted to do. To do so, they applied the reverse logic of what it would cost us to clean up nitrogen pollution, if oysters and clams weren't there to do the dirty work.

They focused their study on the American coastal town of Greenwich in Connecticut, where oyster and clam aquaculture is part of the local economy. Using their method, called 'transferable replacement cost', they estimated how much it would cost to build and maintain the infrastructure that would be needed to replace the water-cleansing contribution of bivalves.

To tally that up, they first had to estimated how much of a dent shellfish aquaculture currently makes on different sources of nitrogen pollution from Greenwich. This revealed that the beds of diligent bivalves, filtering away, currently remove almost 10% of Greenwich's overall nitrogen load - which amounts to 14,000 kilograms each year. Broken down by source, that figure went up notably. Clams and bivalves, it turns out, remove 38% of the nitrogen that originates from local fertilizer use on land, and a striking 51 % of nitrogen from septic sources - which are those originating from households and wastewater flow.

The multiple sources of nitrogen on land means that tackling it with infrastructure can be a challenge, because it requires a variety of different technological approaches such as improved stormwater management, and specialised septic tanks, to intercept the pollutant on its journey to the coast. And this increased infrastructure would be costly too, the researchers proved.

They showed that if the contributions currently made by oysters and clams had to be replaced by infrastructural upgrades to tackle nitrogen pollution, it would cost Greenwich an additional $2.3 to $5.8 million a year. But by filtering away beneath the surface, shellfish quietly sink this invisible cost.

Beyond cost-savings, the researchers mention the multiple other benefits that shellfish aquaculture can also bring, and which they didn't explore in the study - such as cleansing pollutants other than nitrogen out of the water, creating habitat for aquatic life, providing coastal buffering against weather extremes, and of course, food if those shellfish are harvested for human consumption .

It's clear from the data, however, that shellfish - however efficient - aren't a complete solution to nitrogen pollution. Human-made infrastructure and technologies are needed too, and ideally some of those would be devoted to capturing more nitrogen at source, before it gets into rivers, lakes, and the sea.

Yet the study does show just how surprisingly large a role these natural cleaners can play in dealing with some of our worst environmental challenges. And although Greenwich is just one case study, the researchers hope that by demonstrating the clear cost savings, it might encourage other coastal towns and cities to embrace shellfish aquaculture too. "Our hope is that the approach we developed here can help inform local discussions about aquaculture around the country," they say. In Brief

The contribution of marine and coastal ecosystems in carbon sequestration, or "blue carbon," has only recently begun to gain traction in market-based ecosystem management discussions.

At present, existing methods of measuring and monitoring carbon offsets are geared towards terrestrial ecosystems, and do not account for the carbon stored in coastal, marine or wetland soils and biomass.

There are a number of mechanisms in place to facilitate investment in terrestrial carbon through regulatory markets which could be adapted to include blue carbon.

Mangroves on Florida's Manatee River / Rick Schwai1z / CC BY-NC 2.0

Oceans and coastal plant species such as mangroves and seagrasses cover only a small fraction of the earth, but are responsible for sequestering over half of all the carbon captured by living organisms. However, despite being some of the most efficient known carbon sinks, they are also among the ecosystems most threatened by climate change. Threats such as rising sea levels and temperatures, offshore drilling, erosion, and pollution have resulted in the rapid deterioration of coastal and marine areas.

The concept of forest carbon, or the sequestration and storing of carbon by forests, is well known and utilized by voluntary carbon markets and payments through the global Reducing Emissions from Deforestation and Forest Degradation (REDD+) program. However, the critical contribution of marine and coastal ecosystems in carbon sequestration, or "blue carbon," has only recently begun to gain traction in market-based ecosystem management discussions. These ecosystems are often biodiversity hotspots, and provide essential services such as food security, water quality, shoreline protection, and the provision of livelihoods to coastal communities. They are therefore ideal ecosystems for conservation efforts worldwide.

However, mobilizing capital investments for conservation remains one of the primary obstacles in managing coastal and marine ecosystems. Therefore, blue carbon could be crucial in facilitating both private and public capital investment in these dynamic ecosystems. The blue carbon market is, at present, still nascent. Governments and international institutions are revising methods of monitoring carbon to include blue carbon and develop structures to encourage private investment in blue carbon offsets. This article explores these efforts to facilitate the generation and trade of blue carbon credits.

How Is Blue Carbon Different?

Blue carbon is sequestered and stored in coastal and marine ecosystems that include mangroves, tidal marshes and seagrass meadows. In terrestrial ecosystems, carbon credits reflect the storage and sequestration from forests, grasslands, soil and other sources of biomass. However, the carbon stored in coastal ecosystems differs in that biomass accumulates not only from sources like fallen leaves and twigs, but also from organic matter being washed up by the tide. Additionally, this organic matter is covered in saltwater, which inhibits breakdown of the material.

Ecosystems such as mangroves, tidal marshes and seagrass meadows cover only 2-6% ofthe surface area covered by terrestrial forests, but sequester carbon dioxide at much higher rates.

A 2017 study found that this improved preservation of organic material not only allows coasts to keep up with a certain degree of sea level rise through organic matter build-up, but also means that layers of coastal organic matter can be up to six meters deep or more. Terrestrial soil organic matters typically reaches up to 30 centimeter in depth. Because of these deeper organic horizons, per capita carbon stocks in coastal ecosystems are significantly higher.

According to the Blue Carbon Initiative, ecosystems such as mangroves, tidal marshes and seagrass meadows cover only 2-6% of the surface area covered by terrestrial forests, but sequester carbon dioxide (CO2) at much higher rates. In fact, it is estimated that mangroves can store up to 1,030 megagrams (Mg) of CO2 equivalent per hectare, and tidal marshes and seagrass meadows can store 920 and 520 Mg of CO2 equivalent per hectare respectively. The degradation or conversion of these ecosystems has led to a subsequent release of an average of 0.15- 1.02 billion tons of CO2 annually.

Jennifer Howard, coordinator of the Blue Carbon Policy Working Group run by Conservation International and the International Union for the Conservation of Nature, explained in an interview that when it comes to blue carbon crediting, managers have to account for a much deeper organic horizon. In terrestrial ecosystems, cutting trees means losing the previously sequestered carbon stock that was stored in the trees. Emission of stored carbon in the trees only occurs if they are cleared and then burned. In coastal ecosystems, ecosystem degradation through cutting down mangroves or draining wetlands leads not only to the loss of previously sequestered carbon, but also active re-emission of the carbon that was trapped in the soil by the saltwater regardless of how the cleared biomass is utilized or disposed.

"Terrestrially, you lose carbon with degradation," Howard said. "But on the coast, you lose carbon and then become an active emitter."

Is There a Market?

By virtue of being measurable and standardized, blue carbon has the potential to be adopted into regulatory carbon markets across the world. However, blue carbon is still a relatively new concept. At present, existing methods of measuring and monitoring carbon offsets are geared towards terrestrial ecosystems, and do not account for the carbon stored in coastal, marine or wetland soils and biomass. Current efforts are therefore working towards including wetlands in regulatory and monitoring mechanisms so as to create a framework that allows for better methods to account for and trade blue carbon credits. While some companies, such as ~ and coastal restoration group Blue Ventures, are investing in voluntary markets for blue carbon, the market for private investment is still new. Carbon accounting frameworks need to be modified to facilitate the widespread uptake of blue carbon into the voluntary offset market. Reports suggest that a majority of voluntary corporate carbon offset buyers look for credits that fit with their broader mission as a company, as well as lead to co-benefits such as greater biodiversity and improved community livelihoods. This suggests that carbon credit buyers from industries such as tourism, oil and gas, and shipping could benefit from blue carbon projects in coastal and marine ecosystems.

Expanding Carbon Crediting Frameworks

There are a number of mechanisms in place to facilitate investment in terrestrial carbon through regulatory markets which could be adapted to include blue carbon.

Traditionally, a majority of the nationally detennined contributions (NDCs) at the core of the Paris Agreement on climate change have been through the REDD+ program, which monitors forest degradation and carbon restoration efforts. The revision ofNDCs every few years gives regulatory markets the opportunity to improve their methods of monitoring and accounting for carbon emissions, thereby facilitating the trade of these credits. While these mechanisms have historically been focused on forest standards, a report published by the Nicholas Institute of Environmental Policy Solutions lays out the opportunities for integrating wetlands and mangroves into programs like REDD+ as an extension of forest carbon monitoring, an idea that organizations such as the Blue Carbon Initiative and Conservation International are now working towards implementing.

Another avenue for the integration of blue carbon into the NDCs is through the greenhouse gas inventories that monitor the quantity and sources of emissions from each country. An effort led by Stephen Crooks of the Blue Carbon Initiative is now working with the U.S. Environmental Protection Agency (EPA) to include wetlands into the inventories for the United States. The "once in never out" nature of greenhouse gas inventories means that the inclusion of wetlands will ensure that these emissions will at least be monitored consistently over time, which can provide crucial data for the inclusion of blue carbon into regulatory trading markets.

Aiming to assist with this implementation around the world is the International Partnership for Blue Carbon, a group of countries that have partnered with NGOs and academic institutions to provide technical support to countries looking to integrate blue-carbon ecosystems into national monitoring and trading policies.

There are a number ofmechanisms in place to facilitate investment in terrestrial carbon through regulatory markets which could be adapted to include blue carbon.

Blue Ventures' efforts, for example, could benefit from the integration of blue carbon accounting and trading methods into national policies in Madagascar. Blue Ventures is exploring the use of blue carbon as a long-term :financial mechanism for community-based mangrove management in Madagascar. Since 2011, the project has conducted stakeholder consultations and community­ developed coastal ecosystem restoration projects, and estimated carbon stocks that could be credited to finance restoration work. Efforts such as these would benefit from nationally recognized carbon accounting methods that include blue carbon in their methodology and account for the carbon that is stored both above and below ground in coastal ecosystems.

According to Howard, blue carbon's novel nature makes it challenging for a smooth uptake into the market, as many countries and national agencies do not have sufficient experience with carbon project development in coastal and marine ecosystems and lack regional carbon storage and sequestration data.

While blue carbon is beginning to gain recognition by federal agencies such as the United States Fish and Wildlife Service and the EPA, many other agencies around the world still lack the capacity and expertise required to incorporate blue carbon into federal and state policies and regulations. This is where technical support from organizations such as the Blue Carbon Initiative can help address knowledge gaps and assist with the adoption of blue carbon markets.

Addressing Investment Risks

One concern about investing in blue carbon is that coastal ecosystems are particularlv vulnerable to climate change and may be degrading at higher rates than terrestrial ecosystems due to rising sea levels, varying temperatures and coastal land reclamation. However, blue carbon crediting methods are within the Verra verified carbon standards, and therefore include a 15% risk­ reduction buffer in the amount of credits calculated for a given ecosystem. This 15% typically accounts for credits lost to storms, illegal activities and sea level rise. Of course, this buffer may change as models for climate predictions change, but it ensures that blue carbon projects account for the risks associated with climate change in determining their carbon credit value. So while blue carbon markets are yet to mature, existing frameworks for blue carbon accounting can allow for trading and addressing risk.

Another risk when it comes to investing in blue carbon is that in some cases, the cost of conservation and restoration of coastal ecosystems can be higher than the potential income that can be generated from the credits they provide. Blue carbon ecosystems are mostly found close to coastlines and therefore it is hard to reach a scale cost-effective for conservation or restoration projects.

Additionally, if the income from alternative land uses, such as tourism, is higher than the projected income from selling blue carbon credits, the credits by themselves will not be sufficient to justify conservation.

In these cases, blended finance steps in as one potential solution for addressing the risks of participating in blue carbon credit markets. In a project run by Apple and Conservation International in Colombia, for example, credits generated from blue carbon ecosystems are added to a centralized fund, according to Howard. The fund includes contributions from government­ allocated funds for development or conservation in the area, as well as other financial streams.

"We're still figuring out what those [additional streams] are," Howard said. "They could be from ecotourism and/or fisheries, depending on what industry they want to build around there. So, for instance, that could be a dollar added to every night at the hotel and that dollar then is allocated to the fund."

The Way Forward

In May 2019, the Blended Finance Task Force's investor roundtable agreed that blue carbon could be a crucial pathway for increasing private investment in coastal and projects, as it provides a standardized and measurable tool. To make these investments viable, blue carbon revenue streams could be combined with projects such as sustainable fisheries, ecotourism and coastal infrastructure. While mitigating risk is still a big challenge for coastal projects, collaborations such as the Blue Carbon Initiative, Blue Carbon Policy Working Group, and the International Partnership for Blue Carbon, among others, are working to make this market scalable and expand blue carbon investments beyond their current niche. 0 • • Clams Can Boost Seagrass Restoration: Study

05/0712021 by Lena Beck

Seagrass seeds sown with other species such as planted clams may help improve chances for restoration efforts, according to a recent Duke University Marine Lab study. Photo: R. Gittman/ECU Coastal seagrass beds are critical parts of ecosystem function. Seagrasses are a foundation species, providing essential habitat for fish and birds, protecting against erosion and improving water quality.

A study published recently in Frontiers in Marine Science called "Inclusion of Intra- and lnterspecific Facilitation Expands the Theoretical Framework for Seagrass Restoration" took a closer look at restoration methods.

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The lead author, Dr. Y. Stacy Zhang, currently at the University of North Carolina Chapel Hill Institute of Marine Sciences in Morehead City, wanted to investigate how restoration efforts usually take place, and how they might be improved by different planting strategies. She conducted the research while a doctoral student at Duke University Marine Lab in Beaufort.

The study documented two direct experiments as well as a global survey of others who have worked in seagrass restoration.

For the survey, Zhang and her team reached out to 750 individuals and organizations involved in restoration in 23 countries. Of those, Zhang received 152 responses. Participants filled out a 20-question form about their restoration strategies and practices. Demographically, respondents included academic, nonprofit and governmental agencies.

The results indicated that 86% of respondents planted using dispersed arrangements, as opposed to planting large patches of seagrass. Additionally, efforts rarely attempted to restore seagrass alongside other species from the natural habitat.

Zhang hypothesizes that there could be different reasons why more people don't attempt multispecies restoration. One reason could be funding constraints. This is a factor that Zhang keeps at the forefront of her research.

"For restoration to be successful, it has to be cost-effective, and produce yields," Zhang said. "I think that's sort of the goal that we are trying to reach with a lot of our seagrass restoration experiments."

Postdoctoral researcher Stacy Zhang collects data on the shoreline of the Institute of Marine Sciences March 30 in Morehead City. Photo: Johnny Andrews/UNC The survey indicated that the current theoretical framework used for coastal restoration is derived from forestry science. These strategies aim to decrease environmental stressors by trying to minimize competitiveness amongst species. But this framework has still resulted in a high failure rate for seagrass restoration projects. According to Zhang, this means it is necessary to figure out some new ways to improve the chances of successful restoration.

To this end, Zhang experimented with different intra- and interspecific planting arrangements. An "interspecific" approach means planting different species alongside each other. In the case of this experiment, Zhang implemented the use of clams in some of the seagrass plots. The "intraspecific" approach meant planting members of the same species alongside each other, instead of in a dispersed arrangement.

They tried both of these approaches in a couple of different treatments, both with plots of seagrass seeds and with adult outplant shoots.

What they found was that interspecific planting significantly aided in the growth of the seagrass seeds, both in shoot size and patch expansion. On average, seed patches with clams expanded by 500%, while those without barely changed.

Transplanted shoots weren't significantly affected by clams. Zhang hypothesizes that seagrass seeds have different nitrogen needs than more mature plants. The clams were able to facilitate a boost in nitrogen for the seeds. By contrast, intraspecific planting - large, intact plots of seagrass as opposed to dispersed planting arrangements - helped the adult outplant shoots grow faster and expand in patch size. Altogether, the study shows that positive species interactions maximize restoration productivity. They could even increase resilience across the whole ecosystem.

Zhang said she didn't expect the results to be as dramatic as they were.

''What we really ended up seeing instead was almost that it was changing the trajectory of these experimental restoration plots from failure to success," Zhang said.

According to Dr. Shelby Ziegler, postdoctoral research associate at Moss Landing Marine Labs in California, this study is on the forefront of a new wave of seagrass research.

"It's one of the first studies to look at both inter- and intraspecific facilitation and how that affects restoration," Ziegler said. "So instead of just restoring one species, you can look at restoring two different types of species or different organisms together, and see how that enhances the overall restoration effects. This could be really important for the future of restoration and how we think about restoration practices."

North Carolina has one of the highest numbers of seagrass meadows on the East Coast. This fact, plus the plethora of ecosystem services that seagrasses provide, make seagrass an excellent lens for viewing coastal restoration. Ziegler said that seagrass is critical for both ecosystem needs and human activity, though people rarely realize it.

"People don't realize how important those habitats are to enhancing their everyday livelihood," Ziegler said.

Seagrass beds provide habitat for waterfowl, which attract hunters to the coast. They also provide shelter to fish like red drum, the official state saltwater fish. And, said Ziegler, when people go out to fish, the effects of seagrass beds on water quality are the reason they can see through the water.

Zhang's study emphasizes the idea that a multispecies approach to restoration could increase their success rates. This idea is reflected in broader restoration efforts, and has been a growing trend for the last few decades.

According to Zhang, restoration work is currently undergoing a transition from focusing on a single species to a whole ecosystem. The effectiveness of this approach was supported by the results of the study. Positive interactions amongst species can bolster seagrass shoot growth and patch expansion.

Still, the approach is fairly novel when it comes to seagrass, but considering the significance of seagrass in the coastal ecosystem, the implications could be huge, and not just in North Carolina but around the globe. According to Zhang, taking this type of view and expanding the body of knowledge surrounding inter- and intraspecific planting could help coastal restoration efforts become more effective long term.

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Lena Beck is a graduate student at the University of Montana, pursuing a master's in environmental science and natural resource journalism. Originally from Oregon, she lived in Washington State for seven years where she wrote for the Seattle University Spectator and Seattle Magazine. She now lives in Missoula, Montana, where she researches and writes about sustainable food and agriculture issues. Get the news of the North Carolina coast delivered daily. Subscribe to Coastal Review I I I

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• Editorial Policy & Terms of Use © 2021 North Carolina Coastal Federation. All rights reserved. Why the Market for 'Blue Carbon' Credits May Be Poised to Take Off

Seagrasses, mangrove forests, and coastal wetlands store vast amounts of carbon, and their preservation and restoration hold great potential to bank CO2 and keep it out of the atmosphere. But can the blue carbon market avoid the pitfalls that have plagued land-based programs?

BY NICOLA JONES APRIL 13, 2021

• • •

Off the shores of Virginia, vast meadows of seagrass sway in the shallow waters. Over the past two decades, conservation scientists have spread more than 70 million seeds in the bays there, restoring 3,600 hectares (9,000 acres) of an ecosystem devastated by disease in the 1930s. The work has brought back eelgrass (Zostera marina) - a keystone species that supports crustaceans, fish, and scallops, and is now absorbing the equivalent of nearly half a metric ton of CO2 per hectare per year.

Now, the Virginia Nature Conservancy is aiming to turn those tons into carbon credits that it can sell for cash.

The collaborative project - with planting done by the Virginia Institute of Marine Science (VIMS) and the Nature Conservancy, and long-term carbon data provided by the University of Virginia - is the first seagrass project in the world to apply for carbon credit certification with the Washington-based nonprofit Verra, the world's largest overseer of carbon credit projects. "It's proof of concept - that's the important part here," says Christopher Patrick, director of the VIMS seagrass restoration and monitoring program. "We' re not going to change global climate with this one project. But we can show it's a viable approach."

If successful, it will join a handful of other blue carbon credit projects around the world, the vast majority of which are mangrove restoration efforts - a trickle of blue that many anticipate will soon become a flood. So far, Verra has issued a grand total of just under 970,000 credits (representing 970,000 metric tons of CO2 equivalents) to blue carbon projects. But mangrove projects are now ramping up dramatically in scope, with one alone aiming to soak up millions of tons of CO2 equivalents a year. And scientists are working hard to account for the carbon in other ecosystem types - seagrasses, salt marshes, seaweeds, and seafloor sediments - so they, too, can enter the market.

The rules to allow these other ecosystems to cla im credits are new. In 2015, Verra published its first methodology to give credits to tidal wetland and seagrass restoration, but only last September did Verra expand its rules to cover wetland conservation. That was "a very big deal," says Jennifer Howard, marine climate change director for Conservation International. " I know of at least 20 different projects right now that are all trying to get developed and on the market in the next two years. I think we' re going to see a big explosion."

Corporations, including Apple, have been very vocal about their blue carbon purchases and projects.

"The market is small but growing exponentially," agrees marine ecologist Oscar Serrano at Edith Cowan University in Perth, who has helped to catalog the capacity for Australia's blue carbon reserves in mitigating climate change.

Amy Schmid, ecologist and manager of natural climate solutions development for Verra, says, "there's a lot of demand for blue carbon credits." Companies in shipping and tourism are keen to put money back into conserving the landscapes they have an impact on, she says, while offsetting their own emissions. And many of these projects offer win-win-win stories for people, biodiversity, and carbon, which boosts the price that organizations can get for their credits on the open market. Corporations, including Geneva-based MSC Cruises and Apple, have been very vocal about their blue carbon purchases and projects.

Carbon credits have been around since the late 1990s; it has long been possible to offset, say, the emissions from your wedding in California by buying carbon credits from planting trees in the Amazon. Along with Verra, other nonprofits that have sprung up to write the rule book and keep registries of carbon credit projects include the Geneva-based Gold Standard and Edinburgh-based Plan Vivo. The carbon market in general has a checkered past, with problems surrounding double-counting of carbon cuts, the failure to channel the money to local communities, or the creation of perverse collateral damage along the way, like razing one crop to plant another for credits. These are the issues that the methodologies published by entities like Verra attempt to avoid. The Taskforce on Scaling Voluntary Carbor Markets, set up last September, is working hard to ensure future carbon credits - including blue ones - are sound. And experts agree that both companies and nations need to work hard to decarbonize first before turning to offsets for their remaining emissions.

That's especially important since the market for all forms of carbon credits is growing fast. More than 1,600 projects registered with Verra account for 620 million tons of CO2-equivalent, enough to counteract the emissions from about 150 coal-fired power plants, with trading staying strong despite the pandemic. When parties to the UN Convention on Climate Change meet this November in Glasgow, they will hash out the notoriously thorny Article 6, which governs how countries can use carbon markets to meet their government-mandated targets. That's expected to help guide and boost the voluntary carbon credit market.

The Taskforce's January 2021 report concluded that demand for carbon credits will likely increase by a factor of 15 by 2030, making the market worth $50 billion. Blue carbon project planners are hoping to get their slice of that pie. UNESCO, for example, noted in its blue carbon report last month that its SO marine Heritage Sites, which together account for 15 percent of the planet's blue carbon assets, could finance at least part of their conservation work by claiming and selling carbon credits.

So far, though, marine-based efforts have lagged behind land-based forestation projects that offer easier, cheaper, and larger-scale operation. But the ocean's capacity for keeping global warming in check - while also providing food, boosting biodiversity, and protecting local coasts from storms and tides - is huge. "The ocean has long been seen as a victim of climate change, but it's also a big part of the solution," says explorer-in-residence Enric Sala, who studies blue carbon.

Three types of marine ecosystems have so far garnered the most attention - salt marshes, mangroves, and seagrasses. These make up only a thin blue line on global maps, but each sequesters more carbon per hectare per year than do tropical forests. Disturbing a hectare of mangroves, for example, has been estimated to produce as much emissions as plowing down 3 to 5 hectares of tropical forest. Preventing or reversing that destruction is not only good for the planet but provides a lot of "bang for bucks" in terms of investment, says Howard.

About 20 percent of the world's mangrove forests are ripe for blue carbon projects.

According to a 2019 High Level Panel for a Sustainable Ocean Economy report, protecting and restoring these ecosystems globally, alongside seaweed farming, could reduce emissions by as much as 1.4 billion tons of CO2-equivalent emissions annually by 2050. That's just a few percentage points of the total cuts the planet needs to make in order to hit net zero by 2050. But for some countries, it's huge. " For Indonesia, up to 20 percent of their national emissions come from mangroves," notes Howard, as mangroves are converted to aquaculture and their carbon sinks are lost.

Mangrove restoration is the best studied and most advanced kind of blue carbon credit project to date. A recent assessment concluded that about 20 percent of the world's mangrove forests are ripe for such projects, and about half of that could be affordably protected with inexpensive carbon credit prices of $5 per ton or more.

So far, only a scattering of mangrove projects are underway or in development, including in Kenya, Senegal, Sumatra, India's Sunderbans, and Colombia, as well as a couple of marine protected areas in Madagascar and Kenya . Most aim to reduce emissions by thousands to hundreds of thousands of tons of CO2 equivalents per year. But such projects are just now hitting their stride.

"All of a sudden in the last year really we've gone from these very small, very few projects to a real scaling up," says coastal geomorphologist Steve Crooks with the San Francisco-based consultancy Silvestrum Climate Associates. He points to one massive project he has been helping with to reforest more than 200,000 acres of mangroves in the Indus De lta in Pakistan. It aims to absorb 2 million tons of CO2-equivalent per year, selling 1 million credits in 2021, says Crooks - a scale that will "blow other blue carbon projects out of the water."

Seagrasses may have more carbon mitigation potential than mangroves simply because there are so many of them, and they're rapidly disappearing at about 2 to 7 percent per year. (According to the High Level Panel, seagrasses alone might account for half of the 1.4 billion tons of blue carbon greenhouse gas-mitigation potential.) The Virginia project has pioneered efforts to quantify the carbon soaked up by seagrasses, doing the hard work of monitoring both the CO2 absorbed by the plants as well as the emissions of other greenhouse gases like methane. In 2020, researchers published a paper showing that the carbon credits generated by one part of the meadow, 700 hectares in South Bay, should offset about 10 percent of that project's restoration costs of $800,000.

The Virginia project is special, however, notes project leader Patrick, because that ecosystem hasn't been degraded by climate change or pollution, making it easier to successfully restore the grasses. "A lot of seagrass restorations fail because you're planting grass or putting in seed where the environmental drivers that caused the collapse haven't been fixed in the first place," he says. Although the VIMS project will hopefully pave the way for other sea grass programs to earn credits, many of those other projects will likely involve more work and be more expensive. For those reasons, says Howard, conservation might be an easier target for seagrass credit projects than restoration.

There is also ample scope for restoring and protecting sa lt marshes, especially in Australia, home to about a third of the planet's tidal marshes. But the years of required data on carbon storage and release aren't there yet, says Crooks. Intensive research into wetlands by the Pacific North West Coastal Blue Carbon Working Group has shown that although these landscapes hold a lot of carbon, some naturally release so much methane that carbon credits may not be a viable long-term financial option. Monitoring a wetland involves a lot of " walking through a lot of mud and muck," says Schmid, and emissions of gases like methane can be highly variable from spot to spot and over time, making monitoring onerous.

A big shakeup to the blue carbon-credit movement could come if the doors are opened to one particular new carbon source : seaweed. Seaweeds - like the massive kelp forests in Australia - are a major stock of blue carbon under threat in many parts of the world. The High Level Panel highlighted seaweed farming as a viable emissions mitigator and a way of producing sustainable food. But there are still doubts about exactly where all the carbon from seaweed farms goes, says Howard.

If the science behind the carbon accounting holds up, seaweed could be added to carbon credit methodologies.

If the science behind the carbon accounting holds up, seaweed could be added to carbon credit methodologies.

HHow much falls to the seafloor, how much is eaten by fish, and how much they poop, how much carbon is being moved - we just don't know," she says. Verra is actively watching this realm with interest, says Schmid; if the science behind the carbon accounting holds up, seaweed could be added to the non profit's carbon credit methodologies within a couple of years. Crooks says he is helping to develop a credit-for­ seaweed-farming project now in British Columbia.

Organic-rich sediments on the seafloor are also contenders for credits. Sala and colleagues estimate that fishing boats dragging nets along the seafloor are kicking up 1.47 billion tons of CO2 - about as much as released by the aviation industry today, and more than the 1.4 billion-ton mitigation potential of mangroves, salt marshes, seagrasses, and seaweed farming combined. The science on where this carbon goes is highly uncertain, says Howard. It's not clear, for example, if the carbon kicked up from the seafloor makes it all the way up to the air, or stays dissolved in the water, making it more acidic.

ALSO ON YALE E360

Is the 'legacy' carbon credit market a climate plus or just hype? Read more.

Like land-based carbon credit projects, blue carbon projects face issues, says Serrano. Many of these projects are expensive, he notes, which makes it hard for carbon credits to make a dent in project costs. And ensuring permanence of the carbon stocks can be hard in the face of storms or marine heatwaves.

Carbon credits are just one way to finance these nature-based solutions for carbon sequestration; there are also philanthropic donations and government-funded grants or subsidies. However, says Howard, "the [carbon credit] market is good, because the private sector has all the money. We need long-term, sustainable finance to keep our projects going."

• • •

Nicola Jones is a freelance journalist based in Pemberton How Much is a Clam Worth to a Coastal Community?

April 05, 2021

A new study looks at the value of the water quality benefits provided by shellfish aquaculture.

Feature Story New England/Mid-Atlantic

A new study estimates that oyster and clam aquaculture provides $2.8-5.8 million in services that remove excess nitrogen from the coastal waters of Greenwich, Connecticut. The study was conducted by shellfish biologists, economists, and modelers from NOAA Fisheries, NOAA National Centers for Coastal Ocean Science, and Stony Brook University. It was recently published in Environmental Science & Technology.

Researchers used a "transferable replacement cost methodology" to estimate the ecological and economic value of nitrogen reduction that results from oyster and clam aquaculture in this coastal community. The replacement cost method puts a dollar va lue on ecosystem services by estimating what it would cost for humans to provide those services. In this case, that was the cost of improving wastewater treatment, upgrading septic systems, and better managing stormwater.

Summer kayakers enjoying the water quality provided in part by shellfish in Greenwich, Connecticut. Credit: NOAA Fisheries "When we started discussing this work, I had a long list of ecosystem services in mind-not just nitrogen remediation, but water clarity for swimming and seagrass colonization, habitat for recreational fish-all leading to improved quality of life in a coastal town," said Gary Wikfors. Wikfors is chief of the Aquaculture Sustainability Branch at NOAA's Northeast Fisheries Science Center's Milford Laboratory in Milford, Connecticut, and a co-author of the study. "As a biologist, I learned from this study how complex a comprehensive economic valuation is! The economic benefit estimates in this report are just a small fraction of the total-the tip of the iceberg-but still appreciable at the municipal level," he said. Oysters and Clams as Nutrient Management Nitrogen is a nutrient that enters coastal waters from many different sources, including agriculture, fertilizer, septic systems, and treated wastewater. In excess it fuels algal growth, which can affect water quality and human health. As a result, a growing number of communities are required to follow regulations to release less nitrogen. Shellfish can be a valuable part of a community's nutrient management plan when preventing nitrogen release is not enough.

Field experiments to measure feeding and nutrient uptake by shellfish in the Greenwich watershed in 2015. Credit: NOAA Fisheries Growing bivalve shellfish, including oysters and clams, provides direct economic benefits to a community by supporting jobs and making fresh local seafood available to consumers. It also provides ecosystem services-benefits that nature provides to people-including habitat for native species and improved water quality.

An adult oyster can filter up to SO gallons of water per day. While clams filter a little more slowly, large adult clams can filter up to about 40 gallons daily. Both clams and oysters take up nutrients when they filter feed on algae. Some of those nutrients become part of their shells and tissue, and are taken out of the watershed when shellfish are harvested. Nutrient removal is beneficial to the watershed. It reduces the risk of excessive algal growth that can starve fish and other organisms of oxygen, resulting in fish kills and other negative outcomes. Estimating the dollar value of those water quality benefits required a multidisciplinary approach; one that got biologists thinking about economics and economists thinking in ecological terms. Economic Value of Water Quality Improvements More than half of the local nitrogen input in Greenwich is non point source, such as runoff from lawn fertilizer. The rest is point source input, such as treated wastewater. Nonpoint source input is often more challenging and expensive to reduce than point source input, requiring a multifaceted strategy. Eastern oysters from Stella Mar Oysters studied in this project. Credit Steve Schafer, Stella Mar Oysters The researchers found that replacing the nutrient removal benefits of shellfish aquaculture in Greenwich with traditional, engineered nutrient reduction strategies would cost between $2.8-5.8 million per year. The estimate assumes nitrogen removal by shellfish would be replaced with a combination of wastewater treatment improvements, septic system upgrades, and stormwater best management practices in proportion to the local nitrogen sources.

Clam and oyster aquaculture removes approximately 9 percent of the locally­ deposited nitrogen from Greenwich's coastal waters annually. That's about 31,000 pounds of nitrogen per year. The percentage removed is even greater when considering only nitrogen from nonpoint sources (16 percent), fertilizer (28 percent), or septic sources (51 percent). Per-acre nitrogen removal for oyster aquaculture was higher because oysters are grown more densely, but clams contributed more to nutrient reduction because more clams are harvested overall. Shellfish are unique because they take up nitrogen across all sources, whether from lawn fertilizer, deposition from the atmosphere, or treated wastewater. Residents of the community benefit from shellfish aquaculture whether or not they eat oysters, as they enjoy improved water quality. "Shellfish provide water quality benefits that coastal residents and visitors may not fully appreciate on a day-to-day basis. Our findings show that shellfish populations grown for harvest may complement land-based nutrient management approaches as part of the portfolio of solutions for excess nitrogen in our coastal waters," said Anthony Dvarskas, who co-led the study while an assistant professor at Stony Brook University. Developing a Transferable Approach

Workers at Atlantic Clam Farms sorting clams in Greenwich, Connecticut. Credit: NOAA Fisheries The team developed two ways to estimate the value of shellfish nitrogen remediation. One is appropriate for a well-established shellfish aquaculture industry and estimates nitrogen removal from the annual harvest. The second allows ecosystem managers to project the nitrogen removal of a new or growing industry. "We developed a method to estimate potential harvest in communities with limited or no current aquaculture, but with opportunities to expand or start aquaculture, to highlight possibilities," said project co-lead Suzanne Bricker from NOM's National Centers for Coastal Ocean Science. Bricker used computer models to calculate the amount of nitrogen removed. The approach detailed in this study can be applied to other communities wishing to reduce nutrients to improve water quality. Even without a local shellfish aquaculture industry, decision makers will find the study useful in understanding the environmental benefits of shellfish to their coastal waters. "There is growing interest in shellfish aquaculture in coastal communities around the United States, and our hope is that the approach we developed here can help inform local discussions about aquaculture around the country," said project co­ lead Julie Rose from the Milford Laboratory. Rose added, ''The next phase of our project will be estimating the value of all of the clams and oysters taking up nitrogen from Greenwich waters, rather than just the harvested portion." Local Clam and Oyster Growers Pitch In

A tidal embayment with shellfish in Greenwich, Connecticut. Credit Roger Bowgen/Greenwich Shellfish Commission Greenwich is a community with a thriving shellfish aquaculture industry located on a populous coastline. It serves as an ideal case study for the nutrient-capture benefits of shel lfish. About 60 percent of the seafloor off Greenwich is used for shellfish activities, including aquaculture, recreational areas, and seed beds. Particularly in communities with diverse and diffuse nitrogen sources like Greenwich, growing shellfish for food can make a big difference to nutrient management. Partnerships with two local shellfish growers, Atlantic Clam Farms and Stella Mar Oyster Company, were crucial to this study. The companies provided data on their annual shellfish harvest and local aquaculture practices, which researchers used to model the amount of nitrogen removed. The shellfish industry in Greenwich has been supported by an active municipal shellfish commission for more than 30 years. The Greenwich Shellfish Commission was an enthusiastic partner in this research. They made local field logistics possible and will include these findings in their ongoing education and outreach efforts. "Our commission assisted by providing access to field sites and pinpointing locations for sampling. When we're involved in a NOAA project, it's an educational experience," said Roger Bowgen, Greenwich Shellfish Commissioner. ''The more we learn, the more we can explain to coastal homeowners and the general public when we engage them in conversations about shellfish aquaculture. It's a chain of discussion: everyone tells someone else."

The owner of Atlantic Clam Farms, Ed Stilwagen, on his boat. Credit: NOAA Fisheries The owner of Atlantic Clam Farms, Ed Stilwagen, also goes by the moniker "Captain Clam." He has been growing shellfish in Greenwich waters for more than 20 years and shellfishing since the 1940s. He invented a system for more environmentally­ friendly harvesting, and frequently cleans up marine debris while tending to his leases. "Shellfish are a wonderful food source, and we have perfect conditions to grow them here," said Stilwagen. ''They don't call me Captain Clam for nothing. I get a lot of interest when I tell people I'm a shellfish farmer-people want to know how many there are and how many I harvest. I hardly ever meet people who don't like clams, but even if they don't, they can appreciate that they take care of the environment by filtering the water. Having shellfish in the water improves water quality."

More Information

• Environmental Science & Technology 2020 54 (24) • Milford Lab - Current Research

Recent News

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Greenwich CT-Anthropocene: Researches calculate Value of Bivalve: 3/5/2021 https: //www. ant h ro poce ne magazine. org/2021/03 / r ese archers-ca le u late-th e-va Iu e-of-bi va Ives-appetite­ fo r -po 11 ut ion-its-h uge/?utm source-rss&utm medium- rss&utm campaign-researchers-calculate-the­ value-of-bivalves-appetite-for-pollution-its- huge&utm source-Anthropocene&utm campaign-de48756a34- Anthropocene+science+to+AM&utm medium- email&utm term-0 ececcea89a-de48756a34- 294259197

Indian River: 12/27/2020 htt ps : //www. florid atoday. com/story/ n ews/1 oca I/environment/lagoon/ 2020/12/27 /trans pla nted-su per - clams-spark-hope-cleansing-indian-river-lagoon/3893226001/

Sea & Shoreline Completes Mercabo Cove Seagrass Installation, Creating A Thriving Habitat for Manatees And Sea Life; April 8, 2021 https://markets.businessinsider.com/news/stocks/sea-shoreline-completes-mercabo-cove-seagras s­ installation-creating-a-thriving-habitat-for-manatees-and-sea-life-1030285642

Clams-Shrinking sea meadows store more carbon than forests. Scientists are racing to track what's left I April 8, 2021 https://www.reuters.com/article/us-climate-change-seagrass-idUSK BN2BVOMV

This ties to the ongoing United Nations collaborations that we have been engaged in for the last decade. April 29, 2021 https://theconversation.com/farming-fish-in-fresh-water-is-more-affordable-and-sustainable-than-in­ the-ocea n-151904

This is the Blue Community initiative that Dr David Randle leads and where Richard Jordan assists. https://www.bluecommunity.info/

This is the bio haven, microbial based nutrient mitigation technology that Bruce Kan ia leads. https://www. float ingisla ndinternationa I.com/solutions/

Shellfish motivation: the climate crisis could be solved with seas, not trees: The FISH Site;

Herald Tribune

Growing Seagrass In The Indian River Lagoon, Fort .. .: https://youtu.be/Qw9NMKl8QXk Tetsu Article : Support for Mote Marine site at Pier ://www.heraldtribune.com/story/opinion/columns/guest/2021/04/30/opinion-we-must-act-now­ protect-sarasota-bay/4886790001/

https://researchmap.jp/7000020213/presentations/11877970?lang=en

Jeff Sedacca organization : https://www.aguacultureall iance.org/about-gaa/

New Shellfish Permit Geared for Restoration: Coastal Review Online https ://www. coasta Ireview. org/ 20 21/04 / new-s hel lfish-pe rm it-geared-for· restoration/

Blue carbon Credits https://www.wired.com/story/blue-carbon-credits-could-help-restore-ecosystems/

Rerouting the Mississippi River https://www.sciencemag.org/news/2021/04/rerouting-mississiopi-river-could-build-new-land-and-save­ retreating-coast

Curt Hemmel:

2019: https://www.sarasotamagazine.com/eat-and-drink/2019/04/bay-shellfish-clam-hatchery

2017: https: //www.observernews.net/2017 /09/14/growing-shellfish-to-help-save-the-bay-and-a­ seafood-t rade-deficit/ ------

Gulf Shellfish Institute: Homepage http://www.gulfshellfishinstitute.org/

!Gulf Seafood Foundation:j ':f_O_l'!l~l)age ___ _ .. ---{ Commented [JS1 ]: https://gulfseafoodfoundation.org/

April 4, 2019 htt ps ://www. perishable news. com/ se afood/biva lve-r e-cla m-at ion-fight s-flo rida-re d-t ide-i n- tam pa-bay/ 2016/2017 http://wwv..tbrpc.org/wp-contentiuploads/2018/ 11 /START-GCORR-Program- I0. 13.2018.pdf

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Solutions to Avoid Red Tide (START)

Home Page: https://startl.org/gulf-coast-oyster-recycling-renewal-gcorr-program/

Clam Seeding Program 2019: https://startl.org/clam-seeding-program/

Oyster Reclamation Program : 2018: https://startl.org/news/start-extends-successful-oyster­ reclamation-program/ ------·------

AMI Sun: 2019: https://www.amisun.com/2019/03/02/clams-restored-in-sarasota-bay/

2019: https://issuu.com/annamariaislandsun/docs/march 6 2019 full issue

Tampa Bay Times Article: A FAILURE TO ACT https://tampabaytimes-fl.newsmemory.com/?publink=lebf3c9b0 1345d16

Ed's article Herald Tribune: Feb 24, 2020: A small Beach Town is on the Verge of Making a difference ... https://www.heraldtribune.com/opinion/20200224/guest-editorial-bradenton­ beach-bets- on-clams-to-restore-water-guality

Sun Ray Clams August 12, 2015 https: //www. tam pa bay. com/things-to-do/con sum er/sun r av-ven us-c la ms-cou Id-be-florid as-next -big­ aqua cu It u re-crop/2241100 / GULF COAST RESTORATION INITIATIVE

Ed Chiles

Affiliates: Gulf Shellfish Institute, Sea & Shoreline Aquatic Restoration, Solutions to Avoid Red Tide (START), Sunnyvale Seafood Company (SSC) ALL CLAMS ON DECK: GETTING ON BOARD TO RESTORE FLORIDA'S ESTUARIES • Paradise under pressure: • Development, Pollution, Runoff • Storms & Hurricanes • Harmful Algal Blooms • Economic consequences • Coastal communities • Commercial and Recreational Fisheries • Florida tourism

Photo credit: Capt. Scott Moore BIOLOGICAL MITIGATION STRATEGIES: USING NATURE’S TOOLBOXAquacultured Seagrass & Hard Clams

FEDERAL FUNDING & FLORIDA LEGISLATION

• $15 M will support proof of concept to research and promote large-scale restoration efforts in 3 National Estuaries • Seagrass restoration & Hard clam deployment • Tampa Bay, Sarasota Bay, Charlotte Harbor

• Florida Governor and Legislative Ask • Certify bivalves for mitigation credits and create legislation that provides avenue to proceed • Increase mitigation tools available • Increase capacity of Florida’s shellfish aquaculture industry IT’S TIME TO ACT.

Website coming soon: AllClamsOnDeck.org