Beyond bioextraction: the role of oyster-mediated denitrification in nutrient management

Abstract/Summary:

Recently, interest has grown in using oyster-mediated denitrification resulting from aquaculture and restoration as mechanisms for reactive nitrogen (N) removal. To date, short-term N removal through bioextraction has received the most management interest, but there is a growing body of research that has shown oysters can also mediate the long-term removal of N through denitrification (the microbial conversion of reactive N to relatively inert di-nitrogen (N₂) gas). Oyster suspension feeding and subsequent ammonium releases and deposition of organic matter to the sediments can stimulate nitrification-denitrification cycling near oyster reefs and aquaculture sites. Oysters harbor a diverse microbial community in their tissue and shell promoting denitrification activity and enhanced N removal. Additionally, the surface area of oyster reefs also provides habitat for other filter-feeding macrofaunal communities that can further enhance denitrification. Denitrification is a complex biogeochemical process and is also difficult to convey to stakeholders. These complexities have limited consideration and inclusion of oyster-mediated denitrification within nutrient management. Although oyster-mediated denitrification will not be a standalone solution to excess N loading, it may provide an additional management tool that can leverage oyster aquaculture and habitat restoration as a N mitigation strategy. Here we provide an overview of the biogeochemical processes involved in oyster-mediated denitrification and summarize how it could be incorporated into nutrient management efforts by various stakeholders.

Graphical Abstract

Introduction:

One of the most serious threats to coastal ecosystems globally is excess nitrogen (N) loading and subsequent eutrophication (NRC 2000, Galloway et al. 2003, Smith et al. 2006). Local (e.g., runoff, sewage discharge) regional, and global (e.g., fertilizer use, fossil fuel burning) activities increase the amount of N discharged to coastal waters. While N is necessary for all life, too much of it leads to a range of negative ecological consequences such as shifts in primary producer (e.g., phytoplankton, macroalgae) composition and abundance, increased frequency and duration of low oxygen conditions (Rabalais et al. 2002) and decreases in biodiversity (Breitburg et al. 2009, Paerl and Scott 2010). These ecological consequences drive negative societal changes too, such as declines in economic prosperity when fisheries decline (Oczkowski and Nixon 2008), reduced property values (Walsh et al. 2017), degraded recreational experiences (Johnston et al. 2002), and loss of tourism revenue (Bechard 2020).

In order to protect and restore our coastal systems a variety of technologies, policy mandates, and management plans have been developed to reduce N inputs and mitigate impacts of excess N. Traditional management and policy initiatives focused on intercepting and removing N from point - (e.g. wastewater treatment plants) and non-point sources (e.g. agricultural fields) before it reaches coastal areas. Removal techniques include improved wastewater treatment infrastructure and applying best management practices for fertilizer application (Riemann et al. 2016). Unfortunately, implementing such watershed-scale source control is costly and can take decades to be realized (Duarte and Krause-Jensen 2018). Given the logistical and economic challenges associated with successfully implementing N source control programs additional tools that allow for removal of N directly from coastal systems are being explored (Duarte and Krause-Jensen 2018).

Typically, in situ N reduction practices work by enhancing N removal by an ecological community or habitat within a system. Familiar examples include restoring a wetland plant community or installing floating islands of wetland plants to a coastal area. These practices are already included in some N management plans in the United States (Craig et al. 2008, Mulbry et al. 2010). Another example would be restoring or installing communities of bivalves or macroalgae to support N removal via bioextraction (Rose et al. 2014). In bioextraction, the N incorporated into the biomass of shellfish or seaweed is removed during harvest (Sebatiano et al. 2015). Total N mitigation via bioextraction is a relatively simple metric to quantify and is therefore increasingly used by managers seeking to reduce N pollution in coastal areas. A prominent example is bioextraction through oyster aquaculture, which is now being implemented or considered as a management tool for N mitigation throughout the United States (e.g., Chesapeake Bay, Cape Cod estuaries, Long Island Sound; Reichert-Nguyen et al. 2016, Cape Cod Commission 2015, Long Island Nitrogen Action Plan Scope 2016, Bricker et al. 2017, Bricker et al. 2019) and internationally (e.g., Songsangjinda et al. 2000, Gifford et al. 2005). Shellfish can provide another mechanism of N removal via the enhancement of denitrification (the microbial conversion of reactive N to inert di-nitrogen (N₂) gas). Here we provide stakeholders and decision-makers with an overview of oyster mediated denitrification, examples of its use for potential incorporation into future N management programs, and areas of further study.

Oysters and Denitrification

Not all N has the same impact on coastal ecosystems, and in fact, almost 80 percent of our atmosphere is di-nitrogen (N₂) gas. We refer to N₂ gas as un-reactive or biologically unavailable because most organisms cannot use it to grow. We refer to other forms of N such as nitrate or ammonium as reactive or biologically available because these nitrogen compounds support or are products of growth and cell metabolism (Stein and Klotz 2016). Denitrification is a microbially driven process that converts reactive nitrogen (e.g., nitrate) to unreactive nitrogen (e.g., N₂ gas) and thus permanently removes the N from the waterbody. In many coastal ecosystems, denitrification is coupled to nitrification. During nitrification, microbes convert ammonium to nitrate which subsequently fuels denitrification. Denitrification is regulated by a variety of environmental conditions including the availability of nitrate as well as the the quality and quantity of available organic matter. Oysters can stimulate denitrification in at least three ways, by: 1) enhancing denitrification through increasing organic matter deposition to the sediments; 2) hosting denitrifying bacteria on or within their bodies and/or; 3) providing habitat for other filter-feeding macrofaunal communities (Figure 1).

Figure 1.

Nitrogen removal in oyster habitats. Oysters are efficient filter feeders and they can increase organic matter deposition to the sediments via biodeposition. In turn, this organic matter is decomposed releasing ammonium (NH₄⁺) to the environment. This ammonium can fuel phytoplankton and macroalgae production or it can be converted to nitrate (NO₃⁻) via nitrification. This nitrate can then fuel denitrification, the natural filtering process that converts biologically usable nitrogen to di-nitrogen gas (N₂) or nitrous oxide (N₂O). These nitrogen cycling processes can take place in the sediments beneath or surrounding oyster reefs and cultivation operations as well as within the microbial community associated with the oyster themselves.

First, oysters are efficient filter feeders and ingest large amounts of particulate matter from the water which is then released to the sediments as biodeposits (Figure 1). Biodeposits include feces or “pseudofeces,” which are rejected particles wrapped in mucus (Newell et al. 2004). These organic matter rich biodeposits can help fuel denitrification. Oysters also directly excrete ammonium and stimulate sediment ammonium flux. In the presence of oxygen, this ammonium can help fuel coupled nitrification-denitrification.

Demonstrating enhanced sediment denitrification from oyster biodeposition in a reef or aquaculture setting requires showing significantly higher rates compared to bare (i.e., no oysters) sediments. Past individual studies report varying effects of oysters on denitrification. For oyster aquaculture, some studies report a decrease in denitrification (e.g., Higgins et al. 2013), some an increase (e.g., Humphries et al. 2016, Vieillard et al. 2017, Lunstrum et al. 2018), and others report no change at all (Mortazavi et al. 2015, Erler et al. 2017). For oyster reefs, studies generally report enhanced sediment denitrification (Piehler and Smyth 2011, Smyth et al. 2013, Kellogg et al. 2013, Hoellein et al. 2015, Humphries et al. 2016) compared to bare sediment, although Westbrook et al. (2019) and Ayvazian et al. (In Review) found no difference. The discrepancy in the reported results likely comes from a variety of study variables including the different techniques used to measure denitrification, the time and spatial scales of measurement, and the inclusion or exclusion of oysters in the denitrification measurements (Ray and Fulweiler 2020). Recently however, a recent meta-analysis used a statistical approach to deal with inter-study variability and demonstrated that when examining all the studies together oysters enhance sediment dentification. Sediment denitrification rates are similar in reef restoration and oyster aquaculture producing positive effects on N removal via denitrification (Ray and Fulweiler 2020). This meta-analysis could not identify common environmental characteristics driving the enhanced denitrification because such data are typically not reported or not measured, which is an important research need.

Second, oysters themselves contain a diverse microbiome on their shells and in their digestive tracks (Chuahan et al. 2014, Arfken et al. 2017) which can both recycle and remove N (Caffrey et al. 2016, Ray et al. 2019) (Figure 1). Studies report high rates of denitrification (Smyth et al. 2013, Caffrey et al. 2016, Arfken et al. 2017, Ray et al. 2019) as well as high rates of nitrification (Caffrey et al. 2016) in the bodies of oysters and oyster shells. Ray et al. (2019) synthesized these studies and found up to a four times difference in the rates of denitrification across studies for live oysters. Results from studies examining denitrification in oyster shells alone (i.e., dead oysters within a reef) have been mixed. Some studies found that shells had reduced denitrification (Caffrey et al. 2016) or no denitrification (Ray et al. 2019) compared to live oysters, while other studies have found similar rates of denitrification between live oysters and shells only (Arfken et al. 2017).

Third, oysters create habitat for other filter-feeding organisms, such as mussels, tunicates, and barnacles (Kellogg et al. 2013, Jackson et al. 2018). These macrofaunal communities living on the surface area of oyster reefs may contribute additional opportunities for enhanced denitrification. Jackson et al. (2018) found that the biogeochemical measurements of intact oyster clumps from a restored reef that had undisturbed macrofaunal communities produced high rates of denitrification. While this study did not directly assess the macrofaunal communities, it suggests that a measurement approach that incorporates the whole reef community (e.g., oysters, oyster-associated macrofauna, sediment microorganisms) likely produces estimates closer to the total N reduction from oyster-mediated denitrification. However, current methods to establish denitrification rates of whole reef communities are costly and more complex than sediment measurements alone.

Implementing oyster-mediated denitrification as a mitigation tool will require measurements of denitrification rates from oyster habitat and non-oyster habitat for comparison. Recently an effort was undertaken to develop recommendations for managers on how best to measure denitrification and what environmental characteristics should simultaneously be collected to help inform future management goals (Ray et al. In Review). Some of these recommendations include directly measuring denitrification with the N₂/Ar technique (determines the net N₂ production as the difference between N₂ production by denitrification and N₂ consumption by N-fixation), collecting rate measurements seasonally, and reporting environmental parameters such as sediment oxygen demand and inorganic nutrient concentrations (i.e., ammonium and nitrate concentrations) (Ray et al. In Review). Additionally, there are efforts that are developing enhanced denitrification estimates by using data where the sediments and the whole reef community are included in the N₂-N flux measurements to determine the total N reduction from denitrification per reef acre (Cornwell et al. 2019a).

Implementing oyster denitrification into nitrogen management

Oyster habitats (aquaculture and restoration) contribute to coastal communities by providing a range of ecosystem services (e.g., food, jobs, habitat, storm protection, etc.) (Grabowski et al. 2012, Beck et al. 2011, Coen et al. 2007). Now denitrification is being evaluated as a tool for helping states and municipalities meet regulatory nutrient mitigation requirements. Many coastal areas in the United States are required by law to improve water quality using nutrient reduction targets for point- (e.g., wastewater) and non-point (e.g., stormwater runoff, agricultural runoff) sources which is called a Total Maximum Daily Load (TMDL). Historically, the establishment, expanded capacity, and treatment technologies of wastewater treatment facilities and sewering have been implemented to address N reduction goals in TMDLs. Currently, states and municipalities faced with TMDLs are also seeking innovative and non-traditional solutions to their non-point water quality issues, including oyster-mediated denitrification. The Chesapeake Bay Program Partnership (Reichert-Nguyen et al. 2016, Cornwell et al. 2019b) and Cape Cod’s Clean Water Act Section 208 Area Wide Water Quality Management Plan Update (Cape Cod Commission 2015) are exploring the use of oysters to mitigate N in managing water quality.

The Chesapeake Bay Program Partnership has implemented one of the most comprehensive nutrient-reduction programs in the world, and its efforts are resulting in improvements of water quality (Zhang et al. 2018). The program uses a suite of best management practices (BMPs) that are recommended by expert panels. The Chesapeake Bay Program Partnership has already approved oyster aquaculture BMPs for the bioextraction of N and phosphorus (P) from harvested tissue for use in crediting towards TMDL requirements (Reichert-Nguyen et al. 2016). They are now in the process of evaluating BMPs involving sequestered N and P and oyster-mediated denitrification through oyster reef restoration. Specifically, the Chesapeake Bay Program Partnership has given interim approval to BMPs for N reduction through sequestration in tissue and shell (Reichert-Nguyen et al. 2019) and enhanced denitrification (Cornwell et al. 2019b) from oyster reef restoration practices using hatchery-produced oysters and/or reef substrate. Interim BMPs have not been fully approved to receive credit in the TMDL but have been given approval for use in planning purposes since they are near completion of the BMP panel review process. The enhanced denitrification protocol for the interim oyster restoration BMPs was developed from efforts in Harris Creek, Maryland using methods that assessed the whole reef community (Cornwell et al. 2019b).

The BMP approval processes are intentionally stakeholder inclusive, with several required meetings, webinars, and public review of report drafts throughout the approval process. For each BMP, an expert panel is charged with reviewing available science and developing recommendations on the nutrient reduction effectiveness of proposed practices following the Chesapeake Bay Program Partnership’s BMP Review Protocol (Chesapeake Bay Program 2015). These recommendations are reviewed by the Chesapeake Bay Program Partnership for approval. Practices for BMP review are typically proposed by jurisdictions to the Chesapeake Bay Program to allow them to use these practices for credit in meeting TMDL requirements (e.g., City of Virginia Beach sent a letter to the Chesapeake Bay Program requesting that denitrification from sanctuary oyster reefs undergo BMP consideration). The panels comprise a mix of academic, government, and nonprofit researchers and practitioners (e.g., the panelists from the Oyster BMP Expert Panel can be found in Reichert-Nguyen et al. [2016]). The Oyster BMP Expert Panel convened multiple stakeholder meetings that included representatives from various industries (commercial fishing, aquaculture, and those developing nutrient crediting businesses), environmental groups, academic researchers, as well as local, state, and federal agencies.

As the process for BMP review and approval can take several years, the interim BMP status allows states charged with developing plans to meet TMDL requirements to incorporate BMPs that are likely to become available in the near future for nutrient management strategies. Both Maryland and Virginia have identified interest in using enhanced denitrification in their Watershed Implementation Plans. The interim approval of the oyster reef restoration BMP is the most formalized use of oyster-mediated denitrification in the United States to address N reduction targets. The Oyster BMP Expert Panel is in the process of submitting their complete BMP recommendations on the N reduction effectiveness of enhanced denitrification from oyster reef restoration practices for stakeholder review and Chesapeake Bay Program Partnership approval.

The Chesapeake Bay Program is the most advanced in its consideration of oyster-mediated denitrification as a management tool. Other regions such as Cape Cod, Massachusetts, are also considering this practice. There are several towns experimenting with the use of oysters as an in-water mitigation tool for their coastal nutrient pollution challenges (Cape Cod Commission 2015, Reitsma et al. 2017, Rivero Lopez 2018, Howes and Eichner 2018, Town of Mashpee Sewer Commission 2015). Currently, all mitigation projects involving shellfish that have been accepted by the state for meeting the TMDLs require the removal of oysters (i.e., bioextraction; Cape Cod Commission 2015). In addition, some municipalities have explored getting credits for denitrification from oysters. Howes and Eichner (2018) determined N removal potential of oyster bioextraction and oyster-mediated sediment denitrification for Lonnie’s Pond, a sub-estuary of Pleasant Bay; however, to date, Massachusetts regulators have not approved the use of oyster-mediated sediment denitrification values to meet individual waterbody TMDLs.

As states and towns have explored the use of oyster-mediated denitrification as a BMP, they have often found the complexity of the measurements, variability of the spatial and temporal rates of denitrification, and application of the calculations too challenging to integrate into a nutrient management framework. Efforts to resolve these issues in coastal areas could help not only Chesapeake Bay, but also Cape Cod, Long Island, and other coastal communities to develop implementation strategies for the use of oyster-mediated denitrification that can help meet TMDL requirements.

Stakeholder Engagement and Communication in Oyster-Mediated Denitrification BMPs

Meeting N reduction goals necessitates behavior change by residents and governments as well as public support of localized and regional mitigation efforts (Perry et al. 2020). Stakeholder engagement is a critical piece in the implementation of all nutrient BMPs, because it broadens the ideas and creativity of management efforts (Beierle and Cayford 2002) and increases acceptance from local communities and decision makers (Giordano et al. 2005). For example, engaging diverse perspectives in environmental management can increase the perception of fairness as well as the trust of those who may affect or be affected by the management efforts (Costanza and Ruth 1998). Thus, for oyster-mediated denitrification to work as a part of nutrient management strategies, stakeholders must be included. Denitrification is a complicated topic and requires varied communication approaches specific for individual stakeholder groups. For example, what a wastewater treatment plant (WWTP) operator needs to know to meet their local nitrogen management goals is different from what the wider public needs to understand. Different approaches and discussion points may be needed when communicating the potential of oyster-mediated denitrification. Applying key principles of effective public engagement, it is important to consider:

• Who are the stakeholders?

• What are their roles in nutrient management?

• How do they best receive AND provide information?

• What challenges may exist that may impede the ability to communicate and ultimately achieve “support” for the effort?

There is a contingent of common stakeholders that may need to be engaged in a nutrient management process that is considering the use of oyster-mediated denitrification BMPs (Table 1). Stakeholder engagement and communication needs to include both formal and informal methods (Buanes et al. 2005). Some suggested mechanisms for engagement and communication include the development of simplified infographics, guest lectures from respected scientists, site visits to restoration or aquaculture sites, citizen science water quality monitoring programs, technical reports, newspaper and other general news media, community meetings, workshops, webinars, and direct one-on-one meetings.

Table 1.

Common stakeholder groups and their roles in oyster-mediated denitrification best management practices (BMPs). This list provides some common roles, but is not a comprehensive representation of all potential roles.

Stakeholder Group	Example Roles in Oyster-Mediated Denitrification BMPs
Federal, state, and local decision makers	-Deliver messages to other groups (stakeholder communication) -Develop program and management options for oyster-mediated denitrification, including reporting mechanism and monitoring -Secure funding to support program -Serve as a clearing house for concerns and issues -Coordinate and convene management efforts
WWTP operators and public works	-Consider alternatives financially and in practice -Support as an option to contribute to meeting their nutrient reduction needs -Implement program for denitrification (monitoring)
Community residents/ general public	-Understand need for abatement of excess nitrogen and oyster-mediated denitrification concepts -Support nitrogen abatement actions
Water recreationists (boaters, anglers, shellfish harvesters)	-Identify and avoid shellfish farms or reefs -Refrain from harvesting shellfish from non-designated (i.e. closed) areas -Limit activities that could harm farms or reefs, including discharge of waste -Collect data as part of citizen science monitoring efforts
Shoreline property owners	-Understand their potential role in creating excess nitrogen, need for nitrogen abatement, and potential actions they can take to support reduction -Support the role of oyster-mediated denitrification in nitrogen loading and abatement actions
Environmental and civic organizations	-Implement oyster restoration -Conduct monitoring of restoration sites and water quality -Stakeholder communication -Secure or provide funding to support programs for restoring oyster reefs or increasing oyster aquaculture production
Aquaculture industry	-Grow oysters -Monitor oyster “growth” to support denitrification calculations -Provide education through tours and other public outreach opportunities on their farms and practices -Collaborate with researchers to collect data at their farm sites -Stakeholder communication -Participation in BMP review stakeholder panels
Ports /working waterfront	-Consider role in nitrogen loading and consider abatement actions -Consider opportunities for oyster growing
Community industries/polluters	-Consider role in nitrogen loading and consider abatement actions -May develop/implement a management plan to help meet TMDL

While engagement, collaboration, and communication in BMP development is important, it can also be challenging (Bryson et al. 2006). Stakeholder groups have different incentives to participate and anticipating these differences by examining localized elections or funding initiatives will help frame productive stakeholder conversations. In some cases, a lack of interest may inhibit stakeholder engagement. For example, members of the general public may be antagonistic towards increased aquaculture or reef restorations out of concerns for impacts on the aesthetics or available uses of local waters. This was highlighted in a recent study that found support for aquaculture was not a clear cut for/against attitude. Instead, support depended upon the waterbody, the acreage of the farm, and farming methods (Dalton and Jin 2018).

Implementation will also be heavily dependent upon the ability to permit the reef restorations or increases in oyster production as well as funding for restoration, monitoring, and maintenance. Integrating oyster aquaculture and restoration activities into BMPs can become complicated because of the private industry, public institutions, and other stakeholders who may be involved. Allocation and acquisition of funding can be contentious, and many of these projects can be quite expensive. For example, Bayraktarov et al. (2016) estimated a median restoration cost for oyster reefs at $189,665 (2010 USD$) per hectare. Clearly, articulating a cost-benefit analysis, including comparing the costs of oyster-mediated denitrification with other N removal strategies (e.g., advanced treatment septic systems or permeable reactive barriers) will be key. One such study used an avoided cost analysis, with wastewater treatment as the alternative management measure, to calculate the maximum potential value of N removal from Great Bay, New Hampshire (Bricker et al. 2019). Estimation of the value of N removal via assimilation from aquaculture and restored reef oysters, and denitrification from reef oysters, is $461,000 and $760,000 for current and expanded leased aquaculture areas, respectively.

Perceptions from different stakeholders may come down to not understanding the complex processes involved in oyster-mediated denitrification. This is something that can be overcome by developing a communication approach that clearly emphasizes the potential importance of oyster-mediated denitrification to each type of stakeholder. For example, building off the insights from Dalton and Jin (2018) that support for aquaculture varies depending on the place and type of farming could allow for more targeted communication to coastal homeowners or zoning officials about the potential co-benefits of denitrification within their specific waterbodies. This communication is particularly challenging as eutrophication and denitrification are highly technical and can be difficult to explain, thus it is critical to communicate select key messages with stakeholders (for a general set of key messages, see Figure 2). These messages include the need for basic public information about the impacts of nutrients on coastal waters which may include simplified explanations of the nitrogen cycle or nutrient impacts. It is essential that all stakeholders understand that oyster-mediated denitrification will not meet the entire TMDL requirements but can be a useful component of a larger multifaceted approach.

Figure 2.

Examples of key messages for communicating oyster-mediated denitrification to many of the stakeholders identified in Table 1. Images in the example factsheet are from The Noun Project (thenounproject.com: Eucalyp, “oyster;” Yu Luck, “water pollution;” Smalllike, “oyster;” and Olena Panasovska, “Communication”).

Next Steps

Implementation Needs.

To date, oyster-mediated denitrification has not been formally included in a watershed management plan for N reduction. As a step towards integrating this approach into nutrient management plans, the Chesapeake Bay Partnership has initiated strategies for developing spatially explicit verifiable metrics for including oyster-mediated denitrification rates of the whole reef community to apply toward meeting TMDL N loading targets. To gain widespread acceptance for inclusion of oyster-mediated denitrification in N management plans one state or a group of states will have to pioneer proposed approaches through to implementation, and that may prove challenging. Implementation will depend on creating BMP guidelines for standardized procedures to verify denitrification rates, followed by monitoring protocols, and maintenance for either a restoration site or an aquaculture operation. Once an oyster aquaculture operation is expanded or a restoration effort is implemented, crediting these approaches can take any number of forms, all of which require agreements among diverse stakeholders and agencies. The existing strategy for bioextraction in the Chesapeake Bay can serve as a model to be built upon for future management implementation of oyster-mediated denitrification as monitoring standards are developed and management implications are better understood.

Research Needs.

One of the most salient scientific needs is the demand for consistent, rapid, and cost effective methodologies and metrics for quantifying denitrification, including enhanced sediment denitrification, individual-oyster based denitrification through shell and gut microbial activity, and whole reef community denitrification measurements. Successful use of oyster-mediated sediment denitrification includes calculating N budgets for both restoration and aquaculture efforts that include both bioextraction and denitrification values, identifying N burial potential, determining legacy impacts on sediments from oyster aquaculture, calculating estuary-specific oyster growth potential, tracking fate of oyster biodeposits, and identifying adequate larval recruitment to ensure reef sustainability. For oyster microbial communities, if individual-oyster denitrification values can be calculated and replicated, it may be possible to implement denitrification credits for individual oysters and incorporate into a BMP for nutrient credit schemes. Whole reef community denitrification requires more research from different habitat types (e.g., intertidal, subtidal), differing levels of disturbance (e.g., water flow, harvesting method, harvesting schedules), and varying water quality/nutrient gradients to better understand factors affecting denitrification rates leading to improved estimates for N reduction crediting. Additional research is also needed to reduce uncertainty surrounding the denitrification potential given high variability in denitrification measurements. Urgent future research will need to determine how multiple biological and chemical-physical drivers (e.g., oyster size, density, reef age, cultured vs. reef oysters, water column N, temperature, salinity, dissolved oxygen, seasonal variation) may affect denitrification rates. Identifying the environmental conditions that enhance N removal in oyster habitats would enable better use in N management. In building these research efforts, deliberate and informative engagement with a range of stakeholders may also identify additional research needs that will better facilitate the use of oyster-mediated denitrification in nutrient management.

Limitations.

Although oyster-mediated denitrification offers considerable promise for contributing to N reduction in coastal waters, it will not replace extensive source control efforts. In particular, there are concerns that focusing on in-situ remediation will lead to less efforts preventing N from entering the system. There are limits to both ecological and social carrying capacity in coastal systems for oyster aquaculture and restoration (Dalton et al. 2017; Byron et al. 2015). Ecological constraints could include food availability, appropriate habitat, and water quality (Coen and Luckenbach 2000). Social acceptance has been identified as a primary deterrent to the use of BMPs such as oyster aquaculture (Dalton and Jin 2018; Dalton et al. 2017; Rose et al. 2014). Social constraints may include conflicts in use of the space by recreational users or aesthetic impacts on coastal homeowners and visitors (Dalton and Jin 2018; Dalton et al. 2017).

Moving Forward.

Tackling N pollution remains a great environmental challenge in coastal systems across our nation and the world. Oyster-mediated denitrification has the potential to make important contributions to N reduction and management planning in conjunction with more traditional point source control and other BMPs. Broader incorporation into management necessitates a better understanding of how denitrification works and what limitations exist in the implementation of oyster-mediated denitrification by managers and practitioners. Careful engagements with a range of stakeholders to identify information and research needs, facilitate adoption, and incorporate limitations is critical for increasing the use of oyster-mediated denitrification for nitrogen reduction. With advancements in research and engagement, there is considerable opportunity for the incorporation of oyster-mediated denitrification into nutrient mitigation policies in coastal areas.

Short Synopsis:

Oysters are a promising tool for nitrogen mitigation as they can enhance denitrification, a natural microbially driven nitrogen removal process.