Conservation aquaculture as a tool for imperiled marine species: Evaluation of opportunities and risks for Olympia oysters, Ostrea lurida.

Conservation aquaculture is becoming an important tool to support the recovery of declining marine species and meet human needs. However, this tool comes with risks as well as rewards, which must be assessed to guide aquaculture activities and recovery efforts. Olympia oysters (Ostrea lurida) provide key ecosystem functions and services along the west coast of North America, but populations have declined to the point of local extinction in some estuaries. Here, we present a species-level, range-wide approach to strategically planning the use of aquaculture to promote recovery of Olympia oysters. We identified 12 benefits of culturing Olympia oysters, including identifying climate-resilient phenotypes that add diversity to growers' portfolios. We also identified 11 key risks, including potential negative ecological and genetic consequences associated with the transfer of hatchery-raised oysters into wild populations. Informed by these trade-offs, we identified ten priority estuaries where aquaculture is most likely to benefit Olympia oyster recovery. The two highest scoring estuaries have isolated populations with extreme recruitment limitation-issues that can be addressed via aquaculture if hatchery capacity is expanded in priority areas. By integrating social criteria, we evaluated which project types would likely meet the goals of local stakeholders in each estuary. Community restoration was most broadly suited to the priority areas, with limited commercial aquaculture and no current community harvest of the species, although this is a future stakeholder goal. The framework we developed to evaluate aquaculture as a tool to support species recovery is transferable to other systems and species globally; we provide a guide to prioritizing local knowledge and developing recommendations for implementation by using transparent criteria. Our collaborative process engaging diverse stakeholders including managers, scientists, Indigenous Tribal representatives, and shellfish growers can be used elsewhere to seek win-win opportunities to expand conservation aquaculture where benefits are maximized for both people and imperiled species.

Introduction

Marine biodiversity and the ecosystem services marine species provide are in decline globally, but it is not too late for these changes to be reversed [1]. Marine foundation species (e.g. kelp, mangroves, corals, oysters) are critical to the structure and resilience of coastal ecosystems, providing key ecosystem services to human communities around the world [2, 3]. Many marine foundation species have suffered severe population declines due to human activities including overfishing, habitat loss, and climate change (e.g. [4, 5]). Oysters act as foundation species by creating habitat for other estuarine species and providing key ecosystem services to human communities around the world [6-8]. In addition to ameliorating environmental stressors, such as dampening storm surges [9] and improving water quality via increased filtration [10], oysters have been a food source for people around the world for millennia, through both harvest of wild populations and aquaculture [11]. However, like many other marine foundation species, oyster populations have declined precipitously: in the United States, there has been an 88% loss in oyster biomass [12] and worldwide, an estimated 85% of oyster reefs have been lost, a figure exceeding the estimated loss of coral reefs [9]. Simultaneously, ever-rising global demand for protein, among other factors, is driving the rapid expansion of shellfish aquaculture [13-15], including oyster farming, while the restoration of native oyster species and wild oyster beds has become a priority for maintaining the health and ecosystem function of estuaries [16, 17].

The Olympia oyster (Ostrea lurida) is native to estuaries from British Columbia, Canada to Baja California, Mexico [18, 19], and a prime example of a foundation species whose populations have drastically declined. Olympia oysters historically created habitat for numerous estuarine and coastal species [20, 21], were harvested by Indigenous people [22, 23], and supported a vital fishery [24]. However, populations declined throughout its range due to over-harvesting and habitat degradation following European settlement [25, 26]. In some regions, populations have been reduced to 1% of their historic levels and face local extinction [10]. Thus, while Olympia oysters are still present in many estuaries, they no longer form dense, habitat-forming beds in many places. Wild populations of the native oyster are further challenged by the alteration of estuarine habitats, non-native predators, poor water quality, sedimentation, and lack of natural recruitment [27, 28]. Importantly, a recent synthesis revealed that recruitment limitation is the second biggest challenge to restoration success with Olympia oysters throughout their range, negatively affecting over 70% of all projects [28].

Conservation aquaculture–defined by Froehlich [29] as human cultivation of an aquatic organism for the planned management and protection of a natural resource–is a tool with enormous potential to benefit both nature and people, by simultaneously supporting populations of marine species and providing economic and social benefits to human communities. Conservation aquaculture emphasizes the importance of ecologically responsible methods to implement, and scientifically rigorous methods to evaluate, the use of aquaculture techniques that purposefully align with conservation goals. Its techniques also specifically seek to minimize the risks sometimes associated with conventional aquaculture. For example, conservation hatchery protocols address risks related to the release of hatchery-reared organisms, including preserving the genetic diversity of the wild population and minimizing the propagation of invasive species [30, 31]. Here, we focus specifically on the application of conservation aquaculture as a tool to aid the recovery of an imperiled species, although its definition and benefits can be much broader [29]. Conservation aquaculture programs have been successful in supporting the recovery of endangered fish (e.g. white sturgeon: [32]) and invertebrate populations (e.g. white abalone [33]), and aquaculture techniques have successfully supported restoration of declined oyster populations (e.g. eastern oyster Crassostrea virginica [34]; European flat oyster Ostrea edulis [35]). However, aquaculture has generally been used opportunistically, at sites where existing hatcheries or conservation organizations are located, without range-wide strategic planning to prioritize locations that would most benefit imperiled species.

In fact, conservation aquaculture is likely to be of greatest benefit in supporting imperiled populations where reproduction is a key bottleneck to population growth, and where conditions are favorable for survival of juveniles [36]. Aquaculture is only one of many conservation tools and may be most effectively used for species recovery when integrated into a holistic management strategy (e.g. alongside fishing regulations and/or habitat improvement planning; [37, 38]). Importantly, conservation aquaculture also comes with potential risks such as the loss of genetic adaptations of the wild population and modification of habitat by the placement of commercial gear or artificial reef structures [39]. These concerns were recently highlighted by efforts to use conservation aquaculture to restore populations of reef building corals [40]. Froehlich [37] emphasized the importance of exploring potential ecological trade-offs associated with conservation aquaculture and the need to collaboratively work with stakeholders to set shared conservation goals and priorities.

The use of aquaculture techniques to support the recovery of Olympia oyster populations is relatively limited to date. Efforts to produce oysters for restoration were pioneered in Oregon and Washington in the 1990s, through individual partnerships between managers and commercial or tribal hatcheries. The first conservation hatchery for this species, the Chew Center, was established in 2013, increasing capacity for restoration efforts in Washington via a partnership between the National Oceanic and Atmospheric Administration and Puget Sound Restoration Fund. A few aquaculture-assisted restoration projects have since been employed in central California and Oregon where estuary-wide recruitment failure is common [27, 36]. However, the majority of projects throughout the species’ range have not utilized aquaculture to restore or enhance populations [28].

Likewise, since the onset of the cultivation of Olympia oysters, commercial aquaculture of the native oyster has remained very limited [24]. The Pacific oyster (Crassostrea gigas)—a hardy, fast-growing native of east Asia—has instead been the dominant commercially grown oyster on the West Coast [41]. While some commercial growers raise Olympia oysters as a specialty product, they may be more motivated by an interest in the ecology and heritage of the species than its current monetary value. However, consumer interest and demand for Olympia oysters is increasing, and with it the potential for additional growers to create a larger Olympia oyster market, with prices equal to or greater than Pacific oysters [42].

To our knowledge, there has been no thorough evaluation of the rewards versus risks of conservation aquaculture to guide strategic planning for any marine species on this coast. Here, we present a species-level, range-wide approach to strategically planning the expanded use of aquaculture as a tool to support recovery of Olympia oysters. Before funders, planners, regulators, conservation organizations, or growers move forward with aquaculture initiatives, there is a pressing need to conduct a robust, collaborative evaluation of whether and under what conditions the rewards outweigh the risks. Additionally, detailed spatial analyses are needed to identify the specific locations where conservation aquaculture efforts can be expected to have a high likelihood for success. A transparent and consistent evaluation process is essential to assess sites across the range of the species, so stakeholders can jointly identify those places where aquaculture is most likely to support species recovery and/or enhance local communities. Funders and conservation organizations require assistance to make strategic investments to gain the greatest impact on species recovery, resource management agencies want to know where risks are lowest, and growers want greater confidence in determining how and where their native oyster aquaculture investments can support conservation efforts. Decision-support tools have been developed to inform strategic planning for aquaculture in other regions [43, 44].

Our goal was to conduct strategic planning and develop a framework to evaluate the use of aquaculture to support recovery of Olympia oysters across the range of the species. We also assessed human dimensions of aquaculture, including the potential for community harvest and commercial production, within the framework of supporting recovery of wild populations. We designed an inclusive process of engaging stakeholders from the beginning, which is much more likely to yield results and reduce conflict [45]. We thus drew from and expanded upon the membership of the Native Olympia Oyster Collaborative (https://olympiaoysternet.ucdavis.edu/), which brings together local stakeholders united by the belief that a coast-wide perspective will lead to better conservation outcomes for the species. Our team of growers, tribal representatives, scientists, and conservation practitioners evaluated the potential of conservation aquaculture for this species, benefitting from both the local expertise represented by participants, and the commitment to coast-wide collaboration. Together, we explored the rewards and risks of aquaculture for this species, identified priority locations for new or expanded investment in this tool, and assessed human dimensions, to consider the types of aquaculture projects most appropriate for those locations. This collaborative approach, with jointly developed criteria applied consistently at a broad geographic scale, can serve as a model for other species where aquaculture may assist in recovery of wild populations.

Methods and materials

Collaborative process with stakeholder team

We engaged a diverse group of 30 stakeholders with expertise or interests related to Olympia oyster restoration, conservation, and production of native oysters for local food systems. Members of the stakeholder group were selected from the full geographic range of this species from British Columbia, Canada to Baja California, Mexico, based on their expertise in working with Olympia oysters, with attention to engaging stakeholders with different goals and perspectives. Most were already affiliated with the Native Olympia Oyster Collaborative and were known to our core team as a result of our earlier work establishing this network, though some were new partners referred to us by members. Our stakeholder group included conservation scientists, restoration practitioners, aquaculture specialists from non-profit organizations and state and federal agencies, marine resource managers, representatives from two Western Washington Treaty Tribes, and commercial oyster growers (S1 Table). To iteratively incorporate expertise with ecological, social, and economic factors, we engaged the stakeholder group in three primary stages: (1) qualitatively identifying and refining the rewards and risks (i.e. trade-offs) for conservation aquaculture of this species, (2) selecting estuaries to evaluate, and (3) creating and scoring the conservation aquaculture indices for each estuary. We communicated through many small virtual meetings and through review of shared on-line documents, and also held discussions with the full group in a two-day virtual workshop. We used collaborative, iterative processes to gather the best available quantitative data, elicit the group’s expert opinion, and/or solicit the input of additional local stakeholders where appropriate through focused meetings in particular regions. Our work did not involve ‘research on human subjects’; we did not collect information about participating members or study their individual perspectives, and thus did not require Institutional Review Board approval. Instead, the input from stakeholders with diverse expertise was synthesized as a collaborative activity with all stakeholders involved in the team effort.

Rewards and risks of conservation aquaculture with Olympia oysters

Conservation aquaculture provides a suite of rewards and risks that are specific to the species and population under consideration. In March 2020, the stakeholder group met to explore the wide range of potential rewards and risks associated with conservation aquaculture of Olympia oysters in western North America. The range of potential rewards and risks was then condensed into broad categories based on the primary beneficiary: (1) Olympia oyster populations, (2) the coastal ecosystem, (3) Tribes / First Nations, and other local community members, (4) conservation practitioners, and (5) commercial growers. Due to the overlap of rewards and risks identified for Tribes / First Nations and local community members, these were later combined into one user group. This list was further condensed to focus on the rewards and risks that were specific to conservation aquaculture, rather than general rewards and risks that could also be applied to oyster restoration.

While the rewards and risks were often determined to have more than one recipient group, one primary recipient group was identified and listed. We separately present the rewards and risks relative to our focal beneficiary categories as they can differ according to which entities the project is designed to benefit. For example, projects including harvest or commercial production will have different associated rewards and risks than projects focused solely on restoration. Likewise, there are different rewards and risks involved if project goals include community engagement than if the project is conducted by staff at a conservation organization. Our stakeholders represented, and were interested in the full spectrum of project types and goals, and we evaluated the rewards and risks associated with each of them. From the identified rewards and risks, we then formed recommendations for minimizing risks and maximizing rewards.

Estuary selection

Olympia oysters are almost entirely limited to estuaries; there are no large populations along the open coast [18, 24]. Consequently, we focused on evaluating estuaries across the biogeographic range of the species from British Columbia to Baja California (Fig 1). We started with a comprehensive list of US West Coast estuaries [Appendix A in 46]. The stakeholder team then narrowed the list by removing estuaries that are unsuitable for Olympia oysters, such as those known to have extended periods of low salinity or stagnation (i.e. bar-built estuaries, small lagoons that are closed for extensive periods). Team members from Mexico and Canada also added appropriate estuaries from their regions to the US list. For the two largest estuaries—San Francisco Bay in California, and the Salish Sea in Washington / British Columbia—regional team members delineated sub-basins that could be assessed separately (S1 Fig).

Fig 1

Location of estuaries and their ecological priority index scores.

Names of the numbered estuaries are provided in Fig 2.

Fig 2

Conservation aquaculture indices.

Estuaries are arranged from North to South, with the exception of subbasin areas, which are grouped for simplicity. Province or state abbreviations are shown (BCC = British Columbia, Canada; WA = Washington, OR = Oregon, CA = California, USA; BCM = Baja California, Mexico). The names of the ten estuaries that emerged as ecological priorities are shown in bold font; all index scores ≥0.5 are highlighted. The individual scores for each criterion are shown to the right (darker shading represents higher scores; missing data shown in white).

Conservation aquaculture indices

We developed 14 criteria to assess the potential value and feasibility of new or enhanced investment in aquaculture to support conservation efforts for the native oyster across its range (Table 1). We focused our assessment on differential benefits, asking where the use of aquaculture may provide a relatively larger conservation benefit or have a greater likelihood of success. It became clear from stakeholder discussions that more information was available on spatial differences in benefits than on risks—risks such as habitat damage from gear or loss of genetic diversity could occur anywhere, and we lacked clear evidence of such risks being greater in some places than others. Both ecological and social criteria were included. These criteria were generated and refined from a longer initial list (21 were originally identified) through an iterative process with the stakeholder team; we dropped those for which there was insufficient information or that upon further consideration did not seem critical to the evaluation. The criteria were phrased as questions to clearly articulate what each criterion is addressing. We also jointly crafted a statement of rationale for inclusion of the criteria. Scoring guidelines were developed for each criterion (S2 Table).

Table 1

Criteria used in evaluating estuaries for conservation aquaculture.

Each criterion is framed as a question, and the rationale for inclusion is provided. In the final four columns, the weighting of each criterion used to calculate the four indices is shown; if blank, this criterion was not included in the index.

	Criterion question	Rationale for inclusion in index	Ecological Priority	Community Restoration	Community Harvest	Commercial Production
1	Is recruitment limited?	Aquaculture has potential to make biggest positive difference in estuaries with low recruitment.	4
2	Is the Olympia oyster population at risk of local extinction?	Aquaculture has the potential to make the biggest positive difference in estuaries with very low adult populations that are at risk of disappearing.	3
3	Is post-settlement mortality low?	Places with high post-recruitment survival should be prioritized, so return on aquaculture investment is maximized; avoid sites with high mortality due to high drill predation, freshwater events, etc.	2	2	2	1
4	How isolated is this Olympia oyster population?	Estuaries that are geographically and/or genetically isolated and do not have larval exchange from nearby populations are more vulnerable to a potential loss of an entire population, and may benefit more from aquaculture as a tool.	2
5	Is there a nearby hatchery that has produced Olympia oyster spat from local broodstock using conservation protocols?	A hatchery that is in the same estuary will reduce risks associated with shipping spat from greater distances including introducing pathogens, parasites, or non-native fouling species. Conservation protocols are aimed at retaining local genetic adaptations and diversity.		1	1	2
6	Is it safe to eat shellfish?	Only areas where water quality allows for safe consumption of shellfish can be used for commercial production or community harvesting.			3	3
7	Do regulations allow harvest of Olympia oysters?	Areas where harvest is allowed should be prioritized for community groups interested in harvest.			2
8	Is post-settlement growth of Olympia oysters high?	High growth rates reduce the length of time between outplant and harvest, relevant to community harvest groups and commercial growers.			1	1
9	Are Olympia oysters or any other species of bivalves currently being farmed in this estuary?	New or expanded Olympia oyster aquaculture by community groups or commercial growers is facilitated if there is existing infrastructure for farming bivalves, and a track record of safe water quality, harvest, etc.			1	1
10	Is local Olympia oyster restoration/enhancement part of the management or conservation plan of any organizations?	Aquaculture investment and permitting is facilitated where native oyster restoration is identified as a priority by multiple organizations.		2
11	Are there community or volunteer groups currently engaged in Olympia oyster restoration?	Aquaculture-based restoration is more likely to succeed and positively affect people where there are engaged communities.		2
12	Are other community groups currently engaged in restoration of other species of bivalve/shellfish?	Existing groups engaged in restoration with similar species could indicate a capacity for or interest in incorporating Olympia oyster restoration in the future.		1
13	Are there Native American Tribes or First Nations currently engaged in bivalve/shellfish restoration or wild harvest?	Indigenous stewardship increases the chances of successful long-term restoration and management of oyster populations, and increases the priority of doing so, to sustain a legacy of cultural practices.		1	1
14	Are other community groups (non-commercial) growing shellfish (oysters or other species) for harvest?	Existing groups that grow and harvest shellfish can increase the success of restoration efforts via the stewardship, maintenance and management of oyster beds.			1	1

Each estuary was assigned a score (2 = high, 1 = medium, 0 = low) for each of the 14 criteria, with higher scores indicating higher priority for aquaculture. We assigned a score of zero to fields with missing data (leading to conservative results—in the future if data are available, these scores may increase). Each estuary was scored first by the expert or experts most familiar with it, using quantitative data (e.g. on recruitment, survival, or growth from their own monitoring or publications) where available, their own expertise, and the assistance of additional local experts where appropriate. Next, multiple stakeholders worked in regional teams to review and discuss scores, provide additional relevant information and resources, and reach consensus on scores. Some estuaries are very well-studied with robust data on factors such as recruitment rates or growth rates, while others are poorly characterized. To reflect such differences, each score was annotated with a certainty level: not very certain (*), fairly certain (**), or very certain (***). To document the decision-making process in scoring, the basis for each score was briefly explained, and any relevant citations or internet resources listed; names of stakeholders that conducted the scoring for each estuary were also documented (S3 Table). It should be noted that the evaluation process described above resulted from a larger collective effort than is reflected in the author list alone (S1 Table).

To identify the places where new or enhanced investment in aquaculture could most benefit Olympia oyster populations, we developed an ecological priority index using only the first four ecological criteria. Our team considered the relative importance of each and decided on a weighting scheme that gave recruitment limitation the highest weight, followed by risk of extinction, and finally isolation and post-settlement mortality (Table 1). Index scores were calculated by summing the weighted scores and then dividing by the maximum possible score, so that index scores ranged between 0 (lowest) and 1 (highest). Any estuary with an index of ≥0.50 was considered an ecological priority, as this threshold is transparent and indicates that a majority of criteria were met. Estuaries that had no information for the first three criteria (recruitment, extinction risk, mortality) were initially evaluated (S3 Table) but omitted from subsequent analyses because these three criteria are fundamental to any consideration of conservation aquaculture. Our prioritization thus is conservative; in the future, if more data are available, more estuaries may emerge as priority sites for conservation aquaculture.

We then developed three additional indices: a community restoration index, a community harvest index, and a commercial production index. At any estuary, a conservation organization or resource management agency could potentially implement small-scale conservation aquaculture if a need to do so is identified, working with a local hatchery to outplant juveniles solely to enhance natural populations. However, we were interested in also addressing the suitability of each estuary for three other types of conservation aquaculture projects: 1) community restoration (restoration involving hatchery-raised oysters that is primarily driven by local community interests or engagement), 2) community harvest (deployment of hatchery-raised oysters specifically in order to be harvested and consumed by the local community), and 3) commercial production (aquaculture of oysters raised by growers and sold for profit). The indices for all three of these project types included one ecological criterion, post-settlement mortality, because engaging in novel aquaculture endeavors is likely to fail in places with high mortality. Each of the three indices used a different suite of other criteria, weighted differentially (Table 1), as determined by discussion among the stakeholder team. The indices were calculated summing weighted scores and then divided by the maximum possible value (to obtain scores from 0–1) with two exceptions. For community harvest, an estuary automatically received an index score of zero if it had received a zero for safety of shellfish consumption or legality of Olympia oyster harvest, since either of these preclude community harvest. For commercial production, an estuary automatically received an index score of zero if it had received a zero for safety of shellfish consumption. Again, estuaries were deemed a high priority for consideration of a particular project type if the index score was ≥0.50.

Results

Initially, the stakeholder team identified 32 different potential rewards and 29 potential risks associated with conservation aquaculture of Olympia oysters. These were aggregated and refined to 12 rewards and 11 risks that had direct relevance solely to conservation aquaculture projects (e.g. not general rewards that would also be associated with oyster restoration, such as water filtration). Social, cultural, and economic benefits from conservation aquaculture were the most represented benefits (67%), compared to the ecological returns (33%). The risks were generally more varied: ecological risks were represented most strongly (55%), followed by economic (27%), and then social and cultural (18%). Each benefit or risk was assigned to one of the categories we identified based on the primary beneficiary: Olympia oyster populations, the coastal ecosystem, conservation practitioners, Tribes / First Nations, local community members, and commercial growers.

For Olympia oyster populations, the primary benefit of utilizing conservation aquaculture was the potential to dramatically increase local population numbers fairly rapidly, particularly in recruitment-limited estuaries (Table 2). The primary risks to populations involved genetic concerns associated with using hatchery-reared oysters, including reduced genetic diversity and loss of local adaptations, and the potential for the density-dependent emergence and spread of diseases within native oyster populations (Table 3).

Table 2

Potential rewards of conservation aquaculture of Olympia oysters, organized by primary recipient group.

Only those rewards uniquely associated with conservation aquaculture, not with oyster restoration through any means (e.g. water filtration), are presented.

Reward to (primary recipient)	Benefit of Olympia Oyster Conservation Aquaculture
Olympia Oysters	Scaled or rapidly increased population numbers where there is low recruitment or recruitment failure for populations that are severely declined, at risk of local extinction, and/or isolated from other populations
	Increased genetic diversity in small populations, where genetic bottleneck/allee effects are likely to occur
Coastal Ecosystems	Increased structure and habitat for other fish and marine invertebrates from aquaculture gear
	Reduced introduction of non-native fouling species if fewer non-native oysters are commercially grown, if native oysters become commercially viable
Conservation Practitioners	Ability to manipulate reproduction, test tolerances to environmental conditions (e.g. to search for phenotypes more resilient to climate change effects)
	Leveraging private industry for conservation gain through partnerships with commercial growers
Tribes / First Nations or Local Community Members	Increased community engagement with, knowledge of, and/or stewardship of coastal ecosystem through consumption/harvest of a local food source made possible at a larger scale through aquaculture
	Additional revenue streams (e.g. ancillary downstream businesses) for waterfront and community
	Increased traditional food source benefit
	Maintained social/cultural continuity of traditional food gathering
Commercial Growers	Potential to improve perceptions of aquaculture and/or increase interest in native aquaculture species
	Diversification of, increased income, and increased resilience (climate or other) for grower portfolio

Table 3

Potential risks of conservation aquaculture of Olympia oysters, organized by primary recipient group.

Risk to (primary recipient)	Risk of Olympia Oyster Conservation Aquaculture
Olympia Oysters	Reduced genetic diversity of hatchery-raised animals vs. wild population
	Reduced local adaptation and/or plasticity
	Increased disease emergence and/or spread; increase of parasites with increasing population densities
	Increased risk of poaching if hatchery production raises profile of native oysters and increases awareness of wild or restored oyster locations
Coastal Ecosystems	Increased disease or pests spread from Olympia oysters to nearby native species or habitat
	Negative alterations of the natural habitat from aquaculture gear, including increased plastics in the marine environment
Conservation Practitioners	Difficulty in creating BMPs at appropriate scales and/or risk of growers producing or selling Olympia oysters without adhering to BMPs and protocols
	Greater competition between industry and conservation groups for funding and/or resources
Tribes / First Nations or Local Community Members	Disempowerment by not taking into account local community priorities or restricted tribal areas
Commercial Growers	Riskier and less profitable species to raise than non-native species due to slow growth/longer time to harvest
	Increased abundance of Olympia oysters from aquaculture could lead to increased larval production and settlement on other cultivated species, with negative results for both other species and Olympias in being removed from water

While stakeholders originally identified many benefits for the coastal ecosystem derived from Olympia oyster populations, only two were specific to projects employing aquaculture, providing additive value beyond traditional (non-aquaculture) Olympia oyster restoration. These potential benefits were the reduced introduction of non-native fouling species associated with the culture of native oysters versus introduced oysters, and the benefits of additional (artificial) habitat provided by aquaculture gear, particularly in areas such as unstructured mudflats (Table 2). Potential risks included negative ecological consequences associated with the transfer of oysters from within hatcheries into wild populations and potential negative alterations of the coastal habitat as a result of the use of commercial farming via aquaculture gear (Table 3).

For conservation practitioners, conservation aquaculture techniques may support the management of oyster populations for future climate conditions, since they enable the search for phenotypes that are more resilient to environmental stressors. Conservation practitioners may also benefit from engaging new partners and leveraging the private industry (that are using their own resources for commercial oyster production) for conservation gain (Table 2). Two risks involved the creation and adherence to conservation-centered better management practices (BMPs): the difficulty in creating (BMPs) at appropriate scales for commercial hatcheries, and the potential for some in the commercial oyster industry to produce Olympia oysters without adhering to protocols that further the goals associated with conservation aquaculture. An additional risk was the potential for greater competition between industry and conservation groups for funding and/or resources (Table 3).

For Tribes, First Nations, and community groups, a primary benefit of conservation aquaculture projects was the harvest and consumption of a native, locally sourced food in estuaries where wild Olympia oyster populations cannot sustain a harvest. For communities of Indigenous Tribes and First Nations in particular, benefits also included increased access to a traditional food source and the maintenance of social/cultural traditional food practices (Table 2). However, we also identified the potential for lack of early consultation with Tribes and/or First Nations as a primary risk which could lead to disempowerment if the management and stewardship priorities of these communities are not taken into account prior to the start of a project (Table 3).

Finally, for commercial oyster growers, adding Olympia oysters to complement existing farmed species can provide diversification of the grower’s portfolio, which may be key to continued commercial viability. Additionally, conservation aquaculture of native Olympia oysters can provide benefits related to improving public perceptions of aquaculture and potentially result in increased interest in cultured seafood (Table 2). Risks included Olympia oysters being a generally less profitable and often riskier species to raise due to their slow growth, and the potential of Olympias bio-fouling or settling on other cultivated species (Table 3).

Priority estuaries and project types

We identified 66 estuaries as suitable for Olympia oyster populations throughout the species’ range along the west coast of North America (with sub-basins of the Salish Sea and San Francisco Bay treated as estuaries). Each of these estuaries was scored for all 14 conservation aquaculture criteria, with scoring rationale and references clearly documented (S3 Table). Of these, 40 estuaries had sufficient data for the first three ecological criteria, which were vital for evaluating the value of conservation aquaculture (Figs 1 and 2). The remaining 26 estuaries had insufficient information and were not considered further. Overall, more estuaries at both the northern and southern ends of the distribution were omitted due to limited available data, and the remaining estuaries that were retained in British Columbia and Baja California still had many “unknown” scores for individual criteria. Thus, our results are likely conservative given the data limitations (scores of 0 for missing data will later be increased as data become available).

Of the 40 estuaries with sufficient data, ten estuaries were identified as ecological priorities (Figs 1 and 2) for new or increased investment in conservation aquaculture of Olympia oysters. Two of these estuaries (Netarts Bay in Oregon and Elkhorn Slough in California) received the highest possible index score (1.0). Three other estuaries scored quite high (>0.7): Whidbey Basin in Washington and Morro Bay and Carpinteria Marsh in California.

The ten ecological priority estuaries varied in the appropriateness of different project types (Fig 2, S2 Fig). Half of these estuaries ranked highly for community restoration (five estuaries = >.50), and 40% ranked highly for community harvest and commercial production each (four estuaries = >.50 for each project type). Four of the ecological priority estuaries—all within the central range of the species from San Francisco Bay to Mugu Lagoon—did not rank highly for any of the three project types, and are instead currently best suited for projects led by conservation or resource management organizations.

Discussion

Our assessment of conservation aquaculture for Olympia oysters is timely and highlights the need to consider this strategic approach to mitigate the steep declines faced by other marine species globally. We have developed and implemented a transparent and analytical framework (Fig 3) designed to evaluate conservation aquaculture as a tool to support imperiled species, by linking specific rewards and risks with particular end-user groups. Throughout the planning process, we identified ways in which conservation aquaculture can address both current management challenges (e.g. recruitment failure), and advance forward-thinking strategies for future challenges (e.g. resilience of oysters to the effects of future climate change scenarios). This type of assessment is needed for other foundation species, especially where aquaculture is already being used as a tool to address declines (e.g. reef-building corals).

Fig 3

Conceptual diagram of steps to take in evaluating conservation aquaculture for a new species or region.

The diagram follows a logical chronological flow, but in practice some steps may occur simultaneously or there may be iterative rounds revisiting particular steps. For the first steps, the process should only move forward if the determination of the previous step is affirmative (e.g. only move to step 2 if the species requires restoration, to step 3 if reproduction is deemed limiting, to step 4 if aquaculture is feasible, to step 5 if there is a team, etc.).

Tradeoffs and risk mitigation of conservation aquaculture

Our collaborative process engaging diverse stakeholders identified the key rewards and risks of conservation aquaculture for Olympia oysters. Below, we discuss these by end user or beneficiary, and make recommendations to minimize these risks.

Olympia oyster populations

Any successful restoration directly benefits the focal species that is being restored. As such, restoration efforts aimed at rebuilding Olympia oyster populations can be beneficial for restoring numbers and distribution towards historical baselines, and in very threatened populations, for preventing local extinction. What makes restoration via conservation aquaculture different from other restoration approaches is the potential to dramatically increase local population numbers fairly rapidly. In recruitment-limited estuaries, this cannot be achieved simply by providing bare settlement substrates, which is the most common restoration approach for Olympia oysters [28]. Supplying thousands of hatchery-raised juveniles can boost recovering populations to a threshold where they can become self-sustaining, as has been accomplished in Sequim Bay and Fidalgo Bay in Washington [47].

The primary risks identified by our stakeholder team involved genetic concerns associated with using hatchery-reared oysters, including reduced genetic diversity and loss of local adaptations [48]. Olympia oysters have locally differentiated population structure [49, 50] and have been shown to exhibit local adaptations for the timing of reproduction [51] and tolerance to salinity fluctuations [52]. Maintaining such local adaptations when possible is important, thus we recommend the use of responsible conservation aquaculture protocols such as those developed for the Chew Center by Puget Sound Restoration Fund and Washington Department of Fish & Wildlife (e.g. [31]). These include the use of large numbers of local adult oysters for broodstock, and techniques specifically aimed at reducing hatchery selection. Considering hatchery conditions is also critical since Olympia oysters have been shown to have strong carryover effects on reproduction relative to environmental conditions [53].

For extremely small populations, especially those facing local extinction, the benefit of increasing the population size may outweigh genetic concerns such as outbreeding depression [41]. Introducing genetic diversity into these populations may also be beneficial now, and in the future as environmental conditions change due to climate change [54]. Our ecological priority index resulted in recommendations for increased use of this tool primarily in estuaries with very small populations, where potential genetic risks are likely overshadowed by genetic benefits and decreased extinction risk.

The risk of density-dependent emergence and spread of diseases within native oyster populations was also identified as a concern. Currently, diseases and pathogens do not appear to play a major role in Olympia oyster mortality [55]. However, higher densities in the hatchery or estuary can increase this risk [56]. Careful monitoring for pathogens, and avoidance of transfers among hatcheries, should be used to manage this risk.

Coastal ecosystems

Olympia oyster restoration through any means provides benefits to the ecosystem, such as increasing the diversity of benthic-water column coupling and filter feeders [57] and enhancing habitat for other fish and marine invertebrates [21]. While our stakeholder team did not identify many ecosystem-wide benefits exclusive to aquaculture-based restoration, these general benefits also result from conservation aquaculture projects. One potential reward specific to conservation aquaculture is the reduced introduction of non-native fouling species, which include parasites and pathogens associated with culture of non-native species in distant hatcheries, versus native species in local ones. However, this benefit would only accrue if Olympia oysters become commercially viable and production is widespread, resulting in concurrent decreases in aquaculture of non-native species. In addition, the artificial structure provided by aquaculture gear in areas such as unstructured mudflats can provide similar benefits for fish and invertebrates as other ‘artificial reefs’ [8, 58].

However, any aquaculture endeavor involves some level of risk of transferring non-native species, including pathogens and parasites. There are potential negative ecological consequences of conservation aquaculture associated with the transfer of oysters from within hatcheries into wild populations, although disease risks appear modest [55]. In addition, negative alterations of the coastal habitat can occur as a result of the use of commercial farming via aquaculture gear, for example by possibly contributing to microplastics in the estuaries where oysters are grown commercially [59]. Aquaculture gear also has the potential to damage particularly sensitive estuarine habitats or create space conflicts with other declining marine foundation species in need of protection, such as seagrasses [5, 60]. We recommend that native oyster culture take place within the existing footprint of commercial operations when possible to minimize negative impacts on natural estuarine habitat that can occur on small spatial scales as the result of shading and increased sedimentation. It is worth noting that at larger scales, there may be positive effects of aquaculture gear, due to increased water column nutrients for seagrasses and structural refugia for fish and invertebrates provided by gear in unstructured mudflat habitats [61-63]. We recommend that the overall positive and negative impacts—and the spatial scales of those impacts—be carefully assessed in the deployment of commercial aquaculture gear.

Conservation practitioners

Conservation aquaculture represents a relatively new and unique tool for practitioners to use for the enhancement or rebuilding of Olympia oyster populations where traditional restoration practices have not been successful or well-funded. As climate change increasingly affects coastal ecosystems, conservation practitioners may also use aquaculture techniques to search for phenotypes more resilient to climate change effects (e.g. those with higher tolerances to changed or predicted climate-driven environmental conditions), as has been done with other species like corals [64]. Despite its promise, due to the high degree of uncertainty about climate effects on Olympia oysters [65], we recommend further study before we can explicitly support assisted evolution approaches with this species.

Conservation practitioners can also benefit by engaging new partners and leveraging private industry funds and resources from commercial oyster production for conservation purposes. Considerable benefits may be realized despite the limited public funding for conservation in general and for restoration of the Olympia oyster in particular. However, there are risks to conservation practitioners engaging in these new partnerships. One is the difficulty of creating conservation-centered best management practices (BMPs) at appropriate scales that can or will be followed in commercial hatcheries. A related risk is the potential for some in the commercial oyster industry to produce and sell Olympia oysters without adhering to protocols that further the goals associated with conservation aquaculture. Finally, there is potential for greater competition between industry and conservation groups for funding and/or resources.

To address the risks associated with industry partnerships, we recommend that conservation practitioners work with hatcheries that have clear, appropriate conservation practices and protocols in place, and that they work with commercial growers to understand the particular challenges and opportunities faced by hatcheries following these conservation BMPs, to ensure that all parties continue toward shared goals. We also recommend conservation practitioners have transparent conservation-first policies in place regarding their rationales and conditions in which they partner with industries (e.g. [66]).

Tribes, first nations, and community groups

Where populations of oysters cannot sustain a wild harvest, conservation aquaculture projects can provide some specific benefits through the harvest and consumption of Olympia oysters, including connecting people with coastal ecosystems through the enjoyment of a native, locally sourced food. This is evidenced by the recent increase in interest in Olympia oysters in the Pacific Northwest and California as part of the popular “slow food” movement [67]. Rebuilding populations of Olympia oysters can also encourage an increased engagement with, knowledge about, and/or stewardship of coastal ecosystems within communities that may otherwise lack connection with native oysters as a component of West Coast estuaries. For communities in Indigenous Tribes and First Nations in particular, conservation aquaculture projects can increase access to a traditional food source and serve to maintain social/cultural continuity of traditional food practices [68, 69].

However, our group identified the potential for lack of early consultation with Tribes and/or First Nations as a primary risk which could lead to the disempowerment of these communities if the management and stewardship priorities for tribally ceded areas are not taken into account prior to the start of a project. Further risk ensues when restricted tribal properties are accessed or prioritized for conservation aquaculture by those outside of the community without the appropriate prior consultation and consent from the Tribe or First Nation. While Indigenous Tribes, First Nations, and local communities were combined into one user group in this analysis due to the overlap of rewards and risks identified, it should be noted that Indigenous Tribes and First Nations are not stakeholder groups, but sovereign Governments that do not always share the same values, nor are governed by the same regulations, as their non-Indigenous neighboring communities.

We recommend the continuation and expansion of engaging communities in conservation aquaculture projects for restoration and harvest wherever possible. It is critical that any organization partnering with Indigenous Tribes and First Nations involve those communities directly from the start of the planning of a project and respect tribal access to, applicable legal authorities over, and stewardship of traditional lands. This includes asking permissions to access and conduct projects on land where appropriate and engaging in a collaborative process to ensure that the community’s priorities for resource management, cultural heritage, and stewardship of the land are helping drive the project goals. We also recommend that conservation aquaculture projects that involve harvest include a component of public education about not harvesting or disturbing wild Olympia oyster populations that are on restoration sites or in non-harvestable areas.

Commercial growers

For commercial oyster growers, adding a species such as the Olympia oyster to complement existing farmed species can provide diversification to the grower’s portfolio. With the increasing impacts of climate change, and an often unpredictable marine environment [70, 71], diversification may be key to continued commercial viability. As with other fisheries, having a more diverse portfolio of oyster species could create additional economic opportunities or buffer against economic loss [72]. For example, a recent outbreak of oyster herpesvirus (OsHV-1) in the Crassostrea gigas population in Southern California required the destruction of a season’s worth of infected oysters, which could not be sold, representing significant financial losses for growers [73]. Olympia oysters are not as vulnerable to herpes, or many of the other diseases that plague other commercial species, including Crassostrea [55], and show relatively increased resilience to climate effects [65], thus making them ideal to add to the grower’s portfolio to buffer against such losses. Olympia oysters also provide an entirely different flavor profile than Pacific oysters, and represent a locally sourced native species, which could provide additional marketing and market differentiation opportunities [42].

Engaging in conservation aquaculture of Olympia oysters can also provide potential benefits related to public perceptions of aquaculture. In addition to farmed bivalves being one of the lowest-impact forms of marine aquaculture and ways of producing animal protein [74], there is emerging research on the positive ecosystem services that “restorative” commercial shellfish and seaweed aquaculture can provide for water quality, habitat structure, and climate resilience [8, 61, 75]. Despite this, there remain some negative associations in the US with farmed seafood and marine aquaculture. By focusing on growing a native species and for a stated benefit of increasing native species populations, commercial growers can engage the public under an explicit conservation framework and potentially see increased interest from or improved public perceptions of farmed seafood.

While diversification and perceptions are important, it must be noted that Olympia oysters are generally less profitable, due to their smaller size and longer growing period, and therefore a riskier species for farmers to grow. Also, if Olympia oysters are grown in close proximity to other species, there is the risk that larval overflow could increase “bio-fouling” when Olympia oyster larvae settle on other cultivated species [76], with negative results for both the other cultured species and the Olympias oysters that are removed from the estuaries during harvest.

We recommend engagement of conservation aquaculture by commercial oyster growers in priority areas where: the ecological benefits outweigh the risks; the grower has enough internal financial capacity to support the growing of a species that can take 1–2 years longer to mature and may be initially less profitable than other oyster species; and there is a desire to grow Olympia oysters for both commercial and non-commercial reasons. While it is currently not as profitable as other species, the commercial growers in our expert group that choose to focus on growing and providing Olympia oysters to the public were doing so not only for the market differentiation and potential future profits, but with historical and cultural education benefits, and cultural continuity in mind.

Geographic prioritization with conservation aquaculture indices

We identified ten estuaries along the entire biogeographic range of the Olympia oyster where new or increased investment in conservation aquaculture is a high priority. Application of the ecological priority index provided a transparent, robust approach to selection of these priority estuaries from 66 estuaries that were evaluated in a consistent manner. The Native Olympia Oyster Collaborative (https://olympiaoysternet.ucdavis.edu/) was formed to provide such regional perspectives and syntheses, complementing the on-the-ground restoration work which is largely place-based and locally driven, by individual members of the Collaborative. For funders working at a broad spatial scale (e.g. The Nature Conservancy, Pew Charitable Trusts or NOAA), identification of the ten priority estuaries will help direct future grants for conservation aquaculture to the places where the return on investment is highest. For regulatory agencies, a robust process conducted regionally but drawing on local knowledge will help to inform the permitting process for the highest priority estuaries. While our evaluation was conducted across the full range of the species, the tool we developed can be applied at any scale, for instance for selecting sites within an estuary. We have provided a spreadsheet version (S3 Table) with weighting and formulae so other end users can customize it for their needs. Our tabular approach complements GIS-based decision-support tools developed to prioritize oyster restoration sites [75, 77].

Ecological priority areas

The ecological priority index was designed to prioritize sites where the rewards of aquaculture are likely to greatly outweigh the potential risks. The ten estuaries that emerged as ecological priorities thus represent locations where our stakeholder team can confidently recommend consideration of increased investment in aquaculture as a tool to support native oyster conservation. We weighted recruitment limitation most highly among ecological criteria, since oyster populations where estuary-wide recruitment failure is common (no successful reproduction anywhere in the estuary in many years) stand to benefit the most from enhancement of reproduction through aquaculture. Risk of local extinction due to small or declining population size, and high isolation resulting in lack of larval transport from other populations were also critical determinants of ecological priority. The other key requirement was high post-recruitment survival, since investment in aquaculture is not merited if all outplanted juveniles die.

The two estuaries that scored highest as ecological priorities for conservation aquaculture (Netarts Bay in Oregon and Elkhorn Slough in California) are places where estuary-wide recruitment failure is common, because current populations are tiny due to past declines, and because larval retention is challenged by low residence time resulting from strong tidal currents [78]. Both are in areas where genetic analyses suggest isolation is high, with limited connectivity to other populations [50]. Restoration incorporating aquaculture has been attempted in both places [36, 79]. We recommend scaling up these efforts until populations there are self-sustaining, large enough, and located in areas of higher residence time so that successful recruitment occurs at least in some locations in the estuary in most years.

While we identified ten sites along the coast that represent high priorities for future investment, it is clear that further consideration of the feasibility and potential benefits of conservation aquaculture is required at a local or regional scale before proceeding with new projects. Our index used four critical criteria to identify these priority sites, but at a smaller spatial scale, much more information can be used to inform decision-making. Such additional information might lead to local adjustment of prioritization. For instance, Hood Canal in Washington did not emerge as a priority in our index, but conservation aquaculture projects are being considered in the lower portion of the Canal because this location appears to be recruitment limited, other restoration methods may not prove effective in this area, and because there is strong local support for boosting populations. Conversely, Richardson Bay in California did emerge as a priority, but local practitioners have indicated that invasive oyster drills pose a strong threat in many locations, and risks from the predatory drills must be mitigated before proceeding with aquaculture-based restoration at sites with high densities of drills.

Project types

The project type indices reveal which approaches are currently possible at each site. At every estuary, a conservation organization or resource management organization could lead a conservation aquaculture project for Olympia oysters. Such projects typically engage community members as volunteers or in outreach, but are not community-driven—the design and coordination of the project is led by paid staff from the conservation organization. An example of this is a recent aquaculture-based restoration project at Elkhorn Slough in central California, led by the Elkhorn Slough National Estuarine Research Reserve (Fig 4A).

Fig 4

Examples of different approaches to implementing conservation aquaculture with Olympia oysters.

A) Restoration with hatchery-raised juveniles led by a coastal management organization. Staff of the Elkhorn Slough National Estuarine Research Reserve, with community volunteers and partners, assemble stakes with clam shells bearing hatchery-raised juveniles. (Photo: B. Tougher). B) Community restoration. Staff members from the Swinomish Indian Tribal Community work with AmeriCorps volunteers from the Nooksack Salmon Enhancement Association to enhance habitat for Olympia oysters on Swinomish tidelands. (Photo: J. Barber); C) Commercial production and sale of Olympia oysters (Photo: M. Wilkinson, Hog Island Oyster Company). All individuals shown in images provided prior consent.

The capacity to implement other types of projects is site dependent, and currently more limited across estuaries. Restoration led by the community rather than by conservation organizations or resource management agencies appears a viable approach in many places, and currently ranks high as a potential project type at half of the ten priority estuaries (Fig 2). Community restoration depends on leadership by local individuals or groups with strong interests in growing oysters for restoration purposes. For example, in South Puget Sound, tideland owners are passionate about supporting Olympia oysters, and purchase spat to grow juveniles on their tidelands as “shellfish gardens”. In North Puget Sound, the Swinomish Indian Tribal Community is engaged in restoration of oyster habitat as a cultural legacy and to support other species such as salmon (Fig 4B).

Community harvest involves local individuals or groups growing oysters specifically for harvest and human consumption, and ranks high as a potential approach at four of the ten priority estuaries (Fig 2). When community harvest occurs in ecological priority areas and contributes to supporting non-harvested components of the population in the estuary through larval spillover, we consider the practice a part of conservation aquaculture. This type of project has promise for Olympia oysters, but is mostly still in the concept stage; we do not know of any examples of successful projects of this type to date. The slower growth rate and lower availability of hatchery-raised spat makes community harvest projects with the native oyster species more challenging than projects involving the non-native Pacific oyster. Various Tribes in the Puget Sound area and Oregon are interested in restoration of the native oyster for eventual harvest, but since populations are so depleted near Tribal communities, the first step is to rebuild healthy oyster beds, with harvest still an aspirational future goal.

Commercial aquaculture projects also show potential for supporting oyster populations, and ranked high in four of the ten priority estuaries (Fig 2). If conducted in ecological priority areas using local broodstock, a nearby hatchery, and conservation protocols, this can contribute to conservation and restoration by generating larvae which support the wild population in the area. Various small-scale growers produce Olympia oysters as a part of their portfolio and implement appropriate protocols (Fig 4C). Humboldt Bay and Morro Bay both have commercial aquaculture operations for non-native Pacific oysters; if there were a hatchery nearby producing Olympia oysters from local broodstock, these would also rank as high priorities for Olympia oyster commercial production.

Regional recommendations

Our analysis revealed strong regional differences in knowledge and capacity for implementing conservation aquaculture projects, which could be decreased through strategic funding and planning efforts. The information available on Olympia oysters varies substantially across the species’ range (i.e. variations in missing data in Fig 2). Information needed to assess the benefits or risks of restoration is particularly lacking at both the southern and northern ends of their distribution. In Baja California, additional funding could help to fill critical data gaps and allow more thorough exploration of restoration needs and potential. In British Columbia, oyster restoration is not currently a governmental management strategy; current management goals are met through implementing the Species at Risk Management Plan for the Olympia Oyster, including surveys to assess shifts in abundance and restrictions on harvest.

The engagement of Indigenous Tribes in oyster restoration and harvest only in Washington and Oregon (high scores for criterion 13 only in top/northern section of Fig 2) is another striking regional pattern. Indigenous Tribes and First Nations harvested oysters for millenia along the entire range of the Olympia oyster [22, 23, 80]. Where possible given regional policy and regulations, conservation organizations and resource management agencies could work to engage Indigenous communities that are interested in collaborative efforts to restore native oyster harvests as a traditional food source and cultural practice. However, this could prove challenging where Indigenous people no longer have access to estuaries, or where water quality is so poor as to preclude consumption of shellfish, as is the case in heavily urban and agricultural areas of central and southern California.

Finally, the distribution of hatcheries that could produce native oysters and facilitate aquaculture-assisted efforts is also centered in the Pacific Northwest. Indeed, to our knowledge no hatchery has produced Olympia oysters south of Elkhorn Slough in central California—leaving about 1500 km of the southern range of the species without current hatchery capacity. We recommend that such capacity be advanced in coming years, perhaps by university marine laboratories, particularly somewhere near the three southern California ecological priority sites (Morro Bay, Carpinteria, Mugu Lagoon).

Conclusions

The new approach and assessment tools developed to evaluate conservation aquaculture for Olympia oysters provide a template that is clearly needed to evaluate the potential use of conservation aquaculture for other declined species, and especially in evaluating the tradeoffs between rewards and risks where aquaculture is already being used as a tool to address declines (e.g. reef-building corals). Initiatives are being undertaken globally at many international conservation organizations to engage in conservation aquaculture, and our evaluation can contribute to shaping the use of conservation aquaculture as a tool worldwide. We take an ecological approach that centers on the measurable benefits that conservation aquaculture can uniquely provide to at-risk populations. We incorporate broad stakeholder involvement from the start of the process to develop an explicit risk/reward framework that facilitates decision-making for different goals such as commercial production, community restoration, and community harvest. Our work illustrates how to create and leverage existing partnerships between agencies, non-profit groups, growers, Indigenous and other communities in order to successfully implement conservation aquaculture. Thus, our Olympia oyster case study provides a model for engaging diverse stakeholders to recommend strategic use of conservation aquaculture where the rewards outweigh risks.

Boundaries among sub-basins of the two largest estuaries on this coast.

For the Washington sub-basins, the regional team delineated these areas by integrating known oceanographic features, such as sills and straits, with established sub-basin divisions outlined by Washington Department of Fish & Wildlife and expert opinion provided by local marine scientists and restoration practitioners [81, 82]. For BC, the team delineated areas based on published work by the Department of Fisheries and Oceans in combination with expert opinion. For San Francisco Bay, California, the regional team delineated sub-basins based on extensive studies of this region [83] together with expert opinion from regional scientists. Numbers are the same as used in Figs 1 and 2 in the main paper; additional estuaries that were initially considered but were excluded from the index calculations due to insufficient data are labeled with letters.

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Map of project type indices at the ten sites scoring highest on the ecological priority index.

Bar heights correspond to site specific values in Fig 2 in the main paper.

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Stakeholders who contributed to the development and scoring of the reward vs. risk tables and conservation aquaculture indices.

(PDF)

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Scoring guidance for all criteria.

(PDF)

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Detailed version of conservation aquaculture scores and indices in Excel, including scores and rationale for them for all 66 estuaries, and including formulae for calculating indices, so that users can add new sites, new data, or change weightings using this template.

(XLSX)

Click here for additional data file.

25 Jan 2021

PONE-D-20-38508

Conservation Aquaculture as a Tool for Imperiled Marine Species: Evaluation of Opportunities and Risks for Olympia Oysters

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The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: No

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: This study titled “Conservation Aquaculture as a Tool for Imperiled Marine Species: Evaluation of Opportunities and Risks for Olympia Oyster” characterized the benefits and risks of Olympia oyster aquaculture conservation by using four criteria: social, cultural, economic and conservation. Generally, the initial idea is relatively good for conservation. However, the write up of the manuscript is too long and lacks focus. The authors presented too much information without filtering for key issues to provide a clear message to readers. The whole manuscript is boring to read and difficult to follow. The methods have no scientific background to support the issues mentioned. Specific issues on the manuscript are given below and on the attached annotated PDF.

Abstract

1. Too much information is presented on background. Reducing the text on this part will make the abstract more focused.

2. The method section is not adequately given.

3. The results of the study are inadequately presented. More results should be presented.

4. The conclusion is not clear enough to readers.

Introduction

1. The introduction is generally long, repetitive and unfocused.

2. The scientific problem the study intends to solve is not shown clearly. The authors should reduce the long introduction in order to provide a clear scientific problem.

3. The objective is also not clear enough to readers.

Methods

The methods need to be improved.

1. It long and unfocused.

2. It includes unnecessary information for a publication.

3. It uses uncommon fonts and styles.

4. It is very difficult to follow and understand what the authors did.

Results

The results should be shorted by highlighting only the important results. Can the results and discussion be presented together?

Discussion

The discussion is too long. It should be shortened. Discuss briefly the important results and not everything.

Reviewer #2: GENERAL COMMENTS

The manuscripts presents findings from a study that aimed at assessing potential risks and rewards associated with a conservation aquaculture as an important tool to support recovery of declining species particularly Olympia oysters (Ostrea lurida). The study also came up with key recommendations for establishing conservation aquaculture. Generally the manuscript is fairly well written. However, there are few areas that needs specific attention before is recommended for publication in the journal as follows:

1) Authors are advised to strongly minimize personalization of the work such as we, our study etc! Although it gives a good story but this is more of impressing than communicating. In science we write to communicate facts.

2) Authors are trying to put too many or multiple things within a single sentence which is in most cases may confuse readers. “A sentence should express a single thought or proposition”. Authors should avoid long and rambling sentences.

3) It is advisable to have section where key recommendations from this study can be found.

TITLE

It is okay. However, inclusion of a scientific name of Olympia oyster at this stage could add a lot of value.

ABSTRACT

It is okay. Authors may consider inclusion of a sentence that provides some principal findings of this study.

INTRODUCTION

Lines 39 to 42: Start with giving worldwide figure and then those from United States of America. Also, provide the estimated figure for loss of coral reefs.

MATERIALS AND METHODS

1) Lines I61 to 164: In the S1 Table, to my opinion, multiple categories could have their own specific category just like the way it is for say those who fall specifically to Grower (G), Manager or Resource Agency representative (M), NGO member (N), Conservation Scientist (S), or Tribal Representative (T). Those who fall under multiple categories should be treated separately and their opinion provided. This information should also be indicated somewhere in lines 161 to 164.

2) Line 193: Please refine the sentence to make it clearer.

3) Line 194 (for Tables 2 & 3) compared with line 224 (Table 1). Tables and figures should be cited serially by starting with 1 (Start with Table 1 or Figure 1). Thus the arrangement could be Table 2 changed to Table 1; Table 3 changed to Table 1 and finally Table 1 changed to Table 3 and cited accordingly for consistency purposes.

4) Line 202 and part of line 203: This is information plus the references can be moved to somewhere in the introductory part. In this section just tell the reader the area focused by the study.

5) Lines 215 to 216: Can Authors show the criteria used to delineate the sub-basins?

6) Lines 334 to 338 (many others): It is fortunate that authors are good in English language. Otherwise, most of the sentences are very long! Imagine a sentence of 63 words!! Not recommended for scientific writings!

RESULTS

Please see some track changes in this section in the main manuscript.

DISCUSSION

1) Line 436: Unpublished data cannot be accessible by readers. As such it is not recommended in scientific publications.

2) Lines 443 to 447: Very long sentence. Readers may not enjoy reading long sentences! Again a reference to those protocols or even a website link where those institutions can found could be very useful to readers.

3) Line 460 and several other places: The use of phrases such as “…..our stakeholders” is monotonous in this manuscript. Authors can frame this work in such a way that such phrases only remain in the Materials and Methods section. Then, make sure that whatever is presented in the results and discussed in the discussion section reflects the findings from stakeholder’s views. I believe this I believe this is doable.

4) Lines 510 to 516: How can 77 words be in a single sentence!! Readers cannot follow! There is a time where readers may lose the flow contents!

5) Lines 557 to 559: Something is missing in this sentence. Please make it clear.

CONCLUSION

The conclusion is somewhat okay. An opening sentence summarising the overall objectives of the study followed by key take home messages would add a lot of value. Authors should strictly provide the main conclusion as a result of carrying this study. Please try to reduce the “hows” here i.e the way the study was undertaken.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: Yes: Amon Paul Shoko

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

Submitted filename: PONE-D-20-38508_reviewer_annotated PDF.pdf

Click here for additional data file.

Submitted filename: PONE-D-20-38508_reviewer_27_12_2020.pdf

Click here for additional data file.

Submitted filename: comments to Authors.docx

Click here for additional data file.

23 Mar 2021

Review Comments to the Author

Reviewer #1 (Anonymous): This study titled “Conservation Aquaculture as a Tool for Imperiled Marine Species: Evaluation of Opportunities and Risks for Olympia Oyster” characterized the benefits and risks of Olympia oyster aquaculture conservation by using four criteria: social, cultural, economic and conservation. Generally, the initial idea is relatively good for conservation. However, the write up of the manuscript is too long and lacks focus. The authors presented too much information without filtering for key issues to provide a clear message to readers. The whole manuscript is boring to read and difficult to follow. The methods have no scientific background to support the issues mentioned. Specific issues on the manuscript are given below and on the attached annotated PDF.

We are pleased that the reviewer sees the conservation value that this manuscript provides. We appreciated and incorporated a great many of the reviewer’s suggestions to cut back on the overall length of the manuscript, particularly in the introduction, and to sharpen the focus of the text in some sections, which we address with the specific comments below. We also provided additional subheadings in the Discussion to increase structure and ease of reading.

Abstract

We thank the reviewer for these guiding comments about the Abstract and have completely rewritten this section. In each section, we indicate general changes made.

1. Too much information is presented on background. Reducing the text on this part will make the abstract more focused.

We have reduced the background information.

2. The method section is not adequately given.

We believe that the abstract now better highlights both the engaging of a collaborative team and the quantitative methods we used to evaluate locations and projects.

3. The results of the study are inadequately presented. More results should be presented.

We re-wrote the abstract to include results specific to Olympia oysters, including key risks and rewards of using aquaculture as a tool for this species, top ecological priority areas for expansion and their shared trends (i.e. recruitment limitation and isolation), and the applicability of different project types across estuaries.

4. The conclusion is not clear enough to readers

We edited the last 2 sentences of the abstract to clarify the conclusion.

Introduction

1. The introduction is generally long, repetitive and unfocused.

We thank the reviewer for the specific suggestions provided in the annotated pdf. Using these as a guide, we have refocused the introduction, cutting out repetitive text, rearranging information and greatly reducing the overall length.

2. The scientific problem the study intends to solve is not shown clearly. The authors should reduce the long introduction in order to provide a clear scientific problem.

We have shortened and refocused the introduction to address this comment, and thank the reviewer for their specific in-line edits, which guided our revision of this section. Our scientific problem is stated as such: “To our knowledge, there has been no thorough evaluation of the rewards versus risks of conservation aquaculture to guide strategic planning for any species on this coast, let alone for Olympia oysters. Before funders, planners, regulators, conservation organizations, or growers move forward with aquaculture initiatives, there is a pressing need to conduct a robust, collaborative evaluation of whether and under what conditions the rewards outweigh the risks. Additionally, detailed spatial analyses are needed to identify the specific locations where conservation aquaculture efforts can be expected to have a high likelihood for success.”

3. The objective is also not clear enough to readers.

We specify our goal/objective in the introduction:

“Our goal was to conduct strategic planning and develop decision-support tools to identify the use of aquaculture to support recovery of Olympia oysters across the range of the species.”

Methods

The methods need to be improved.

1. It long and unfocused.

We incorporated some of the reviewer’s specific edits provided in the annotated pdf to ensure more concise, focused writing in this section.

2. It includes unnecessary information for a publication.

Unfortunately, we cannot tell from this comment which information the reviewer feels is unnecessary for a publication. Again, where the reviewer made specific edits that shortened and focused the text in this section, we incorporated them.

3. It uses uncommon fonts and styles.

Thank you for catching these font inconsistencies. We have corrected them in the revised text.

4. It is very difficult to follow and understand what the authors did.

We incorporated any edits the reviewer provided that shortened and/or focused the text in this section in order to make the methods easier for the reader to follow.

Results

The results should be shorted by highlighting only the important results. Can the results and discussion be presented together?

The idea of combining the results and discussion is one that was raised among our co-authors as well. We also believe that these types of results are best presented in a mixed results and discussion format, but this violates the journal format, unfortunately. To address this, we kept the results as brief as possible and the discussion is lengthier than it would otherwise be.

Discussion

The discussion is too long. It should be shortened. Discuss briefly the important results and not everything.

Please see the previous comment about the length of the discussion. We provided additional subheadings to the discussion to further focus it, and accepted any specific edits provided in the annotated .pdf that shortened and/or focused the text in this section.

Reviewer #2, Dr. Amon Paul Shoko

GENERAL COMMENTS The manuscripts presents findings from a study that aimed at assessing potential risks and rewards associated with a conservation aquaculture as an important tool to support recovery of declining species particularly Olympia oysters (Ostrea lurida). The study also came up with key recommendations for establishing conservation aquaculture. Generally the manuscript is fairly well written.

We thank Dr. Shoko for his detailed review. The revisions that he has suggested have certainly improved the clarity of our writing. We believe that these revisions make the paper easier to read, and thus our messages easier to understand. We detail the ways in which we’ve incorporated his suggestions below.

However, there are few areas that needs specific attention before is recommended for publication in the journal as follows:

1) Authors are advised to strongly minimize personalization of the work such as we, our study etc! Although it gives a good story but this is more of impressing than communicating. In science we write to communicate facts.

Some of the terms that connote personalization (“stakeholders” “we”, etc.) have been changed to address this style comment, especially in places in the text where the reviewer suggests this (in the annotated pdf provided). However, we continue to use the active voice, particularly in the Methods section, to accurately describe our process.

2) Authors are trying to put too many or multiple things within a single sentence which is in most cases may confuse readers. “A sentence should express a single thought or proposition”. Authors should avoid long and rambling sentences.

We thank you for highlighting sentences that were too long, and for pointing out that audiences for whom English is a second language might be especially confused by this type of writing. We appreciate the opportunity to make our writing clearer and more accessible to all audiences, and have taken the reviewer’s suggestions to break up long sentences in every instance.

3) It is advisable to have section where key recommendations from this study can be found.

We provide key recommendations for conservation aquaculture with Olympia oysters specifically by beneficiary/user group, and then by location/region in the Discussion. We have added a number of subheadings to clarify the location of recommendations in the Discussion (e.g. “Regional Recommendations”). With Figure 3, we provide an explicit process which we recommend to create similar strategic planning for the use of aquaculture to support other imperiled species.

TITLE

It is okay. However, inclusion of a scientific name of Olympia oyster at this stage could add a lot of value.

We have added the scientific name to the title

ABSTRACT

It is okay. Authors may consider inclusion of a sentence that provides some principal findings of this study.

We thank the reviewer for this comment and have completely rewritten this section to include some principle findings specific to Olympia oysters, including key risks and rewards of aquaculture as a tool for this species, top ecological priority areas for expansion and their shared trends (i.e. recruitment limitation and isolation), and the applicability of different project types across estuaries.

INTRODUCTION

Lines 39 to 42: Start with giving worldwide figure and then those from United States of America. Also, provide the estimated figure for loss of coral reefs.

While we appreciate this suggestion, the figure of oyster loss from the U.S. is the most relevant to the species we are evaluating, and changing the order of these statistics will obscure that. The citation provided will give global context for oyster loss, and the comparison to coral reef losses in more detail for interested readers.

MATERIALS AND METHODS

1) Lines I61 to 164: In the S1 Table, to my opinion, multiple categories could have their own specific category just like the way it is for say those who fall specifically to Grower (G), Manager or Resource Agency representative (M), NGO member (N), Conservation Scientist (S), or Tribal Representative (T). Those who fall under multiple categories should be treated separately and their opinion provided. This information should also be indicated somewhere in lines 161 to 164.

We thank the reviewer for his suggestion. However, we feel that having an additional “many categories” category would obscure the point of this table, which is to make stakeholder identity clear. We generated these categories to differentiate stakeholders from one another (e.g. we use “conservation scientists” to describe academic PIs, but this term could also be used to describe researchers employed by NGOs), and asked each person to self-identify the role they would be assuming while working on this project. To clarify this point, we have added the following line to the legend for S1 Table: “While some fall into multiple categories, we asked each stakeholder to identify the primary role that they assumed to contribute to this project.”

2) Line 193: Please refine the sentence to make it clearer.

We edited this sentence for clarity.

3) Line 194 (for Tables 2 & 3) compared with line 224 (Table 1). Tables and figures should be cited serially by starting with 1 (Start with Table 1 or Figure 1). Thus the arrangement could be Table 2 changed to Table 1; Table 3 changed to Table 1 and finally Table 1 changed to Table 3 and cited accordingly for consistency purposes.

Thank you for pointing out this inconsistency in the text. We have removed the reference to Tables 2 and 3 in the Methods section so that the tables are cited serially in the order that they are numbered.

4) Line 202 and part of line 203: This is information plus the references can be moved to somewhere in the introductory part. In this section just tell the reader the area focused by the study.

We agree that normally a methods section doesn’t include citations or background. However, this sentence is meant to context the methods immediately following, as it speaks to why we focused on estuaries vs. the open coast. We also suspect that such a minor detail would be lost in an already long introduction. For these reasons, we feel this is well placed.

5) Lines 215 to 216: Can Authors show the criteria used to delineate the sub-basins?

We agree that we need to elaborate on these criteria. They are now outlined in the legend for S1 Fig, and three relevant citations have been added to the references:

“ Boundaries among sub-basins of the two largest estuaries on this coast. For the Washington sub-basins, the regional team delineated these areas by integrating known oceanographic features, such as sills and straits, with established sub-basin divisions outlined by Washington Department of Fish & Wildlife and expert opinion provided by local marine scientists and restoration practitioners [81, 82]. For BC, the team delineated areas based on published work by the Department of Fisheries and Oceans in combination with expert opinion. For San Francisco Bay, California, the regional team delineated sub-basins based on extensive studies of this region [83] together with expert opinion from regional scientists. Numbers are the same as used in Figs. 1-2 in the main paper; additional estuaries that were initially considered but were excluded from the index calculations due to insufficient data are labeled with letters.”

6) Lines 334 to 338 (many others): It is fortunate that authors are good in English language. Otherwise, most of the sentences are very long! Imagine a sentence of 63 words!! Not recommended for scientific writings!

We thank the reviewer for bringing this long sentence to our attention. It has been broken up into 2 sentences, both edited for clarity.

RESULTS

Please see some track changes in this section in the main manuscript.

We thank the reviewer for his comments in the Results section.

DISCUSSION

1) Line 436: Unpublished data cannot be accessible by readers. As such it is not recommended in scientific publications.

We have removed the reference to unpublished data.

2) Lines 443 to 447: Very long sentence. Readers may not enjoy reading long sentences! Again a reference to those protocols or even a website link where those institutions can found could be very useful to readers.

We thank the reviewer for pointing this long sentence out. We have broken the sentence into 2, eliminated the long hatchery name and used an existing citation to reference the hatchery protocols.

3) Line 460 and several other places: The use of phrases such as “…..our stakeholders” is monotonous in this manuscript. Authors can frame this work in such a way that such phrases only remain in the Materials and Methods section. Then, make sure that whatever is presented in the results and discussed in the discussion section reflects the findings from stakeholder’s views. I believe this I believe this is doable.

Some of the terms that connote personalization (“stakeholders” “we”, etc.) have been changed to address this style comment, especially in places in the text where the reviewer suggested this (in the annotated pdf provided). We especially took note of places in which these phrases were monotonous or overused and adjusted the text. Please see our general comment above about why we did not eliminate all of this language.

4) Lines 510 to 516: How can 77 words be in a single sentence!! Readers cannot follow! There is a time where readers may lose the flow contents!

We thank the reviewer for pointing this long sentence out. We have broken the sentence into 3 separate sentences for clarity.

5) Lines 557 to 559: Something is missing in this sentence. Please make it clear.

We have edited this line to read:

“We also recommend that conservation aquaculture projects that involve harvest include a component of public education about not harvesting or disturbing wild Olympia oyster populations that are on restoration sites or in non-harvestable areas.”

CONCLUSION

The conclusion is somewhat okay. An opening sentence summarising the overall objectives of the study followed by key take home messages would add a lot of value. Authors should strictly provide the main conclusion as a result of carrying this study. Please try to reduce the “hows” here i.e the way the study was undertaken.

The opening sentence concluding the importance of the work is:

“The new approach and assessment tools developed to evaluate conservation aquaculture for Olympia oysters provide a template that is clearly needed to evaluate the potential use of conservation aquaculture for other species that have undergone declines, and especially in evaluating the tradeoffs between rewards and risks where aquaculture is already being used as a tool to address declines (e.g. reef-building corals).”

We feel additional take-home messages in this section would lengthen an already very long discussion. Any reference to how the study was undertaken (using a collaborative process with diverse stakeholders) is a conclusion/main take away message, because the process we used to evaluate this tool is a product of the study as much as the index framework we created.

Submitted filename: Ridlon_20_Response to Reviewers_PLOS.pdf

Click here for additional data file.

24 May 2021

Conservation Aquaculture as a Tool for Imperiled Marine Species: Evaluation of Opportunities and Risks for Olympia Oysters, Ostrea lurida

PONE-D-20-38508R1

Dear Dr. Ridlon,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact

Kind regards,

Ismael Aaron Kimirei, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Please respond to the minor comments made by reviewer #2

Reviewers' comments:

Reviewer's Responses to Questions

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: N/A

Reviewer #2: No

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: (No Response)

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The said subtitles on the discussion section in the response were present in the original file. Very little improvement has been made on reducing the length of the manuscript.

Reviewer #2: 3. Has the statistical analysis been performed appropriately and rigorously?

Actually this is the area that needs some clarification. Is there any statistical analysis undertaken in this work or was it not necessary? How can the results be justifiable scientifically? Is there any good explanation to this observation!

The authors have tried to address most of the comments. However, clarification is needed on statistical analysis as indicated in question 3 above. Do the authors mean that the nature of data did not allow for any kind of statistical analysis!?

**********

7. PLOS authors have the option to publish the peer review history of their article (

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Reviewer #1: No

Reviewer #2: No

10 Jun 2021

PONE-D-20-38508R1

Conservation Aquaculture as a Tool for Imperiled Marine Species: Evaluation of Opportunities and Risks for Olympia Oysters, Ostrea lurida

Dear Dr. Ridlon:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Ismael Aaron Kimirei

Academic Editor

PLOS ONE