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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., Competing Interests: While the following authors were affiliated with commercial companies - Gary Fleener, Hog Island Oyster Company; Gifford Pinchot IV, Chelsea Farms; and John Adams, Sound Fresh Clams and Oysters – they did not receive any salary support to contribute to the manuscript. This commercial affiliation does not alter their adherence to PLOS ONE policies on sharing data and materials.

The emerging field of conservation aquaculture focuses on the potential for incorporating aquaculture techniques into restoration. Extensive loss of oyster reefs worldwide has led to restoration initiatives that sometimes incorporate aquaculture, but few scientific studies of this approach have been published. We developed a scientific framework to determine whether aquaculture is an appropriate conservation tool, and applied it to Olympia oysters (Ostrea lurida) in Elkhorn Slough, an estuary in central California, USA. Over 12 years of monitoring, we documented precipitous declines in density, highlighting the need for restoration. We tracked settled oysters and found that growth and survivorship is high, showing that hatchery-raised juveniles have the potential to survive to reproductive age. No natural recruitment has occurred in the estuary in seven years, suggesting that this population is recruitment limited. Thus, we determined a need for conservation aquaculture. We produced juvenile oysters from local broodstock in a hatchery and settled them on native clam shells, which we attached to stakes to form small clusters that mimic natural biogenic habitat created by this species. We deployed these near the upper limit of the intertidal range of oysters, where oyster cover dominates over non-native fouling species. The outplanted oysters grew to adult, reproductive size within months of outplanting, and survivorship was generally high, providing the first new generation of oysters in this estuary in seven years. The science-based approach we implemented and our incorporation of traditional restoration principles of natural habitat structure and dominance by native species can serve as a model for conservation aquaculture for oysters and other species. [ABSTRACT FROM AUTHOR]