Assessing condition

Ultimately, reef size is a function of the number of living oysters…

The decline of oyster fisheries follows a common sequence of events… extensive harvest of wild oyster populations results in the loss of reef structure. … There are few if any bays where only one stressor has affected oyster reefs.

Wild fisheries and remaining reefs

Most of the world’s remaining wild capture of native oysters comes from just five eco-regions on the East and Gulf coasts of North America, which together account for more than 75% of the global catch .

Only 10 eco-regions in the world reported wild oyster capture rates of more than 1000 metric tons per year from 1995 to 2004;

Only 6 eco-regions have average captures above 5500 metric tons, 5 of these are in eastern North America (Virginian to Southern Gulf of Mexico ecoregions).

• Although there is catch remaining in these six eco-regions,  in some cases the loss has been more than 99%.

Regional data gaps

We could not identify the condition of oyster reefs for several ecoregions, including parts of South Africa, China, Japan, and the Korea. There is no indication that the patterns of loss in data-poor areas are different from those in data-rich regions, or that filling the gaps in data would significantly change the global estimates of decline. However, there is not enough information for firm estimates of condition in these ecoregions.

The temperate areas of Asia pose special challenges for characterizing the status of oyster reefs…. These regions, with about 20 recorded species (Guo et al. 1999), are at the epicenter of oyster diversity. Ancient reefs were widespread in these areas several thousand years ago. There have been significant losses of natural reefs, even in the past few decades, primarily from overfishing and habitat destruction.

Overfishing was a major issue from the 1960s to 1980s as oysters were collected for food and lime. Direct habitat loss was also a significant problem as nearby cities expanded and reefs were demolished to provide access for commercial ships. Pollution from the chemical industries in the area caused further deterioration (Deng and Jin 2000), as did higher salinity as a result of reduced discharge from the Yellow and Liaohe rivers (Lin et al. 2001). Recently, the aquaculture of Crassostrea gigas has also caused major changes on the remaining Dajiawa oyster reefs.

The cultivation of oysters has been practiced for at least 2000 years in temperate Asia and has increased dramatically in recent decades (Guo et al. 1999).

Oyster reefs and ecosystem services

Native oyster reefs provide many ecosystem services including

• water filtration,
• food and habitat for many animals (e.g., fish, crabs, birds),
• shoreline stabilization and coastal defense,
• fisheries (reviewed in Grabowski and Peterson 2007, NRC 2010).

Shelfish remove suspended solids from surrounding waters, thereby

• increasing water clarity (reviewed in Newell 2004)
• enable seagrass growth
• reduce the likelihood of harmful algal blooms, which have important impacts ecologically and economically (Cerrato et al. 2004, Newell and Koch 2004).

Shellfish can also

• help to remove excess nutrients from coastal bays
• facilitat[e] de-nitrification in surrounding sediments,  which has tremendous economic value in areas where nutrient removal is a high priority for coastal policymakers (Newell et al. 2005).

Shellfish also serve as natural coastal buffers,

• absorbing wave energy directed at shorelines
• reducing erosion caused by
  • boat wakes,
  • sea-level rise,
  • storms (Meyer 1997, Piazza et al. 2005).

In addition, shellfish reefs play an important role as habitat for other species; fishes produced on oyster reefs have significant value to coastal economies (Grabowski and Peterson 2007).

Services from oyster reefs and oyster aquaculture have been examined extensively recently (Coen et al. 2007, NRC 2010). These services are well quantified compared with many other marine ecosystems and thus provide a real basis for estimating value lost to degradation and recovered through restoration.

New decision-support models are being developed to help design restoration efforts that maximize ecosystem service benefits (North et al. 2010).

A further step is to develop markets for these services; for example,

• credits for water filtration and de-nitrification from restored reefs could be bought and sold.

• Some nascent markets are being developed, but their expansion will require better quantification of ecosystem services (NRC 2010).

• In addition to ecosystem service markets, better valuations overall would allow managers and others to assess the true costs associated with the deterioration of natural oyster ecosystem services (NRC 2010).

• Such costs might then be recovered from those who degrade reefs intentionally.

Toward improving condition

Despite the continued decline of oyster reefs, their condition may be improved through conservation, restoration, and management of fisheries and nonnative species. Our analy- ses of reef condition help identify opportunities for improv- ing reef abundance and condition. Many of the countries in which oyster reefs were most abundant have comparatively strong marine management regimes (Mora  et  al. 2009); this suggests a real, albeit unrealized, opportunity for reef recovery and conservation.

New thinking and approaches are needed to ensure that oyster reefs are managed not only for fisheries production but also as fundamental ecological components of bays and coasts and for the return of other associated critical ecosystem services.

Shellfish reefs once dominated many of the temperate and subtropical estuaries on Earth. Recorded accounts indicate the existence of vast reefs with significant structural complexity in bays around the world.

In many ways they were the temperate-climate equivalents of coral reefs, with large calcareous formations critical for creating habitat and maintaining biodiversity (Lenihan and Peterson 1998,  Grabowski  and  Peterson  2007).

Estimates  of  the loss of mangrove and salt marsh (30%–50%), sea grass (approximately 30%), and coral reef (approximately 20%) ecosystems have been influential in developing science and policy actions (Valiela et al. 2001, Wilkinson 2002, Zedler and Kercher 2005, Waycott et al. 2009, Spalding et al. 2010). Given the severity of oyster reef loss (85%), the need for action is clearly urgent.

The devastation of shellfish reefs has been decades and centuries in the making, but this loss is not just a problem of the past. Oysters still are managed without regard for the structure or function of reefs.

Reef conservation.

Native oyster reefs should be recognized as an important habitat and ecosystem and a priority for habitat management and conservation.

We have identified several areas with remaining reefs that are critical for conservation, including those bays with reefs in fair to good condition, particularly if these bays are in ecoregions with more than 90% reef loss overall. The need for action is pressing for flat oysters (Ostrea spp.) in Europe, Australia, and Pacific North America.

Protected areas have been used effectively for the conservation of coral reefs and other ecosystems. A few small, protected areas for oyster reef ecosystems have been established recently and are showing signs of success. For example, newly protected areas can be found in China (Jiangsu Prov- ince), the United States (North Carolina and Virginia), and Chile (Region X) (Peterson et al. 2003, Powers et al. 2009). These examples indicate that protected areas are useful tools for oyster reef conservation and should be expanded.

The extent of oyster reef habitat loss justifies more explicit recognition in protected areas policies. The European Union identifies biogenic reefs as a habitat for protection under Natura 2000. Although such recognition is encouraging, native oyster reefs of O. edulis should be clearly identified and elevated to a priority habitat type given their functional extinction throughout much of Europe. Oyster reefs should be specifically identified for protection under the Ramsar Convention; furthermore, they should be regarded  with other similar wetlands (e.g., seagrasses, coral reefs, man- groves, kelp forests) as an “under-represented wetland type.” International agencies and environmental organizations could bolster local efforts by adding temperate reefs to their conservation programs.

Oysters have been identified as a threatened or imperiled species and as a threatened and declining habitat by a number of countries in Northern Europe, around the Black Sea, in the United Kingdom, and elsewhere.  Similar listings are appropriate in many regions and countries, including in the United States and Australia.

Fisheries  management.

For many other fisheries, rebuilding plans are being developed, and there have been some important successes (Worm et al. 2009). However, plans for rebuilding oysters are rare.  While scientists and managers focus attention on relatively few well-known estuaries with oysters, such as the Chesapeake Bay (e.g., Jack- son et al. 2001, Lotze et al. 2006), needs are not being met elsewhere and opportunities are being missed.

Oysters have many of the elements that underpin successful efforts to sustainably manage other fisheries…

Sustainable shellfish harvests have been achieved elsewhere through a mixture of

• protected areas for important populations,
• cooperative fishery management,
• user rights,
• use of aquaculture to reduce harvests of wild stocks.
• institutional arrangements that provide for the co-management of exploited oyster populations and the allocation of territorial user rights in fisheries help link sustainability and economic growth.

These approaches include local fishers in land-use policy and management decisions and give them rights to manage biological resources.

These catch share–based management approaches are being applied with success in artisanal benthic shellfisheries, including oyster and mussel fisheries, in South America (Castilla et al. 2007, Carranza et al. 2008, 2009).Reef recovery and restoration.There have been some small- to medium-scale efforts to restore oyster habitats. Given the scale of losses, reef recovery and restoration efforts will need to be enhanced.It is possible to achieve better returns on existing restoration investments, and new funding streams to rebuild services from reefs should become available (Coen et al. 2007).Present funding for native oyster restoration is directed mainly at fishery enhancement and harm mitigation.In the United States, tens of millions of dollars have been spent in the past decade to recover fisheries (e.g., North Carolina, Chesapeake Bay, Delaware Bay) and to regain fishery production following hurricanes in the Gulf of Mexico.

Often billed as restoration, the outcomes of these investments are measured mainly in near-term harvests; the other services provided by reefs are rarely measured.

Indeed, if just the landings of other fish that use restored and protected reefs are considered, the habitat value of reefs can be greater than the oyster harvest value (Peterson et al. 2003, Grabowski and Peterson 2007).

Assisting oyster fishers to overcome the effects of natural and human disasters and the legacy of poor management are important goals, but investment outcomes should be measured over the longer term (e.g., not just the put-and-take of oysters). Desired investment outcomes should include rebuilding the natural capital of reefs for long-term sustainable harvests and greater resilience to storms.

Oyster managers and industry could play a central role in new restoration efforts. The recent British Petroleum Deepwater Horizon oil spill and the actions in response to it have already had major impacts on fisheries and oyster reefs, and there will be significant investments in response and restoration. These impacts and investments underscore the importance of re-envisioning our management and restoration approaches to support a sustainable future for both reefs and fishermen.

Improved recognition and measurement of the socio-economic benefits from native reefs can create opportunities for new funding sources for restoration (Laing et al. 2006).

As sea-levels rise and the economic impacts of storms worsen, new funding should be generated for climate adaptation to restore oyster reefs for shoreline protection (Piazza et al. 2005).

Markets are emerging for the trade of nitrogen pollution credits in coastal watersheds, and this approach has been used to fund the restoration of riverine buffers. Such markets might fund reef restoration if the nitrogen removal capacity of oyster reefs were harnessed appropriately.

As this field of ecosystem services develops, we must take care to ensure that ecosystems and services are restored.

There are real opportunities for conservation and restoration in areas where oyster harvest is limited by closures caused by poor water quality. Enhanced filtration by larger populations of native bivalves may even improve degraded waters. Leadership from the US Interstate Shellfish Sanitation Conference, among others, could help to identify solutions… and thus support enhancing shellfish abundance. Other disincentives to restoration should also be addressed,  including  the  notion that… planting shells in the water is sometimes regulated as ocean dumping or “fill.”

Although there have been only a few concerted efforts at oyster habitat restoration beyond small-scale projects, the groundwork for success has been laid. Some of the places where there have been initial successes in recovery and restoration include key areas within the Chesapeake Bay, Pamlico Sound (North Carolina), Strangford Lough (Northern Ireland), and Limfjord (Denmark), among others (Lenihan 1999, Brumbaugh et al. 2000, Laing et al. 2006, Brumbaugh and Coen 2009, Powers et al. 2009, Schulte et al. 2009, Smyth et al. 2009). Returns should accelerate greatly as reefs rebuild and become self-sustaining.

Nonnative species.

The International Council for the Exploration of the Sea (ICES) has developed codes of practice for marine introductions and transfers that should be followed in aquaculture to reduce the likelihood that new invaders are released into the wild (ICES 2004).

Shellfish aquaculture has provided pressure to spread nonnatives, but aquaculture has also been a part of the solution in restoring native oyster reefs (Dumbauld et al. 2009). Shellfish aquaculture is more sustainable than most other forms of aquaculture (Naylor et al. 2000). Aquaculture can also reduce harvest pressure on wild shellfish populations when it is coupled with other capture fishery management tools (Castilla et al. 2007, Carranza et al. 2009). Aquaculture companies can play an even greater role in restoration given their expertise in oyster growing and oyster seed production. The aquaculture industry, public agencies, and environmental nongovernmental organizations are natural partners for promoting the restoration of native oysters and their services. Together, these groups could promote businesses to help produce native oyster species that can be sold for market while generating funds and seed oysters for habitat and population restoration.

There is also common ground among the aquaculture industry, environmental groups, and managers in conserving and restoring coastal water quality. Oysters are useful bio-indicators for coastal condition and can be used to help target and monitor needed remediation actions in watershed management (Volety et al. 2009). Indeed, watershed management will prove to be one of the biggest challenges to conserving shellfish and other coastal ecosystems. The fate of oysters is tied to overall estuarine condition. Improving estuaries will require significant effort, especially because such efforts must be watershed based.

Conclusions

• The condition of oyster reef ecosystems is poor
• The challenge in revitalizing native oyster reefs is great,
• We have identified many reasonable actions that can be expanded across local to regional to global scales.
• Actions recommended to reverse this decline and enhance oyster reef condition include
  • improving protection;
  • restoring eco-systems and ecosystem services;
  • fishing sustainably;
  • stopping the spread of nonnatives;
  • capitalizing on joint interests in conservation, management, and business to improve estuaries that support oysters.

Estimates of oyster reef abundance and condition across many bays and ecoregions provide a baseline for setting much-needed and realistic goals for restoration and conservation and for evaluating the progress in meeting them.Many obstacles hinder successful management of oyster reefs;

• one of the most  pervasive  is  simply  the  perception among managers and stakeholders that no major problems exist (Laing et al. 2006).
• the common misperceptions that shellfish habitats cannot be successfully recovered and that nonnative shellfish in aquaculture can replace natives. Put simply, native oysters must be recognized for the reef habitat that they provide. A growing number of examples demonstrate that recovery is feasible.
• We need new approaches within the regulatory and management communities to lead to shellfish habitat conservation and restoration designed not just for fisheries production but specifically to recover these critical ecosystems and their services.

Acknowledgments

This work was funded by the Kabcenell Family Foundation, NOAA Restoration Center, AdriaBio (University of Bologna), and the Santa Barbara Coastal Long-Term Ecological Research program (NSF OCE-0620276). The authors thank Christine Shepard, Zach Ferdaña, Jeff Vincent, Antonella Fatone, and Bill Arnold for help with the data and Peter Kareiva, Lynne Hale, and David Strayer for thoughtful reviews of the manuscript.

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