The role of oyster reefs as essential fish habitat: a review of current knowledge and some new perspectives

—The importance of molluscan-dominated systems (e.g., oysters reefs, mussel beds, vermetid gastropods) to the maintenance of commercially and ecologically important species has not been as broadly recognized as has been the importance of other structurally complex estuarine habitats such as sea grass beds and salt marshes. As a consequence, these systems have often been unappreciated and understudied. Important ecosystem services of molluscan-dominated systems include: (1) filtering capacity; (2) benthic– pelagic coupling; (3) creation of refugia from predation; (4) creation of feeding habitat for juvenile and adult mobile species as well as sessile stages of species that attach directly to molluscan shells; and (5) provision of nesting habitat. Destructive harvesting and overfishing can reduce habitat extent and impair habitat functioning. Only recently have ecosystem services been incorporated into the management of these systems. The role of oyster reefs as “essential fish habitat” falls into two principal categories: (1) reefs as habitat for oysters and (2) reefs as habitat for resident and transient species. Although the former role has received some attention as part of efforts to restore oyster resources, the latter role remains largely unexplored. The role of oyster reefs as critical habitat for other species is suggested by the diverse fauna associated with them; however, the factors that control the development of these reef-associated assemblages are generally unknown, and enumeration of specific habitat services using replicated field experiments is just beginning. Using data summarized from studies in Maryland, Virginia, North Carolina, South Carolina, and Texas, we classify finfish assemblages associated with reefs based upon the degree of their association and include an extensive finfish and decapod species list. We conclude, within the context of the current state of knowledge, that (1) the construction of reef bases using materials that provide adequate vertical relief and interstitial space and (2) the establishment of broodstock sanctuaries protected from harvesting pressure are important for restoring oyster populations. Utilization of reef habitats by numerous commercially, recreationally, and ecologically important species across a wide geographic range likely portends the reef habitats’ importance as essential fish habitat, but many functional relationships remain to be evaluated. Future oyster habitat research needs include (1) defining the morphological and spatial reef characteristics that support enhanced oyster growth and survival; (2) improving understanding of how harvest methods affect reef integrity and function; (3) determining the critical services provided by reef habitats in the life cycles of important species; and (4) further clarifying the trophic links between the resident fauna on oyster reefs and transient species. ROLE OF OYSTER REEFS 439 to as EFH). The law defined EFH as “those waters and substrate necessary to fish for spawning, breeding, feeding, and or growth to maturity,” and “fish” was defined to include “finfish, molluscs, crustaceans, and all other forms of marine animal and plant life other than marine mammals and birds” (USDOC 1997). The ability of fishery managers to identify EFH depends on the availability of information on various habitats. For many habitats, a wealth of information is available, but for other habitats information is scarce. Therefore, as part of the habitat information-gathering process, it is important to understand the extent to which estuaries and specific estuarine habitats serve as EFH and what estuarine habitat characteristics are most important to EFHrelated processes. There is no question that oyster reefs qualify as EFH because of the importance of reefs to the oysters themselves. However, we are just beginning to understand what precise characteristics of oyster reefs enhance oyster recruitment, growth, and survival. In addition, recent research has highlighted the importance of oyster reefs to ecosystem-level processes and as habitat for fishes and macroinvertebrates other than oysters. In this paper we summarize the current state of our knowledge of oyster (specifically the eastern oyster C assostrea virginica) reefs as (1) important to ecosystem-level processes in estuaries; (2) essential habitat for oysters; and (3) important habitat for ecologically, commercially, and recreationally important finfish and crustacean species. We include in this study existing descriptive data on oyster-reef habitat ecology and recent and ongoing experimental investigations that are relevant to understanding how the structure and ecological function of oyster reefs may be incorporated into an EFH framework. We also discuss issues relating to tradeoffs between habitat and resource management and protection, the value of areas closed to harvesting due to poor water quality, and habitat restoration and enhancement (see Coen and Luckenbach, in press, for more information on habitat enhancement). Decline of the Oyster Fishery and Reef Habitat The range of the eastern oyster C assostrea virginica (Gmelin) extends from the Saint Lawrence River in Canada to the Atlantic coast of Argentina (Carriker and Gaffney 1996), with introductions into the northwest Pacific region of the United States. The eastern oyster is a reef-forming organism, but it varies throughout its range in habitat and growth form. Eastern oyster reefs may be intertidal or subtidal, fringing or patch reefs, and may vary in size from a few square meters to many hectares. Greatest abundances are found in areas where a partial predation refuge exists, such as low-salinity (<15 ppt) waters or in the intertidal zone (e.g., MacKenzie 1983, 1996a, 1996b; Burrell 1986; Kennedy et al. 1996). Although intensive, hatchery-based aquaculture of oysters is increasing in the United States, the oyster fishery historically has been based upon wild stocks. Some areas in the United States still have wild oyster stocks supporting valuable fisheries (see MacKenzie et al. 1997a, 1997b), but most stocks are in decline owing to the following factors (Gross and Smyth 1946; MacKenzie 1983, 1996a, 1996b; Rothschild et al. 1994; Kennedy et al. 1996; NOAA 1997; Lenihan and Peterson 1998; Hargis and Haven, in press; Luckenbach et al., in press): • overfishing and associated habitat destruction; • shortages of oyster cultch (i.e., shell or other hard substrate); • disturbance (e.g., dredging, boating, storms); • reduced water and habitat quality; • alteration of natural flow and salinity patterns; • natural and introduced predators and competitors; and • oyster disease pressures. Between 1880 and 1910, the oyster fishery peaked at more than 72.7 million kg of meat per year (Brooks 1891; MacKenzie 1996a), but by 1995, U.S. landings had declined to 18.4 million kg (MacKenzie 1996a). The once highly productive fisheries of the Chesapeake and Delaware Bays and North Carolina (Frankenberg 1995) have virtually collapsed. Although diseases are often cited as the reason for recent declines, overharvesting and resultant habitat destruction with little shell replacement (considered analogous to strip mining by some [see Hargis and Haven, in press]) have certainly been major causes for the dramatic declines throughout much of the mid-Atlantic region (see Brooks 1891; Gross and Smyth 1946; Rothschild et al. 1994; Lenihan and Peterson 1998; H. Lenihan and F. Micheli, University of North Carolina, unpublished data). Oyster fishing methodologies, such as handand hydraulically operated tongs, dredges pulled by sailing and motor-powered vessels, and hand-harvest-