Historical oyster reef connections to Chesapeake Bay – a framework for consideration

Estuarine, Coastal and Shelf Science 64 (2005) 119e134 www.elsevier.com/locate/ECSS

Historical oyster reef connections to Chesapeake Bay e a framework for consideration Jerry McCormick-Ray Department Environmental Sciences, University of Virginia, Charlottesville, VA 22904, USA Accepted 1 February 2005

Abstract Lieutenant Francis Winslow’s 1878 oyster survey data of the lower Chesapeake Bay provided the spatial context for considering connectivities of Crassostrea virginica to estuarine function and food web dynamics. Winslow measured the area, water depths, and in some cases bed thickness for 70 distinct oyster beds in the 368 km2 Tangier-Pocomoke complex, and 12 beds in 35 km2 of the James River oyster reef habitat. Individual beds showed great size variations, yet most were !2 km2. Beds occupied variable water depths, but most occurred in 1e4 m depths near shore and 2e12 m depths along channels. Varied bed-top topography and elevation changes created complex structures and hydrologic corridors between shores and tributaries. This historical spatial data provide a framework for considering oyster beds in the context of modern research to suggest they formed resource patches in the seascape at the estuarine scale. It is suggested that beds at different locations are connected by hydrologic corridors, and they facilitate dispersion, migration, and recruitment. Also, oyster-reef habitat added topographic roughness and spatial heterogeneity that increase resource-use options important to an active and diverse estuarine community moving between shore and tributary systems, and between Bay waters and watershed systems. Ó 2005 Elsevier Ltd. All rights reserved. Key words: oyster beds; estuarine reef; seascape ecology; benthic ecology; food web linkages; historical data; hydrologic corridors; Chesapeake Bay

1. Introduction Considering the historical ‘‘connectivity’’ role of oysters draws on concepts from land/seascape ecology. Oysters, like most organisms, are distributed in patches across the landscape. A landscape patch is a non-linear surface area that differs in appearance from surrounding areas (Forman and Godron, 1986). Patches have edges that expose the patch community to species that use or depend on corridors as routes for movement. A corridor is a narrow strip of landscape/seascape space over which energy, materials, and species flow, occupying a space different from that of adjacent landscape features that it connects. Patches are often embedded in a matrix, an E-mail address: [email protected]. 0272-7714/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2005.02.011

area that surrounds the patch, and composed of different species’ structure or composition. How connected or spatially continuous a corridor is may be quantified simply by identifying the number of breaks per unit length of corridor, e.g. the number of discrete oyster beds along a corridor. Historical surveys provide evidence for considering the role of oysters in Bay-wide connectivity. Sessile invertebrates create a physical structure that is an organizing force for an estuarine community, with significant effects on current velocities (Widdows et al., 1998; Dean, 1981). Movement of water near the sediment-water interface is restrained by contact with the bottom, where a boundary layer develops that is determined by bulk flow velocity and roughness at the sediment-water interface. Boundary layer thickness is generally 1 m, depending on current velocity (Wildish

120

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

and Kristmanson, 1979). Local (elevation-dependent) time-averaged current velocity in the turbulent boundary layer, a region close to the bed, shows a close association with the log of the elevation (Wright et al., 1990). Turbulent flow over smooth and rough seabeds results in small- scale vortices associated with formation of elongate streaks of high-speed downward flows and low-speed upward flows. These flows induce bursting events responsible for seabed sediment movements (Le Couturier et al., 2000). Large bedforms in the flow path create flow structures that may extend 10 to 20 m streamwise and exceed 1 m vertically, possibly related to flow separation effects. Sessile invertebrates in a flow path redirect flows, altering velocities and influencing erosion, sedimentation, recruitment, dispersion, distribution and abundance. There is much evidence supporting interactive connections between oysters and hydrology (Pritchard, 1952, 1989; Manning and Whaley, 1954; Kech et al., 1973; Andrews, 1983; Wright et al., 1987, 1990; Mann, 1988; Ruzecki and Hargis, 1989; Kennedy, 1996a,b; Lenihan, 1999; and many others). Highly variable oyster shell shapes and variable bed structures formed by interactions with geology, geographic location, predators, and aerial exposures relate to hydrology (Kennedy and Sanford, 1999). Larval dispersal, recruitment, and migration among oyster beds depend on hydrology (Winslow, 1882; Pritchard, 1952; Andrews, l951; Galtsoff, 1964; Eggleston, 1999; others), the outcome being variable bed configurations and increased hydrologic complexity. Where currents and feeding conditions are appropriate, a loaf-shaped bed can form and accrete upward to connect with the water’s surface. Bed morphology is the outcome of the interactions of oyster life history successes and tidal channel conditions. These interactions create varied bed structures when observed at local levels and seascape patterns when observed at the landscape scale (McCormick-Ray, 1998). A fringing reef thus forms near shore, string reefs form when beds occur at right angles to shore and tidal currents, and patch reefs form as compact, irregular beds away from shore (Hedgpeth, 1953; Stenzel, 1971; Kennedy and Sanford, 1999; Smith et al., 2003). Historical accounts make clear the extent, abundance, and value of oysters in the Chesapeake Bay. In the 1800s, the Bay was the world center for commercial oyster production (Ingersoll, 1887). William K. Brooks (1891), the noted authority on oysters from Johns Hopkins University, estimated from records that 400 million bushels of oysters were harvested from Chesapeake Bay between 1834 and 1890. The 1887 U.S. national fisheries census reported that, ‘‘The Chesapeake Bay and its numerous salt-water tributaries contain the most prolific and valuable oyster beds in the world, probably about equally divided between the two States of Maryland and Virginia’’ (Ingersoll, 1887,

p. 429). The national, Eighth Census reported that in the 1858e1859 oyster season, Virginia harvested two million bushels from areas of the York river, Rappahannock, Potomac, and Hampton Roads waters, with many more unaccounted (Secretary of the Interior, 1866, p. 540). ‘‘The creeks and coves along the bay shore were formerly filled with natural beds of oysters.’’ (Earll, 1887, p. 461), when in 1824e1825 Virginia began shipping oysters to Boston, New York and New Jersey for transplanting to their depleted beds (Md. Oyster Comm., 1882, p. 38). Peak harvest in the Bay was reached in 1880, when Maryland harvested 10.6 million bushels and Virginia 6.8 million bushels (Ingersoll, 1887, p. vii). At this time, the oyster fisheries ranked among the top U.S. fisheries, e.g. with whales, fur seals, seals, salmon, cod, sturgeon, shad, herring, menhaden, mackerel, alewife, eel, and clam fisheries (Baird, 1887; Ingersoll, 1887). In 1908, the Bay supplied an estimated 11 million bushels of oysters (Smith, 1913). The 1800s accounting of Bay oyster production was conservative and arguable, but clearly evident that oysters concentrated non-randomly around the Bay in varied spatial and temporal distributions. Harvest production is estimated from the number of oysters contained in a bushel, but the numbers varied with location and with oyster size. A bushel of large oysters contained !250 oysters (first class), of medium oysters contained 200e400 oysters (second class), of small oysters contained O400 oysters (third class). Young growth were very small oysters !1 inch (2.5 cm) (Maryland Oyster Commission, 1884, p. 18). Natural production was revealed from observations that in one day in 1878, w2408 bushels of large oysters (150 to 200 per bushel) were harvested from Tangier Sound, with an estimated 361e482 thousand reproducing oysters and w486 thousand young (Winslow, 1882). And at the beginning of this oyster season, 7e 9.5 million oysters were harvested from Tangier and Pocomoke sounds, located on the southeastern region of the Bay. These conservative estimates of harvest hint at the massive production of meat, larvae, shells and metabolites that one dominant benthic species contributed in restoration of discrete oyster beds during the important summer season. What remains of interest is how historical distributions of oysters might relate to modern ecological studies. How might historical oysters have contributed to estuarine fish abundance and food web dynamics? How might bed interactions with hydrology have influenced dispersal, migration and dependency, bed recovery and habitat persistence? And did historical oyster beds create discrete ‘‘resource patches’’ in a web of hydrologic corridors that connected life history patterns to fish production and ecosystem function? A seascape approach provides a preliminary framework for considering such connectivities in the historical Chesapeake Bay ecosystem.

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

121

2. The historical oyster beds A natural oyster bed in the Chesapeake Bay in the 1800s is described in the Report of the Oyster Commission of the State of Maryland (Oyster Commission, 1884, p. 82). ‘‘An examination of a Coast Survey chart of any part of the Chesapeake Bay or of any of its tributaries will show that there is usually a mid-channel or line of deep water, where the bottom is generally soft and where no oysters are met with, and on each side of this, an area where the bottom is hard, running from the edge of the channel to the shore. This hard strip is the oyster area. It varies in width from a few yards to several miles, and the depth of water varies upon it from a few feet to five or six fathoms, or even more. But there is usually a sudden fall at the edge of the channel where the oysters stop, and we pass onto hard bottom; and a cross section of the channel would show a hard, flat plane, with oysters on each side of the deep, muddy channel. The oyster bottom is pretty continuous, except opposite the mouth of a tributary, where it is cut across by a deep, muddy channel. The solid oyster rocks are usually situated along the outer edge of this plateau, although in many cases they are found over its whole width nearly up to low-tide mark, or beyond. The whole of the hard belt is not uniformly covered with oysters, but it is divided up into separate oyster rocks, between which comparatively few can be found. The boundaries of a natural rock which has not been changed by dredging, are usually well defined, and few oysters are to be found beyond its limits. The oysters are crowded together so closely that they cannot lie flat but grow vertically upwards, side by side. They are long and narrow, are fastened together in clusters, and are known as ‘coon oysters’. When such a bed is carefully examined it will be found that most of the rock is made up of empty shells, and a little examination will show that the crowding is so great that the growth of one oyster prevents adjacent ones from opening their shells, and thus crowds them out. Usually the oysters upon such a bed are small, but in some places shells twelve to fourteen inches long are met with..’’ Congregations of oysters were called beds, grounds, bars, reefs, or rocks (Ingersoll, 1887, p. 508). Oyster beds lined subtidal bottoms near most shores and tidal channels of the Chesapeake Bay (Fig. 1). Winslow (1882) surveyed two important oyster areas, Tangier-Pocomoke sounds and James River, August 7 to October 15, 1878. He documented and mapped bed area, thickness, character, and water depths at mean low water, and graphed bed profiles (McCormick-Ray, 1998). Oysters grew long and narrow on hard, natural, undredged beds, forming clusters of 3 to 4, 4e12, and 15 oysters, with tufts of red or white sponge attached. ‘‘The mature first and second class oysters were covered and the interstices between them was (sic) filled with those

Fig. 1. Historical fringing reef of Chesapeake Bay, with Tangier Sound complex located in box (from Funderburk et al., 1991).

of the third and fourth classes of oysters and with numerous barnacles, some crepidula, and very few tubicola.’’ Undisturbed oyster beds, surrounded by soft bottom, thus contained oyster clusters variably distributed and along dense ridges, with diverse assemblages of mussels, barnacles, anemones, worms, small crabs, sponges and tunicates. Borders of soft sand or mud marked the edges of hard beds. The soft bottom formed distinct boundaries between beds. When edges were disturbed by dredging, oysters colonized adjacent sand,

122

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

Table 1 James River oyster Beds e 1878 (Data from Winslow 1882) Name

Bed size (km2)

Water depth over beds (m) Minimum

Maximum

Mulberry Point Point of Shoals Jail Island Burrells Bay Blunt Point White Shoal Thomas’s point Kettle Hole Brown Shoal Bally Smash Naseway Shoal Cruiser’s-Nansemond Ridge Craney Is./Elizabeth Total

3.1 12.3 4.8 deteriorate 0.9 1.2 0.8 1.5 1.5 0.8 2.5 5.8 e 35.2

0.3 0.6 0.9 e 0 0.4 0.3 0.9 0.9 1.2 1.8 2.1 1.8 0.3e2.1

7.3 9.1 4.9 e 2.4 3.3 0.9 1.5 5.5 1.2 2.4 2.4 4.6 0.9e9.1

grew large and round (of commercial interest), and individual beds coalesced.

3. Analysis Winslow’s survey provides quantitative measurements for comparison of oyster bed habitat for the James River (Table 1; Fig. 2) and Tangier-Pocomoke complex (Fig. 3; see McCormick-Ray, 1998). Table 2 gives the number of beds, sizes, water depth, substratum thickness, and total area of oyster coverage. The 70 beds in 368 km2 of Tangier/Pocomoke complex cover an area 10! larger than the 35 km2 and 12 beds in the James River. Twenty solid beds in Tangier Sound alone

Location to deepest channel

Northwest Northwest Northwest Southwest North Central Central North Central North Central North Central South Central South Central Southeast Southeast

formed hard bottom seascape that covered 59 km2, and scattered oysters occupied another 154 km2 for a total area of 213 km2 between the axial tidal channel and marshy shores. Tangier Sound beds were deepest (2.7 m to 16.5 m) of all beds and shallowest beds occurred in the James (0.0 to 9.1 m) and Pocomoke (0.3 m to 7.3 m). Substratum thickness of Tangier beds (0.3 me0.9 mC) was difficult to measure due to deep water. Thickest beds occurred toward tributaries: Nanticoke/Monie Bay (1.5 m), Manokin (1.2), Fishing Bay (north) (1.8 m), and upstream of the James on Jail Island (1.2 m). Individual bed sizes varied greatly (Fig. 4a). Most (83%) were !2 km2, and these occurred in channels approaching land, toward heads of Tangier sounds as

Fig. 2. Winslow survey map of measured James River oyster beds, redrawn for clarity and emphasis of deepest and shallowest channel depths (from Winslow, 1882).

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

Fig. 3. Winslow survey map of measured Tangier Sound oyster beds. Darker shades indicate hard beds; dark line on beds indicates dense oyster concentrations; dashes enclose scattered oysters around beds; dots between beds indicate deepest axial channel depths (from Winslow, 1882; McCormick-Ray, 1998).

123

Winslow observed. Eighteen percent of the beds broadly ranged in size between 3e24 km2. The 12 km2 Pt. of Shoals area in the James River was composed of several beds, and separated from Jail Island beds by a soft bottom swash channel. And the 24 km2 Fishing Bay bed at the head of Tangier Sound, defined as one hard bottom, contained 43 small ‘‘rocks’’, the sizes becoming smaller as the head of the Bay was reached. Groups of oysters, and those of different ages classes, were separate from areas occupied by grass and sponge. These oyster groups were sometimes cut by small mud slough, as in Fishing Bay, and by mud and sand areas, swashes, sloughs, depressions, deep holes and varied topography. Deeper soft mud/sand channels separated beds, between which few oysters grew. Oyster beds generally formed on shoals, but not always, and oysters did not occur in channels, but not always. Overall, oyster beds occurred between 0.0 and 16.5 m water depths, and most occurred in 1 m to !12 m. Local and regional differences relate to basin and tidal channel geomorphology. Pt. of Shoals water depths of 0.6 me9.1 m were more varied than the 3.7 me5.5 m depths covering the large 7 km2 bed (Great Bed) in Tangier Sound. The shallow depths of 1.2e3 m for beds of the northern portion of Fishing Bay deepened to 2.4 me3.7 m in its southern portion indicating a gradient toward the head of the Bay. Furthermore, beds generally sloped from a minimum near shore depth to a maximum near channel depth. An average of 61 beds shows a mean minimum depth of 3.2 m (SD, 1.6) nearshore, compared to more variable mean maximum depth of 6.5m (SD, 3.7) near the axial channel. Most beds (94%) had minimum depths !4 m, with 7% in O4 m (Fig. 4b). Maximum bed depths near the edge of the channel for 78% of the beds were 2e12 m, with only 9% !2 m, and 13% O14 m (Fig. 4c). The daily tidal ranges of 0.7 m in Tangier and 0.8 m in the James indicate that 15% of the beds (James River, Pocomoke Sound) were intertidal. Fifty-eight percent exhibited a water depth change of 1e4 m (Fig. 4d), indicating a sloped bed-top terrace from shore to channel. Eleven percent changed slope !1 m and 3% changed as much as 11e12.9 m. Average conditions, however, mask the variable topographic relief. For example, the complex, variable bed topography illustrated in Fig. 5 exemplifies a single bed’s vertical complexity along Tangier Sound channel. The bed is dominated by oysters in uneven distributions, and separated by small percentages of areas covered by mud and sand. For James River, bed topographic complexity is illustrated in Fig. 2, showing beds with deep holes O4.5 m that lacked oysters as on Point of Shoals, and shallow areas !0.7 m. Deepest channel depths of 14 m around Pt. of Shoals indicate the deep axial flow into Burwells Bay, where old beds were being covered by mud on the southern shore. The deepest axial channel depth of 45.8 m occurred at the base of Jail

124

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

Table 2 Winslow (1882) sub-regional summary (Cindicates limit of probe penetration) Name

Total area (km2) Solid beds

Scattered

Oyster area

Tangier/Pocomoke Complex Nanticoke/Monie Bay Fishing Bay Northern Tangier (between Fishing Bay and Tangier Sound) Tangier Sound Manokin R. Big Annemessex R. Pocomoke Sound James River Tributary

79 3 3 3

277 e 21 e

59 5 2 4 e

154 e e 102 e

No. of beds

Solid bed thickness (m) Min

Max

Min

Max

368 3 24 3

70 5 1 2

0.2 0.2 0.3 e

1.8 1.5 1.8 0.6

0.3 1.2 1.2 2.4

16.5 6.4 3.7 4.6

213 5 2 117 35.2

20 15 10 17 12

0.3 0.2 e 0.3 e

0.9C 1.2 0.2 0.9C 1.2

2.7 2.4 2.1 0.3 0.0

16.5 8.2 10.0 7.3 9.1

Island bed, and deep axial depths O9 m separate northern and southern beds toward the tributary entrance, where the channel widened and deepened into a natural harbor. North of Cruisers bed, depths reached 23 m then shallowed at the broad entrance. Point of Shoals and Cruiser beds occur at opposite ends of oyster habitat and cross the axis of tidal flow, deflecting currents that formed into strong counter currents and eddies, as observed by Winslow. The middle beds between them laid in the general direction of flow, where current velocities and direction were less variable.

Water depth range (m)

The Tangier-Pocomoke complex and James River oyster beds are imbedded in a larger spatial scale habitat matrix, as illustrated in a recent study of surface lithology in the James (Fig. 6). The topographically complex oyster reef habitat occurs between shore and channel, and between marine-bay water and fluvialfreshwater systems. In this larger context, the oyster bed system increases the overall morphological, ecological, and hydrological complexity of the lower James River tributary. The vertical and horizontal relief and habitat complexity of the shoals, shores, and channel increase

Fig. 4. Number of beds and percentages (rounded) indicating variations in (a) Bed size; (b) Shallowest depth over beds; (c) Deepest depths over beds; (d) Change in water depth, from shallow to deep.

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

Fig. 5. An example of the variable dimensions of an oyster bed, measured and graphed by Winslow (1882) (m). Muscle Bed is presented in two profiles: AZopen squares; BZsolid squares. Water depths measured from mean low water (MLW), and bed elevation measured from lowest bed point. Surface covered by oystersZ66%, 89%; sandZ0, 11%; mudZ34%, 0 on A, B profiles, respectively. Muscle Bed was located on the western side of Tangier Channel, opposite the 18 m depth of the axial channel (McCormick-Ray, 1998).

spatial heterogeneity in this mesohaline portion of the James, an important ecological region subject to conditions imposed by the watershed, climate, and geomorphology.

4. Discussion 4.1. Nodes of intense activity Modern measurements substantiate and increase understanding of Winslow’s survey results. Winslow observed that beds are composed of hard oyster rock that concentrate oysters, extensive hard shelly-mud-sand bottom with fewer oysters, and soft mud or sandy bottom where few if any oysters occurred. Haven and Whitcomb (1983) quantified such benthic habitats for oyster beds of the James, designating oyster rock as ‘‘oyster reef,’’ that ‘‘area with firm bottom and probe penetration of 0e5 cm,’’ where oyster density was

125

quantitatively higher than mud-shell areas. Beds included associated sand-shell and mud-shell bottom that contained lower densities of oysters and shells. And soft sand bottom that seldom contained shells or oysters, and soft mud bottoms that could contain significant numbers of oyster, but growth and survival were poor. Different parts of the estuary varied in the size of oyster rock and its distinctive outline, and densities of oysters and shell material differed among the varied bottom types. However, the productive beds remain in nearly the same location since Winslow, the structure and boundaries altered by human interference (Moore, 1910; Haven and Whitcomb, 1983). These hard oyster areas and hard shelly bottom attract a diverse, densely populated, seasonally changing faunal assemblage (Larsen, 1985), where macrofauna were quantitatively more dense and more diverse than areas of soft bottom, as Winslow observed. Furthermore, Larsen found that density and diversity significantly differed among beds and shifted with season. Density and diversity changed up the salinity gradient as well, being higher at Browns Shoal in salinity of 13.8-17.6 to lower levels at Deep Water Shoal beds located above Mulberry Pt. in salinity of 0.7e6.2. The low number of species that Larsen found on the large Point of Shoal oyster beds in the James relates to low salinity exposures, where mature oysters are typically small (!7.6 cm) and harvested as ‘‘seed’’ oysters. Wells (1961) found similar salinity results in North Carolina. Research has shown that oyster beds attract diverse and productive species (Bahr and Lanier, 1981; Lenihan et al., 2001; Peterson et al., 2003), forming heterotropic ‘‘hot spot’’ in the seascape (Bahr and Lanier, 1981). They are also persistent features (Winslow, 1882; Moore, 1910; Haven and Whitcomb, 1983; Hargis,

Fig. 6. Modern surface lithology of the James River suggests habitat heterogeneity available to a diverse estuarine community. Dense oyster shells (oyster rock), sand, mud, gravel and shelly bottom habitats are bounded shore and axial channel habitats, and marine and fluvial water exposures (from Nichols et al., 1991).

126

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

1999). Buried beds represent thousands of years of accumulations (Norris, 1953; Smith et al., 2003). Growth rates of beds in the James potentially could keep pace with sea level rise (DeAlteris, 1988), and some may accrete vertically to break the water surface and create an island fringed by living oysters (Kennedy and Sanford, 1999). Bed growth and persistence are fueled by the combined activity of associated filter feeders e barnacles, tunicates, lamellibranchs e and many other invertebrates. For every square meter on 11.4 km2 of intertidal reefs in Georgia, Bahr (1974) calculated epifauna could colonization at least 50 m2. This oyster community could generate an area-specific energy metabolism higher than coral reef, sublittoral soft bottom, or salt marsh communities. An oyster cluster also provides a spatial refuge attractive to a high abundance of cryptic organisms, which are poor competitors for space (Wells, 1961). Substrate size might also be a factor in species coverage, as small sizes have fewer interactions among resident species that could restrict planktonic larvae from colonizing, unlike large or non-isolated benthic patches (Keough, 1984). Thus, oyster beds are permanent benthic features that attract a seasonally changing community. They are distributed across several salinity zones attractive to species with preferred salinity tolerances. The bed assemblage fulfills many ecological roles by removing phytoplankton from the water column through feeding activities and by releasing massive amounts of gametes for heterotrophic consumers and metabolic products. These products are in the form of ammonium and orthophosphate utilized by phytoplankton (Dame, 1993, p. 261). Through these releases and utilization, the oyster bed assemblage connects the water column to the benthos, to marshes, and to other estuarine habitats. Models suggest important links between oysters and benthic production, fish stocks and phytoplankton productivity (Newell, 1988; Ulanowicz and Tuttle, 1992; Dame, 1996; Lenihan et al., 2001). 4.2. Hydrologic corridors connect resource patches Hydrological corridors that are subject to changes in direction and force also connect oysters to estuarine habitats downstream and upstream, and to shores and channels. Following concepts from landscape ecology (Forman and Godron, 1986), oyster beds may be visualized as seascape patches separated by hydrologic corridors of variable distances and width. The network of corridors form dominant routes for ebb and flood tidal currents, which oyster bed assemblages require for removal of wastes, importation of nutrients, gamete dispersion, recruitment, transport and oyster performance and abundance (Lenihan, 1999). Freshwater drainage from land flowing over shallow depths, daily pumping by asymmetrical forces of ebb and flood tides,

and stochastic storm events require water to escape through corridors separating shallow oyster rocks, hard shelly bottom, and soft mud/sand bottom on routes into tidal channels. The morphology, topographical depressions, and vertical changes in bed height create a hydrologic regime different from mud/sand seascapes and overlying waters. At low current speeds sediment without macrofauna in areas of extensive mudflats, exhibit a smooth, erodable surface that at increasing current velocities, as in periods of maximum tidal flow, is resuspended (Widdows et al., 1998). Biogenic structures and shelly bottoms create a rough bottom to slow velocities and break down the orderly flow of boundary currents (Wright et al., 1987). This roughness can enhance food supply to benthic organisms (Butman et al., 1994) and feeding activities deplete food to others downstream (Wildish and Kristmanson, 1985). Local variations in boundary flow pattern and strength can affect recruitment and successional patterns of small larvae and juveniles (Jumars and Nowell, 1984). Bed size and distance between beds influence velocities that generally increase at 1m above the bed (Lenihan, 1999). And within a meter of the bed, oyster ‘‘rocks’’ can slow currents (Breitburg et al., 1995). Bed roughness and configuration in channels also influence the boundary between ‘‘hydrodynamically rough’’ and ‘‘hydrodyamically transitional’’ (Sternberg, 1968). Hydrologic flows vary with topography, geomorphology, and bed configuration. Bed configuration can modify velocities across a reef terrace, channeling flow through small corridors between spaces for transport and exchange of organisms and materials to other beds, marshes, and estuarine ecosystems in a network of channels. Oyster bed hydrology that entrains particles can affect the rate and retention of planktonic larvae and sediment distribution (Nowell et al., 1981; Jumars and Nowell, 1984; Butman et al., 1994; Lenihan, 1999), all of which affect development of a heterogeneous benthic community. Oysters in shallow marshes may influence the evolution of marsh-estuarine systems (Grave, 1905; Dame et al., 1992) and interact with ebb- and flood-exchanges in tidal discharge and current speed to affect net transport over broad, shallow areas (Boon, 1975; Dyer, 1977; Friedricks et al., 1992). Impedance of shallow-water flow creates hydrologic corridors for movements of particles into and out of mud flats, seagrass beds, marshes, and among beds. The vertical relief created by the beds might be comparable to a low-energy coral-reef environment, where water pumped onto it may escape through outlet channels (Gourlay, 1996). At increasingly large scales, tributary flows connect oysters to watershed systems and Chesapeake Bay as a whole. Modern studies show that the James River is the third largest contributor of freshwater to the Bay

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

system (Nichols et al., 1991). Oysters reside within a 35 km section of the River, downstream from a 26,000 km2 watershed system and 26 km upstream from its mouth that adjoins the Bay. Axial currents interact with topographic structures that cover broad shoals and beds, above which are steep ancient bluffs (5e18 m high), cliff-faced marshes (w1 m high), narrow beaches, and a few sand spits and creeks. As shown above, oyster beds span a salinity gradient between marine and brackish water, and these beds are connected by tidal currents that generally set northwest/southeast and create a complex circulation pattern with freshwater. The intensity of freshwater flow can shift the salinity pattern up and down the estuary (Pritchard, 1952), and in conjunction with tidal velocities and channel geomorphology can determine water column homogeneity or stratification (Pritchard, 1989). Exposures to springneap tides (Haas, 1977), storm events such as Tropical Storm Agnes (Larsen, 1976; Nichols, 1977), and extreme flooding and drought that produce exceptional hydrographic conditions may transport larvae out of the tributary and into the Bay. Where abundant oyster larvae in the water column are transported to old or new locations to colonize exposed shells, a ‘‘rescue effect’’ may occur to restore damaged oyster beds. From such dynamic events, buried and dead oyster shell becomes available substrate for colonization by other species mobilized from other areas of the Bay. Hence, the Bay might be interconnected by hydrologic channels that transport mobilized larvae whose success depend on life history timing, habitat availability, and seasonal conditions. The broadly shallow Tangier-Pocomoke complex that oysters once covered contrasts with the James River. Oysters subtidally lined both sides of the 66.6 km axial Tangier Sound channel from Watts Island to Fishing Bay, occurring in varying water depths and connecting with Nanticoke, Wicomico and Pocomoke, a paleochannel system (Mixon, 1985). Tidal currents generally set north/south along the Tangier channel to interact with extensive shallow mudflats, low-relief salt marshes, and tributaries that drain from small watershed systems. The Nanticoke and Wicomico rivers in the northeast (Monie Bay), Manokin and Big Annemessex rivers on the east, and Pocomoke River in the southeast deliver relatively small amounts of freshwater into a broad, shallow, and topographically complex Sound occupied by extensive oyster beds. Hydrologic corridors, winds, and complex oyster bed topography interact to disperse larvae and to mix limited freshwaters with saline Bay waters for a vertically homogeneous water column. The extensive area covered by Tangier Sound oysters was 6! larger than the confined oyster area of the James River, restricted to narrow shoals and fluvial/ marine barriers. And higher salinity in the Tangier region is due to low freshwater inflow, non-local forcing,

127

and to the rotational effects of the Earth that contribute to higher tidal range and velocities than on western and upper Bay shores (Carter and Pritchard, 1988). Currents following the axial north/south corridor diverge slightly at tributary mouths and straits that separate marshy islands, where Sound water inter-connects with Bay water. Recruitment of planktonic organisms may be regulated by hydrologic corridors that deliver them to different regions of the Bay (Tyler and Seliger, 1989), subject to conditions in the Bay. Topography, geometry, winds, freshwater pulses, and oceanographic forces that mix or stratify Bay waters (Boicourt et al., 1999) affect the complex hydrologic corridors that cross the entire Bay and connect habitat patches to one another. The Bay’s basin is a long, variably narrow, relatively shallow (!18 m deep) paleochannel system carved by the ancient Susquehanna River. The northern 70,000 km2 Susquehanna watershed provides a dominant freshwater input, supplemented by large watershed systems entering on the western side of the Bay. Freshwater delivered in varying pulses from western tributaries creates estuarine fronts and transport systems interacting with the progressive wave that moves up and down the length of the Bay over a 12-hour period, altered by friction and reflection (Carter and Pritchard, 1988). Regional differences are evident in circulation patterns: the generally warmer waters of Maryland than Virginia and higher salinity on the southeastern side of the Bay. The eastern side is fed by small watersheds, where 70% of the surface drainage flows south-west toward the axis of the Chesapeake Basin (Oertel and Foyle, 1995). At the landscape scale, eastern shores are characterized by small watersheds, extensive low-relief salt marshes, and shallow bays that contrast with western shore that can be steep, tributaries that are fed by large watersheds, and extensive marshes that are brackish and tidal freshwater. The network of hydrologic corridors that connects this asymmetric distribution of habitats is subject to storms and droughts that strike the Bay and alter connections. 4.3. Connections among oyster beds: recruitment, dispersal and migration The complex hydrologic conditions of the Bay and tributaries give rise to complex recruitment patterns. Interactions among tidal and freshwater flow patterns, wind patterns acting over shallow depths and tidal change, and uneven distributions of spawning oysters all create highly complicated dispersal and recruitment for oysters, which vary with location and time (Shumway, 1996). Highly variable fecundity occurs within and among locations, and attributed to differences in oyster size, asynchrony, prior spawning and salinity regimes (Cox and Mann, 1992). Yet settlement rate in the James

128

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

was shown to be fairly consistent year to year for 17 years, 1944e1950, to sustain harvest and remain productive (Andrews, 1951, 1983). The interaction of tidally oscillating stratified flow with topographical features may be an important feature for estuarine dispersion and mixing (Dyer, 1989) of oyster larvae. Bed size, location and spacing are critical factors, and recruitment success may in part depend on small, variably distributed beds. Keough (1984) found that patch size and isolation strongly influence sessile species occupation. Species composition on non-isolated or large patches is mostly from asexual growth of colonial organisms located on adjacent patches, where interference competition plays a stronger role than larvae recruitment. Sponges and colonial tunicates, for example, were the most common taxa on non-isolated patches, whereas bryozoans were most abundant on small isolated patches and their planktonic larvae could colonize with little competition. A greater number and variety of species potentially could colonize isolated patches, especially large substrata. Variable pulses in oyster bed spawning occur along channels extending the length of oyster occupation, with spawning frequency timed to important mechanisms for larval transport and dispersal. In the James, for example, oysters release gametes over shallow inshore flats and beds at least weekly from late June through September, then continuously from July to October when the estuarine current forms. The most successful recruitment period occurs in late Augusteearly September, a period of low-freshwater discharge from the watershed, high salinity, and water stratification. The early stages of larval development occur when they are over flats and over the axial channel, then carried downstream in shallow surface water and recycled several times up the channel before setting on the flats. Recruitment to up stream beds depend in part on the spawning population at the mouth of the James (Andrews, 1951, 1983), and on up-stream beds that may be a spawning source as well (Ruzecki and Hargis, 1989; Cox and Mann, 1992). Spawning season for oysters in the Chesapeake Bay is generally between May and October, influenced by watershed, climate, stratification, and bed locations that together result in variable recruitment success. With larvae being released in variable pulses from separated beds connected by hydrologic corridors, beds become a dynamic source/sink for recruitment that may be locally or regionally connected. Seliger et al. (1982) explained his results of higher recruitment in one tributary relative to adjoining tributaries by hydrologic transport and tidal pumping. In the James River, oyster spawning time and recruitment patterns are unlike the rest of Chesapeake Bay, and an estimated 95% of the larvae in a period of 10 days can be exported (Andrews, 1983). The larvae may recruit to neighboring York and

Rappahannock tributaries, which have different timing and magnitudes in oyster settlement (Haven et al., 1978), and were historically productive oyster areas (Secretary of the Interior, 1866, p. 540). Thus the timing of an oyster larvae’s entry into the transport pathways maybe critical not only to its survival success, but to its colonization of new areas and restoration of old beds. Local, seasonal, and annual hydrologic and climatic variations may result in trapping and isolation, in broad interconnectedness, or combinations of both. 4.4. Connecting oysters to food web dynamics Benthic high-density food patches may be important to higher trophic levels, including pelagic predators (Vetter, 1994). Varieties of benthic fishes prey on benthic invertebrates, and relatively large piscivores prey on benthic fishes (Lenihan et al., 2001). In a seasonal burst of summer reproduction and feeding activity, oyster beds attract such species as the cow-nose ray (Rhinoptera bonasus) and striped bass (Morone saxatilis). Anadromous striped bass regularly forages on oyster beds, as do black drum (Pogonia cromis) (Murdy et al., 1997). Oyster beds attract salt marsh species, such as mud crabs and blue crabs (Callinectes sapidus) that move to the beds to prey on shallow water organisms (Bahr and Lanier, 1981). Oyster beds also attract terrestrial animals, such as raccoons and wading birds, including oystercatchers (Haematopus ostralegus) that prey on and around exposed beds at ebb and low tide. Reefs attract fishes that display varying degrees of fidelity to the bed. This fidelity may be broadly grouped as residents, facultative residents, and transients, although distinction sometimes may be unclear (Breitburg, 1999). Breitburg studied the Flag Pond oyster bed, located on the western shore of Chesapeake Bay, and found some fishes always present, feeding on benthic invertebrates and fishes or seeking shelter. These were considered resident. Resident oyster toadfish (Opsanus tau) attaches eggs to oyster shells and may show fidelity to a particular bed. Facultative residents, on the other hand, appear to remain on beds for several months. Highly mobile transients, adults and juveniles of a variety of species, move among beds with uncertain fidelity, as in the case of striped bass and bluefish (Harding and Mann, 2001). Another example of a resident species is naked gobies (Gobiosoma bosc). Naked gobies are common on vegetated flats. They occur in the water column during flood tide and near the bottom at ebb flow, and concentrate on reefs (Murdy et al., 1997, p. 216). Larvae prey intensely on copepods in the mesozooplankton community and are prey of juvenile striped bass. The larvae are among the most abundant in mesohaline areas of Bay tributaries in summer, ranking second in abundance only to bay anchovy larvae. They have been

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

shown to settle on the Flag Pond bed at consistently high rates, at rates that surpass coral reef and temperate fishes to suggest their ecological importance in estuarine trophic interactions (Breitburg, 1999). Another example of transient species are spot (Leiostomus xanthurus), the most abundant demersal fish in the Bay. These transient adults concentrate and forage around reefs in depths of 6e10 m, and favor muddy areas (Homer and Mihursky, 1991; Murdy et al., 1997). A coastal-ocean species, spot spawn outside the Bay in late fall and winter and enter the Bay in late spring to late fall. In spring, the planktivorous larvae, juveniles, and adults are distributed in various age classes throughout the Bay and tributaries. Larvae are most abundant in brackish tidal creeks in AprileMay and juveniles feed on small benthic invertebrates (copepods, polychaetes, and small bivalves) before most leave estuaries in fall. Spot appear to regulate prey densities of benthic communities, to structure microdistributions, and to play a key role in trophic dynamics as the prey of striped bass, weakfish, bluefish, and people. Heterogeneous, heterotrophic oyster beds positioned in the path of tidal flows attract biological activity that couple primary production into food webs. From their studies, Lenihan et al. (2001) have suggested an oyster bed-based food web for fishes and invertebrates, where oysters, mussels, crabs and shrimp are at the base. Oysters filter small diatoms, bacteria, and detritus from the water column, as do the associated filter feeders such as barnacles, tunicates, hydroides, bryozoans, sponges, and other lamellibranchs, transferring pelagic production to the benthos. Oysters and their community deposit organic-rich feces and pseudofeces (biodeposits) at high rates, along with algae species, detritus, and bacteria. When oysters die, their calcium carbonate shell is deposited and provides shelter for some and new substrate for colonizing young oysters. Crabs, fishes and birds are among the numerous predators of oysters, with blue crabs being major predators of juvenile oysters, especially when oyster densities are high (Eggleston, 1990). And species of decapods and fish occur more abundantly over oyster beds than adjacent sandflats (Posey et al., 1999). The abundance of xanthid crabs (Panopeus herbstii and Eurypanopeus depressus) that inhabit the intertidal North Carolina oyster reefs seek refuge in oyster shells, the former exploiting the subsurface stratum and the latter exploiting the surface shell clusters (Meyer, 1994). In the Gulf of Mexico, decapod assemblages associated with oyster beds form distinct populations from those in seagrass and marsh edge habitat (Glancy et al., 2003). Thus, oyster beds couple seasonal primary production and primary consumers to numerous estuarine feeders including various fishes, potentially influencing energy transfer efficiencies and community metabolism.

129

Oyster beds contribute to pelagic system connectivities. The fecundity of reproducing oysters in summer months places their larvae in an important time and location for trophic web connectance in the water column. Oysters spawn numerous gametes, 40e50 mm (the size of a clay particle) into the water column. In less than three weeks of development, these maturing larvae feed on micro-algae as they grow (to !300 mm) and change location by estuarine transport, a time when a diverse array of metazoan suspension feeders (heterotrophic nanoflagellates and micro-heterotrophs) are in the water and are actively feeding. As oyster larvae are consumed by fish larvae, and numerous epifaunal suspension feeders (Andrews, 1979; Kennedy, 1996b), larvae connect micro-autotrophs to secondary consumers in the micro-pelagic estuarine food web. Zooplantivores include the larvae and juvenile stages of several very abundant fishes that potentially fed on concentrations of oyster larvae and other reef-associated zooplankton. Critical links may be formed through spawning pulses and life history timing, when phytoplankton concentrations are high and oyster larvae are abundant and actively feeding. These links may be important to small and developing fishes in summer months when juvenile filter-feeding fishes (e.g., Atlantic menhaden) make up a substantial biomass (Cross et al., 1975), when bay anchovy (Anchoa mitchilli) larval densities reach up to 100 mÿ3 (MayeSeptember), and adult bay anchovy biomass is at a peak (JuneeJuly) (Rilling and Houde, 1999). 4.5. Connectities to landscape functions A key component of trophic dynamics in marine ecosystems is the rate at which large marine organisms converge into limited areas (Schneider, 1995). The types, quality and spatial arrangements of habitat patches within a landscape influence the distribution and abundance of populations (Eggleston, 1999). The many distinct beds provide options for species to hide, forage, and seek opportunities, and juveniles can disperse and improve survival options by means of hydrologic corridors. However, some species are physiologically constrained by salinity zones and do not penetrate into mesohaline or brackish water, and others (e.g., anadromous fish) migrate through tidal corridors that cross several salinity zones (Carriker, 1967; Patrick, 1994; Bulger et al., 1993). The complex oyster reef structure crosses several salinity zones to substantially increase fish biomass and density (Charbonnel et al., 2002). Increased habitat heterogeneity in the system that oysters created could augment energy transfer efficiencies, and oyster bed redundancy could add optional choices in species survival. By segregating uses among reefs, eelgrass beds, mud flats, and marshes during summer’s peak biological

130

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

activity, feeding opportunities are enhanced for dozens of abundant benthic and demersal fishes. Abele (1974) found that the number of substrates is the most important factor in determining the number of decapod crab species present, probably because each species can make differential use of each substrate. Use can be divided spatially and temporally within and between habitat types, day and night, seasons, slack, low and high tides, and environmental variables such as temperature and salinity. For example, blue crabs move to mud flats for molting (Wolcott and Hines, 1990), to oyster beds for feeding, and into tidal channels and Bay waters for reproduction, thus using of a variety of habitats. Mud crabs (Panopeus sp) forage on and around oyster beds. Sheepshead (Archosargus probatocephalus) enter brackish water and move to oyster beds to feed on oysters, mussels, and barnacles, and their young inhabit grassy flats before dispersing to oyster beds to feed (Murdy et al., 1997). The abundant sheepshead minnow (Cyprinodon variegatus) that frequent shallow flats, marshes and tidal ponds in summer and retreats in winter to channels or burrows in silt in marsh ponds, feeds on reefs at flood tide (Bahr and Lanier, 1981; Murdy et al., 1997). Tautog (Tautoga onitis) and cunner (Tautogolabrus adspersus) use eelgrass beds or macroalgae beds seasonally by day and reefs (or other hard protective substrate) by night and perennially in winter (Auster, 1989). In all cases, change in current speed and direction can result in small-scale shifts in the distribution and vulnerability of prey. Areas exposed to currents can become prey refuges until velocity increases and fish segregate. When tidal current direction shifts again, prey refuges again become available. And some year-round, resident Bay species such as gobies use channels, shallow water flats, and oyster beds that change with season. The small (52 mm) seaboard goby (Gobiosoma ginsburgi), the most abundant goby in open waters, is a year round Bay resident (Murdy et al., 1997, p. 217). In spring to autumn, it typically occurs on oyster reefs and deeper flats, spawning on dead shells and feeding on small crustaceans before retreating to channels in winter. The green goby (Microgobius thalassinus), also a year round resident, frequents mud and oyster habitat, being associated with the sponge (Microciona prolifera), then in winter retreats to channels and channel edges. The Bay’s matrix of seascape habitats adjacent to channels may have provided other important functions. An estuarine front is created by lighter water moving from the shoal into denser tidal channel water, and interacting near the edge of shoals to form strong lateral density gradients (Sarabun, 1993). Lateral shear fronts appear most prominently after ebb at slack tide, when the axial channel waters attain greater velocities than those in shoals, occurring with alterations in stratification and with pycnocline depth to give rise to a strong

vertical convergence and up-welling (Tyler and Seliger, 1989, p. 207). This up-welled nutrient-rich water increases phytoplankton concentrations consumed by fishes and influencing their distribution, as in the case of juvenile menhaden (Friedland et al., 1996). Beds distributed on shoals along corridors may also increase swimming efficiencies for fish. Fish have complex muscular architecture and locomotion strategies that minimize energy expenditure (Liao et al., 2003). Many species spend most of their time cruising only within a restricted area, such as a territory or a feeding range, and try to adopt some optimum speed in which the amount of energy per unit distance covered is minimal. The matrix of seascape habitats and estuarine fronts create advantages that might aid estuarine fishes along their migratory paths to spawning, feeding, and nursery areas of corridor systems. Striped bass, for example, use tidal channels in Tangier Sound area to reach their major spawning area in Nanticoke River (Richkus et al., 1994, p. 157).

5. Conclusion Historical distributions of oyster beds provide a spatial context for relating modern science and landscape ecology to estuarine function. Oyster beds, as spatial nodes of biological activity attractive to estuarine species seeking food, shelter, and rest, couple benthic heterotrophic activity to intense predator-prey interactions. Historic surveys carried out when fisheries production in the Bay was high provide evidence for considering the oysters’ connectivity to the Chesapeake Bay system. New knowledge of temporal pulses, habitat nodes, and food web linkages at increasing hierarchical scales suggest connections at the landscape scale. However, many questions still remain about application of historical spatial data to present day findings. For example: What role does variable pulses of spawning over numerous beds along a corridor play during fish migrations and larval development? What hydrologic structure is created over and around beds, between beds, and across the oyster reef habitat? Do hydrologic corridors assist species at the scale of individual beds, and what bed size and numbers of corridors optimize species recruitment, dispersion, and retention? What spatial arrangement (reef location, size, and shape) and scale might best influence the distribution and abundance of estuarine fish populations? How did historical oyster beds influence erosion and sedimentation favorable to sea grasses, marshes, and shoreline stability? And how did the location of the beds and the distribution of filter-feeding oysters influence delivery of detritus from land, water clarity, water column mixing, and summer time anoxia?

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

In 1884, Maryland’s Oyster Commission warned, ‘‘Owing to the great extent of the oyster beds in the bay, and their immense annual production, it may be some years before there is an oyster famine, but sooner or later it is coming, unless there is a radical change in some of the present phases of the business’’ (p. 24). What lesson might this resource warn of over-exploitation of other abundant natural resources? Of greatest concern is the environmental debt inherited from the lost role the abundance of oysters played in the ecosystem. Modern studies have considered the impact of dredging on long-term dynamics of oysters and reef system (Rothschild et al., 1994), and long-term impacts might relate to the example of Wadden Sea. In 1850s, Mo¨bius (1883, p. 721) considered oyster beds a bioco¨nose, a community ‘‘richer in all kinds of animal life than any other portion of the sea bottom.’’ The oyster bottom he studied has since disappeared, replaced today by a muddy bottom dominated by polychaetes and mussel banks (Reise, 1982). In particular, there is organic enrichment, intensified erosion, expansion of mussel beds, species impoverishment, increased polychaete abundance; and bottom trawling may be a contributing factor (Reise et al., 1989). Could such changes be affecting the Chesapeake Bay and its fisheries?

Acknowledgements Much appreciation is given to David Secor for the invitation to the ERF Estuarine Symposium and for his helpful review and editing of this manuscript. I also wish to thank Helen Woods, William Hargis, Dexter Haven, and Maynard Nichols of Virginia Institute Marine Science for their contributions, to Carleton Ray (University of Virginia) for his review, and Robert L. Smith for graphics.

References Abele, L.G., 1974. Species diversity of decapod crustaceans in marine habitats. Ecology 55, 156e161. Andrews, J.D., 1951. Seasonal patterns of oyster setting in the James River and Chesapeake Bay. Ecology 32 (4), 752e758. Andrews, J.D., 1979. Pelecypods and lesser classes. In: Giese, A.C., Pearse, J.S. (Eds.), Reproduction of Marine Invertebrates. Academic Press, New York, pp. 293e341. Andrews, J.D., 1983. Transport of bivalve larvae in James River, Virginia. Journal Shellfish Research 3 (1), 29e40. Auster, P.J., 1989. Species Profiles: Life Histories and Environmental Requirements of Coastal Fishes and Invertebrates: North and MidAtlantic. Tautog and Cunner. Biological Report 82(11.105) TR EL-82-4, U.S. Fish and Wildlife Service, Washington, DC. Bahr Jr., L.M., 1974. Aspects of the Structure and Function of the Intertidal Oyster Reef Community in Georgia. Dissertation

131

submitted to the Graduate Faculty, University Georgia, Athens, Georgia. Bahr Jr., L.M., Lanier, W.P., 1981. The Ecology of Intertidal Oyster Reefs of the South Atlantic Coast: A Community Profile. FWS/ OBS-81/15, Office of Biological Services, United States Fish and Wildlife Service, Washington, DC. Baird, S.F., 1887. Letter of Transmittal. The Fisheries and Fishery Industries of the United States. Section V, History and Methods of the Fisheries, Volume II, pp. V11-. United States Commission of Fish and Fisheries, Government Printing Office, Washington, DC. Boicourt, W.C., Kuzmic, M., Hookins, T.S., 1999. The inland sea: circulation of Chesapeake Bay and the Northern Adriatic. In: Ecosystems at the Land-Sea Margin: Drainage Basin to Coastal Sea. Coastal and Estuarine Studies, 55. American Geophysical Union, Washington, DC, pp. 81e129. Boon III, J.D., 1975. Tidal discharge asymmetry in a salt marsh drainage system. Limnology and Oceanography 20 (1), 71e80. Breitburg, D.L., 1999. Are three-dimensional structure and healthy oyster populations the keys to an ecologically interesting and important fish community? In: Luckenbach, M.W., Mann, R., Wesson, J.A. (Eds.), Oyster Reef Habitat Restoration: A Synopsis and Synthesis of Approaches. Proceedings from the Symposium, Williamsburg, Virginia, April 1995. Virginia Institute of Marine Science, Gloucester, Virginia, pp. 239e250. Breitburg, D.L., Palmer, M.A., Loher, T., 1995. Larval distributions and the spatial patterns of settlement of an oyster reef fish: responses to flow and structure. Marine Ecology Progress Series 125, 45e60. Brooks, W.K., 1891. The Oyster. The Johns Hopkins University Press, Baltimore. Republished in 1996. Bulger, A.J., Hayden, B.P., Monaco, M.E., Nelson, D.M., McCormick-Ray, M.G., 1993. Biologically-based estuarine salinity zones derived from a multivariate analysis. Estuaries 16 (2), 311e 322. Butman, C.A., Frechette, M., Geyer, W.R., Starczark, V.R., 1994. Flume experiments on food supply to the blue mussel Mytilus edulis L. as a function of boundary-layer flow. Limnology and Oceanography 39 (7), 1755e1768. Carriker, M.R., 1967. Ecology of estuarine benthic invertebrates: a perspective. In: Lauff, G.H. (Ed.), Estuaries. AAAS, Washington, DC, pp. 442e487. Carter, H.H., Pritchard, D.W., 1988. Oceanography of Chesapeake Bay. In: Kjerfve, B. (Ed.), Hydrodaynamics of Estuaries, II, Estuarine Case Studies. CRC Press, Inc., Boca Raton, pp. 1e16. Charbonnel, E., Serre, C., Ruitton, S., Harmelin, J.-G., Jensen, A., 2002. Effects of increased habitat complexity on fish assemblages associated with large artificial reef units (French Mediterranean Coast). ICES Journal of Marine Science 59, S208eS213. Cox, C., Mann, R., 1992. Temporal and spatial changes in fecundity of eastern oysters, Crassostrea virginica (Gmelin, 1791) in the James River, Virginia. Journal of Shellfish Research 11 (1), 49e54. Cross, F.A., Willis, J.N., Hardy, L.H., Jones, N.Y., Lewis, J.M., 1975. Role of juvenile fish in cycling of Mn, Fe, Cu, and Zn in a coastalplain estuary. In: Cronin, L.E. (Ed.), Estuarine Research, I. Academic Press, Inc., New York, pp. 45e63. Dame, R.F., 1993. The role of bivalve filter feeder material fluxes in estuarine ecosystems. In: Dame, R.F. (Ed.), Bivalve Filter Feeders in Estuarine and Coastal Ecosystems Processes. NATO ASI Series vol. G 33. Springer-Verlag, Berlin, Heidelberg, pp. 245e 269. Dame, R.F., 1996. Ecology of Marine Bivalves. An Ecosystem Approach. CRC Press, Boca Raton. Dame, R., Childers, D., Koepfler, E., 1992. A geohydrologic continuum theory for the spatial and temporal evolution of marsh-estuarine ecosystems. Netherlands Journal of Sea Research 30, 63e72.

132

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

Dean, T.A., 1981. Structural aspects of sessile invertebrates as organizing forces in an estuarine fouling community. Journal of Experimental Marine Biology and Ecology 53, 163e180. DeAlteris, J.T., 1988. The geomorphic development of wreck shoal, a subtidal oyster reef of the James River, Virginia. Estuaries 11 (4), 240e249. Dyer, K.R., 1977. Lateral circulation effects in estuaries. In: Estuaries, Geophysics, and the Environment. National Academy of Sciences, Washington, DC, pp. 22e29. Dyer, K.R., 1989. Estuarine flow interaction with topography lateral and longitudinal effects. In: Neilson, B.J., Kuo, A., Brubaker, J. (Eds.), Estuarine Circulation. The Humana Press, Inc., Clifton, New Jersey, pp. 39e59. Earll, R.E., 1887. Maryland and its fisheries. The Fisheries and Fishery Industries of the United States. Section V, History and Methods of the Fisheries, vol. II. United States Commission of Fish and Fisheries, Government Printing Office, Washington, DC, pp. 421e 464. Eggleston, D.B., 1990. Foraging behavior of the blue crab, Callinectes sapidus, on juvenile oysters, Crassostrea virginica: effects of prey density and size. Bulletin of Marine Science 46 (1), 62e82. Eggleston, D.B., 1999. Application of landscape ecological principles to oyster reef habitat restoration. In: Luckenbach, M.W., Mann, R., Wesson, J.A. (Eds.), Oyster Reef Habitat Restoration: A Synopsis and Synthesis of Approaches. Virginia Institute of Marine Science, VIMS Press, pp. 213e227. Forman, R.T.T., Godron, M., 1986. Landscape Ecology. John Wiley & Sons, New York. Friedland, K.D., Ahrenholz, D.W., Guthrie, J.F., 1996. Formation and seasonal evolution of Atlantic Menhaden Juvenile Nurseries in coastal estuaries. Estuaries 19 (1), 105e114. Friedricks, C.T., Lynch, D.R., Aubry, D.G., 1992. Velocity asymmetries in frictionally-dominated tidal embayments: longitudinal and lateral variability. In: Prandle, D. (Ed.), Dynamics and Exchanges in Estuaries and the Coastal Zone. Coastal and Estuarine Studies 40. American Geophysical Union, Washington, DC, pp. 277e308. Funderburk, S.L., Mihursky, J.A., Jordan, S.J., Riley, D. (Eds.), 1991. Habitat Requirements for Chesapeake Bay Living Resources, second ed. Chesapeake Research Consortium, Inc., Solomons, Maryland. Galtsoff, P.S., 1964. The american oyster Crassostrea virginica gmelin. Fishery Bulletin 64, 1e480. Glancy, T.P., Frazer, T.K., Cichra, C.E., Lindberg, W.J., 2003. Comparative patterns of occupancy by decapod crustaceans in seagrass, oyster, and marsh-edge habitats in a Northeast Gulf of Mexico Estuary. Estuaries 26 (5), 1291e1301. Gourlay, M.R., 1996. Wave set-up oncoral reefs. 2. Sep-up on reefs with various profiles. Coastal Engineering 28, 17e55. Grave, C., 1901. The oyster reefs of North Carolina: a geological and economic study. The Johns Hopkins University Circulars 151, 1e9. Haas, L.W., 1977. The effect of the spring-neap tidal cycle on the vertical salinity structure of the James, York and Rappahannock Rivers, Virginia, U.S.A. Estuarine and Coastal Marine Science 5, 485e496. Harding, J.M., Mann, R., 2001. Diet and habitat use by bluefish, Pomatomus saltatrix, in a Chesapeake Bay Estuary. Environmental Biology of Fishes 60, 401e409. Hargis Jr., W.J., 1999. The evolution of the Chesapeake oyster reef system during the holocene epoch. In: Luckenbach, M.W., Mann, R., Wesson, J.A. (Eds.), Oyster Reef Habitat Restoration: A Synopsis and Synthesis of Approaches. Virginia Institute of Marine Science, Gloucester Point, VA, pp. 5e23. Haven, D.S., Whitcomb, J.P., 1983. The origin and extent of oyster reefs in the James River, Virginia. Journal of Shellfish Research 3 (2), 141e151. Haven, D.S., Hargis, W.J., Kendal, P.C., 1978. The Oyster Industry of Virginia: Its Status, Problems and Promise. VIMS Special Papers in

Marine Science, 4. Virginia institute of Marine Science, Gloucester Point, VA. Hedgpeth, J.W., 1953. An introduction to the zoogeography of the Northwestern Gulf of Mexico with reference to the invertebrate fauna. Publications of the Institute of Marine Science 3 (1), 107e 224. University of Texas, Port Aransas, Texas. Homer, M.L., Mihursky, J.A., 1991. Spot. In: Funderburk, S.L., Mihursky, J.A., Jordan, S.J., Riley, D. (Eds.), Habitat Requirements for Chesapeake Bay Living Resources, second ed. Chesapeake Research Consortium, Inc., Solomons, Maryland, pp. 11-1-19. Ingersoll, E., 1887. Part XX. The Oyster, Scallop, Clam, Mussel, and Abalone Industries. 1. The Oyster Industry. 1. Introduction, Defining American Oysters. The Fisheries and Fishery Industries of the United States. Section V, History and Methods of the Fisheries, vol. II, with Letters of Transmittal. United States Commission of Fish and Fisheries, Government Printing Office, Washington, DC, pp. 507e605. Jumars, P.A., Nowell, A.R.M., 1984. Fluid and sediment dynamic effects on marine benthic community structure. American Zoology 24, 45e55. Kech, R., Mauerer, D., Watling, L., 1973. Tidal stream development and its effect on the distribution of the American oyster. Hydrobiologia 42, 369e379. Kennedy, V.S., 1996a. Biology of larvae and spat. In: Kennedy, V.S., Newell, R.I.E., Eble, A.F. (Eds.), The Eastern Oyster Crassostrea Virginica. Maryland Sea Grant book, College Park, Maryland, pp. 371e421. Kennedy, V.S., 1996b. The ecological role of the eastern oyster, Crassostrea virginica, with remarks on disease. Journal of Shellfish Research 15 (1), 177e183. Kennedy, V.S., Sanford, L.P., 1999. Characteristics of relatively unexploited beds of the eastern oyster, Crassostrea virginica, and early restoration programs. In: Luckenbach, M.W., Mann, R., Wesson, J.A. (Eds.), Oyster Reef Habitat Restoration: A Synopsis and Synthesis of Approaches. Proceedings from the Symposium, Williamsburg, Virginia, April 1995. Virginia Institute of Marine Science, Gloucester, Virginia, pp. 25e46. Keough, M.J., 1984. Effects of patch size on the abundance of sessile marine invertebrates. Ecology 65 (2), 423e437. Larsen, P.F., 1976. Patterns of Distribution of Estuarine Organisms and Their Response to a Catastrophic Decrease in Salinity. The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System. The Chesapeake Research Consortium, Inc. Nov. CRC Publication #54. Johns Hopkins Press, Baltimore. Larsen, P.F., 1985. The benthic macrofauna associated with the oyster reefs of the James River Estuary, Virginia, U.S.A. International Revue ges. Hydrobiological 70 (6), 797e814. Le Couturier, M.N., Grochowski, N.T., Heathershaw, A., Oikonomou, E., Collins, M.B., 2000. Turbulent and macroturbulent structures developed in the benthic boundary layer downstream of topographic features. Estuarine, Coastal and Shelf Science 50, 817e833. Lenihan, H.S., 1999. Physical-biological coupling on oyster reefs: how habitat structure influences individual performance. Ecological Monograph 69 (3), 251e275. Lenihan, H.S., Peterson, C.H., Byers, J.E., Grabowski, J.H., Thayer, G.W., Colby, D.R., 2001. Cascading of habitat degradation: oyster reefs invaded by refugee fishes escaping stress. Ecological Applications 11 (3), 764e782. Liao, J.C., Beal, D.N., Lauder, G.V., Triantafyllou, M.S., 2003. Fish exploiting vortices decrease muscle activity. Science 302, 1566e1569. Mann, R., 1988. Distribution of bivalve larvae at a frontal system in the James River, Virginia. Marine Ecological Progress Series 50, 29e44. Manning, J.H., Whaley, H.H., 1954. Distribution of oyster larvae and spat in relation to some environmental factors in a tidal estuary. Proceedings of the National Shellfisheries Association 45, 56e65.

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134 McCormick-Ray, M.G., 1998. Oyster reefs in 1878 seascape pattern e Winslow revisited. Estuaries 21 (4B), 784e800. Md. Oyster Comm., 1882. Report of the Maryland Oyster Commission. James Young, State Printer, Annapolis, 183 pp. Meyer, D.L., 1994. Habitat partitioning between the Xanthid crabs Panopeus herbstii and Eurypanopeus depressus on intertidal oyster reefs (Crassostrea virginica) in Southwestern North Carolina. Estuaries 17 (3), 674e679. Mixon, R.B., 1985. Stratigraphic and Geographic Framework of Upper Cenozoic Deposits in the Southern Delmarva Peninsula, Virginia and Maryland. U.S. Geological Survey Professional Paper 1067-G. Mo¨bius, K., 1883. The Oyster and Oyster Culture. XXVII. Report of the Commissioner of the United States Commission of Fish and Fisheries, 1880, Spencer F. Baird, Commissioner. U.S. Government Printing Office, Washington, DC. Moore, H.F., 1910. Condition and Extent of the Oyster Beds of James River, Virginia. Bureau of Fisheries, Doc #729, Dept. of Commerce and Labor. Government Printing Office, Washington, DC. Murdy, E.O., Birdsong, R.S., Musick, J.A., 1997. Fishes of Chesapeake Bay. Smithsonian Institution Press, Washington, DC. Newell, R.I.E., 1988. Ecological Changes in Chesapeake Bay: Are They the Result of Overharvesting the American Oyster, Crassostrea virginica? In: Understanding the Estuary: Advances in Chesapeake Bay Research. Proceedings of a Conference, 29e31 March l988, Baltimore Maryland. Chesapeake Research Consortium Publication 129, Solomons MD, pp. 536e546. Nichols, M.M., 1977. Response and recovery of an estuary following a river flood. Journal of Sedimentary Petrology 47 (3), 1171e1186. Nichols, M.M., Johnson, G.H., Peebles, P.C., 1991. Modern sediments and facies model for a microtidal coastal plain estuary, the James Estuary, Virginia. Journal of Sedimentary Petrology 61 (6), 883e 889. Norris, R.M., 1953. Buried oyster reefs in some Texas bays. Journal of Paleontology 27 (4), 569e576. Nowell, A.R.M., Jumars, P.A., Eckman, J.E., 1981. Effects of biological activity on the entrainment of marine sediments. Marine Geology 42, 133e153. Oertel, G.F., Foyle, A.M., 1995. Drainage displacement by sea-level fluctuation at the outer margin of the Chesapeake Seaway. Journal of Coastal Research 11, 583e604. Oyster Commission, 1884. Report of the Oyster Commission of the State of Maryland. January. Annapolis, MD. Patrick, R., 1994. Rivers of the World. John Wiley and Sons, New York. Peterson, C.H., Grabowshi, J.H., Powers, S.P., 2003. Estimated enhancement of fish production resulting from restoring oyster reef habitat: quantitative valuation. Marine Ecology Progress Series 264, 249e264. Posey, M.H., Alphin, T.D., Powell, C.M., 1999. Use of oyster reefs as habitat for epibenthic fish and decapods. In: Luckenbach, M.W., Mann, R., Wesson, J.A. (Eds.), Oyster Reef Habitat Restoration: A Synopsis and Synthesis of Approaches. Proceedings from the Symposium, Williamsburg, Virginia, April 1995. Virginia Institute of Marine Science, Gloucester, Virginia, pp. 229e237. Pritchard, D.W., 1952. Distribution of Oyster Larvae in Relation to Hydrographic Conditions. Proceedings of the Gulf and Caribbean Fisheries Institute, Fifth Annual Session, Miami Beach, Nov. University of Miami Lab, Coral Gables. Pritchard, D.W., 1989. Estuarine classification e a help or a hindrance. In: Neilson, B.J., Kuo, A., Brubaker, J. (Eds.), Estuarine Circulation. The Humana Press, Inc., Cliffton, NJ, pp. 1e38. Reise, K., 1982. Long-term changes in the macrobenthic invertebrate fauna of the Wadden Sea: are polychaetes about to take over? Netherlands Journal of Sea Research 16, 29e36.

133

Reise, K., Herre, E., Sturm, 1989. Historical changes in the benthos of the Wadden Sea around the Islandn of Sylt in the North Sea. Helgola¨nder Meeresuntersuchungen 43, 417e433. Richkus, W.A., Jacobson, P., Ranasinghe, A., Shaughnessy, A., Chaillou, J., Kazyak, P, DeLisle, C., Batiuk, R., 1994. BasinSpecific Characterizations of Chesapeake Bay Living Resources Status. U.S. Environmental Protection Agency for the Chesapeake Bay Program, Annapolis. Rilling, G.R., Houde, E., 1999. Regional and temporal variability in distribution and abundance of Bay Anchovy (Anchoa mitchilli) eggs, larvae, and adult biomass in the Chesapeake Bay. Estuaries 22 (4), 1096e1109. Rothschild, B.J., Ault, J.S., Goulletquer, P., He´ral, M., 1994. Decline of the Chesapeake Bay oyster population: a century of habitat destruction and overfishing. Marine Ecology Progress Series 111, 29e39. Ruzecki, E.P., Hargis Jr., W.J., 1989. Interaction between circulation of the estuary of the James River and transport of oyster larvae. In: Neilson, B.J., Kuo, A., Brubaker, J. (Eds.), Estuarine Circulation. The Humana Press, Inc., Clifton, New Jersey, pp. 255e278. Sarabun Jr., C.C., 1993. Observations of a Chesapeake Bay Tidal Front. Estuaries 16 (1), 68e73. Schneider, D.C., 1995. Spatial and temporal scaling of energy flux through populations of marine nekton. In: Skjoldal, H.R., Hopkins, C., Erikstad, K.E., Leinaas, H.P. (Eds.), Ecology of Fjords and Coastal Waters. Elsevier Science B.V, Amsterdam, pp. 419e427. Secretary of the Interior, 1866. Statistics of the United States in 1860 of the Eight Census. Government Printing Office, Washington, DC. Seliger, H.H., Boggs, J.A., Rivkin, R.B., Biggley, W.H., Aspden, K.R.H., 1982. The transport of oyster larvae in an estuary. Marine Biology 71, 57e72. Shumway, S.E., 1996. Natural environmental factors. In: Kennedy, V.S., Newell, R.I.E., Eble, A.F. (Eds.), The Eastern Oyster Crassostrea Virginica. Maryland Sea Grant Book, College Park, Maryland, pp. 467e513. Smith, H.M., 1913. Oysters: The world’s most valuable water crop. The National Geographic 24 (3), 260e275. Smith, G.F., Roach, E.B., Bruce, D.G., 2003. The location, composition, and origin of oyster bars in Mesohaline Chesapeake Bay. Estuarine, Coastal and Shelf Science 56, 391e409. Stenzel, H.B., 1971. Oysters. Treatise on Invertebraate Paleontology. Part N, Bivalvia. The University of Kansas and the Geological Society of America, Lawrence, Kansas. Sternberg, R.W., 1968. Friction factors in tidal channels with differing bed roughness. Marine Geology 6, 243e260. Tyler, M.A., Seliger, H.H., 1989. Time scale variations of estuarine stratification parameters and impact on the food chains of the Chesapeake Bay. In: Neilson, B.J., Kuo, A., Brubaker, J. (Eds.), Estuarine Circulation. The Humana Press, Inc., Clifton, New Jersey, pp. 201e233. Ulanowicz, R.E., Tuttle, J.H., 1992. The trophic consequences of oyster stock rehabilitation in Chesapeake Bay. Estuaries 15 (3), 298e306. Vetter, E.W., 1994. Hotspots of benthic production. Nature 372, 47. Wells, H.W., 1961. The fauna of oyster beds, with special reference to the salinity factor. Ecological Monographs 31, 239e266. Widdows, J., Brinsley, M.D., Salkeld, P.N., Elliott, M., 1998. Use of annual flumes to determine the influence of current velocity and bivalves on material flux at the sediment-water interface. Estuaries 21 (4A), 552e559. Wildish, D.J., Kristmanson, D.D., 1979. Tidal energy and sublittoral macrobenthic animals in estuaries. Journal of Fisheries Research Board of Canada 36, 1197e1206. Wildish, D.J., Kristmanson, D.D., 1985. Control of suspension feeding bivalve production by current speed. Helgolander Meeresuntersunchungen 39, 237e243.

134

J. McCormick-Ray / Estuarine, Coastal and Shelf Science 64 (2005) 119e134

Winslow, F., 1882. Methods and Results. Report of the Oyster Beds of the James River, Va. and of Tangier and Pocomoke Sounds, Maryland and Virginia. U.S. Coast and Geological Survey, Appendix No. 11. U.S. Government Printing Office, Washington, DC. Wolcott, T.G., Hines, A.H., 1990. Ultrasonic telemetry of small-scales movements and microhabitat selection by molting blue crabs (Callinectes sapidus). Bulletin of Marine Science 46 (1), 83e94.

Wright, L.D., Prior, D.B., Hobbs, C.H., Byrne, R.J., Boon, J.D., Schaffner, L.C., Green, M.O., 1987. Spatial variability of bottom types in the lower Chesapeake Bay and adjoining estuaries and inner shelf. Estuarine, Coastal and Shelf Science 24, 765e784. Wright, L.D., Gammisch, R.A., Byrne, R.J., 1990. Hydraulic roughness and mobility of three oyster-bed artificial substrate materials. Journal of Coastal Research 6 (4), 867e878.