oyster reef habitat restoration: relationships between oyster …€¦ · 64-78 | west palm beach,...

I Journal of Coastal Research I SI 1 40 T 64-78 | West Palm Beach, Florida I Winter 2005

Oyster Reef Habitat Restoration:Relationships Between Oyster Abundanceand Community Development based onTwo Studies in Virginia and SouthCarolinaMark W. Luckenbacht, Loren D. Coent, P.G. Ross, Jr.§, and Jessica A. Stephentt

tVirginia Institute ofMarine Science

College of William andMary

P.O. Box 350Wachapreague, VA

23480, [email protected]

tMarine ResourcesResearch Institute

South CarolinaDepartment ofNatural Resources

P.O. Box 12559Charleston, SC 29422,

[email protected].

sc.us

§Virginia Institute ofMarine Science

College of William andMary

P.O. Box 350Wachapreague, VA

23480, [email protected]

ttMarine ResourcesResearch Institute

South CarolinaDepartment ofNatural Resources

P.O. Box 12559Charleston, SC 29422,

[email protected].

state.sc.us

ABSTRACT

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LUCKENBACH, M.W.; COEN, L.D.; ROSS, P.G. JR. and STEPHEN, JA., 2005. Oyster reef habitat res-toration: relationships between oyster abundance and community development based on two studies inVirginia and South Carolina. Journal of Coastal Research, SI(40), 64-78. West Palm Beach (Florida), ISSN0749-0208.

Most Atlantic and Gulf coast U.S. states with an oyster fishery have operated some form of oyoter reefenhancement program over the past 50 years. Although programs were initially only directed at oysterfisheries augmentation, recent emphasis has shifted to include the restoration of their ecological functions.Furthermore, many of these programs are managed by environmental organizations or state agencies nottraditionally involved in fisheries management or research, but rather in ecological restoration, monitoring,and/or environmental education. A simple assessment of shellfish meetings over the past five years, in-cluding the inaugural Restore America's Estuaries meeting from which this paper is derived, revealed morethan 300 presentations related to oyster restoration, with fewer than 25% focused solely on oyster fisheryrestoration. Unfortunately, many of those efforts lacked well-defined "success criteria," with progress oftenjudged using fisheries-based metrics ouch as market-sized (generally 75 mm or 3") oysters. Here we discussour findings as they relate to the value of alterative restoration metrics and associated success criteriausing data from two very different systems and approaches: one conducted in Virginia's lower ChesapeakeBay (Rappahannock River), based on data from a two-year program utilizing oubtidally constructed reefsof different reef "scale," and the other a long-term study in South Carolna focusing on intertidal reefs. Foreach system, we compared newly created reef structures, relating oyster abundance and size to residentspecies abundance and biodiversity over time. Our results revealed positive correlations between severalcommunity descriptors and the size and density of oysters on the reefs. Of the 15 significant (and b mar-ginaly insignificant) correlations observed out of a total of 78 examined across both studies, al but onewere positive. The exception was for epifaunal invertebrate diversity vs. oyster biomass on the Rappahan-nock reefs. Despite these numnerous positive correlations, none indicated that market-sized oysters are aprerequisite for supporting an abundant and diverse community. For example, intertidal oysters >75 mmin South Carolina typically make up <10% of all reef oysters, with a maximnum of 18%. Finally, until wehave a more thorough understanding of the interactions between individual species and the mechanismslinking oyster populations and reef community attributes, we propose that oyster abundancelsize structurebe used for assessments. Future studies need to develop and evaluate restoration progress using a combi-nation of standardized criteria that can be applied to reef success over a wide geographical range andsurrogate or indirect ecological measures (eg., filtering, habitat use).

ADDMIONAL INDEX WORDS: Ecological restoration, habitat, oysters, metrics, success criteria, South Car-olina, Virginia, intertidal, subtidal, reefs, Crassootrea virginica.

INTRODUCTION

Recognition of the important ecological role ofCrassostrea virginica (Eastern oyster) in many es-

04-0349 received 20 August 2004.

tuaries along the U.S. Atlantic and Gulf of Mexicocoasts (NEWELL, 1988; BREITBURG, 1999; LENIHAN,1996, 1999; LENIHAN et al, 1999; DAME, 1999; COEN

et al, 1999a; LUCKENBACH et al, 1999; COEN andLUCKENBACH, 2000) has fueled increased efforts to

Evaluating Success Criteria and Reef Development for Oyster Restoration

restore depressed oyster populations over the pastdecade since the workshop on oyster restoration in1995 at the Virginia Institute of Marine Science(LUCKENBACH et al, 1999). There is now evidencethat oysters can (or could at historical abundances)control phytoplankton abundance and alter estu-arine food webs by enhancing benthic-pelagic cou-pling (DAME et al., 1984, 2001; DAME and LIBES,1993; NEWELL, 1988; ULANowicz and TUTTLE, 1992;ROTHSCHILD et al., 1994). Indeed, there is an in-creasing recognition that top-down control of phy-toplankton abundance via oysters should be an im-portant part of overall strategies to improve waterquality in eutrophic estuaries (NEWELL, 1988;KAUFMAN and DAYTON, 1997; PETERSON and LuB-CHENCO, 1997; JACKSON et al., 2001). Moreover, oys-ters are quintessential "ecosystem engineers"(JoNEs et al., 1994; LENIHAN, 1999), constructingbiogenic habitats that provide refuges, nestingsites, and foraging grounds for a variety of resi-dent and transient species (LENrHAN and GRA-BOWSKI, 1998; BREITGURG, 1999; COEN et al, 1999b;EGGLESTON et al, 1999; HARDING and MANN, 1999;POSEY et al, 1999). Several studies have nowdemonstrated greater biodiversity associated withoyster reefs than with adjacent sedimentary hab-itats (POSEY et al, 1999; COEN and LUCKENBACH,2000; O'BEIRN et al, 2000). In fact, for many es-tuaries along the Mid-Atlantic and Gulf coasts ofthe U.S., oyster reefs are the primary source ofhard substrate, and as such they may supportunique assemblages of organisms. Further, thereis evidence that oyster reefs contribute signifi-cantly to enhanced production, not merely the con-centration of finfish and decapod crustaceans (PE-TERSON et al., 2003).

Over the past decade, the number of oyster res-toration projects along the U.S. Atlantic and Gulfof Mexico coasts has increased dramatically, large-ly in an effort to restore one or more of the poten-tially lost ecological services (see reviews above).Many of these projects are being conducted bystate and federal agencies not typically involved infisheries management, such as the Virginia De-partment of Environmental Quality, the SouthCarolina Department of Health and Environmen-tal Control, the National Oceanic and AtmosphericAdministration (NOAA) Restoration Center, theNOAA Coastal Services Center, and the U.S. ArmyCorps of Engineers. In addition, numerous non-governmental organizations and communitygroups (e.g, NY/NJ Baykeepers, Chesapeake BayFoundation, South Carolina's Oyster Restoration

and Enhancement Program (or SCORE) withSouth Carolina Coastal Conservation League andCoastal Conservation Association (CCA), NorthCarolina Coastal Federation, and Tampa Bay-watch) are actively involved in oyster reef resto-ration for ecological motives. Funding sources foroyster restoration have also included agencies andorganizations with environmental restorationagendas (e.g., NOAA's Community RestorationProgram and FishAmerica). One indication of thisenhanced level of restoration activity is the largenumber of papers presented by such groups on oys-ter restoration at recent meetings of the Interna-tional Conference of Shellfish Restoration, the Na-tional Shellfisheries Association, and at the Ma-rine Benthic Ecology meeting. A review of the pub-lished abstracts and program schedules for thosemeetings over the past five years and the inau-gural meeting of Restore America's Estuaries re-veals more than 300 presentations related to oys-ter restoration with fewer than 25% focused onoyster fishery restoration (LUCKENBACH, unpub-lished data).

Unfortunately, many of the projects referred toin the previous section have limited data, with fewresults published to date in the primary literature.In the absence of expressly stated success criteria(COEN and LUCKENBACH, 2000) and directed mon-itoring, the early success of oyster restoration pro-jects, unfortunately, tends to be judged based sole-ly on either the abundance of market-sized (typi-cally 75 mm or 3") oysters or fishery landings data,neither of which may be crucial to achieving moreecologically based restoration goals.

Previously, we (COEN and LUCKENBACH, 2000)stressed the importance of developing metrics forevaluating the specific goals of ecological restora-tion. It is clear from that earlier work that a viableoyster population is a critical component of a suc-cessful oyster reef restoration effort. However, itis not clear if harvestable quantities of market-sized (75 mm shell height (SH)) oysters are a crit-ical requisite for restoration success. In stateswhere minimum harvest sizes are regulated (e.g.,75 mm SH in Virginia and elsewhere) oysters maybe reproductively capable and populations sustain-able, with relatively low abundances of market-sized animals. Studies have now begun to dem-onstrate that not all of the "ecological services" ofoyster communities come only after the oyster pop-ulations are well established. In several recent re-views (COEN et al, 1999a, 1999b, 2000; COEN andLUCKENBACH, 2000; BREITBURG et al, 2000) we sug-

Journal of Coastal Research, Special Issue No. 40, 2005

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Luckenbach et al.

gested that oysters, although the key to a fullyfunctioning oyster reef, are not necessary to pro-vide many of the ecosystem services that, for ex-ample, artificial reefs provide, such as structureand refugia (BREITBURG, 1999; EGGLESTON et al.,1999; LEHNERT and ALLEN, 2002; GLANcY, 2003).Biogeochemical coupling benefits as measured inthe "CREEK" Project in South Carolina (DAME etal., 2000, 2001) showed that nekton feeding cou-pled nutrients around structured sites without liveoysters. Hence, oysters may not be critical, initial-ly, in judging success and should not be used toimply failure early in the life of a restoration pro-gram.

Alternatively, as suggested by COFN et al.(1999a) and BREITBURG et al. (2000), large oystersand "mature" reefs may be critical to achievingboth fisheries enhancement and restoration goals.In discussing many of the challenges faced in at-tempting to meet fisheries rehabilitation and eco-logical restoration goals for oyster reefs, COEN andLUCKENBACH (2000) further stressed the impor-tance of developing meaningful success measuresand implementing rigorous monitoring programsto track progress towards those goals. Thus, to bet-ter evaluate the success of ecological restorationefforts, we need to develop a better understandingof the relationship between oyster populationstructure and abundance and any potential "eco-logical services" that we are seeking to restore.

In response to this need, we present the resultsfrom two studies conducted in different estuarieson the U.S. Atlantic coast. One study in the Rap-pahannock River, a mesohaline sub-estuary of theChesapeake Bay, is still ongoing and is addressingthe role of spatial scale (ranging from a few metersto several kilometers) on the development of oysterpopulations and associated fauna. The other study,conducted along the central coast of South Caro-lina, compared the development of oyster popula-tions and associated assemblages on constructedreefs to adjacent natural intertidal reefs over a six-year period between 1995 and 2001. Both studiesafford the opportunity to relate the reef-associatedassemblages of organisms to oyster densities andpopulation size structure over time. Our objectivein examining these relationships is to provide abasis for beginning to formulate metrics for res-toration success that reflect the biodiversity andhabitat goals of many projects and to make rec-ommendations for future work.

Figure 1. Experimental reef restoration sites in the Rap-pahannock River, Chesapeake Bay, Virginia.

METHODS

Rappahannock River, Virginia

Study Site and Reef Construction

This study was conducted at four sites in thelower portion of the Rappahannock River, Virgin-ia, USA, which is a tributary of the ChesapeakeBay (upriver-most site, Drumming Ground: N 37039.248', W 760 27.648' downriver-most site: MillCreek N 370 35.157', W 760 24.024', see Figure 1).Historically, this region of the Rappahannock wasa highly productive oyster harvesting area, withextensive natural reefs (HARGIs, 1999). The specif-ic sites chosen for the construction of reefs in thisstudy formerly supported viable oyster reefs thatthrough a combination of over-fishing, disease,and habitat degradation had all but disappeared.Reef bases were constructed in August 2000 byplacing shell piles in arrays as shown in Figure 2.Core material for individual mounds was com-prised of surf clam (Spisula solidissima) shell thatwas capped off with a veneer (generally 10-20 cm)of clean oyster shell. Materials were barged to thefour reef sites and deployed via a crane and bucketrig, creating "upside-down egg carton" shaped sub-tidal reefs elevated approximately 3 m above sea-bed and 1-2 m below the water surface at meanlow water (Figure 2). Reefs ranged in area, from


66


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Figure 2. Generalized aerial footprint of reefs denoting in-tra-reef locations. Each circle represents a mound approxi-mately 10 m diameter. Generalized side view of an individ-ual shell mound shown for each replicate reef mound at ar-row.

approximately 400 m2 to 8,000 m2. Intra-reef lo-

cations were designated in relation to distancefrom reef edge along longitudinal axes (Figure 2).A subsequent manuscript will address the devel-opment of oyster populations and associated com-munities in relation to scale. Here we present ourfindings relating the density and population struc-ture of oysters to the development of reef-associ-ated community assemblages. For more detail, seeLUCKENBACH and Ross (2003).

Sampling Methods

Standing stocks of oysters were estimated fromdiver-collected samples taken at all reefs. Fifty-one replicate 0.25 m x 0.25 m quadrates were hap-hazardly placed onto randomly-selected moundswithin ten reefs (number of samples partitioned byreef size, i.e., 5 of the 6, 7 of the 12 and 8 of the20 mounds for small, medium, and large "reefs,"respectively; see Figure 2 and LuCKENBACH andRoss, 2003, for details). One sample was collectedfrom each mound, as mounds were treated as rep-licates within a reef treatment, such that multiplereplicate samples were taken at the time of sam-pling (see Figure 2). All reef material was exca-vated to a depth of 10 cm by divers and transport-ed to the surface in fine mesh bags. All live oystersin each sample were counted and SH (longest lipto hinge linear distance, the standard measure foroyster) measured. Samples were collected in July2001, October 2001, and July 2002.

Figure 3. Inlet Creek study site in Charleston Harbor,South Carolina. See COEN et al., 1999b, and COEN and LucK-ENBACH, 2000, for additional details.

A sub-sample of 132 oysters covering the rangeof oyster SH encountered was measured for drytissue biomass from the October 2001 sample. Theshear number of oysters encountered prohibitedashing all oysters throughout the study, justifyingthe use of a regression equation to estimate bio-mass. Biomass values for oysters were computedfrom a regression of ash-free dry weight on shellheight [biomass (mg) = 0.007 X shell height (inmm)2'5 614, R2 = 0.8988, n = 132]. All sessile epi-fauna on the reef substrate or on the oysters inquadrat samples were identified to the lowestpractical taxon and reported as either densities(e.g., for barnacles and tunicates) or percent cover(e.g, for bryozoans and sponges).

Small resident mobile fishes and crustaceanswere sampled using substrate baskets embeddedin the reef. Thirty-centimeter diameter PVC pipewas cut into 15-cm lengths and one end coveredwith 1-mm plastic mesh. Three 5-cm diameterholes were cut along the midline of the PCV ringand covered with 1-mm mesh. Baskets were thenfilled with clean oyster shells similar to those usedin the reef construction and buried flush with thereef surface by divers. The mesh bottom and holesin the sides permitted the exchange of interstitialpore water with the surrounding reef, while thebasket allowed the retrieval of intact sampleswhich retained the more mobile reef residentssuch as blennies, gobies, and mud crabs. DuringApril 2001, a total of 189 baskets were deployed athaphazardly located positions on a subset of thereef crests (1 per randomly selected replicatemound; see above replicate allocation for the quad-rats) due to logistics and time constraints, versus


67

65 Luckenbach et al.

the alternative of randomly picking the exact spoton each subtidal reef, as we had no reason to thinkthe micro-location of a basket on a small moundwould yield any bias. Divers retrieved the abovereplicate baskets in July 2001 (n = 62), October2001 (n = 60), and July 2002 (n = 24) from allcombinations of reef locations. The small numberof samples retrieved during the last sampling pe-riod reflects loss of gear due to the erosive forcesduring the 15 months that the final baskets werein the field. In the laboratory, all motile organismsin the baskets were thoroughly rinsed over a 1-mmsieve mesh to remove all motile organisms, whichwere fixed in isotonic Normalin® and then trans-ferred to 70% ethanol. All organisms were lateridentified to the lowest practical taxon, enumer-ated, and, where appropriate, measured (decapodcrustaceans, carapace width, and finfish, totallength). Taxa such as amphipods and polychaeteswere not measured.

Transient fishes associated with the reefs weresampled using gill nets. Although nets were setduring 2001, only data collected during two sam-pling efforts in May and June 2002 were used foranalysis. As previously mentioned, we also usedoyster population data from this period for analy-ses. Nets were 9 m long by 3 m high and rigged tofish from the seabed up (i.e. sinking rigged net).Nets utilizing 6.3 cm and 7.5 cm stretch mesh wereused during 2002 and were randomly allocatedthroughout sampling periods. Anchored monofila-ment gill nets were deployed for 3 h on all reefsizes at both inner and outer reef locations whenapplicable. Sets were repeated so that all locationswere sampled with both mesh sizes during bothflood and ebb tidal cycles within sampling periods.Although the majority of gill net sampling oc-curred between dawn and dusk, one sample effortthat included all scale treatments was undertakenduring the night. Nets were randomly allocated tospecific locations witbin each region of the reefs.This resulted in over 200 individual sets (seeLUCKENBACH and Ross, 2003 for more details). Af-ter 3 hr, nets were retrieved and fish were iden-tified, enumerated, measured, and released ashort distance from the reefs. In some cases, dueto high catches, processing of samples had to beundertaken after all nets were harvested and tak-en to a remote location.

Statistical Analyses

Temporal patterns in oyster abundance and bio-mass, along with abundances of selected species

and community metrics, are presented graphicallyfor all sites combined. One-way ANOVAs wereused to test the effect of reef site on oyster abun-dance and biomass for July 2002 samples only (n= 4). Tukey's Multiple Comparisons were subse-quently utilized to elucidate reef site differences(SOKAL and ROHLF, 1981). Furthermore, fordata from this sample period, we tested for differ-ences between individual reefs (n = 10) indepen-dent of geographic location. Both analyses weremeant to provide some background regarding thegeneral oyster populations prior to subsequent cor-relation analyses that are undertaken at the in-dividual reef level. Oyster reefs were constructedin 2000, which resulted in missing oyster settle-ment for that year, so no measured settlement wasquantified until Fall 2001. We chose to use the2002 sampling only because it represented 2001recruitment and mortality, along with recruitmentand mortality through July 2002, therefore paint-ing a more appropriate picture of existing oysterpopulations. This is important because these werenew reefs just developing oyster populations dur-ing the course of this study. Size frequency datafor oysters from this same sampling date are pre-sented graphically by site.

Spearman product-moment correlation coeffi-cients related total oyster abundance, abundanceof age-class-two oysters, and biomass to the abun-dances and biomass of dominant reef-associatedspecies to selected community descriptors. Com-parisons included abundance and biomass (forribbed mussels (Guekinsia demissa) only) of dom-inant (based on measured abundance in thisstudy), reef-associated species in logical groups, aswell as total abundance, species richness, and di-versity (Shannon-Weiner Diversity Index) ofbroader taxonomic groupings. Broad functionalgroupings were (1) epifaunal invertebrates, (2) res-ident finfish, and (3) transient finfish. Dominantspecies/group specific analyses were (1) for at-tached epifauna, barnacles (Balanus spp.), (2) fordecapod crustaceans, mud crabs (Xanthidae), (3)for bivalves, ribbed mussels, (4) for resident fin-fish, skilletfish (Gobiesox strumosus), and (5) fortransient finfish, white perch (Morone american-us). For transient species, in addition to the dom-inant species, striped bass (Morone saxatilis) datawere included because of their management im-portance along the Atlantic seaboard. We deemedthese functional groups to be the most logical as-semblage that we were able to quantitatively sam-ple in this study.




Spearman correlations were computed usingmeans for individual reefs across intra-reef loca-tions for a given sampling period. For epifaunaland transient finfish assemblages, we analyzeddata from the Summer 2002 sampling period. Forthe resident finfish and crustaceans, we used datafrom the Fall 2001 sampling period because someof the later samples were lost during processing.We tested the null hypothesis that these correla-tion coefficients did not differ from zero using t-

tests (SoKAL and ROHLF, 1981). All data sets weretested for normality using the Kolmogorov-Smir-nov test (SAS Institute Inc., 1990) and homosce-dasticity using Hartley's Fm_ Test (SOKAL andROHLF, 1981). Many data sets did not meet theseassumptions, especially for equal variances.Therefore, Spearman's rank correlations were uti-lized for comparisons. All data analyses were car-ried out using SAS, except Hartley's F-Max testswhich were computed manually according to So-KAL and ROHLF (1981). A report (LuCKENBACH andRoss, 2003) and a subsequent manuscript have orwill address variations in relation to reef size andlocation within the reef.

Inlet Creek, South Carolina

Study Site and Background

The South Carolina studies were conducted inInlet Creek, a tributary adjacent to CharlestonHarbor, as part of a larger study examining thedevelopment of intertidal oyster reefs in relationto reef age and season at sites with differing ad-jacent development (COEN et at, 1999b). We alsocompared these intensively studied sites to nu-merous sampling sites from across the state. Forthe purpose of this overview, we focus only on thethree experimental reefs constructed in InletCreek (N 320 47.93', W 790 49.73') and the threeadjacent, natural reef areas (see Figure 3). The de-sign and construction of these reefs, as well as pre-liminary physical descriptions of the site, havebeen reported in detail in WENNER et al, 1996;COEN et al, 1999b; COEN and LUCKENBACH, 2000,so we present only a brief overview here. In Oc-tober 1994, three replicate 24-M2 experimentalreefs were constructed on an intertidal oyster flatwithin Inlet Creek. Each experimental reef wascomprised of 156 plastic trays (0.46 m x 0.31 m x0.11 m) filled with clean oyster shell and arrangedin a 6 x 26 array, with each reef paired with anadjacent natural reef of similar size (see Figure 2in COEN et al., 1999b). Here we discuss the results

for Inlet Creek only, the more undeveloped of thetwo sites at the time of study. Oyster samplingbegan on experimental reefs after initial recruit-ment in the late spring to early summer 1995,whereas resident sampling began earlier in March1995 (COEN et al, 1999a, 1999b; COEN and LucK-ENBACH, 2000). Natural oyster sampling in InletCreek started in 1997. Additional work includedtransients, disease, and environmental samplingduring the overall study from 1995-2001 (seeCOEN et alt 1999a, 1999b). However for this paper,only a portion of the overall dataset was used.

Sampling Methods

Resident fauna (defined here as those organismsremaining within the shell matrix when exposedat low tide) on the experimental reefs were sam-pled by removing three randomly selected "quad-rats" (= trays) sampled only once from each of thethree experimental reefs. We rinsed the materialon a 0.5-mm sieve and retained all organismscaught on the sieve. All oyster shell was thorough-ly sorted and all live oysters counted and mea-sured. For the natural oyster residents, we sam-pled using quadrates randomly placed on adjacentoyster reefs outside of the paired natural reef tominimize disturbance of other sampling. All organ-isms, including oysters, were excavated to a depthof 11 cm and removed. Macrofauna were enumer-ated to the lowest practical taxon for the first fouryears. Thereafter, only decapod crabs and musselswere identified and counted due to logistical con-straints. Macrofaunal biomass was quantified us-ing wet weights (see COEN et al., 1999b) for specifictaxonomic groupings (i.e. "Decapod Crabs" and"Shrimp," "Amphipods," "Isopods," "Polychaetes,"and "Mussels") throughout the entire project du-ration. Sampling for reef residents began in March1995, five months after the experimental reefswere constructed and prior to any recruiting oys-ters, with the reefs sampled bimonthly during thefirst year and quarterly during the second year.The more frequent sampling allowed for better ini-tial resolution as reefs began to receive both oysterand resident recruits. Over the next three years,1997-1999, sampling was reduced to summer andwinter samples, collected from the experimentaland natural reefs as described above. For 2000-2001, resident samples were collected only duringthe winter due to logistical (primarily funding andmanpower) constraints over time (see above also).


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Statistical Analyses

Two-way ANOVAs (PCSAS 8.2) were used totest for the effects of time (categorical dependingon particular sampling frequency) and reef type onoyster abundance and mean shell height. All as-sumptions were tested prior to statistical analyses.Mean abundances and oyster size frequencies fromthe experimental and natural reefs are presentedgraphically for the January sampling period onlyfor 1997 through 2001 for simplicity here. Al-though we sampled and measured oysters from ex-perimental reefs from 1995, we did not begin tomeasure adjacent natural oyster populations until1997, whereas resident sampling began soon afterthe reefs were constructed in March 1995. Sincewe are using both for comparison, we show the1997-2001 data ouly. We computed Pearson prod-uct-moment correlation coefficients (SigmaStat2.0) relating mean oyster abundance and meanshell height to the abundances and biomass ofdominant reef-associated species and to various"community descriptors" for the experimental andnatural reefs. Data from January 1998 were se-lected for this analysis because that representedthe latest time period for which complete data onepifaunal abundance and diversity were availablefor the study.

RESULTS

Rappahannock River, Virginia

Two years after construction, reefs at the foursites in the lower Rappahannock River differed

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Figure 5. Temporal patterns of (A) oyster abundance, (B)oyster biomass, (C) epifaunal abundance, (D) epifaunal di-versity, (E) Geukensia demissa abundance, (F) Balanus spp.abundance, and (G) xanthid crab abundance on the reefs inthe Rappahannock River, Chesapeake Bay, Virginia. Valuesare means ± SE by reef site.

both in abundance and size structure of oysterpopulations (Figure 4). Total oyster density variedsignificantly between sites (F = 5.82, df = 3, P =0.0018), with Parrot's Rock, Drumming Ground,and Temple Bay reefs all having greater meandensities than Mill Creek reef (see Figure 4). How-ever, no significant differences were observed be-tween individual reefs independent of geographic"location" (F = 1.94, df = 9, P = 0.0731). Reefsalso differed in densities of 1-2 year class oysters(i.e. those with SH Ž 20 mm), which are shown inthe size distribution plots in Figure 4. Prior to re-cruitment in the summer of 2001, oyster abun-dances at all of the reef sites were zero (Figure5A). Mean oyster abundances peaked in fall 2001at approximately 350 oyster/M2 following recruit-ment during summer 2001 and fell slightly bysummer 2002. Biomass of oysters on the reefs in-creased throughout this period (Figure 5B), aswould be expected with newly recruiting oysterpopulations on these reefs.

Epifaunal abundances were dominated by bar-


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nacles in the genus Balanus, especially during thefirst summer when densities exceeded 14,000/M2

(Figure 5F). Exclusive of barnacles, epifaunalabundances changed little over the course of thestudy (Figure 5C). Overall diversity of epifauna in-creased throughout the time period (Figure 5D),both as a result of an increase in species richnessand a decline in barnacle densities (Figure 5F).Prominent members of the epifaunal assemblage,in addition to barnacles, included bivalves (Maco-ma balthica, Mulinia lateralis, Mya arenaria, Geu-kensia demissa (Figure 5E), Mytilus edulis, and Pe-tricola pholadiformis), solitary and colonial tuni-cates, an ectoproct (Membranipora tenuis), a ser-pulid polychaete (Hydroides dianthus), andxanthid crabs (Figure 5G). In addition, the reefssupported seasonally abundant and diverse as-semblages of macroalgae.

Within a single season, correlation coefficientsbetween oysters (mean total abundance, meanabundance of year class 2 oysters, and biomassacross reef sites) and various community descrip-tors and dominant species varied considerably (Ta-ble 1). The only significant correlation we foundwith total oyster abundance was with the abun-dance of skillet fish, which showed a very strongpositive correlation, and the total abundance ofresident finfish, which showed a positive correla-tion. Similar significant positive correlations wereobserved with the abundance of year class 2 oys-ters. In addition to these two parameters, barnacleabundance, ribbed mussel biomass, and epifaunaldiversity were also significantly correlated withoyster biomass, with total epifaunal abundanceonly marginally insignificant (P = 0.054, see Table1). Interestingly, the only negative correlation ob-served was between oyster biomass and epifaunaldiversity. It is important to note here that while alarge number of samples and individual organismswere part of these analyses, the correlations wereconducted using means for each individual reefand thus the tests for significance, with only 8 de-grees of freedom, had relatively low power (HOENIG

and HEIsEY, 2001).

Inlet Creek, South Carolina

Overall during the study, we collected over 87resident and 60 transient species associated withour reefs (COEN et al., 1999a). Oyster abundanceon the experimental reefs at Inlet Creek increasedduring the period from January 1997 tbrough Jan-uary 2001, but means (±SE) remained well below

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Figure 7. Temporal patterns for (A) mean oyster abun-dance, (B) mean oyster height, (C) mean epifaunal abun-dance, (D) epifaunal diversity, (E) mean Geukensia demissaabundance, (F) mean xanthid crab abundance, (G) meanEu-rypanopeus depressus abundance, and (H) Panopeus herbstiiabundance for experimental (dashed lines) and natural (solidlines) reefs in Inlet Creek, Charleston Harbor, South Caro-lina. All values are means ± SE by reef type (experimentalvs. natural) except for D, epifaunal diversity.

(e.g., January 2001, mean no. 497 ± 282) densitiesfound on adjacent natural reefs at Inlet (January2000 and 2001, means from 861-1646/M2 ) or anyof the other sites we have sampled across the state(Figures 6 and 7A). For comparison, mean densi-ties across South Carolina ranged from a low of500/M2 (±88) to over 6,436/in2 (±500), for samplescollected by us from 1997 to 2002. A two-way AN-OVA revealed significant effects for reef type (F =201.80, P < 0.0001), time of sampling (F = 3.68,P = 0.0022), and the interaction term (F = 3.37,F = 0.0043) for oyster abundance. Oyster size fre-quency distributions were similar on the experi-mental and natural reefs, with natural reefs at In-let having more oysters above 75 mm SH (Figures6 and 7B), resulting in marginally insignificantdifferences (P = 0.0581) in mean SH of oysters be-tween the reef types.

South Carolina has no harvest size limit, sothese differences are not relevant for the resource.Prominent members of the resident faunal assem-blage (numerically) included polychaetes (Nereissuccinea and Streblospio benedicti), several mus-

sels (Brachidontes exustus and Geukensia demissa),a gastropod (Creedonia succinea), mites, and a per-acarid (Gammarus palustris). In addition to theabove taxa, natural reefs also had large numbersof the gastropod ectoparasite Boonea impressa andthe xanthid crab Eurypanopeus depressus. Epifau-nal abundance and diversity measures are onlyavailable for this site for the years 1996-1998;during January 1997, total epifaunal abundanceon the experimental reefs was similar to that onthe natural reefs because of high abundances ofgastropods (primarily C. succinea), mussels (B. ex-ustus and G. demissa), and acarinids (mites), butdiversity was lower (Figures 7C and D).

Ribbed mussel and xanthid crab (total of 14spp.) abundances showed similar patterns, al-though densities on the natural reefs exceededthose on the experimental reefs until 2001 (Fig-ures 7E and F). Initially high abundances of thexanthid crab Eurypanopeus depressus on the nat-ural reefs declined between 1998 and 1999; abun-dances remained comparatively low during the


72


Table 2. Correlations between oysters (abundance and height), dominant taxa, and community metrics for reefs in Inlet Creek,South Carolina, January 1998. S = Species Richness, H' = Shannon-TWeiner Diversity Index, r = Pearson product momentcoefficients, p = Probability of r = 0. Sample size, n = 9 per site for each in A and B.

Epifaunal Invertebrates Xanthid sp.

Oyster Mean # Total Xanthid G. demissa G. demissa E. depres- P. herbstiiC. virginica species S H' Total Abun. Biomass Abun. Abun. Biomass sus Abun. Abun.

A. Experinental Reefs

Abundancer 0.103 0.513 0.055 -0.118 0.761 0.775 -0.218 0.706 0.605p 17.67 0.791 0.158 0.888 0.762 0.017 0.014 0.574 0.034 0.085

Mean Heightr 0.636 0.070 0.832 0.599 0.374 0.285 0.542 -0.046 0.722p 0.065 0.858 0.005 0.089 0.321 0.457 0.132 0.906 0.028

B. Adjacent Natural ReefsAbundance

r -0.036 0.225 0.661 0.105 0.495 0.745 0.092 0.475 -0.183p 18.78 0.927 0.560 0.053 0.788 0.175 0.021 0.814 0.196 0.637

Mean Heightr 0.203 -0.169 -0.084 -0.285 0.218 -0.144 -0.309 -0.021 0.608p 0.600 0.664 0.829 0.457 0.572 0.712 0.418 0.958 0.083

study on the experimental reefs (Figure 7G). Incontrast, the xanthid crab Panopeus herbstii abun-dances varied in a similar manner on both reeftypes throughout the study (Figure 7H).

Correlation coefficients between oysters (meanabundance and shell height) and community met-rics and dominant species revealed several signif-icant positive relationships on the experimentaland natural reefs (Table 2). For the experimentalreefs, the abundance of the ribbed mussel Geuken-sia demissa and the xanthid crab Eurypanopeusdepressus varied positively with total oyster abun-dance, while total numbers of epifaunal inverte-brates and the abundance of the xanthid crab Pan-opeus herbstii were positively correlated with oys-ter height (Table 2A). On the adjacent natural oys-ter reefs (of unknown age), the only significantcorrelations were between overall oyster abun-dance versus total epifaunal densities or overallmussel abundance (Table 2B). No significant neg-ative correlations were observed between eitheroyster abundance or size and any of the other var-iables.

DISCUSSION

Understanding the relationship between the de-velopment of oyster populations and other reef-as-sociated organisms is a key element in evaluatingthe ecological success of oyster reef restoration ef-forts. The two studies outlined here were each de-

signed with different specific goals in mind; nev-ertheless, they provide an opportunity to examineseveral aspects of community development in re-lation to oyster populations on reefs from very dif-ferent systems. The Rappahannock reefs are rel-atively large, subtidal mounds extending severalmeters above the seabed. In contrast, the SouthCarolina reefs, both natural and experimental, arerelatively small by comparison, located entirelywithin the intertidal zone, and generally extend10-30 cm above the upper sediment surface; al-though oysters extend 1-3 m or more from the lowintertidal to upper intertidal as reefs. The reefs inthe two systems are also at very different stagesof development, with less than two years since con-struction for the Rappahannock River reefs com-pared to from six to seven years for the South Car-olina intertidal reefs. Differences in reef morphol-ogy, experimental design, and sampling tech-niques make direct statistical comparisons of datafrom the two systems inappropriate. However,consideration of patterns within each systemshould make the general conclusions informativewithin a region or reef type (i.e. subtidal or inter-tidal).

Central to our objective here is to ask whetheror not successful ecological restoration of oysterreefs is dependent upon various oyster populationattributes such as "abundance" or "size" (as mea-sured here by shell height or indirectly as bio-


73

Luckenbach et al.

mass). The reefs at the Rappahannock River sitewere still too young to assess patterns in relationto market-sized oysters, but they do allow us toexamine the relationship between the early devel-opment of oyster populations and reef-associatedorganisms. The reef bases in the RappahannockRiver were constructed in August 2000 after nat-ural oyster recruitment had occurred. Samplestaken during the early summer of 2001, prior tothe peak of oyster recruitment in the region, foundno oysters on the reef substrate. By the summer2002, two age classes of oysters were evident onall of the reefs at densities ranging from 77 to 277oysters/m2 . Even at the highest of these densities,oysters do not monopolize the space on the originalsubstrate material and are considerably less abun-dant than on natural and other restored reefs fromthe Chesapeake Bay (O'BEIRN et al., 2000). Nu-merous epifauna, especially barnacles, recruited inlarge numbers to all of the reefs prior to any oysterrecruitment occurring in 2001 (Figure 5). Epifau-nal abundances (exclusive of barnacles) increasedonly slightly over time, as oyster abundance andbiomass increased, while barnacle abundances de-clined with time and presumably reef develop-ment.

Though not presented in the Results section, theabundances of transient finfish averaged across allof the reefs over time revealed a strong seasonalpattern, but no clear inter-annual pattern thatcould be related to oyster abundance or biomass.This study did not include any natural "control"reefs for comparison, so we are unable to relate thevarious descriptors of the reef assemblages to "nat-ural reefs" and must rely on comparisons with oys-ter abundance and "size" (most common measure-ment is shell height or calculated biomass) acrossexperimental reefs. This is in large part due to thefact that there are few or no healthy reefs for com-parison as there are in the South Carolina study.

In contrast to the observation for Virginia thatlarval supply may play a significant role in resto-ration success without the significant addition of"seed" oysters to jump start reef oyster popula-tions, South Carolina restoration success appearsto be simply the result of the addition of the lim-iting substrate, oyster shell. The experimentalreefs in Inlet Creek, South Carolina, did have ex-tensive natural reefs for comparison, and over thetime period from 1995 to 2000 they failed to con-verge with the natural reefs, as measured by ei-ther total oyster density or abundance of market-sized >75 mm oysters observed on the natural

reefs. Using our historical statewide South Caro-lina data, oysters >75 mm typically make up lessthan 10% of all reef oysters, with a maximum of18% at only two of the sites to date. Also, althoughthe filtering capacity of a mature oyster reef maynot have been reached due to low oyster initialdensities, mussels recruited to reefs in large num-bers (as high as 1,500/M2 ), potentially providingpreviously unrealized benefits, not noted for oysterreefs before (COEN et al, 1999). Nesting sites forresident fish are also critical, as is a complexthree-dimensional structure for the associateddecapod crabs (GRANT and McDONALD, 1979;BREITBURG, 1999; COEN et al., 1999; MEYER andTOWNSEND, 2000; GRABOWKSI, 2002; GLANcY et al,2003). Although oysters are not necessary to es-tablish some of these ecological benefits, sustain-ability over time and augmentation of these ben-efits (e.g., increased habitat) does require estab-lishment of oyster populations.

Total epifaunal abundance and epifaunal diver-sity (available only for the period from 1996-1998)did not show temporal patterns (with increasingage) related to either oyster abundance (= density)or "size" (shell height or biomass) over the sametime period, but epifaunal abundance on the ex-perimental reefs did approach that found on thenatural reefs in January 1997, largely as a resultof gastropods (2 spp.) and mussels (2 spp.) recruit-ing in large numbers to the experimental reefs.Temporal patterns of abundance were similar forsome species on the experimental and naturalreefs (e.g., Panopeus herbstii) and different for oth-ers (e.g., Geukensia demissa), though the latter didhave similar abundances during 2001 when oysterabundances on the two reef types began to con-verge.

We used correlation rather than regression inanalyzing relationships between oysters and vari-ous components of the reef assemblage, becausewe were lacking specific information regardingcause and effect relationships among the assem-blage entities and the observed oyster populations.We can hypothesize that positive relationshipsmight be associated with: (1) increased habitatheterogeneity, (2) the provision of refuges, (3)availability of nesting sites for resident fishes(BREITBURG, 1999), and (4) enhanced benthic-pe-lagic coupling. Conversely, competitive interac-tions for (1) space and (2) food, as well as (3) ex-clusion of some species from refuges, could resultin negative relationships between oysters and oth-er species. Alternatively, there may be no direct


74


causal relationship, and the parameters may co-vary in relation to some other factor (e.g., local wa-ter quality, larval supply, or food availability). Itis informative that of the 15 significant (and 5marginally insignificant) correlations out of a totalof 78 examined (or 19% significant) that we ob-served between oysters and the evaluated com-munity descriptors or dominant species acrossboth studies and various reef types, all but onewere positive, the exception being epifaunal inver-tebrate diversity in relation to oyster biomass onthe Rappahannock reefs. For the Virginia subtidalreefs, the most consistent pattern observed was apositive relationship between resident finfish (to-tal abundance and G. strumosus) and all measuresof oyster density (total abundance, year class 2abundance, and biomass). For the South Carolinastudy, three of the seven (or 43%) sigruficant in-vertebrate correlations (Table 2A) observed for theexperimental reefs were with total oyster density,while only one of the seven was significant for nat-ural reefs (Table 2B). For mean height, only twoof the seven and none of the seven were significantfor the experimental and natural reefs, respective-ly (Table 2). For the experimental reefs where oys-ter density is gradually increasing, key communitymetrics such as total xanthid crabs and the meanabundance of either the mussel G. demissa or thexanthid crab E. depressus are potentially valuableindicators of reef progress.

Abundances for some species varied differentlywith oyster abundance or size/biomass dependingon whether they were viewed over temporal orspatial scales. For instance, on the reefs in theRappahannock, the abundance of Balanus spp. de-clines sharply between the summers of 2001 and2002, during which time mean oyster biomass in-creases from 0 to 18 g/m2 (Figures 5B and F);however, when we examine the relationship be-tween oyster biomass and barnacle abundanceduring that last sampling period, we observe a sig-nificant positive relationship (Table 1). Similarly,on both the experimental and natural reefs inSouth Carolina, the abundance of Panopeus herbs-tii is strongly inversely related to mean oyster size(as directly measured here) between 1996 and2001 (compare Figures 7B and H). Yet, when weexamine the relationship between oyster shellheight and P herbstii abundance at a single sam-pling period (January 1998), we find a significantpositive correlation on the experimental reefs (Ta-ble 2A) and a similar, though marginally insignif-icant, pattern on the natural reefs (Table 2B). Po-

tential explanations for these discrepancies be-tween temporal and spatial patterns include: (1)that in either one or both cases that the organismsin question and oysters co-vary in response tosome other factor(s), and (2) that the magnitude oftemporal variations in oyster abundance or "size"(shell height or biomass) over the course of thesestudies exceeds those observed at any one timeacross treatment replicates and thus represents amore robust test of the effects of oysters.

A correlational approach alone will not suffice totruly evaluate the relationships between oysterpopulations and the ecological fuinctions of re-stored oyster reefs. We still need to develop a bet-ter understanding of specific interactions betweenspecies. For instance, we did not observe a consis-tent relationship between either the temporal orspatial patterns of oysters and xanthid crabs ateither study site, despite the fact that xanthidcrabs are an important predator on small oysters,while also providing a refugia for the same crabsand other resident finfish (COEN et al., 1999a; GRA-BowsKi, 2002, in press). Direct and indirect effectsof predator-prey interactions among reef-associat-ed organisms along with their relationship to oys-ter population structure, need to be clarified. Fur-ther, the consequences of the competing roles thatoysters play in facilitating the establishment ofsome species by providing hard substrate, and incompeting with many of those same species forspace and food, are not well understood. Many res-ident fish require large, clean, and dead articulat-ed shells for complex life histories (BREITBURG,1999; COEN et al, 1999a). Additionally, we suspectthat there are numerous aspects of reef morphol-ogy, location within respect to tidal range, and po-sition in the landscape affecting the developmentof reef communities that have yet to be clarified(GRABOWSKI, 2002, in press).

As PALMER et al. (1997) point out, choosing res-toration endpoints is a crucial and often difficulttask in ecological restoration. Habitat restorationsuccess should not be dependent solely on thegrowth/survival of the restored species (CRAFT etal, 1999). A focus only on the resource (eg., har-vestable oysters, fishing mortality) will miss pos-sibly critically important measures of reef resto-ration success (e.g., benthic pelagic coupling, hy-drodynamic effects). In a similar vein, we need tobetter understand how feedbacks work in healthyand degraded systems and whether their restora-tion results in alternative states not predicted


75

76 Luckenbach et al.~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

from past observations and recent work (SUDING,2003).

Declines in Crassostrea virginica abundancesthroughout much of the U.S. Atlantic coast havehad important fisheries and ecological implica-tions (NEWELL, 1988; KAUFMAN and DAYTON, 1997;PETERSON and LUBCHENCO, 1997; COEN et al,1999a; JACKSON et al., 2001; PETERSON et al, 2003).Fisheries restoration is, undoubtedly, a desirablerestoration endpoint and the explicit goal of nu-merous restoration efforts. However, it is restora-tion of lost ecological functions provided by oysterreefs that has been the focus of most recent efforts.While our results reveal positive correlations be-tween the diversity and abundance of reef-associ-ated species and the abundance and direct or in-direct measure of oyster "size" (shell height or bio-mass), they do not indicate that market-sized oys-ters are requisite for supporting an abundant anddiverse community. Although South Carolina ex-perimental reefs have not converged with the nat-ural reefs, even after six years, using numbers ofoysters or some measure of vertical complexity ofoyster clusters versus the natural reefs, they arepersisting with slowly increasing oyster popula-tions, and they support a diverse assemblage ofresident organisms. Similarly, the Rappahannockreefs, at the time of final sampling, were only twoyears old and did not yet support any market-sizedoysters. However, they did support resident andtransient community assemblages, many of whichwere positively correlated with the abundance andsize (shell height or biomass) of oysters on thereefs. Until we develop a more thorough under-standing of the individual species interactions andmechanisms linking oyster population structure tothe composition and diversity of reef communities,we suggest that oyster abundance and some mea-sure of "size" (age) structure provides a quantita-tive measure of restoration success, but harvest-able quantities of market-sized oysters are not re-quired for achieving some level of ecological res-toration.

In the future, we need to develop and evaluaterestoration progress by using standard criteriathat can be applied to projects or programs beingconducted over a wide geographic range. In somecases, it may be easier and more cost effective tomeasure surrogate or indirect benefits (e.g., filter-ing, habitat use) than to focus on the oyster pop-ulations alone. For example, seston uptake mightbe able to estimate the total effect of the oysterreef (constructed or natural) community on water

quality by quantifying the amount of the water col-umn that is cleared of seston (GRIZZLE and LuTz,1989). This is one of the major "ecosystem servic-es" often touted in the oyster restoration litera-ture, but rarely quantified.

ACKNOWLEDGMENTS

We wish to thank F. Holland, D. Bushek, R.Mann, and two anonymous reviewers, among oth-ers, for significant contributions throughout thework. The Virginia Rappahannock work (MWLand PGR) was supported by grants from the Vir-ginia Graduate Sea Grant Consortium and theVirginia Oyster Heritage Program. We are espe-cially grateful to J. Wesson for constructing thereefs and to G. Arnold, A. Birch, S. Bonniwell, J.Nestlerode, B. Parks, L. Sorabella and S. Spearsfor assistance in the field and lab. This is Contri-bution #2598 from the Virginia Institute of MarineScience, College of William and Mary.

For the South Carolina component (LDC andJAS), we cannot list all of the many individualswho were involved in the development, collection,and analyses of the data from the Oyster Re-search Program (ORP). However, we are' espe-cially grateful to R. Giotta, D. Knott, B. Stender,E. Wenner, W. Post. W. Hegler, K. Hammer-strom, B. Conte, J. McAlister, and M. Bolton-Warberg for lab and field assistance. The SouthCarolina portion of this research was funded bygrants from the National Oceanic and Atmo-spheric Administration (NOAA) South CarolinaSea Grant Consortium (#NA86RG0052), theSouth Carolina Marine Recreational FisheriesStamp Program, and the South Carolina Depart-ment of Natural Resources through its MarineResources Research Institute. This is Contribu-tion #541 from the Marine Resources ResearchInstitute, SCDNR.

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TITLE: Oyster Reef Habitat Restoration: Relationships BetweenOyster Abundance and Community Development basedon Two Studies in Virginia and South Carolina

SOURCE: J Coast Res Special Issue no40 Wint 2005WN: 0534907132006

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