Nekton use of subtidal oyster shell habitat in a Southeastern U.S. estuary

1015Q 2002 Estuarine Research Federation

Estuaries Vol. 25, No. 5, p. 1015–1024 October 2002

Nekton Use of Subtidal Oyster Shell Habitat in a Southeastern

U.S. Estuary

RICHARD L. LEHNERT1,* and DENNIS M. ALLEN2

1 Florida Marine Research Institute, FWC, 100 Eighth Avenue Southeast, St. Petersburg, Florida33701

2 Baruch Marine Field Laboratory, University of South Carolina, P. O. Box 1630, Georgetown,South Carolina 29442

ABSTRACT: Subtidal accumulations of oyster shell have been largely overlooked as essential habitat for estuarinenekton. In southeastern U.S. estuaries, where oyster reef development is mostly confined to the intertidal zone, easternoyster (Crassostrea virginica) shell covered bottoms are often the only significant source of hard subtidal structure. Wecharacterized and quantified nekton use of submerged shell rubble bottoms, and compared it to use of intertidal reefsand other subtidal bottoms in the North Inlet estuary, South Carolina. Replicate trays (0.8 m2) filled with shell rubblewere deployed in shallow salt marsh creeks, and were retrieved after soak times of 1 to 25 days from May 1998 to March2000. Thirty six species of fishes, representing 21 families, were identified from the 455 tray collections. Water temper-ature, salinity, soak time and the presence of a shell substrate all affected the catch of fishes in the trays. Catches duringthe warmer months were two to five times greater than those during the winter. Fishes were present in 98% of the trayswith an overall average of 5.7 fish m22. The assemblage was numerically dominated by small resident species includingnaked goby (Gobiosoma bosc), oyster toadfish (Opsanus tau), and crested blenny (Hypleurochilus geminatus). Transientspecies accounted for 23% of all individuals and 62% of the total biomass due to the presence of relatively largesheepshead (Archosargus probatocephalus) and black sea bass (Centropristis striata). Both the transient and resident speciesdisplayed distinct periods of recruitment and rapid growth from April to October. Lower abundances of juvenile gobiesand blennies during 1998 were attributed to long periods of depressed salinity caused by high rainfall associated withEl Nino conditions in spring. Crabs and shrimps, which were often more abundant than the fishes, accounted forcomparable biomass in the tray collections. In comparisons of subtidal tray and trawl catches, trays yielded 10 to 1,000fold higher densities of some demersal fish groups. Comparisons of intertidal and subtidal gear catches indicated thatmany species remain in the subtidal shell bottom at all stages of the tide. This study suggests that subtidal shell bottommay be essential fish habitat for juvenile seabass, groupers, and snappers and that it may be the primary habitat for adiverse assemblage of ecologically important resident fishes and crustaceans. Given the high levels of nekton use andthe areal extent of oyster shell bottoms in eastern U.S. and Gulf estuaries, increased attention to protection and resto-ration of these areas appears justified.

IntroductionEastern oysters (Crassostrea virginica) form ex-

tensive reefs in estuaries along the southeasternU.S. coast and these habitats are critical for thesurvival, growth, and reproduction of many fishand invertebrate species (reviews by Bahr and La-nier 1981; South Atlantic Fishery ManagementCouncil 1998; Coen et al. 1999). Dame (1996)identified oysters as ecosystem engineers, whichmodify, maintain, and create habitats through fil-ter feeding, nutrient cycling, and by providing asource of structure. From southern North Caro-lina to northern Florida, oyster reefs are foundpredominantly in the intertidal zone (Bahr andLanier 1981). Within this region, oyster larvae set-tle in subtidal habitats (Kenny et al. 1990), butspat survival and reef development are apparently

* Corresponding author: tele: 727/896-8626; fax: 727/893-1271; e-mail: [email protected].

limited by predation (Wells 1961; Dame 1996)and by flow and sedimentation rates (Giotta 1999;Lenihan 1999).

Southeastern estuaries from southern NorthCarolina to northern Florida lack submergedaquatic vegetation (seagrasses and structure-en-hancing macroalgae) but remain extremely pro-ductive nurseries for several finfish and shellfishspecies. Most subtidal estuarine sediments predom-inantly consist of unvegetated mud or sand, exceptadjacent to well-developed intertidal oyster reefs.On these bottoms, small oyster clusters and shellaccumulate due to down-slope movement from ad-jacent intertidal reefs and from limited subtidalproduction. Subtidal shell accumulations do nothave as much three-dimensional relief as the inter-tidal oyster reefs, but they provide more structuralcomplexity than sandy or muddy bottoms. Struc-tured and heterogeneous habitats such as these areassociated with both increased species abundances

1016 R. L. Lehnert and D. M. Allen

Fig. 1. Placement of the habitat tray in relation to tidaldepth and the intertidal oyster reefs.

and diversities of fishes and invertebrates (Moyleand Cech 1996; Szedlmayer and Able 1996).

Research on the role that oysters play in creatingessential fish habitat has focused on living intertid-al oyster reefs (reviews by SAFMC 1998; Coen etal. 1999). We propose that subtidal oyster rubblealso constitutes essential fish habitat. The primarygoal of this study was to evaluate the importanceof this understudied habitat. Specific objectiveswere to test the habitat tray as a useful samplingdevice for this habitat, quantify temporal changesin the species and life stage composition of thesubtidal assemblage, compare the habitat traycatches to previous efforts describing subtidal andintertidal fish assemblages in North Inlet, and re-view and reinterpret the presumed habitat func-tions of shell rubble.

Materials and MethodsSTUDY SITE

This study was conducted in North Inlet estuary,Georgetown County, South Carolina (338N, 798W).North Inlet is a high salinity, well-mixed estuarywith semidiurnal tides that average 1.7 m (Kjerfveet al. 1981). Average depth of the waterways athigh tide is 3.5 m, and about 55% of the waterflows to the ocean during ebb tide (Chrzanowskiet al. 1982). The estuary covers approximately3,200 ha, and consists of tidal creeks (20.6%), saltmarsh (73%), mudflats and intertidal oyster reef(6.4%) (Dame et al. 1986). We estimate that . 50ha of the subtidal shell rubble bottom occurs inthe estuary. Although live oysters are uncommonin permanently submerged creek bottoms, otherinvertebrates including sponges, soft corals, andbryozoans are usually well established on the oystershell rubble. The sampling area (300 m along thewestern bank of Town Creek adjacent to its conflu-ence with Clambank Creek: 33819.829N,79811.259W) was typical of this system-wide char-acterization.

SAMPLE COLLECTION

The habitat trays were deployed at a perma-nently submerged location on relatively flat shellbottom adjacent to a creek bank fringed by inter-tidal oyster reefs (Fig. 1). The tray design wasadapted from that of Runyan (1961) and the SouthCarolina Department of Natural Resources (Mc-Govern personal communication). The habitattrays were square baskets (91 3 91 3 20 cm deep),constructed of steel rebar and plastic coated wire.The top and bottom of each tray was formed from16 mm steel rebar bent into a square. Wire mesh(2.5 cm hex.) provided support for the 3 mm plas-tic mesh which lined the interior sides and bottomof the trays. A bridle (6 mm rope) for lifting the

trap was attached to the four corners of the toprebar frame. A standard crab pot buoy markedeach tray’s location.

Six trays filled with approximately 40 l of looseoyster shell and clusters were deployed on eachsampling date. They were set 20 to 30 m apart ina line parallel to the adjacent intertidal reef. De-ployment and retrieval were done by hand from aboat at low tide during daylight hours. Trays werepulled weekly or biweekly from May 1998 to March2000, but soak times were occasionally up to threeweeks. At the time of sampling, salinity and tem-perature measurements were also taken.

To determine if fishes were attracted to the traysthemselves rather than to the shell treatments, onetray with no shell substrate was set out and re-trieved at the same time as the six shell trays duringeach sampling period. The effects of different sub-strates in the trays were compared in shell-filled,sand and mud-filled, and empty trays during Juneand July 2000. For each condition, two trays weredeployed (a total of six trays) and retrieved weeklyat slack low tide. In another set of collections, wecompared tray catches from the subtidal shell bot-tom to those from the adjacent intertidal oysterreef just above the mean low water level. Threeshell-filled trays from each location were retrievedat high slack tide, with soak periods of one day.

In all sampling trials, each tray was manually lift-ed into the boat. Shell rubble was carefully inspect-ed, all fishes were removed, and the tray was re-deployed. The standard length (SL mm), totallength (TL mm), and wet weight (to the nearest0.01 g) was recorded for every individual collected.Between October 1999 and March 2000, all deca-pod invertebrates were also collected from thetrays. Carapace length and wet weight were mea-

Nekton Use of Oyster Shell in a SE Estuary 1017

sured for all individuals. Catches from trays thatwere damaged or partially emptied were excludedfrom the data set; at least four replicate trays weresampled on each date in the two year time series.

DATA ANALYSIS

Catch per tray was assumed to be a function ofa seasonal periodicity component, the quantitativefactors soak time, temperature, and salinity, and alltwo-way and three-way interactions of these mea-sured variables. To test for the effect of each of thequantitative variables on catch, the model was fit-ted as a Poisson regression using the GENMODprocedure of SAS version 6.12 (SAS 1996). Poissonregression was chosen to model the catches be-cause it is well suited for discrete count data (Neteret al. 1996). An overdispersion adjustment was in-cluded in the model via the Pscale option in SAS.This was used to correct for potential extra-Poissonvariation in the count data (McCullagh and Nelder1989). Using a stepwise Type I regression analysis,each of the factors and interactions was tested forsignificance. If a factor was not significant (p .0.05), it was removed from the model and the re-gression was re-fit until only significant terms re-mained. If an interaction was significant, the indi-vidual terms comprising that interaction were alsoassumed significant.

For the initial comparison of shell-filled andempty trays, the Poisson log-linear model with sub-strate entered as a final factor was employed. Thisled to a two-sample test between empty or shell-filled trays after adjustment for possible effects ofthe quantitative factors. During the trials in 2000,soak times were held constant and temperaturesand salinities were relatively invariant, so the Pois-son log-linear model was not necessary. Thesecatch data remained non-normal even after logtransformation, so the Mann-Whitney test was usedto compare catches between intertidal and subtidalsets, as well as between the shell, sand and mud,and empty tray sets.

Catches were compared between seasons via alog-linear model. Winter was defined as the periodfrom early December through late February,spring from March through May, summer fromJune to August, and fall from September throughNovember. In this model, catch was assumed to bea function of soak time, salinity, a soak 3 salinityinteraction, and season or year. A simple two-sam-ple test was used to compare catch between anytwo seasons or years.

ResultsDuring this 22-month study, 36 species of fish,

representing 21 families were caught; 35 specieswere present as juveniles during the year, while

only 13 were collected as adults (Table 1). Ten ofthe species collected were considered year-roundresidents since all life stages are known from theestuary. These species made up 78% of the totalcatch by number and 38% of the total weight. Fishwere collected from 98% of the 455 trays set. Watertemperatures ranged from 10 to 328C, and salinityranged from 11 to 35 ppt during the course of thestudy.

Nine species accounted for 87% of the totalabundance and a slightly different set of 9 speciesaccounted for 95% of the total biomass (Table 2).Fifty percent of the catch by count was composedof two species, the naked goby and oyster toadfish.Two species, sheepshead and oyster toadfish madeup 78% of the total wet weight.

For the entire study, the median catch in theempty trays was one fish and the median catch inshelled-filled trays was . 5 fish. Using the Poissonlog-linear model, the effect of shell in the trays wastested and found to have a significant effect onboth the abundance and number of species of fish-es present (p , 0.001, both cases; Table 3). Threespecies naked goby, pigfish (Orthopristis chrysop-tera), and planehead filefish (Monacanthus hispidus)accounted for 78% of the 87 fish caught in theempty habitat trays. With the exception of nakedgobies, all of the fishes were newly settled or veryyoung individuals.

In the comparison of catches between the inter-tidal oyster reef and adjacent subtidal bottom, sig-nificantly more fish were collected from the sub-tidal than the intertidal trays (Mann-Whitney testp , 0.001). Comparisons between three substratetypes showed significantly more fish in the shell-filled trays than in both the sand and mud andempty trays (Mann-Whitney test with Bonferronicorrection p , 0.01). No significant difference wasfound between the sand and mud and empty trays.

Figure 2 shows how catch per tray varied withthe number of days that the trays were left in thewater between sampling dates. The average catchper tray was 5.7 fish. Due to the high variability inthe data set, no clear linear relationship betweensoak time and catch was apparent. The lowestcatches occurred in the 1 to 2 day and in the 14to 16 day soak times. The highest average catchesoccurred with the 13 day soak, primarily due toone sampling date with unusually high catches. Ta-ble 3 gives the results of the Poisson regressionanalysis that tested for the effect of soak time, tem-perature, salinity, and their interactions on totalcatch and individual species catch per tray. Soaktime significantly affected the catch of all individ-ual species except sheepshead. Temperature andsalinity were also shown to affect the catch evenafter seasonality had been taken into account in


TABLE 1. List of species of fishes collected from subtidal oyster reef habitat in North Inlet estuary, May 1998 through March 2000.Species are listed alphabetically by scientific name. Also indicated are common names, life stage(s) collected ( J 5 juvenile and Ad 5adult), residency status (R 5 resident or T 5 transient), occurrence in the intertidal zone, seasonal occurrence, total abundance,total biomass, range standard length, salinity range, and temperature range. Weight units are grams, length units are mm, salinityunits are parts per thousand (ppt), temperature is in degrees Celsius.

Species Common NameLife

Stage R/TInter-tidal Occurrence

Tot.Catch

Tot.Weight Range Sl.

Sal.Range

Temp.Range

Aluterus schoepfiAnchoa mitchilliArchosargus probatocepalusCaranx hipposCentropristis philadelphica

orange filefishbay anchovysheepsheadcrevalle jackrock seabass

JJ AdJ AdJJ

TTTTT

NoYesYesYesNo

SuSu, Faall yearSuWi

24

5223

102.13.6

18,798.53.9

135.7

90–12033–4867–44620–35

105–120

24–3528–3211–3532–3532–35

28–3023–2610–3226–2910–12

Centropristis striataChaetodipterus faberChaetodon ocellatusChasmodes bosquianusConger oceanicus

black seabassAtlantic spadefishspotfin butterflystriped blennyconger

JJJJ AdJ

TTTRT

NoRareNoYesNo

all yearSu, FaFa, Su, WiSuSp

80351511

2,260.0696.1123.9

1.688.0

32–17019–13532–6942

320

11–3520–3511–353428

10–3223–3212–322923

Diplectrum formosusDiplodus holbrookiEpinephelus morioFundulus heteroclitusGobiesox strumosusGobionellus boleosomaGobiosoma boscHypleurochilus geminatus

sand perchspot-tail pinfishred groupermummichogskilletfishdarter gobynaked gobycrested blenny

JJJJJ AdJ AdJ AdJ Ad

TTTRRRRR

NoNoNoYesYesYesYesNo

SuSuFa, WiSpall yearall yearall yearall year

13

171

5324

742392

17.22.4

518.20.1

84.112.2

168.8348.5

8230–3385–1241311–5819–4011–6512–70

353220–353420–3520–3511–3511–35

282615–292810–3110–3010–3210–32

Hypsoblennius hentzHyposblennius ionthasLagodon rhomboidesLeiostomus xanthurusLutjanus griseusLutjanus synagrisMonacanthus hispidusMugil cephalus

feather blennyfreckled blennypinfishspotgrey snapperlane snapperplanehead filefishstriped mullet

J AdAdJJJJJJ

RRTTTTTT

NoNoYesYesYesYesRareYes

all yearFa, Wiall yearWi, SpFa, WiFa, WiSp, Su, FaSu

14012354466

983

628.534.0

342.317.580.3

149.41,005.2

17.5

14–3844–5314–9015–7956–8869–1208–108

63–76

11–3533–3526–3520–3417–3517–3526–3534

10–3212–1810–3010–2712–1715–2923–3228

Mycteroperca bonaciMycteroperca microlepisMyrophis punctatusOpsanus tauOrthopristis chrysopteraRypticus maculatusScorpaena brasiliensisSphyraena borealisSymphurus plagiusaUrophycis floridana

black groupergag grouperspeckled worm eeloyster toadfishpigfishwhite-spotted soapfishbarbfishnorthern sennetblack-cheeked tonguefishsouthern hake

JJJ AdJ AdJJAJJ AdJ

TTRRTTTTTT

NoNoNoRareYesNoNoNoRareNo

Sp, FaSp, FaSu, Faall yearSp, Su, Faall yearSuSuFaWi, Sp

3107

630148

3114

18

92.0766.254.5

14,940.2964.628.740.52.2

15.2470.5

24–14019–205

108–33012–22011–19541–102

1254959–9278–158

11–3022–3226–3211–3511–3517–35263020–3227–34

23–2423–2820–2610–3220–3210–28272413–2614–19

TABLE 2. Percent of the total catch of the 9 dominant fishspecies by abundance and biomass collected from shell-filledsubtidal trays deployed between May 1998 and March 2000.Other is an aggregate of the remaining 28 species.

Common Name Abundance Biomass

Naked gobyToadfishCrested blennyPigfishFeather blennyPlanehead filefishBlack sea bassSheepsheadSkilletfishAtlantic spadefishGag grouperRed grouperOther

27.022.914.36.45.14.22.91.91.9———

13.4

—34.4

—2.21.42.35.2

43.3—

2.31.81.25.9

the regression model. During both years, totalcatch was significantly higher during summer thanspring, fall, or winter, with incremental increasesor decreases between seasons (Fig. 3). Althoughaverage catch per tray appears higher in spring,summer, and fall of 1998 vs 1999, when correctedfor soak time and salinity, the differences were notsignificant.

The gobies (mainly the naked goby) were by farthe most abundant residents, making up morethan 50% of the total catch from May through De-cember during both years (Fig. 4). Two peaks inabundance were observed for the naked goby. Thefirst peak occured in late spring and consisted ofspawning adults, and the second occured in fallwhen newly settled juveniles were abundant in thetrays. Considered together, the four blenny species(crested, feather (Hypsoblennius hentz), freckled(Hypsoblennius ionthas), and striped (Chasmodes bos-


TABLE 3. P-values for the Type I analysis of each factor used in the model to test effects on catch per tray. NS indicates that thefactor was not significant (p . 0.05). Asterisks (*) indicate a significant interaction between factors, thus no p-values are given formain effects. SK 5 soak, TP 5 temperature, SL 5 salinity.

Soak Temp. Sal. SK 3 TP SK 3 SL TP 3 SL SK 3 TP 3 SL

Total CatchSheepsheadBlack sea bassNaked gobySkilletfishCrested blennyFeather blennyPlanehead filefishPigfishOyster toadfish

*NS**

,0.001,0.001

0.01**

0.005

*NS**

,0.001NSNS**

NS

*NS0.02

,0.001NS

,0.001,0.001

*NSNS

NSNS

0.0480.045

NSNS

0.0460.0090.01NS

0.026NSNSNSNSNSNS

,0.001NSNS

0.011NSNSNSNSNSNS

,0.001NSNS

NSNSNSNSNSNSNS

,0.001NSNS

Fig. 2. Box and whisker plot showing catch abundance pertray for each soak time. The whiskers represent the 90% con-fidence interval. The box represents the interquartile range,with the median as the middle line. The dot marks the mean.

quianus)) were more abundant than gobies duringthe winter and early spring. Declines in the abun-dance of adult gobies and blennies occurred inlate spring or early summer, following their typicalpeak spawning periods. Oyster toadfish were lessabundant in winter than the rest of the year. Al-though relatively few skilletfish (Gobiesox strumosus)were caught, they were collected more frequentlyin the winter.

Seasonal changes in abundance of the transientfish species were more pronounced than those ofthe resident species (Fig. 5). Members of the seabass (Serranidae) and snapper (Lutjanidae) fami-lies were collected more frequently as the seasonsprogressed from spring to late fall and early winter,at which time the catch rates dropped off. Only afew small black sea bass were collected from theestuary throughout the winter and early spring.From April through October three species, Atlan-tic spadefish (Chaetodipterus faber), planehead file-fish, and pigfish accounted for a large portion ofthe catch of non-residents. For discussion purpos-

es, these three species will be referred to as sum-mer transients. The sea basses, snappers, and sum-mer transients were young-of-the-year individualsthat arrived in spring or early summer as newlyrecruited juveniles and departed by late fall. Somemembers of the porgy family (Sparidae), sheeps-head and pinfish (Lagodon rhomboides), were cap-tured year-round, but adults and large juvenileswere not captured in the winter. The remainingtransient species were put in other, which shows apeak during late winter and early spring of 1999,mainly due to large catches of newly recruited spotin February and March. Young southern hake(Urophycis floridana) made up a substantial per-centage of the transient population for a short pe-riod during late winter or early spring of each year.

Among the decapod invertebrates collected, themost numerous species were, in decreasing order,the mud crabs, grass shrimps, and snappingshrimps; all are small cryptic species (Table 4). Onaverage, the Town Creek collections yielded 32decapods per tray from October 1999 throughMarch 2000. During the same period the averagenumber of fish per tray was 4.3.

Discussion

For many estuarine fishes, non-living, subtidal,oyster shell bottoms may be more critical habitatthan flooded intertidal reefs which have been iden-tified as essential fish habitat by fisheries managersand scientists (SAFMC 1998; Coen et al. 1999). Atleast 26 of the 36 species collected in the presentstudy rely on the availability of shelly subtidal bot-toms. Many are uncommon or rare in collectionsfrom intertidal reefs (Wenner et al. 1996; Coen etal. 1999), suggesting that these species remain insubtidal areas throughout the tidal cycle. In a com-parison of four groups of fishes using North Inletestuary creeks, all three groups of demersal fishesoccurred at higher densities over subtidal bottoms(Fig. 6). Year-round residents were on the order of1,000 times more abundant, and the seabasses


TABLE 4. Average catch per tray of decapod invertebrates. Animals were collected from Town Creek between October 1999 andMarch 2000, and the data represents 33 tray collections.

Species Common NameAverageCatch

TotalCatch

TotalWeight

Alpheus formosusAlpheus heterochaelisCallinectes sapidusEurypanopeus depressusLibinia dubiaLysmata wurdemanniMenippe mercenaria

striped snapping shrimpbig claw snapping shrimpblue crabflatback mud crabspider crabpeppermint shrimpstone crab

1.852.300.060.580.060.120.58

61762

1924

19

19.965.525.73.77.40.4

1,024.3Neopanope sayiPalaemonetes vulgarisPanopeus herbstiiPenaeus duorarumPetrolisthes armatusPilumnus sayiPortunus spinimanus

Say mud crabmarsh grass shrimpAtlantic mud crabpink shrimpgreen porcelain crabspineback hairy crabblotched swimming crab

9.0310.646.520.092.820.060.03

298351215

39321

129.5135.6546.8

6.937.41.9

15.8

Total 34.73 1146 2,020.9

Fig. 3. Mean abundance of fishes per tray by month, basedon all collections from subtidal shell-filled trays. Error bars rep-resent the 95% confidence intervals.

Fig. 4. Monthly percentage of the total catch of resident sub-tidal oyster reef species based on abundance data. Blenny dataincludes the crested, feather, freckled, and striped blennies.Goby category includes the naked and darter gobies.

were nearly 500 times more abundant in shelly bot-tom collections. Densities of summer transient spe-cies were about 10 times more abundant in thesubtidal area. Although some of the differences incatch composition and abundance are likely dueto differences in sampling strategies (Rozas andMinello 1997), the relatively low intertidal densityfigures were obtained from a highly efficient wholecreek blocknetting program in creeks with exten-sive living reefs. Gear bias was the major contrib-uting factor to the 1,000 times higher densities ofwater column fishes (e.g., anchovies, silversides,mullets) in the intertidal blocknets. Despite thelimitations of this comparison, the relative impor-tance of shelly subtidal areas to demersal fishes isevident. We propose that the definition of essentialfish habitat be extended to include subtidal oystershell bottoms.

The shelly rubble bottom also supports a more

diverse and abundant demersal fish assemblagethan adjacent sandy or muddy subtidal creek bot-tom. Comparisons of densities of the four fishgroups collected by trawls (Ogburn et al. 1988)and trays are shown in Fig. 6. Although both stud-ies were conducted in the same section of TownCreek, no overlap occurred among the top ninespecies ranked by abundance. Again, differences insampling certainly account for some differences.The trays did not effectively sample either watercolumn fishes or certain other demersal fishes(Bothids and Sciaenids). For these species, thetrawl catch was 10 to 100 times greater per unitarea covered than the tray catch. As a group, oysterresidents were over 10,000 times more abundantin the tray than in trawl collections. The results ofcomparisons between shell and no-shell tray catch-


Fig. 5. Monthly percentage of total catch based on the abun-dance of transient species. The snapper/seabass category in-cludes all snappers, sea bass, and groupers. The summer tran-sients are planehead filefish, pigfish, and Atlantic spadefish.The porgies are sheepshead and pinfish. Others include all oth-er species not classified as residents.

Fig. 6. Comparison of the abundance of four groups of fish-es as determined by three different sampling methods. Thecatches were standardized to square meter area fished. The wa-ter column fishes includes the anchovies, silversides, and mul-lets. The summer transients are planehead filefish, pigfish, andAtlantic spadefish. The seabasses include black sea bass andgroupers. The CREEK study data was obtained from blocknet-ted intertidal creeks close to the tray study site. The trawl studydata was also collected nearby.

es together with the relatively low densities of threedemersal fish groups in nearby open-bottom trawlcollections demonstrate the higher use of shellysubtidal bottoms. An additional point of compari-son is that trays with their small size have little orno impact on natural bottoms. Trawled nets tendto catch and tear on bottom snags, and repeateduse adversely impacts the sediment surface as wellas sessile invertebrate assemblages (Van Dolah etal. 1991).

Avoidance behavior by certain species probablyaffected the extent to which the trays accuratelyrepresented the subtidal shell assemblage. Pinfishwere commonly caught on hook and line in thestudy area during the warmer months, but fewwere caught in the trays. Sheepshead were oftencaught in the trays but not other gear. Differencesin response behavior to the lifting of the trays mayexplain this discrepancy. Another source of biasmay be the attraction of fishes to the tray’s struc-ture, but our tests of this suggest that it is a mini-mal factor. Gear avoidance and escape have notbeen quantified, but abundance values provided bythis study are probably underestimates of theamount of use that these shell habitats receive.Habitat trays yielded six species of fishes that hadnot been collected with a variety of gear during theprevious 25 years of sampling in North Inlet estu-ary.

Soak time, salinity, and temperature were allshown to affect catch rates. Although soak time didnot appear to affect taxonomic or life stage com-position of the catch, an effect on the abundancesof most common species was demonstrated. Vari-

ability associated with most soak times less than 15days was higher than that of longer soak times, sug-gesting that use of the trays becomes more stableas motile animals become more familiar with thesesections of the bottom. We envision the move-ments of fishes into and out of the trays on timescales of minutes to hours in the first few days anda tendency to remain longer as the structures be-come more familiar to (resident) species that tendremain in the vicinity for weeks to months. We con-clude that soak times of 2 to 7 days are sufficientto characterize use of these shelly subtidal bottoms.

Catches of gobies and blennies were reduced atlow salinities and temperatures. In response tochanging environmental conditions, some fishesmay move to the more thermally stable deep chan-nels or to higher salinity areas near the inlet. Dur-ing periods of cold temperatures, lower catchesmay result from decreased activity and movementaround the subtidal shell bottom rather than fromreduced local abundance levels due to emigration.Abundances of these fish were significantly higherin summer 1999 than in summer 1998. Allen andBarker (1990) theorized that low salinities result-ing from high rainfall during the 1983–1984 ElNino event significantly depressed the numbers ofgoby and blenny larvae in 1984 compared to 1983.The winter of 1997–1998 was also an El Nino pe-riod, and salinities were depressed in the NorthInlet estuary to record low levels. Extended peri-ods of extremely low salinities are detrimental tooysters and oyster reefs (Wells 1961). They mayalso affect associated fish populations. Harding(1999) determined that goby and blenny larvae se-


lectively feed on oyster larvae. If a poor spawningby oysters result from low salinity conditions, lessfood may be available to some fishes and highermortality rates could occur. Wells (1961) showedthat the macrofaunal community associated withsubtidal oysters also decreased with decreasing sa-linity. Extended periods of low salinity could killmacrofauna and reduce the food supply to adultblennies and gobies. This may account for the low-er catches of resident species in 1998 than 1999.Despite lower numbers of some common residentspecies in summer 1998, species richness and di-versity were higher compared to 1999; this suggeststhat other factors external to the estuary such aslarval transport of transient species, also play a ma-jor role in determining the composition of theseassemblages.

Oyster shell and clumps of shell provide three-dimensional relief on otherwise flat subtidal bot-toms. This may be the main reason fish and inver-tebrates are drawn to subtidal shell habitat. In oneof the earliest studies, Arve (1960) demonstratedthat plantings of oyster shell on bare substrate in-creased trap catches of fish. For larval fishes newlyarrived in the estuary, water turbulence and flowdisturbances over oyster shell allow for settlement(Breitburg et al. 1995). Complex subtidal habitatssuch as those created by shell have been shown toprovide both substrate and refugia to juvenile fish-es (Shulman 1985; Jordan et al. 1996).

Subtidal shell rubble also provides necessaryspawning habitat for many of the resident species.Striped blennies, skilletfish, naked gobies, crestedblennies, feather blennies, and freckled blenniesall use bivalve shells as spawning substrate (Runyan1961; Crabtree and Middaugh 1982; Kuhlmann1998; Breitburg 1999; Harding and Mann 2000).Gobies, blennies, and toadfish attach their eggs toa substrate, and the males guard the eggs. Kuhl-mann (1998) demonstrated that blennies and skil-letfish preferred shells with unfouled interiors forspawning. Since fouling occurs relatively quickly,continuous replacement of fresh oyster shell is re-quired. The availability of suitable spawning habi-tat may be a major control on the reproduction ofthese fishes. Adult abundance of these fishes hastypically been underestimated; however, it is wellknown that larval gobies and blennies dominatethe summer ichthyoplankton in systems with oysterreefs (Shenker et al. 1983; Allen and Barker 1990;Breitburg 1999). Planktonic larval fishes provideboth an abundant food source for other juvenilefishes and a link between the water column andbenthos (Breitburg 1999).

Estuarine habitats are well recognized as nurseryhabitats, and the results of this study support thatconcept. Comparisons of the lengths of fishes

caught in habitat trays with known age at lengthdata collected elsewhere indicate that with the ex-ception of sheepshead, most of the transient spe-cies collected were under two years old. The lengthfrequency data for groupers, pigfish, seabass,sheepshead, snappers, and toadfish show agree-ment with published studies on the growth pat-terns of these species (Manooch 1984; Radtke etal. 1985; Sutter and McIlwain 1987; Beckman et al.1990; Able et al. 1995; Ross and Moser 1995). Notonly are many of these species almost exclusivelyutilizing the subtidal shell habitat during their firstyears of life, they also appear to grow at rates com-parable to those known from other habitats thathave been defined as essential fish habitat.

The majority of motile macroinvertebrates doc-umented in this study are only associated with hardstructures (Ruppert and Fox 1988). In addition,subtidal shell supports a diverse fouling commu-nity including polychaetes, crustaceans, bryozoans,hydroids, sponges, and tunicates (Ruppert and Fox1988). Invertebrate surveys of inter and subtidaloyster reefs along the southeast coast have docu-mented between 50 and 300 invertebrate speciesliving on the oyster shell (Wells 1961; Dame 1979;Bahr and Lanier 1981).

Invertebrates found in and around subtidal shellprovide food for the fishes associated with thathabitat. The diet of oyster toadfish consists pri-marily of crabs and shrimps living in the subtidalshell rubble. Decapods make up a significant pro-portion of diet of juvenile groupers, sea bass, andsnappers (Crabtree 1978; Mullaney and Gale1996). Porgies (sheepshead and pinfish) andyoung Atlantic spadefish feed on encrusting algaeand the invertebrates associated with subtidalstructures (Stoner 1982; Ogburn 1984; Lindquistet al. 1985; Hayse 1989). The small fish speciesfound in the shell rubble are also consumed byseabass, flounders, seatrout, red drum (Wenner etal. 1990) and hake (Lehnert and Allen unpub-lished data).

This study demonstrates that a spatially distinctand temporally dynamic nekton assemblage is as-sociated with subtidal oyster shell bottoms. Theyfunction as feeding, reproduction, recruitmentand refuge habitat for many estuarine and oceanfishes. The results of this study are probably notsite specific because the same kind of shelly subti-dal habitat occurs wherever reef-building bivalvesoccur, and the oyster, fishes, shrimps and crabs dis-cussed here have wide geographic distributions.Oyster shell deposits should be protected from re-moval or burial by dredging and filling activities.Shellfish management programs should be en-couraged to maximize subtidal shell accumulation.If intertidal reef construction projects can be sited


adjacent to subtidal shell bottoms, associated fishassemblages may be enhanced. The importance ofsubmerged shell rubble habitat to ecologically andeconomically important fishes justifies the need toprotect and enhance its distribution in estuaries.

ACKNOWLEDGMENTS

Funding for this research was provided by the University ofSouth Carolina Marine Science Program, the Baruch Institutefor Marine Biology and Coastal Research, and the Slocum-LunzFoundation. S. Forehand, R. Matthews, B. Milan, M. Pothoff, W.Powell, and the staff of the Baruch Institute provided valuableassistance in both the field and lab during this project. Com-ments by G. Ogburn-Matthews and D. Lohrer significantly im-proved this manuscript. This paper is contribution number1356 from the Belle W. Baruch Institute for Marine Biology andCoastal Research.

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Received for consideration, March 13, 2001Accepted for publication, February 28, 2002

Nekton use of subtidal oyster shell habitat in a Southeastern U.S. estuary

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