Habitat use of intertidal eastern oyster (crassostrea virginica) reefs by Nekton in South Carolina estuaries.
KEY WORDS: Crassostrea virginica, eastern oyster, oyster reefs, nekton, habitat utilization, ecologic services, habitat restoration
The concept of ecosystem engineers was defined by Jones et al. (1994) as "organisms that directly or indirectly modulate the availability of resources (other than themselves) to other species by causing physical state changes in biotic or abiotic materials (p. 374)." Oysters are considered ecosystem engineers because of the variety of ecosystem services that they provide (e.g., Grabowski & Peterson 2003, ASMFC 2007). These services include the stabilization of sediment and shorelines (Dame & Patten 1981, Hadley et al. 2010) and the enhancement of water filtration (Newell 1988), benthic-pelagic coupling, and water quality (Dame & Libes 1993, Dame et al. 2001). Oyster reefs also provide feeding and refuge habitats for other organisms (e.g., Gutierrez et al. 2003), attracting diverse assemblages of other invertebrates and fishes (e.g., Bahr & Lanier 1981, Newell 1988, Coen et al. 1999a, Mann & Harding 1998, Breitburg 1999, Tolley & Volety 2005). Numerous species prey directly on oysters, including xanthid crabs, such as the stone crab Menippe mercenaria, and the Atlantic mud crab Panopeus herbstii (Tolley & Volety 2005). In turn, several finfishes, including the naked goby Gobiosoma bosc and the striped blenny Chasmodes bosquianus, are known to feed on these xanthid crabs, generating trophic complexity and the potential for the formation of trophic cascades (Grabowski 2004). Mann and Harding (1998) investigated the trophic interactions among oysters, fishes, and benthic predators on restored oyster reefs and showed that small and intermediate-size fishes, such as gobies (e.g., seaboard goby Gobiosoma ginsburgi and Gobiosoma bosc) and blennies (e.g., feather blenny Hypsoblennius hentz and C. bosquianus), were abundant in Chesapeake Bay oyster reef-dominated ecosystems. The presence of these species on reef structures is thought to attract larger pelagic predatory species, such as striped bass Morone saxatilis, bluefish Pomatomus saltatrix, weakfish Cynoscion regalis, southern flounder Paralichthys lethostigma, sheepshead Archosargus probatocephalus, and spotted seatrout Cynoscion nebulosus. Other benthic predators, such as the Atlantic blue crab Callinectes sapidus, have also been shown to be associated strongly with Crassostrea virginica reefs (Mann & Harding 1998). In general, it appears that the diverse range of organisms associated with oyster reefs creates complex food webs that sustain higher trophic levels than surrounding sediment or marsh habitats (Wrast 2008, Quan et al. 2012).
Several studies have shown that the 3-dimensional structure of oyster reefs attracts greater numbers of resident and transient nektonic species than sand- or mud-bottom habitats (Posey et al. 1999, Harding & Mann 2001, Lenihan et al. 2001, Plunket & La Peyre 2005, Coen et al. 2007). Breitburg (1999) defined 3 groups of nekton associated with subtidal C. virginica reefs in the Chesapeake Bay: (1) reef residents, whose primary habitat is the reef; (2) faeultative residents generally associated with structured habitats; and (3) transient species, which forage on or near the reef but are wide ranging. Furthermore, a number of oyster reef resident fishes, including G. bosc, C. bosquianus, H. hentz, freckled blenny Hypsoblennius ionthas, skilletfish Gobiesox strumosus, oyster toadfish Opsanus tau, and gulf toadfish Opsanus beta, have been shown to be dependent on oysters for reproduction, depositing their eggs on or inside oyster shells (Breitburg 1999, Coen et al. 1999b).
Despite their clear ecologic importance, populations of C. virginica have declined along much of the mid-Atlantic coast of the United States during the past century as a result of a combination of overharvesting (Gross & Smyth 1946), habitat degradation (Rothschild et al. 1994), reduced water quality (Seliger et al. 1985), disease (Ford & Tripp 1996, Lenihan et al. 1999), the interactions among these factors (Lenihan & Peterson 1998), and ecosystem shifts (Rothschild et al. 1994, Luckenbach et al. 1999, Dame et al. 2002). Indeed, Newell (1988) estimated that oysters in the Chesapeake Bay had been reduced to 1% of their historic biomass. Furthermore, the global extent of oyster reefs is estimated to have been reduced to approximately 15% of its 18th-century level (see the recent review by Beck et al. (2009)).
Due to the widespread depletion of oysters, and the recognition of their ecological and economic importance, habitat restoration and enhancements projects have been widely practiced for many years. Until the late 1990s, however, these projects were focused primarily on the fishery enhancement of C. virginica stocks, although a few also included measurements of water quality to assess changes caused by oyster filtration activities (see review by MacKenzie 1963, Coen & Luckenbach 2000, Peterson et al. 2003). Since that time, C. virginica restoration efforts have begun to focus increasingly on restoring ecosystem services, including the provision of habitat for other macrofauna (e.g., Coen et al. 1999b, Coen et al. 2007, Geraldi et al. 2009, Hadley et al. 2010). Although data exist on the broad diversity of fauna associated with natural oyster reefs, the majority of studies investigating oyster reef nekton community composition have focused on natural, subtidal oyster reefs. By comparison, relatively little is known about these communities on restored or enhanced oyster reefs, or in areas where oysters occur intertidally (Tolley & Volety 2005).
This study focused on natural and enhanced oyster reef habitats in the coastal waters of South Carolina, where more than 95% of C. virginica oyster reefs occur in the intertidal zone (e.g., Bahr & Lanier 1981, Burrell 1986). Since oyster depletion in South Carolina has been much less extensive than in many other areas, such as the Chesapeake Bay, natural populations of C. virginica produce very high levels of natural oyster recruitment (>4,000 oysters/[m.sup.2], South Carolina Department of Natural Resources (SCDNR), unpubl, data). Consequently, the provision of suitable substrate has proved to be a successful strategy for oyster reef restoration and enhancement efforts, many of which have used alternative materials as a result of the cost and limited availability of natural oyster shell (see Brumbaugh and Coen (2009) for review). The primary aim of this study was to compare nekton community composition on both natural and enhanced intertidal oyster reefs in South Carolina. Specifically, we compared the nektonic organisms collected on a reef plot with those collected on an adjacent control plot (i.e., bare sand or mud substrate without oyster reef habitat) at three sites. In addition, we examined temporal changes in nekton community composition by sampling on multiple occasions throughout the year, including spring, summer, and fall.
MATERIALS AND METHODS
Three independent stretches of shoreline along the South Carolina coastline that were similar in surrounding soft sediment habitat and that included either an enhanced intertidal oyster reef (2 sites) or a natural intertidal oyster reef (1 site) were chosen as study sites (Fig. 1). For the purposes of this study, an enhanced oyster reef is defined as solid suitable substrate established for the purpose of creating an oyster reef in an area where there is no evidence that a natural oyster reef existed previously. The tidal range at each site was between 1.5 m and 2.0 m. Each site contained an intertidal oyster reef plot with a lower edge that extended to at least the mean low water mark and that was situated along a stretch of at least 80 m of otherwise uninterrupted shoreline comprising intertidal soft sediment habitat. At each site, the reef plot was paired with a control plot containing no structurally complex benthic habitat (i.e., just bare sand or mud). Each control plot was located approximately 30 m from its paired reef plot at the same tidal elevation and on an equivalent surface sediment type.
The most northerly site comprised a 1-y-old enhanced oyster reef plot that was located along the Atlantic Intraeoastal Waterway (ICW, Fig. 1; 33.079520[degrees] N, 79.445368[degrees] W) on Jeremy Island in McClellanville, SC. The enhanced reef was built using 8 arrays of concrete oyster "castles" (Allied Concrete Company) constructed intertidally in a linear configuration at the mean low water mark in July 2009 as part of a collaborative project between the South Carolina Chapter of The Nature Conservancy and the SCDNR. Each oyster castle array comprised 13 interlocking concrete blocks (castles) arranged in a pyramid with 8 castles on the base layer (in a 3 x 3 arrangement with no center block to increase interstitial space), 4 castles in the middle layer that locked the base layer castles in place, and a single castle on the top that locked the middle castles in place. Each of the castles was 30.5 x 30.5 x 20.3 cm, such that each array was approximately 1 x 1 m wide at the base and 0.5 m high at the center. Arrays were placed 1.8 m apart and constituted a total reef footprint of 8 [m.sup.2]. Between the deployment of the oyster castles and the initiation of sampling, oysters recruited to this substrate at high densities, thereby presenting complex biogenie reef habitat for utilization by nektonic organisms. The ICW site had a sandy substrate and was located near a maritime forest with sparse amounts of cordgrass Spartina alterniflora nearby. The second site comprised a 7-y-old enhanced oyster reef located at Fort Johnson in the Charleston Harbor (FJ, Fig. 1; 32.751199[degrees] N, 79.901606[degrees] W). The settlement substrate for the oyster reef at this site was deployed in 2003 by SCDNR's South Carolina Oyster Restoration and Enhancement (SCORE) Program and constituted nylon bags (23 L) filled with recycled oyster shell (12-20 kg). This enhanced reef measured 23 x 4 m (92 [m.sup.2]) and was built on sandy bottom with a S. alterniflora salt marsh located directly inshore of the uppermost part of the reef. The third site comprised a more than 5-y-old natural oyster reef in First Sister Creek, near the Folly River, SC (FR, Fig. 1; 32.899719[degrees]N, 79.935581[degrees]W), with the upper reef margin situated in close proximity (2-3 m) to a dense S. alterniflora salt marsh habitat. The age of this reef was determined through multidecadal aerial surveys performed by the SCDNR (unpubl. data). At both the Fort Johnson and First Sister Creek sites, the reef plots constituted oyster reefs with high percentage cover (>90%) of live oysters within the reef footprints.
Drop Net Sampling Method
The drop net sampling method developed for this study was a reversed modification of the approach described by Wenner et al. (1996). This method involved suspending a bundled net near the top of 3-m-tall poles positioned around the perimeter of each sampling plot. Nets were positioned around 2 rectangular sampling plots (i.e., reef and control plots), each measuring 24 x 5 m (120 [m.sup.2]). Each drop net was 2.5 m in height and 60 m in length, and consisted of a 6.35-mm (0.25-inch) delta mesh seine net. The net was suspended around the perimeter of each plot using stainless steel brackets attached to 3-m aluminum poles (10 per plot) that held the top of the net above the water at high tide and 2 m above the sediment, allowing organisms to enter and exit the study plots during the incoming tide. At high tide, trigger lines equipped with cotter pins that held the net within the brackets were used to release the weighted bottom of the net, allowing it to drop to the sediment and completely encircle the nektonic organisms within each plot. After deploying the pair of nets at a site, the bottom of each net was secured in place using metal stakes to prevent the net from lifting off the sediment surface as a result of the action of currents, wind, and waves. More details of the specifications of this sampling method can be found in Joyce (2011).
Nekton samples were acquired on dates when a spring high tide occurred between 7 AM and 12 noon. This ensured that sites would be completely exposed during low tide, maximizing the ability to collect all the nektonic organisms as the tide receded. These tides also allowed daylight sampling, which made it easier to find and collect all captured nekton, and standardized sampling time, which is known to affect intertidal nekton composition (e.g., Gibson et al. 1998).
A total of 30 sampling dates (10 per site) occurred between March 30, 2010, and December 21, 2010. The interval between sampling dates at each site ranged from 15-45 days, depending on tide and weather conditions, although the majority of samples (>70%) had intervals of 27-33 days (i.e., approximately 1 sample/mo). Sampling dates were categorized as spring (March to May), summer (June to September) or fall (October to December), based on periods of rising, stable, or decreasing water temperatures, respectively (Fig. 2A). At each site, there were 3 sampling dates in spring, 4 in summer, and 3 in fall.
Salinity (measured in practical salinity units), surface seawater temperature (measured in degrees Celsius), and dissolved oxygen (measured in milligrams per liter) were measured at high tide using a hand-held meter (model no. 85; YSI, Inc., Yellow Springs, Ohio). When the tide had receded to a water depth of 0.3-0.6 m within each plot, dip netting for nektonic organisms began. All nekton collected were placed in buckets (~20 L) of ambient seawater and aerated. Each plot was dip netted continuously until either no more organisms were captured or the water had subsided completely from the plot and the area could be checked thoroughly for nektonic organisms using visual surveillance and manual collection. For each sampling event, equivalent effort was directed toward sampling the reef plot and the control plot. The first few individuals of each new species encountered throughout the study were euthanized using dissolved C[O.sub.2] (Burns & McMahan 1995) and stored in 10% seawater-buffered formalin to serve as voucher specimens as part of the College of Charleston's Grice Marine Laboratory Fish and Invertebrate Collection. All organisms were identified to the lowest taxonomic level possible. Most organisms were identified and measured in the field so that live specimens could be returned to the water immediately adjacent to the sample plots. All species netted directly from the water column were included in our analyses, including some considered traditionally as benthic (e.g., bigclaw snapping shrimp Alpheus heterochaelis).
Seawater Physical Data
Two-way ANOVAs were used to test whether physical conditions (temperature, salinity, and dissolved oxygen) differed among sites and seasons. Site and season, and the interaction between them, were entered as fixed factors.
Analysis of Nekton Abundance, Richness, and Diversity Indices
Our primary objective was to explore the effects of treatment (reef vs. control) and season on nekton abundance, taxon richness, and nekton diversity. Data for nekton abundance were transformed ([log.sub.10][x + 1]) to meet normality assumptions. Nekton diversity was estimated using the Shannon index (H') and the reciprocal of the Simpson index (D) using the equations provided in Krebs (1999). Nekton abundance, taxon richness, and taxon diversity were each analyzed using mixed-model ANOVAs that incorporated site (ICW, FJ, FR) as a blocked random factor, treatment (control, reef) and season (spring, summer, fall) as fixed factors, and sampling date (nested within season) as a random factor. The interaction between season and treatment was also tested, but interactions involving random factors were not (Zar 1998). Variations around means are reported as [+ or -] 1 standard error.
Treatment Effects for Individual Taxa
For each taxon collected on more than 1 occasion, a 2-tailed paired t-test was used to test whether its abundance differed significantly between the reef plots and the control plots. Data were pooled from all sampling events and paired by site and date (i.e., adjacent reef and control plots sampled on the same day). Pairs of zero-catch data were excluded from the analyses. A Bonferroni-corrected significance threshold of 0.05/n was applied to control for multiple tests, where n is the number of taxa tested.
Nektonic faunal assemblages were compared among sites and between treatments using cluster analysis (Community Analysis Program IV; Pisces Conservation Ltd., UK) of abundance and composition data. Cluster analysis allowed similar groups of taxa (based on abundance) to be identified using average distances in a Bray-Curtis dissimilarity matrix (Field et al. 1982). Data were transformed ([log.sub.e][x + 1]) to reduce scalar differences in abundance values.
Seawater Physical Data
Mean surface seawater temperature across all sites was 21.1 [degrees]C (range, 16.5-25.6[degrees]C), 29.6[degrees]C (range, 27.7-31.9[degrees]C), and 15.8[degrees]C (range, 7.4-21.9[degrees]C) during spring, summer, and fall, respectively. Temperature varied significantly with season (P < 0.001, [F.sub.2,20] = 29.8) but not site (Fig. 2A). Mean salinity across all sites was 27.4 (range, 20.2-33.1), 31.8 (range, 27.0-35.4), and 30.4 (range, 25.1-34.5) during spring, summer, and fall, respectively. Salinity varied significantly both among seasons (P = 0.006, [F.sub.2,20] = 6.6) and among sites (P < 0.001, [F.sub.2,20] = 12.9); however, the interaction between these factors was not significant. FR was generally the most saline site, and FJ was the least saline site. Both FJ and ICW experienced lower salinities (20.2-22.0) in early spring before switching to more stable, higher salinity regimes thereafter (Fig. 2B). Mean dissolved oxygen across all sites was 5.6 mg/L (range 4.3-6.5 mg/L), 4.6 mg/L (range, 3.8-5.4 mg/L), and 6.1 mg/L (range, 5.3-8.0 rag/L) during spring, summer, and fall, respectively. Dissolved oxygen varied significantly among seasons (P < 0.001, [F.sub.2,18] = 11.5), with lower values in the summer attributable to higher water temperatures. There was no significant difference in dissolved oxygen levels among sites, and no significant interaction between site and season (Fig. 2C).
A total of 12,161 nektonic organisms were collected, including 5,004 from FR, 4,326 from FJ, and 2,831 from ICW. Total abundance by season (across all sites) was 2,274 during spring, 8,475 during summer, and 1,412 during fall. By treatment, total abundance was 10,291 across all reef plots compared with 1,870 across all control plots (Table 1). Reef plots supported a significantly greater abundance of nekton than control plots (P < 0.001, [F.sub.1,45] = 48.5), with overall mean catches per sample of 343.0 [+ or -] 67.3 organisms and 62.3 [+ or -] 11.8 organisms, respectively. Nekton abundance also varied among seasons (P = 0.010, [F.sub.2,45] = 9.6), with the greatest numbers occurring during the summer (Table 2, Fig. 3A).
It was notable that grass shrimp (Palaemonetes spp.) were especially dominant on reef plots (mean, 90.3% of nekton abundance per reef plot compared with 54.0% on control plots). A second analysis was therefore run with Palaemonetes spp. data removed to test whether this taxon alone was responsible for the higher nekton abundance on reef plots. The mean adjusted nekton abundance (i.e., with Palaemonetes spp. data excluded) per sample across all reef plots and all control plots was 64.2 [+ or -] 12.0 organisms and 40.3 [+ or -] 9.2 organisms, respectively, with the reef values being significantly greater (P = 0.004). Adjusted nekton abundance did not vary significantly among seasons, despite varying among dates within season (P < 0.001, [F.sub.7,45] = 4.5) (Table 2, Fig. 3B).
A total of 60 taxa were identified, of which 57 were identified to the species level. Those not identified to species were Palaemonetes spp. (n = 9,026), Blenniidae sp. (n = 1), and mantis shrimp Squilla sp. (n = 3). Although fin ray counts were not used to determine species in all Menidia specimens collected, all were assumed to be the Atlantic silverside Menidia menidia rather than the inland silverside Menidia beryllina, given that all voucher specimens were confirmed as M. menidia, and that M. menidia typically inhabit higher salinity waters, such as those sampled here (Fay et al. 1983). Twenty-nine taxa were collected in spring, 48 in summer, and 40 in fall (Table 3). A total of 50 taxa were found on reef plots compared with 46 on control plots. FR yielded a total of 42 taxa, compared with 36 from FJ and 37 from ICW. The mean richness per sample was 9.1 [+ or -] 0.8 for all reef plots and 7.2 [+ or -] 0.9 for all control plots, with reef plots having a significantly greater taxon richness (P = 0.029, [F.sub.1,45] = 5.1; Table 2, Fig. 3C). There were no significant effects of season, season x treatment, or site on taxon richness, although taxon richness did vary significantly among dates within season (P = 0.00l, [F.sub.7,45] = 4.5). The number of taxa present accumulated with the number of sampling events at a higher rate on reef plots compared with control plots at both FJ and FR (Fig. 4A, B), but not at ICW (Fig. 4C).
Simpson's index (D) could not be calculated for 3 samples because of insufficient catches (i.e., data excluded were 2 fall dates from the FJ control plot and 1 fall date from the FR control plot when [less than or equal to] 1 taxon was encountered). Diversity indices ranged from 1.07-8.45 for the Simpson index (D) and 0.00-2.24 for the Shannon index (H'). Across all reef and all control plots, mean D per sample was 1.72 [+ or -] 0.12 and 3.51 [+ or -] 0.39, respectively, whereas mean H' was 0.77 [+ or -] 0.07 and 1.14 [+ or -] 0.12, respectively. Both indices were significantly lower on the reef plots (H': P = 0.018, F1,45 = 6.0; D: P < 0.001, [F.sub.1,42] = 18.3), regardless of season, site, or date (Table 2, Fig. 3D, E).
Treatment Effects for Individual Taxa
Of the 60 taxa collected, 36 were found on both reef plots and control plots. Fourteen taxa were unique to the reef plots, whereas 10 taxa were unique to the control plots (Table 1). For data pooled across all sites and seasons, 33 taxa were found to be more numerous on reef plots than control plots, 3 taxa occurred in equal numbers, and 24 taxa were more numerous on control plots than reef plots (Fig. 5). Forty-four taxa were collected on more than 1 occasion, allowing paired t-tests comparing reef plot abundance and control plot abundance to be performed. The bigclaw snapping shrimp A. heterochaelis and Palaemonetes spp. were significantly more abundant on the reef plots at the Bonferroni-adjusted significance threshold, [alpha] of 0.05/44 = 0.001 (P < 0.001 for both taxa; [t.sub.6] = 7.0, [t.sub.29] = 4.1, respectively; Fig. 5). The naked goby G. bosc (P = 0.004, [t.sub.11] = 3.6), mummichog Fundulus heteroclitus (P = 0.008, [t.sub.18] = 3.0), and M. menidia (P = 0.039, [t.sub.18] = 2.2) were also all more abundant on the reef plots at the unadjusted significance threshold ([alpha] = 0.05, Fig. 5). No taxa were significantly more abundant on the control plots for these analyses.
The cluster analysis of overall community structure for data pooled across seasons (Fig. 6A) revealed that plots grouped more closely by site than by treatment. The relative influence of site and treatment on the patterns of plot groupings, however, varied with season. For the spring data alone, groupings were governed primarily by treatment (Fig. 6B), whereas for the summer data alone, groupings were governed primarily by site (Fig. 6C). ICW was less similar to the other 2 sites in summer, mainly because of the lack of transient marine and estuarine species such as C. regalis, southern kingfish Menticirrhus americanus, summer flounder Paralichthys dentatus, P. lethostigma, hogchoker Trinectes maculatus, Spanish mackerel Scomberomorus maculatus, and A. probatocephalus. During the fall, cluster groupings were influenced primarily by site, with FR and ICW grouping together (Fig. 6D). The FJ control plot, however, was a notable outlier during the fall as a result of the extremely low catches of nekton at this site (i.e., only 4 organisms collected), whereas the greater nekton abundance and diversity at the FJ reef plot resulted in it grouping together with FR and ICW (Fig. 6D).
This study demonstrates that nekton abundance and community composition are clearly affected by the presence of intertidal oyster reefs. Nekton abundance was significantly greater on the reef plot than on its paired control plot at each of the 3 sites investigated. For data pooled across all sites and seasons, 33 taxa were found to be more numerous on reef plots than control plots. Furthermore, for the 44 taxa collected on more than 1 occasion, 2 taxa (A. heterochaelis and Palaemonetes spp.) to 5 taxa (previous taxa plus G. bosc, M. menidia, and F. heteroclitus) were significantly more abundant on the reef plot than the control plot, whereas no taxa were significantly more abundant on the control plot. The rates at which new species were encountered in our collections over time (i.e., the steepness of the curves shown in Fig. 4) were generally greatest during the summer, followed by the spring. Conversely, relatively few new species were encountered during the fall. This seasonal pattern is likely to be a result of the shoreward and northerly movement of species that spend the winter either offshore or at more southerly latitudes. New species were encountered at higher rates on the reef plots than on the control plots at both FJ and FR, but not at ICW (Fig. 4), possibly because the reef at ICW was established more recently and had a smaller footprint than at the other sites. Future monitoring on the reef plot at the ICW site may help to differentiate the driving mechanisms there.
Although taxon richness was significantly greater on the reef plots than on the control plots, both species diversity indices were greater for the control plots, regardless of site, date, or season. This may be a result of the incorporation of species evenness when calculating diversity using Shannon (H') and Simpson (D) diversity indices, which calculate species heterogeneity. Specifically, Palaemonetes spp., M. menidia, and Anehoa mitchilli were all collected in much higher relative abundance than other species in the reef plots compared with the control plots, which would generate comparatively lower species diversity indices, despite the fact that taxon richness was higher in the reef plots. A possible explanation for why some species were collected in much greater abundance than others may be a result of their social behavior. Taxa such as Palaemonetes spp., M. menidia, and A. mitchilli tend to form large, dense aggregations, whereas many other species such as inshore lizardfish Synodus foetens, pinfish Lagodon rhomboides, and red drum Sciaenops ocellatus tend to be either solitary or found in smaller groups.
In the current study, the greatest abundance of nektonic organisms was collected at the natural reef (FR), with intermediate abundance collected at the older, enhanced reef (F J) and the lowest overall abundance collected at the most recently established enhanced reef (ICW). This trend is intuitive if, as the created reef ages, it increases in structural complexity, attracts more organisms, and begins functioning more similarly to a natural reef (as supported by Fager (1971), Hueckel and Buckley (1987), Van Dolah et al. (1988), Jensen et al. (1994), Relini et al. (1994), and Thanner et al. (2006)). In addition to differences in reef age, the spatial extent of the reef footprint within the sampling plot varied among sites, and this may have affected nekton abundance, particularly for taxa that are known to be associated closely with oyster reefs. Differentiating the effects of reef age, substrate, salinity, and the distribution of surrounding habitats would require sampling a greater number of sites, for which the newly developed method described here would be well suited. Although expanding the number of sites investigated was beyond the scope of the current study, such efforts offer productive opportunities for future research.
When comparing the nekton communities among sites using cluster analysis, the ICW reef tended to be more closely related to the FR reef than to the FJ reef, although there were seasonal differences. Although site was a more important factor driving cluster formation in summer and fall, treatment had a greater influence in the spring, although the ICW control site still grouped together with the other reef sites before the control sites from FR and FJ. This may be explained, in part, by salinity, which has been shown to be an important factor in determining oyster reef community composition (e.g., Tolley et al. 2006), and tended to be lowest at F J, except during the spring. It is possible that salinity had a greater effect on species composition than on taxon richness. Some of the species driving the cluster separation of FJ were those that use more brackish habitats during juvenile and subadult life stages--namely, A. probatocephalus (Jennings 1985), Atlantic menhaden Brevoortia tyrannus (Rogers & Van Den Avyle 1983), C. nebulosus (Johnson & Seaman 1986), striped killifish Fundulus majalis (Abraham 1985), M. americanus, Atlantic croaker Micropogonias undulatus (Lassuy 1983), P. dentatus (Gilbert 1986), P. lethostigma (Gilbert 1986), black drum Pogonias cromis (Sutter et al. 1986), S. ocellatus (Reagan 1985), and T. maculatus (Dovel et al. 1969). The greater similarity of species community composition between ICW and FR compared with FJ for the combined data set demonstrates that site (primarily salinity) had a stronger influence on overall nekton species community composition than treatment in our study.
The patterns of associations of species communities with particular sites and treatments grouping together was maintained during the summer, but changed during the spring and fall. Because spring and fall are the 2 major migration periods for many species that move in and out of estuaries in the southeastern United States, the migration patterns of certain species (e.g., A. mitchilli, pigfish Orthopristis chrysoptera, gray snapper Lutjanus griseus, and spot Leiostornus xanthurus) may have affected the community structure during these seasons. An additional factor in the species community composition in the spring could also be the enhanced recruitment of juvenile and larval fish to the reef plots based on the protection and food resources afforded by reef habitat. Elevated abundance on the reef plots support the dogma that oyster reefs are an important habitat for these species and indicate that the increased habitat complexity that reefs offer has a greater effect on community structure than site during certain seasons. Based on our analyses, the species most likely driving these associations include G. bosc, A. heteroehaelis, M. menidia, Palaemonetes spp., and F. heteroclitus. These species were found more commonly on the reef plot than on the control plot at both ICW and FR, which would explain why the nektonic communities in the reef plot at these 2 sites were associated more closely during the spring than at other times of the year.
The collection and relative abundance of several species (e.g., A. mitchilli, O. chrysoptera, L. griseus, and L. xanthurus) at certain times of year in this study appear to support the seasonal migration patterns described by Adams (1976). Bay anchovies A. mitchilli were collected year-round in the current study, and since they are migratory, schooling fish, there were major fluctuations in their abundance among individual sampling events and between treatments. According to the system proposed by Breitburg (1999), A. mitchilli is a transient species (see Introduction for definitions), and despite being highly mobile, it was collected in greater abundance on the reef plots than on the control plots. Since A. mitchilli, along with other transient species (e.g., the broad-striped anchovy Anchoa hepsetus, and M. menidia), is planktivorous, it may be attracted to the increased zooplankton densities associated with oyster reefs (Harding 2001). Although only a few individuals of O. chrysoptera were collected in the current study, this species was collected in August, which is consistent with the data reported by Adams (1976).
The collection method presented here allowed plots to be sampled repeatedly over a relatively short timeframe without significant disturbance to the habitat plots under investigation. This allowed nekton to be compared among sites, between treatments, and over time. Previous attempts to document the nektonic communities in restored or enhanced intertidal oyster reef habitats have typically used methods that are destructive (e.g., trawling), intensive in terms of personnel (e.g., lift nets), or can only sample a small area (e.g., habitat trays). Such methods also tend to capture mostly smaller, relatively sedentary organisms, rather than the larger, more motile nektonic organisms (e.g., anchovies, silversides, mullets (Lehnert & Allen 2002)). Furthermore, our drop net method requires relatively few people, samples a relatively large area (i.e., 120-[m.sup.2] study plots), and can be applied to both intertidal oyster reef and soft bottom habitats to evaluate nektonic communities quantitatively in terms of both their abundance and diversity. Although our sampling method involved some degree of habitat disturbance (e.g., temporary installation of net poles), no permanent damage to the study plots, particularly the reefs themselves, occurred. The degree of habitat disturbance associated with our method was less than that of Wenner et al. (1996), which involved considerable sediment disturbance by digging ditches around the study plots on each sampling occasion. Wenner et al. (1996) reported greater abundance of small species (e.g., Palaemonetes spp., white shrimp Litopenaeus setiferus, A. mitehilli) than our study, which we attribute to their use of a smaller mesh size (i.e., 3.20 mm compared with our 6.35-mm mesh). Our sampling method enclosed a large area relative to other sampling techniques, such as habitat traps or quadrats, and also captured a wide size range of nekton, from Palaemonetes spp. (<10 mm) to bonnethead shark Sphyrna tiburo (>1,000 mm). Surprisingly, however, only young-of-the-year S. ocellatus and C. nebulosus were collected, despite the known association of older individuals of these species with oyster reef habitat (see, for example, Bortone (2003) and Arnott et al. (2010), respectively).
The results from this study provide important findings on intertidal oyster reef ecologic services, specifically in the context of habitat provision for nektonic species. Additional issues that arose during the study for future consideration, however, include investigating the effects of the proximity and density of adjacent S. alterniflora habitat, water quality parameters, and substrate type on nekton abundance and diversity. These effects could be tested readily using the established sampling method described here through further sampling over additional years and with the inclusion of more field sites. The findings in this study support the importance of intertidal oyster reefs as critical habitat for nektonic organisms, and validate that the addition of suitable structures in intertidal estuaries along the South Carolina coast, by initiating the development of oyster reefs, increases nekton abundance and species richness within that area. Although the creation of habitat increases nekton abundance and species richness in a short timeframe (within 1 y of creation), it may take several years for that habitat to support nekton abundance and species compositions that are similar to natural oyster reefs. Conversely, when creating an enhanced oyster reef by adding substrate to a mud- or sand-bottom habitat, it is important to consider that certain species rely on these soft sediment natural habitats for a portion of their life cycle. Adding substrate to naturally occurring soft sediment habitats could cause reductions in these types of habitat, resulting in localized harm to species that are adapted to use them. Therefore, it is important to ensure that a balanced mosaic of habitat types is maintained within our coastal marine and estuarine environments.
We thank the Southeast Area Monitoring and Assessment Program (SEAMAP) of the National Marine Fisheries Service (NMFS), The Nature Conservancy's Global Marine Team, and the NOAA Restoration Center's Community-Based Restoration Matching Grants Program for funding this study. The College of Charleston Grice Marine Laboratory's Fish and Invertebrate Collection staff assisted in the identification and accession of voucher specimens. Numerous people helped with field collections, including Amanda Fornal, Benjamin Stone, Michelle Willis, Patrick Biondo, Mark Stratton, Michelle Pate, William Sautter, Alex Woods, Peter Lempesis, Rebecca Cope, David Murray, Bryan Danson, Elise Clopton, Daniel Hawkins, Steven Long, Jared Hulteen, Sean Garrett, and Jennifer Scales. This publication represents SCDNR Marine Resources Research Institute contribution no. 699.
Abraham, B. J. 1985. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (mid Atlantic): mummichog and striped killifish. U.S. Fish and Wildlife Service Biological Report No. 84 (11.40). U.S. Army Corps of Engineers, TR EL-82-4. 23 pp.
Adams, S. M. 1976. The ecology of eelgrass, Zostera marina (L.), fish communities: I. Structural analysis. J. Exp. Mar. Biol. Ecol. 22:269-291.
Arnott, S. A., W. A. Roumillat, J. A. Archambault, C. A. Wenner, J. I. Gerhard, T. L. Darden & M. R. Denson. 2010. Spatial synchrony and temporal dynamics of juvenile red drum, Sciaenops ocellatus populations in South Carolina, USA. Mar. Ecol. Prog. Ser. 415: 221-236.
ASMFC. 2007. The importance of habitat created by molluscan shellfish to managed species along the Atlantic Coast of the United States. Habitat Management Series, No. 8. Washington, DC: ASMFC. 108 pp.
Bahr, L. M. & W. P. Lanier. 1981. The ecology of intertidal oyster reefs of the South Atlantic coast: a community profile. U.S. Fish and Wildlife Service program FWS/OBS/-81/l5. 105 pp.
Beck, M. B., R. D. Brumbaugh, L. Airoldi, A. Carranza, L. D. Coen, C. Crawford, O. Defeo, G. J. Edgar, B. Hancock, M. Kay, H. Lenihan, M. W. Luckenbaeh, C. L. Toropova & G. Zhang. 2009. Shellfish reefs at risk: a global analysis of problems and solutions. Arlington, VA: The Nature Conservancy. 52 pp.
Bortone, S. A. 2003. Biology of spotted seatrout. Boca Raton, FL: CRC Press. 328 pp.
Breitburg, D. C. 1999. Are three-dimensional structure and healthy oyster populations the keys to an ecologically interesting and important fish community? In: M. W. Luckenbach, R. Mann & J. A. Wesson, editors. Oyster reef habitat restoration: a synopsis and synthesis of approaches. Gloucester Point, VA: Virginia Institute of Marine Science Press. pp. 239-250.
Brumbaugh, R. D. & L. D. Coen. 2009. Contemporary approaches for small-scale oyster reef restoration to address substrate versus recruitment limitation: a review and comments relevant for the Olympia oyster, Ostrea lurida, Carpenter (1964). J. Shellfish Res. 28:147-161.
Burns, R. & B. McMahan. 1995. Euthanasia methods for ectothermic vertebrates. In: J. D. Bonagura, editor. Continuing veterinary therapy XII. Philadelphia, PA: W.B. Saunders. pp. 1379-1381.
Burrell, V. G., Jr. 1986. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (South Atlantic): American oyster. U.S. Fish and Wildlife Service Biological Report No. 82 (11.57). U.S. Army Corps of Engineers, TR EL-82-4.17 pp.
Coen, L. D., R. D. Brumbaugh, D. Bushek, R. E. Grizzle, M. W. Luckenbach, M. H. Posey, S. P. Powers & S. G. Tolley. 2007. Ecosystem services related to oyster restoration. Mar. Ecol. Prog. Ser. 341:303-307.
Coen, L. D., D. M. Knott, E. L. Wenner, N. H. Hadley, A. H. Ringwood & M. Y. Bobo. 1999a. South Carolina intertidal oyster reef studies in South Carolina: design, sampling and focus for evaluating habitat value and function. In: M. W. Luckenbach, R. Mann & J. A. Wesson, editors. Oyster reef habitat restoration: a synopsis and synthesis of approaches. Gloucester Point, VA: Virginia Institute of Marine Science Press. pp. 139-158.
Coen, L. D. & M. W. Luckenbach. 2000. Developing success criteria and goals for evaluating oyster reef restoration: ecological function or resource exploitation? Ecol. Eng. 15:323-343.
Coen, L. D., M. W. Luckenbach & D. L. Breitburg. 1999b. The role of oyster reefs as essential fish habitat: a review of current knowledge and some new perspectives. In: L. R. Benaka, editor. Fish habitat: essential fish habitat and rehabilitation. Bethesda, MD: American Fisheries Society. pp. 438-454.
Dame, R. F., D. Bushek, D. Allen, A. J. Lewitus, D. Edwards, E. Koepfler & L. Gregory. 2002. Ecosystem response to bivalve density reduction: management implications. Aquat. Ecol. 36:51-65.
Dame, R. F., D. Bushek & T. Prins. 2001. Benthic suspension feeders as determinants of ecosystem structure and function in shallow coastal waters. Ecol. Stud. 151:11-37.
Dame, R. F. & S. Libes. 1993. Oyster reefs and nutrient retention in tidal creeks. J. Exp. Mar. Biol. Ecol. 171:251-258.
Dame, R. F. & B. C. Patten. 1981. Analysis of energy flows in an intertidal oyster reef. Mar. Ecol. Prog. Ser. 5:115-124.
Dovel, W. L., J. A. Mihursky & A. J. McErlean. 1969. Life history aspects of the hogchoker, Trinectes maculatus, in the Patuxent River Estuary, Maryland. Chesap. Sci. 10:104-119.
Fager, E. W. 1971. Pattern in the development of a marine community. Limnol. Oceanogr. 16:241-253.
Fay, C. W., R. J. Neves & G. B. Pardue. 1983. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (mid Atlantic): Atlantic silverside. U.S. Fish and Wildlife Service Biological Report No. 82 (11.10). U.S. Army Corps of Engineers, TR EL-82-4. 15 pp.
Field, J. G., K. R. Clarke & R. M. Warwick. 1982. A practical strategy for analyzing multispecies distribution patterns. Mar. Ecol. Prog. Ser. 8:37-52.
Ford, S. E. & M. R. Tripp. 1996. Diseases and defense mechanisms. In: V. S. Kennedy, R. I. E. Newell & A. F. Eble, editors. The Eastern oyster, Crassostrea virginica. College Park, MD: Maryland Sea Grant. pp. 581-660.
Geraldi, N. R., S. P. Powers, K. L. Heck & J. Cebrian. 2009. Can habitat restoration be redundant? Response of mobile fishes and crustaceans to oyster reef restoration in marsh tidal creeks. Mar. Ecol. Prog. Ser. 389:171-180.
Gibson, R. N., L. Pihl, M. T. Burrows, J. Modin, H. Wennhage & L. A. Nickell. 1998. Diel movements of juvenile plaice, Pleuronectes platessa in relation to predators, competitors, food availability and abiotic factors on a microtidal nursery ground. Mar. Ecol. Prog. Ser. 165:145-159.
Gilbert, C. R. 1986. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (South Florida): southern, gulf, and summer flounders. U.S. Fish and Wildlife Service Biological Report No. 32 (11.54). U.S. Army Corp of Engineers, TR EL-82-4. 27 pp.
Grabowski, J. H. 2004. Habitat complexity disrupts predator-prey interactions but not the trophic cascade on oyster reefs. Ecology 85: 995-1004.
Grabowski, J. H. & C. H. Peterson. 2003. Restoring oyster reefs to recover ecosystem services. Theor. Ecol. Ser. 4:281-298.
Gross, F. & J. C. Smyth. 1946. The decline of oyster populations. Nature 157:540-542.
Gutierrez, J. L., C. G. Jones, D. L. Strayer & O. O. Iribarne. 2003. Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79-90.
Hadley, N. H., M. Hodges, D. H. Wilber & L. D. Coen. 2010. Evaluating intertidal oyster reef development in South Carolina using associated faunal indicators. Restor. Ecol. 18:691-701.
Harding, J. M. 2001. Temporal variation and patchiness of zooplankton around a restored oyster reef. Estuaries 24:453-466.
Harding, J. M. & R. Mann. 2001. Diet and habitat use by bluefish, Pomatomus saltatrix, in a Chesapeake Bay estuary. Environ. Biol. Fishes 60:401-409.
Hueckel, G. J. & R. M. Buckley. 1987. The influence of prey communities on fish species assemblages on artificial reefs in the Puget Sound, Washington. Environ. Biol. Fishes 19:195-214.
Jennings, C. A. 1985. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Gulf of Mexico): sheepshead. U.S. Fish and Wildlife Service Biological Report No. 82 (11.29). U.S. Army Corps of Engineers, TR EL-82-4. 10 pp.
Jensen, A. C., K. J. Collins, A. P. M. Lockwood, J. J. Mallinson & W. H. Turnpenny. 1994. Colonization and fishery potential of a coal-ash artificial reef, Poole Bay, United Kingdom. Bull. Mar. Sci. 55: 1263-1276.
Johnson, D. R. & W. Seaman, Jr. 1986. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (mid Atlantic): spotted seatrout. U.S. Fish and Wildlife Service Biological Report No. 82 (11.43). U.S. Army Corps of Engineers, TR EL-82-4. 18 pp.
Jones, C. G., J. H. Lawton & M. Shacak. 1994. Organisms as ecosystem engineers. Oikos 69:373-386.
Joyce, R. 2011. Nektonic use of intertidal Eastern oyster reefs (Crassostrea virginica) in South Carolina estuaries. MS thesis, College of Charleston. 99 pp.
Krebs, C. J. 1999. Ecological methodology, 2nd edition. New York: Addison-Wesley Educational Publishers. 624 pp.
Lassuy, D. R. 1983. Species profiles: life histories and environmental requirements (Gulf of Mexico): Atlantic croaker. U.S. Fish and Wildlife Service Office of Biological Services FWS/OBS-82/11.3. U.S. Army Corps of Engineers, TR EL-82-4. 12 pp.
Lehnert, R. L. & D. M. Allen. 2002. Nekton use of subtidal oyster shell habitat in a southeastern U.S. estuary. Estuaries 25:1015-1024.
Lenihan, H. S., F. Micheli, S. W. Shelton & C. H. Peterson. 1999. The influence of multiple environmental stressors on susceptibility to parasites: an experimental determination with oysters. Limnol. Oceanogr. 44:910-924.
Lenihan, H. S. & C. H. Peterson. 1998. How habitat degradation through fishery disturbance enhances impacts of hypoxia on oyster reefs. Ecol. Appl. 8:128-140.
Lenihan, H. S., C. H. Peterson, J. E. Byers, J. H. Grabowski, G. W. Thayer & D. R. Colby. 2001. Cascading of habitat degradation: oyster reefs invaded by refugee fishes escaping stress. Ecol. Appl. 11:764-782.
Luckenbach, M. W., R. Mann & J. A. Wesson, editors. 1999. Oyster reef habitat restoration: a synopsis and synthesis of approaches. Gloucester Point, VA: Virginia Institute of Marine Science Press. 358 pp.
MacKenzie, C. L., Jr. 1963. To increase oyster production in the northeastern United States. Mar. Fish. Rev. 45:1-22.
Mann, R. & J. M. Harding. 1998. Continuing trophic studies on constructed "restored" oyster reefs. Annual research report to the U.S. Environmental Protection Agency, Chesapeake Bay Program, Living Resources Committee. Gloucester Point, VA: Virginia Institute of Marine Science. 71 pp.
Newell, R. I. E. 1988. Ecological changes in Chesapeake Bay: are they the result of over-harvesting the American oyster, Crassostrea virginica? In: M. P. Lynch & E. C. Chrome, editors. Understanding the estuary: advances in Chesapeake Bay research. Proceedings of a Conference. Chesapeake Bay Research Consortium publication 129. Baltimore, MD: Chesapeake Bay Research Consortium. pp. 536-546.
Peterson, C. H., J. H. Grabowski & S. P. Powers. 2003. Estimated enhancement of fish production resulting from restoring oyster reef habitat: quantitative valuation. Mar. Ecol. Prog. Ser. 264:249-264.
Plunket, J. T. & M. K. La Peyre. 2005. Comparison of finfish assemblages at clutched shell bottoms and mud bottoms in Barataria Bay, LA. Bull. Mar. Sci. 77:155-164.
Posey, M. H., T. D. Alphin, C. M. Powell & E. Townsend. 1999. Oyster reefs as habitat for fish and decapods. In: M. W. Luckenbach, R. Mann & J. A. Wesson, editors. Oyster reef habitat restoration: a synopsis and synthesis of approaches. Gloucester Point, VA: Virginia Institute of Marine Science Press. pp. 229-537.
Quan, W.- M., A. T. Humphries, L.- Y. Shi & Y.- Q. Chen. 2012. Determination of trophic transfer at a created intertidal oyster (Crassostrea ariakensis) reef in the Yangtze River estuary using stable isotope analyses. Estuaries Coasts 35:109-120.
Reagan, R. E. 1985. Species profiles: life histories and environmental requirements (Gulf of Mexico): red drum. U.S. Fish and Wildlife Service Office of Biological Services FWS/OBS-82/11.36. U.S. Army Corps of Engineers, TR EL-82-4. 16 pp.
Relini, G., N. Zamboni, F. Tixi & G. Torchia. 1994. Patterns of sessile macrobenthos community development on an artificial reef in the Gulf of Genoa (northwestern Mediterranean). Bull. Mar. Sci. 55: 745-771.
Rogers, S. G. & M. J. Van Den Avyle. 1983. Species profiles: life histories and environmental requirements (Gulf of Mexico): Atlantic menhaden. U.S. Fish and Wildlife Service Office of Biological Services FWS/OBS-82/11.11. U.S. Army Corps of Engineers, TR EL-82-4. 20 pp.
Rothschild, B. J., J. S. Ault, P. Goulletquer & M. Heral. 1994. Decline of the Chesapeake Bay oyster population: a century of habitat destruction and overfishing. Mar. Ecol. Prog. Ser. 111:29-39.
Seliger, H. H., J. A. Boggs & W. H. Biggeley. 1985. Catastrophic anoxia in the Chesapeake Bay in 1984. Science 228:70-73.
Sutter, F. C., R. S. Waller & T. D. McIlwain. 1986. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Gulf of Mexico): black drum. U.S. Fish and Wildlife Service Biological Report No. 82 (11.51). U.S. Army Corps of Engineers, TR EL-82-4. 10 pp.
Thanner, S. E., T. L. McIntosh & S. M. Blair. 2006. Development of benthic and fish assemblages on artificial reef materials compared to adjacent natural reef assemblages in Miami-Dade County, FL. Bull. Mar. Sci. 78:57-70.
Tolley, S. G. & A. K. Volety. 2005. The role of oysters in habitat use of oyster reefs by resident fishes and decapod crustaceans. J. Shellfish Res. 24:1007-1012.
Tolley, S. G., A. K. Volety, M. Savarese, L. D. Walls, C. Linardich & E. M. Everham, III. 2006. Impacts of salinity and freshwater inflow on oyster-reef communities in southwest Florida. Aquat. Living Resour. 19:371-387.
Van Dolah, R. F., P. H. Wendt, D. M. Knott & E. L. Wenner. 1988. Recruitment and community development of sessile fouling assemblages on the continental shelf off South Carolina, U.S.A. Estuar. Coast. Shelf Sci. 26:679-699.
Wenner, E. L., R. Beatty & L. D. Coen. 1996. A method for quantitatively sampling nekton on intertidal oyster reefs. J. Shellfish Res. 15:769-775.
Wrast, J. L. 2008. Spatiotemporal and habitat-mediated food web dynamics in Lavaca Bay, Texas. MS thesis, Texas A&M University at Corpus Christi. 102 pp.
Zar, J. H. 1998. Biostatistical analyses, 4th edition. New Jersey: Prentice-Hall. 929 pp.
PETER R. KINGSLEY-SMITH, (1) * RYAN E. JOYCE, (2) STEPHEN A. ARNOTT, (1) WILLIAM A. ROUMILLAT, (1) CHRISTOPHER J. MCDONOUGH (1) AND MARCEL J. M. REICHERT (1)
(1) Marine Resources Research Institute, South Carolina Department of Natural Resources, 217 Fort Johnson Road, Charleston, SC 29422-2559; (2) Grice Marine Laboratory, College of Charleston, 205 Fort Johnson Road, Charleston, SC 29412
* Corresponding author. E-mail: email@example.com
TABLE 1. Abundance of nektonic organisms collected in drop net samples between March 30, 2010, and December 21, 2010, fisted by site and treatment. Fort Johnson Family Species Common Name Cntrl Reef Alpheidae Alpheus Bigclaw -- -- heterochaelis * snapping shrimp Palaemonidae Palaemonetes spp. Grass shrimp 344 2,561 Penaeidae Farfantepenaeus Brown shrimp 41 55 aztecus Litopenaeus White shrimp 170 14 setiferus Portunidae Callinectes Atlantic blue 60 98 sapidus crab Callinectes Lesser blue 7 7 similis crab Squillidae Squilla sp. Mantis shrimp -- -- Atherinidae Menidia menidia Atlantic 13 116 silverside Batrachoididae Opsanus tau * Oyster -- -- toadfish Belonidae Strongylura Atlantic -- -- marina * needlefish Blenniidae Unknown * Unknown -- -- Hypsoblennius Feather 1 -- hentz blenny Paralichthyidae Citharichthys Bay whiff -- -- spilopterus ([dagger]) Etropus crossotus Fringed -- -- flounder Paralichthys Summer 3 1 dentatus flounder Paralichthys Southern 1 11 lethostigma flounder Carangidae Chloroscomhrus Atlantic 7 26 chrysurus bumper Selene vomer Lookdown -- -- ([dagger]) Trachinotus Permit -- -- falcatus Clupeidae Brevoortia Atlantic -- 1 tyrannus * menhaden Opisthonema Atlantic 1 -- oglinum threadfin herring Cynoglossidae Symphurus Blackcheek 19 1 plagiusa tonguefish Cyprinodontidae Cyprinodon Sheepshead -- 3 variegatus minnow variegatus Fundulus Mummichog 1 69 heteroclitus Fundulus majalis Striped 5 59 killifish Diodontidae Chilomycterus Striped -- 3 schoepfi burrfish Engraulidae Anchoa hepsetus Striped 1 7 anchovy Anchoa mitchilli Bay anchovy 79 389 Gerreidae Diapterus Irish pompano -- -- auratus * Eucinostomus Silver jenny -- -- gula ([dagger]) Gobiidae Ctenogobius Darter goby -- -- boleosoma ([dagger]) Gobiosoma bosc Naked goby -- 2 Microgobius Green goby -- -- thalassinus ([dagger]) Haemulidae Orthopristis Pigfish -- -- chrysoptera * Lutjanidae Lutjanus griseus Gray snapper -- -- Monocanthidae Stephanolepis Planehead -- -- hispidus filefish Mugilidae Mugil cephalus * Striped -- 37 mullet Mugil curema White mullet 1 11 Poeciliidae Poecilia Sailfin molly -- -- latipinna Pomacentridae Abudefduf Sergeant -- -- saxatilis * major Sciaenidae Bairdiella Silver perch 4 3 chrysoura Cynoscion Spotted 2 2 nebulosos seatrout Cynoscion Weakfish 1 -- regalis Larimus Banded drum -- -- fasciatus * Leiostomus Spot 2 15 xanthurus Menticirrhus Southern 34 2 americanos kingfish Micropogonias Atlantic 1 -- undulatus croaker ([dagger]) Sciaenops Red drum -- 3 ocellatus * Scombridae Scomberomorus Spanish 3 -- maculatus mackerel ([dagger]) Soleidae Trinectes Hogchoker 1 -- maculatus ([dagger]) Sparidae Archosargus Sheepshead -- 18 probatoce- phalus * Lagodon Pinfish -- 1 rhomboides Sphyraenidae Sphyraena Guachanche -- -- guachancho barracuda ([dagger]) Syngnathidae Syngnathuse Chain -- -- louisiana pipefish Synodontidae Synodus foetens Inshore -- -- lizardfish Triglidae Prionotus Bighead sea -- -- tribulus robin Dasyatidae Dasyatis sabina Atlantic -- -- ([dagger]) stingray Gymnuridae Gymnura micrura * Smooth -- 2 butterfly ray Sphyrnidae Sphyrna tiburo * Bonnethead -- -- shark Loliginidae Lolliguncula Atlantic 2 3 brevis brief squid TOTAL 804 3,522 Folly River Family Species Common Name Cntrl Reef Alpheidae Alpheus Bigclaw -- 5 heterochaelis * snapping shrimp Palaemonidae Palaemonetes spp. Grass shrimp 71 3,867 Penaeidae Farfantepenaeus Brown shrimp 11 13 aztecus Litopenaeus White shrimp 41 29 setiferus Portunidae Callinectes Atlantic blue 21 16 sapidus crab Callinectes Lesser blue 15 2 similis crab Squillidae Squilla sp. Mantis shrimp 1 2 Atherinidae Menidia menidia Atlantic 30 51 silverside Batrachoididae Opsanus tau * Oyster -- 4 toadfish Belonidae Strongylura Atlantic -- 2 marina * needlefish Blenniidae Unknown * Unknown -- l Hypsoblennius Feather -- 1 hentz blenny Paralichthyidae Citharichthys Bay whiff 5 -- spilopterus ([dagger]) Etropus crossotus Fringed 7 -- flounder Paralichthys Summer -- -- dentatus flounder Paralichthys Southern -- -- lethostigma flounder Carangidae Chloroscomhrus Atlantic 2 -- chrysurus bumper Selene vomer Lookdown 1 -- ([dagger]) Trachinotus Permit -- 1 falcatus Clupeidae Brevoortia Atlantic -- -- tyrannus * menhaden Opisthonema Atlantic -- 23 oglinum threadfin herring Cynoglossidae Symphurus Blackcheek 6 -- plagiusa tonguefish Cyprinodontidae Cyprinodon Sheepshead -- -- variegatus minnow variegatus Fundulus Mummichog 2 47 heteroclitus Fundulus majalis Striped -- -- killifish Diodontidae Chilomycterus Striped -- 2 schoepfi burrfish Engraulidae Anchoa hepsetus Striped 17 10 anchovy Anchoa mitchilli Bay anchovy 240 371 Gerreidae Diapterus Irish pompano -- -- auratus * Eucinostomus Silver jenny 4 -- gula ([dagger]) Gobiidae Ctenogobius Darter goby 2 -- boleosoma ([dagger]) Gobiosoma bosc Naked goby 2 6 Microgobius Green goby 1 -- thalassinus ([dagger]) Haemulidae Orthopristis Pigfish -- 1 chrysoptera * Lutjanidae Lutjanus griseus Gray snapper -- 1 Monocanthidae Stephanolepis Planehead 1 1 hispidus filefish Mugilidae Mugil cephalus * Striped -- 1 mullet Mugil curema White mullet -- 1 Poeciliidae Poecilia Sailfin molly -- -- latipinna Pomacentridae Abudefduf Sergeant -- -- saxatilis * major Sciaenidae Bairdiella Silver perch -- 1 chrysoura Cynoscion Spotted -- -- nebulosos seatrout Cynoscion Weakfish -- 1 regalis Larimus Banded drum -- -- fasciatus * Leiostomus Spot 2 -- xanthurus Menticirrhus Southern -- -- americanos kingfish Micropogonias Atlantic -- -- undulatus croaker ([dagger]) Sciaenops Red drum -- -- ocellatus * Scombridae Scomberomorus Spanish -- -- maculatus mackerel ([dagger]) Soleidae Trinectes Hogchoker -- -- maculatus ([dagger]) Sparidae Archosargus Sheepshead -- -- probatoce- phalus * Lagodon Pinfish ([dagger]) -- 2 rhomboides Sphyraenidae Sphyraena Guachanche -- -- guachancho barracuda ([dagger]) Syngnathidae Syngnathuse Chain 7 3 louisiana pipefish Synodontidae Synodus foetens Inshore -- 1 lizardfish Triglidae Prionotus Bighead sea 1 -- tribulus robin Dasyatidae Dasyatis sabina Atlantic 2 -- ([dagger]) stingray Gymnuridae Gymnura micrura * Smooth -- -- butterfly ray Sphyrnidae Sphyrna tiburo * Bonnethead -- 1 shark Loliginidae Lolliguncula Atlantic 17 28 brevis brief squid TOTAL 509 4,495 ICW Family Species Common Name Cntrl Reef Total Alpheidae Alpheus Bigclaw -- 4 9 heterochaelis * snapping shrimp Palaemonidae Palaemonetes spp. Grass shrimp 247 1,936 9,026 Penaeidae Farfantepenaeus Brown shrimp 34 68 222 aztecus Litopenaeus White shrimp 7 3 264 setiferus Portunidae Callinectes Atlantic blue 27 57 279 sapidus crab Callinectes Lesser blue 52 101 184 similis crab Squillidae Squilla sp. Mantis shrimp -- -- 3 Atherinidae Menidia menidia Atlantic 4 3 217 silverside Batrachoididae Opsanus tau * Oyster -- -- 4 toadfish Belonidae Strongylura Atlantic -- -- 4 marina * needlefish Blenniidae Unknown * Unknown -- -- 1 Hypsoblennius Feather -- -- 2 hentz blenny Paralichthyidae Citharichthys Bay whiff -- -- 5 spilopterus ([dagger]) Etropus crossotus Fringed 7 6 20 flounder Paralichthys Summer 1 1 6 dentatus flounder Paralichthys Southern -- -- 12 lethostigma flounder Carangidae Chloroscomhrus Atlantic -- -- 35 chrysurus bumper Selene vomer Lookdown 2 -- 3 ([dagger]) Trachinotus Permit 3 -- 4 falcatus Clupeidae Brevoortia Atlantic -- -- 1 tyrannus * menhaden Opisthonema Atlantic -- -- 24 oglinum threadfin herring Cynoglossidae Symphurus Blackcheek 9 20 55 plagiusa tonguefish Cyprinodontidae Cyprinodon Sheepshead 1 -- 4 variegatus minnow variegatus Fundulus Mummichog 5 18 142 heteroclitus Fundulus majalis Striped 3 5 72 killifish Diodontidae Chilomycterus Striped 11 2 18 schoepfi burrfish Engraulidae Anchoa hepsetus Striped 1 1 37 anchovy Anchoa mitchilli Bay anchovy 32 6 1,117 Gerreidae Diapterus Irish pompano -- 1 1 auratus * Eucinostomus Silver jenny 1 -- 5 gula ([dagger]) Gobiidae Ctenogobius Darter goby -- -- 2 boleosoma ([dagger]) Gobiosoma bosc Naked goby -- 14 24 Microgobius Green goby -- -- 1 thalassinus ([dagger]) Haemulidae Orthopristis Pigfish -- -- 1 chrysoptera * Lutjanidae Lutjanus griseus Gray snapper 3 3 7 Monocanthidae Stephanolepis Planehead 24 3 29 hispidus filefish Mugilidae Mugil cephalus * Striped -- 1 39 mullet Mugil curema White mullet 2 -- 15 Poeciliidae Poecilia Sailfin molly 3 1 4 latipinna Pomacentridae Abudefduf Sergeant -- 1 1 saxatilis * major Sciaenidae Bairdiella Silver perch 2 -- 10 chrysoura Cynoscion Spotted 1 3 8 nebulosos seatrout Cynoscion Weakfish -- -- 2 regalis Larimus Banded drum -- 1 1 fasciatus * Leiostomus Spot 1 2 22 xanthurus Menticirrhus Southern -- -- 36 americanos kingfish Micropogonias Atlantic -- -- 1 undulatus croaker ([dagger]) Sciaenops Red drum -- -- 3 ocellatus * Scombridae Scomberomorus Spanish -- -- 3 maculatus mackerel ([dagger]) Soleidae Trinectes Hogchoker -- -- 1 maculatus ([dagger]) Sparidae Archosargus Sheepshead -- -- 18 probatoce- phalus * Lagodon Pinfish 1 1 5 rhomboides Sphyraenidae Sphyraena Guachanche 2 -- 2 guachancho barracuda ([dagger]) Syngnathidae Syngnathuse Chain 6 -- 16 louisiana pipefish Synodontidae Synodus foetens Inshore 2 1 4 lizardfish Triglidae Prionotus Bighead sea 18 4 23 tribulus robin Dasyatidae Dasyatis sabina Atlantic -- -- 2 ([dagger]) stingray Gymnuridae Gymnura micrura * Smooth -- -- 2 butterfly ray Sphyrnidae Sphyrna tiburo * Bonnethead -- -- 1 shark Loliginidae Lolliguncula Atlantic 45 7 102 brevis brief squid TOTAL 557 2,274 12,161 * Species unique to reef plots. ([dagger]) Species unique to control plots. Cntrl, control; ICW, Atlantic Intracoastal Waterway. TABLE 2. P values from mixed-model ANOVAs testing the effects of site, season, date (nested within season), and treatment on total nekton abundance, adjusted total nekton abundance (Palaemonetes spp. data removed), taxon richness, and diversity indices (Shannon H' and Simpson D). Adjusted Factor Abundance Abundance Richness Site 0.509 0.193 0.451 Season 0.010 ([double dagger])# 0.174 0.098 Date (Season) 0.093 0.001# 0.001# Treatment 0.001 *# 0.004 *# 0.029 *# Season x treatment 0.903 0.536 0.912 Factor H' D Site 0.569 0.529 Season 0.846 0.522 Date (Season) 0.052 0.498 Treatment 0.018 ([dagger])# 0.001 ([dagger])# Season x treatment 0.149 0.401 * Greater on reef plots. ([dagger]) Greater on control plots. ([double dagger]) Greater in summer. P-values shown in bold indicate significant effects of factors on nekton parameters (i.e., <0.05). Note: P-values significant effects of factors on nekton parameters (i.e., <0.05) are indicated with #. TABLE 3. Total nekton abundance listed by species and month in order of earliest to latest encounter date. Spring Species Mar Apr May Jun Anchoa mitchilli 1 35 126 5 Bairdiella chrysoura 1 -- -- 1 Cyprinodon variegatus 1 variegatus Poecilia latipinna 1 Callinectes sapidus 2 10 36 29 Fundulus heteroclitus 3 35 9 15 Palaemonetes spp. 14 463 1,297 1,109 Strongylura marina 1 1 Paralichthys dentatus 1 1 Opsanustau 1 Archosargus 1 probatocephalus Paralichthys lethostigma 2 7 Fundulus majalis 3 4 Alpheus heterochaelis 3 Gobiosoma base 7 3 Leiostomus xanthurus 13 7 Menidia menidia 17 88 17 Anchoa hepsetus 1 1 Callinectes similis 1 2 Stephanolepis hispidus 1 Gymnura micrura 1 Citharichthys spilopterus 1 Brevoortia tyrannus 1 Micropogonias undulatus 1 Syngnathus louisianae 2 3 Lagodon rhomboides 2 Lolliguncula brevis 5 1 Mugil cephalus 35 Farfantepenaeus aztecus 37 13 Chilomycterus schoepfi 1 Mugil curema 1 Sphyrna tiburo 1 Synodus foetens 2 Etropus crossotus 6 Cynoscion nebulosus Selene vomer Prionotus tribulus Blenniidae sp. Squilla sp. Hypsoblennius hentz Menticirrhus americanus Symphurus plagiusa Litopenaeus setiferus Dasyatis sabina Orthopristis chrysoptera Trinectes maculates Cynoscion regalis Chloroscombrus chrysours Sciaenops ocellatus Scomberomorus maculates Trachinotusfalcatus Lutjanus griseus Opisthonema oglinum Abudefduf saxatilis Larimus fasciatus Microgobius thalassinus Ctenogobius boleosoma Sphyraena guachancho Eucinostomus gula Diapterus auratus Summer Species Jul Aug Sept Anchoa mitchilli 43 308 319 Bairdiella chrysoura 5 3 -- Cyprinodon variegatus 1 2 variegatus Poecilia latipinna Callinectes sapidus 79 43 38 Fundulus heteroclitus 46 9 19 Palaemonetes spp. 2,284 1,340 1,735 Strongylura marina 2 Paralichthys dentatus 2 1 Opsanustau 2 Archosargus 2 probatocephalus Paralichthys lethostigma 3 Fundulus majalis 37 14 Alpheus heterochaelis 1 3 Gobiosoma base 3 2 7 Leiostomus xanthurus 1 Menidia menidia 16 5 41 Anchoa hepsetus 26 5 3 Callinectes similis 27 4 95 Stephanolepis hispidus 1 8 Gymnura micrura 1 Citharichthys spilopterus Brevoortia tyrannus Micropogonias undulatus Syngnathus louisianae 3 1 2 Lagodon rhomboides 2 Lolliguncula brevis 27 8 37 Mugil cephalus Farfantepenaeus aztecus 43 15 88 Chilomycterus schoepfi 3 2 7 Mugil curema 4 8 Sphyrna tiburo Synodus foetens 2 Etropus crossotus 4 6 Cynoscion nebulosus 1 3 4 Selene vomer 1 2 Prionotus tribulus 1 6 Blenniidae sp. 1 Squilla sp. 2 1 Hypsoblennius hentz 2 Menticirrhus americanus 7 27 2 Symphurus plagiusa 38 3 Litopenaeus setiferus 76 150 12 Dasyatis sabina 1 1 Orthopristis chrysoptera 1 Trinectes maculates 1 Cynoscion regalis 2 Chloroscombrus 26 9 chrysours Sciaenops ocellatus 1 Scomberomorus 1 maculates Trachinotusfalcatus 2 Lutjanus griseus 5 Opisthonema oglinum 23 Abudefduf saxatilis Larimus fasciatus Microgobius thalassinus Ctenogobius boleosoma Sphyraena guachancho Eucinostomus gula Diapterus auratus Fall Species Oct Nov Dec Anchoa mitchilli 84 196 -- Bairdiella chrysoura -- -- Cyprinodon variegatus variegatus Poecilia latipinna Callinectes sapidus 25 10 7 Fundulus heteroclitus 2 3 1 Palaemonetes spp. 374 226 184 Strongylura marina Paralichthys dentatus 1 Opsanustau 1 Archosargus 14 1 probatocephalus Paralichthys lethostigma Fundulus majalis 5 9 Alpheus heterochaelis 1 1 Gobiosoma base 1 1 Leiostomus xanthurus 1 Menidia menidia 14 17 2 Anchoa hepsetus 1 Callinectes similis 44 10 1 Stephanolepis hispidus 13 6 Gymnura micrura Citharichthys spilopterus 4 Brevoortia tyrannus Micropogonias undulatus Syngnathus louisianae 4 1 Lagodon rhomboides 1 Lolliguncula brevis 11 13 Mugil cephalus 1 3 Farfantepenaeus aztecus 12 14 Chilomycterus schoepfi 5 Mugil curema 1 1 Sphyrna tiburo Synodus foetens Etropus crossotus 4 Cynoscion nebulosus Selene vomer Prionotus tribulus 14 2 Blenniidae sp. Squilla sp. Hypsoblennius hentz Menticirrhus americanus Symphurus plagiusa 13 1 Litopenaeus setiferus 22 4 Dasyatis sabina Orthopristis chrysoptera Trinectes maculates Cynoscion regalis Chloroscombrus chrysours Sciaenops ocellatus 2 Scomberomorus 2 maculates Trachinotusfalcatus 2 Lutjanus griseus 2 Opisthonema oglinum 1 Abudefduf saxatilis 1 Larimus fasciatus 1 Microgobius thalassinus 1 Ctenogobius boleosoma 2 Sphyraena guachancho 2 Eucinostomus gula 4 1 Diapterus auratus 1
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|Author:||Kingsley-Smith, Peter R.; Joyce, Ryan E.; Arnott, Stephen A.; Roumillat, William A.; McDonough, Chri|
|Publication:||Journal of Shellfish Research|
|Date:||Dec 1, 2012|
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