Oyster and associated benthic macrofaunal development on a created intertidal oyster (Crassostrea ariakensis) reef in the Yangtze River estuary, China.
Article Type: Report
Subject: Artificial reefs (Research)
Fish habitat improvement (Research)
Oysters (Research)
Shellfish fisheries (Research)
Authors: Quan, Weimin
Humphries, Austin T.
Shen, Xinqiang
Chen, Yaqu
Pub Date: 08/01/2012
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2012 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: August, 2012 Source Volume: 31 Source Issue: 3
Topic: Event Code: 310 Science & research
Geographic: Geographic Scope: China Geographic Code: 9CHIN China
Accession Number: 303011381
Full Text: ABSTRACT Oysters and the reefs they build are being recognized and restored increasingly for the broad suite of ecosystem services they can provide. However, surprisingly little effort has been devoted to documenting the outcomes of such restoration or creation projects through time, or to comparing projects from different regions. In this study, we examined the oyster (Crassostrea ariakensis) and benthic macrofaunal development on a created intertidal oyster (Crassostrea ariakensis) reef along a salinity and exposure (vertical position on reef) gradient 5 y after creation in the Yangtze River estuary, China. Three years after reef creation, sustainable oyster populations were established successfully and market-size oysters accounted for more than 24% of the total reef cover, with mean abundances ranging from 95-225 adult oysters/[m.sup.2]. Associated community metrics (species richness, abundance, and biomass) of benthic macrofauna showed generally increasing trends with reef development during the 5-y period; however, crustaceans and polychaetes were correlated most strongly with oyster development. Barnacle (Balanus albicostatus) abundance and biomass were correlated negatively with oyster and reef development. Salinity and exposure frequently interacted, suggesting that development at different places along the reef or salinity gradient was dependent on the vertical position along the reef or the degree of exposure at low tide. Oyster development on this created reef appears to be at a self-sustaining level and provides habitat for associated benthic macrofauna comparable with other regions globally.

KEY WORDS: restoration, oyster, reef, Crassostrea ariakensis, habitat, estuary, Yangtze, China


Oyster reefs are being restored increasingly for the broad suite of ecosystem services they provide the surrounding environment (Coen et al. 2007a). Traditionally, many programs have been driven by managers with the specific goal of developing enhanced oyster fisheries or establishing oyster populations at self-sustaining levels (Breitburg et al. 2000, Coen & Luckenbach 2000, Coen et al. 2007b, Brumbaugh & Coen 2009). However, recent emphasis has shifted from focusing primarily on oysters, and the reefs they create, to the full array of ecosystem services and functions that oyster reefs provide (i.e., ecosystem engineering) (Jones et al. 1994, Coen et al. 2007b, Grabowski & Peterson 2007, Gregalis et al. 2009, Hadley et al. 2010, Beck et al. 2011). These services include water filtration (Newell 2004, Grizzle et al. 2006, Grizzle et al. 2008), erosion control (Meyer et al. 1997, Piazza et al. 2005), and the rebuilding of habitat that provide foraging, refuge, and nursery habitats for resident and transient macrofauna (Coen et al. 1999, Harding & Mann 1999, Peterson et al. 2003, Plunket & La Peyre 2005, Quan et al. 2009, Stunz et al. 2010). Because of spatial, temporal, or methodological differences among studies, consistent correlations between oyster reef development and the associated community have been somewhat equivocal and inconsistent (Luckenbach et al. 1999, Coen et al. 2007b).

Habitat restoration success should not be dependent solely on the growth and/or survival of the targeted species (Craft et al. 1999). Some studies judge the success of oyster reef restoration based solely on the abundance of market-size oysters or on total oyster counts (Tolley & Volety 2005, Powers et al. 2009). However, this ignores the other ecosystem services that nonmarket-size oysters or other sessile invertebrates (i.e., barnacles) may provide (Luckenbach et al. 2005, Coen et al. 2007b). In fact, a few recent studies have indicated that oyster reef ecological function does not necessarily require the presence of large oysters (Luckenbach et al. 2005, Hadley et al. 2010). For example, Hadley et al. (2010) showed that the habitat value of oyster reef for mussels and crabs was independent of large, dense oyster assemblages. More studies that determine oyster development and faunal utilization are needed because exclusive assessments of oyster population alone may not reflect the reef's full ecological function (Brumbaugh et al. 2006, Oyster Restoration Evaluation Team 2009, Powers et al. 2009).

The Yangtze River estuary is the largest estuary in China and has been recognized as one of the most important ecotones in the world (Chen et al. 1988, Quan et al. 2009). Since the early 1980s, the estuary has been going through profound physical and chemical changes as a result of extensive anthropogenic disturbances such as overfishing, environmental pollution, bio-invasion, wetland reclamation, and large-scale basin and estuarine projects (e.g., Chen et al. 2003, Quan et al. 2005, Chai et al. 2006). Some of these changes include increasing nutrient loads and frequency of red tides, loss or extinction of terrestrial and aquatic species, mass outbreaks of jellyfish (Phylum Cnidaria), decreased stock and biodiversity of benthos and fishes, as well as overall reclamation of wetlands (Chen et al. 2003, Quan et al. 2005, Chai et al. 2006). To mitigate some of these changes, there have been local efforts to cultivate and release native aquatic species for stock enhancement (Chen et al. 2003, Quan et al. 2006, Quan et al. 2009). In April 2004, creation of an intertidal oyster reef was initiated by transplanting hatchery-derived oyster (Crassostrea ariakensis; Fujita, 1913) seed to artificial concrete modular (dikes and groins) units as part of the Deepwater Navigation Channel Regulation Project (DNCRP). Before the DNCRP, few efforts had been made to restore or rebuild previous naturally occurring biogenic habitats (e.g., saltmarsh, oyster reef).

Previous studies have demonstrated that the created oyster reef is able to support sustainable oyster (C. ariakensis) populations (Quan et al. 2009), provide important ecosystem services (Quan et al. 2007), create significant habitat structure for resident and transient species (Quan et al. 2009), and maintain a higher average trophic level and more robust food web than adjacent saltmarsh (Quan et al. 2012). This study explored the development (from reef creation to year 5) of the oyster population and associated benthic macrofaunal communities using sites along an exposure and salinity gradient on the created intertidal reef in the Yangtze River estuary, China. Specifically, we ask the question: Can the created C. ariakensis reef be considered an "ecosystem engineer" in the Yangtze River estuary, China? We answer the question by examining oyster and associated benthic macrofaunal development on the created reef as well as the association between oysters and benthic macrofauna (e.g., species richness, abundance, biomass).


Study Site and Reef Construction

The Yangtze River estuary is well mixed, ranging from oligoto polyhaline, with 4 major inlets to the East China Sea. Tides are semidiurnal, averaging 4.5 m and 2.6 m at spring and neap tides, respectively. The climate is characterized by an annual mean precipitation of 1,124 cm and a mean temperature of 15.7[degrees]C (Chen et al. 1988, Quan et al. 2009).

The Yangtze River originally carried 468 x [10.sup.6] t/y of sediment into the East China Sea (Chen et al. 1988). More than half the sediment from the river was deposited in the estuarine area, which formed a large sand bar and decreased significantly the shipment capability of the Yangtze River (Chen et al. 1988). To deepen the navigation channel, the Chinese government authorized the DNCRP in 1997. The main structures of the DNCRP--including 2 dikes (south dike, 48 km; north dike, 49.2 km) and 19 groins (total length, 30 km)--were constructed in 1998 to 2003 in the north passage of the south channel (Fig. 1). One objective of the DNCRP was to increase water flow and decrease sediment deposition within the estuary (Quan et al. 2009). The dikes and groins of the DNCRP form an intertidal concrete modular structure, and provide hard substratum (~260 ha) for oyster settlement and growth, as well as associated benthic macrofauna. In April 2004, the East China Sea Fisheries Research Institute, working in cooperation with the Administration Bureau of Navigation in the Yangtze River Estuary, initiated a restoration project to establish a self-sustaining oyster population on the concrete modular structure. The restoration project aimed to mitigate the destruction and loss of suitable nekton habitats caused by DNCRP construction.

Low recruitment of larval oysters limited the success of the restored reef at the beginning of the DNCRP (Chen et al. 2003, Quan et al. 2009); therefore, broodstock enhancement was established in 2004 on the concrete modular structure (dikes and groins) (Chen et al. 2003). Seed oyster was obtained from the Xiangshan Bay (29[degrees]30' 34.1 "N, 121[degrees]28'39.2" E), approximately 160 km southwest of the DNCRP. In July 2002, the cultch were set for larval recruitment in the intertidal zone of the bay using recycled bicycle tires (external diameter, 58 cm; inner diameter, 50 cm). In April 2004, we seeded 786,000 (1,500 tires, 524 adult oysters per tire, and a total oyster fresh weight of 20 t) adult oysters (C. ariakensis; mean shell height (SH), 63 mm) to portions of the reef (Fig. 1A: N6, N8-N9, S5, S7-S8, S9), covering approximately 10 km of the reef at a mean density of 5.6 oysters/[m.sup.2]. The oysters at the reef were identified initially as the jinjiang oyster (Crassostrea rivularis), but were later recognized as the Asian oyster (C. ariakensis) according to the recent classification based on shell morphology and flesh color (Wang et al. 2004, Quan et al. 2012). Furthermore, identification of oyster species at the DNCRP reef was completed using multiplex species-specific PCR genetic markers; more than 85% of oyster specimens were recognized as C. ariakensis (others were identified as Crassostrea sikamea) (Quan, unpubl, data). These 2 oyster species seem to have a zonal distribution--namely, C. ariakensis appears in the lower and middle zone, whereas C. sikamea can tolerate longer exposure durations and is distributed primarily in the high intertidal zone (Quan, unpubl, data).


The cross-section of the reef resembles an isosceles trapezoid, with a width of 4 m for the short parallel side and 18.4 m for the long parallel side, and it stands 2.5 m above mean low water (MLW) during spring tide (Fig. 1B). Dense oysters and typical 3-dimensional reef structure (dead and live oyster matrix) only appeared in the lower (MLW) and middle (1.2 m MLW) intertidal zone, whereas sporadic oysters are distributed in the high (2.5 m MLW) intertidal zone of the created reef (see Quan et al. 2009, Quan et al. 2012).

Sampling Regime

We sampled resident sessile (e.g., oysters, barnacles) and mobile benthic macrofauna (e.g., molluscs, crustaceans, polychaetes) at the reef 8 times since construction: September 2004, August 2005, August and November 2007, April and July 2008, and May and September 2009. All sampling took place when the reef was exposed during spring low tide, which allowed approximately 2 h to complete sampling on the reef. Each sampling period took 3-4 days to complete. We defined benthic macrofauna as those organisms exclusive of oysters and barnacles found within the shell matrix when exposed at low spring tide (Coen et al. 1999, Luckenbach et al. 2005), and we refer to these organisms as "benthic macrofauna" throughout this study. Species-specific data were not collected at the 2004 and 2005 sampling periods; therefore, only mean abundance and biomass of oyster and benthic macrofauna are reported.

The oyster C. ariakensis spawns primarily in June to July each year (Quan, unpubl, data); therefore, sampling in the mid spring (April to early June) and late summer (August to September) during 2007 to 2009 was carried out to describe the survivorship, growth, and mortality of the oyster population before and after spat recruitment. We set 5 sampling sites at the created reef along a salinity gradient to account for spatial variation within the estuary. Depending on the tide, runoff flow, and climate conditions, salinity ranged from 0.6-7.3[per thousand] at site S2, from 2.5-16.8[per thousand] at sites S5 and N6, and from 8.9-23.4[per thousand] at sites S8 and N9 (Quan et al. 2009). Water temperature and dissolved oxygen at the reef were determined seasonally in situ during 2007 and 2008 (Hach Instruments, Sension5 model). Mean water temperature varies at the reef, from 4.2[degrees]C in winter to 30.8[degrees]C in summer, and dissolved oxygen ranges between 5.56 mg/L and 8.79 mg/L (Quan et al. 2010).

At each of the 5 sampling sites, the reef was subdivided further into 3 tidal strata: high (reef crest, 2.5 m above MLW), middle (reef flank, about 1.2 m above MLW), and low intertidal zones (reef base, at the MLW; Fig. 1B). At each tidal level, 3 0.3 x 0.3-m quadrats were collected from each side of the reef to avoid the bias of wave energy. All the material in each 0.09-[m.sup.2] quadrat was excavated down to the surface of the modular concrete reef, then sorted using a 1.0-mm mesh sieve. All live oysters (exclusive of recruits, SH [greater than or equal to] 20 mm) were measured to the nearest millimeter and weighed to the nearest 0.1 g, and barnacles (Balanus albicostatus Pilsbry; hereafter, "barnacle") were enumerated and weighed. Remaining benthic macrofauna (e.g., molluscs, crustaceans, polychaetes) were preserved in 75% ethanol, then enumerated and identified to the lowest possible taxonomic level, and weighed to the nearest 0.01 g wet weight. Mollusc weights were converted to flesh biomass based on an established ratio of flesh to shell (Quan et al. 2009). The abundance and biomass of benthic macrofauna were expressed as the individuals per square meter and wet weight per square meter, respectively. Species richness was represented as the mean species number in each quadrat.


Statistical Analyses

Oysters were sorted for market size (SH, [greater than or equal to]70 mm), and total counts exclusive of recruits (SH, <20 mm). The market-size ratios of oysters were calculated based on the size-frequency distribution. Separate 2-factor analysis of variance (ANOVA; STATISTICA 6.0) were carried out to examine differences in the abundance and biomass of oyster, barnacles, and the benthic macrofaunal communities for each sampling event (Factors: sampling site and tidal level). Prior to all analyses, data were tested for normality (Kolmogorov-Smirnov test) and homogeneity of variances (Cochran's test). If necessary, the data were log(x + 1) transformed. Post hoc pairwise comparisons were made on least-squared means using Tukey's HSD (P < 0.05). Correlations between oyster metrics (abundance and biomass) and associated benthic macrofaunal descriptors (species richness, abundance, and biomass) of the total and major taxonomic groups (e.g., molluscs, crustaceans, polychaetes) were explored further using Pearson's product moment correlation coefficients.


Oyster and Barnacle

Immediately after reef creation, mean oyster abundance (new recruitment) increased rapidly and peaked in summer 2005 at 3,410 oysters/[m.sup.2] (Fig. 2A). Abundance then decreased until fall 2007, when the reef reached 366 oysters/[m.sup.2], then increased slightly until fall 2009 with 810 oysters/[m.sup.2]. Mean oyster biomass followed similar trends as abundance; however, a greater increase was observed in biomass from 2008 to 2009 (Fig. 2B). Barnacles displayed similar temporal patterns as oysters in mean abundance and biomass during 2004 to 2007 (Fig. 2B). Thereafter, mean abundance and biomass decreased gradually from 2007 to 2009.

Oyster size frequency distributions varied with reef age, and mean oyster size generally increased throughout the study period (Fig. 3). Maximum SH was no more than 40 mm, and no market-size individuals (SH, [greater than or equal to] 70 mm) appeared at the reef 1 y after construction (Fig. 3A). By the third year, mean SH had increased to more than 50 mm, and market-size oysters represented more than 20% of the total population (Fig. 3B). Through time, interannual differences in oyster size-frequency distributions were less distinct, and there were similar ratios of market-size oysters (>20%) from 2007 to 2009 (Fig. 3B-D).

Mean biomass (tissue wet weight) of oysters and barnacles varied significantly (P < 0.05) among sampling sites and among intertidal levels (Table 1). A strong interaction was present in 2007 and 2009 (P < 0.05, Table l). Abundance followed similar trends as biomass. There was significantly (P < 0.05) greater oyster biomass in the low intertidal zones than in the high intertidal zones (Table 1). Conversely, the greatest barnacle biomass (tissue wet weight) was found in the high intertidal zone (Table 1). There were significant negative correlations between oysters and barnacles (abundance and biomass) for all years (P < 0.001, Table 2).


Benthic Macrofauna

Thirty-six species (Table 3) of benthic macrofauna were collected within quadrats during the 5-y study period. Crustacea (14 species) represented the most abundant phylum, followed by Mollusca (12 species) and Polychaeta (5 species). Other phyla observed included Chordata (2 species), Echinodermata (1 species), Platyhelminthes (1 species) and Cnidaria (1 species).

From 2007 to 2009, abundant benthic macrofauna (taxa accounting for greater than 5% of total abundance combined) at the reef included the nerite Nerita yoldi Recluz, the Asian periwinkle Littorina brevicula (Philippi, 1844), the periwinkle Littoraria intermedia (Philippi, 1846), and the nereid worm Perinereis aibuhitensis Grube. The microcotylid monogeneans Lutianicola sp. increased in 2008 and accounted for 13% of the total abundance for that year. Overall, N. yoldi accounted for 39.6% of the total abundance and was the most abundant reef resident, followed by L. brevicula (19.4%), P. aibuhitensis (13.1%), and L. intermedia (12.1%). Mollusca dominated the samples in abundance regardless of sampling period (Table 3, Fig. 4). Relative abundance of molluscan species declined with reef development, whereas crustaceans and polychaetes increased (Fig. 4).

Species richness of benthic macrofauna increased throughout the course of the study (Fig. 5A, B). There was a general trend of increasing absolute abundance and biomass of all organisms and several taxonomic groups (crustaceans, molluscs, and polychaetes) with reef development (Fig. 5C-J). The total abundance and biomass of benthic macrofaunal communities differed significantly (P < 0.05, Table 1) among sampling sites (salinity) and among intertidal levels (exposure), with greater values found in the lower intertidal zone and at sites with higher mean salinity (P < 0.05, Table 1). There was a significant interaction (P < 0.05, Table 1) between site and intertidal level for the total biomass of benthic macrofauna in most years. The mean abundance and biomass of benthic macrofauna generally showed increasing trends along the salinity gradient.

Correlations Between Oyster and Benthic Macrofauna

Correlation coefficients between oyster biomass and the overall benthic macrofaunal community (species richness, abundance, and biomass) varied considerably. Generally, the oyster abundance showed similar correlations with benthic macrofaunal community descriptors as did oyster biomass. There were significantly (P < 0.05) positive correlations between oyster biomass and polychaetes (abundance and biomass), with one exception being biomass in July 2009 (P > 0.1, Table 2). There were consistent negative correlations between molluscs and oysters; however, only 4 of the 12 paired components across the study were statistically significant (P< 0.05) (see Table 2). In 6 of 12 observations, crustaceans were positively correlated with oyster biomass (Table 2).


Crassostrea ariakensis: An Ecosystem Engineer

Through the recruitment, settlement, and growth of the larvae released by transplanted C. ariakensis seed, a complex 3-dimensional habitat was created for other benthic macrofaunal species. Our results using C. ariakensis provide results similar to studies that examined reefs created by the Eastern oyster Crassostrea virginica (Gmelin, 1791) (e.g., Rodney & Paynter 2006, Hadley et al. 2010), the Pacific oyster Crassostrea gigas (Thunberg, 1793) (e.g., Lejart & Hily 2011), the Olympia oyster Ostrea lurida (Carpenter 1864) (e.g., Dinnel et al. 2009), and the European oyster Ostrea edulis (e.g., Smyth & Roberts 2010) in which structure facilitated habitat creation for reef-associated species. Harwell et al. (2010) concluded functional equivalency between C. virginica and C. ariakensis through comparisons of habitat complexity and associated benthic communities in the Chesapeake Bay. The oyster C. ariakensis can provide suitable habitat for benthic communities that is similar to that of other species and can therefore be considered an ecosystem engineer (Coen & Luckenbach 2000) in the Yangtze River estuary, China.

This study shows that C. ariakensis can establish self-sustaining oyster populations and create a complex 3-dimensional reef structure in the intertidal zone. We found that C. ariakensis had generally greater abundance in the low intertidal zone than the high intertidal zone, but that C. ariakensis could survive for relatively long emersion periods (approximately 3 h) in the middle and high intertidal zones. This contrasts with previous findings in the Chesapeake Bay, where no C. ariakensis survived in the high intertidal (3.5-h emersion) and middle intertidal (2-h emersion) zones (Kingsley-Smith & Luckenbach 2008). Kingsley-Smith and Luckenbach (2008) also reported that C. ariakensis suffered from higher mortality when exposed in the high intertidal zone, but that C. ariakensis grew faster than C. virginica in subtidal locations. One possible explanation for this is that local variations (native vs. nonnative) in emersion time resulting from the neap-spring cycle and meteorological conditions affected the tolerance of C. ariakensis to aerial exposure, desiccation, and thermal stress (Kingsley-Smith & Luckenbach 2008).

Oyster Development

Oyster spat began to settle on the artificial modular reef immediately after seed transplanting in 2004, and the highest abundances were present 1 y later. After this initial colonization, a rapid decrease was observed in mean oyster abundance, possibly because of a self-thinning process. As in plants, the explanations for self-thinning in marine organisms emphasize intraspecific competition (Woodin & Jackson 1979). The crowded conditions reduce the per-individual ration of food and space (Petraitis 1995, Frechette et al. 1996).

The mean oyster abundance (exclusive of oyster spat < 20 mm in SH) on our created reef at the end of the 5 y of sampling (810 oysters/[m.sup.2]; mean size, 60 mm; September 2009) was higher than those recorded from restored/created subtidal reefs (Table 4), such as the Great Bay estuary, NH (200-600 oysters/[m.sup.2]) (Greene & Grizzle 2005); Chesapeake Bay, MD (173 oysters/[m.sup.2]) (Rodney & Paynter 2006); Indian River Bay, DE (254 oysters/[m.sup.2]) (Erbland & Ozbay 2008); Rappahannock River, VA (77-257 oysters/[m.sup.2]) (Luckenbach et al. 2005); and Inlet Creek, SC (497 oysters/[m.sup.2]) (Luckenbach et al. 2005). Our values were more similar to the restored subtidal reef (850 oysters/[m.sup.2]) located in Mobile Bay, AL (Gregalis et al. 2009), but were lower than those in most of the restored intertidal reefs, such as Cape Shore of Delaware Bay (2,100 oysters/[m.sup.2]) (Taylor & Bushek 2008), Fisherman's Island (~1,800 oysters/[m.sup.2]) (Nestlerode et al. 2007), and the South Carolina coast (1,460-2,887 oysters/[m.sup.2]) (Hadley et al. 2010). There was greater oyster abundance on our created reef than on natural reefs in James River, VA (300-500 oysters/[m.sup.2]) (Mann et al. 2009); West Bay, TX (38 oysters/[m.sup.2]) (Zimmerman et al. 1989); and Suwannee River estuary, FL (511 oysters/[m.sup.2]) (Bergquist et al. 2006), but means remained well below abundance found on natural reefs in Charleston harbor, SC (861-1,646 oysters/[m.sup.2]) (Luckenbach et al. 2005) and Crystal River, FL (3,800 oysters/[m.sup.2]) (Lehman 1974). The potential underestimation at our reef as a result of the exclusion of oyster spat is a possible reason for the relative low abundance compared with other restored intertidal reefs.

The trends observed in overall size distribution and SH indicated that a sustainable oyster population had established on our created reef 5 y after creation. The abundance of market-size oysters (SH [greater than or equal to] 70 mm, 95-225 oysters/[m.sup.2]) in 2007 to 2009 was comparable with that reported on natural intertidal reefs along the South Carolina coast (25-472 large oysters/[m.sup.2], SH > 60 mm), and was consistently greater than those from 45 restored reefs (77 large oysters/[m.sup.2], SH > 60 mm) throughout South Carolina (Hadley et al. 2010) and natural intertidal reefs in the Suwannee River estuary, FL (37 3-in oysters/[m.sup.2]) (Bergquist et al. 2006). Similar values were reported on the natural or constructed reef in South Carolina, with a maximum market-size percentage of 18% (Luckenbach et al. 2005).

Developing metrics to evaluate the success of restored or created oyster reefs is vital for managers and future projects (Coen & Luckenbach 2000, Powers et al. 2009, Harwell et al. 2010). A workshop sponsored by South Carolina Sea Grant in 2004 presented the most appropriate success metrics (e.g., oyster density, size frequency, associated reef fauna, reef size, reef architecture, landscape fragmentation, and water quality parameters) for oyster reef restoration based on identified project and site-specific characteristics (Coen et al. 2007b). Powers et al. (2009) evaluated the success of 94 oyster reefs (88 constructed, 6 natural) within 11 no-harvest sanctuaries located in North Carolina using the following success criteria: vertical relief more than 20 cm in height, living oyster more than 10 oysters/[m.sup.2], evidence of recent recruitment in 1 of 2 y of the survey. Harwell et al. (2010) set a target density of ~400 oysters/[m.sup.2] as success criteria for 4 restored oyster reefs in Chesapeake Bay. Our reefs (810 oysters/[m.sup.2], persistent recruitment, and complex 3-dimensional reef structure) satisfy all the aforementioned criteria and can therefore be considered a viable model to create and restore self-sustainable oyster reefs in the Yangtze River estuary, China.

Associated Assemblage Metrics

The structurally complex surface that oysters create can provide a unique habitat for reef-associated benthic organisms that serve as prey for economically and ecologically important nekton species (Harding & Mann 2001, Luckenbach et al. 2005, Quan et al. 2012). A number of studies have used quantitative or qualitative methods to investigate species demographics on natural or restored oyster reefs (e.g., Dame 1979, Larsen 1985, Zimmerman et al. 1989, Wenner et al. 1996, Luckenbach et al. 2005, Rodney & Paynter 2006, Walters & Coen 2006, Taylor & Bushek 2008, Lejart & Hily 2011). In these studies, community metrics varied substantially with site location, reef characteristics, sampling method, and physiochemical factors (Table 4). The total abundance of reef-associated benthic organisms at our created intertidal reef was most similar to those found at restored and young subtidal reefs (1-2 y) in the Rappahannock River, VA (Luckenbach et al. 2005); Indian River Bay, DE (Erbland & Ozbay 2008); and Mobile Bay, AL (Gregalis et al. 2009); but was below the values observed at older restored (e.g., Luckenbach et al. 2005, Rodney & Paynter 2006) or natural reefs (e.g., Frey 1946, Bahr 1974, Lehman 1974, Dame 1979, Larsen 1985, Coen et al. 1999, Walters & Coen 2006). Reef age seems to be an important factor controlling oyster development and therefore associated species demographics (Burt et al. 2011); abundance of reef-associated benthic organisms gradually increases with reef development (e.g., the current study, Coen & Luckenbach 2000, Luckenbach et al. 2005, Hadley et al. 2010), which provides evidence for the positive effect reef age has on the community metrics of other species.


In the current study, we found that the abundance and biomass of the oysters and associated benthic macrofaunal communities generally increased from the upstream to downstream portions of the reef along the salinity gradient. The greatest abundances often appeared at sampling sites S5 or S8, where higher salinities facilitated greater larvae recruitment and growth (Quan et al. 2009). Similar patterns have been recorded at natural or restored reefs (e.g., Tolley et al. 2005, Rodney & Paynter 2006, Harwell et al. 2010); however, Bergquist et al. (2006) found that percentage cover and density of live oysters were correlated inversely with salinity (10-30) in the Suwannee River estuary, FL. This was likely a result of increased predation and parasitic Dermo infection under higher salinity conditions (Bergquist et al. 2006), and these factors do not seem to be significant in the Yangtze River estuary.


Molluscs, polychaetes, and crustaceans typically dominate the benthic macrofaunal communities at natural or restored oyster reefs (Zimmerman et al. 1989, O'Beirn et al. 2004, Rodney & Paynter 2006). For example, several studies (e.g., Wells 1961, Larsen 1985, O'Beirn et al. 2004, Rodney & Paynter 2006) demonstrated that these 3 taxonomic groups accounted for approximately 70% of the total species number of benthic organisms in natural and subtidal oyster reefs. However, polychaetes (5 species) recorded at our created reef were less abundant in the total species assemblage compared with other studies (Wells 1961, Larsen 1985). The main contributors (>75%) to species richness in our created reefs were crustaceans (14 species) and molluscs (12 species). Rank and composition within each taxonomic group was similar to results from previous oyster reef studies in the United States (e.g., Zimmerman et al. 1989, O'Beirn et al. 2004, Rodney & Paynter 2006); gastropods ranked first in abundance followed by crustaceans. Interestingly, the relative abundance of molluscs generally decreased with reef development, whereas an increasing trend was evident for crustaceans and polychaetes. In addition, crab densities (98 crab/[m.sup.2] in September 2009) at our intertidal reef were considerably lower than those reported on restored intertidal oyster reefs along the North Carolina coast (150 crab/ [m.sup.2]) (Meyer & Townsend 2000); the South Carolina coast (158-360 crab/[m.sup.2]) (Hadley et al. 2010); Mobile Bay, AL (~170 crab/[m.sup.2]) (Gregalis et al. 2009); and the Caloosahatchee estuary of Florida (640 crab/[m.sup.2]) (Tolley & Volety 2005); but were similar to those on the restored subtidal reef at Inlet Creek, SC (100 crab/[m.sup.2]) (Luckenbach et al. 2005) and the natural subtidal oyster beds in Barataria Bay, LA (111 crab/[m.sup.2]) (Plunket & La Peyre 2005). Similarity, the mean abundance of polychaetes (<200 individuals/[m.sup.2]) at our reef was lower than those observed from restored subtidal reefs in the Chesapeake Bay (approximately 1,300 polychaetes/[m.sup.2]) (Rodney & Paynter 2006) and natural intertidal reefs in West Bay, TX (about 3,000 individuals/[m.sup.2]) (Zimmerman et al. 1989).

Relationship Between Oyster Population and Benthic Macrofaunal Community

The barnacle B. albicostatus was the most abundant sessile invertebrate other than C. ariakensis on the reef. The barnacles had greater settlement and recruitment than oysters during the early stages of reef deployment (April to September 2004); however, its mean abundance and biomass declined with reef development. Luckenbach et al. (2005) also observed a decline in barnacle densities on a restored subtidal oyster reef in the Rappahannock River, VA. In contrast to the spatial patterns of the oyster, the mean abundances and biomass or B. albicostatus gradually decreased from the high intertidal zone to the low intertidal zone throughout the current study. Other studies have recorded similar zonation patterns for oysters and barnacles as a result of competitive exclusion for space and food (Luckens 1975, Lohse 2002, Luckenbach et al. 2005).

Associations between overall benthic macrofauna descriptors and oyster population metrics (abundance and biomass) were not always consistent at our created reef (Table 2). However, when benthic macrofauna were examined by phylum or functional group, stronger correlations were present. Polychaetes and crustaceans were consistently correlated with oyster development in the current study. This result is consistent with other studies (e.g., Bergquist et al. 2006, Hadley et al. 2010) and may indicate that reef structural complexity and interstitial space provide refugia for crustaceans and polychaetes. Conversely, molluscs failed to be consistently correlated with oyster development and, therefore, may be less dependent on oysters for habitat. Similar patterns have been reported for the Chesapeake Bay in that there were no significant correlations between oyster metrics and overall assemblage parameters of resident benthic organisms (Luckenbach et al. 2005, Hadley et al. 2010). These results may demonstrate that other factors such as environmental (e.g., salinity) or spatial (e.g., setting, landscape fragmentation, connectivity) characteristics could mediate benthic macrofauna more so than oyster populations (Grabowski et al. 2005). For example, several studies indicated that salinity appeared to be a stronger predictor of community metrics of benthic organisms than oyster reef development (e.g., Tolley et al. 2005, Bergquist et al. 2006, Harwell et al. 2010). Future studies should aim to determine the relative contributions of these factors and the interplay between biotic and abiotic interactions.

Conclusions and Implications

This study showed that self-sustaining oyster populations have been established through transplanting seed oysters at a created reef in the Yangtze River estuary, China, and may be considered an ecosystem engineer in this system. Oysters colonized the reef quickly, grew to market size, and now represent a thriving population. Greater abundance of oysters was found in the lower intertidal zone and at higher salinities, whereas barnacles showed opposite trends. The species number, abundance, and biomass of associated benthic macrofauna generally showed increasing trends with reef development, or age. However, oyster abundance appeared to be a stronger predictor for barnacles, crustaceans, and polychaetes rather than total abundance and diversity of overall benthic macrofauna or molluscs. In the future, additional monitoring of reef development and function is needed to track ecological succession of restored and created oyster reefs to determine the relative contributions of oyster development and environmental forcing in mediating associated organisms.


We thank Yun-long Wang, Jiang-xin Zhu, Ming-bo Luo, Ang-lv Shen, Yun-long Zhao, and Chuan-guang An, who contributed to the ideas and provided help with sample collection and processing. This study was supported by grants from the Special Research Fund for the National Non-profit Institutes (East China Sea Fisheries Research Institute) (2011M01), the Administration Bureau of Navigation in Yangtze River estuary, and the National Key Basic Research Program of China (973 program; no. 2010CB429005).


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(1) Key and Open Laboratory of Marine and Estuarine Fishery Resource and Ecology, Ministry of Agriculture, East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, 300 Jungong Road, Yang Pu District, Shanghai 200090, China; (2) School of Renewable Natural Resources, Louisiana State University AgCenter, 227 Renewable Natural Resources Bldg, Baton Rouge, LA 70803

* Corresponding author. E-mail: quanweim@ 163.com

([dagger]) Current address: Coastal Research Group, Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa

DOI: 10.2983/035.031.0302
Mean biomass by site (see text for abbreviations) and 2-way ANOVA
results for the oyster Crassostrea ariakensis, barnacle Balanus
albicostatus, and benthic macrofauna on the created reef.

                                  Mean biomass (g/[m.sup.2])

                       S2      S5       S8       H       M        L

  August 2007          986   1,897    5,096     391   3,008    4,309
  November 2007        769   1,561      409     101     531    2,632
  April 2008           812   2,192      703     183   1,376    2,122
  July 2008          2,308   3,414    3,363     601   3,013    4,481
  May 2009             919   4,153    4,590     440   2,737    5,988
  September 2009     1,798   5,533    2,320   1,555   2,687    5,584
  August 2007          275   1,041    1,429   1,343     699      110
  November 2007        512     486    1,703   1,139   1,091      569
  April 2008            19     879    1,514   1,038     522      266
  July 2008          1,667     703      250   1,575     567      188
  May 2009              17     676      961     958     517      463
  September 2009       404     416      476   2,458     175        0
Benthic macrofauna
  August 2007        14.75   21.22    51.82   51.28   38.47    33.48
  November 2007      10.03   30.07    36.96   28.46   23.76    25.06
  April 2008         13.47   31.57    83.23   51.51   36.05    32.55
  July 2008          21.20   51.32    70.98   29.84   55.04    54.60
  May 2009           11.31   51.18   170.09   27.26   63.54   122.35
  September 2009     18.41   28.78    96.69   47.12   19.38   69.644

                                       2-Way ANOVA

                     Sites (df= 4)      Intertidal         Site x
                                         (df= 2)         Intertidal
                                                          (df = 8)

  August 2007       19.56 (<0.001)#   31.88 (<0.001)#  13.53 (<0.001)#
  November 2007     12.09 (<0.001)#   16.97 (<0.001)#  11.87 (<0.001)#
  April 2008         3.69 (0.023)#    30.73 (<0.001)#   0.87 (0.531)
  July 2008          4.08 (0.009)#    21.13 (<0.001)#   0.99 (0.462)
  May 2009           6.83 (<0.001)#   18.69 (<0.001)#   3.70 (0.003)#
  September 2009    40.84 (<0.001)#   68.40 (<0.001)#  16.86 (<0.001)#
  August 2007       15.90 (<0.001)#  260.60 (<0.001)#  15.91 (<0.001)#
  November 2007      7.25 (0.003)#    16.80 (<0.001)#   7.79 (<0.001)#
  April 2008        11.40 (<0.001)#    5.29 (0.011)#    1.12 (0.377)
  July 2008          2.83 (0.042)#    11.39 (<0.001)#   1.09 (0.396)
  May 2009          26.64 (<0.001)#    2.85 (0.073)     5.95 (0.007)#
  September 2009     2.09 (0.111)     16.74 (<0.001#    3.90 (0.002)#
Benthic macrofauna
  August 2007       10.30 (<0.001)#   12.46 (0.001)#    3.06 (0.012)#
  November 2007      6.95 (<0.001)#    1.94 (0.158)     4.05 (0.003)#
  April 2008         7.27 (<0.001)#    1.24 (0.304)#    0.72 (0.640)
  July 2008          4.53 (0.006)#     6.85 (0.004)#    3.31 (0.008)#
  May 2009          18.55 (<0.001)#   14.93 (<0.001)#   1.72 (0.141)
  September 2009    19.24 (<0.001)#   14.70 (<0.001)#   6.82 (<0.001)#

F values are shown with significance level (P value) in
parenthesis. Bold type indicates statistical significance
(p < 0.05).

Note: Statistical significance (p < 0.05) indicated with #.

Correlations between oyster biomass and reef community metrics
(species richness, abundance, biomass) by sampling date for the
created intertidal reef in the Yangtze River estuary.

                        Barnacle               Total

Oyster   S              Abundance   Bio-mass   Abundance   Bio-mass

Oyster biomass in August 2007
r         0.464#        -0.639#     -0.712#    -0.130      -0.037
P         0.001#        <0.001#     <0.001#     0.385       0.805
Oyster biomass in November 2007
r         0.041         -0.539#     -0.605#    -0.196       0.102
P         0.780         <0.001#     <0.001#     0.181       0.492
Oyster biomass in April 2008
r         0.030         -0.715#     -0.657#    -0.173       0.112
P         0.852         <0.001#     <0.001#     0.272       0.479
Oyster biomass in July 2008
r         0.096         -0.547#     -0.550#    -0.259       0.324#
P         0.531         <0.001#     <0.001#     0.085       0.030#
Oyster biomass in May 2009
r         0.488#        -0.558#     -0.549#     0.409#      0.584#
P        <0.001#        <0.001#     <0.001#     0.005#     <0.001#
Oyster biomass in September 2009
r        -0.158         -0.426#     -0.425#    -0.440#      0.015
P         0.172         <0.001#     <0.001#    <0.001#      0.894

         Crustacean             Mollusca

Oyster   Abundance   Bio-mass   Abundance   Bio-mass

Oyster biomass in August 2007
r        0.248        0.362#    -0.188      -0.169
P        0.093        0.013#     0.206       0.256
Oyster biomass in November 2007
r        0.066       -0.002     -0.261      -0.240
P        0.657        0.988      0.073       0.100
Oyster biomass in April 2008
r        0.268        0.288     -0.262      -0.269
P        0.086        0.065      0.094       0.085
Oyster biomass in July 2008
r        0.465#       0.538#    -0.235      -0.167
P        0.001#      <0.001#     0.121       0.274
Oyster biomass in May 2009
r        0.453#       0.476#    -0.293#     -0.463#
P        0.003#       0.001#     0.050#      0.001#
Oyster biomass in September 2009
r        0.163        0.312#    -0.601#     -0.439#
P        0.159        0.006#    <0.001#     <0.001#


Oyster   Abundance   Bio-mass

Oyster biomass in August 2007
r         0.522#      0.429#
P        <0.001#      0.003#
Oyster biomass in November 20
r         0.620#      0.728#
P        <0.001#     <0.001#
Oyster biomass in April 2008
r         0.560#      0.630#
P        <0.001#     <0.001#
Oyster biomass in July 2008
r         0.325#      0.234
P         0.029#      0.122
Oyster biomass in May 2009
r         0.683#      0.630#
P        <0.001#     <0.001#
Oyster biomass in September 2
r         0.397#      0.410#
P        <0.001#     <0.001#

Sample size, n = 90 for overall sample number (5 sites x 3 tidal
levels x 6 quadrats).

P, probability of r = 0. r, Pearson product coefficients; S,
species richness (species each 0.09/[m.sup.2]). Bold type
indicates statistical significance (p < 0.05).

Note: statistical significance (p < 0.05) indicated with #.

Total number of benthic macrofauna (total area surveyed, 16.2
[m.sup.2]) collected on the created intertidal oyster reef  in
the Yangtze River estuary, China.

Phylum           Species                     2007   2008   2009  Total

Crustacea        Alpheus japonicas              4      0     52     56
                   (snapping shrimp)
                 Eriocheir leptognathus        18     13     17     48
                   (grapsid crab)
                 Gnorimosphaeroma rayi          0      0    109    109
                 Hemigrapsus penicillatus       1      0      6      7
                   (grapsid crab)
                 Hemigrapsus sanguineus         0      0      6      6
                   (grapsid crab)
                 Metopograpsus latifrons      is      30      2     47
                   (grapsid crab)
                 Metopograpsus jrontalis        1      0      0      1
                   (grapsid crab)
                 Metopograpsus                  1      0      6      7
                   (grapsid crab)
                 Orchestia platensis            0      0     44     44
                 Pilumnus scabrisculus         19     36     50    105
                   (xanthid crab)
                 Sesarma dehaani(grapsid       13      0      8     21
                 Sesarma bidens (grapsid       14      0      9     23
                 Sesarma tripectinis            2      0      0      2
                   (grapsid crab)
                 Svnidotea laevidorsalis       12      0     23     35

Mollusca         Barbatia bistrigata           61     77    182    320
                   (ark clam)
                 Diodora mus (fissurellid       0      1      0      1
                 Littoraria intermedia        963    192    237  1,392
                   (littorine snail)
                 Littorina brevicula          686  1,031    509  2,226
                   (littorine snail)
                 Modiolus favidus              30      0     13     43
                   (mytilid mussel)
                 Nerita yoldi (nerite       1,887  1,079  1,579  45,45
                 Purpura clavigera              4      0     17     21
                   (muricid snail)
                 Pyrene bella (pyramid          1      0     46     47
                 Rapana bezoar (muricid         0      0      1      1
                 Sinonovacula constricta        0      1      0      1
                   (razor clam)
                 Trapezium liratum              0      0     16     16
                   (trapezid clam)
                 vignadida atrata              48     72     51    171
                   (mytilid mussel)
Polychaeta       Arnaeana occidentalis          1      0      5      6
                   (terebellid worm)
                 Neanthes japonica             98      0      0     98
                   (nereid worm)
                 Nephtvs polvbranchia           0      0      7      7
                   (nephtyid worm)
                 Perinereis aibzrhitensis     222    404    874  1,500
                   (nereid worm)
                 Perinnereis nuntia             0      0    110    110
                   (nereid worm)
Echinodermata    Protankyra bidentata           0      0      1      1
                   (synaptid sea cucumber)
Platyhelminthes  Lutianicola sp.                8    440      0    448
Cnidaria         Haliplanella sp.               0      6      4     10
                   (acontiate sea anemone)
Chordata         Liciogobius guttatus           1      2     11     14
                 Omobranchus elegans            1      0      0      1

Comparisons of oyster and associated benthic macrofauna at various
natural or restored oyster reefs worldwide.

                                                  Oyster abundance
                          Reef           Reef       (individuals/
Location            Characteristics     Age (y)      [m.sup.2])

Great Bay         Restored, subtidal       1          200-600 *
  Estuary, NH
Potomac           Natural
  River, MD
Chesapeake        Restored, subtidal      3-5    173 [+ or -] 25.5 *
  Bay, MD
Cape Shore, DE    Restored, intertidal     1           2,100 *

Indian River      Restored, subtidal       2       254.4 [+ or -]
  Bay, DE                                               73.6 *
Rappahannock      Restored, subtidal       2          77-257 *
  River, VA
Fisherman's       Restored, intertidal     3          ~1,800 *
  Island, VA
James River, VA   Natural                             300-500 *

James River       Natural
  Estuary, VA
Great Wicomico    Restored, subtidal       3      1,026.7 [+ or -]
  River, VA                                          51.5 (HRR)
                                                    250.4 [+ or -]
                                                     32.3 (LRR)
North Inlet, SC   Natural, intertidal
Inlet Creek, SC   Restored, intertidal     6     497 [+ or -] 282 *

Charleston        Natural, intertidal               861-1,646 (a)
  harbor, SC
South Carolina    Restored, intertidal     3        1,460-2,887 *
Sapelo Island,    Natural, intertidal
Mobile Bay, AL    Restored, subtidal       1            850 *

West Bay, TX      Natural, intertidal                   38 *

Suwannee River    Natural, intertidal                   511 *
  estuary, FL
Crystal River,    Natural                              3,800 *
Yangtze River     Restored, intertidal     5      810 [+ or -] 295
  estuary, China                                     ([dagger])

                   Resident Epibenthic Macrofauna

Location            Species no.      (individuals/[m.sup.2])

Great Bay
  Estuary, NH
Potomac                 41                   ~4,000
  River, MD
Chesapeake              35                    4,057
  Bay, MD
Cape Shore, DE

Indian River                                   414
  Bay, DE
Rappahannock                            ~900 ([section])
  River, VA
  Island, VA
James River, VA

James River             142               5,757-57,857
  Estuary, VA
Great Wicomico
  River, VA

North Inlet, SC         37                 2,476-4,077
Inlet Creek, SC                              ~2,200

  harbor, SC
South Carolina                     418-3,989 mussel/[m.sup.2],
  coast                              158-360 crab/[m.sup.2]
Sapelo Island,          42                    3800
Mobile Bay, AL          21                     900

West Bay, TX       63 (winter),         56,400 (winter),
                    59 (summer)          34,200 (summer)
Suwannee River          31
  estuary, FL
Crystal River,          31                    6200
Yangtze River           45              765 [+ or -] 241
  estuary, China                        ([double dagger])

Location                Source

Great Bay          Greene and
  Estuary, NH        Grizzle (2005)
Potomac            Frey (1946)
  River, MD
Chesapeake         Rodney and
  Bay, MD            Paynter (2006)
Cape Shore, DE     Taylor and
                     Bushek (2008)
Indian River       Erbland and
  Bay, DE            Ozbay (2008)
Rappahannock       Luckenbach
  River, VA          et al. (2005)
Fisherman's        Nestlerode
  Island, VA         et al. (2007)
James River, VA    Mann
                     et al. (2009)
James River        Larsen (1985)
  Estuary, VA
Great Wicomico     Schulte
  River, VA          et al. (2009)

North Inlet, SC    Dame (1979)
Inlet Creek, SC    Luckenbach
                     et al. (2005)
Charleston         Luckenbach
  harbor, SC         et al. (2005)
South Carolina     Hadley
  coast              et al. (2010)
Sapelo Island,     Bahr (1974)
Mobile Bay, AL     Gregalis et al.
West Bay, TX       Zimmerman
                     et al. (1989)
Suwannee River     Bergquist
  estuary, FL        et al. (2006)
Crystal River,     Lehman (1974)
Yangtze River      Current study
  estuary, China

* All live oysters.

([dagger]) Oyster shell height [greater than or equal to] 20 mm
exclusive of recruits.

([double dagger]) Exclusive of barnacles, the barnacle Balanus
aibicostatus was the most abundant reef resident exception for
the oyster Crassostrea ariakensis. HRR, restored high-relief
reef, LRR, restored low-relief reef.
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