Faunal utilization of constructed intertidal oyster (Crassostrea rivularis) reef in the Yangtze River estuary, China

Ecological Engineering 35 (2009) 1466–1475

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Faunal utilization of constructed intertidal oyster (Crassostrea rivularis) reef in the Yangtze River estuary, China Wei-min Quan ∗ , Jiang-xing Zhu, Yong Ni, Li-yan Shi, Ya-qu Chen ∗ Key and Open Laboratory of Marine and Estuarine Fishery, Ministry of Agriculture, East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, China

a r t i c l e

i n f o

Article history: Received 13 January 2009 Received in revised form 12 May 2009 Accepted 1 June 2009

Keywords: Community Fish Habitat Restoration Nekton

a b s t r a c t An intertidal oyster reef (∼260 ha) was created by planting hatchery-reared seed oysters (Crassostrea rivularis) on an artificial concrete modular reef in the Deepwater Navigation Channel Regulation Project of the Yangtze River estuary. We examined the development of reef communities (oyster, barnacle and motile epibenthic macrofauna), characterized nekton use and assessed the habitat value of the constructed reef. The C. rivularis oyster population showed a rapid exponential increase with time and reached maximum density (3410 ± 241 ind./m2 ) and biomass (3175 ± 532 g/m2 ) after one year of restoration. The barnacle Balanus albicostatus was the most abundant sessile macrofauna and had a significantly greater density in the high intertidal zone than in the low intertidal zone (P < 0.05). The reef also supported diverse motile epibenthic macrofauna (11 mollusks, 11 crustaceans, 4 annelids and 2 fishes), and the reef-associated communities were numerically dominated by Neanthes japonica, Perinereis aibuhitensis, Nerita yoldi and Littorinopsis intermedia. A total of 50 nekton species (31 fishes, 9 shrimps and 10 crabs) utilized the constructed intertidal oyster reef, and grass shrimp Palaemon spp. dominated the nekton communities in term of abundance. Since the constructed intertidal oyster reef supports a variety of reef communities and abundant nektons, it should be recognized as an important and protective fish habitat in the Yangtze River estuary. Crown Copyright © 2009 Published by Elsevier B.V. All rights reserved.

1. Introduction Oyster reefs are widely recognized as key marine habitats (Jackson et al., 2001) that also provide numerous economic and ecological benefits, including commercial fisheries (Breitburg et al., 2000; Peterson et al., 2003), water quality purification (Dame et al., 2000; Newell, 2004), erosion control (Meyer et al., 1997), biodiversity conservation (Coen and Luckenbach, 2000; Thomsen et al., 2007), fish habitats (Meyer and Townsend, 2000; Steimle and Zetlin, 2000) and nutrient cycling (Dame et al., 1984; Dame and Libes, 1993; Lehnert and Allen, 2002). In the past century, most of the oyster reefs on the Atlantic coast of the USA diminished due to overfishing, habitat destruction and outbreak of disease, which led to the decline of oyster production, loss of dominant suspensionfeeder, higher frequency of toxic dinoflagellate blooms as well as degradation of aquatic ecosystems (Hackney, 2000; Jackson et al., 2001; McCormick-Ray, 2005).

∗ Corresponding authors at: East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, 300 Jungong Road, YangPu District, Shanghai 200090, China. Tel.: +86 21 6568 0293; fax: +86 21 6568 0293. E-mail addresses: [email protected] (W.-m. Quan), [email protected] (Y.-q. Chen).

Since the late 1950s, substantial state and federal resources have been allocated in an attempt to restore and rebuild the oyster reefs in several coastal states of the USA, including North Carolina, Maryland, Virginia and Florida (Meyer and Townsend, 2000; Mann and Powell, 2007). Many studies demonstrated that restored or constructed oyster reefs provided three-dimensional complex habitats and rich food resources for large variety of macroinvertebrates and fish, including fishery species (Lehnert and Allen, 2002; Grabowski et al., 2005; Boesch, 2006). However, most efforts have focused on species richness and community structure of resident macrofauna on constructed oyster reefs over a short-period or with coarse temporal resolution (Coen and Luckenbach, 2000). Additionally, as the existing knowledge of oyster reefs was mainly obtained from the USA (Meyer and Townsend, 2000; Lehnert and Allen, 2002; Rodney and Paynter, 2006), we know little about the ecological importance of oyster reefs in other countries such as China. The Yangtze River is the largest river in China and the third largest in the world. It originally carried about 928 × 109 m3 year−1 of water and 468 × 106 t year−1 of fine sediments into the East China Sea (Chen et al., 1986). More than half of the sediments from the river were deposited in the estuarine area, which formed a large area of sand bar and seriously decreased the shipment capability of the Yangtze River, which had been called the “golden channel” (Chen et al., 1986). In order to deepen the navigation channel, the

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W.-m. Quan et al. / Ecological Engineering 35 (2009) 1466–1475

Chinese government authorized the Deepwater Navigation Channel Regulation Project of the Yangtze River estuary (hereafter called DNCRP) in 1997. Two dikes (south dike: 48 km, north dike: 49.2 km) and 19 groins (total length: 30 km) were constructed to increase water flow and decrease sediment deposition. These dikes and groins constructed an intertidal concrete modular reef (∼260 ha) in the Yangtze River estuary. In April 2004, an oyster reef restoration project was initiated to mitigate the damage and disturbance to the Yangtze River estuary ecosystem caused by DNCRP. As the natural recruitment and settlement of larval oysters occur at very low rates, about 20 t of hatchery-reared seed oysters (Crassostrea rivularis) from Xiangshan Bay (Zhejiang Province) were transplanted to the artificial concrete modular reef (dikes and groins) in the DNCRP to create an intertidal oyster reef (Chen et al., 2003). Since the restoration, several field surveys have been conducted to examine the increase in the C. rivularis oyster population and characterize the utilization of the constructed intertidal oyster reef by motile epibenthic macrofauna and mobile nektons. The primary objective of this study was to comprehensively evaluate the habitat value and ecological importance of the constructed intertidal oyster reef. 2. Material and methods 2.1. Study site The DNCRP is located on the north passage of the south channel in the Yangtze River estuary (Fig. 1). The two dikes and 19 groins that constitute the hard substrata for the constructed intertidal oyster reef were built from concrete modular with a total length of 130 km, a mean width of 20 m and height of 2.5 m above the mean low water. The Yangtze River estuary is a low-salinity, well-mixed estuary with a semi-diurnal mesotidal regime averaging 4.5 m in spring tides and 2.6 m in neap tides. The climate is characterized by an annual precipitation of 1124 mm and a mean temperature of 15.7 ◦ C (Chen et al., 1986). 2.2. Sample collection and processing We visited the intertidal oyster reef during spring tides in September 2004, June 2005 and August 2007. Sessile and motile epibenthic macrofauna were examined by density quadrat method

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during each field investigation. A total of six sampling sites were set along an increasing salinity gradient (Fig. 1). At each sampling site, three tidal levels were sampled: high intertidal, middle intertidal and low intertidal. The high intertidal level was defined as the top of the artificial concrete modular reef (dikes and groins), while the low intertidal level was defined as the mean low water during spring tides and the middle intertidal level was located at the halfway point between the high and low intertidal levels of the constructed oyster reef. At each tidal level, six replicate 0.3 m × 0.3 m quadrat samples were collected at slack low tide. All the material in each 0.09 m2 quadrat was excavated to determine the macrofaunal species richness, density and biomass. Excavated material was cleaned on a 1.0-mm mesh sieve and retained material was examined for macrofauna (i.e., oyster, barnacles, decapods, mollusks, annelids and fishes). All live organisms were preserved in 75% ethanol and identified, enumerated and weighed in the laboratory. The weight of the mollusks was transformed to the biomass based on the ratio of flesh to shell. The density and biomass of the macrofauna were expressed as the individuals and weight per m2 , respectively. During low tide, salinity was determined in parts per thousand (‰) using a temperature-compensated refractometer, water temperature by field thermometer and total suspended sediment (TSS) by the filtration method. In the last field investigation (August 2007), we sampled nektons entering the constructed intertidal oyster reef at flood tide and leaving at ebb tide. Nekton samples for quantitative analysis were collected with the aid of local fisherman during daylight hours by means of fish traps. The fishing gear was mainly used to collect the demersal nektons that utilized the intertidal oyster reef. At slack low tide at each sampling site, six fish traps were deployed at 50 m intervals along a straight line to the bottom of the constructed oyster reef (Fig. 1). Each fish trap was composed of 30 rectangular cages (0.5 m × 0.3 m × 0.3 m height) with steel bars and plastic coated wire. The top and bottom of each fish trap were made of 10 mm steel rebar bent into a rectangular box structure with walls of 4 mm nylon mesh. The walls of each rectangular box were sloped to form entrance tunnels that extended inwardly from opposite ends of the trap and terminated in a rectangular frame, which provided an opening through which the nektons could fall. In two ends of the fish trap, one mesh bag was set for collecting nekton samples. A bridle (6 mm rope) for lifting the trap was attached to the tail of the

Fig. 1. Study site locations. (a)Yangtze River estuary, China. (b) Artificial concrete modular reef and six sampling sites (solid black circles). (c) Schematic diagram of density quadrat (empty circles) and fish trap (solid triangles) deployment for collecting macrofauna.

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Table 1 Physical properties of overlaying water in the constructed intertidal oyster reef (August 2007). Site

Water temperature (◦ C)

Salinity (‰)

SS (mg/l)

S2 S5 S8 N2 N6 N9

29.5 29.3 30.0 29.5 29.8 29.7

2.03 3.87 16.05 0.46 10.02 16.02

743 742 356 841 671 298

mesh bag and two metal buoys marked the location of each trap. The apparatus was retrieved and the sample was collected at the next low tide. Additionally, at high tide a gill net (mesh: 30 mm; height: 1.5 m; length: 100 m) was deployed at each sampling site for 3 h to collect the pelagic nektons that utilized the constructed oyster reef. The samples collected by gill nets were only used to qualitatively identify the species that utilized the reef, while the data from the fish traps were used to characterize the composition and structure of the nekton communities on the constructed oyster reef. All the nekton samples were preserved in a 10% formalin solution. The organisms were identified to species level, measured to the nearest 1 mm and weighted to 0.1 g. Relative abundance (N%) and weight (W%) of each species were calculated as percentage of the total catch from the fish trap, which permitted identification of the dominant taxa of the nekton communities.

Fig. 2. Mean (±SE, n = 6) biomass and density of the oyster Crassostrea rivularis in the high (H), middle (M) and low intertidal (L) zones of the constructed oyster reef in August 2007. A star indicates that no data were collected. Different letters denote significant differences between the intertidal sampling levels at the sampling site (P < 0.05).

2.3. Statistical analysis One-way ANOVA (post hoc Turkey-HSD test) was carried out to examine the differences in density and biomass of macrofauna among the three tidal levels at each sampling site (P < 0.05). When assumptions of homogeneity of variances were not met, the data were log (x + 1) transformed prior to statistical analysis. Multivariate statistic (PRIMER software package, version 6.0) was utilized to compare the structure of nekton communities among the six sampling sites (Clarke, 1993). Using a ranked similarity matrix based on Bray–Curtis similarity measures, an ordination plot was produced by non-metric multi-dimensional scaling (MDS). 3. Results 3.1. Physical properties Water temperature at all sampling sites was relatively consistent but typically varied with seasons. Low tide salinity varied substantially between 0.46‰ and 16.05‰, and showed an increasing trend from upper to lower stations of the constructed oyster reef. TSS ranged between 300 and 800 mg/l, and showed a decreasing trend from upper to lower stations of the reef (Table 1). 3.2. Sessile macrofauna (oyster and barnacles) A large number of oysters were observed at five of the six sampling sites, but not at sampling site N2. No oyster appeared in the high intertidal zone of sampling sites S2, S5 or N9. Although mean oyster density was clearly greater in the middle and low intertidal

Fig. 3. Mean (±SE, n = 6) biomass and density of the barnacle Balanus albicostatus on the constructed oyster reef in August 2007. The symbols are described in Fig. 2.

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zones than in the high intertidal zone of sampling sites S8 and N6, there were no significant differences among the three intertidal levels (P > 0.05, Fig. 2). The most abundant sessile macrofauna on the constructed oyster reef was the barnacle Balanus albicostatus. The mean density and biomass of this species were 1304 ± 223 ind./m2 and 598 ± 96 g/m2 , respectively. The greatest density (6125 ± 452 ind./m2 ) appeared in the high intertidal zone of sampling site S8, while the barnacle was absent at sampling site N2 as well as in the middle and low intertidal zones of sampling site S2. In general, the density of the barnacle B. albicostatus was greater in the high intertidal zone than in the middle or low intertidal zones, and there were significant differences between the high and low intertidal zones (P < 0.05, Fig. 3). Development of constructed oyster reef as measured by the density and biomass of the oysters increased rapidly over the three years studied (Fig. 4). Within five months after reef restoration, the density and biomass of the oyster C. rivularis increased significantly. The density and biomass of this oyster increased to the maximum values one year later. Thereafter, its density showed a significant decline (P < 0.05, Fig. 4) due to self-thinning when the oysters grew to a larger size. Correspondingly, the biomass was stable over time (P > 0.05, Fig. 4).

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Fig. 4. The increase of the oyster population on the constructed intertidal reef. The symbols are described in Fig. 2.

in June 2005 and 25 species in August 2007; the total abundance showed a significant increase with time (P < 0.05, Fig. 5). Correspondingly, the abundances of the dominant macrofauna Neanthes japonica also increased rapidly with reef development (Fig. 5). The mean density and biomass of motile epibenthic macrofauna were 409 ± 125 ind./m2 and 31.41 ± 10.9 g/m2 , respectively (Fig. 6). The greatest density (3611 ± 1162 ind./m2 ) appeared in the high intertidal zone of sampling site N9, while no macrofauna were

3.3. Motile epibenthic macrofauna A total of 28 motile epibenthic macrofauna species (11 crustaceans, 11 mollusks, 4 annelids and 2 fishes) were recorded on the constructed intertidal oyster reef (Table 2). The species richness rapidly increased from 5 species in September 2004 to 16 species

Table 2 Motile epibenthic macrofauna collected from the constructed intertidal oyster reef during the study. Species name

Site

Date

S2

S5

S8

N2

N6

N9

9/2004

6/2005

8/2007

Crustacean Alpheus japonicus Eriocheir leptognathus Hemigrapsus penicillatus Metopograpsus frontalis Metopograpsus latifrons Metopograpsus quadridentatus Pilumnus scabrisculus Sesarma bidens Sesarma dehaani Sesarma tripectinis Synidotea laevidorsalis

– P P – – – – P P – P

P – – – – P P – P P P

P – – P – – P P – – –

– – – – – – – – – – –

– – – – P – P – P P –

P P – – – – P P – – –

– – – – – – P P – – –

P – P P P – P P P – P

P P P P P P P P P P P

Mollusk Barbatia bistrigata Littorinopsis intermedia Littorina brevicula Modiolus flavidus Mytilus edulis Nassarius succinctus Nassarius variciferus Nerita yoldi Pyrene bella Thais clavigera Trapezium liratum

– – – – – – – P – – –

P P – – P P P P – – –

P P P P – P – P P P P

– – – – – – – – – – –

– P – – P P – P P – –

P P P P – P P P – – –

P – – P – – – – – – –

P P – – P P – – P – P

P P P P – P P P – P –

Annelid Neanthes japonica Perinereis aibuhitensis Serpula vermicularis Amaeana occidentalis

P – – –

P P P –

P – – P

– – – –

P P – –

– P – –

P – – –

P – P –

P P P P

Fish Liciogobius guttatus Omobranchus elegans

– –

– –

P –

– –

– –

– P

– –

– –

P P

Total species present

7

15

16

0

11

13

5

16

25

(P) Present, (–) absent.

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Fig. 5. The increase in the density of motile epibenthic macrofauna (a) and the dominant species Neanthes japonica (b) on the constructed intertidal oyster reef. The symbols are described in Fig. 2.

found at sampling site N2. The mean density and biomass of motile epibenthic macrofauna were significantly greater in the middle and low intertidal zones than in the high intertidal zone of sampling sites S2 and S8 (P < 0.05, Fig. 6). However, at sampling sites S5, N6 and N9, there were no significant differences in density or biomass of motile epibenthic macrofauna among the three intertidal sampling levels (P > 0.05, Fig. 6). The most abundant motile epibenthic macrofauna on the constructed oyster reef were N. japonica, Perinereis aibuhitensis, Nerita

Fig. 6. Mean (±SE, n = 6) biomass and density of motile epibenthic macrofauna on the constructed oyster reef in August 2007. The symbols are described in Fig. 2.

yoldi and Littorinopsis intermedia (Fig. 7). It is evident that N. japonica mainly distributed at sampling sites S2, S5 and S8. P. aibuhitensis appeared at sampling sites S5, N6 and N9, with the greatest density (75 ± 23 ind./m2 ) in the low intertidal zone of sampling site S5. One-way ANOVA found that there were no significant differences in the density of P. aibuhitensis among the three intertidal sampling levels of sampling sites N6 and N9 (P > 0.05). With the exception

Fig. 7. Mean (±SE, n = 6) density of four dominant motile epibenthic macrofauna on the constructed oyster reef in August 2007. The symbols are described in Fig. 2.

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Table 3 List of mobile nekton species collected from the constructed intertidal oyster reef by fish traps and gill nets. Species

Fig. 8. Relative abundances of nektons collected from the constructed intertidal oyster reef by fish traps.

of sampling site N2, N. yoldi was present at almost all sampling sites. The greatest density (1214 ± 568 ind./m2 ) occurred in the high intertidal zone of sampling sites N9, but there was no significant difference among the three intertidal sampling levels of sampling site N9 (P > 0.05). L. intermedia was observed at sampling sites S5, S8, N6 and N9, with the greatest density (1439 ± 447 ind./m2 ) in the high intertidal zone of sampling site N9. 3.4. Nektons A total of 50 nekton species (31 fishes, 9 shrimps and 10 crabs) were recorded on the constructed oyster reef, though only two species (Arius sinensis and Tridentiger barbatus) were common to all the sampling sites (Table 3). The main taxonomic groups included gobies, mullets, sea bass, cunner, spots, Japanese eel, puffer, mud crab, blue crab, grass shrimp and white prawn. The species richness varied greatly among the six sampling sites, with the greatest value (26) at sampling site N6 and the lowest value (15) at sampling site N2. Fig. 8 shows the relative abundances of nektons on the constructed intertidal oyster reef. The nekton communities at sampling sites S2, S5, S8 and N6 were strongly dominated by the oriental shrimp Palaemon macrodactylus (%N > 65%). The dominant nekton at sampling site N2 was the oriental river shrimp Macrobrachium nipponense. At sampling site N9, oriental shrimp P. macrodacty-

Sampling method

Sampling site S2

S5

S8

N2

N6

N9

F F F, G G G F, G F G G G F, G G F, G F, G G G G G G G F, G G G G G F G G G F G

P P P – P P P – P P P – P P P P – P – – – – – – – – – – – P –

P P P – P P P – – P P – P – – – – – – – P P – P P – – – – P –

– – P – – – P – – P P P P – – – P – P – P – – – – – – – – P –

P – P P P P – P – – – – – P P – – – – P – – – – – P – – – P P

P – P – – P P – – P P – P – – – – – – – – – – – – – P P – P P

– – P – – P P – – P P – P – – – – – – – – – P – – – – – P P –

Shrimp Alpheus japonicus Exopalaemon annandalei Exopalaemon carinicauda Leptochela gracilis Metapenaeus joyneri Macrobrachium nipponense Palaemon gravieri Palaemon macrodactylus Penaeus japonicus

F F F, G F F F F F F

– P P – – P – P –

– – P – – P P P –

P – P – – – P P –

– – – – – P – – –

P P P P – P P P P

P P P – P – P P –

Crab Charybdis affinis Charybdis japonica Eriocheir sinensis Eriocheir leptognathus Helice wuana Macrophthalmus dilatatum Macrophthalmus japonicus Portunus trituberculatus Scylla serrata Sesarma bidens

G F, G F, G F, G F G G G F, G F

– – P P – P P – – –

– P – P – – – – P P

– P – P – – – P P –

– – P P – – – – – –

– P P P P – – P P P

P P – – – – – P – –

Fish Acanthogobius ommaturus Anguilla japonica Arius sinensis Boleophthalmus pectinirostris Coilia ectenes Coilia mystus Coilichthys lucidus Cultrichthys erythropterus Cynoglossus gracilis Eleutheronema rhamdinum Harpodon nehereus Johnius belengerii Johnius distinctus Lateolabrax maculatus Liza carinatus Liza haematocheilus Miichthys miiuy Mugil cephalus Muraenesox cinereus Mylopharyngodon piceus Nibea albiflora Nibea miichthioides Odontamblyopus lacepedii Platycephalus indicus Protosalanx chinensis Saurogobio dumerili Takifugu bimaculatus Takifugu niphobles Takifugu xanthopterus Tridentiger barbatus Tridentiger trigonocephalus

Sampling methods: F – fish trap, G – gill net. (P) Present, (–) absent.

Fig. 9. Relative weight of nektons collected from the constructed intertidal oyster reef by fish traps.

lus (%N = 43.9%) and Chinese ditch prawn P. gravieri (%N = 41.2%) accounted for the nekton communities. In terms of weight, the nekton communities were highly dominated by P. macrodactylus (%W > 45%) at sampling sites S2, S5 and N6 (Fig. 9). However, at sampling sites S8 and N9, the dominant nekton in terms of weight was the Japanese stone crab Charybdis japonica (%W > 50%). At sampling site N2, M. nipponense (%W = 27.8%), Dumeril’s longnose gudgeon Saurogobio dumerili (%W = 27.4%) and Asian freshwater goby Acanthogobius ommaturus (%W = 23.4%) dominated the nekton communities in term of weight. Non-metric MDS ordination indicated spatially distinct nekton communities at the constructed reef, and found that the nekton community at sampling site N2

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Fig. 10. Non-metric multi-dimensional scaling (MDS) ordination of nekton communities on the constructed intertidal oyster reef.

was significantly different from those at the other five sampling sites (Fig. 10).

It is evident that development of oyster populations in constructed reefs is significantly correlated with substrate materials (i.e., shell, concrete/rock, coal ash, etc.) and configuration (i.e., size, shape, relief, interstitial space, etc.) of the constructed reefs (Coen and Luckenbach, 2000; Greene and Grizzle, 2005). Compared with the other reef materials, high density of oysters often recruited to and survived on shell reefs (Coen and Luckenbach, 2000). However, the mean oyster density on our constructed reef was comparable with those reported from natural or constructed reefs in USA (Coen and Luckenbach, 2000; Greene and Grizzle, 2005; Bergquist et al., 2006), which indicated that the artificial concrete modular reef in the DNCRP could recruit equivalent numbers of oysters as shell reefs. Similarly, Greene and Grizzle (2005) demonstrated that concrete/rock was a suitable choice for setting of oyster larvae in comparison to natural shell. Burke and Lipcius (2005) also recorded that an artificial concrete modular reef was heavily colonized by higher density of native oyster and mussel due to greater vertical complexity, reef stability and substrate surface area than many restored shell reefs. Consequently, the concrete modular reef in the DNCRP was high quality of substrate for oyster setting, and presented much more space allowing for greater water flow and food availability than natural shell reefs.

4. Discussion 4.2. Faunal utilization 4.1. Oyster colonization The abundance, survival and mortality of oysters vary substantially with salinity and river flow conditions (Bergquist et al., 2006). In general, oyster recruitment and adult biomass are highest at intermediate salinity levels of 5–15‰ (Hulathduwa and Brown, 2006; Volety et al., 2004). Lower salinities depress oyster reproduction and growth, but under higher salinities they typically suffer from an increase of exposure to predation and parasites (Hulathduwa and Brown, 2006). In our constructed intertidal oyster reef, the density and biomass of the oyster C. rivularis varied highly among the six sampling sites. At sampling site N2, very low salinity (∼0.5‰) suppressed oyster survival. At the other five sampling sites, the oyster density generally showed an increase along the salinity gradient (3–16‰). The present results clearly contrast with those reported by Bergquist et al. (2006). They found that percentage cover and density of live oysters were inversely correlated with salinity (10–30‰) in the Suwannee River estuary, which was likely result of increased predation and parasitic infection under higher salinity conditions. It is possible that relatively low salinities in the estuary suppressed predation and parasitic infection of the oyster C. rivularis on our constructed intertidal oyster reef. Tidal height also significantly influences the distribution and abundance of oysters in the intertidal or subtidal regions (Roegner and Mann, 1995; Bergquist et al., 2006; Hulathduwa and Brown, 2006). Intertidal oysters grow slower and support less diverse communities of associated species, while oysters living subtidally suffer from greater mortality due to increased predation and parasites (Roegner and Mann, 1995; Anderson and Connell, 1999; Bartol et al., 1999; Bergquist et al., 2006). Additionally, aerial exposure in intertidal oyster reefs also limits the foraging abilities of oyster predators (Hulathduwa and Brown, 2006). Therefore, most oyster reefs occur in the intertidal zone along the Gulf of Mexico as predators (e.g., oyster drills, stone crabs and black drum) remove most of subtidal oysters (Hulathduwa and Brown, 2006). The present study found that oyster density in the middle and low intertidal zones was greater than in the high intertidal zone. This distribution pattern may reflect the consequences of higher mortality due to reduced feeding time and increased metabolic stress associated with emergence in the high intertidal zone (Peterson and Black, 1987; Roegner and Mann, 1995).

Oysters are the key species and have been called “physical ecosystem engineers” because they add structural complexity (or microhabitats) to environment (Steimle and Zetlin, 2000; Lehnert and Allen, 2002; Kimbro and Grosholz, 2006). Oyster reefs can reduce water flow and accumulate fine sediment as well as increase the growth of benthic microalgae, which provide rich food for motile epibenthic macrofauna (Meyer and Townsend, 2000; Lehnert and Allen, 2002; Grabowski et al., 2005). Oyster reefs typically supported between 18 and 74 motile epibenthic macrofauna species at density ranging from 400 to approximately 6000 ind./m2 (Table 4). The values observed on the constructed intertidal oyster reefs were relatively lower than those reported by Dame (1979), Coen and Luckenbach (2000) and Rodney and Paynter (2006). However, the comparison was complicated by differences in location, sampling methods, size and structure of live oysters and other factors (Ross et al., 2005; Tolley et al., 2005). Natural or constructed oyster reefs not only support abundant sessile and motile macrofauna but also attract nektons that make transient use of the habitats (Coen and Luckenbach, 2000; Meyer and Townsend, 2000; Harding and Mann, 2001). Studies of species richness on oyster reefs using a variety of sampling methods have found 11–42 fish species (Table 4, Zimmerman et al., 1989; Harding and Mann, 1999, 2001; Lenihan et al., 2001; Lehnert and Allen, 2002; Coen and Grizzle, 2007). The values reported in the present study were comparable to those reported by Lehnert and Allen (2002) and Harding and Mann (1999, 2001). However, it is necessary to note the wide range of sampling gear types, geographical locations and reef characteristics involved when comparing these results to published studies of oyster reefs and shell bottoms. For example, Zimmerman et al. (1989) captured few large transient fishes on an intertidal reef in the Gulf of Mexico using drop samplers. Tolley and Volety (2005) only collected a total of 11 fishes and 7 decapods using a 1 m2 lift net on an oyster reef in Tarpon Bay. Other studies using gill nets (e.g., Harding and Mann, 1999, 2001), trawls (e.g., Harding and Mann, 1999, 2001), substrate tray (e.g., Lehnert and Allen, 2002) and flume-lift nets (e.g., Coen and Luckenbach, 2000) sampled much more intensively and may have captured more species. Surveys of oyster reefs in Maryland, Virginia, North Carolina, South Carolina and Texas found a total of 122 fish and 17 decapod species (Coen and Grizzle, 2007). The common

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Table 4 Species richness and abundance of motile epibenthic and mobile macrofauna communities found on intertidal or subtidal oyster reefs or shell habitats at various coastal locations. Location

Reef type

Motile epibenthic macrofauna Indian River Bay, Restored, subtidal Delaware Chesapeake Bay Restored, subtidal Restored, intertidal Harker’s Island, Swansboro and Snead’s Ferry, North Carolina Charleston, South Restored, intertidal Carolina North Inlet, South Intertidal Carolina Restored, intertidal Yangtze River estuary, China Mobile finfish and invertebrates Caloosahatchee estuary, Intertidal Florida Barataria Bay, Louisiana Subtidal oyster shell

Sampling method

No. of species

Abundance (ind. m−2 )

Source

Retrieving basket

18

Erbland and Ozbay, 2008

Plastic bakery tray Quadrat

35 33

414 in oyster reefs 959 in oyster cages 4057

Quadrat

74

5714

Coen and Luckenbach, 2000

Quadrat

37

2476–4077

Dame, 1979

Quadrat

28

409

The present study

Life net

11 fish, 7 decapods

Gill net, substrate tray

23 fish, 3 decapods

33.6 fish m2

Plunket, 2003

170.6 decapods m2 6.9 fish m2

Plunket and LaPeyre, 2005 Lehnert and Allen, 2002

North Inlet estuary, South Carolina

Natural, subtidal shell rubble

Substrate tray

36 fish, 14 decapods

Piankatank River, Virginia

Restored, intertidal

32 fish

Charleston, South Carolina West Bay, Texas

Restored, intertidal

Gill net, trawl, crab pots, nest substrates Flume-lift net

Intertidal

Drop sampler

Yangtze River estuary, China

Restored, intertidal

Fish trap, gill net

Rodney and Paynter, 2006 Meyer and Townsend, 2000

Tolley and Volety, 2005; Tolley et al., 2005

38.6 decapods m2

species that utilized oyster reefs were gobies, spot, striped bass, black sea bass, white perch, toadfish, scup, drum, spot, American eel, sheephead porgy, northern puffer, Atlantic cod, grass shrimp, mud crabs, blue crabs and American lobsters (Harding and Mann, 1999, 2001; Steimle and Zetlin, 2000; Lehnert and Allen, 2002). Most of these taxonomic assemblages were also present on our constructed intertidal oyster reef. Oyster reefs often rival other habitats (e.g., salt marshes, seagrass bed, muflat) in terms of species diversity and abundance of organisms because of greater availability and diversity of food (Harding and Mann, 2001; Tolley and Volety, 2005). Oyster reef communities are highly diverse, including species not found in adjacent areas of soft bottom (Dame, 1979; Meyer and Townsend, 2000). Zimmerman et al. (1989) compared abundance and diversity of fish and invertebrates at intertidal oyster reefs, salt marshes, and subtidal mud bottoms in a Texas estuary, and found that both oyster reefs and salt marshes supported more organisms than mud bottoms, with unique community assemblages. Oyster reefs attracted fewer juvenile transient fish and decapod crustaceans than salt marshes. Tolley and Volety (2005) indicated that organism density, biomass and richness were all greater for treatments with shell (live oyster clusters or cleaned, articulated shells) compared with sand-bottom (no-shell) treatments in the Caloosahatchee estuary, Florida. Additionally, several studies indicated that clutched shell bottom supports a species richness similar to that supported by three-dimensional oyster reefs (Table 4, Lehnert and Allen, 2002; Harding and Mann, 2001), but transient fish size and abundance increased as habitat complexity increased along the gradient from oyster shell bar through oyster reef (Harding and Mann, 2001). Ross et al. (2005) also revealed pair-wise positive correlations between the diversity and abundance of some important reef-associated species and the abundance and size structure of oysters.

42 fish 15 fish 4 decapods 31 fish, 19 decapods

Harding and Mann, 1999, 2001

230 grass shrimp m2 34.0 fish m2

Coen and Luckenbach, 2000 Zimmerman et al., 1989 The present study

Nekton utilization of oyster reefs often varies substantially among species or life stages (Coen and Luckenbach, 2000; Meyer and Townsend, 2000; Lehnert and Allen, 2002). Complex threedimensional oyster reef habitats provide both substrata and refuges to juvenile fish and shrimp (Meyer and Townsend, 2000; Lehnert and Allen, 2002). This may explain the presence of a large number of grass shrimp Palaemon spp. and white prawn Exopalaemon spp. on our constructed intertidal oyster reef. Posey et al. (1999) revealed the value of oyster reefs as refuges for grass shrimp Palaemonetes pugio with a mesocosm experiment. In the presence of fish predators, grass shrimp preferred to shelter among oysters rather than seagrass or shallow water. Some fish make use of oyster reef habitats as reproduction sites (Coen and Luckenbach, 2000; Lehnert and Allen, 2002). For examples, oyster toadfish often attach eggs to the underside of oyster shells, while gobies, blennies and skillet fish lay eggs on the inside of recently dead oyster shells (Coen and Luckenbach, 2000). In addition, abundant macroinvertebrates on oyster reefs also provide food for associated fish (Breitburg, 1999; Harding, 1999; Meyer and Townsend, 2000). Many predatory fishes often move into oyster reefs to forage, thus facilitating the transfer of energy from the benthos to higher trophic levels. Breitburg (1999) reported that large numbers of juvenile striped bass aggregated over the reef surface and actively fed on naked goby larvae, while adult spot, croaker and white perch primarily fed on benthic prey such as polychaetes, mollusks, small crustaceans and demersal fishes on oyster reefs. Our gut content analysis also showed that some high trophic level fishes (such as sea bass and spot) mainly predated on grass shrimp, white prawn, polychaetes, small crustaceans and gobies on the constructed intertidal oyster reef. Additionally, the present study found that nekton communities at sampling site N2 where no oyster grew were extensively different from those at other five sampling sites of the constructed oyster

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reef. A possible explanation for this difference is that either the absence of the oyster or low salinity at the sampling site led to the different nekton utilization. Similar results were reported by Tolley et al. (2005). They revealed that decapods and fishes present in oyster reefs of the upper station for each of three southwestern Florida estuaries were distinct from those at middle and lower stations, and community structures of oyster reef associates exhibited greater variability within an estuary than between estuaries. 4.3. Ecological implications and remarks To our knowledge, the present study is the first report on the constructed oyster reef in China. The results demonstrated that the constructed intertidal oyster reef supported a high density of sessile macrofauna (oysters and barnacles), diverse motile epibenthic macrofauna (28 species) and high nekton richness (50 species). Since many of the species that benefited from reef restoration are important fish prey items, the constructed oyster reef clearly has the potential to improve fishery production in the Yangtze River estuary by providing high quality habitat and prey to a variety of commercially important fishes. The preservation and restoration of oyster reefs are of great benefit to oyster fisheries and ancillary benefit to the health of aquatic ecosystem (Ulanowicz and Tuttle, 1992; Coen and Luckenbach, 2000; Walters and Coen, 2006; Mann and Powell, 2007). Our constructed intertidal oyster reef not only improved water quality by filter feeding and produced value in environmental services of about $500,000 year−1 (Quan et al., 2006, 2007), but also supported a large variety of motile macrofauna and functioned as a feeding, reproduction and refuge habitat for many estuarine and coastal fishes. Therefore, this important fish habitat in the Yangtze River estuary should be protected. A long-term program needs to be undertaken to further examine the development of the oyster population and reef community, understand the utilization pattern of the constructed oyster reef habitat by resident and non-resident macrofaunal species, and exploit the energy flow pathway and trophic relationship of the reef-associated community. Acknowledgements We wish to thank Anglv Shen, Minbo Luo, Jinhong Peng and Yongxin Zhang for their help in sample collection and processing, two anonymous reviewers and Professor Sixng Chen who made valuable comment on the manuscript. This study was supported by grants from the Administration Bureau of Navigation in Yangtze River estuary and the Special Research Fund for the National Non-profit Institutes (East China Sea Fisheries Research Institute) (2007M03). References Anderson, M.J., Connell, S.D., 1999. Predation by fish on intertidal oysters. Mar. Ecol. Prog. Ser. 187, 203–211. Bartol, I.K., Mann, R., Luckenbach, M., 1999. Growth and mortality of oysters (Crassostrea virginica) on constructed intertidal reefs: effects of tidal height and substrate level. J. Exp. Mar. Biol. Ecol. 237, 157–184. Bergquist, D.C., Hale, J.A., Baker, P., Baker, S.M., 2006. Development of ecosystem indicators for the Suwannee River estuary: oyster reef habitat quality along a salinity gradient. Estuar. Coast. 29, 353–360. Boesch, D.F., 2006. Scientific requirements for ecosystem-based management in the restoration of Chesapeake Bay and Coastal Louisiana. Ecol. Eng. 26, 6–26. Breitburg, D.L., 1999. Are three-dimensional structure and healthy oyster populations the keys to an ecologically interesting and important fish community? In: Luckenbach, M.W., Mann, R., Wesson, J.A. (Eds.), Oyster Reef Habitat Restoration: A Synopsis and Synthesis of Approaches. Virginia Institute of Marine Science Press, Gloucester Point, VA, pp. 239–250. Breitburg, D.L., Coen, L.D., Luckenbach, M.W., Mann, R., Posey, M., Wesson, J.A., 2000. Oyster reef restoration: convergence of harvest and conservation strategies. J. Shellfish Res. 19, 371–377.

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