Oyster farming control on phytoplankton bloom promoted by thermal discharge from a power plant in a eutrophic, semi-enclosed bay

Water Research 159 (2019) 1e9

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Oyster farming control on phytoplankton bloom promoted by thermal discharge from a power plant in a eutrophic, semi-enclosed bay Zhibing Jiang a, b, c, Ping Du a, b, Yibo Liao a, c, Qiang Liu a, Quanzhen Chen a, Lu Shou a, **, Jiangning Zeng a, *, Jianfang Chen a, c a Key Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, China b Function Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, China c State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 8 December 2018 Received in revised form 1 April 2019 Accepted 10 April 2019 Available online 13 April 2019

Temperature increase caused by thermal discharge from power plants promotes phytoplankton growth and frequent bloom in eutrophic subtropical waters, particularly in cold seasons. Suspension filterfeeding bivalves show size-selective grazing on phytoplankton. Thus, we hypothesized that algal bloom under thermal stimulation could be controlled and that phytoplankton community was structured by oyster farming. Here, ten cruises were conducted in two oyster farms (OFs) and control areas (CAs) adjacent to the Ninghai Power Plant in the upper section of Xiangshan Bay during 2009e2015. We found that thermal discharge induced severe winter algal blooms. Phytoplankton abundance and chlorophyll a (chla) were significantly lower (46.3% and 28.3%, respectively) in OF than in CA, indicating a high filtration efficiency by oysters and the associated biofouling assemblages. In addition, oyster farming significantly increased species richness (by 26.3%), ShannoneWiener diversity (by 38.3%), and Pielou's evenness indices (by 28.8%) and reduced suspended solids (by 12.2%), total organic carbon (by 18.4%), dissolved inorganic nitrogen (by 1.5%), and phosphorus (by 3.7%). Furthermore, oyster farming considerably reduced (increased) micro-chla contribution (pheophytin/chla) by 34.8% (71.1%), suggesting a strong size-selective grazing on phytoplankton. Analysis of similarity revealed a significant difference in phytoplankton community composition between OF and CA. However, after the removal of culture rafts, all the abundance, chla, species diversity, dominant species, size structure, and community composition of phytoplankton showed no significant difference. Our study demonstrated that oyster farming effectively alleviated eutrophication and algal bloom and enhanced phytoplankton diversity, which provides guidance for aquaculture and ecological restoration in subtropical coastal eutrophic waters. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Oyster farming Phytoplankton Size-selective grazing Species diversity Thermal discharge Xiangshan bay

1. Introduction Eutrophication is a key driver of increased harmful algal blooms in coastal waters (Heisler et al., 2008; Jiang et al., 2014). Additionally, the magnitude, frequency, and duration of harmful algal blooms have been frequently linked to warming (Moore et al., 2008; Paerl and Scott, 2010). For example, temperature increase caused by thermal discharge from power plants promotes phytoplankton growth and frequent bloom in eutrophic subtropical

* Corresponding author. ** Corresponding author. E-mail addresses: [email protected] (L. Shou), [email protected] (J. Zeng). https://doi.org/10.1016/j.watres.2019.04.023 0043-1354/© 2019 Elsevier Ltd. All rights reserved.

waters (Yu et al., 2007; Jiang et al., 2019a, 2019b). How to control eutrophication and algal blooms under accelerated warming has been the focus of research in area of environmental problems in coastal ecosystems worldwide. Oysters and the associated biofouling assemblages (OBAs; including ascidians, bryozoans, sponges, polychaete, and macroalgae) remove nutrients directly or indirectly by filtering phytoplankton and other microbial particles (Cloern, 1982; Dame, 1996; Newell, 2004; Froj
an et al., 2014; Grizzle et al., 2018) and enhance the fluxes of organic matter and nutrients toward sediments (Newell, 2004; Kellogg et al., 2014). Additionally, the harvest represents a net removal of nitrogen (N) and phosphorus (P) from the ecosystem. Therefore, the aquaculture and restoration of the

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Z. Jiang et al. / Water Research 159 (2019) 1e9

oyster population have been proposed as an ecological restore tool for top-down control of phytoplankton blooms and reversal of eutrophication in coastal waters (Newell, 2004; Huang et al., 2008; Wheat and Ruesink, 2013; Rose et al., 2014; Bricker et al., 2018); however, its ecosystem service function remains controversial (Pomeroy et al., 2006; Kellogg et al., 2014). As a critical restoration technique, oyster culture and reefs have been widely adopted, such as in Long Island Sound (Bricker et al., 2018), Yangtze River Estuary (Quan et al., 2009), and Chesapeake Bay (Ray et al., 2015). In shallow eutrophic waters, consumption of phytoplankton by OBAs directly reduces a large amount of particulate organic matter available to be remineralized by pelagic consumers and bacterioplankton (Cloern, 1982; Newell, 2004; Kellogg et al., 2014). However, the excretion and regeneration of organic/inorganic nutrients promotes algal growth and production (Cloern, 1982; Newell, 2004;
n et al., 2014; Nizzoli et al., 2005; Broekhoven et al., 2014; Froja Porter et al., 2018). Therefore, the observed biomass and community composition of phytoplankton are not only the result of nutrient release (bottom-up effect) but also are affected by changes in grazer organisms that exert top-down control (Souchu et al., 2001; Newell, 2004; Ray et al., 2015). Knowledge regarding the top-down and bottom-up effects on phytoplankton is useful to evaluate the ecological function and restoration outcomes of bivalve farming. Bivalves usually engage in size-selective grazing on seston (the sum of phytoplankton, heterotrophic protists, and other particulates) and effectively reduce the biomass of large-celled phytoplankton (Newell et al., 1989; Souchu et al., 2001; La Rosa et al., 2002; Ward and Shumway, 2004; Trottet et al., 2007; Jiang et al., 2016). Bivalve cultivation profoundly influences the microbial food web dynamics (Dame, 1996; Dupuy et al., 2000; Wetz et al.,
n et al., 2014; Lu et al., 2015; 2002; Trottet et al., 2008; Froja Jacobs et al., 2015). Model simulations have suggested that bivalve grazing affects both phytoplankton biomass and community composition in shallow Suisun Bay (Lucas et al., 2016). Only a few field studies have focused on the responses of the phytoplankton community structure to oyster farming (Jiang et al., 2012, 2016). China is the biggest oyster culture country in the world; however, the effects of oyster farming on the phytoplankton community and water column biogeochemistry in coastal waters of China remains poorly understood. Xiangshan Bay (XSB) is a long (~60 km), narrow (~3e8 km), eutrophic, semi-enclosed subtropical bay located at the northern East China Sea, with long water-residence time (~80 days for 90% water exchanges) in the upper section (Ning and Hu, 2002). Oyster farming in this bay has been expanded since the 1980s, reflecting China's tremendously increased cultural scale. Shellfish production during 2005e2006 was estimated to be 45 000 t year
1, of which 93% was oyster produced either on ropes or in intertidal areas (Nobre et al., 2010). The Ninghai Power Plant (NPP) located in the upper bay began to operate since December 17, 2005, and produced a large amount of thermal discharge (82.5 m3 s
1), which caused a strong increase in the temperature of receiving waters adjacent to the NPP, including oyster farms (OFs) in the upper XSB. This temperature increase stimulated phytoplankton growth and frequent bloom in the upper bay, particularly in cold seasons (Jiang et al., 2012, 2019a; 2019b). In this context, we hypothesize that oyster farming results in top-down control of algal bloom under thermal stimulation and that the phytoplankton community structure is altered by size-selective grazing and the bottom-up effect. To test our hypothesis, ten cruises were conducted in the Chinese pleated oyster (Crassostrea plicatula) OFs and control areas (CAs) adjacent to the NPP in XSB during 2009e2015. We examined how oyster farming affects the phytoplankton community (chlorophyll a [chla], abundance, diversity, dominant species, and size structure) and physicochemical variables (temperature,

transparency, suspended solids, oxygen, nutrients, and organic carbon). Our objectives were (1) to quantify the removal of phytoplankton biomass by OBAs under thermal stimulation, (2) to investigate the effects of oyster farming on the phytoplankton community structure and physicochemical variables, and (3) to evaluate the mitigation potential of algal bloom and eutrophication by using oyster farming. Our study can help understand the effect of oyster farming on the coastal ecosystem and guide future policy formulating of mariculture and ecological restoration. 2. Materials and methods 2.1. Study area and sampling dates Fig. 1 shows old and new oyster rafts adjacent to the NPP located in the upper XSB. Four cruises were conducted in the old OF and CA on February 25, 2009, August 03, 2009, January 29, 2010, and April 23, 2010. Thereafter, the old OF was removed, and six cruises were conducted in the sites of old OF and CA on July 15, 2010, November 16, 2010, January 19, 2015, April 28, 2015, July 16, 2015, and October 13, 2015 to investigate the effects of the presence/absence of oyster farming on the phytoplankton community and physicochemical properties. Five cruises were conducted in the new OF and CA on November 16, 2010, January 19, 2015, April 28, 2015, July 16, 2015, and October 13, 2015. Sampling stations were setting at the center and 500e1000 m apart from the edge (CA) of OF. Three stations each were set in both OF and CA during 2015, and one station each was set in OF (at the center) and CA during 2009 and 2010 (Fig. 1). The sampling stations in old and new OFs and CAs are located within the area envelope 1  C increase (Jiang et al., 2019b). 2.2. Environmental parameters Surface (0.5 m depth) and bottom (0.5 m above the seabed)

Fig. 1. Sampling stations (hollow circles) in old and new oyster farms (close to the Ninghai Power Plant) in the upper section of Xiangshan Bay. OOF: old oyster farm; NOF: new oyster farm; NPP: Ninghai Power Plant. Three stations each were set in both the oyster farm (OF) and control area (CA) during 2015, and one station each was set in OF (at the center) and CA during 2009 and 2010.

Z. Jiang et al. / Water Research 159 (2019) 1e9

water at each station were collected in 5-L Niskin bottles. Temperature and salinity were measured in situ by using a YSI model 30 salinity meter and transparency was measured using a Secchi disc. Dissolved oxygen (DO) was measured by performing Winkler titrations. To detect other parameters, including dissolved inorganic nitrogen (DIN), phosphorus (DIP), and silicate (DSi), chla, total organic carbon (TOC), and suspended solids, water samples filled in 5-l buckets were preserved in dark and deep frozen surroundings before the laboratory operation. Water samples for dissolved nutrient analyses were filtered through a 0.45-mm cellulose acetate filter and saturated HgCl2 solution was added to conduct further analysis by using colorimetric methods. TOC was estimated using the elemental analysis (vario MICRO cube, elemental analyzer). To analyze suspended solids, filters were dried at 105  C to a constant mass and weighed after the samples (1e2 L seawater) were filtered through preweighed filters (Whatman GF/C). 2.3. Chla Water samples (100 mL) for chla were filtered through a 0.7-mm GF/F filters (Whatman). However, size-fractionated chla was measured in all seasons during 2015. Chla was size fractionated into micro (>20 mm), nano (2e20 mm), and picophytoplankton (<2.0 mm) by filtering through three types of filters (20, 2, and 0.7 mm). First, water was filtered through a 20-mm nylon filter (Millipore) and immediately after through 2-mm polycarbonate and 0.7-mm GF/F filters. The size-fractionated chla retained on filters was analyzed using a Turner Design Fluorometer after extraction in 90% acetone for 24 h at
20  C. Pheophytin (pheo) was measured after the addition of two drops of 5% 1N HCl. Pheopigments are chlorophyll degradation products that are diagnostic of phytoplankton mortality and pheo/chla usually indicates the grazing of phytoplankton (Taylor et al., 2012). 2.4. Phytoplankton community Three water samples for phytoplankton analysis were collected from the surface and bottom at each station during 2009 and 2010. One phytoplankton sample was collected at each station during 2015. All phytoplankton samples (400e1000 mL) were fixed with formalin to a final concentration of 2%. After 48-h sedimentation, the preserved samples were concentrated to 10e50 mL by slowly siphoning off the supernatant. Phytoplankton taxa were subsequently identified and counted on a 0.1-mL scaled slide by using a light microscope (Leica DM2500 or DM6B) at 200  , 400  , or 630  magnification. The size limit for identifying species was approximately 5 mm. We counted at least 300 units (individual cells or colonies) in each sample. 2.5. Data analysis Species richness (number, S), diversity (Shannon‒Wiener index, H0 ), and evenness (Pielou indices, J0 ) were calculated using PRIMER 5.0. Data on environmental (including transparency, suspended solids, temperature, salinity, and nutrients) and phytoplankton (including abundance, chla, dominant species, S, H0 , and J0 ) parameters on February 25, 2009, January 29, 2010, and 1 April 23, 2010 have been described previously (Jiang et al., 2012). SPSS 20.0 was also used for data analysis. A two-way (area and water layer) analysis of variance (ANOVA) was used to test for significant differences in phytoplankton community, size-fractionated chla, and environmental variables between OF and CA. Before ANOVA, all variables were tested for normality (Kolmogorov‒Smirnov test) and homogeneity (Levene test). Data that did not satisfy the assumptions of normality and homogeneity were analyzed using the

3

Mann‒Whitney test. Species abundance was transformed by log(xþ1) and standardized before the estimation of BrayeCurtis similarities between sample pairs. A two-way (area and water layer) analysis of similarity (ANOSIM) was used to test phytoplankton community differences on different sampling dates. Spearman's rank correlation was used to determine the relationship between the decreased percentage of phytoplankton biomass and environmental parameters during the oyster culture period. 3. Results 3.1. Environmental parameters Water depth and transparency ranged from 2.0 to 14.0 m and from 0.5 to 2.3 m, respectively (Figs. S1a and c). During the oyster culture period, transparency (suspended solids) was considerably higher (lower) in OF than in CA (Fig. 2a, d). However, no significant difference was found between OF and CA in all cases except on Aprial 28, 2015 (Table S1). Compared with CA, transparency (suspended solids) in OF increased (decreased) by 29.1% (12.2%) on average (Table 1). Temperature, salinity, and DO varied slightly between OF and CA (Fig. 2b, c, e), but showed apparent seasonsal changes, ranging from 10.0 to 27.9  C, 16.0 to 25.7, and 6.47e10.02 mg/L, respectively (Fig. S1). No stratification was found in warm seasons according to temperature and salinity vertical distributions. Temperature and DO in the new OF and CA showed a significant (p < 0.05) regional difference in cold but not in warm seasons. DIN and DIP concentrations were usually lower in OF than in CA during the oyster culture period except on January 19, 2015 (Fig. 2 and Fig. S1). Particularly on April 28, 2015 and October 13, 2015, DIP and DIN showed significant (p < 0.05) regional differences between the new OF and CA, respectively (Table S1). The DSi concentration varied slightly between OF and CA (Fig. 2h and Fig. S1i). TOC was considerably lower in OF than in CA in all cases (Fig. 2i and Fig. S1j). However, after the removal of the old farm, no significant regional difference was found for nutrients and TOC. Table 1 shows that oyster farming reduced the concentration of DIN, DIP, and TOC in the water column by 1.5%, 3.7%, and 18.4% on average, respectively. Overall, the concentrations of DIN, DIP, and TOC were higher on the surface than on at the bottom during the oyster culture period (Fig. 2), although no significant differences within the water layer were usually found (Table S1). 3.2. Phytoplankton abundance and chla The phytoplankton abundance (Fig. 3a and Fig. S2a) and chla concentration (Fig. 4a and Fig. S3) were significantly (p < 0.05) lower in OF than in CA during the oyster culture period (Tables S2 and S3). However, no significant difference between OF and CA was found after the removal of cultured rafts. Table 1 shows that oyster farming reduced the phytoplankton abundance and chla concentration by 46.3% and 18.4% on average, respectively. Thermal discharge from the NPP likely promoted phytoplankton growth and even bloom (with chla >6 mg/L on the surface in CA) during winter of 2009, 2010, and 2015 (Fig. S3). However, oyster farming effectively controlled winter algal bloom with >30% reduction in the phytoplankton abundance and chla concentration. Oyster farming profoundly influenced phytoplankton size structure that effectively reduced micro-chla contribution by 34.8% but increased nano- (by 8.7%) and pico-chla contribution (by 95.0%; Table 2). The water column micro- and nano-chla concentration was lower in OF than in CA in all seasons, but the pico-chla concentration showed the opposite results (Fig. 4). Pico-chla concentrations were higher in OF (0.31, 0.74, and 0.36 mg/L) than in CA

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Z. Jiang et al. / Water Research 159 (2019) 1e9

Fig. 2. Environmental variables on the surface (S) and bottom (B) in OF and CA during the oyster culture period and after the removal of oyster culture rafts. DO: dissolved oxygen; DIN: dissolved inorganic nitrogen; DIP: dissolved inorganic phosphorus; DSi: dissolved silicate; TOC: total organic carbon. The color bars in other subfigures are the same as that shown in Fig. 2a. These environmental variables in OF and CA on different sampling dates are shown in Fig. S1. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Table 1 Increased percentage (%) of the environmental parameters and phytoplankton community of the water column in OF compared with CA on different dates. Tran: transparency; SS: suspended solids; Abun: abundance; S: species richness, H’: ShannoneWiener diversity index; J’: Pielou's evenness index; n.d.: no data. Superscripted lower-case letters of different dates indicate old/new farms. a: during the oyster culture period of the old farm; b: during the oyster culture period of the new farm. Date a

02/25/2009 08/03/2009a 01/29/2010a 04/23/2010a 11/16/2010b 01/19/2015b 04/28/2015b 07/16/2015b 10/13/2015b Average

Tran

SS

DO

DIN

DIP

DSi

TOC

Chla

Abun

S

H0

J0

0.0 44.4 50.0 53.3 25.0 0.0 70.6 11.1 7.7 29.1


15.7
9.6
14.2
18.2
19.4
6.1
21.3
3.1
2.3
12.2


1.7
5.2
1.0 0.6 0.0
12.1 2.3
0.7
0.6
2.1


3.8
0.3 7.1
16.6
1.9 9.9
3.2
0.4
4.4
1.5


9.2
24.0
3.4 1.2
24.5 33.8
5.1
0.2
1.9
3.7

13.8
5.3 9.2
12.0 0.5 22.2
0.8
1.2
1.3 2.8


63.1
2.7
12.4
2.1 n.d.
23.3
19.2
8.2
16.7
18.4


32.8
24.8
34.1
18.7
17.0
76.6
19.3
22.4
9.3
28.3


41.6
65.1
31.8
3.3
46.6
93.0
65.0
28.2
42.0
46.3

23.2 10.0 14.1 29.8 27.0 18.5 65.1 26.8 22.7 26.3

14.9 8.8 26.9 11.3 47.3 56.6 147 10.8 20.9 38.3

8.1 5.7 22.6 1.9 38.3 49.7 114 4.3 14.3 28.8

Table 2 Increased percentage (%) of the pheo/chla and size-fractionated chla contribution to total chla of the water column in the new OF compared with CA on different dates. Date

Pheo/chla

Micro-chla

Nano-chla

Pico-chla

01/19/2015 04/28/2015 07/16/2015 10/13/2015 Average

177.2 48.5 22.7 36.0 71.1


21.9
31.7
62.2
23.3
34.8

33.0
5.4 0.8 6.5 8.7

106.1 138.3 85.5 50.3 95.0

(0.16, 0.51, and 0.26 mg/L) in spring, autumn, and summer. Fig. 4b and Table S3 show that the pheo/chla was significantly (p < 0.05) higher in OF than in CA. On average, oyster farming increased the

pheo/chla by 71.1% (Table 2), suggesting a high grazing rate on phytoplankton. 3.3. Phytoplankton species diversity Phytoplankton diversity indices (S, H0 , and J0 ) on both the surface and bottom were considerably higher in OF than in CA during the oyster culture period (Fig. 3 and Fig. S2). S, H0 , and J0 varied significantly (p < 0.05) between OF and CA in most cases (Table S2). Table 1 shows that oyster farming increased S, H0 , and J0 by 26.3%, 38.3%, and 28.8% on average, respectively. However, after the removal of cultured rafts, diversity indices did not significantly differ between OF and CA (Table S2).

Z. Jiang et al. / Water Research 159 (2019) 1e9

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Fig. 3. Phytoplankton abundance (cells/mL), S, H0 , and J0 on the surface and bottom in OF and CA during the oyster culture period and after the removal of oyster culture rafts. The color bars in other subfigures are the same as that in Fig. 3b. These parameters in OF and CA on different sampling dates are shown in Fig. S2. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 4. Chla concentration, pheophytin/chla (pheo/chla), and size structure (micro and pico-chla contribution to total chla) on the surface and bottom in OF and CA on different dates. Note that chla concentrations in the old and new farms during the oyster culture period and after the removal of oyster culture rafts are indicated in Fig. 4a. The color bars in Fig. 4b, d are the same as that shown in Fig. 4c. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

3.4. Dominant phytoplankton species

selective grazing on phytoplankton species by the oysters.

Dominant phytoplankton species included diatoms (e.g., Chaetoceros, Skeletonema, Thalassiosira, and Coscinodiscus), dinoflagellates (e.g., Prorocentrum minimum, Scripposciella trochoidea, and Karlodinium veneficum), cryptophytes (Teleaulax), euglenophyte (Eutreptia lanowii and Eutreptiella gymnastica), cyanobacteria (Trichodesmium erythraeum), and chlorophyte (unidentified species with cell size of ~5 mm). The dominance of large-celled (e.g., Coscinodiscus, Ditylum brightwelli, and Guinardia delicatula) or chain-formed (e.g., Chaetoceros and Skeletonema) diatoms was lower in OF than in CA during the oyster culture period (Fig. S4). Micro- and nano-sized species (e.g., P. minimum and Teleaulax) also frequently showed lower dominance in OF. By contrast, the dominance of small-sized unidentified chlorophytes was higher in OF than in CA. However, no discernible difference in the contribution of dominant species between OF and CA was found after the removal of culture rafts (Figs. S4eej). These findings indicated

3.5. Phytoplankton community composition The results of two-way ANOSIM showed a significant (p < 0.05) difference in the phytoplankton community composition between OF and CA during the oyster culture period despite the water layer difference (Table 3). However, no significant spatial difference in the phytoplankton community was found after the removal of culture rafts. This finding indicated that oyster farming significantly influences phytoplankton composition. 3.6. Relationship between algal biomass deficit and environmental variables Spearman's rank correlation showed that the decreased percentage of phytoplankton biomass was positively and significantly (p < 0.05) correlated with surrounding phytoplankton abundance

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Z. Jiang et al. / Water Research 159 (2019) 1e9

2001; Trottet et al., 2007; Jacobs et al., 2015). Our study showed that the phytoplankton abundance (Fig. 3a and Fig. S2a) and chla concentration (Fig. 4 and Fig. S3) were significantly (p < 0.05) lower in OF than in CA during the oyster culture period (Table S2). However, after the removal of culture rafts, no significant differences in phytoplankton biomass between OF and CA were found. Table 1 shows that the average deficits of phytoplankton abundance and chla concentration were 46.3% and 28.3%, respectively. This finding indicated strong filtration efficiency by OBAs in XSB. Similarly, Huang et al. (2008) found that phytoplankton abundance, chla, and primary production increased significantly after the removal of culture racks in OF in a eutrophic lagoon, Taiwan, suggesting an effective top-down control on algal biomass and production. Phytoplankton biomass (chla or carbon) depletion has been widely reported (Souchu et al., 2001; Wheat and Ruesink, ~ iga et al., 2013; Ray et al., 2015; Jiang et al., 2016), 2013; Zún including a noticeable reduction in phytoplankton biomass in entire systems of South San Francisco (Cloern, 1982) and Tapong Bays (Huang et al., 2008). However, algal biomass deficit is not universal (La Rosa et al., 2002; Trottet et al., 2008). The algal biomass increase has been mainly attributed to the local phytoplankton composition (dominance of small cells), food source (mainly heterotrophic plankton), and low culture density (Trottet et al., 2007, 2008). Higher deficits of phytoplankton abundance and chla in winter (>30%) than in warm seasons were observed (Table 1). Table 4 shows that the reduction of chla was negatively correlated with temperature, although algal abundance was not correlated with temperature. This finding might be attributed to the reproductive and culture period of the oysters in XSB. For example, the clearance rate of another cultivated Portuguese oyster (Crassostrea angulata) in Dapeng Cove, northern South China Sea increased with increasing temperature until at ~25  C and then declined outside of the reproductive period, but decreased to the minimum during the reproductive period (August; Yu et al., 2017). Gu and Li (1998) found that spawning of C. plicatula in XSB usually occurred monthly from May to October. Furthermore, the cultivated oyster in XSB begins seeding in warm seasons and grows into adults in winter of the following year (Nobre et al., 2010). Adult oysters filter more algal biomass than juvenile oysters. These studies indicate that the filtration rate of oyster might be suppressed in summer with temperatures close to 30  C. In winter, however, the temperature increase caused by thermal discharge enhances oyster filtration rate, resulting in a strong top-down control on phytoplankton. Thus, oyster farming effectively mitigates winter algal bloom under thermal stimulation in the upper XSB. In addition to temperature, depletion of phytoplankton biomass in OF was positively and significantly (p < 0.05) correlated with surrounding phytoplankton abundance and chla, but not with transparency, suspended solids, DIN, and DIP (Table 4). Fournier et al. (2012) found that the quantity and origin of carbon filtered by pearl oysters were highly related to the concentration and composition of plankton in Ahe atoll Lagoon, French Polynesia. However, in Ría de Vigo, Galicia, the organic ingestion rate and absorption efficiency of mussels (Mytilus galloprovincialis) were more strongly correlated with the plankton carbon contents than with particulate organic carbon and chla, suggesting the

Table 3 Results (R value) of two-way analysis of similarity (ANOSIM) for phytoplankton community among regions and water layers on different dates. ns no significance; * p < 0.05; **p < 0.01. Superscripted lower-case letters of different dates indicate presence/absence and old/new oyster-cultured rafts, a: during the oyster culture period of the old farm; b: during the oyster culture period of the new farm; c: after the removal of the old oyster culture rafts. Date

OF vs. CA

Surface vs. Bottom

02/25/2009a 08/03/2009a 01/29/2010a 04/23/2010a 07/15/2010c 11/16/2010c 01/19/2015c 04/28/2015c 07/16/2015c 10/13/2015c 11/16/2010b 01/19/2015b 04/28/2015b 07/16/2015b 10/13/2015b

0.593* 1.000** 0.722** 0.926** 0.259ns
0.370ns
0.222ns
0.352ns
0.259ns
0.167ns 1.000** 0.667** 1.000** 0.648** 0.981**

0.667** 1.000** 0.704** 1.000** 1.000** 1.000**
0.222ns 0.093ns
0.019ns 0.241ns 1.000** 0.222ns 0.444ns 0.241ns 0.056ns

and chla and were negatively correlated with transparency, DIP, and DSi (Table 4). However, there was no significant correlation between the reduction of algal biomass and environmental parameters except for DSi. 4. Discussion 4.1. Top-down control on algal bloom by oyster farming under thermal stimulation Severe algal blooms with a surface chla concentration of >6 mg/L in CA were found in the winter of 2009, 2010, and 2015 (Fig. S3). Our simultaneous observations revealed that the temperature increase caused by thermal discharge from the NPP promoted phytoplankton growth and even bloom in the upper XSB characterized by abundant nutrients and relatively high transparency and water column stability, particularly in cold seasons (Jiang et al., 2012, 2019a; 2019b). Similar result was observed in eutrophic Daya Bay, northern South China Sea because of thermal discharge from a nuclear power station (Yu et al., 2007). Additionally, it seems that algal bloom seasonality has shifted forward from spring and early summer to winter since the power plant operation in 2006 (Jiang et al., 2019a, 2019b). Our previous studies demonstrated that phytoplankton abundance (Jiang et al., 2019b) and chla concentration (Jiang et al., 2019a) were significantly higher in upper than in middle and lower XSB in all seasons. Moreover, thermal discharge accelerated the warming trend in XSB because of long water-residence time (Jiang et al., 2019a), which significantly influence phytoplankton community composition (e.g., increase in dominance of dinoflagellates) under increasing eutrophication (Jiang et al., 2019a, 2019b). These findings warrant consideration in mitigating algal bloom and eutrophication in XSB through oyster farming. Phytoplankton are the main food source for sustaining intensive cultivation of filter-feeding bivalves (Cloern, 1982; Souchu et al.,

Table 4 Spearman's rank correlation coefficients between the decreased percentage of phytoplankton biomass (Abun and chla) and environmental variables in CA during the oyster culture period. Reduced percentage Abun Chla

Abun *

0.67 0.48ns

Chla ns

0.38 0.95**

TOC

Temp ns


0.52 0.05ns

ns

0.12
0.52ns

Tran

SS ns


0.60
0.36ns

DIN ns

0.07 0.25ns

DIP ns

0.33
0.38ns

DSi ns


0.22
0.62ns


0.22ns
0.75*

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~ iga importance of heterotrophic plankton as a food source (Zún et al., 2013). Trottet et al. (2007) also emphasized that heterotrophic plankton (mostly naked ciliates and tintinnids) could be an
e Lagoon. essential food source for cultured mussels in Grande Entre We speculated that the top-down control of phytoplankton biomass is highly dependent on culture density, growth, and cultivation period of oyster, and on phytoplankton abundance and composition. Additional studies should investigate the role of heterotrophic microbial plankton during oyster farming. 4.2. Effects of oyster farming on the phytoplankton community composition Our study found that oyster farming considerably reduced (increased) micro-chla (pico-chla) contribution by 34.8% (95.0%) on average (Table 2). Fig. 4 and Table S3 show that micro-chla (picochla) contribution was significantly (p < 0.05) lower (higher) in OF than in CA in all seasons except summer, probably due to the lower filtration at high temperature as mentioned earlier (Gu and Li, 1998; Yu et al., 2017). However, pheo/chla was significantly (p < 0.05) higher in OF than in CA (Fig. 4b). On average, oyster farming increased pheo/chla by 71.1% (Table 2), suggesting a high grazing pressure on phytoplankton. These results indicated that OBAs tended to filter relatively large-celled phytoplankton, consistent with previous reports (Souchu et al., 2001; La Rosa et al., 2002; Trottet et al., 2008; Fournier et al., 2012; Froj
an et al., 2014; Jacobs et al., 215; Lu et al., 2015; Jiang et al., 2016). A higher picochla concentration in OF than in CA was observed in all seasons except winter. Jiang et al. (2016) also found higher picoeukaryote (mostly prasinophyte) abundance in OF than that at a reference site in Daya Bay. We speculated that oyster farming favored picophytoplankton under size-selective filtration and a decrease in predators (e.g., flagellates and ciliates grazed by the OBAs). Our previous study found that pico-chla contribution increased significantly with increasing nutrient amounts from the lower to the upper XSB (Jiang et al., 2019a). This result is not consistent with the principle of phytoplankton cell-size tradeoffs that small cells thrive in warm, oligotrophic waters, whereas large cells are dominant in eutrophic waters (Irwin et al., 2006). We inferred that thermal discharge and oyster farming were partially responsible for the relatively high pico-chla contribution in the upper bay, apart from water column stability. Oyster farming exerts a top-down control on size structure by consuming micro- and nanophytoplankton but stimulating picophytoplankton growth, which profoundly influences local pelagic food web and biogeochemical processes under trophic interaction (Legendre and Rassoulzadegan, 1996; Dupuy et al., 2000; Lu et al., 2015). Size-fractionated chla data in CA indicated that the sum of micro- and nano-fraction accounted for >85% in all seasons (Fig. 4). Thus, our present phytoplankton abundance through microscope counting (with the size limit at ~5 mm) represented the almost total algal biomass. Because of size-selective filtration, the dominance of large-sized dominant phytoplankton species decreased, particularly micro-sized or chain-formed diatoms and nano-sized flagellates (Fig. S4). Additionally, we found that many epiphytic/epizoic diatom species (e.g., Diploneis, Gyrosigma, and Pleurosigma) with low abundance were divorced from the rafts, ropes, and OBAs during the oyster culture period (Jiang et al., 2012), which increased phytoplankton diversity. Consequently, phytoplankton species diversity indices (S, H0 , and J0 ) were significantly (p < 0.05) higher in OF than in CA in most cases (Fig. S2 and Table S2). On average, oyster farming increased S, H0 , and J0 by 26.3%, 38.3%, and 28.8%, respectively (Table 1). An ANOSIM test showed a significant (p < 0.05) difference in the phytoplankton community composition between OF and CA during the oyster culture period (Table 3).

7

However, after the removal of cultured rafts, diversity indices and community composition of phytoplankton in OF were consistent with those in CA. These findings confirmed our hypothesis that oyster farming exhibits strong top-down control on the phytoplankton community. Suspension-feeding bivalves usually show selective filtration on phytoplankton not only based on size but also on cell properties and nutrition (Shumway et al., 1985; Loret et al., 2000; Ward and Shumway, 2004). Our study demonstrated a frequent reduction of P. minimum and Teleaulax in OF, in addition to large-celled diatoms (Fig. S4). This finding is consistent with those of other studies on Ostrea edulis (Shumway et al., 1985) and Mytilus edulis (Bougrier et al., 1997) in the laboratory. Additionally, Loret et al. (2000) indicated that nanoflagellates (particularly cryptophytes) were preferentially ingested by the pearl oyster Pinctada margaritifera in the natural phytoplankton community in Takapoto Atoll Lagoon, based on the findings of optical microscopy and HPLC pigment analysis. We speculated that dominant micro-sized diatoms and nanoflagellates (particularly cryptophytes and dinoflagellates) are potential nutrition sources of OBAs in XSB, resulting in niche occupation by picoplankton (Fig. 4). In this condition, oyster farming significantly altered the phytoplankton community composition through grazing and trophic interaction. Similarly, Dupuy et al. (2000) revealed that oyster grazing triggered dramatic changes in the protist community composition, including the abundance and contribution of bacterioplankton, >5-mm and <5mm flagellates, ciliates, diatoms, and dinoflagellates. Moreover, they hypothesized that oysters may access the strong bacterioplanktonic production through hetero/mixotrophic protists, which would thus allow carbon transfer from the microbial loop to oysters. By contrast, Trottet et al. (2008) found no significant influence of mussel farming on the planktonic community because of the relatively low culture mussel production. 4.3. Effects of oyster farming on water quality Cultivated bivalves exhibit a natural cleansing process and remove phytoplankton and other organic and inorganic particles from the water column (Dupuy et al., 2000; Trottet et al., 2007; Jacobs et al., 2015). Moreover, oysters have a well-developed ability to preferentially ingest various types of organic material and to reject other particles as pseudofaeces (Newell and Jordan, 1983). Our study showed considerable depletion of suspended solids and TOC (by 12.2% and 18.4%, respectively) and increased transparency (by 29.1%) during oyster culture period (Table 1), although these parameters did not vary significantly between OF and CA in all cases (Table S1). Previous studies have also reported that suspended solids in OF were retained by oysters, potentially increasing light availability to the bottom and thereby providing enhanced growth and production of benthic microphytobenthos, seagrasses, and marcoalgae (Newell, 2004; Grizzle et al., 2018). Additionally, DO was consumed by the OBAs and organic degradation, resulting in a slight depletion (2.1%) of DO (Table 1), consistent with early reports (Souchu et al., 2001; Bricker et al., 2018). Nizzoli et al. (2005) demonstrated that the mussel (M. galloprovincialis) rope community was an enormous sink for oxygen and particulate organic matter in Sacca di Goro Lagoon using in situ incubation. In addition to the top-down control on phytoplankton, suspension-feeding bivalves also stimulate algal growth (bottomup effect) by excretion and regeneration of nutrients (Newell, 2004;
n et al., 2014). Our Nizzoli et al., 2005; Kellogg et al., 2014; Froja study found a slight depletion (by 1.5% and 3.7%, respectively) of DIN and DIP during the oyster culture period, suggesting an absorption and utilization of nutrients. Bricker et al. (2018) estimated that 1.31% and 2.68% of the total annual N input in Long Island

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Sound could be removed by current and expanded oyster production, respectively, using system-scale modeling. These findings were not consistent with previous studies, which reported that bivalve farming increased nutrient level (Souchu et al., 2001; La Rosa et al., 2002; Lu et al., 2015; Ray et al., 2015). Kellogg et al. (2014) suggested that N removal by oysters varied by orders of magnitude among sites, seasons, and growing conditions. In the eutrophic upper XSB, food source (phytoplankton and organic particles) was abundant enough for filtering by oysters. Fig. S3 shows high surrounding chla concentrations (>2 mg/L) in all cases, with the highest chla concentration (21.6 mg/L) on the surface in the winter of 2015. Such abundant phytoplankton can consume a large amount of excreted and regenerated organic/inorganic nutrients, thereby accelerating phytoplankton production and turnover under oyster grazing (Fig. 5; Souchu et al., 2001; Nizzoli et al., 2005; Broekhoven et al., 2014) and thermal addition (Jiang et al., 2012, 2019a; 2019b). Through filtration, some of the N and P that was originally incorporated in phytoplankton, but was not digested by OBAs, can transform into their organic composition and buried in the accumulating sediments, including undigested remains, mucus-bound faces, and pseudofeces (Fig. 5). Otherwise, large numbers of epibiotic macroalgae on rafts and ropes assimilate partial N and P. Moreover, turbidity reduction favored the growth of phytoplankton in the water column and microphytobenthos on the sediment, thereby increasing absorption and utilization of nutrients. Consequently, oyster farming removed some N and P and reduced nutrient level in the upper XSB. Organic/particulate N and P, however, might increase due to oyster excretion and biodeposit resuspension (Fig. 5; Newell, 2004; Kellogg et al., 2014; Porter et al., 2018). Further studies are warranted on the response of organic/ particulate N and P associated with phytoplankton to oyster farming. 5. Conclusions This study confirms our hypothesis that oyster farming in the upper XSB significantly reduced phytoplankton biomass and exerted a strong top-down control on winter algal bloom under thermal

stimulation. Under size-selective grazing and bottom-up effect of OBAs, oyster farming reduced microphytoplankton contribution but promoted picophytoplankton growth, thereby sharply increasing picophytoplankton contribution. Such a shift in phytoplankton cell size may profoundly influence local food web dynamics and biogeochemical processes, which warrants further study. Interestingly, OBAs tended to filter dinoflagellates (e.g., P. minimum) and cryptophytes (Teleaulax) in addition to largecelled diatoms, suggesting that this selective filtration is based not only on size but also on cell properties or nutrition. Furthermore, oyster farming significantly enhanced phytoplankton diversity. We concluded that the phytoplankton community structure was largely shaped by oyster farming through both top-down and bottom-up controls. Oyster farming considerably reduced suspended solids and TOC and increased transparency, which might enhance primary production in the water column and on the sediment, thereby reducing N and P levels. Overall, oyster farming slightly reduced DIN and DIP concentrations. Based on these findings, we proposed oyster farming as a vital restoration tool to improve water quality and control algal bloom in XSB and subtropical eutrophic coastal waters worldwide. Acknowledgments We are grateful to Xiaoya Liu for providing physicochemical data. We also thank the editor and two anonymous reviewers for their constructive comments. This work was supported by the National Key Research and Development Program of China (2018YFD0900901), Scientific Research Fund of the Second Institute of Oceanography, Ministry of Natural Resources (QNYC1703 and JT1602), National Marine Public Welfare Research Project of China (201305043-3), National Natural Science Foundation of China (41876198, 41806136, and 41706125), Project of State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography (SOEDZZ1803), and Project of Long-term Observation and Research Plan in the Changjiang Estuary and Adjacent East China Sea (14282). Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.watres.2019.04.023. References

Fig. 5. Conceptual diagram of the biogeochemical cycle of nutrients (N and P) during oyster farming. N and P incorporated in phytoplankton consumed by oysters can be assimilated into oyster tissue and shell and associated biofouling fauna, buried in the sediments, and returned to the water column and atmosphere.

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