Biological productivity evaluation at lower trophic levels with intensive Pacific oyster farming of Crassostrea gigas in Hiroshima Bay, Japan

Accepted Manuscript Biological productivity evaluation at lower trophic levels with intensive Pacific oyster farming of Crassostrea gigas in Hiroshima Bay, Japan

Akira Umehara, Satoshi Asaoka, Naoki Fujii, Sosuke Otani, Hironori Yamamoto, Satoshi Nakai, Tetsuji Okuda, Wataru Nishijima PII: DOI: Reference:

S0044-8486(17)32366-9 doi:10.1016/j.aquaculture.2018.05.048 AQUA 633277

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aquaculture

Received date: Revised date: Accepted date:

30 November 2017 27 May 2018 28 May 2018

Please cite this article as: Akira Umehara, Satoshi Asaoka, Naoki Fujii, Sosuke Otani, Hironori Yamamoto, Satoshi Nakai, Tetsuji Okuda, Wataru Nishijima , Biological productivity evaluation at lower trophic levels with intensive Pacific oyster farming of Crassostrea gigas in Hiroshima Bay, Japan. Aqua (2017), doi:10.1016/ j.aquaculture.2018.05.048

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Biological productivity evaluation at lower trophic levels with intensive Pacific oyster farming of Crassostrea gigas in Hiroshima Bay, Japan

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Akira Umehara1*, Satoshi Asaoka2, Naoki Fujii3, Sosuke Otani4, Hironori Yamamoto5, Satoshi Nakai6, Tetsuji Okuda7, Wataru Nishijima1

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1. Environmental Research and Management Center, Hiroshima University, 1-5-3 Kagamiyama, Higashi-hiroshima, Hiroshima, 739-8513, Japan 2. Research Center for Inland Seas, Kobe University, 5-1-1 Fukaeminami, Higashinada, Kobe, 658-0022, Japan 3. Faculty of Agriculture, Saga University, Honjo 1, Saga, 840-8502, Japan 4. Department of Technological Systems, Osaka Prefecture University College of Technology, 26-12 Neyagawa, Osaka, 572-8572, Japan 5. FUKKEN Co. Ltd., 2-10-11 Hikari, Higashi-ku, Hiroshima-shi, Hiroshima, 732-0052, Japan 6. Graduate School of Science and Engineering, Hiroshima University, 1-4-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8527, Japan 7. Department of Environmental Solution Technology, Faculty of Science and Technology, Ryukoku University, 1-5 Yokoya, Seta Oe-cho, Otsu, Shiga, 520-2194, Japan

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* Corresponding author. Tel: +81 82-424-6195, E-mail: [email protected]

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Abstract Enclosed seas are suitable for bivalve farming due to high primary production, which provides food sources. The impact of oyster farming on the biological productivity of lower trophic levels was evaluated in Hiroshima Bay. The area-weighted mean primary production in the estuary (northeastern bay; NB) was 1.1 to 2.1 times higher than that of the offshore area (southwestern bay; SB) in all four seasons. In contrast, the area-weighted mean secondary production by net zooplankton in the NB was lower than that of the SB, except in August. The area-weighted mean secondary production by oysters in the NB was 2.2 to 2.8 times higher than that of the SB in all four seasons, and exhibited a similar spatial pattern to that of the primary production. The primary production was more efficiently utilized and transferred to secondary producers in the SB (16.7% on average) than in the NB (9.4% on average). This study provides guidance for oyster farming in Japan.

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Keywords: Primary production, Secondary production, Seto Inland Sea, Transfer efficiency

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1. Introduction Mollusk farming, which includes bivalves, is increasing rapidly around the world (FAO, 2009) and was responsible for 24% of global farming production in 2010 (Mathiesen, 2012). Bivalve farming also inhibits excessive phytoplankton growth, including harmful algal blooms (HABs), through the consumption of phytoplankton (Hallegraeff, 1993). Eutrophic water areas, primarily enclosed seas such as bays and saline lakes, are suitable for bivalve farming due to high primary production, which provide food sources. On the other hand, bivalve farming can have ecological impacts on these areas, such as presence of bivalve pests (fouling pests, toxic/noxious microalgae, and diseases), creation of new habitat in the bivalve shells, alteration of nutrient cycling, depletion of suspended particulate matter, and changes in ecosystem structure, especially in higher trophic level animals including fish, seabirds, and marine mammals (Forrest et al., 2009). These impacts have been studied using molecular approaches to reveal the effects of pests and genetic pollution, and through mass-balance approaches to evaluate nutrient cycling (Friedman et al., 2005; Murray and Hare, 2006; Cerco and Noel, 2007; Filgueira et al., 2013; Filgueira et al., 2014). The carrying capacity of bivalve farming has also been studied to minimize its effects on ecosystems. Mass-balance modeling using Ecopath is usually used to estimate the carrying capacity of bivalve farming (Byron et al., 2011a; Byron et al., 2011b). Byron et al. (2011a) estimated that the ecological carrying capacity in barrier-beach lagoons of the southern shore of Rhode Island, U.S.A., was 15 g dry weight (DW) m-2, whereas the current farmed oyster biomass was 0.23 gDW m-2. They also estimated the carrying capacity of Narragansett Bay in Rhode Island as 5.9 gDW m-2, which was much larger than the current farmed oyster biomass (0.0095 gDW m-2) (Byron et al., 2011b). In trophic modeling using Ecopath, the ecological carrying capacity was defined as the maximum amount of cultured bivalve biomass that would not cause the biomass of any other group to fall below 10% of its original biomass (Kluger et al., 2016). Ecopath is a static, mass-balanced snapshot of an ecosystem, but production, including that of phytoplankton and oysters, fluctuates widely throughout the year. Therefore, investigating the same area throughout the year would provide valuable information relevant to the study of productive structures of an ecosystem. The oyster (Crassostrea gigas) is a dominant species in bivalve farming worldwide and is also an important commercially farmed bivalve in Japan. Hiroshima Bay, which is located in the Seto Inland Sea, is the primary site of oyster farming in Japan, wherein production of farmed oysters is approximately 50–60%. In the bay, oyster farming has been developed since the 1950s, and the annual soft-tissue production in recent years was approximately 20 thousand tons. The current soft-tissue biomass of farmed oysters in the northeastern part of Hiroshima Bay (162 km2) is approximately 19–153 gDW m-2 (Songsangjinda et al., 2000; Yamamoto et al., 2011), assuming that the carbon to dry weight (C:DW) and carbon to nitrogen (C:N) ratios of bivalve tissue were 0.39 and 4.7, respectively (Nakamura et al., 2003; Smaal and Vonck, 1997). This value is similar to those of other large-scale oyster farming regions of the world (Oleron Bay, 57 gDW m-2; Chesapeake Bay, 2–90 gDW m-2 soft-tissue biomass) (Ulanowicz and Tuttle, 1992; Leguerrier et al., 2004), but higher than the carrying capacities in barrier-beach lagoons of the southern shore (Byron et al., 2011a) and Narragansett Bay, Rhode Island (Byron et al., 2011b), as mentioned above. Consequently, oyster farming in Hiroshima Bay may be one of the most intensive

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bivalve farming operations in the world. Oyster farming in Hiroshima Bay is supported by high primary production due to high nutrient loads from land. However, high nutrient loads can induce excess eutrophication resulting in frequent red tides. Thus, there are continuing efforts to reduce organic matter and nutrient (nitrogen and phosphorus) loading based on the Water Pollution Control Law of 1970 and the Law Concerning Special Measures for Conservation of the Environment of the Seto Inland Sea (1973). The supplies of nitrogen and phosphorus from land to the bay were estimated to be 32 and 3.0 t km-2 d-1, respectively, in 1979, and were reduced to 23 (28% reduction from 1979) and 1.5 t km-2 d-1 (50% reduction from 1979), respectively, in 2009 (Ministry of the Environment, private data). In the bay, the production of fish began to decrease in the 1990s, and in recent years, the amount of fish production was less than half of the production in 1988, which was the peak year (Ministry of Agriculture, Forestry and Fisheries, 2017). The cause of the reduction in fish production is not clear, but may be due to a reduction of nutrient loads from land and the subsequent reduction in production at lower trophic levels. In these situations, it is important to understand the effects of intensive oyster farming on the ecosystem of Hiroshima Bay and to manage oyster farming accordingly. In this study, we conducted seasonal investigations in Hiroshima Bay on the species composition of phytoplankton, and primary and secondary production by net zooplankton and oysters. We also estimated the carbon transfer efficiency to clarify the impact of oyster farming on the biological productivity of lower trophic levels.

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2. Materials and methods 2.1 Study area Hiroshima Bay, in the midwestern part of the Seto Inland Sea, is one of the most eutrophic (mean value of TP [total phosphorus] during 1980 and 1998, 0.68 tons P d-1; Yamamoto et al., 2002a) semi-enclosed bays in the Seto Inland Sea. Based on the geological structure of the bay, the bay was horizontally divided into two areas, the northeastern part (NB; 162 km2) and the southwestern part (SB; 225 km2), (Kittiwanich et al., 2016). The area and the population density of the watershed area are 1,710 km 2 and 570 persons km-2, respectively, wherein Hiroshima City is included in this area (Ozaki et al., 2010). The mean depth of the bay is 26 m. The Ohta River empties into the innermost part of the bay, and the mean river water discharge is approximately 7 × 106 m-3 d-1 (Yamamoto et al., 2002a). In the whole bay throughout the year, the water temperature and salinity of the surface water range from 12–28°C and from 24.5–34.5 practical salinity unit (PSU), respectively (Yamamoto et al., 2002b). The salinity tends to be lower in the northern part of the bay due to discharge from the Ohta River. Seven sampling stations (H1–7) in Hiroshima Bay, Seto Inland Sea, Japan (H5: 34°15’59” N, 132°20’59” E) were established (Fig. 1). Seasonal investigations (four times per year) of the biological productivity of the lower trophic levels at these stations between November 2014 and August 2015 were conducted. To clarify the spatiotemporal variations in species composition and cell density of the phytoplankton in the bay, the seasonal monitoring data collected by the Ministry of the Environment (MOE) during 1982 and 2014 were used. The data from two stations (M1 and M2), which were available for long-term analysis, were used. There are many rafts for oyster farming throughout the entire bay, which are densely arranged in the northeastern part of the bay, as illustrated in Figure 2 (Sixth Regional Coast Guard Headquarters, Japan

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Coast Guard, 2017).

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2.2. Sampling procedures At the seven stations (H1–7), hydrological measurements and water and zooplankton sampling were carried out from a ship. Water quality measurements (temperature, salinity, fluorescence, and photon flux density) were conducted vertically using a probe (AAQ176, JFE Advantec, Kobe, Japan), and 4-L water samples were collected in plastic bottles with a Van Dorn water sampler at depths of 100, 50, and 10% surface irradiance. To decide the collection depths at 50 and 10% surface irradiance, photon flux density (µmol-photons m-2 s-1) were previously measured vertically at depths of every 1 m. The net zooplankton samples were collected vertically with a Kitahara plankton net (100 μm mesh opening) from 1 m above the sea floor to the surface, and were fixed immediately with formaldehyde on the ship.

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2.3. Sample treatment and analysis In the laboratory, surface water samples fixed with 1% glutaraldehyde were observed under a microscope, and the cell densities of the phytoplankton were determined both in our survey and from the MOE investigation (mainly Lugol’s solution). To determine chlorophyll a (Chl. a) concentrations, 300-mL water samples were filtered through glass-fiber filters (GF/F; Whatman, Maidstone, UK), and the residues on the filters were extracted with 10 mL of 90% acetone in the dark at –20°C for 16−24 h. The extracts were sonicated for 20 min, and Chl. a concentrations were determined fluorophotometrically (10-AU-5; Turner Designs, Sunnyvale, CA, USA), according to the Welschmeyer method (Welschmeyer, 1994) both in our survey and in the MOE investigation. The water samples were filtered onto pre-combusted GF/F filters (450℃, 4 h), dried in an oven at 60°C for 48 h, vacuum desiccated over silica gel for 24 h, and weighed to determine the amounts of suspended solids in the water. The filters were further combusted (600℃, 2 h) to remove organic matter, and weighed again to determine the concentration of particulate organic matter (POM) in the water. To estimate primary production, the water samples were filtered through a 220-μm mesh screen to remove large zooplankton and transferred into 500-mL polycarbonate bottles (one bottle per sample), wherein the light intensity (50 and 10%) was regulated by density filters. After the addition of NaH13CO3, the bottles were immediately incubated in a water bath at in situ temperature at approximately 200-μmol photons m-2 sec-1 light intensity for 4 h. After incubation, the samples were filtered through precombusted GF/F filters, treated with 1 N HCl to remove inorganic carbon, washed in 3% NaCl, and stored at –20°C until isotope analysis. Particulate organic carbon (POC) and atom % of 13C of the residuals on the dried filters (80°C, 48 h) were analyzed by elemental analyzer-isotope ratio mass spectrometer (FlashA EA1112-DELTA V ADVANTAGE; Thermo Fisher Scientific, Waltham, MA, USA). The analytical error for 13C measurements was less than 0.001 atom %. The photosynthetic rate was calculated according to Hama et al. (1983). Dissolved inorganic carbon (DIC) concentrations were estimated using pH, water temperature, and alkalinity calculated from salinity of the water in the field according to Taguchi et al. (2009). Before the investigations of this study, the relationship between estimated and measured DIC concentrations using ion probe (IM32P, DKK−TOA Co. Ltd., Japan) was obtained in Hiroshima Bay (1.14 × estimated DIC conc. − 0.517, r2 = 0.874), and the DIC concentrations of the water in each investigation was determined using the regression

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2.4. Estimation of primary production At first, the relationships between relative irradiance (%) and Chl. a-specific productivity (mgC mgChl. a-1 h-1) using the data at the depths of 100, 50, and 10% surface irradiance in the bay were obtained seasonally. In each station, Chl. a-specific productivity at depths of every 1 m in the euphotic zone was estimated using the regression equations and measured relative irradiance. Then, photosynthetic rate (mgC m-3 h-1) at depths of every 1 m was estimated using Chl. a-specific productivity and measured Chl. a concentration. The Chl. a-specific productivity was estimated as (1) PB = PP / CHL where PB indicates the Chl. a-specific productivity (mgC mgChl. a-1 h-1); PP is the photosynthetic rate (mgC m-3 h-1); and CHL is the Chl. a concentration (mgChl. a m-3). Primary production in the euphotic zone (surface to depth of 1% surface irradiance) of the bay was obtained using the following equations:

PPSTN =12 ´ ò (PBZ ´CHLZ )dz PBZ = a ´(I Z / I 0 )´100

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(3) where PPSTN is primary production in the euphotic zone at a station (mgC m d ); PBZ and CHLZ are Chl. a-specific productivity (mgC mgChl. a-1 h-1) and Chl. a concentration (mgChl. a m-3) at a depth of z m, respectively; a is the regression coefficient between relative irradiance (%) and Chl. a-specific productivity in the bay at each seasonal investigation; and Iz and I0 indicate photon flux density (μmol photons m-2 sec-1) at depth z and at the surface, respectively. -2

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2.5. Estimation of secondary production To estimate the secondary production, the net zooplankton collected from the fields were identified and counted, and their body lengths were measured under a microscope. The biomass of the net zooplankton was estimated using length-weight relationships for each species by the following equation; 𝐶 = 𝑎 × 𝐵𝐿𝑏 (4) where C is biomass (µgC); BL is the body length (µm); a, b are coefficients for each species in the Seto Inland Sea reported by Uye (1982) and Uye et al. (1996). Secondary production was calculated with a regression equation between specific growth rate and temperature as follows; 𝑆𝐺 = 𝑐 × 𝑒 𝑑𝑇 (5) 𝑃 = 𝐵 × 𝑆𝐺 (6) where SG indicates the specific growth rate (d-1); T is temperature (℃); c, d are coefficients for each species in the Seto Inland Sea (Uye and Shimazu, 1997); P and B indicate the secondary production (mgC m-2 d-1) and biomass (mgC m-2), respectively. The secondary production by oysters was calculated based on the growth model of the soft tissue of the suspended culture oysters (C. gigas; 1.2–2.7 g dry flesh weight per individual) reported by Gangnery et al. (2003). The model was developed in the Thau Lagoon in France, which exhibits similar environmental conditions (8.5–27℃, 34– 40 PSU, 0.4–6.5 mgChl. a m-3) to Hiroshima Bay. Growth rate (G; gDW ind.-1 d-1) was modeled as a function of food source, temperature, and individual size according to the following equation: (7) G = a ´ F b ´T c ´Y d

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where F is POM concentration as a food source (mg L-1); T is temperature (℃); and Y is individual dry flesh meat (gDW ind.-1). The coefficients a, b, c, and d were 5.95 × 10-6, 0.38, 2.36, and 0.33, respectively (Gangnery et al., 2003). The mean values of the surface 9-m layer in the water column at all stations during seasonal investigations were used for F and T. The model computations of the biomass, density, and individual dry flesh meat (Y; 0.8–2.4 gDW ind.-1) of the oysters between 2009 and 2013 using 1 km × 1 km horizontal meshes in the bay were conducted according to Yamamoto et al. (2011), under the assumption that the ropes of the oyster rafts were 9 m in length (Hiroshima City Agriculture, Forestry and Fisheries Promotion Center, 2017). The values were then made up on a sectional basis, and 5-year mean values representative of recent years were obtained seasonally (spring, April–June; summer, July–September; autumn, October–December; winter, January–March). The secondary production (mgDW m-2 d-1) was calculated by multiplying the growth rate (gDW ind.-1 d-1) by the density (ind. m-2). The C:DW ratio of 0.39 for oysters was used to convert biomass into carbon (Nakamura et al., 2003). Although the calculation period for oysters between 2009 and 2013 did not coincide with the field-monitoring period from 2014–2015, the fluctuations (difference from the mean value) in oyster production (with shells) in Hiroshima Bay during the last decade (2006–2015) was within 10% (96,800–116,700 tons y-1) (Ministry of Agriculture, Forestry and Fisheries, 2017). Therefore, the biomass and the secondary production by oysters between 2009 and 2013 was nearly the same as those from 2014–2015.

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2.6. Data analyses Hiroshima Bay was horizontally divided into seven sections based on sampling stations (H1–7) by Voronoi tesselation. The area-weighted mean production of the NB (stations H1–4) and the SB (stations H5 and H6) were evaluated by the following equation (station H7 was removed from analysis due to its enclosed area and extremely limited water exchange with outside water mass (Mutsuda et al., 2008)):

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PPSEA = å(PPSTN ´ ASEC ) / ASEA

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where PPSEA indicates the area-weighted mean production of NB or SB (mgC m-2 d-1); ASEC is the area of each section corresponding to the stations defined by Voronoi tessellation (m2); and ASEA is the area of NB or SB (m2). The transfer efficiencies of carbon from the primary producer to the secondary producers (net zooplankton and oysters) were calculated as the ratio (%) of primary production to secondary production. 3. Results 3.1. Spatial and temporal distributions of phytoplankton The long-term variations in the species composition and density of phytoplankton at stations M1 and M2 as representative stations in the NB and the SB, respectively, are summarized from the MOE seasonal monitoring data (Fig. 3). At both stations, a long-term trend of decreased cell density was observed (Fig. 3e,j). The decreasing trend differed seasonally, and the cell density in spring was markedly decreased (about 1/95 and 1/65 from 1982–1986 to 2012–2014 at stations M1 and M2, respectively). On the other hand, the cell density in winter decreased approximately one-quarter and approximately one-half from 1982–1986 to 2012–2014 at stations M1 and M2,

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respectively. The cell densities in recent years (2012–2014) varied seasonally, at 46 ± 44 (mean ± standard deviation), 2,000 ± 1,900, 1,600 ± 650, and 30 ± 21 cells mL-1 at station M1 in spring, summer, autumn, and winter, respectively (Fig. 3e). The seasonal cell densities were 61 ± 27, 720 ± 1,100, 550 ± 400, and 43 ± 31 cells mL-1, respectively, at station M2 (Fig. 3j). Diatoms have been dominant (> 50%) since 1982, except in the springs from 1987–2001 and 2007–2014 at station M1 (Fig. 3a-d). In the diatoms, Skeletonema costatum dominated in autumn at both stations (Fig. 3c,h). In the other seasons, Chaetoceros spp., Leptocylindrus spp., and Nitzschia spp. sometimes dominated the phytoplankton assemblages during the long-term monitoring period (Fig. 3a,b,d,f,g,i). During the exception periods, Dinophyceae spp., Chlorophyceae spp., and other flagellates were mainly observed. In our investigation from 2014–2015, the cell density of the NB in each season was similar to or higher than that of the SB (Table 1). The cell densities varied seasonally, and were 2,100 ± 670, 12,000 ± 8,900, 1,900 ± 1,600, and 250 ± 340 cells mL-1 in the NB, and 810, 720, 1,800, and 70 cells mL-1 in the SB in May, August, November, and February, respectively. The levels of the cell densities in our investigation during 2014–2015 were relatively higher than those in the most recent years from the long-term monitoring data (2012–2014) in both areas, except in the SB in the summer, due to occasional algal blooms. Diatoms dominated at all stations (Fig. 4). The dominant species changed seasonally. S. costatum dominated in November 2014 (NB, 70 ± 40%; SB, 87%) and in August 2015 (NB, 61 ± 21%; SB, 20%), whereas Chaetoceros spp. (NB, 43 ± 18%; SB, 39%) and Leptocylindrus spp. (NB, 45 ± 17%; SB, 67%) dominated in February and May 2015, respectively. There was no clear difference in the dominant species between the NB and the SB except in August. Leptocylindrus spp. and Nitzschia spp. dominated along with S. costatum in the SB, whereas S. costatum was the dominant species in the NB. Although the cell densities in 2014–2015 in our investigation was higher than that of recent years in the MOE monitoring data, it could be considered representative of recent years in terms of the phytoplankton assemblages.

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3.2. Primary production The structure of the lower trophic ecosystem in Hiroshima Bay is expected to differ between the NB and the SB due to the large differences in phytoplankton biomass and the intensity of oyster farming. Seasonal and spatial variations in primary production in the bay are shown in Figure 5. The regression coefficient (a) between relative irradiance (%) and Chl. a-specific productivity (mgC mgChl. a-1 h-1) in the bay in November, February, May, and August were 0.0219 (r2 = 1.0), 0.0209 (r2 = 0.99), 0.0174 (r2 = 1.0), and 0.0251 (r2 = 1.0), respectively. During the study period, the primary production in the sampling stations ranged from 208 to 1,080 mgC m-2 d-1 in the NB, and from 152 to 567 mgC m-2 d-1 in the SB. The area-weighted mean primary production in the NB was 487, 319, 393, and 919 mgC m-2 d-1 in November, February, May, and August, respectively (530 mgC m-2 d-1 on average); whereas in the SB it was 439, 183, 185, and 443 mgC m-2 d-1, respectively (310 mgC m-2 d-1 on average). The area-weighted mean primary production in the NB was 1.1 to 2.1 times higher than that of the SB throughout the four seasons. 3.3. Secondary production by net zooplankton The population density of the net zooplankton ranged from 190 to 2,440 × 103 ind.

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m-2, and copepods of the genera Oithona and Paracalanus dominated (mean 45.7%) at the sampling stations during the study period. The mean temperature in the water column at the seven stations in the bay ranged from 20.7−21.3, 10.9−11.4, 14.1−16.0, and 22.9−24.4 ℃ in November, February, May, and August, respectively, and secondary production by the net zooplankton were estimated based on the species composition in each sampling station using the regression equation between specific growth rate and water temperature described in the Materials and methods section. Biomass and secondary production by the net zooplankton were 46–675 mgC m-2 and 8.2–197 mgC m-2 d-1, respectively, in the NB, and 54–387 mgC m-2 and 8.0–97 mgC m-2 d-1, respectively, in the SB (Fig. 6). The distribution of the net zooplankton differed from that of the phytoplankton. High net zooplankton biomass was observed in the central part (station H5 in the SB) and the northeastern part (H2 in the NB) of Hiroshima bay. The area-weighted mean secondary production by net zooplankton in the NB was 15, 10, 17, and 116 mgC m-2 d-1 in November, February, May, and August, respectively (39 mgC m-2 d-1 on average). In the SB, it was 80, 25, 17, and 73 mgC m-2 d-1, respectively (49 mgC m-2 d-1 on average). The area-weighted mean secondary production by net zooplankton in the NB was higher than that of the SB in August, whereas the values in the NB were lower than those in the SB in November and February.

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3.4. Secondary production by oysters During the study period, the water temperature (T) and the POM concentration as a food source (F) for oysters ranged from 10.3–25.0°C and 1.9–6.6 mg L-1, respectively. The POM concentrations in August were high at all seven stations due to phytoplankton blooms (4.9 ± 1.1 mg L-1). Biomass and secondary production by oysters also increased in the summer (5-year mean during July to September) at every station (Fig. 7). The maximum production was always observed at station H7 throughout the year (18.1–167 mgC m-2 d-1), where the oyster rafts were densely arranged. The oyster rafts were more densely arranged in the NB than in the SB (Fig. 2). The biomass and secondary production by oysters ranged from 2.8–15.0 gDW m-2 and from 4.6–58.1 mgC m-2 d-1, respectively, in the NB, and from 1.0–5.5 gDW m-2 and from 1.7–24.6 mgC m-2 d-1, respectively, in the SB. The area-weighted mean secondary production by oysters in the NB was 28, 6.2, 12, and 34 mgC m-2 d-1 in November, February, May, and August, respectively (20 mgC m-2 d-1 on average). In the SB, the levels of secondary production were 10, 2.4, 4.3, and 15 mgC m-2 d-1, respectively (8.0 mgC m-2 d-1 on average). The area-weighted mean secondary production by oysters in the NB was 2.2–2.8 times higher than that of the SB in all four seasons, and showed similar spatial patterns as primary production. 3.5. Transfer efficiency The area-weighted mean secondary production, which was the sum of production by the net zooplankton and by the oysters, was 43, 16, 29, and 150 mgC m-2 d-1 in November, February, May, and August, respectively (59 mgC m-2 d-1 on average) in the NB, whereas in the SB, the values were 90, 27, 21, and 88 mgC m-2 d-1, respectively (57 mgC m-2 d-1 on average). The contribution of farmed oysters to the secondary production was limited in the SB (11, 9, 20, and 17% in November, February, May, and August, respectively; 14% on average), whereas it was 65, 38, 42, and 23%, respectively (34% on average), in the NB. To evaluate the spatial differences in biological productivity at the lower trophic levels in the bay, the seasonal and annual

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transfer efficiencies of carbon from the primary producers to the secondary producers, including the net zooplankton and the oysters, were estimated (Fig. 8). Primary production was more efficiently utilized and transferred to the secondary producers in the SB (11.4–20.6%; 16.7% on average) than in the NB (5.1–16.3%; 9.4% on average).

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4. Discussion 4.1. Food competition between net zooplankton and oysters Net zooplankton and suspension-feeding bivalves such as oysters compete directly for food (Gerritsen et al., 1994). The density and biomass of the zooplankton per unit volume in the estuary, where primary production is relatively high, tended to be one to ten times higher than that of the offshore area (Roman et al., 2001; Magalhães et al., 2006; Walkusz et al., 2009). Oyster farming is frequently carried out in estuaries due to the rich food availability and convenience. Stable isotope (δ13C and δ15N) and carbon mass-balance studies suggested potential food sources of the suspension-feeding oysters (Crassostrea gigas). Planktonic micro-algae were known as the main food source of oyster when algae were abundant. On the other hand, when foods were scarce, the source can change to micro-zooplankton and detritus with the appropriate size specification (Dupuy et al., 2000; Dubois et al., 2007). A stable isotope study revealed that Crassostrea gigas consumed particulate organic matter (POM) including mainly phytoplanktons (ca. 89%) in Jiaozhou Bay of China (Xu and Yang, 2007). Therefore, in the present study, competition between net zooplankton and farmed oysters was highly expected in estuaries such as NB, where primary production was relatively high. In Hiroshima Bay, more intensive oyster farming is carried out in the NB than in the SB. The area-weighted mean secondary production by oysters was 20.0 ± 13.0 mgC m-2 d-1, reaching approximately half of the mean secondary production by net zooplankton (39.4 ± 51.1 mgC m-2 d-1) in the NB, whereas the production by oysters was 8.0 ± 5.9 mgC m-2 d-1, much less than that of the net zooplankton (48.8 ± 32.5 mgC m-2 d-1) in the SB. Consequently, competition for food between the net zooplankton and the farmed oysters in the NB was severe. The carrying capacity of oyster farming in Hiroshima Bay was not evaluated in this study. We attempted to compare the situation in Hiroshima Bay (387 km 2) and Narragansett Bay (355 km2) in Rhode Island, where the carrying capacity was evaluated by Ecopath, because of the similar areas of the bays. In Narragansett Bay, the annual mean primary production and the annual mean soft tissue biomass of the farmed oysters were 323 gC m-2 y-1 (885 mgC m-2 d-1) (Oviatt et al., 2002) and 0.0095 gDW m-2 (Byron et al., 2011b), respectively, and the carrying capacity of the oyster farms was estimated to be 5.9 gDW m-2. In contrast, in Hiroshima Bay, the annual mean primary production and the annual mean soft tissue biomass of farmed oysters were 530 mgC m-2 d-1 and 7.1 gDW m-2 in the NB, and 310 mgC m-2 d-1 and 2.4 gDW m-2 in the SB. The annual mean primary production in the NB and SB were approximately two-thirds and one-third of that in Narragansett Bay, respectively. On the other hand, the annual mean soft tissue biomasses of the farmed oysters in the NB and the SB were 1.2 times higher than and almost the same as the carrying capacity of Narragansett Bay, respectively. Consequently, it is likely that oyster farming in Hiroshima Bay has reached the ecological carrying capacity. The high contribution of oysters to secondary production (34%) indicates that oyster farming in the NB will inhibit the production of net zooplankton. The recent decrease in the cell density of phytoplankton in the bay (Fig. 3)

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may intensify the competition for food between net zooplankton and oysters.

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4.2. Spatial differences in productive structure Regarding the spatial differences in the transfer efficiencies to the secondary producers in Hiroshima Bay, our results showed relatively low efficiencies in the NB (5.1–16.3%; 9.4% on average) compared to the SB (11.4–20.6%; 16.7% on average) (Fig. 8). The relatively low transfer efficiencies from primary to secondary production in the NB may be explained by excess primary production and/or the lack of consideration of micro-zooplankton in this evaluation. In highly productive coastal areas, negative impacts such as increased organic enrichment of the sediment, the occurrence of hypoxic waters due to aerobic decomposition of organisms produced in the water, and increases in the acid-volatile sulfide (AVS) content of the sediment have been reported (e.g., Tsutsumi et al., 2015). The NB had experienced excess phytoplankton blooms such as red tides on occasion (Imai et al., 1993; Lee et al., 1996; Tomaru et al., 2004), as well as hypoxic waters every summer (Kimura, 1975; Yamamoto et al., 2011), indicating that significant amounts of phytoplankton were deposited, polluting the sediment without being used by secondary producers (Bodungen et al., 1986). The organic pollution in the sediment of the NB was also explained by low dissolved oxygen concentrations in bottom waters (4.3 ± 1.1 mg L-1 at M1) compared to the SB (6.3 ± 0.6 mg L-1 at M2) in the summer during the last decade (2005–2014) as recorded by the MOE. On the other hand, micro-zooplankton such as heterotrophic protists and ciliates are also known to be a food source for secondary producers. Fessenden and Cowles (1994) reported that ciliates contributed 16–100% of the estimated carbon ingested by copepods during non-upwelling months and during diatom blooms. Dupuy et al. (2000) suggested that oysters (C. gigas) consume suspended matter as a food source, which contains not only phytoplankton but also heterotrophic protists, allowing the transfer of carbon from the microbial loop to the oysters. In the case of the Seto Inland Sea, which includes Hiroshima Bay, Hashimoto et al. (1997) estimated that annual mean production by the micro-zooplankton (79.9 mgC m-2 d-1) was about one-tenth that of phytoplankton (781 mgC m-2 d-1) in an investigation from 1993–1994. If the ratio remained comparably small in our study period, the contribution of micro-zooplankton as food for secondary producers would be negligible.

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5. Conclusions The aims of the present study included the effects of bivalve farming on the productivity of lower trophic levels in coastal areas and the spatial differences in primary production, secondary production, and the transfer efficiencies from primary producers to secondary producers between an estuary and an offshore area of the bay. The conclusions obtained were as follows: (1) The area-weighted mean secondary production by oysters in the NB was 20.0 ± 13.0 mgC m-2 d-1, about half of that of the net zooplankton (39.4 ± 51.1 mgC m-2 d-1), meaning that the competition for food between the net zooplankton and the farmed oysters was severe. On the other hand, the production by oysters in the SB was 8.0 ± 5.9 mgC m-2 d-1, much lower than that of the net zooplankton (48.8 ± 32.5 mgC m-2 d-1), meaning that the competition between them was limited. (2) The transfer efficiencies in the NB and the SB differed significantly, as the

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efficiencies in the NB (5.1–16.3%; 9.4% on average) were relatively low compared to those in the SB (11.4–20.6%; 16.7% on average). The energy was transported efficiently in the offshore area via the classical grazing food chain.

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Acknowledgments The authors would like to thank Mr. Kouji Takeuchi, Mr. Youhei Shigeoka, Mr. Katsuya Ohura, and Mr. Yoshiyuki Takahashi for piloting the survey ship (HIKARI). We express our gratitude to Hiroshi Shibata, M.Sc., and the students of Hiroshima University, Kobe University, and the National Institute of Technology, Hiroshima College, for their support during the surveys, and to Dr. Cervinia V. Manalo (Hiroshima University) for her English language proofreading. This research was financially supported by the Environment Research and Technology Development Fund (S-13) granted by the Ministry of the Environment (MOE), Japan.

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Fig. 1. Our sampling sites (Stns H1-7) and monitoring site of the MOE (Stns M1-2) in Hiroshima Bay, Seto Inland Sea, Japan. Dashed lines in the bay indicate the border lines of the sea sections defined by Voronoi tesselation. The bay was divided into northeastern (NB; H1-4) and southwest part of the bay (SB; H5, 6) based on the geological structure (Kittiwanich et al., 2016). Fig. 2. Distribution of the rafts for oyster farming in the Hiroshima Bay. The grey

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polygons indicate the permission area to set the oyster rafts. Fig. 3. Temporal distribution in the species compositions (a-d, f-i) and the cell density (e, j) of phytoplanktons at Stns M1 (northeastern part) and M2 (southwestern part) between 1982 and 2014 collected by MOE. Five year mean values were used. The unavailable data in 1997 and 2008 were excluded from the analysis, and three years mean values during 2012 and 2014 were showed.

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Fig. 4. Seasonal variations of the species compositions (%) of phytoplanktons in the NB (Stns H1-4) and the SB (Stns H5, 6) in the bay between November 2014 and August 2015.

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Fig. 5. Seasonal and spatial variations of primary production in euphotic zone of the bay. Seasonal values of the regression coefficient (a) between relative irradiance and Chl. a-specific productivity were indicated in the figures.

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Fig. 6. Seasonal and spatial variations of biomass (a-d) and secondary production (f-i) of net zooplanktons in the bay. (e) and (j) show the mean values of the biomass and the

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secondary production in the seasonal investigations. Fig. 7. Seasonal and spatial variations of secondary production of oysters in each

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section of the bay. Five-year mean values as representative for recent years were obtained seasonally (Spring, April to June; Summer, July to September; Autumn,

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October to December; Winter, January to March). Fig. 8. Seasonal variations of the carbon transfer efficiencies from the primary producer (phytoplanktons) to the secondary producers (oysters and net zooplanktons) in the NB (Stns H1-4) and SB (H5, 6).

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Table 1. Seasonal variations of cell density of phytoplanktons in the NB (Stns H1-4) (cells mL-1)

Nov. 2014

Feb. 2015

May 2015

Aug. 2015 12,000 ±

1,900 ± 1,600

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NB (Stns H1-4)

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Highlights Impact of the oyster farming on productivity of lower trophic levels was evaluated.

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The primary productions in the estuary were higher than those in the offshore area.

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The net zooplankton productions were relatively low in the estuary.

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The oyster productions in the estuary were higher than those in the offshore area.

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The transfer efficiencies in the estuary were lower than those in the offshore area.

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Figure 8