FOOD COMPOSITION FOR BLUE MUSSELS (MYTILUS EDULIS) IN THE MENAI STRAIT, UK, BASED ON PHYSICAL AND BIOCHEMICAL ANALYSES.
The blue mussel Mytilus edulis is one of the most important aquaculture species in the North Atlantic coastal regions. Approximately two-thirds of the total mussel production in the United Kingdom are harvested in Wales, particularly in the Menai Strait (Saurel et al. 2004). The Menai Strait has very unique characteristics in terms of hydrodynamics and topography. The strait is 31 km long and 0.3-8 km wide (Fig. 1) and is characterized by large tidal flats in the northern region and strong tidal currents (>2.5 m [s.sup.-1]) in the central region and southern mouth of the strait. Direction of residual flow in the strait is southwest and its volume transport during neap and spring tides is estimated to be approximately 330 and 800 [m.sup.3] [s.sup.-1], respectively (Simpson et al. 1971). The water residence time is estimated to be approximately 2-3 days (Rippeth et al. 2002).
An important function of phytoplankton transported from Liverpool Bay into the Menai Strait for the mussel production has been pointed out by Tweddle et al. (2005) and Simpson et al. (2007). They estimated that up to 50% of the transported phytoplankton was removed by filter feeders near the mussel bed. On the other hand, benthic microalgae on tidal flats would also contribute to the growth of mussels in the Menai Strait (Saurel et al. 2007. Widdows et al. 2009).
In addition, detritus of macroalgae may be another important food source for mussels in some cases (Duggins & Eckman 1997, Lefebvre et al. 2009). Historically. Field (1911, 1923) has already pointed out food of mussels in the United States coasts based on stomach content analyses. The contribution of each food source to mussel production, however, has not been quantitatively clarified yet in the Menai Strait.
In the last two decades, stable isotopes have been used to quantify the roles of food sources for bivalves in estuaries and coastal regions (Riera & Richard 1996, Riera 1998, 2007, Kang et al. 1999. 2003. Kasai & Nakata 2005, Kasai et al. 2006. Dubois et al. 2007b). Stable isotopic ratios of carbon and nitrogen in consumer tissues are affected by the isotope ratios for each food source and relative proportions of assimilation and fractionation, which are defined by stepwise enrichment at each trophic level (Vander Zanden & Rasmussen 2001). Marine primary producers (pelagic phytoplankton, benthic microalgae, and macroalgae) and terrestrial C3 photosynthesis plants typically have well-separated carbon stable isotope ratios, whereas a relatively large fractionation of the nitrogen stable isotope ratio is observed among trophic steps (De Niro & Epstein 1978, Minagawa & Wada 1984). The carbon stable isotope ratio is mainly used to determine the ratio of primary productions, and the ratio of nitrogen is used to identify the trophic level (McCutchan et al. 2003). These ratios have increasingly been used in coastal ecology to identify potential food sources (Fry 2006). Recent studies on isotopic trophic-step fractionation of bivalves have made it possible to accurately estimate the contribution of food sources to bivalve diets (Kasai et al. 2006, Dubois et al. 2007a, Yokoyama 2008). Stable isotope analyses of mussels, phytoplankton. and benthic microalgae are therefore one of the useful tools to estimate the contribution of food sources to mussels in the Menai Strait.
The aim of the present study was to assess the roles of different components of particulate organic matter (POM) as food for the blue mussel (Mytilus edulis) by comparing the inside and outside of the Menai Strait based on stable isotope analyses and hydrographic observation. Species identification of pelagic and benthic phytoplankton is important information for the quantitative analyses of the contribution. Investigation of these processes would make it possible to clarify effective food supply and consumption systems for benthic filter feeders and help to determine where to put new mussel bed culture systems.
MATERIALS AND METHODS
The study area was located between Liverpool and Caernarfon bays as shown in Figure 1. The depth of the strait is shallower than 15 m at low water. The tidal flats are located in the northern and southern regions of the strait, and the northern tidal flats are larger than the southern flats. The commercial mussel bed is located on the northern tidal flats (53.23[degrees] N 4.12[degrees] W).
Physical Observations and Collection of Samples
Tidal flow data sets were collected along seven observational transect lines (Fig. 1). Thirteen-hour hydrographic observations were conducted from May 16 to 23, 2007, using a ship-equipped Acoustic Doppler Current Profiler (ADCP; Teledyne RD Instruments 1.2-MHz Workhorse). Longitudinal flow velocity data were collected at intervals of 1-1.5 h to clarify changes in flow velocity during the semidiurnal tidal cycle. Flow velocity was measured at depths with intervals of 0.5 m from 1.45 m below the surface to the bottom. Measured flow velocities were averaged vertically and longitudinally along each observational transect line.
Measurements using a conductivity-temperature--depth profiler (CTD; Seabird Electronics) at four fixed points (Stations 1-4, Fig. 1) were performed with intervals of 1-1.5 h during the Acoustic Doppler Current Profiler observations. Surface water samples were collected during CTD casts with plastic bottles to measure the concentrations of chlorophyll-a, particulate organic carbon (POC), and nitrogen (PON), and the stable isotope ratios of carbon and nitrogen in POM.
Seawater samples of 200 ml for chlorophyll-a concentration were filtered through Whatman GF/F glass fiber filters (diameter, 47 mm) and the concentrations were estimated in accordance with the JGOFS fluorometric analysis method (JGOFS 1996). In this method, pigments were extracted with acetone and chlorophyll-a fluorescence was measured using a Turner Design 10-AU fluorometer.
For collection of POM, seawater samples of 2,000 ml prefiltered with a 250-[micro]m mesh nylon filter were filtered with Whatman GF/F glass fiber filters. The GF/F filters were preheated at 500[degrees]C to remove organic matter contaminants before the filtration.
Mussels were collected from 15 sites in the Menai Strait during May 18-23, 2007, and were classified into four regions based on CTD and water sampling stations (Fig. 1). Fifteen mussels with 30-65 mm shell lengths were randomly selected at each sampling site and cleaned before being oven-dried at 65[degrees]C for more than 12 h. Adductor muscles were extirpated, powdered after oven-drying, and processed for lipid extraction before measuring their stable isotope ratios. Lipids were extracted by a chloroform and methanol method following Folch et al. (1957). In accordance with the method, samples were placed into 2-ml micro test tubes with a 1.5 ml chloroform and methanol mixture (1:1, in volume), and the mixture was removed by direct suction 48 h after the first treatment and evaporated at 60[degrees]C for more than 20 h. Nitrogen stable isotope ratios were measured from samples without lipids being extracted. Green and brown macroalgae (Ulva sp. and Ascophyllum nodosum) samples were also collected from near Station 2.
Benthic microalgae were collected from approximately 1,000 g of surface 1-cm-depth sediments from four intertidal sites on mud and sandy flats on July 24, 2008, and July 26, 2008 (Fig. 1). The benthic microalgae were separated from the sediments using sands preheated at 500[degrees]C and fluorescent light on the basis of phototaxis, in accordance with the procedure described by Riera and Richard (1996).
Stable Isotopic Analysis of Carbon and Nitrogen
The filtered POM and powdered mussels, benthic microalgae, and macroalgae were packed in tin capsules and subsequently compressed at 50 kg [cm.sup.-1] to remove any remaining air nitrogen. After combustion of these tin capsules at 1,000[degrees]C and extraction of C[O.sub.2] and [N.sub.2] gases, the POC and PON concentrations and their isotopic ratios were measured with an isotope ratio mass spectrometer (DELTAplus, Finigan Mat) through a Conflo III interface. The carbon and nitrogen stable isotope ratios ([[delta].sup.13]C, [[delta].sup.15]N) are expressed in a usual delta notation as follows:
[[delta].sup.13]C or [[delta].sup.15]N([per thousand]) = (([R.sub.sample]/[R.sub.standard]) - 1) x 1,000,
where [R.sub.sample] and [R.sub.standard] are isotopic ratios of sample and standard material, respectively. Standard material was cretaceous Vienna PeeDee Belemnite for [[delta].sup.13]C and air [N.sub.2] for [[delta].sub.15]N. Glycine was used as a secondary standard reference material to calibrate the measurements of POC, PON, and isotope ratios.
Assessment of Origin and Components of POM
The carbon isotope ratio of POM can be used to determine its origin based on the isotopic differences among primary producers (C3 terrestrial plants and marine primary producers). The mean [[delta].sub.13]C of C3 terrestrial plants is almost -28.2[per thousand] (range, -30.0[per thousand] to -26.7[per thousand]; Yokoyama 2008), whereas that in marine primary producers is higher than -25%" (Riera & Richard 1996, Yokoyama & Ishihi 2007, Banaru et al. 2007, Dubois et al. 2007b). Furthermore, [[delta].sup.13]C in benthic microalgae was often 5[per thousand] higher than that in phytoplankton (France, 1995). Fry and Sherr (1984) reported that the [[delta].sup.13]C in phytoplankton and benthic microalgae was from -24[per thousand] to -18[per thousand] and from -20[per thousand] to -10[per thousand] respectively. According to Savoye et al. (2003), C:N molar ratio is another good indicator to know the origins of POM. A C.N ratio in the range 6-10 represents phytoplankton and that in 3-6 represents zooplankton and bacteria. The ratio of terrestrial organic matter is typically higher than 12. The origins of POM can be estimated from a combination of C:N and stable isotope ratio.
To assess the components of POM, the rate of planktonic primary producer (pelagic phytoplankton and resuspended benthic microalgae) biomass in POM from the chemical concentrations was calculated using the following equation:
RPB(%) = [gamma][chl.a]/[POC] x 100,
where RPB is the rate of planktonic primary producer biomass, [gamma] is the slope of the regression line between organic carbon and chlorophyll-a observed in this study as shown in Figure 2 (45.2, determined by linear regression, P < 0.05, [R.sup.2] = 0.42), and [chl.a] and [POC] are the concentrations of chlorophyll-a and POC, respectively. In this study, the other components of POM were regarded as detritus which did not contain chlorophyll-a.
The consumption of the primary producers ([P.sub.C] t C [day.sup.-1]) in the Menai Strait was calculated from the volume transport of residual flow and difference in the mean chlorophyll-a concentration between Stations 2 and 4 ([DELTA]chl.a). The equation is as follows:
Pc = [gamma] x Q x [DELTA]chl.a,
where Q is the flux of volume transport of the residual flow (510 [m.sup.3] [s.sup.-1], shown in the Results section) and [gamma] is the slope of the regression line between POC and chlorophyll-a shown in Figure 2.
Isotope Mixing Model
To estimate the contribution of potential food resources to mussels, a single source (carbon) isotope two end-member mixing model (Phillips & Gregg 2001) was used. The potential primary producers in the Menai Strait comprise pelagic phytoplankton supplied mainly from outside of the strait, and benthic microalgae and macroalgae. The carbon stable isotope ratio of POM at Station 1 during southwestward flow periods (-22.1[per thousand]) was used as being representative of the pelagic phytoplankton from outside of the strait because Station 1 was facing the outer ocean and would represent the outside oceanic conditions when southwestward tidal flow was dominant. The internal production of phytoplankton in the strait would be lower because the short residence time is insufficient for phytoplankton proliferation (Simpson et al. 2007). Terrestrial organic matter in the strait is negligible because estimation of the origin of POM indicates less contamination by terrestrial organic matter. The mean isotope ratio of benthic microalgae was estimated from this study. The 2.17[per thousand] was used for [[delta].sup.13]C of trophic stepwise isotope fractionation of mussels (Dubois et al. 2007a). The contribution of the two potential food resources was estimated as
[[delta].sup.13][C.sub.Mu] - 2.17 = [f.sub.POM] [[delta].sup.13][C.sub.POM] + (1 - [f.sub.POM]) [[delta].sup.13] [C.sub.BM],
where [[delta].sup.13][C.sub.Mu], [[delta].sup.13][C.sub.POM] and [[delta].sub.13][C.sub.BM] are the carbon isotope value of mussels, POM, and benthic microalgae, respectively, and fpoivi is the contribution rate of POM to mussel foods.
Microscopic Observation of Phytoplankton Community
Bottom seawater (0.5 m above the bed) at Stations 1 and 2 for phytoplankton observation was collected from June 29 and July 1, 2010, respectively. Samples of 250 ml of seawater were collected at intervals of 1-2 h in daytime over 12.5 h. Each water sample was fixed within plastic bottles by the addition of glutaraldehyde to give a final concentration of 1% in sample volume. Phytoplankton samples were settled over 48 h in bottles and collected in 10-ml glass tubes by using a pipette. Phytoplankton of over 250 cells in each water sample were counted and identified below the genus level using an optical microscope (x400). The number of cells of each genus was converted to relative cell abundance compared with total phytoplankton cells. Identified genera were grouped based on the habitat into two groups: pelagic and thycopelagic (living in both pelagic and benthic environments) species (Rouillon et al. 2005).
Flow Structure in the Menai Strait
Semidiurnal tidal current was observed in the Menai Strait (Fig. 3). The maximum velocities of the tidal currents were 0.5-1.0 m [s.sup.-1]during the northeastward flow and 0.6-1.3 m [s.sup.-1] during the southwestward flow. The highest flow velocity in this survey was recorded at line 5 during the southwestward flow (1.3 m [s.sup.-1]). The high and low waters were concurrent in the strait. The occurrence of slack water at each observational transect line was, however, delayed by 0-5 h when comparing high and low waters. For example, the occurrence of slack water at line 1 (the northern mouth of the strait) was observed on high and low waters and was delayed by 3 h at line 4 (the mussel bed) and 5 h at line 7 (the southern mouth). The occurrence of slack water at line 7 was observed on the second high or low water period. The slack water moved toward the southern region of the strait. This flow pattern can be interpreted as the water inflow from the mouth into the strait during the flood tide and the outflow during the ebb tide. Souza and Hill (2006) reported similar flow patterns in the Menai Strait as the phase shifts between flow variation and tidal level. The largest residual flux of water was observed at line 5 (510 [m.sup.3] [s.sup.-1]), which is the same as the average pointed out by Simpson et al. (1971).
Salinity and Water Temperature
Figure 4 shows the time series of physical and biochemical parameters (POC, PON, C:N ratio, chlorophyll-a, RPB, salinity, temperature, and current velocity) for each station. Salinity and temperature in the Menai Strait ranged from 32.4 to 33.4[degrees]C and 11.9 to 14.2[degrees]C, respectively. Salinity and temperature at the central region (Stations 2 and 3) showed relatively low values compared with those near the mouth regions (Stations 1 and 4). This slight difference in salinity may be caused by freshwater inflow from small streams in the central region of the strait.
Variation and Relation of Environmental Parameters in the Menai Strait
The POC, PON, and chlorophyll-a decreased with salinity and C:N ratio at Station 1, when the northeastward flow was dominant. This indicates that the chlorophyll-a depleted water on the mussel bed was withdrawn from the strait. After slack water, the tidal flow direction changed to southwest and the biochemical parameters (POC, PON, and chlorophyll-a) returned to their initial values with increasing salinity. These parameters fluctuated simultaneously. This indicates that water inflow from outside of the strait causes increases in chlorophyll-a through transport of dense pelagic phytoplankton from Liverpool Bay. During the southwestward flow at Station 2, increases in chlorophyll-a and RPB were recognized. The mean concentrations of POC, PON, and chlorophyll-a at Station 2 were higher than those at Station 1, because Station 2 was located 11 km away from Station 1 and the effect of water intrusion from outside of the strait would be smaller. This indicates that high primary production occurs locally at Station 2 and resuspended microalgae are the likely source of that production.
At Station 2, the highest chlorophyll-a concentration (7.2 [micro]g [L.sup.-1]) was observed 30 min before slack water when the flow direction changed from southwestward to northeastward. The concentration, however, decreased rapidly 30 min after the slack water (2.06 [micro]g [L.sup.-1]). This steep decrease in chlorophyll-a indicates there was an inflow of phytoplankton depleted water from the mussel bed. During the low chlorophyll-a period at Station 2, RPB decreased to 22.6% from 72.4%. This suggests that the pelagic phytoplankton and resuspended microalgae in POM were strongly grazed by mussels.
At Station 4 located in the southern area of the strait, an inflow of outside saline water from Caernarfon Bay was observed during the northeastward flow. Temporal variations in POC, PON, and chlorophyll-a, however, changed only slightly and these mean concentrations were smaller than those at Station 1. The effect of inflow of pelagic phytoplankton from the southern mouth would be limited. Because the mean chlorophyll-a concentration at Station 4 was the lowest in the strait, primary production by resuspended microalgae in this region was very small, and the inflow of chlorophyll-a depleted water from the northern mussel bed by the residual flow probably contributed to the low concentration.
Origins and Components of POM in the Menai Strait
The C:N ratio of POM in the Menai Strait ranged from 5.9 to 10.1 (Fig. 4). According to the interpretation by Savoye et al. (2003), results in the present study indicate that POM in the Menai Strait mainly originated from marine primary production and was less affected by terrestrial organic matter. The C:N ratio of POM in the strait exhibited a decrease from the northern region to the southern region. This indicates there was a change in the ratio of components of POM during movement of the water mass associated with the residual current. A decrease in the C:N ratio suggests an increase in the fraction of bacteria and zooplankton (Savoye et al. 2003) and that secondary production would be enhanced as the water mass moves from north to south.
Averaged [[delta].sup.13]C and [[delta].sup.15]N values of POM were -21.7[per thousand] [+ or -] 0.5[per thousand] and 9.1[per thousand] [+ or -] 1.0[per thousand], respectively (Fig. 5). Because the [[delta].sup.13]C was higher than -25[per thousand], the organisms probably originated from marine primary producers. This result is consistent with the results of the C:N ratio. Terrestrial organic matter, therefore, would be a minor food source for mussels in the Menai Strait. The mean [[delta].sup.13]C and [[delta].sub.15]N in POM were significantly higher at Stations 2 and 3 compared with those at Stations 1 and 4. These significant differences indicate that the ratios of components in POM changed in the central region of the strait.
The consumption of the primary producers, Pc, in this study was estimated to be approximately 6.3 t C [day.sup.-1].
Phytoplankton of 15 genera were identified in the samples from the Menai Strait (Table 1). Diatoms were dominant, whereas dinoflagellates were present in smaller proportions. In the phytoplankton community, pelagic and thycopelagic (living in both pelagic and benthic environments) species comprised 59.3%-77.2% and 12.8%-40.7% of the cells, respectively. This result suggests that resuspension of benthic microalgae occurred less than that for thycopelagic species in the strait. The dominant genus at each station was different; the group of long horn pennates and Thalassiosira spp. were dominant at Stations 1 and 2, respectively. The cell abundance ratio of thycopelagic species at Station 1 facing the outer ocean was larger than that at Station 2. This suggests that primary production by resuspended benthic species in the Liverpool Bay region is considerably larger than that in the Menai Strait region.
Contribution of Food Resources to Mussel Production
The mean [[delta].sup.13]C and [[delta].sub.15]N stable isotope ratios of mussels were -18.0[per thousand] [+ or -] 1% and 11.0[per thousand] [+ or -] 0.5[per thousand], respectively (Fig. 5). These ratios were significantly higher in the central region of the strait. This trend is similar to that of the POM, suggesting that the food environment for mussels is controlled by differences in the ratio of components in local POM.
Carbon and nitrogen stable isotope ratios of the benthic microalgae collected from surface sediments were measured as -16.2[per thousand] [+ or -] 2.5[per thousand] and 7.0[per thousand] [+ or -] 1.8[per thousand], respectively. In accordance with the C-N map based on all observed results (Fig. 6), the ratio of [[delta].sub.13]C for green macroalgae Uha sp. and brown macroalgae Ascophyllum nodosum had a similar value as benthic microalgae. For [[delta].sub.15]N, the ratio of Uha sp. was relatively higher than that of benthic microalgae, whereas A. nodosum was located on the same range of benthic microalgae. The estimated stable isotope ratios of food for mussels from stepwise trophic fractionation were located in the midpoint of benthic microalgae and local POM at Station 1 as being representative of the pelagic phytoplankton from outside of the strait.
Table 2 shows the estimated food source contributions to mussel production based on the carbon stable isotope mixing model. The mean carbon stable isotope ratio of benthic microalgae estimated from this study, -16.2%, was used in the model. The contribution of benthic microalgae was estimated to be 22%-50%, and it was greater in the central and south regions of the strait. The other contribution by the pelagic phytoplankton was estimated to be 50%-78%. This effect gradually decreased from the strait mouth to the inside.
In this study, it was confirmed that the food environment for mussels in the Menai Strait was constituted by a combined supply of pelagic and benthic primary production. The tidal current could play an important role in the supply of food source. In the area near the commercial mussel bed, the most suitable condition for food was established by a combination of external and internal sources of organic matter. External pelagic phytoplankton supplied from Liverpool Bay was critical for mussel production in the northern region of the strait, and the role of benthic primary production was not negligible, particularly in the central and southern regions. Semidiurnal tidal current during southwestward flow was stronger than that during northeastward flow in the Menai Strait, and the southwestward residual flux of water was dominant. Variation of environmental parameters corresponded well with the tidal flow. Biochemical estimations in this study, therefore, could present the detailed state of biological production influenced by the tidal flow in the Menai Strait.
Page and Hubbard (1987) indicated that mussel growth was correlated with regional variation of food availability. Rouillon and Navarro (2003) indicated the difference in utilization for Mytilus edulis between the diatom Phaeodactylum tricornutum and the flagellate Tetraselmis suecica. Decreases in food supply reduce the mussel growth in bay-scale mussel aquaculture (Waite et al. 2005). Commercial mussel beds seem to be located in the most suitable areas for rapid growth because of high abundance of food. From the hydro-graphic point of view, Simpson et al. (2007) and Widdows et al. (2009) indicated that the mussel colony structure enhanced the near-bed turbulence and resuspension of benthic microalgae, which could contribute to improvement of the food environment for mussels. Asmus and Asmus (1991) suggested mussel beds significantly promote primary production by releasing ammonia. Dame et al. (1991) and Prins and Smaal (1994) suggested mussel beds release ammonia and affect the nutrient flux. The commercial mussel bed itself has a potential to increase the local primary production. From this biochemical point of view, the Menai Strait would be expected to be a good location for
mussel beds. The nitrogen stable isotope ratio of POM at Station 2 near the mussel bed was relatively higher than that in the other stations. The nitrogen stable isotope ratio of ammonia excreted from zooplankton is lower than the ratio of their food (Mullin et al. 1984, Hoch et al. 1996). Rolff (2000) suggested the stable isotope ratio of phytoplankton decreased in summer because of the use of excreted ammonia from zooplankton. The high nitrogen stable isotope ratio of POM in the central region, therefore, would not be caused by direct utilization of ammonia released from mussels. Large tidal excursion would instead contribute to horizontal nutrients transport in the Menai Strait, but not the aforementioned biochemical process.
As a result, the consumption of the primary producers in this study was estimated to be approximately 6.3 t C [day.sup.-1], which was slightly larger than the amount consumed on the mussel bed (approximately 4.5 t C [day.sup.-1]) estimated by Tweddle et al. (2005). This difference may be caused by seasonal differences in the grazing activity of mussels, additional consumption by zooplankton and other benthic filter feeders, or differences in [gamma] determination. To obtain a more accurate consumption amount, the effect of grazing by zooplankton and other filter feeders should be considered. Particularly in the south region of the strait, the existence of other filter feeders could account for the observed low chlorophyll-a concentration. The common cockle Cerastoderma edule has been identified as one of the potentially important primary consumers (Saurel et al. 2007). A good correspondence of almost the same values in this and previous studies suggests, however, that 5-6 t C [day.sup.-1] could be regarded as an average consumption rate of the primary production in the Menai Strait.
The stable isotope ratio of POM at Station 1 representing outside pelagic phytoplankton largely differed from the estimated stable isotope ratio of food for mussels. Because the [[delta].sup.13] C of benthic microalgae was considerably higher than that of pelagic phytoplankton, benthic microalgae would cause the spatial change in POM components. In this study, the contribution rate of benthic microalgae to mussel production was estimated to be 22%-50%. In accordance with a result of numerical simulation (Simpson et al. 2007), -50% of pelagic phytoplankton from outside of the strait was consumed near the mussel bed. Thus, this ratio corresponds to 50%-78% contribution rate of pelagic phytoplankton for mussel production.
The larger decrease in RPB in Station 2 in contrast to the smaller change of POC suggests that mussels do not assimilate all components of POM and that the phytoplankton fraction in POM is easily assimilated. Levinton et al. (2002) demonstrated that mussels can ingest low-quality (cellulose-rich) food and assimilate the more nutritionally rich phytoplankton cells. The filtration/ingestion of suitable foods by bivalves has been reported for clams from stable isotope analyses (Kasai & Nakata 2005). Ward et al. (1998) reported that the Pacific oyster Crassostrea gigas and the American oyster Crassostrea virginica can differentially filter out living algal cells from detritus. Williams (1981) suggested that the blue mussel Mytilus edulis have low assimilability of detritus from salt marsh vascular plants from feeding experiments. Levinton et al. (2002) found that kelp detritus was not a suitable food for Mytilus trossulus. These studies indicate that detritus would be a poor food source for mussels. In the present study, detritus accounted for more than 50% of POM according to the results of RPB, indicating that mussels assimilate only half of the components of POM. Because the estimated carbon and nitrogen stable isotope ratio of POM contains a detritus fraction, the estimated contribution rate of benthic microalgae would be smaller.
In the present study, most of the phytoplankton taxa were pelagic or thytopelagic species that live in both pelagic and benthic environments at both Stations 1 and 2, and the key species were limited to Thalassiosira spp. and long horn pennates at both stations. Cell abundance ratio in species at Station 1 was considerably different from that at Station 2. This difference would be caused by transport from Liverpool Bay. Survey of pelagic phytoplankton taxa and estimation of the transport rate from Liverpool Bay, therefore, would be also necessary to confirm effects of Liverpool Bay in the future. Muschenheim and Newell (1992) indicated that the resuspended benthic diatoms in near bed layer (~5 cm) would act as an important food source of mussel because of the result of cell abundance. In the Menai Strait, resuspended benthic diatoms were also recognized in water column and act as an important food source. The comparison on horizontal and vertical difference of phytoplankton community would be able to provide more useful information of the food composition and supply for the mussel aquaculture.
In some cases, terrestrial organic matter affects bivalve food sources (Riera & Richard 1997, Kasai & Nakata 2005). In the present study, the carbon stable isotope ratio and C:N ratio of POM revealed that POM was less affected by terrestrial organic matter mainly composed of detritus of vascular plants. The small ratio of terrestrial organic matter in POM would result from limited river discharge in the Menai Strait. Simpson and Nunes (1981) reported that the freshwater inflow into the Menai Strait was approximately 500 x [10.sup.3] [m.sup.3], whereas the mass of seawater was greater than 80 x [10.sup.6] [m.sup.3] in the M2 tide. Mussels showed high carbon stable isotope ratio compared with terrestrial organic matter (< -25[per thousand]). Furthermore, previous stable isotopic studies (Dubois et al. 2007b) indicated low contribution of terrestrial organic matter. This study also confirmed that terrestrial organic matter would be negligible food source in the Menai Strait.
Ecological models could be one of the strong tools for quantitative assessment of the carrying capacity in marine ecosystem (McKindsey et al. 2006). Cugier et al. (2010) assessed the role of filter feeders for primary production in coastal bivalve aquaculture region using the ecological model. Newell and Richardson (2014) studied about the aquaculture hydrodynamics on food supply for mussel in raft aquaculture region using the hydrodynamic model collaborated with food consumption model. They revealed that mussel growth rate could be improved by design and position of raft for optimizing hydrodynamics for increasing food supply. These models could enhance more accurate calculation of the carrying capacity of mussels and more appropriate management of bivalve aquaculture in coastal ecosystems such as in the Menai Strait.
The authors thank J. H. Simpson for encouragement in the study and P. Williams, B. Brex for field and laboratory work in the School of Ocean Science, Bangor University, UK, T. Miyajima for performing mass-spectrometry in the Atmosphere and Ocean Research Institute, the University of Tokyo, and M. Miller for English correction with critical reading in Nihon University. This research was supported by Grant-in-Aid for Scientific Research (JSPS KAKENHI Grant Numbers JP18405030) and Bilateral Joint Research Project from the Japan Society for the Promotion of Science (JSPS).
Asmus, R. M. & H. Asmus. 1991. Mussel beds--limiting or promoting phytoplankton. J. Exp. Mar. Biol. Ecol. 148:215-232.
Banaru, D., M. Harmelin-Vivien, M. T. Gomoiu & T. M. Onciu. 2007. Influence of the Danube river inputs on C and N stable isotope ratios of the Romanian coastal waters and sediment (Black Sea). Mar. Pollut. Bull. 54:1385-1394.
Cugier, P., C. Struski, M. Blanchard. J. Mazurie, S. Pouvreau, F. Olivier & E. Thiebaut. 2010. Assessing the role of benthic filter feeders on phytoplankton production in a shellfish farming site: Mont Saint Michel Bay, France. J. Mar. Syst. 82:21-34.
Dame, R., N. Dankers, T. Prins. H. Jongsma & A. Smaal. 1991. The influence of mussel beds on nutrients in the western Wadden Sea and eastern Scheldt Estuaries. Estuaries 14:130-138.
De Niro, M. J. & S. Epstein. 1978. Influence of diet on distribution of carbon isotopes in animals. Geochim. Cosmochim. Ada 42:495-506.
Dubois, S., B. Jean-Louis, B. Bertrand & S. Lefebvre. 2007a. Isotope trophic-step fractionation of suspension-feeding species: implications for food partitioning in coastal ecosystems. J. Exp. Mar. Biol. Ecol. 351:121-128.
Dubois, S., F. Orvain, J. C. Marin-Leal. M. Ropert & S. Lefebvre. 2007b. Small-scale spatial variability of food partitioning between cultivated oysters and associated suspension-feeding species, as revealed by stable isotopes. Mar. Ecol. Prog. Ser. 336:151-160.
Duggins. D. O. & J. E. Eckman. 1997. Is kelp detritus a good food for suspension feeders? Effects of kelp species, age and secondary metabolites. Mar. Biol. 128:489-495.
Field, I. A. 1911. The food value of sea mussels. Bull. Bureau Fish. 29 1909:85-128.
Field, I. A. 1923. Biology and economic value of the sea mussel. Bull. U.S. Bur. Fish. 38 1921-1922:127-259.
Folch, J., M. Lees & G. H. S. Stanley. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226:497-509.
Fry, B. 2006. Stable isotope ecology. New York, NY: Springer.
Fry, B. & E. B. Sherr. 1984. Delta-C-13 measurements as indicators of carbon flow in marine and fresh-water ecosystems. Contrih. Mar. Sci. 27:13-47.
Hoch, M. P., R. A. Snyder, L. A. Cifuentes & R. B. Coffin. 1996. Stable isotope dynamics of nitrogen recycled during interactions among marine bacteria and protists. Mar. Ecol. Prog. Ser. 132:229-239.
JGOFS (Joint Global Ocean Flux Study). 1996. Protocols for the Joint Global Ocean Flux Study (JGOFS) core measurement. Report 19:119-122.
Kang, C. K., J. B. Kim, K. S. Lee, J. B. Kim, P. Y. Lee & J. S. Hong. 2003. Trophic importance of benthic microalgae to macrozoobenthos in coastal bay systems in Korea: dual stable C and N isotope analyses. Mar. Ecol. Prog. Ser. 259:79-92.
Kang. C. K., P. G. Sauriau, P. Richard & G. F. Blanchard. 1999. Food sources of the infaunal suspension-feeding bivalve Cerastoderma edule in a muddy sandflat of Marennes-Oleron Bay, as determined by analyses of carbon and nitrogen stable isotopes. Mar. Ecol. Prog. Ser. 187:147-158.
Kasai, A. & A. Nakata. 2005. Utilization of terrestrial organic matter by the bivalve Corhicula japonica estimated from stable isotope analysis. Fish. Sci. 71:151-158.
Kasai, A., H. Toyohara, A. Nakata, T. Miura & N. Azuma. 2006. Food sources for the bivalve Corbicula japonica in the foremost fishing lakes estimated from stable isotope analysis. Fish. Sci. 72:105-114.
Lefebvre, S., J. C. M. Leal, S. Dubois, F. Orvain, J. L. Blin, M. P. Bataill, A. Ourry & R. Galois. 2009. Seasonal dynamics of trophic relationships among co-occurring suspension-feeders in two shellfish culture dominated ecosystems. Estuar. Coast. Shelf Sci. 82:415-425.
Levinton, J. S., J. E. Ward & S. E. Shumway. 2002. Feeding responses of the bivalves Crassostrea gigas and Mytilus trossulus to chemical composition of fresh and aged kelp detritus. Mar. Biol. 141:367-376.
McCutchan, J. H., W. M. Lewis, C. Kendall & C. C. McGrath. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378-390.
McKindsey, C. W., H. Thetmeyer, T. Landry & W. Silvert. 2006. Review of recent carrying capacity models for bivalve culture and recommendations for research and management. Aquaculture 261:451-462.
Minagawa, M. & E. Wada. 1984. Stepwise enrichment of N-15 along food-chains - further evidence and the relation between delta-N-15 and animal age. Geochim. Cosmochim. Acta 48:1135-1140.
Mullin, M. M., G. H. Rau & R. W. Eppley. 1984. Stable nitrogen isotopes in zooplankton--some geographic and temporal variations in the North Pacific. Limnol. Oceanogr. 29:1267-1273.
Muschenheim. D. K. & C. R. Newell. 1992. Utilization of seston flux over a mussel bed. Mar. Ecol. Prog. Ser. 85:131-136.
Newell, C. R. & J. Richardson. 2014. The effects of ambient and aquaculture structure hydrodynamics on the food supply and demand of mussel rafts. J. Shellfish Res. 33:257-272.
Page. H. M. & D. M. Hubbard. 1987. Temporal and spatial patterns of growth in mussels Mytilus edulis on an offshore platform--relationships to water temperature and food availability. J. Exp. Mar. Biol. Ecol. 111:159-179.
Phillips, D. L. & J. W. Gregg. 2001. Uncertainty in source partitioning using stable isotopes. Oecologia 127:171-179.
Prins, T. C. & A. C. Smaal. 1994. The role of the blue mussel Mytilus edulis in the cycling of nutrients in the Oosterschelde Estuary (The Netherlands). Hydrobiologia 283:413-429.
Riera. P. 1998. Delta N-15 of organic matter sources and benthic invertebrates along an estuarine gradient in Marennes-Oleron Bay (France): implications for the study of trophic structure. Mar. Ecol. Prog. Ser. 166:143-150.
Riera, P. 2007. Trophic subsidies of Crassostrea gigas. Mytilus edulis and Crepidula fornicata in the Bay of Mont Saint Michel (France): a delta C-13 and delta N-15 investigation. Estuar. Coast. Shelf Sci. 72:33-41.
Riera, P. & P. Richard. 1996. Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine Bay of Marennes-Oleron. Estuar. Coast. Shelf Sci. 42:347-360.
Riera, P. & P. Richard. 1997. Temporal variation of [[delta].sup.13]C in particulate organic matter and oyster Crassostrea gigas in Marennes- Oleron Bay (France): effect of freshwater inflow. Mar. Ecol. Prog. Ser. 147:105-115.
Rippeth, T. P., E. Williams & J. H. Simpson. 2002. Reynolds stress and turbulent energy production in a tidal channel. J. Phys. Oceanogr. 32:1242-1251.
Rolff, C. 2000. Seasonal variation in delta C-13 and delta N-15 of size-fractionated plankton at a coastal station in the northern Baltic proper. Mar. Ecol. Prog. Ser. 203:47-65.
Rouillon, G. & E. Navarro. 2003. Differential utilization of species of phytoplankton by the mussel Mytilus edulis. Acta Oecologica. 24: S299-S305.
Rouillon, G., J. G. Rivas, N. Ochoa & E. Navarro. 2005. Phytoplankton composition of the stomach contents of the mussel Mytilus edulis L. from two populations: comparison with its food supply. J. Shellfish Res. 24:5-14.
Saurel, C., J. Gascoigne & M. J. Kaiser. 2004. The ecology of seed mussel beds literature review. ICES Document Appendix 1. FC1015, CSA 6506.
Saurel, C., J. C. Gascoigne, M. R. Palmer & M. J. Kaiser. 2007. In situ mussel feeding behaviour in relation to multiple environmental factors: regulation through food concentration and tidal conditions. Limnol. Oceanogr. 52:1919-1929.
Savoye, N., A. Aminot, P. Treguer, M. Fontugne, N. Naulet & R. Kerouel. 2003. Dynamics of particulate organic matter delta N-15 and delta C-13 during spring phytoplankton blooms in a macrotidal ecosystem (Bay of Seine, France). Mar. Ecol. Prog. Ser. 255:27-41.
Simpson, J. H., W. J. Gould & A. M. G. Forbe. 1971. Electromagnetic observations of water flow in the Menai Straits. Geophys. J. R. Astron. Soc. 24:245-253.
Simpson, J. H., B. Berx, J. Gascoigne & C. Saurel. 2007. The interaction of tidal advection, diffusion and mussel nitration in a tidal channel. J. Mar. Syst. 68:556-568.
Simpson, J. H. & R. A. Nunes. 1981. The tidal intrusion front-an estuarine convergence zone. Estuar. Coast. Shelf Sci. 13:257-266.
Souza, A. J. & A. E. Hill. 2006. Tidal dynamics in channels: single channels. J. Geophys. Res. Oceans 111:C09037.
Tweddle, J. F., J. H. Simpson & C. D. Janzen. 2005. Physical controls of food supply to benthic filter feeders in the Menai Strait, UK. Mar. Ecol. Prog. Ser. 289:79-88.
Vander Zanden, M. J. & J. B. Rasmussen. 2001. Variation in delta N-15 and delta C-13 trophic fractionation: implications for aquatic food web studies. Limnol. Oceanogr. 46:2061-2066.
Waite, L., J. Grant & J. Davidson. 2005. Bay-scale spatial growth variation of mussels Mytilus edulis in suspended culture, Prince Edward Island, Canada. Mar. Ecol. Prog. Ser. 297:157-167.
Ward, J. E., J. S. Levinton, S. E. Shumway & T. Cucci. 1998. Particle sorting in bivalves: in vivo determination of the pallial organs of selection, Mar. Bio. 131:283-292.
Widdows, J., N. D. Pope, M. D. Brinsley, J. Gascoigne & M. J. Kaiser. 2009. Influence of self-organised structures on near-bed hydrodynamics and sediment dynamics within a mussel (Mytilus edulis) bed in the Menai Strait. J. Exp. Mar. Biol. Ecol. 379:92-100.
Williams, P. 1981. Detritus utilization by Mytilus edulis. Estuar. Coast. Shelf Sci. 12:739-746.
Yokoyama, H. 2008. Food sources of consumers in temperate estuaries and coastal waters: achievements and potential problems of isotopic studies. Jap. J. Ecol. 58:23-36.
Yokoyama, H. & Y. Ishihi. 2007. Variation in food sources of the macrobenthos along a land-sea transect: a stable isotope study. Mar. Ecol. Prog. Ser. 346:127-141.
HIROSHI MORIOKA, (1,4) AKIHIDE KASAI, (2) YOICHI MIYAKE, (1) TAKASHI KITAGAWA (3) AND SHINGO KIMURA (1*)
(1) Graduate School of Frontier Sciences! Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiha 277-8564, Japan; (2) Facuty of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate, Hokkaido 041-8611, Japan;(3) Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiha 277-8564, Japan; (4) Japan Coast Guard, 2-1-3 Kasumigaseki, Chiyoda, Tokyo 100-8918, Japan
(*) Corresponding author. E-mail: email@example.com
TABLE 1. Relative cell abundance in the phytoplankton community in the Menai Strait. Cell abundance (%) Genus Habitat Station-1 Station-2 Asterionellopsis sp. Pelagic 0.2 0.8 Chaetoceros sp. Pelagic 3.1 5.4 Coscinodiscus sp. Pelagic 1.8 0.5 Dactyliosolen sp. Pelagic 8.8 5.5 Guinardia sp. Pelagic 6.0 1.2 Merosila sp. Pelagic 8.3 2.8 Rhizosolcnia spp. Pelagic 11.8 2.8 Skeletonema spp. Pelagic 4.1 4.8 Thalassiosira spp. Pelagic 12.3 61.1 Thalassionema sp. Pelagic 0.4 0.1 Bacillaria spp. Tychopelagic 0.2 0.2 Long horn pennates Tychopelagic 27.8 8.7 Pleurosigma sp. Tychopelagic 2.6 0.5 Other pennates Tychopelagic 10.1 3.4 Ceratium spp. Pelagic 1.3 1.1 Prorocentrum sp. Pelagic 0.8 1.1 The group of long horn pennates includes Nitzschia longissima and Ceratoneis closlerium. Thycopelagic species live in both pelagic and benthic environments. TABLE 2. Contribution of food sources (%) to mussel production in the Menai Strait. Station 1 Station 2 Station 3 Station 4 Pelagic phytoplankton 78 64 50 59 Benthic microalgae 22 36 50 41 Pelagic phytoplankton is represented by POM at Station 1 facing the outer ocean in this study.
|Printer friendly Cite/link Email Feedback|
|Author:||Morioka, Hiroshi; Kasai, Akihide; Miyake, Yoichi; Kitagawa, Takashi; Kimura, Shingo|
|Publication:||Journal of Shellfish Research|
|Date:||Dec 1, 2017|
|Previous Article:||CARBOHYDRATE-RICH DIETS MEET ENERGY DEMANDS OF GAMETOGENESIS IN HATCHERY-CONDITIONED MUSSELS (MODIOLUS CAPAX) AT INCREASING TEMPERATURES.|
|Next Article:||RELATIONSHIPS BETWEEN SHELL MORPHOLOGICAL TRAITS AND THE BYSSUS DIMENSIONS IN THE WINGED PEARL OYSTER PTERIA PENGUIN (RODING, 1798) CULTIVATED IN...|