Feeding behavior of the mussel Mytilus galloprovincialis (L.) in a Mediterranean estuary: A field study

Aquaculture 314 (2011) 236–243

Contents lists available at ScienceDirect

Aquaculture j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / a q u a - o n l i n e

Feeding behavior of the mussel Mytilus galloprovincialis (L.) in a Mediterranean estuary: A field study Eve Galimany a,d,⁎, Montserrat Ramón a,b,d, Irrintzi Ibarrola c a

ICM-CSIC, Psg. Marítim de la Barceloneta 37-49, Barcelona 08003, Spain IEO-Centre Oceanogràfic de les Balears, Moll de Ponent s/n, Palma 07015, Spain Dpto. Genética, Antropología Física y Fisiología Animal, Facultad de Ciencia y Tecnología, Universidad del País Vasco/Euskal Herriko Unibertsitatea, Bilbao 48080, Spain d Xarxa de Referència de Recerca i Desenvolupament en Aqüicultura de la Generalitat de Catalunya, XRAq, Spain b c

a r t i c l e

i n f o

Article history: Received 3 September 2010 Received in revised form 19 January 2011 Accepted 24 January 2011 Available online 31 January 2011 Keywords: Mussels Bivalve physiology In situ experiment Alfacs Bay Seston

a b s t r a c t The feeding behavior of the mussel Mytilus galloprovincialis was investigated in the field on top of a mussel raft in Alfacs Bay, NW Mediterranean Sea. The experiments were performed in November 2006 and February, April and July 2007 using a flow-through filter feeding device. Total particulate matter (TPM), particulate organic matter (POM) and particulate inorganic matter (PIM) were calculated for the bay water, as well as the feces and pseudofeces of the mussels. These were used with the biodeposition method to estimate several feeding-physiological parameters, such as the clearance rate (CR), rejection rate through pseudofeces production (RP), organic ingestion rate (OIR), absorption rate (AR) and absorption efficiency (AE). The results showed that the characteristics of available suspended matter for mussels in terms of particle concentration (TPM: mg/l) and organic content (f defined as POM/TPM) ranged 1.03–2.30 mg/l, and 0.48 to 0.73 respectively throughout the study period. This indicates a rather stable feeding environment of low concentrations of high organic content particles despite the wide range of temperatures recorded (from 10 to 26 °C). However, a characteristic of such a variation pattern of particle suspension (TPM and f) was that shortterm variations (in the course of days) covered the whole range of annual variation. Accordingly, physiological parameters characterizing both food acquisition and absorption in mussels were found to respond to shortterm variations in food regime. Pseudofeces production in mussels was low (less than 5% in most cases) and they tended to reduce their clearance rate instead of increasing their pseudofeces production in response to rising particle concentration. The absorption efficiency was positively related to the organic content of the seston particles. There was also a positive correlation between clearance rate and absorption efficiency. The reduction of clearance, ingestion and absorption rates obtained in July highlights a negative influence of high water temperatures upon feeding and digestive processes of mussels. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Mussels are filter feeding bivalves, ideal for aquaculture due to their wide distribution and adaptability. Mussels are harvested for human consumption worldwide (Figueiras et al., 2002; Mortensen et al., 2006) with production of the species Mytilus galloprovincialis and Mytilus edulis above 300,000 t per year (FAO, 2009), mostly cultured in Spain, the leading mussel producer in Europe (Pérez Camacho et al., 1991; Keldany, 2002). Mussels (M. galloprovincialis) on the Spanish Mediterranean coast are mainly cultured in the two Ebro Delta bays, Fangar and Alfacs, with an annual production of 3000 t per year (Ramón et al., 2005a). They are cultured in suspension on a total of 166 fixed rafts divided between the bays of Alfacs ⁎ Corresponding author at: Northeast Fisheries Science Center, National Marine Fisheries Service, NOAA, 212 Rogers Avenue, Milford, CT 06460, USA. Tel.: + 1 203 882 6588; fax: + 34 203 882 6570. E-mail address: [email protected] (E. Galimany). 0044-8486/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2011.01.035

(90 farms) and Fangar (76 farms). One raft is composed by rectangular wooden frames measuring 200 m × 15 m, from which 2 to 3 m long mussel ropes are suspended. Mussel growth follows a seasonal pattern in Fangar Bay, with higher rates from March to May and the lowest rates in winter. The growth and mortality of mussels cultured in the two bays are affected greatly by the high seawater temperatures reached during July and August, which lead to a cessation in growth and high mortalities of adults and juveniles (Ramón et al., 2005a). Areas that have bivalve cultures are characterized by high primary production that can sustain the grazing pressure of the bivalves. Facing the Mediterranean Sea, Thau Lagoon (SE France) has high primary production (Gasc, 1997), with particulate organic matter (POM) values ranging from 0.1 to 1.7 mg l− 1 (Gangnery et al., 2004). The study site, Alfacs Bay (NE Spain), has a chlorophyll a level that is one order of magnitude above the surrounding Mediterranean Sea (Delgado, 1987). POM values in the study site range from 1 to 3.4 mg l− 1 (Ramón et al., 2005b) higher than in the Galician Rías (NW Spain), the largest mussel

E. Galimany et al. / Aquaculture 314 (2011) 236–243

producer in Europe (Pérez Camacho et al., 1991; Keldany, 2002). In addition to the POM, food quality expressed as POM/TPM can have a significant influence on the growth of bivalves due to its positive effect on the food absorption efficiency (Bayne et al., 1987; Navarro et al., 1991; Urrutia et al., 1996). There is a high percentage of organic content in the water of both Ría de Arousa and Alfacs Bay, and values can reach up to 50–60% (Babarro et al., 2003; Ramón et al., 2005b). Different approaches have been used to study the feeding behavior of mussels. Foster-Smith (1975) calculated filtration rates from the particle removal rates from a fixed volume of suspension. For a better approach to natural conditions, other authors estimated clearance rates by monitoring the removal of suspended particles as water passed through mussels; therefore, the filtration rates could be calculated as the clearing of water particles from the environmental water (Riisgård, 1977; Bayne and Widdows, 1978; Widdows et al., 1979). Similarly, Yahel et al. (2005) based his filtration rates study on the simultaneous pair wise collection of the water inhaled and exhaled by some filter feeding invertebrates in situ by means of scuba diving. Nevertheless, this technique cannot be used in some environments due to, i.e. weather conditions. Therefore, there was need to design new devices which simulated real conditions in order to better understand the feeding behavior in the field. Smith and Wikfors (1998) developed an automated rearing chamber system for studies of shellfish feeding behavior, and Babarro et al. (2000) used a portable box raft experimental chamber to conduct experiments in situ on top of mussel rafts. Different portable filter feeding devices have been designed in order to better understand the feeding physiological parameters of mussels (Filgueira et al., 2006; Grizzle et al., 2006). Nowadays, there are different methods for measuring filtration rates in suspension feeding bivalves, each of which should be used according to the particular experimental conditions and taking into account their advantages and disadvantages (reviewed by Riisgård, 2001). Ecological and commercial information on the mussel M. galloprovincialis, one of the most important bivalve species in the Mediterranean Sea, is still needed in this area. Many studies have been conducted with M. edulis; however, the results may not be totally applicable to M. galloprovincialis. Studies have been performed with these species on the Atlantic side of their geographical distribution, but the Atlantic environmental conditions, especially the temperature regime, are quite different to the Mediterranean conditions. In this sense, there is a lack of physiological data that would help to predict the potential for mussel cultivation in the Mediterranean (Sarà and Pusceddu, 2008). The aim of the present study is to determine the main physiological parameters related to feeding behavior of the mussel M. galloprovincialis in a Mediterranean estuary where bivalve aquaculture takes place. For a more realistic approach the experiments were carried out in the field at four different periods of the year. These results will be useful to improve shellfish aquaculture management in Alfacs Bay. 2. Materials and methods 2.1. Experimental design and animals The filter feeding experiments were performed from November 2006 to July 2007 on top of a mussel raft in Alfacs Bay, NW Mediterranean Sea. Four filter feeding experiments, lasting 2 h each, were carried out per sampling period (i.e., November 2006, and February, April and July 2007), corresponding to 2 consecutive days in 2 consecutive weeks in each period, except for July, in which only 3 experiments were carried out. Each experiment was conducted with a different group of mussels of similar sizes; the mussel sizes in each sampling period corresponded to the growth cycle in the area. Mussels, M. galloprovincialis, were collected from a mussel aquaculture farming site in Alfacs Bay (Ebro Delta) the day before each experiment.

237

Twenty mussels per experiment were collected, and epiphytes and other encrusting organisms were removed from the shells. A little plastic hook and loop fastener was glued to one of the two shells of each individual. When the glue dried, mussels were hung back on the raft where the experiments were performed the following day. Acclimation was not necessary as the mussels were always submerged in the bay water. Fake mussels were made by collecting four of the twenty fresh mussels, taking out the flesh and gluing the shells back together to act as controls. 2.2. Flow-through devices Two portable filter feeding flow-through devices were designed to simulate in vivo conditions of mussel feeding (Fig. 1). One portable filter feeding device consisted in a common PVC tank (length 560 mm, width 300 mm, height 150 mm) that received bay water from an underwater pump hung from the mussel raft poles at 1 m depth. Laterally, the tank was provided with an extra flow exit tube. Aeration was added to mix the bay water in the common tank. Ten rubber tubes emerged from the lower part of the tank and each tube was connected to an individual PVC aquarium. The individual aquaria measured 45 × 180 × 60 mm (length× width× height). Each aquarium contained a single mussel except for two of the aquaria, which contained one fake mussel each and were used as controls. The mussels were positioned near the flow exit tube of the aquaria and attached to the bottom with a piece of plastic hook and loop fastener. The flow of bay water from the common tank to each aquarium was regulated through a manual valve and maintained at a constant rate of 12 l h− 1. This flux was determined by previous laboratory experiments and 12 l h− 1 showed a homogeneous distribution of particles between aquaria and no water recirculation occurred in any of the aquaria. 2.3. Characteristics of the bay water Bay water (1 l) from the tanks with fake mussels (acting as controls) was collected every 15 min. The feces and pseudofeces of each mussel were collected throughout the experiment with a pipette. All samples (water, feces and pseudofeces) were filtered separately through washed Whatman GF/C filters (25 mm Ø) and rinsed with ammonium formate. In the laboratory, filters with water samples were dried at 60 °C for 48 h and weighed to obtain the dry weight, which accounted for the total particulate matter (TPM). Afterwards, filters were ashed at 450 °C for 4 h before the final weighing to obtain the particulate inorganic matter (PIM). The particulate organic matter (POM) was calculated as the weight loss between TPM and PIM. The organic content of the bay water (f) was calculated as the average fraction between POM and TPM. 2.4. Physiological feeding parameters Mussels were placed in the individual chambers of the feedingdevices and allowed to rest to recover from any stress associated with handling. The individual chambers were cleaned before the beginning of the experiment. The feces and pseudofeces of each mussel were then collected separately with a pipette as soon as they were produced. During approximately 2 h we collected enough biodeposits to end the experiment. Feces and pseudofeces produced by each mussel (n= 16) were filtered individually and processed for organic and inorganic matter (as indicated for the water samples) in order to compute the total, organic and inorganic rates of egestion and rejection respectively. The physiological components of the absorptive balance (Table 1) were then calculated according to the biodeposition method (Iglesias et al., 1998). The ingestion rates of the total matter (TIR: mg/h) and organic matter (OIR: mg/h) were obtained as the difference between the filtration and rejection rates of either the total or organic matter. In order to quantify the preingestive selection of food through pseudofeces production, we expressed rejection as a percentage of

238

E. Galimany et al. / Aquaculture 314 (2011) 236–243

Mussel raft surface

3

2

2

aeration

3

aeration

4

4

5

5

7

control control

control control

7

6

6

1

Under water Fig. 1. Diagram of the two portable filter feeding devices. 1: underwater pump; 2: common PVC tanks; 3: common tank extra flow exit tube; 4: aeration; 5: rubber tubes; 6: aquarium extra flow exit tubes; 7: manual valves.

filtered matter. Finally, the organic content of ingested matter was calculated as OIR/TIR. It was necessary to estimate the gut transit time (GTT) to determine the minimum time for an organic particle to pass through the digestive tract of the mussel after ingestion. With this information the seston ingested can be compared with the corresponding biodeposits produced by the mussels in terms of TPM, PIM and POM. Therefore, the GTT was calculated before each experiment using a method adapted from Hawkins et al. (1996). Five mussels were placed individually in a beaker in a mixture of bay water and Tetraselmis suecica monoculture. The time that elapsed between the beginning of exposure and the deposition of green colored feces was considered to be the GTT (min). All parameters were standardized to 1 g of dried mussel flesh using the following equation:

2.5. Statistical analyses Data were checked for normality and variance homogeneity. A nonparametric test (Kolmogorov–Smirnov) was used to compare the results obtained for the TPM, POM, PIM and the organic content of the bay water (f) with the two filter feeding devices. The results for TPM, POM, PIM and the percentage of organic content of the bay water, gut transit time (GTT) and the in situ filter feeding parameters were compared between sampling periods using the Kruskal–Wallis one-way Analysis of Variance. The statistical software used was Statgraphics Plus (Manugistics, Inc., Rockville, MD, USA). Correlations were established between f and TPM and AE, between CR and TPM, and between AE and CR using non-linear regression models and the statistical software SPSS Statistic 17.0 (SPSS Inc, Chicago). 3. Results

b

Ys =Ye x ð1=We Þ

3.1. Bay water where, in the case of the physiological parameters, Ys is the standardized physiological rate, Ye is the experimentally determined rate, and We is the dry body mass measured for each mussel. We used a b value of 0.67, as commonly used in mussel feeding studies (Bayne et al., 1989, 1993; Jones et al., 1992; Hawkins et al., 1997). In the case of the GTT, Ys is the standardized GTT, Ye is the experimentally determined GTT, and We is the dry body mass measured for each mussel. We used a b value of 0.34, as determined by Hawkins et al. (1990).

TPM, POM, PIM and the organic content of seston (f) of the bay water showed no significant differences between the two flowthrough devices when all the samplings were analyzed together (p N 0.05). Nevertheless, when the two devices were compared for each sampling day and period of the study, TPM, POM and PIM showed significant differences for April and day 9 (the first sampling day of April) (p b 0.05). When data from day 9 were not considered in

Table 1 Physiological components of absorptive balance for mussels in Alfacs Bay. Parameter

Acronym

Units

Calculation

Clearance rate

CR

l h− 1

Filtration rate Rejection proportion Organic ingestion rate Absorption rate Absorption efficiency Selection efficiency

FR RP OIR AR AE SE

mg h− 1 % mg h− 1 mg 1h− 1 Fraction Fraction

(mg inorganic matter from both feces and pseudofeces per unit of time (mg h− 1))/(mg inorganic matter (PIM; mg l− 1) in bay water) CR × Total particulate matter (TPM:mg l− 1) in the bay water [(total rejection rate mg h− 1)/(total filtration rate (mg h− 1)] × 100 (CR × Particulate organic matter (mg l− 1) in the bay water) − (rejection rate of organic matter (mg h− 1)) OIR − (egestion rate of organic matter) AR/OIR 1 − [(organic fraction within pseudofeces)/(organic fraction within total particles available in bay water)]

E. Galimany et al. / Aquaculture 314 (2011) 236–243

239

the statistical analyses, the devices did not show any significant differences between days or sampling periods (p N 0.05). Therefore, day 9 was not taken into account in the study of mussel filter feeding parameters, as the devices were not comparable on that day for unknown reasons. Food characteristics varied within a narrow range in the 14 days considered in the present set of experiments: TPM ranged from 1.03 to 2.30 mg l− 1, POM from 0.67 to 1.36 mg l−1, PIM from 0.36 to 1.18 mg l−1 and f from 0.48 to 0.73 (Table 2). To analyze the variation in the gravimetric characteristics of the water we plotted the organic content (f) as a function of the total particulate matter (TPM) using all the measurements taken during the entire study period (Fig. 2); the following negative relationship was obtained (f = 0.827 (± 0.021) e−0.183 (± 0.014) x TPM; r² = 0.466) (p b 0.001). 3.2. Characteristics of the experimental mussels Average mussel shell length increased from 42.27 mm in November to 63.85 mm in July, with the highest growth rates between November and April. Nevertheless, growth in weight did not follow a similar increase due to a steady situation in April in comparison with February (Table 3), which was also reflected by the low condition index values in April. The longest GTT value recorded was 81 min and the shortest was 61 min, obtained in February and July respectively (Table 3). GTT values did not increase with mussel size or sampling period. 3.3. Feeding parameters Table 4 shows daily mean values of physiological measurements for a common standard sized (1 g) mussel throughout the study period. Short-term (day to day) variations were observed in the filtering and ingestion rates. For instance, whereas the total annual variation of the clearance rate ranged from a minimum of 0.86 l h− 1 (July) to a maximum of 4.83 l h− 1 (February), on two different days in November the CR ranged from 1.51 to 4.34 l h− 1. To analyze variations in feeding behavior of mussels in Alfacs Bay we plotted the daily means of CR as a function of TPM with all data (Fig. 3). The relationship fits to the following negative exponential equation: −0:722ðF0:188Þ x TPM

CR = 7:600 ðF2:513Þ e 2 r = 0:36; F = 14:710 ; pb0:01

;

This suggests that CR is negatively affected by increasing seston. Rejection of filtered matter (%RP) by mussels showed two different periods (Table 4): during November, February and April, rejection represents a low fraction (b 5% except for one day in November, and even no pseudofeces production was observed on two occasions), but

Fig. 2. Relationship between the organic content of seston (f) and total particulate matter (TPM) from the bay water during the different study periods (Nov: November 2006; Feb: February 2007; Apr: April 2007; Jul: July 2007). Exponential correlation shown in graph.

in July rejection percentages increased up to 13–16% of the filtration rate (p b 0.05). As a result of the variation in clearance and rejection rates, the ingestion rate of organic matter (OIR; Table 4) was found to vary less than the CR between experiments. Mean OIR of mussels ranged from 1.58 to 3.58 in November, from 1.60 to 3.33 in February, from 2.06 to 2.90 in April, and finally, from 0.94 to 2.48 in July. Daily mean values of absorption efficiency (AE) ranged from a minimum of 0.55 (July) to a maximum of 0.80 (February) and showed significant short-term variations; i.e., AE changed from 0.61 to 0.80 from the first to the fourth sampling day of February. Fig. 4 shows daily means of AE as a function of food organic content (f). For comparative purposes we have included plots of hyperbolic relationships for AE and f published for Galician raft mussels by Pérez Camacho et al. (2000), Figueiras et al. (2002) and Babarro et al. (2003). The figure shows that AE for Alfacs mussels rises with increasing f both in November and February within the range of values published for Galician mussels. However, AE in April and July followed a random pattern, and fell (with only one exception in April) to much lower values. CR decreased with increasing TPM (i.e. reduced f) and AE increased with f; therefore, there is a positive relationship between AE and CR. The relationship between daily mean values of AE and CR has been plotted in Fig. 5. As shown in the figure the two parameters are positively correlated and a simple linear regression indicates a high coefficient of determination (r2 = 0.605). The resulting food absorption rates (AR) are plotted as a function of available POM (Fig. 6). Within the narrow range of POM availability

Table 2 Mean values (± SE) of temperature (T) for each sampling period and of total particulate matter (TPM), particulate organic matter (POM), particulate inorganic matter (PIM) and quality of seston (f) of the bay water for each sampling day. T (°C)

Sampling day

TPM (mg l− 1)

POM (mg l− 1)

PIM (mg l− 1)

f (POM/TPM)

November 2006

18.1 ± 0.1

February 2007

10.5 ± 0.1

April 2007

16.7 ± 0.1

July 2007

25.9 ± 0.1

1 2 3 4 5 6 7 8 10 11 12 13 14 15

1.55 ± 0.04 1.41 ± 0.04 1.29 ± 0.04 2.05 ± 0.06 2.26 ± 0.04 1.52 ± 0.04 1.16 ± 0.04 1.03 ± 0.04 1.72 ± 0.04 1.98 ± 0.04 1.78 ± 0.04 2.30 ± 0.04 2.17 ± 0.04 1.51 ± 0.04

1.00 ± 0.02 0.86 ± 0.02 0.78 ± 0.02 1.14 ± 0.02 1.08 ± 0.02 0.90 ± 0.02 0.69 ± 0.02 0.67 ± 0.2 0.99 ± 0.02 1.27 ± 0.02 1.15 ± 0.02 1.32 ± 0.02 1.36 ± 0.02 1.11 ± 0.02

0.55 ± 0.02 0.55 ± 0.02 0.50 ± 0.02 0.91 ± 0.03 1.18 ± 0.02 0.62 ± 0.02 0.47 ± 0.02 0.36 ± 0.02 0.72 ± 0.02 0.71 ± 0.02 0.58 ± 0.02 1.00 ± 0.02 0.80 ± 0.02 0.40 ± 0.02

0.64 ± 0.01 0.60 ± 0.01 0.61 ± 0.01 0.56 ± 0.01 0.48 ± 0.01 0.60 ± 0.01 0.59 ± 0.01 0.65 ± 0.01 0.58 ± 0.01 0.64 ± 0.01 0.65 ± 0.01 0.57 ± 0.01 0.63 ± 0.01 0.73 ± 0.01

240

E. Galimany et al. / Aquaculture 314 (2011) 236–243

Table 3 Information of the experimental mussels: mean values (± SE) of shell length, dry weight, condition index (CI), number of individuals (N), gut transit time (GTT) and standardized GTT for each sampling period. Sampling period

Length (mm)

Dry weight (mg)

CI (DW/L)

N

GTT (min)

St GTT (min)

N

November 06 February 07 April 07 July 07

42.27 ± 4.02 50.85 ± 4.72 59.09 ± 4.99 63.85 ± 7.28

446.66 ± 134.95 804.04 ± 294.76 872.60 ± 266.36 1136.97 ± 490.56

10.43 ± 2.46 15.53 ± 4.69 14.57 ± 3.53 17.48 ± 6.26

52 56 41 44

73.75 ± 8.54 81.0 ± 18.38 67.33 ± 4.04 61.76 ± 2.89

93.46 ± 10.82 102.66 ± 23.30 85.34 ± 5.12 78.16 ± 3.66

20 20 20 20

encountered on the different sampling days (from ≈0.67 to 1.36) the absorption rates of mussels vary greatly. We have not attempted to perform any statistical fitting of the data, but AR seems to follow a unimodal distribution with a tendency to decrease with POM values above approximately 1.0 mg l− 1, which mainly occurred in April (2 occasions) and July (3 occasions). To compare possible significant differences between the physiological rates of the studied sampling periods we grouped the results from the different experiments of each period (Fig. 7). November and February showed no significant differences (p = 0.88) and had higher CR and AE values than those observed in April (p = 0.008). The April values were in turn higher than those recorded in July (p = 0.0001). Nevertheless, there were no significant differences between OIR and AR for November, February and April (p = 0.30), although July had lower values for these feeding rates (p = 0.0001). 4. Discussion The characteristics of the seston available for mussels (quantity and organic content) in Alfacs Bay recorded in the present experiments are similar to those previously obtained in the area (Ramón et al., 2005b). They indicate that the trophic conditions for the production of M. galloprovincialis in Alfacs Bay are similar to those encountered in the Galician Rías (Atlantic coast of Spain), which is the largest mussel production site in Europe (Navarro et al., 1991; Babarro et al., 2000, 2003). Briefly, these systems are characterized by i) low total particulate matter concentrations (TPM), which are below or on the limit of the pseudofeces threshold for mussels (above 5.0 mg l− 1 according to Widdows et al., 1979; Bayne and Worrall, 1980; Bayne et al., 1993); and ii) high organic content of the particle complex due to high proportions of phytoplankton cells. In detail, in Alfacs Bay, the development of phytoplankton blooms is frequent in the summer and fall, and the chlorophyll concentrations can vary from 1–3 to 10–25 mgm−3 during such blooms (Delgado, 1987). Our results indicate that the seston (f) is of high organic content with an average value of 0.62, even higher than mean f values reported for the Galician Rías (≈ 0.5; Figueiras et al., 2002; Babarro et al., 2000, 2003). Other mussel production sites on the Mediterranean coast,

such as Gaeta Gulf (Sicily), have different seston conditions, which classify them as meso-trophical waters with a higher mean TPM concentration (4.8 ± 3.9 mg l− 1) and lower average POM concentration (0.22 mg l− 1), giving average values of f around 0.05 (Mazzola et al., 1999; Sarà and Mazzola, 2004). However, two environmental aspects differentiate the Ebro Bays from the Galician Rías: whereas the latter have a rather constant water temperature (maximum seasonal variation of less than 3 °C in Ría de Arousa) (Babarro et al., 2000), in Alfacs Bay the water temperature has very high seasonal variation (from 10 to 26 °C from February to July in the present study, and from 6 to 30 °C reported for Fangar Bay by Ramón et al., 2007). Moreover, similar values of TPM and POM in several studies in the Galician Rías, particularly in Ría de Arousa (Cabanas et al., 1979; Navarro et al., 1991; Iglesias et al., 1996) suggest that these parameters have remarkable spatial and temporal constancy. However, the present study shows that short-term variation (between days) in Alfacs Bay might be as large as the variability found for the different seasonal periods. This could be due to silt resuspension events driven by wind action and shallow depth (5 m maximum in Alfacs Bay), as reported in other estuarine ecosystems, which would tend to diminish organic content of particles in the water column (Hawkins et al., 1996; Velasco and Navarro, 2005). The present experiments highlight three main components in the feeding behavior of mussels in Alfacs Bay: 1) consistently with both low TPM and high f values, production of pseudofeces in mussels was a minor component (less than 10% of FR) of the feeding behavior (except in July); 2) the clearance rate and food absorption efficiency were found to change significantly in the short-term; and 3) a significant reduction in AR was recorded in July coinciding with the highest TPM values and the highest water temperatures (above 26 °C). Previous estimations of mussel CR performed in two Mediterranean areas gave values of 2.2±1.2 lh− 1 (Gulf of Gaeta) and 3.2±1.2 lh− 1 (Gulf of Castellammare) (Sarà and Mazzola, 2004), which are in the range of the CR values estimated in our study (0.86 to 4.83 lh− 1). However, rather than absolute values, it is the response of feeding rates to environmental variations the feature that allows comparison of results

Table 4 Mean values (± SE) of clearance rate (CR), filtration rate (FR), rejection proportion (RP), selection efficiency (SE), organic ingestion rate (OIR), absorption rate (AR) and absorption efficiency (AE) for each sampling day. — means lack of pseudefeces production.

November 2006

February 2007

April 2007

July 2007

Sampling day

CR (l h− 1)

FR (mg h− 1)

RP (%)

SE

OIR (mg h− 1)

AR (mg h− 1)

AE

1 2 3 4 5 6 7 8 10 11 12 13 14 15

2.99 ± 0.37 4.34 ± 0.39 3.21 ± 0.39 1.51 ± 0.85 3.17 ± 0.46 3.17 ± 0.38 2.31 ± 0.37 4.83 ± 0.41 2.93 ± 0.40 1.86 ± 0.41 1.97 ± 0.41 2.05 ± 0.36 0.86 ± 0.40 0.97 ± 0.38

4.54 ± 0.57 6.11 ± 0.64 4.12 ± 0.64 3.07 ± 1.39 7.24 ± 0.76 4.56 ± 0.62 2.68 ± 0.60 4.99 ± 0.67 4.96 ± 0.63 3.67 ± 0.69 3.26 ± 0.67 4.66 ± 0.60 1.88 ± 0.67 1.45 ± 0.64

2.92 ± 2.36 4.51 ± 2.44 1.38 ± 2.36 9.70 ± 5.27 4.23 ± 2.89 1.27 ± 2.36 — 0.22 ± 2.53 — 5.78 ± 2.30 2.73 ± 2.53 4.09 ± 1.99 13.85 ± 2.53 16.08 ± 2.71

0.22 ± 0.18 0.72 ± 0.10 0.88 ± 0.10 0.75 ± 0.23 0.77 ± 0.13 0.83 ± 0.10 — 0.57 ± 0.11 — 0.70 ± 0.11 0.73 ± 0.11 0.61 ± 0.10 0.54 ± 0.11 0.59 ± 0.11

2.86 ± 0.32 3.58 ± 0.34 2.47 ± 0.34 1.58 ± 0.73 3.33 ± 0.43 2.75 ± 0.35 1.60 ± 0.32 3.11 ± 0.38 2.90 ± 0.35 2.16 ± 0.37 2.06 ± 0.38 2.48 ± 0.32 1.03 ± 0.36 0.94 ± 0.34

2.25 ± 0.26 2.65 ± 0.29 1.70 ±0.29 1.03 ± 0.63 2.18 ± 0.34 2.08 ± 0.28 1.09 ± 0.27 2.50 ± 0.30 2.13 ± 0.29 1.34 ± 0.31 1.38 ± 0.30 1.48 ± 0.27 0.61 ± 0.29 0.64 ± 0.28

0.75 ± 0.02 0.73 ± 0.02 0.67 ± 0.02 0.62 ± 0.05 0.61 ± 0.03 0.73 ± 0.02 0.65 ± 0.02 0.80 ± 0.02 0.72 ± 0.02 0.56 ± 0.02 0.65 ± 0.02 0.58 ± 0.02 0.55 ± 0.02 0.65 ± 0.02

E. Galimany et al. / Aquaculture 314 (2011) 236–243

Nov

Feb

Apr

Nov

Jul

Apr

Feb

Jul

6

6 5

5

4

4

CR (l h-1)

CR (l h-1)

241

3 2 1

3 2 1

0 0.5

1

1.5

2

2.5

TPM (mg l-1)

0 0.5

Fig. 3. Relationship between the clearance rate (CR) and total particulate matter (TPM) from the bay water during the different study periods (Nov: November 2006; Feb: February 2007; Apr: April 2007; Jul: July 2007).

between populations. In a recent in situ study, MacDonald and Ward (2009) recorded the variation of CR in mussels (M. edulis) and scallops (Placopecten magellanicus) over a 12 h time period (full tidal cycle) in two sites on the Canadian coast. As reported by these authors for M. edulis, M. galloprovincialis from Alfacs Bay has been shown to change its CR by a factor of 2 or 3 from one day to the following sampling day, although in the present study the significant negative relationship between CR and TPM suggests the opposite dependency to that shown by M. edulis between these variables. It is likely that rather than inter-specific differences, the above discrepancy could be the consequence of large differences in the seston concentration (above and below the pseudofeces threshold for Canadian and Mediterranean mussels respectively). Mussels have been reported to have broad physiological plasticity that allows different feeding responses to changes imposed by shortterm variations in the trophic environment. With low organic contents, mussels tend to increase filtration and pseudofeces production in response to the increased TPM. This allows a relatively constant ingestion rate to be maintained while the organic content of the ingested matter is enriched through preingestive selection of organic particles, thus promoting the optimal conditions for increasing net absorption efficiency (Widdows et al., 1979; Newell and Shumway, 1993; Bayne et al., 1993; Hawkins et al., 1996, 1998). However, under different environmental conditions such as those encountered in Galician Rías and Alfacs Bay, which are characterized by low seston

Nov

Feb

Jul

Apr

A

B

0.6

0.7

0.8

0.9

AE Fig. 5. Relationship between the clearance rate (CR) and the absorption efficiency (AE) during the different study periods (Nov: November 2006; Feb: February 2007; Apr: April 2007; Jul: July 2007).

loads of high organic content, mussels have found to behave in a different manner. For instance, Navarro et al. (1991) reported that M. galloprovincialis cultivated in outer rafts of Ría de Arosa had significantly higher clearance rates (35 to 90% higher) than those mussels on inner rafts that were exposed to higher values of TPM of a same organic content. Furthermore, they also found that mussels at the front of the rafts, where particle organic content was higher, had significantly higher clearance rates than those growing at the back of the rafts. In situ determinations of mussel feeding activity on the rafts by Pérez Camacho et al. (2000) showed that clearance rates varied from 3.6 to 6.9 l h− 1 (for small and medium sized mussels respectively) to 2.2 to 4.0 l/h, when food characteristics changed from TPM = 0.568 and f = 69% to TPM = 1.007 and f = 33%. These findings suggest that in systems characterized by low seston loads, the changes in seston organic content promote regulatory adjustments of the clearance rate in mussels. A similar conclusion might be inferred from results reported by Gardner (2002) for M. galloprovincialis from New Zealand, who reported that the CR was more positively correlated with f than with any other environmental parameter. Such an active feeding response could have beneficial effects on the absorptive processes. On one hand, maintenance (or increase) of CR in response to increasing food concentration within TPM values below pseudofeces threshold, would lead to increasing ingestion rates, but the benefits in terms of absorption rate could be negatively affected by reduction in gut passage time promoting

C

0.9

Nov

Feb

Apr

Jul

3.5 3

AR (mg h-1)

AE

0.8

0.7

0.6

2.5 2 1.5 1 0.5

0.5 0.5

0.55

0.6

0.65

0.7

0.75

0.8

f

0 0.5

0.7

0.9

1.1

1.3

1.5

POM (mg l-1) Fig. 4. Absorption efficiency (AE) related to the food organic content (f). The relationship between AE and f for Galician mussels has been plotted on the graph for comparative purposes. Data obtained by A: Perez Camacho et al. (2000); B: Figueiras et al. (2002); C: Babarro et al. (2000).

Fig. 6. Relationship between the absorption rate (AR) and particulate organic matter (POM) from the bay water during the different study periods (Nov: November 2006; Feb: February 2007; Apr: April 2007; Jul: July 2007).

242

E. Galimany et al. / Aquaculture 314 (2011) 236–243

4

4

A

B 3

OIR (mg h-1)

CR (L h -1)

3

2

1

2

1

0

0 Nov

Feb

Apr

Jul

Nov

2.5

Feb

Apr

Jul

0.8

C

D 0.6

1.5

AE

AR (mg h-1)

2.0

0.4

1.0 0.2

0.5 0.0

0.0 Nov

Feb

Apr

Jul

Nov

Feb

Apr

Jul

Fig. 7. Mean values for each sampling period (Nov: November 2006; Feb: February 2007; Apr: April 2007; Jul: July 2007) of the following feeding parameters: A. clearance rate (CR); B. organic ingestion rate (OIR); C. absorption rate (AR); D. absorption efficiency (AE). SE shown in bars.

lower absorption efficiencies (Bayne et al., 1989; Navarro et al., 1992, 1994). On the other hand, absorption efficiency would be maximized with high food organic content. Under natural feeding conditions, AE in mussels is a positive exponential function of the ingested organic content (Pérez Camacho et al., 2000; Figueiras et al., 2002; Babarro et al., 2003; Hawkins et al., 1996; 1998). The positive relationship found in Alfacs Bay between AE and CR suggests that the clearance rate is maximized under conditions that allow optimal absorption of food. Interestingly, Navarro et al. (1996) found a similar positive relationship between AE and CR for Galician raft mussels fed on a combination of experimental diets elaborated by mixing different proportions of bottom sediments with phytoplankton. Furthermore, Gardner (2002) found a similar relationship for M. galloprovincialis from New Zealand submitted to natural variations of TPM and f. In addition to the short-term fluctuations of TPM and f, other factors such as water temperature and phytoplankton composition might have also affected the feeding behavior of mussels recorded in the present study. In July, under maximal annual temperatures, in addition to low clearance rates that might be partially explain by relatively high TPM values, both an increase in the food rejection rates (N10% of FR) and a significant reduction in AE, contributed to reduce the energy intake in mussels. These results deserve special attention and may be explain due to two factors that occurred in July: a) the presence of a large proportion of the diatom Cyclotella meneghiniana (up to 60% of living phytoplankton, Galimany et al., unpublished data) and, b) the rising of the water temperature up to extremely high values (26 °C). Regarding a possible negative effect of phytoplanktonic blooms, Prins and Smaal (1994) reported that M. edulis from the Wadden Sea reduced clearance rates during April–June coinciding with a bloom of an haptophycean microalgae (Phaeocystis sp.). The possibility that C. meneghiniana could limit food ingestion and absorption in mussels from Alfacs is a question that should be investigated. Currently, however, there is no published information on possible adverse effects of C. meneghiniana on bivalves. On the contrary, a negative thermal effect on mussel physiology seems to be a

more probable explanation for the results found in this study during July. Anestis et al. (2010) have recently demonstrated that the clearance rate of M. galloprovincialis from the Thermaikos Gulf is reduced at temperatures over 24 °C (very severely at 28 °C), thus leading to a significant decline in the energy balance. The reduction in the aerobic scope for activity and the onset of an anaerobic metabolism (Anestis et al., 2010) drastically reduce the capacity of mussels to filter and absorb available food. The present findings correlate with the growth pattern of farmed mussels in Alfacs Bay which is characterized by two larger growth periods (from October to January and from April to May), a smaller growth rate period (from January to April) and no growth from June to August. The lack of growth in weight recorded in April (but not in size), related to the decrease in the condition index in the present study, could be due to the mussel spawning period, as previous studies have indicated a mussel spawning period at this site during April (Galimany et al., 2005). The increase in weight observed from April to July could have occurred at the beginning of the period (April and May), before the water temperature reached values above 25 °C. During summer, when the end of the cycle culture occurs, the high water temperature can negatively influence the mussels in Alfacs Bay. The present study demonstrates that during this period of the year the mussels decrease their feeding ingestion and absorption rates and efficiencies. In accordance with this, Anestis et al. (2010) determined a decrease in the scope for growth above 24 °C. Mussels exposed to such high water temperatures are not able to use food acquisition to compensate for the energetic demand related to the high temperatures, which would explain the high mortality rates recorded during summer in Alfacs Bay (Ramón et al., 2007). In conclusion, the present experiments demonstrate that mussels in Alfacs Bay actively respond to short-term changes in the food characteristics obtaining energetic intakes that promote comparable growth rates and productivity to those in Galician estuaries during most of the year (Ramón et al., 2007). However, high water temperatures during summer might severely limit the productivity of the site as they lead to reduced clearance rate and absorption efficiency.

E. Galimany et al. / Aquaculture 314 (2011) 236–243

Acknowledgements This study has been partially financed by the RTA04-023 INIA research project and the Centre de Referència en Aqüicultura of the Generalitat de Catalunya. The first author was supported by a grant co-financed by the Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) and the Institut de Recerca i Tecnologia Agroalimentaria (IRTA). We would like to thank Xavier Mas, Xavier Leal and David Pina from ICM-CSIC for their advice and help during the construction of the flow-through devices. We would also like to acknowledge J. M. Reverté, Vanesa Castán and Esther Dámaso for their help during the field work. References Anestis, A., Pörtner, H.O., Karagiannis, D., Angelidis, P., Staikou, A., Michaelidis, B., 2010. Response of Mytilus galloprovincialis (L.) to increasing seawater temperature and to marteliosis: metabolic and physiological parameters. Comp. Biochem. Physiol. A 156, 57–66. Babarro, J.M.F., Fernández-Reiriz, M.J., Labarta, U., 2000. Feeding behavior of seed mussel Mytilus galloprovincialis: environmental parameters and seed origin. J. Shellfish Res. 19, 195–201. Babarro, J.M.F., Fernández-Reiriz, M.J., Labarta, U., 2003. In situ absorption efficiency processes for the cultured mussel Mytilus galloprovincialis in Ría de Arousa (north–west Spain). J. Mar. Biol. Ass. UK 83, 1059–1064. Bayne, B.L., Widdows, J., 1978. The physiological ecology of two populations of Mytilus edulis L. Oecologia 37, 137–162. Bayne, B.L., Worrall, C.M., 1980. Growth and production of mussels Mytilus edulis from two populations. Mar. Ecol. Prog. Ser. 3, 313–328. Bayne, B.L., Hawkins, A.J.S., Navarro, E., 1987. Feeding and digestion by the mussel Mytilus edulis L. (Bivalvia: Mollusca) in mixtures of silt and algal cells at low concentration. J. Exp. Mar. Biol. Ecol. 111, 1–22. Bayne, B.L., Hawkins, A.J.S., Navarro, E., Iglesias, J.I.P., 1989. Effects of seston concentration on feeding, digestion and growth in the mussel, Mytilus edulis. Mar. Ecol. Prog. Ser. 55, 47–54. Bayne, B.L., Iglesias, J.I.P., Hawkins, A.J.S., Navarro, E., Heral, M., Deslous Paoli, J.M., 1993. Feeding behaviour of the mussel, Mytilus edulis: responses to variations in quantity and organic content of the seston. J. Mar. Biol. Ass. UK 73, 813–829. Cabanas, J.M., González, J.J., Mariño, J., Pérez Camacho, A., Román, G., 1979. Estudio del mejillón y de su epifauna en los cultivos flotantes de la Ría de Arosa III. Observaciones previas retención partículas biodeposición una batea. Bol. Inst. Esp. Oceanogr. 5, 45–50. Delgado, M., 1987. Fitoplancton de las bahías del delta del Ebro. Inv. Pesq. 51, 517–548. FAO, 2009. Food and Agriculture Organization of the United Nations. In: FAO (Ed.), http://www.fao.org/. Figueiras, F.J., Labarta, U., Fernández-Reiriz, M.J., 2002. Coastal upwelling, primary production and mussel growth in the Rías Baixas of Galicia. Hydrobiologia 484, 121–131. Filgueira, R., Labarta, U., Fernández-Reiriz, M.J., 2006. Flow-through chamber method for clearance rate measurements in bivalves: design and validation of individual chambers and mesocosm. Limnol. Oceanogr. Methods 4, 284–292. Foster-Smith, R.L., 1975. The effect of concentration of suspension on the filtration rates and pseudofaecal production for Mytilus edulis L., Cerastoderma edule (L.) and Venerupis pullastra (Montagu). J. Exp. Mar. Biol. Ecol. 17, 1–22. Galimany, E., Ramón, M., Durfort, M., 2005. Desarrollo gonadal del mejillón Mytilus galloprovincialis de la bahía de Alfacs (Delta del Ebro). X Congreso Nacional de Acuicultura, Gandía, Spain. pp. 616–617. Gangnery, A., Bacher, C., Buestel, D., 2004. Application of a population dynamics model to the Mediterranean mussel, Mytilus galloprovincialis, reared in Thau Lagoon (France). Aquaculture 229, 289–313. Gardner, J.P.A., 2002. Effects of seston variability on the clearance rate and absorption efficiency of the mussels Aulacomya maoriana, Mytilus galloprovincialis and Perna canaliculus from New Zealand. J. Exp. Mar. Biol. Ecol. 268, 83–101. Gasc, A., 1997. Study of regenerated primary production in a mollusc culture ecosystem: the Thau lagoon, Thesis, University of Montpellier (France), 216 pp. (in French). Grizzle, R.E., Greene, J.K., Luckenbach, M.W., Coen, L.D., 2006. A new in situ method for measuring seston uptake by suspension-feeding bivalve molluscs. J. Shellfish Res. 25, 643–649. Hawkins, A.J.S., Navarro, E., Iglesias, J.I.P., 1990. Comparative allometries of gut-passage time, gut content and metabolic faecal loss in Mytilus edulis and Cerastoderma edule. Mar. Biol. 105, 197–204. Hawkins, A.J.S., Smith, R.F.M., Bayne, B.L., Héral, M., 1996. Novel observations underlying the fast growth of suspension-feeding shellfish in turbid environments: Mytilus edulis. Mar. Ecol. Prog. Ser. 131, 179–190.

243

Hawkins, A.J.S., Smith, R.F.M., Bougrier, S., Bayne, B.L., Héral, M., 1997. Manipulation of dietary conditions for maximal growth in mussels, Mytilus edulis L., from the Marennes-Oléron, France. AquatLiving Res 10, 13–22. Hawkins, A.J.S., Bayne, B.L., Bougrier, S., Héral, M., Iglesias, J.I.P., Navarro, E., Smith, R.F.M., Urrutia, M.B., 1998. Some general relationships in comparing the feeding physiology of suspension-feeding bivalve molluscs. J. Exp. Mar. Biol. Ecol. 219, 87–103. Iglesias, J.I.P., Pérez Camacho, A., Navarro, E., Labarta, U., Beiras, R., Hawkins, A.J.S., Widdows, J., 1996. Microgeographic variability in feeding, absorption, and condition of mussels (Mytilus galloprovincialis Lmk.): a transplant experiment. J. Shellfish Res 15, 673–680. Iglesias, J.I.P., Urrutia, M.B., Ibarrola, I., 1998. Measuring feeding and absorption in suspension-feeding bivalves: an appraisal of the biodeposition method. J. Exp. Mar. Biol. Ecol. 219, 71–86. Jones, H.D., Richards, O.G., Southern, T.A., 1992. Gill dimensions, water pumping rate and body size in the mussel Mytilus edulis L. J. Exp. Mar. Biol. Ecol. 155, 213–237. Keldany, B., 2002. Overview of the Galician mussel industry. Bull. Aquacult. Assoc. Can. 102, 58–65. MacDonald, B.A., Ward, J.E., 2009. Feeding activity of scallops and mussels measured simultaneously in the field: repeated measures sampling and implications for modelling. J. Exp. Mar. Biol. Ecol. 371, 42–50. Mazzola, A., Rosa, T.L., Savona, B., Sarà, G., 1999. Seston dynamics and food availability in a mussel system (Gulf of Gaeta, southern Tyrrhenian Sea, Italy). J. Shellfish Res. 18, 331. Mortensen, S., Duinker, A., Strand, Ø., Andersen, S., 2006. Production of bivalves. Fisken Havet Saernummer 2, 156–159. Navarro, E., Iglesias, J.I.P., Pérez Camacho, A., Labarta, U., Beiras, R., 1991. The physiological energetics of mussels (Mytilus galloprovincialis Lmk) from different cultivation rafts in the Ria de Arosa (Galicia, N. W. Spain). Aquaculture 94, 197–212. Navarro, E., Iglesias, J.I.P., Ortega, M.M., 1992. Natural sediment as a food source for the cockle Cerastoderma edule (L) effect of variable particle concentration on feeding digestion and scope for growth. J. Exp. Mar. Biol. Ecol. 156, 69–87. Navarro, E., Iglesias, J.I.P., Ortega, M.M., Larretxea, X., 1994. The basis for a functional response to variable food quantity and quality in cockles Cerastoderma edule (Bivalvia, Cardiidae). Physiol. Zool. 67, 468–498. Navarro, E., Iglesias, J.I.P., Pérez Camacho, A., Labarta, U., 1996. The effect of diets of phytoplankton and suspended bottom material on feeding and absorption of raft mussels (Mytilus galloprovincialis Lmk). J. Exp. Mar. Biol. Ecol. 198, 175–189. Newell, R.C., Shumway, S.E., 1993. Grazing of natural particulates by bivalve molluscs: a spatial and temporal perspective. In: Dame, R.F. (Ed.), Bivalve filter feeders in estuarine and coastal ecosystem processes. Springer-Verlag, Berlin, pp. 85–148. Pérez Camacho, A., González, R., Fuentes, J., 1991. Mussel culture in Galicia (NW Spain). Aquaculture 94, 263–278. Pérez Camacho, A., Labarta, U., Navarro, E., 2000. Energy balance of mussels Mytilus galloprovincialis: the effect of length and age. Mar. Ecol. Prog. Ser. 199, 149–158. Prins, T.C., Smaal, A.C., 1994. The role of the blue mussel Mytilus edulis in the cycling of nutrients in the Oosterschelde estuary (The Netherlands). Hydrobiologia 413, 413–429. Ramón, M., Cano, J., Peña, J.B., Campos, M.J., 2005a. Current status and perspectives of mollusk (bivalves and gastropods) culture in the Spanish Mediterranean. Bol. Inst. Esp. Oceanogr. 21, 361–373. Ramón, M., Fernández, M., Galimany, E., 2005b. Mussel (Mytilus galloprovincialis) culture in the Ebro Delta bays (NE Spain), IV International Congress of the European Malacological Societies, Abstracts book 31. Napoli, Italy. Ramón, M., Fernández, M., Galimany, E., 2007. Development of mussel (Mytilus galloprovincialis) seed from two different origins in a semi-enclosed Mediterranean Bay (N.E. Spain). Aquaculture 264, 148–159. Riisgård, H.U., 1977. On measurements of the filtration rates of suspension feeding bivalves in a flow system. Ophelia 16, 167–173. Riisgård, H.U., 2001. On measurements of filtration rates in bivalves—the stony road to reliable data: review and interpretation. Mar. Ecol. Prog. Ser. 211, 275–291. Sarà, G., Pusceddu, A., 2008. Scope for growth of Mytilus galloprovincialis (Lmk., 1819) in oligotrophic coastal waters (Southern Tyrrhenian Sea, Italy). Mar. Biol. 156, 117–126. Sarà, G., Mazzola, A., 2004. The carrying capacity for Mediterranean bivalve suspension feeders: evidence from analysis of food availability and hydrodynamics and their integration into a local model. Ecol. Mod. 179, 281–296. Smith, B.C., Wikfors, G.H., 1998. An automated rearing chamber system for studies of shellfish feeding. Aquacult. Eng. 17, 69–77. Urrutia, M.B., Iglesias, J.I.P., Navarro, E., Prou, J., 1996. Feeding and absorption in Cerastoderma edule under environmental conditions in the bay of Marennes-Oleron (Western France). J. Mar. Biol. Ass. UK 76, 431–450. Velasco, L.A., Navarro, J.M., 2005. Feeding physiology of two bivalves under laboratory and field conditions in response to variable food concentrations. Mar. Ecol. Prog. Ser. 291, 115–124. Widdows, J., Fieth, P., Worrall, C.M., 1979. Relationships between seston, available food and feeding activity in the common mussel Mytilus edulis. Mar. Biol. 50, 195–207. Yahel, G., Marie, D., Genin, A., 2005. InEx—a direct in situ method to measure filtration rates, nutritition, and metabolism of active suspension feeders. Limnol. Oceanogr. Meth. 3, 46–58.