Hydrobiologia 475/476: 505–511, 2002. E. Orive, M. Elliott & V.N. de Jonge (eds), Nutrients and Eutrophication in Estuaries and Coastal Waters. 505 © 2002 Kluwer Academic Publishers. Printed in the Netherlands.

Physiological response of subtruncata (da Costa, 1778) to different seston quantity and quality

Jose L. Rueda∗ & Aad C. Smaal Netherlands Institute for Fisheries Research (RIVO). P.O. Box 77, 4400 AB Yerseke, The Netherlands ∗Present address: Marine and Estuarine Ecology Unit, Department of Zoology and Entomology, University of Queensland, St. Lucia, Qld 4072, Australia E-mail: [email protected]

Key words: bivalve, feeding behaviour, filtration, ingestion, regulation

Abstract Individuals of the bivalve Spisula subtruncata were fed a mixed diet comprising of sea water enriched with the diatom Phaeodactylum tricornutum and ashed silt within a range of concentrations, simulating natural conditions above pseudofaeces threshold. The designed ranges for total particulate matter were between 10 and 30 mg l−1and organic content of seston 15–40%. Filtration rate, rejection rate, ingestion rate and absorption rate were measured at those different conditions. Filtration rate and rejection rate were significantly correlated to total particulate matter and percentage of organic matter, with higher rates at higher values of total particulate matter and lower values of percentage organic matter. Ingestion rate was maintained at similar levels in all the treatments and organic enrichment of the ingested food occurred due to preingestive selection of the filtered material. A differential absorption rate occurred at different levels of organic matter in the diet with high rates at high values of the organic content of the diet. S. subtruncata showed different physiological responses to changes of the food conditions: (1) Increase of pseudofaeces production at increasing levels of particulate matter, (2) preingestive selection of organic material which enriched the organic fraction of ingested food, (3) stabilized ingestion rate and (4) increase of the absorption rate at high organic levels of the seston.

Introduction ditions, season or location within the coast. The effects of the variability of suspended particles in the water Spisula subtruncata (da Costa, 1778) is a common column has never been studied up to date in S. sub- bivalve which lives in coastal areas of Europe with truncata, but it has been described for other bivalve a distribution from Norway to the Mediterranean and species both in temperate (Bayne et al., 1989; Iglesias the Atlantic coast of Morocco (Tebble, 1966). The et al., 1996; Navarro & Widdows, 1997) and tropical habitat of this species in the North Sea (sandy bot- waters (Yukihira et al., 1999; Wong & Cheung, 1999). toms between 2 and 30 m) represents an environment There is a controversy about the effects of the where the concentration of suspended particulate mat- quantity and quality of seston in the feeding processes ter (seston) may be variable in time as a result of of bivalves. Jørgensen (1990, 1996) have suggested resuspension of fine sediments during periods of high that responses to environmental changes are determ- current velocity, wind-wave activity and storm events, ined solely by the physical properties of the cilliary especially in the shallow bottoms. For example, in the mechanisms of pumping and filtration. On the other Dutch coastal area, seston concentrations in the wa- hand, several authors (Bayne et al., 1989, 1993; Ig- ter column can vary between 2 and 150 mg l−1, with lesias et al., 1992, 1998; Navarro et al., 1996; Navarro values between 5 and 10 mg l−1 being most frequent & Widdows, 1997; Hawkins et al., 1998; Yukihira et (RIKZ, 1999). Between 5 and 40% of this seston may al., 1999; Wong & Cheung, 1999; Pouvreau et al., be organic in nature, with Chlorophyll concentrations 2000) have observed bivalve filter feeding resulting in between 0 and 11 µgl−1, depending on weather con- relative constancy of rates of absorption and ingestion. 506

Table 1. Number (N), shell length (SL: mm) and ash free dry weight (AFDW: mg) of the used in the different experiments (Exp) at different levels of total particulate − matter (TPM: mg.l 1) and percentage of organic matter (%OM). Date (year/month/day). Mean value ± standard deviation

Exp Date TPM %OM N SL AFDW

1 990804 12.59 ± 0.67 16.21 ± 1.33 7 25.4 ± 1.5 130.0 ± 19.7 2 990805 11.49 ± 0.41 26.41 ± 2.05 7 25.3 ± 1.1 118.6 ± 15.4 3 990802 10.66 ± 1.76 35.71 ± 1.65 7 25.3 ± 1.4 114.3 ± 16.0 4 990720 22.44 ± 0.95 17.53 ± 2.07 7 24.5 ± 1.2 103.6 ± 9.8 5 990723 18.98 ± 0.08 25.13 ± 0.63 7 25.3 ± 1.3 113.2 ± 21.2 6 990730 21.52 ± 0.56 43.66 ± 4.18 7 25.6 ± 1.6 119.4 ± 45.8 7 990719 29.48 ± 2.64 14.34 ± 0.99 7 24.8 ± 1.5 92.8 ± 22.5 8 990803 30.28 ± 0.8 25.17 ± 1.72 7 25.4 ± 1.5 132.0 ± 17.3 9 990729 30.31 ± 2.57 39.17 ± 1.41 7 24.7 ± 0.8 116.9 ± 33.5

The following modes of regulating the ingestion rate lands) during June and July 1999 and transported of food have been described: (1) changing the pump- to the Field station of RIKZ at Jacobahaven (Oost- ing or the clearance rate (Navarro et al., 1992, 1994; erschelde, S.W. Netherlands) where the experiments Iglesias et al., 1996; Navarro & Widdows, 1997), or were executed. Selected individuals for experiments (2) increasing rejection of pseudofaeces above a cer- had a shell length of around 25 mm (Table 1). Ac- tain threshold of seston quantity and quality (Iglesias climatisation to laboratory conditions proceed for one et al., 1992; Navarro et al., 1992; Navarro & Wid- week. During this time the animals were placed in a dows, 1997). There are other mechanisms to increase container with fine sand and natural sea water pumped the food ingestion and absorption by a preingestive se- continuously from the coast. Parameters from the wa- lection of organic matter from filtered material (Bayne ter were similar to those from the place of collection et al., 1993; Navarro & Iglesias, 1993; Iglesias et al., of the animals. Afterwards 7 individuals of S. subtrun- 1996; Hawkins et al., 1998; Wong & Cheung, 1999) cata were placed in experimental chambers and fed on and adjustment of the absorption efficiency to changes experimental diets for 5 h prior to start of the meas- in gut passage time (Bayne et al., 1989; Navarro et al., urements. Collection of biodeposits were carried out 1994) or the gut content (Hawkins et al., 1990). Little 8 h after the start of the experiment. Two samples of information about feeding and ecophysiology of Spi- biodeposits were collected for each individual on each sula subtruncata is available (Møhlenberg & Riisgård, experiment. 1979; Kiørboe & Møhlenberg, 1981; Møhlenberg & Kiørboe, 1981). Research related to its growth in the North sea has been carried out recently (Degraer, 1999). Experimental diets The aim of the experiment reported here is to de- Dietary composition included the following compon- termine how physiological rates are affected in Spisula ents: (1) Cells of the pelagic diatom Phaeodactylum subtruncata by different diets. The hypothesis is that tricornutum and (2) silt particles (<50 µm) previously this filter feeder is able to respond to variation in food ashed for removing the organic material. The mixtures quality and quantity by adjustments of physiological of algaes and silt were added to natural sea water di- rates. luted with filtered sea water in a reservoir tank. A mixer was placed in the bottom and suspension of Material and methods particles was promoted by aeration. A pump provided a flow of water through each chamber (2.8 l h−1) Collection and maintenance in which the depletion of particles by the clams was below 30% of the total. For making and controlling Individuals of Spisula subtruncata were dredged from the diets, the concentration of particles was monitored populations in the Molengat (North of The Nether- with a Coulter Counter fitted with a 100 µm tube. 507

The designed ranges for the diets were: total par- (f=p) and when SE = 1, there is a complete selection ticulate matter (TPM: mg l−1) 10–30 mg l−1 and per- and ingestion of organic particles. centage organic matter of seston 15–40%. Details of the different experimental diets are shown in Table 1. Size standardization of physiological rates In each experiment, 3 water samples were taken during the experimental period from the inflow of the control Once the physiological measurements were com- chambers. For determinations of TPM, water samples pleted, shell length of each individual was recorded to (1 l) were filtered onto pre-ashed (450 ◦C for 4 h) and the nearest 0.1 mm as well as the ash-free dry weight of the soft tissues (weight after dry the soft tissues at weighed GFC filters, rinsed with sea water-isotonic ◦ ◦ ammonium formate and dried at 80 ◦C. The dry weight 80 C during 24 h − weight after calcination at 520 C of retained material gave the TPM and the weight loss during 4 h). Rates were assumed to scale with body on ignition at 450 ◦C for 4 h gave the ash weight or size, and consequently, measurements were standard- particulate inorganic matter (PIM: mg l−1) from which ised to an equivalent of 150 mg ash free dry tissue of − ∗ the particulate organic matter (POM: mg l 1)wasde- S. subtruncata by using the formula Ys = Ye (150/ b rived (POM = TPM − PIM). The percentage organic We) ,whereYs = physiological rate of a standard- content of suspended matter was computed as: % OM sized , Ye = uncorrected physiological rate, We =(POM× 100)/TPM. = ash-free dry weight (mg) of the experimental animal and b = the weight power established for clearance rate of the bivalve filter feeders (b=0.58; Bayne & Newell, Collection of biodeposits and calculations of rates 1983), which has been assumed to represent the size During the experiment, faeces and pseudofaeces were dependence for rates of food processing in general. collected separately at time intervals of 2–3 hours by using a Pasteur pipette. Biodeposits were sep- Statistical analysis arately filtered onto preashed and preweighed GFC The effects of different seston concentrations and per- filters. The total, inorganic and organic mass of biode- centage organic matter values on the physiological posits were determined by methods similar to those responses of Spisula subtruncata was tested with Two- described above for sea water samples. The follow- way analyses of variance (ANOVA). The significance ing physiological rates were calculated: Filtration rate of differences between treatments was analysed with (FR: mg h−1), rejection rates of pseudofaeces (RR: mg a Tukey–Kramer procedure as post-hoc test (Sokal h−1), ingestion rate (IR: mg h−1) and absorption rate & Rohlf, 1995). Regression analysis were performed (AR: mg h−1). Referring to Conover (1966), absorp- with Systat 9.0. A significance level of 5% was used tion of inorganic matter through the digestive system in all tests. is negligible, in this case the sum of inorganic rejec- tion rate of pseudofaeces and inorganic egestion rate of faeces was considered to represent the inorganic Results filtration rate (IFR: mg h−1), hence, clearance rates −1 (CR: l h ) were estimated as CR = IFR/PIM. Filtra- Filtration rate tionrate(FR:mgh−1) was calculated as FR = CR × TPM and filtration rate of particulate organic matter Total filtration rate (FR: mg h−1) was tested at dif- −1 (OFR: mg h )asOFR=CR× POM. Ingestion rate ferent levels of organic matter content (%OM) and was calculated as IR = FR − RR and the organic in- total particulate matter (TPM: mg l−1)ofthediet −1 gestion rate (OIR: mg h ) as the difference between (Table 2A). FR was significantly higher at high TPM −1 OFR and the organic rejection rate (ORR: mg h ). and at low percentages of organic matter (Fig. 1). Therateoffoodabsorption(AR:mgh−1) was com- puted as the difference of the organic rate of ingestion Rejection rate & preingestive selection of the organic and the organic rate of egestion of faeces. Preingestive material selection efficiency (SE) of the filtered organic matter was estimated as SE = 1 − (p/f), where p is the organic Rejection rate of pseudofaeces (RR: mg h−1)in- content of the pseudofaeces (p= ORR/RR) and f is, as creased significantly with FR and the regression equa- defined above, the organic content of suspended matter tion is RR = 0.78 FR −1.34 (R2=0.85, N=116, (f= POM/TPM). When SE = 0, there is no selection p<0.01). RR reached higher values at increasing TPM 508

Table 2. Statistical test of influences of total particu- late matter (TPM) and percentage organic matter (% OM) on filtration rate (A), Rejection rate (B), Selec- tion efficiency (C) and Absorption rate (D) of Spisula subtruncata in the different experimental conditions. Values are degrees of freedom (df), mean square (MS) and probability (P) of ANOVA

Source of variation df MS P

(A) Filtration rate − Figure 1. Filtration rate (mg h 1)ofSpisula subtruncata as a TPM 2 113.29 <0.001 response to different concentrations of total particulate matter − %OM 2 109.90 <0.001 (TPM: mg l 1) and at different levels of organic matter. Mean value × TPM %OM 4 4.06 0.126 + standard deviation. Error 107 2.20

(B) Rejection rate TPM 2 62.10 <0.001 %OM 2 94.74 <0.001 TPM × %OM 4 3.69 0.071 Error 107 1.18

(C) Selection efficiency TPM 2 0.003 0.853 %OM 2 22.08 <0.001 TPM × %OM 4 0.30 0.878 Error 103 0.02

− (D) Absorption rate Figure 2. Rejection rate (mg h 1)ofSpisula subtruncata as a TPM 2 0.121 0.101 response to different concentrations of total particulate matter −1 %OM 2 1.133 <0.001 (TPM: mg l ) and at different levels of organic matter. Mean + TPM × %OM 4 0.033 0.112 standard deviation. Error 101 0.017

and decreased at high percentages of organic matter within the same level of seston concentration (Fig. 2). The different treatments resulted in significantly dif- ferent rejection rates of S. subtruncata at different seston quantity and quality (Table 2B). Together with the rejection of pseudofaeces preingestive selection of organic material occurred with a certain selection ef- ficiency (SE). SE is significantly correlated with the quality of seston but not with the quantity (Table 2C). Figure 3. Preingestive selection efficiency (%) at different total par- − SE reaches high values at high percentages of organic ticulate matter concentrations (TPM: mg l 1) and percentages of the matter in the diet (Fig. 3). organic matter from the diet. Mean value + standard deviation.

Ingestion rate & absorption rate well. As described above, SE was high at high per- centages of organic matter in the diet and then OIR Ingestion rate showed no significant relation with dif- is increased as a function of SE. However, values ferent levels of seston concentration and percentage of OIR are underestimated by this procedure because organic matter from the diet (Fig. 4). The organic we could not quantify the mucus rejection rate as a ingestion rate (OIR: mg h−1) was a function of SE component of the organic rejection rate. with the following equation: OIR = 2.59 SE + 0.28 A positive relation occurs between the absorption (R2=0.41; N=111; p<0.01), both physiological para- rate of the ingested food (AR: mg h−1)andtheper- meters are dependent on the organic matter content as centage organic matter (% OM:%) of the diet but 509

the cockle Cerastoderma edule (Linné, 1758). Sim- ilar behaviour was observed in Mytilus edulis (Linné, 1758) by Bayne et al. (1993). In S. subtruncata the filtration rate increases with TPM but the increment is lower at higher food quality. This same effect has been described in C. edule both at low (Iglesias et al., 1992) and high (Navarro & Widdows, 1997) seston concentrations. A high FR is an efficient mechanism to enhance the energy gain from a turbid environment, because the species can process large amounts of par- ticulate matter. S. subtruncata have the capacity to sort −1 Figure 4. Ingestion rate (mg h )ofSpisula subtruncata as a and preferentially ingest organic particles, and reject response to different concentrations of total particulate matter − (TPM: mg l 1) and at different levels of organic matter. Mean + a high proportion of inorganic matter in the form of standard deviation. pseudofaeces. Rejection of pseudofaeces has been described as a regulatory mechanism of ingestion rate (Iglesias et al., 1992; Navarro et al., 1992). Hawkins et al. (1996) found that the production of pseudofaeces in M. edulis depends on the FR, which increased with seston con- centrations up to 112 mg l−1. Navarro & Widdows (1997) obtained similar results for C. edule indicating an increase of the rejection rate with seston concen- trations and a similar pattern for FR. In our study we have observed the same trend for S. subtruncata with an increase of RR at higher seston concentrations. At high quality of the diet there was a decrease of the − Figure 5. Absorption rate (mg h 1)ofSpisula subtruncata at dif- rejection rate of S. subtruncata. Navarro & Widdows −1 ferent concentrations of total particulate matter (TPM: mg l )and (1997) indicated that C. edule shows a mechanisms percentages of organic matter. Mean values + standard deviation. for regulating ingestion by increasing the rejection rates at high levels of FR but this mechanism can be not with the TPM (Table 2D). The equation relat- modified by the quantity and quality of the suspended ing AR with quality of the seston is AR = −0.53 particulate matter. Iglesias et al. (1992) and Navarro 2 + 0.04%OM (R =0.65; N=111; p<0.01) (Fig. 5). et al. (1992) concluded that the mechanism of regu- Absorption efficiency values ranged from 0.3 to 0.8. lation in C. edule is determined by food composition, with reductions of clearance rate as the most important regulatory mechanism under high quality diets, and Discussion the production of pseudofaeces playing that role un- der low quality conditions. In S. subtruncata as an Many studies have been carried out relating food avail- effect of filtration and rejection rate, ingestion rate (IR) ability and filtration rate in marine bivalves, using was stable at different levels of organic matter content seston concentrations below the threshold of pseudo- or seston concentration. Apparently increasing RR at faeces production (Navarro & Winter, 1982; Bayne et different food conditions regulates IR. This regulatory al., 1989) or above this threshold (Iglesias et al., 1992; mechanism has been described by Bayne et al. (1989) Navarro et al., 1992; Bayne et al., 1993; Hawkins in the mussel M. edulis. They showed that maximisa- et al., 1996). The present study showed that filtra- tion of the ingestion rate occurred above the threshold tion rate (FR) increased with seston concentration and of pseudofaeces production. decreased with higher values of food quality. Some au- It is well established that bivalves are able to sort thors (Iglesias et al., 1992; Navarro et al., 1992, 1994; particles using their labial palps (Kiørboe & Møhlen- Navarro & Widdows, 1997) also found an increase of berg, 1981; Newell & Jordan, 1983; Newell et al., FR with values of concentration of the seston (from 1989, Ward et al., 1991) resulting in the preferential 1to300mgl−1) in another infaunal bivalve such as rejection of inorganic material in pseudofaeces. In S. 510 subtruncata the selection efficiency (SE) increased at constant ingestion rate. As a consequence, this species high organic matter contents of the diets, although is well adapted to survive in environments with fluctu- some negative values of SE occurred in experiments ations in seston quality and quantity and maximizing with diets containing low organic content due to mu- the energy gain at high levels of organic matter in the cus rejection. A pre-ingestive mechanism represents water column caused by algal blooms in the coastal an adaptation to conditions with different quality of waters and a lower resuspension of fine sediments the diet. The trend recorded in our study is similar to compared with estuarine waters. other previous experiments with C. edule (Iglesias et al., 1992; Urrutia et al., 1996) but in our case lower values were obtained for similar organic contents. Ig- Acknowledgements lesias et al. (1992) assumed that the rejected material by C. edule at food qualities below 40% of organic The authors are grateful to the National Institute for matter contains approximately constant fractions of Coastal and Marine Management (RIKZ), The Neth- mucus and that pseudofaecal mucus loss could be the erlands, for providing research facilities and to Joke explanation of the lower values of SE. These same au- Kesteloo from Netherlands Institute for Fisheries re- thors suggested that the loss of secreted mucus in the search (RIVO), The Netherlands, for the collection of pseudofaeces would be similar to the metabolic faecal the individuals of Spisula subtruncata.Wealsoap- losses associated with digestive processes. preciate valuable comments and suggestions made by Absorption rate (AR) in S. subtruncata was pos- two anonymous referees. This research has been sup- itively correlated to organic content of seston and ported by a Marie-Curie training research grant of the no dependence was found with seston concentration. European Commission, within the project SIMCERE This is a result of both preingestive and digestive (FAIR GT97-4525). mechanisms at different seston qualities. Preingestive selection gives high OIR. 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