Maurice Heral

Some general relationships in comparing the feeding physiology of suspension-feeding bivalve molluscs

We have studied feeding behaviour in the cockle Cerastoderma edule (L.), the oyster Crassostrea gigas (Thunberg) and the mussel Mytilus edulis (L.) for input to a model predicting the environmental capacity of the bay of Marennes-Oleron, France for shellfish culture. We present a common set of equations that summarize functional interrelations observed between component processes of feeding physiology, whilst allowing predictions of feeding behaviour and net organic absorption rate on the basis of seston abundance and seston organic content alone. Selective processes, and the consequences of those processes, are an important feature of those interrelations. Each species was able selectively to enrich the organic content of ingested matter relative to filtered matter, preferentially rejecting inorganic matter prior to ingestion as pseudofaeces. When feeding upon natural seston, the efficiency of that selection varied positively with both the mass of seston filtered h−1 and the organic content of filtered matter. At the highest food availabilities, when the mass of seston filtered h−1 was greatest, more than 60% of the organic matter ingested h−1 by each species resulted from selective processes. Physiological consequences of that selection were amplified by positive exponential relations between the net absorption efficiency for ingested organics and the organic content of ingested matter. We show that our common set of equations satisfactorily predict net organic absorption rate measured directly in all three species feeding throughout the same natural tidal variations of food. Collective findings therefore establish that similar functional interrelations control feeding responses in each species, and identify key relations affecting selection and absorption for use in the future modelling of growth and environmental relations. By fitting a common set of equations to responses measured directly under the same natural conditions of seston availability, we have standardised the comparison of environmental influences upon rates and efficiencies of feeding behaviour for each species. The mass of seston filtered h−1 increased in similar positive relations with seston abundance in each species. However, there were significant behavioural differences in the processing of filtered particles. Compared with the epifaunal species C. gigas and M. edulis, C. edule is normally infaunal, and demonstrated a lower capacity to selectively ingest organic matter. Alternatively, compared with M. edulis, C. gigas was not as efficient either in the net selection of organic matter or in digesting and/or assimilating ingested organics, resulting in lower rates of net energy gain. These differences are discussed bearing in mind present experimental conditions, as well as the natural habitat and comparative morphology of each studied species.

Effects of high natural seston concentrations on the feeding, selection, and absorption of the oyster Crassostrea gigas (Thunberg)

Feeding, selection and absorption were determined for the Pacific oyster Crassostrea gigas cultivated in the Bay of Marennes-Oleron, over a spring/neap tidal cycle. Physiological determinations were related to the highly variable food environment with continuous recordings of turbidity and fluorescence. In this bay, resuspension processes have a major influence on food availability and quality. Seston characteristics experienced by oysters can be summarized by high turbidity levels from 20 to 350 mg·l−1 and a predominance of the detritic fraction among the organic fraction (mean C/N ratio=16.57). Food is diluted by the fine resuspended sediment, and organic content of particulate matter in the water column decreases from 30% to 10% with increasing seston loads. Significant differences (Ancova, P<0.01), due to low retention efficiencies of the smaller particle size range, were recorded between the food quality (estimated by the organic content and the total pigment content) measured in the water column and the fraction retained by the oysters gill. Below seston concentrations of 90 mg·l−1 ingestion rate was regulated by pseudofaecal production. Above 90 mg·l−1, a sharp reduction of filtration and rejection rates suggests physical constraints limiting food acquisition. The oyster selectively rejects inorganic from organic particles, enriching the ingested fraction. Amongst the potentially nutritive particles, significantly fewer particles containing phytopigments were rejected relative to organic particles (non-linear regressions, P<0.001). The negative influence, through food dilution, of high seston loads on net absorption efficiency was determined. This efficiency decreases with decreasing organic ingested fraction. Scope for growth calculations confirm the negative influence of seston loads, but show, supported by field growth measurements, that resuspended organic particles play an important role in the oysters nutrition.

Preingestive selection of different microalgal mixtures in Crassostrea gigas and Mytilus edulis, analysed by flow cytometry

Abstract The potential impact of selective grazing by filter-feeding bivalves was studied on the relative composition of both planktonic and benthic algae that are commonly suspended in coastal areas. Different feeding behaviour was observed in the oyster Crassostrea gigas and the mussel Mytilus edulis. C. gigas preferentially filtered and rejected (as pseudofaeces prior to ingestion) diatom species relative to flagellates. These differences appear to depend upon differences in algal shape and flexibility. Findings also suggest that ratios of rejection to filtration for flagellate species were influenced by the planktonic or benthic origin of the other available algal species. Future studies of trophic flux and resource utilisation should therefore consider the extent to which different filter-feeding species may preferentially filter and/or ingest separate algal species that are simultaneously available in the surrounding seston.

Variability of feeding processes in the cockle Cerastoderma edule (L.) in response to changes in seston concentration and composition

Physiological processes controlling food acquisition by the filter feeding bivalve Cerastoderma edule (L.) were quantified under a broad range of seston concentrations and compositions. Experimental diets consisted of suspensions elaborated by adding variable amounts of microalgal cells of different species (or sediment particles in one case) to natural sea-water. Clearance rates exponentially decreased with seston concentration, but the rate of reduction was higher with suspensions of high organic content. Pseudofaeces production appeared as a positive function of the rate of particle filtration; however, for a given filtration rate, more pseudofaeces were rejected when filtered matter had a low organic content. As a consequence, after an initial elevation, ingestion rate remained almost constant across particle concentrations. Pre-ingestive food selection enhanced the rate of particulate organic matter ingestion and this organic enrichment of ingested matter became more pronounced for diets of low food value, where most filtered matter was being rejected as pseudofaeces. Selection of particles at the pre-ingestive level was more efficient in terms of chlorophyll, revealing preferential ingestion of algal particles compared with the whole organic matter. Stronger selection for algae, however, was not evident in terms of preferential nitrogen ingestion, as compared with carbon, which was probably due to similar low values of the CN ratios in all experimental conditions. Absorption efficiency depended on the organic content of ingested matter according to an exponential, saturating function. In general, feeding processes of cockles appear well adapted to cope with elevations in particle concentration and simultaneous reductions in the food value of available seston that occur when resuspended bottom sediments constitute a significant fraction of particulate materials of the water column. Under these conditions, high rates of seston filtration and pseudofaeces production, together with preferential organic ingestion act to compensate for the dilution of organic matter in suspension and its detrimental effect on the rate of food absorption. However, this compensatory behaviour is not so efficient as to make absorption rate independent of the organic value of available particles. The organic content of resuspensible sediments may thus become the main determinant of food acquisition in cockles.

No influence of food quality, but ration-dependent retention efficiencies in the Japanese oyster Crassostrea gigas

Abstract Relative retention efficiency (Er) in Crassostrea gigas was estimated in the laboratory with seven artificial diets consisting of variable proportions of algae and silt, as well as in the natural environment at high seston concentrations up to 64.37 mg/1. Crassostrea gigas did not adjust retention efficiency according to the food quality, gill porosity being controlled by the concentration of paniculate matter. At low seston load (1.34 mg/1), the oyster showed no change in retention for particles larger than 3–4 μm (Equivalent Spherical Diameter, ESD). But at the highest concentration (64.37 mg/1), it could only retain particles larger than 12 μm (ESD) with maximum efficiencies. The Japanese oyster therefore has an active response to high particle concentration, and which was described by a model where retention efficiency (Er) varied with suspended particulate matter (Vol mm 3 /l) as follows: Er= − 12.537 Vol e (−0.304 ESD ) + 100

Ecophysiological model of growth and reproduction of the black pearl oyster, Pinctada margaritifera: potential applications for pearl farming in French Polynesia

A model of bioenergetics of the black pearl oyster (Pinctada margaritifera) was built to simulate growth, reproduction and spawning in suspended culture at field sites in Takapoto lagoon (French Polynesia). This model was based on allometric scaling of physiological functions and scope for growth (SFG) calculations. The input functions were clearance rate (CR, 1 day(-1)), retention efficiency (RE, %) for each kind of particle encountered in suspended matter, pseudofaeces and faeces productions (PF and F, mg C day(-1)), excretion and respiration rate (U and R, mg C day(-1)). The assimilated carbon (i.e., SFG, mg C day(-1)) was partitioned to the three internal state variables (somatic tissue, shell and gonad) according to the asymptotic increase of the reproductive effort (ER, %) with the age. Given organic and mineral particulate matter in suspension in lagoon water (POM and PIM, mg L-1) and assuming that the taxonomic composition of POM was fairly constant throughout the year, the model predicted annual evolution of total tissue weight (W-Tissue, g dry weight), shell weight (W-Shell, g DW) and gonad weight (W-Gonad, g DW) of pearl oysters at various ages. Data on tissue and shell growth, but also on gonad development of cultivated pearl oysters, acquired in 1997-1998 in Takapoto lagoon, were used to validate the model outputs. Results of the simulations indicated that the P. margaritifera growth model provided realistic growth trajectories for shell, somatic tissue and gonad, for pearl oysters aged from 1 to 4 years.

Correction for particulate organic matter as estimated by loss on ignition in estuarine ecosystems

Abstract Loss on ignition (LOI) is a simple, inexpensive method widely used to estimate organic matter in the water column and sediment of marine and freshwater ecosystems. Suspended particulate matter in estuarine waters however often contains a large fraction of argillaceous minerals whose loss of structural water can introduce significant bias to the method. The accuracy of LOI, in comparison with elemental analysis, was evaluated in 105 water samples from the Marennes-Oleron Bay (French Atlantic coast). The suspended particulate matter analysed ranged from 7 to 108 mg l −1 , with a mean inorganic fraction of 81.3±s.d. 7.2%. LOI overestimated particulate organic matter (POM) concentrations by up to 300% (mean 98 ± s.d. 28%), and this overestimation was significantly related to particulate inorganic matter (PIM) concentrations. POM overestimation increased linearly with PIM, representing a mean 8.7±s.d. 2.0% of PIM. This value was compared with a theoretical correction factor based on the specific clay composition of PIM at the study site and on thermo-gravimetric analysis for standard clay. The clay fraction, which represents 90% of PIM in the Marennes-Oleron Sound, consists of 40% illite, 30% kaolinite and 30% montmorillonite. The similarity between the theoretical correction factor (9.3% of PIM) and the overestimation based on measurements (8.7%), suggests that a priori correction of POM data is possible. In fact, for three bodies of water along the French Atlantic coast, whose inorganic resuspended matter shows the same mineralogical composition, POM concentrations as estimated by LOI can be corrected by subtracting 9.3% of PIM mass.

Why Carrying Capacity Models are Useful Tools for Management of Bivalve Molluscs Culture

In areas where oyster or mussel culture is very intensive, declines of growth rate and decreases of survival rate have occurred. For these reasons, plans have been proposed to regulate the cultivated biomasses in order to fit the carrying capacity of the different ecosystems (Heral et al 1990; Heral, 1991). In areas where new aquaculture of molluscs is beginning, oyster or mussel farmers need to know how large the extension of the culture could be and what the maximal densities should be in order to obtain the maximum economic benefit. Furthermore, as mollusc cultures are developed in coastal areas, they are very susceptible to changes in environmental conditions that can modify trophic relationships, or directly reduce growth rate, physiological functions, recruitment and mortality processes. To give responses to these three types of questions concerning regulation, development, and environmental impact, it is necessary to build models. These models should predict responses in terms of bivalve growth rate in relation to the different management strategies, taking into account biomasses, new species and environmental modifications that can be planned. Two types of models have been developed to achieve these goals, (i) general models based on long term series of population dynamics of the cultivated species, and (ii) trophic models that describe the main relationships that govern the major fluxes of energy, carbon or nutrients in ecosystems.

Ecophysiologie et bilan énergétique de la palourde japonaise d'élevage Ruditapes philippinarum

Rates of filtration and respiration both follow a nonlinear model based on temperature of the form: Y = a × (T−T0)c × e −b(T−T0 with maximal values at 15 and 20°C, respectively. Quantities of seston varying from 0 to 30 mg · 1−1 have no effect in reducing the filtration rate. > 8 mg · 1−1, ingestion is regulated by the production of pseudofaeces. Maximal assimilation efficiency is ≈ 78%, but this is considerably reduced when the mineral content of the water increases. Assimilation efficiency for the Manila clam is reduced at both high (> 10 mm3· h−1) or low (< 2 mm3· h−1) values of ingested ration. The estimated value of growth efficiency (75%) and values of growth efficiency derived from the model k1 = 33%, K2 = 51% are optimized when ingested volumes are between 1 and 2 mm3. Standard metabolism is estimated as 0.11 ml O2 · h−1. Zero growth efficiency occurs at a ration level of 2 J · h−1 for an adult. The individual energy budget shows that production is dependent more on temperature than on the energy value of the food. Comparison of calculated and measured production reveals differences resulting from the higher levels of seston found in the field. In particular, during the winter when the mineral content of the seston is high (90 mg · 1−1), there is a continuous loss of weight. This results from a lower assimilation efficiency together with production of pseudofaeces. Excretion of organic nitrogen varies throughout the year, ammonia representing no more than a mean of 29.8% of the total nitrogen excretion.

A genetic and metabolic basis for faster growth among triploids induced by blocking meiosis I but not meiosis II in the larviparous European flat oyster, Ostrea edulis L.

This study establishes a genetic and metabolic basis to faster triploid growth in the oyster Ostrea edulis. Triploidy was induced using cytochalasin B, and image analysis of biopsied tissue employed to ensure similar ploidy of all animals within each class. Results indicate that lifetime growth in total dry tissue weight over 15 months was more than 60% faster (p<0.001) in meiosis I triploids than in diploid siblings or meiosis II triploids, with no difference between meiosis II triploids and their diploid siblings. For six polymorphic enzyme loci, single-locus heterozygosity was consistently greatest in meiosis I triploids (p<0.001), so that average multiple-locus heterozygosity in meiosis I triploids was 49% higher than in normal diploids, and 55% higher than in meiosis II triploids (p<0.001). This suggests that faster growth resulted from increased allelic diversity, rather than the increased allelic quantity that results from the addition of one entire set of chromosomes among triploids generally. Results also confirm that the faster growth of meiosis I triploids resulted from reduced energy expenditure, associated with lower concentrations of RNA per unit total tissue protein, which infer reduced rates of whole-body protein turnover. Statistical analyses confirmed that differences in oxygen consumption and growth were associated with both ploidy class and average multiple-locus heterozygosity, indicating that performance in meiosis I triploids is not only improved as a result of reduced reproductive output, but also through the metabolic consequences associated with increased heterozygosity.