Anthony J.S. Hawkins

Mathematical modelling to assess the carrying capacity for multi-species culture within coastal waters

Abstract In the context of aquaculture, carrying capacity is generally understood as the standing stock of a particular species at which production is maximised without negatively affecting growth rates. The estimation of carrying capacity for aquaculture is a complex issue. That complexity stems from the many interactions between and among cultivated and non-cultivated species, as well as between those species and their physical and chemical environments. Mathematical models may help to resolve these interactions, by analysing them in a dynamic manner. Previous carrying capacity models have considered the biogeochemical processes that influence growth of cultivated species in great detail. However, physical processes tend to have been addressed very simplistically. Further, most modelling has been for monocultures, despite the increasing importance of multi-species (=polyculture) systems. We present here a two-dimensional coupled physical–biogeochemical model implemented for Sungo Bay, Shandong Province, People’s Republic of China. Sungo Bay is used for extensive polyculture, where bivalve shellfish and kelp are the most important cultivated species. Data collected over 13 years (1983–2000) was available for modelling. Our main objectives were to implement the model, achieving reasonable calibration and validation with independent data sets, for use in estimating the environmental carrying capacity for polyculture of scallops and oysters. Findings indicate that the model successfully reproduces some of the main features of the simulated system. Although requiring some further work to improve predictive capability in parts, predictions clearly indicate that Sungo Bay is being exploited close to the environmental carrying capacity for suspension-feeding shellfish. Comparison of different culture scenarios also indicates that any significant increase in yield will depend largely on a more optimal spatial distribution of the different cultivated species.

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.

A functional model of responsive suspension-feeding and growth in bivalve shellfish, configured and validated for the scallop Chlamys farreri during culture in China

A dynamic growth model is presented for the suspension-feeding scallop Chlamys farreri. The model is configured and validated for C. farreri cultured in Sungo Bay, China, using functional relations to simulate rapid and sensitive adjustments in feeding and metabolism as observed in response to the highly changeable environment there. Notable novel elements include resolving significant adjustments in the relative processing of living chlorophyll-rich phytoplankton organics, non-phytoplankton organics and the remaining inorganic matter during both differential retention on the gill and selective pre-ingestive rejection within pseudofaeces. We also include a facility to predict the energy content of non-phytoplankton organics. This is significant, for living phytoplankton contributed less than 20% towards suspended particulate organic matter within Sungo Bay. Further, the energy content of non-phytoplankton organics was very much more variable than for phytoplankton organics. Whether using that facility or assuming an average value for the energy content of non-phytoplankton organics, resolution of the relative processing of different particle types allows simulation of how the rates, organic compositions and energy contents of filtered, ingested and deposited matter change in response to differences in seawater temperature, seston availability and seston composition. Dependent relations predict rates of energy absorption, energy expenditure and excretion. By these means, our model replicates dynamic adjustments in feeding and metabolism across full ranges of relevant natural variability, and successfully simulates scallop growth from larvae or seed to harvestable size under different temporal and spatial scenarios of culture. This is an important advance compared with simpler models that do simulate responsive adjustments. Only by modelling the complex set of feedbacks, both positive and negative, whereby suspension feeding shellfish interact with ecosystem processes, can one realistically hope to assess environmental capacities for culture.

Nutrition of the giant clam Tridacna gigas (L.) I. Contribution of filter feeding and photosynthates to respiration and growth

The total carbon requirements (growth + respiration) of the host tissues of the giant clam Tridacna gigas from Davies Reef on the Great Barrier reef were measured, and compared with rates with which nutrients were acquired from the two potential sources, translocated photosynthates (estimated from oxygen flux-CZAR method) and filter feeding. Results showed that the giant clam is an efficient utilizer of particulate organic matter available in reef waters (Davies Reef mean: 97 μg C·1−1), retaining on average 75% of particles between 2 and 50 μm, and absorbing from them 54% of C. Clearance rates (CR, 1·h−1) of clams were size dependent as defined by the function: CR = 1.85 W0.58 (r2 = 0.85, n = 56). There are major differences between typical non-symbiotic bivalves and Tridacna gigas regarding the relative allocations of energy to respiration and growth. The proportion of carbon deposited in tissues relative to that respired is high in giant clams relative to completely heterotrophic bivalves. We conclude that autotrophy is the major source of carbon to this clam, potentially capable of satisfying all respiratory requirements of the host. However, the potential importance of heterotrophy to total energy needs of the host is also significant and changes with the size of clam. The spectacular rates of growth in this clam are such that filter feeding is able to provide 65% of the total carbon needed both for respiration and growth in small clams (100 mg dry tissue wt), whereas large clams (10 g) acquire only 34% of their carbon from this source.

Seasonal changes in stress-70 protein levels reflect thermal tolerance in the marine bivalve Mytilus edulis L.

Fluctuating concentrations of cellular stress proteins may be especially significant in the environmental adaptation of eurythermal ectotherms. This study has demonstrated that endogenous levels of stress-70 proteins in M. edulis vary seasonally and are positively correlated with seasonal changes both in environmental temperature and thermal tolerance. The levels of stress-70 protein isoforms of 70, 72 and 78 kDa were analyzed in M. edulis L. collected at six consecutive bimonthly intervals from the River Exe (Devon, UK). Significant seasonal differences in endogenous levels of the stress-70 proteins in M. edulis were observed. Levels of these protein isoforms correlated positively with seasonal changes in environmental temperature. Levels of the 70 kDa protein showed a larger seasonal variation, more closely related to natural temperature change, than levels of the 72 and 78 kDa proteins. Additional mussels from the same samples were heat-stressed at 28.5°C, a temperature at which M. edulis is unable to acclimate. M. edulis survived longer at 28.5°C during the warmer months of the year. There were also positive correlations between time of survival at 28.5°C and the coincident levels of endogenous stress-70 proteins. Our results provide evidence that environmental stress may have been sufficient to cause at least partial protein denaturation during a significant proportion of the year, and suggest that high natural concentrations of stress-70 proteins may promote thermal tolerance. Evidence from other studies suggests that maintaining high levels of stress proteins have significant energetic costs and may be detrimental to organismal fitness. We discuss our findings in terms of the costs and benefits associated with stress protein synthesis, and consequences for the ecology and distribution of marine ectotherms.

The metabolic basis of genetic differences in growth efficiency among marine animals

This paper initially reviews evidence for genetic influences upon growth efficiency. We then discuss recent advances in our understanding of the metabolic links whereby genotype affects whole-animal physiology and growth efficiency through differences in protein metabolism. Most evidently, these differences are in protein turnover, defined as the continuous breakdown and replacement of cellular proteins and which provides the flux that is necessary for metabolic regulation and adaptation. Whether comparing individuals, including associations with genetic heterozygosity, or considering the response to breeding, selection or genetic manipulation, reduced whole-body protein turnover consistently underlies lower energy expenditure and higher growth efficiencies. The present paper describes results from our recent studies that have explored the metabolic basis and functional consequences of these differences in whole-body protein turnover by comparing the component activities of specific proteolytic pathways in the mussel Mytilus edulis. Traditionally, it has been thought that requirements for biosynthesis dominate energy expenditure. Nevertheless, a large component of about 30% of the empirical costs of protein deposition cannot be attributed to known synthetic processes and it has been suggested that costs of protein turnover may contribute to the discrepancy. Findings are presented showing that separate whole-body activities of the four main lysosomal proteases were collectively associated with as much as 73% of the variation in maintenance energy expenditure observed between individual mussels. These associations were positive for cathepsin B, cathepsin D and leucine aminopeptidase (Lap-2). Alternatively, higher whole-body activity of cathepsin L was associated with lower maintenance energy expenditure, possibly because cathepsin L was most active in the main tissue of nutrient storage, thereby mobilising energy reserves and reducing the need for protein turnover in remaining tissues. Results therefore indicate profound physiological consequences of lysosomal proteolysis under conditions of partial starvation, but which vary according to functional differences between separate proteolytic pathways. These findings establish that the relative balance between proteolytic pathways is central to our understanding of different efficiencie 12989as in energy requirements and conversion efficiency.

Effects of temperature change on ectotherm metabolism and evolution: Metabolic and physiological interrelations underlying the superiority of multi-locus heterozygotes in heterogeneous environments

Abstract 1. 1. Metabolic sensitivity to environmental temperature change increases in positive exponential relation with initial acclimated rates of energy expenditure, and is influenced by the relative rate with which intracellular amino acids are being mobilised by protein turnover. 2. 2. Greater metabolic sensitivity results in greater physiological variability with fluctuating temperatures, higher energy costs incurred during the response to temperature change, and reduced viability upon exposure to extreme high temperatures. 3. 3. These interrelations help explain the faster production and greater viability of multi-locus heterozygotes experimentally exposed to increased temperature and other stressors, as well as ecogeographical associations indicating the superiority of multi-locus heterozygotes in heterogeneous environments. 4. 4. Implications are discussed for understanding the effects of temperature change on ectotherm metabolism and evolution.

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.

PROTEIN METABOLISM, THE COSTS OF GROWTH, AND GENOMIC HETEROZYGOSITY : EXPERIMENTS WITH THE MUSSEL MYTILUS GALLOPROVINCIALIS LMK

A single cohort of small individuals (31 mm mean shell length, 112 mg mean dry flesh weight) of the marine bivalve mollusc Mytilus galloprovincialis Lmk. was held sequentially for 2 wk at each of four food levels equivalent to ingested rations of less than 0.1%, 2.6%, 3.1%, and 7.4% of dry body weight per day. Growth rate reached a maximum at the highest ration level and was strongly correlated, amongst individuals, with mean heterozygosity measured across nine enzyme loci. Rates of energy expenditure were analysed separately as maintenance metabolic rate and the energy costs of growth (J mg−1 dry tissue). The maintenance metabolic rate correlated with traits of protein metabolism (protein synthesis, deposition, and breakdown), and the separate energy costs of both maintenance and growth correlated with the efficiency of protein deposition (protein growth as a proportion of synthesis). The energy costs of growth also varied in negative relation to mean individual heterozygosity. In a multiple regression analysis, the energy allocation to the costs of growth, body size, mean heterozygos‐ity, and the efficiency of protein deposition together explained 90% of the variance amongst individuals in observed rates of growth. The results support the hypothesis that individual variability in the energy costs of protein turnover and in the efficiency of protein deposition during rapid growth are significant factors providing a link between individual genotype and its phenotypic expression as growth.

Stress-70 protein induction in Mytilus edulis: Tissue-specific responses to elevated temperature reflect relative vulnerability and physiological function

Abstract The exposure of organisms to environmental stressors affects the expression levels of certain “stress proteins” that play an important role in protein homeostasis and stress tolerance. We have used an antibody to monitor this response to elevated temperature in the gill, mantle and muscle tissues of the mussel Mytilus edulis. The antibody detected four isoforms of the highly conserved stress-70 family of proteins, which appear homologous with the hsp70, hsc70, hsp72, and grp78 proteins that are detected by the same antibody in humans. Compared with mantle and adductor muscle tissues, gill tissue showed much the greatest increase in levels of both the 70 and 72 kDa proteins. Levels of the 70 and 72 kDa proteins increased for the first 48 hours of heat stress in the gill, and subsequently decreased between 48 and 72 hours. A 78 kDa protein was present in the gill and mantle tissues, but was absent from the adductor muscle. Alternatively, the 70 kDa protein was more abundant in unstressed adductor muscle than in unstressed gill or mantle tissues. Results are discussed in terms of the proposed cellular locations and function of these proteins, the processes contributing to thermally-induced death, and their implications for our understanding of how temperature affects the physiology, ecology and distribution limits of marine organisms.