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Phenotypic Flexibility and Physiological Tradeoffs in the Feeding and Growth of Marine Bivalve Molluscs1
1 Ecological Impacts of Coastal Cities, Marine Ecology Laboratories, A 11 University of Sydney, NSW 2006, Australia
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Bivalve molluscs have a highly plastic feeding and growth physiology. The increasing availability of families artificially selected for faster growth has enabled physiological experiments to investigate the genetic basis for variable rates of growth. Fast growth is achieved by a combination of increased rates of feeding, reduced metabolic rates and lower metabolic costs of growth. In at least one species there is a trade-off between growth in protein and the storage of lipids that are utilized in gametogenesis. Energy requirements for maintenance are also higher in slow-growing individuals. Reduced costs of growth are due in part to increased efficiencies of protein turnover. Nevertheless, high protein turnover (and therefore high metabolic cost) may benefit fitness in the later stages of gametogenesis. Faster feeding rates do not impair flexibility in feeding behavior which compensates for changes in the food environment. Both inter- and intra-species differences in feeding behavior are evident and suggest possible constraints imposed by faster feeding on the efficiency of selection between food particles of different nutritional value.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONGROWTH, METABOLIC EFFICIENCY AND...FLEXIBILITY IN FEEDINGDISCUSSIONReferences |
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Many suspension-feeding marine bivalve molluscs live in variable environments such as estuaries and shallow coastal waters. Temperatures may vary annually over more than 20°C. Food particles vary in concentration, size and chemical composition over different time-scales, from diurnal, tidally-driven events, to the seasonal cycles of phytoplankton production and decline. Bivalves are mostly sessile as adults. In such circumstances they are expected to have plastic phenotypic traits for feeding and growth (Levins, 1968
). Also, given that growth is indeterminate, theory suggests that energy allocations to maintenance, growth and reproduction are also likely to be flexible (Stearns, 1992).
This plasticity ("the ability of a single genotype to produce more than one alternative form of morphology, physiological state and/or behavior in response to environmental conditions"; West-Eberhard, 1989, p. 249) has been the subject of considerable interest, from simple curiosity in the range of traits expressed, to a growing interest in the evolution of reaction norms within and between species. In this paper I consider some aspects of phenotypic plasticity in bivalves with an emphasis on feeding behavior and growth. I will discuss recent evidence for the existence of physiological tradeoffs ("linkage between two traits that affects the relative fitness of genotypes and thereby prevents the traits from evolving independently"; Angilletta et al., 2003, p. 234) and describe some of the proximate physiological processes that underlie individual growth differences. The picture that emerges is one of considerable behavioral flexibility in response to changes in the food environment, linked with a strong genetic component to growth through a complex synergy of physiological traits.
I shall concentrate on responses to the food environment, rather than temperature. Although growth in bivalves depends on both temperature and food (see review by Gosling, 2003), field studies frequently confirm the primacy of variations in food availability in determining observed growth rate. For mussels (Mytilus edulis) off the California coast (Page and Hubbard, 1987), the clam, Arctica islandica, in the North Sea (Witbaard et al., 1999), the scallop, Argopecten purpuratus, in Chile (Navarro et al., 2000) and the oyster, Saccostrea glomerata, in NSW, Australia (Patterson et al., 2003), amongst others, growth is mostly controlled by nutrient availability, so that "...the underlying capacity for growth is either never realized, or only attained for short periods of time" (Clarke, 2003, p. 576).
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GROWTH, METABOLIC EFFICIENCY AND ENERGY ALLOCATION |
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Growth in bivalves is indeterminate. Rates of growth amongst individuals are highly variable, and much of this is genetically controlled (Hedgecock et al., 1996
; Dittman et al., 1998). Heritability estimates for growth rate in different bivalve species range between 0.21 and 0.59. To quote from a recent review; "that variation for growth in bivalves has a genetic basis is without question" (Gosling, 2003, p. 192). The component processes that have received most attention in the physiological analysis of growth are summarized in the energy balance equation, where Growth (or Net Energy Balance, P) is the difference between energy consumption (A) and energy expenditure (R). If Rmaint and Rgrow are energy expenditures on body maintenance and growth, respectively (and expenditure on reproduction is incorporated into Rgrow), then R = Rmaint + P·Cg, where Cg is the metabolic cost of growth and reproduction, and P = (A – Rmaint)/(1 + Cg).
Working with the oysters Crassostrea gigas and Saccostrea glomerata from genetically distinct lines selected for fast growth, Bayne (1999, 2000) and Bayne et al. (1999a, b) postulated that growth differences between these and control oysters would be due to one of three possibilities implicit in the energy balance equation; differences in energy acquisition (A, or the metabolisable energy intake, MEI), the differential allocation of metabolisable energy to maintenance and growth, or differences in metabolic efficiencies such as the costs of growth (Cg). In the event, there was a marked covariance between component processes distinguishing between growth-rate categories. Oysters selected for fast growth showed "a higher rate of protein growth, at greater efficiency, and fuelled by a higher metabolisable energy intake" than control, not-selected, oysters (Bayne, 2000, p. 200).
Increased metabolisable energy intake results from changes in both the pre- and post-ingestive processes of feeding behavior (see Fig. 1). Pre-ingestive processes include the capture of suspended particles and the sorting of these between organic-rich and organic-poor components, the former for ingestion, the latter for rejection as pseudofaeces. Post-ingestive processes include further particle sorting, digestion, absorption and egestion of true faeces. Efficiencies associated with these processes include pre-ingestive selection efficiency between particles of different organic/nutritional content, and post-ingestive absorption efficiency with which nutrients from ingested particles are absorbed into the body.
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In experiments on crosses between inbred lines of C. gigas, Bayne et al. (1999a)
analysed aspects of feeding behavior as contributing to observed differences in growth. When fed a diet of high food quality (organic content OC = 35%, chlorophyll a = 23.1 ± 4.5 µg liter–1) and compared with a low-quality diet (OC = 20%, chlorophyll a = 4.5 ± 2.1 µg liter–1) all crosses increased their rates of feeding, but the inbred individuals ("homozygotes") had slower feeding rates than the outbred individuals ("heterozygotes"). Rates of rejection of filtered material as pseudofaeces increased in both groups, as did the efficiency of selection for organic-rich particles. These feeding behaviors resulted in faster acquisition rates for organic matter in the heterozygotes, at both ration conditions. As the inbred oysters had higher metabolic rates than the heterozygotes, the net result was significantly faster rates of growth by the heterozygotes (growth heterosis). Experiments with S. glomerata that had been selected over four generations for faster growth, compared with wild conspecifics, confirmed these trends in a different species (Bayne, 2000).
These results with oysters reflected earlier studies in which growth rate differences between individuals of different mean heterozygosity in populations of mussels (Mytilus edulis and M. galloprovincialis) were due to physiological differences in feeding behavior, the costs of protein turnover and the efficiency of protein deposition for both maintenance and growth (Hawkins et al., 1986; Bayne and Hawkins, 1997). Phenotypic differences, whether between hybrids and their respective inbred lines, or between lines selected for fast growth are therefore evident in a wide range of physiological traits, including feeding rates and the metabolic efficiencies associated with protein deposition and growth.
Table 1 summarizes the evidence for different energy allocation strategies in fast- and slow-growing lines of Sydney rock oysters (Bayne, 2000). The oysters selected for fast growth showed greater relative allocation of the metabolisable energy intake to growth, including protein growth, than control individuals, but lower allocations to both maintenance and lipid storage. Slow-growing wild oysters supplemented lipid storage by a greater utilization of tissue carbohydrates. There was no evidence of a growth/size tradeoff i.e., the relation between growth and size did not differ statistically between fast- and slow-growing strains.
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An analysis of growth over a wide range of ingestion rates allows the estimation of potential efficiency discriminators between fast- and slow-growing individuals (Fig. 2). The ingestion rate at zero growth estimates the ingestion requirement for maintenance. The slope (exponent) of the relationship differs below and above this point. Between zero food intake and the food intake at zero energy balance, the exponent affords an estimate of the conversion efficiency of ingested energy for maintenance. The exponent for the relationship above maintenance is the gross conversion efficiency (or K1) of ingested energy for growth. Net conversion efficiency (or K2) may be estimated as the exponent for the relation between growth and the absorbed ration, or metabolisable energy intake.
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, •) were used to estimate the efficiency of utilization of ingested matter for maintenance and the maintenance requirement for ingested matter. Values at higher ration levels (
, 
) were used to estimate the efficiency of utilization of ingested matter for growth. FIG. 2B. Crassostrea gigas. Rates of metabolism at different rates of ingestion below the maintenance requirement, for fast- (Figure 2A shows results for fast- and slow-growing strains of C. gigas. These strains differed in their maintenance requirements (equivalent to ingestion rates of 1.36% and 0.98% of body weight per day for slow and fast growers, respectively). Faster-growing individuals converted more of their ingested ration into growth, but the efficiency of this conversion did not differ between growth categories, either for maintenance (overall mean = 0.83 ± 0.20) or for growth (0.65 ± 0.10).
Metabolic rates (R: Joules d–1) also increased with rates of ingestion (Fig. 2B), and were faster in slower-growing oysters. R at the level of the maintenance requirement estimates the maintenance metabolic rate (Rmaint), which was lower for the fast growers. R – Rmaint provides an estimate of the metabolic expenditure on growth; this increased with the rate of growth (Fig. 2C) and the exponent in this relationship estimates the unit cost of growth, Cg. Costs of growth were higher in the slower growing oysters. As argued by Wieser (1994), a useful ‘apparent efficiency of growth’ (K3) is the ratio of growth to the sum of growth and the metabolic expenditure on growth, P/(P + Rgrow); see Table 2. Faster growers achieved higher apparent growth efficiency, whereas conversion efficiencies did not differ significantly between growth categories.
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The metabolisable energy intake above the maintenance requirement is utilized for protein and lipid accumulation but in different ways in the two growth categories (Fig. 3). In the faster-growing individuals (Fig. 3A) protein accumulation is favoured over lipids; proportional allocations, estimated from the exponents in these relationships, are 0.38 ± 0.05 and 0.07 ± 0.02 for proteins and lipids, respectively. The opposite case holds for the slower-growing individuals (Fig. 3B), with allocations of 0.10 ± 0.04 and 0.26 ± 0.06 for proteins and lipids, respectively. These results complement and confirm those in Table 1.
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The fuel store in bivalves (lipids and/or complex carbohydrates) is used primarily for gametogenesis. A higher level of investment in storage is therefore expected to reflect an increase in gamete production. Preliminary evidence suggests that the unit metabolic costs of gonad growth are similar for both fast- and slow-growing individuals. Honkoop (2003)
has calculated that by suppressing gonad growth, rock oysters could increase somatic growth by as much as 64%.
The reduced costs of growth in oysters selected for fast growth are related to increased efficiency of protein deposition (EPD). The EPD is measured as the amount of protein deposited in growth as a proportion of protein synthesised. Protein synthesis carries a high metabolic cost of between 9 and 13 J mg protein–1 (Hawkins et al., 1986; Morgan et al., 2000; but see Marsh et al., 2001), and any metabolic "savings" on protein turnover are likely to be reflected in reductions in the overall energy costs of growth (Wieser, 2002). Reducing the costs of growth by increasing the efficiency of protein deposition is a common feature of intra-specific growth rate differences amongst bivalves (Hawkins and Bayne, 1992; Table 2).
Protein deposition is the difference between synthesis and breakdown which, together, comprise protein turnover. Deposition can therefore be increased either by an increase in protein synthesis, a reduction in breakdown, or a reduction in turnover that increases the difference between synthesis and breakdown (Carter et al., 1998). In both bivalves and fish, increased growth is mediated by reduced protein turnover rather than increased protein synthesis alone (Hawkins and Day, 1996; Morgan et al., 2000). The net result for fast and slow-growing oysters is a difference in the metabolic losses associated with protein growth, which range between 0.4 and 1.8 J J–1 protein deposited (Table 2).
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FLEXIBILITY IN FEEDING |
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As discussed above, quantitative differences in feeding behaviour contribute to the observed variability in growth, and these differences are strongly influenced by genotype. Feeding in bivalves is responsive to both the abundance and the composition of available food (Fig. 1). Abundance is usually measured as the mass of total suspended particles within a range of diameters appropriate to the species' filtration capabilities, and referred to here as total particulate matter (TPM). Measures of food composition include the particulate organic matter (POM) as a proportion of TPM (i.e., the organic content of the food, or OC).
The physiological processes and efficiencies that make up the feeding behavior of bivalves are regulated in response to changes in food availability, as documented in a large number of publications (e.g., Bayne, 1998; Cranford et al., 1998; Hawkins et al., 1998, 2001; Cranford and Hill, 1999; Navarro et al., 2000, 2003; Urrutia et al., 2001; Levinton et al., 2002; Brillant and MacDonald, 2003; Velasco and Navarro, 2003; Ward et al., 2003; for an alternative view see Clausen and Riisgård, 1996). The morphological basis for this flexibility is the subject of current research (Ward et al., 1998, 2003; Beninger and Venoit, 1999; Cognie et al., 2003). It exists both at the level of ciliary and mucous-producing systems that contribute to the regulation of feeding rate (Ward et al., 2003; Ward and Shumway, 2004) and in terms of the relative sizes of the feeding organs themselves (Honkoop et al., 2003). The relevant time-scales in the factors stimulating this flexibility range from tidal events such as sediment resuspension, to seasonal scales, over which changes in endogenous metabolic requirements are important.
This physiological flexibility is not without cost. The metabolic costs of digestion and absorption may amount to 15–20% of total energy expenditure (Widdows and Hawkins, 1989), and other costs are evident. For example, feeding in bivalves is significantly dependent on the secretion of mucus (Beninger and Venoit, 1999), some of which is lost within the pseudofaeces. Urrutia et al. (2001) argue that the balance between investment in mucus production and the gains that ensue from effective selection of food particles for ingestion may be a major determinant of bivalve feeding strategies. Mucus losses are also a factor in metabolic faecal loss, i.e., the loss of endogenous matter (including cell debris and protein secretions) that accompanies post-ingestive selection and the egestion of true faeces. Milke and Ward (2003) discuss other possible "time-costs" inherent in variable feeding behavior of bivalves.
Flexible feeding behavior enhances energy intake in response to changes in the food environment: to give just two examples, one pre- and one post-ingestive. Urrutia et al. (2001) conclude, from their work on the European cockle, Cerastoderma edule: "Cockles increase (food) processing rates when faced with an increase in particulate matter associated with a decrease in quality. Regulation of ingestion rate by high rates of rejection coupled to high rates of filtration leads to a significant increment in the organic fraction of ingested matter" (p. 184). The efficiency with which organic matter is absorbed from ingested food (AE) depends on the organic content of the food. Oysters (Crassostrea gigas) show a seasonal variability in this relationship which serves to maintain AE relatively unchanged in spite of a decline in the organic content of the seston (Bayne, 2002). The net result is an improvement by a factor of four in efficiency over a theoretical value with no compensation. Clearly, such flexibility in feeding behavior will be reflected in faster rates of growth. Genetically controlled increase in growth rates depend in part on faster rates of feeding, but is this at the expense of further behavioral flexibility?
The answer to this question appears to be "no." The results from a field study with S. glomerata (Table 3) confirmed that individuals from a line selected for fast growth had higher rates of filtration than non-selected individuals. During the two months of this experiment, the natural diet increased in abundance from 8.0 to 29.3 mg liter–1, but declined in organic content from 21% to 13%; water temperatures were similar on the two occasions (19.8 and 21.5°C). Oysters in both growth categories responded by increasing filtration rates, but the relative increase was greater for the selected, faster-growing oysters. In addition, whereas faster-growing individuals also increased selection efficiency, the slower-growing oysters did not. The benefit of these behaviors can be scaled as a ratio between the organic content of the ingested matter (OCI) and the organic content of the available suspended particles (OC). This ratio increased significantly in the selected oysters but did not change in the control group (Table 3). Absorption efficiencies did not differ significantly between growth categories, but increased from September to November. The net result was an increase in absorption rates between months, but the increase amongst the selected oysters was significantly greater than for the control group.
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DISCUSSION |
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Bivalve molluscs, in common with many other species, are predicted to show fitness benefits deriving from rapid somatic growth (Stearns, 1992
). Fecundity and reproductive effort increase sharply with size (Bayne et al., 1983). For many species there is a size-related refuge from predation, whether by starfish, crabs, gastropods or fish (Anderson and Connell, 1999). Nevertheless, evidence from genetic studies on selection for increased growth rate, in keeping with recent life-history models (Abrams et al., 1996), suggests that growth may be optimized rather than maximized, and that trade-offs occur with other fitness-related traits.
The trade-offs, however, are unlikely to be simple (Angiletta et al., 2003). Variations in patterns of energy allocation to different fitness traits may depend on differences in rates of energy acquisition (van Noordwijk and de Jong, 1986; Jokela and Mutikainen, 1995). Limits to specific metabolic efficiencies may force what Wieser (2002) has called different "strategic decisions," affecting both acquisition and allocation. To unravel these complexities requires careful case-by-case analysis (Billerbeck et al., 2001; Lankford et al., 2001). For example, "the primary mechanism for success of hybrid tadpoles is probably behavioral, through increased feeding time and food consumption, and not physiological via growth efficiency" (Rist et al., 1997, p. 735). For Drosophila, Moed et al. (1998) conclude (p. 169) "that differences in absorption rate are the main cause of both environmental and genetic differences in growth rate." In both Atlantic silverside (Present and Conover, 1992) and Atlantic salmon (Thodesen et al., 1999), increased growth rates are the result of both greater food consumption and higher growth efficiency.
Artificial selection for faster growth in Sydney rock oysters (S. glomerata) resulted in an increase in age-related size of up to 22% (Nell et al., 1998; Bayne et al., 1999b). Two lines of Pacific oysters (C. gigas) differed by 40% in their rates of growth (Bayne, 1999), and age-related size of inbred and cross-bred progenies of three families of this species differed by as much as 50% (Hedgecock et al., 1996). In all of these cases faster growth was associated with increased rates of feeding and reduced metabolic expenditure. Slow-growing individuals have a larger energy requirement for maintenance and a higher cost of growth than faster-growing conspecifics. In S. glomerata there is also an allocation trade-off between growth and lipid storage which probably reflects earlier reproduction amongst slow growers; this is a "disproportionate effect" on the energy budget (Wieser, 1994), comprising both an increased energy input and altered energy allocation.
Constraints in feeding behavior, particularly particle selection and rejection, may force a trade-off between feeding performance on particles of high and low organic content, but there is no evidence to date that the faster rates of energy acquisition associated with increased growth rate act to constrain behavioral flexibility. We do not yet have a full functional explanation for selection-dependent differences in feeding behavior. Recent studies by Ward et al. (2003) and Milke and Ward (2003) show the way forward (see review by Ward and Shumway, 2004). These demonstrate that differential control of particle transport on the main feeding organs determine, at least in part, the capacity of different species to regulate feeding behavior in compensation for changes in the food. These are likely to be the proximate processes that also respond to selection. Milke and Ward (2003) suggest the possibility that time-costs associated with particle selection may impose a fundamental constraint on the pre-ingestive feeding processes. The challenge is to relate these studies to aspects of feeding flexibility that underpin genotype-dependent aspects of performance.
A large component of the observed differences amongst growth categories in the efficiency and metabolic costs of growth are due to aspects of protein synthesis and turnover. The costs of protein turnover contribute significantly to metabolic rate (see review by Hulbert and Else, 2000), and there appears to be considerable metabolic scope for modifying the net cost of protein turnover during growth, and so effecting changes in growth efficiency (Hawkins and Bayne, 1992). Reduced maintenance costs, coupled with increased efficiency of protein synthesis, yield a significant increase in growth potential within the constraints of a balanced energy budget. The consequences of shifting the balance between protein synthesis and breakdown, in terms of potential physiological trade-offs, remain to be resolved, although responses to some stresses, and the efficiency of repair processes, may favor higher rates of turnover (Hawkins, 1991; Houlihan et al., 1994).
Seasonal factors of changing metabolic demand may also be important. For example, in mussels (M. edulis) rates of whole-body protein turnover per unit tissue protein were significantly increased in the spring, when the demand for nitrogen, in the later stages of the seasonal cycle of gametogenesis, was high. To quote Hawkins and Bayne (1991), under these conditions "there was a need for enhanced mobilization and catabolism of structural protein (and) presumably, faster protein turnover was incurred as a regulated response ... enabling the preferential catabolism of non-essential amino acids" (p. 185). Taken together with evidence of metabolic adaptations which control the relative anabolic and catabolic fates of exogenous protein (Kreeger et al., 1995), these results suggest a highly plastic set of traits of nitrogen metabolism. It may be that selection for reduced protein turnover, with a consequent reduction in the metabolic cost of growth, may actually be disadvantageous at a time when internal recycling of protein is needed to complete gametogenesis, so compounding the trade-off between growth and reproduction. When food is scarce but the nutritional demands of gametogenesis are high, tissue protein is the main contributor of energy in both mussels (Gabbott and Bayne, 1973) and oysters (Whyte et al., 1990).
An underlying feature of flexibility in both feeding behavior and the metabolic efficiencies of maintenance and growth is the strong implication of linkage between the individual, proximate, processes. This suggests in turn the existence of a smaller number of controlling processes, both endocrine (e.g., Dufty et al., 2002) and otherwise, that determine the form of the relevant reaction norms. Research to describe the proximate processes that are amenable to selection and evolutionary change should seek at the same time to determine the part played by these controlling factors.
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ACKNOWLEDGMENTS |
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I am grateful to the Research Centre on Ecological Impacts of Coastal Cities, the Director Tony Underwood and Deputy Director Gee Chapman, for their kind support and encouragement, and to the technical staff. The University of Sydney and the Australian Research Council provided financial support. My particular thanks go to Pieter Honkoop for his collaboration in many of the studies which underpin this paper, to Peter Cranford for permission to use his original diagram, slightly modified, as my Figure 1, and to Mike Angiletta for inviting me to contribute to this symposium.
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FOOTNOTES |
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1 From the Symposium Evolution of Thermal Reaction Norms for Growth Rate and Body Size in Ectotherms presented at the Annual Meeting of the Society for Integrative and comparative Bioloigy, 5– 9 January 2004, at New Orleans, Louisiana.
2 Present address: 16 Lockington Avenue, Plymouth PL3 5QR, England; E-mail: baynebrian{at}hotmail.com
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