MARINE ECOLOGY PROGRESS SERIES Vol. 171: 71-84, 1998 Published October 1 Mar Ecol Prog Ser
Comparative effects of microalgal species and food concentration on suspension feeding and energy budgets of the pearl oysters Pinctada margaritifera and P. maxima (Bivalvia: Pteriidae)
'Department of Zoology and Tropical Ecology, School of Biological Sciences, James Cook University, Townsville, Queensland 481 1, Australia 2~ustralianInstitute of Marine Science, PMB 3, Townsville MC. Queensland 4810, Australia 3Departrnent of Aquaculture. School of Biological Sciences, James Cook University, Townsville, Queensland 481 1, Australia
ABSTRACT- This study aimed to determine the influence of microalgal species and food concentration on various physiological parameters and Scope for Growth (SFG) in adults of 2 pearl oysters, Pinctada margantifera and P maxima. Clearance rate, pseudofaecal production rate, absorption efficiency, res- piration rate and excretion rate were determined over a range of food concentrations using 2 microalgal diets, Tah~tian Isochrysis sp. (T-Iso) and Dunaliella primolecta at 28'C. Clearance, pseudofaecal pro- duction and respiration rates were significantly affected by microalgal diet. From these results, and because of the higher energy content of T-Iso, pearl oysters feeding on T-lso had maximum values of SFG that were 1.5 to 2 1 times higher than when feeding on D. pnmolecta. Clearance rate and absorp- tion efficiency were significantly related to food concentration as negative exponential relationships (p c 0 001). Generally, pseudofaecal production, respiration and excretion rates were significantly related to food concentration as positive linear relationships (p < 0.005) Optimal food concentrations for max~mumSFG for P margarjtifera and P maxima were 1 to 2 mg I-' and 2 to 3 mg I-', respectively. P. maxima was better adapted to a wider range of food concentrations. P. maxima maintained positive SFG up to 9 mg I-' food concentration when feeding on T-lso and up to 7 mg I-' when feeding on D. primolecta, while equivalent values for P. margaritifera were 7 mg 1-' and 5 mg I-',respectively. Thesc results are in accordance with P. maxin~aoccurring in a wider range of habitats than P margaritiferd, and experiencing greater concentration ranges of suspended particulate matter
KEYWORDS: B~valve. Pinctada marydritifera Pinctada maxima Food Suspension feeding Scope for Growth Energy
INTRODUCTION bivalves (the exception is giant clams). These studies of temperate bivalves aimed to better understand their Food concentration and microalgal diet are major ecophysiology and trophic roles in aquatic ecosystems factors influencing the growth and reproduction of (Tenore & Dunstan 1973a, b, Widdows et al. 1979, suspension feeding bivalves. The relationships between Navarro et a1 1992, Hawkins et al. 1996). Some also suspension feeding and energy budget versus food sought to determine optimum food conditions for aqua- concentration and food quality have been well studied culture purposes (Tenoi-e & Dunstan 19?3a, b, Kirby- in temperate bivalves, but not generally in tropical Smith & Barber 1974, Navarro & Winter 1982, Beiras et al. 1993, 1994, Navarro et al. 1996). In particular, energy balances obtained for various microalgal diets 'Addressee for correspondence. and concentrations are of interest for bivalve aquacul- E-mail: [email protected] ture because pure cultures of unicellular microalgae
O Inter-Research 1998 Resale of full artlcle not pernlitted 7 2 Mar Ecol Prog Ser 171: 71-84. 1998
are widely used as food for rearing larvae and spat, appropriate to examlne the effects of microalgal spe- and for broodstock maturation. However, in spite of cies and food concentration on feeding and energy comparisons of nutritive values of microalgae (Finlay & budgets of P. margaritiferaand P. maxima. Uhlig 1981, Pillsbury 1985, Helm & Laing 1987, Whyte Effects of various algal diets and concentrations on 1987) and growth rates of bivalves (Walne 1970, Helm feeding rates (Hayashi 1983), larval growth (N~shimura 1977, Ewart & Epifanio 1981, Langdon & Waldock 1980), and spat growth (Wada 1973, Okauchi 1990) 1981) on various diets, the way that different micro- have been examined for the Japanese pearl oyster algal diets influence feeding (filtration, pseudofaeces Pinctada fucata martensii.However, there has not production, ingestion and digestion) and energy bal- been a comprehensive study of the effects of food spe- ance has not been fully appreciated. Thus, studies of cies and concentration on feeding and energy budgets the influence of microalgal diet and concentration on of a Pinctadaspecies. The first aim of the present study feeding and energy balance of commercially important was therefore to compare the suspension feeding bivalve species can provide useful information for both (clearance, pseudofaeces production and absorption ecology and aquaculture. rates) and energy budgets (absorbed, respired and Pinctada margaritiferaand P. maximaare economi- excreted energy) of P. margantiferaand P. maxima cally important bivalves, as well as being typical sus- feeding on 2 microalgae species over a range of food pension feeders occurring in tropical waters. They are concentrations. The second was to consider whether among the largest species of pearl oysters (Bivalvia: the results on feeding and energy budgets are related Pteriidae) and are used extensively in cultured pearl to differences between habitats of these pearl oyster production (Doumenge et al. 1991, Shirai 1994). They species. The energy budgets of the pearl oysters were tend to occur in different habitats. P. margaritiferais summarised in the parameter Scope for Growth. found in greatest numbers in the oligotrophic waters of atoll lagoons; it tends to be excluded from turbld waters (Tranter 1959). On the other hand, P. maxima MATERIALS AND METHODS inhabits a variety of areas, from seagrass beds to deep- water 'reefs' on substrates varying from mud to sand The techniques used in this study were similar to and gravel (Kailola et al. 1993). Its inshore habitats those of Yukihira et al. (1998). All experiments were may have considerable terrigenous sediment, and sub- carried out at 28 + 0.5"C. stantial nutrient inputs and productivity levels (Gervis Pearl oysters. Large Pinctadamaxima (132 to 237 mm & Sims 1992). The distribution of P. maximasuggests shell height, n = 30) and P. margaritifera(121 to 180 mm that it will experience a wide range of concentrations shell height, n = 40) were put into pocket nets (Gervis of suspended particulate matter (SPM). SPM may also & Sims 1992) kept at ca 1.5 m depth suspended be high in its inshore habitats, with SPM quality from a pontoon at Cape Ferguson, Australian Institute depending on meteorological and tidal conditions. The of Marine Science, North Queensland (19" IS'S, 2 oyster species inhabit such different waters that food 147" 05'E). They were acclimated to these conditions particle concentration and food quallty should be im- for at least 3 wk before use in all experiments. Water portant factors for their ecology and energetics. The 2 temperature varied from 26.0 to 29.5"C over the species may correspondingly show different patterns study period. The shells of all oysters were thoroughly of energy gain and expenditure over various food cleaned of epibiota during the acclimation period and concentrations and types. were re-cleaned the day before use in experiments. Scope for Growth (SFG, J h-') is a measure of the After the completion of each experiment, shell height energy available to the animal for growth and repro- (SH, mm), which is the greatest distance from the duction (Warren & Davis 1967, Bayne & Newel1 1983, umbo to the bottom of a finger or growth process, was Griffiths & Griffiths 1987). Yukihira et al. (1998) de- recorded. Measurements of feeding, respiration, and monstrated that in simulated oligotrophic conditions excretion rates and food absorption efficiency were (0.5 mg 1-' Tahitian Isochrysissp.), Pinctada margari- performed as described below on a sample size of 30 to tifera and P. maximaboth had high clearance rates 40 oysters. (CR) and high values of SFG compared to most other Microalgae. Two unicellular microalgal species, bivalves, including bivalves feeding on higher food Tahitian Isochrysis aff. galbana Green (T-Iso) and concentrations. It appears that both species are capa- Dunaliella primolectaButcher, were separately used ble of growing and reproducing under conditions of as food suspensions. These algae were selected for low food supply. This is most notable for P, maxima their range of cell size (4 to 8 pm) and because they are because its habitats may have high levels of SPM. used in mariculture, or resemble natural phytoplank- Thus, following on from these findings for a low con- ton (T-Iso). The energy contents of the microalgae centration of one microalga (Yukihira et al. 1998), it is were determined using a Parr 1421 semi-micro oxygen Yukihlra et al.Effect of food on oyster energy budgets 13
bomb calorimeter (following Whyte 1987).Experiments excretion rate (see below). Samples were filtered onto were conducted over an algal concentration range pre-rinsed-and-ashed GF/C filter papers, rinsed with between 0 (= no food) and 11 mg dry wt 1-' uslng algal distilled water, dried and ashed at 450°C for 5 h. Food cells from cultures in their logarithinic growth phase. san~plesconsisting of 2 1 samples of water and algae Clearance rates. The volume of water each oyster were collected from the control chamber and treated in cleared of particulate material (CR, l h-') was deter- the same way. mined using a flow-through system in which 0.45 pm Respiration rate. Respiration rates (R, m1 h-') were filtered seawater containing a constant concentration determined in 4 sealed chambers using YSI dissolved of algal food was allowed to run through a set of 4 oxygen electrodes (Model 55). Three sizes of cham- chambers. Three of these contained an oyster, while bers, 2, 5 and 13 1, were used to hold the oysters, ac- the remaining one acted as a control. From the flow cording to size. Before the experiments, oysters were rate (F, 1 h-'), and the concentrations of algae immedi- fed the appropriate food concentration for at least 2 h ately surrounding each oyster (Co),in the outflow of in a 100 1 tank with aeration. Then 3 oysters were control chamber (C,)and in the outflow of each exper- placed individually into sealed chambers with 0.45 pm imental chamber (C2),clearance rates were calculated filtered seawater and algal food at the appropriate from the following equation (after Hildreth & Crisp concentration. The fourth chamber served as a control. 1976): Water in each chamber was thoroughly mixed by a magnetic stirrer. A mesh platform separated oyster CR (l h-') = F (CI C2)/C0 - from stirrer bar. Oxygen concentration in each cham- Two chamber volumes, 6 and 18 1,were used to hold ber was monitored at 5 min intervals. Preliminary the oysters according to their size. A constant flow rate research revealed that both species took at most between 25 and 35 1 h-' was maintained during the 15 min to stabilise in the conditions of the respirometer experiment. Oysters were placed in the flow-through chamber. Since the clearance rates of the oysters were chambers and kept undisturbed. Measurements were quite high compared to the chamber volumes, which commenced at least 1 h after they showed enough meant that the animals would quickly deplete the food gape as evidence of feeding. Algal concentrations suspension in the chamber, recordings were restricted were measured at 1 h intervals (means of 5 counts) to the first 10 or 15 min after the initial equilibration using a high-speed particle counter (Coulter M.ulti- period. R was determined after Bayne et al. (1985). sizer) with a 140 pm orifice tube. The ration level of Excretion rate. The rate of ammonia excretion each oyster was expressed as a mean value of C,. (E,mg NH,-N h-') was determined on the completion Pseudofaeces. Pseudofaeces is uningested material of CR measurements. Oysters were carefully trans- that is rejected from the labial palps. Both oyster ferred into another set of 4 chambers containing species tended to produce mucus-like, fragile masses 0.45 pm-filtered seawater. Three of these contained an of pseudofaeces at the higher food concentrations. oyster, while the remaining chamber acted as a con- These were distinguished by their colour and texture trol. Oysters were kept undisturbed for 60 to 90 min from faeces, which were darker-coloured ribbons or according to the volume of water and the oyster's body pellets. Deposited pseudofaeces were carefully col- size. Duplicate samples (10 ml) were collected from lected from each chamber during and on completion of each chamber and filtered through a 0.45 pm Sartorius experiments. Pseudofaecal production was quantified minisart filter and frozen until assaying. Analyses for by filtering samples onto pre-rinsed-and-ashed GF/C ammonia content were conducted using the phenol- filter papers, rinsing with distilled water, drying, and hypochlorite method of Solorzano (1969). ashing at 450°C for 5 h. Proportion of pseudofaeces to Size standardisation of CR. R and E. The dry tissue total food filtered (PF, %) was then calculated. weight of each experimental oyster was calculated Absorption efficiency. The percentage of food con- from shell height (SH) using the SH-tissue weight rela- sumed that was then absorbed was determined by tionships determined in a previous study (Yukihira et comparing the fraction of faeces lost on ashing with al. 1998). CR, R and E were standardised to that of a that of samples of food suspension treated in the same specimen of 10 g dry tissue weight (wt) to allow com- way. Absorption efficiency (abs.eff., %) was then cal- parisons according to the equation: culated according to the equation of Conover (1966): Ys = (Ws/We)'. Ye (Navarro et al. 1991) where Ys = size-standardised physiological rate, Ws = where f and e are the fractions of food and faeces lost standard size (dry tissue weight) = 10 g, We = dry tissue on ashing, respectively. wt of animal, b = size-weight exponent, and Ye = uncor- Collection of faeces from the chambers was carried rected physiological rate. Table 1 shows b values used out on completion of the measurements of CR and for the standardisation of CR, R and E of both species. 74 Mar Ecol Prog Ser 171: 71-84, 1998
Scope for growth. Absorbed energy (AE,J h-') was calculated as follows: %- P. margaribfera -@- P. maxima AE = CR(1 -PF)(abs.eff.)(energycontent of the algal food) food: T-ISO Relationships between AE and food concentration were expressed by polynomial regression curves. Re- spired energy (RE,J h-') and excreted energy (EE,J h-') were calculated after Bayne et al. (1985) Scope for Growth (SFG,J h-') was determined using the equation: SFG (J h-') = AE - (RE + EE) Data analysis. When the regression analysis showed that CR, PF, R, abs.eff. and E were correlated with in- creasing food concentration, differences in these para- 0a, meters between oyster species and microalgal diet S food: D. pnmolecta were examined using ANCOVA with food concentra- 03 tion as the covariate. Since R of Pinctadamaxima was independent of ration level, the effect of microalgal diet was tested using l-way ANOVA. Predicted mean values from regression equations and their 95 % confi- dence limits (95% CL) for AE and RE were used to assess differences in SFG values between the 2 micro- algal diets and 2 oyster species.
RESULTS 0 2 4 6 8 10 Microalgae Food concentration (mg I-') Fig. 1. Pinctada margaritifera and P. maxima. Clearance rate T-Iso had a mean diameter of ca 4.5 pm and con- versus food concentration for oysters feeding on Tahitian tained 20.27 J mg-' dry wt. Dunaliella primolecta was Isochrysis sp. (T-Iso) (top) and Dunaliella primolecta (bottom). larger (ca 7.0 pm) and contained less energy: 15.06 J Each data point is the rate for a single oyster, standardised to 10 g dry tlssue wt. Regression, equations are in Table 2 mg-' dry wt.
Clearance rates creased significantly more than that of P. maxima Clearance rates (CR, 1 h-') of both oysters were sig- (Fig. 1, Table 3a). CRs of oysters feeding on Dunaliella nificantly, negatively correlated with food concentra- primolecta decreased significantly more with increas- tion (Fig. 1). Relationships between CR and food con- ing FC than the CRs of oysters feeding on T-Iso (Fig. 1, centration (FC, mg I-' dry wt) were best described Table 3c, d). Thus, the relationships between clear- by exponential functions (Table 2). Slopes of the re- ance rate and food concentration reflected both micro- gresslons of clearance rate on food concentration algal species and oyster species. differed significantly between oyster species and be- We observed that :he shell gape of both oyster spe- tween microalgal diets (Table 3). With increasing food cies tended to decrease at higher food concentrations, concentration the CR of Pinctada margaritifera de- and the gills were never observed to extend beyond the shell margins. (Similarly, Palmer [l9801 and Palmer Table l. Pinctada margantlfera and P. maxima. Size-rate ex- & Williams [l9801 found that high clearance rates in ponents (b values) ot clearance rate (CR, 1 h-'), respiration scallops at low food concentrations were typically rate (R,m1 o2h-') dnd excretion rate (E,mg NH4-Nh-') (from reflected in a wide shell gape.) Yukihira et al. 1998)
Species Weight (g) CR R E Pseudofaecal production P. margaritlfera 0.043-12.83 0.613 0.439 0.642 P maxima 0.044-20.39 0.613 0.561 0.789 Relationships between pseudofaecal production (PF, % of total food filtered) and FC were described by Yukih~r~~et al.: Eff~ctof food on oyster energy budgets 75
Tdhle 2. Pinctada margal-~tjfera and P. maxjma. Relationships between clear- linear functions (Table 2). PF, although ance (lh.'), pseudofaecal production (":, of total food filtered), ahsorpt~on elii- showing considerable variability, In- ciency (':#S),respiration (m1 O? h-')and excretion rates (nqNH,-N h-!),and food creased s~gniflcantly with increasing concentration (FC, mg rnl-' dry wt) of oysters feeding on Tahitidn Isochrysis sp [T-lso) or Dunaliella prin~olr,cta food concentration (Fig. 2).When the 2 oyster species were compared, slopes of the regressions of pseudofaeces Function Pearl oyster species Microalgae species P. rnargaritifera P maxima production on food concentration were found to be significantly different for Clearance rate (CR) Dunaliella primolecta but not for T-Iso T- SO C'R = 56.67 X 10.' "" CR = 47.00 X 10 "'""'- (Table 3a, b). However, the intercepts (r'=074,n=50,p<0.001) (r2=0.90,n=43,p<0.001) differed, significantly between the oys- D. primolecta CR = 58 31 X 10-"""' CR = 49.81 X 10-0 ~>i:"- (rL=0.89,n=45, p<0.001) (r2=0.91,n =33, p Table 3 Summary of ANCOVA testing for similarity In slopes and intercepts of regression lines of clearance rate (CR, l h-'), pseudofaecal production (PF, ";, of Absorption efficiency (abs.eff.,%) filtered material), absorption efficiency (abs.~ff.,'';>) and excretion rate (E, mg NH,-N h-') versus food concentration (mg 1' dry tvt) in pearl oyster Pinctada margaritifera dnd P. niaxima, and food Tahitian lsochrysis sp. (T-lso) and Relationships between abs.eff. and Dunalielld pnmolecta. Whtn there was no significant difference In slope, then food concentration (FC) were best difference in intercept was tcstcd. ns: not s~~jn~f~cantat p 0.05; 'p < 0.05; "p < described by the exponential functions 0.01; "'p < 0.001 (Table 2). Abs-eff. declined signifi- cantly with increasing food concen- C R - P F abs eff. E tration (Fig 3) Slopes or interccpts of (a) Comparison between P. margar~lifera and P. maxima feeding on ?'-Is0 the regressions of abs.eff, on food con- Slopes ns ns centration varied significantly be- Intercepts .. . ns ns tween oyster species and microalgal (b) Comparison between P mdrganhfera and P maxima feeding on D. primolecta diets (Table 3). Pinctada maxima had S.. Slopes .. n S ns higher abs.eff. than P. margaritifera Intercepts .. . ns regardless of diet. P. maxima had (c) Cornpalison between T-Iso and D. primolecta fed on by P margar~tifera higher abs.eff. of Dunaliella PI-imo- Slopes .. . ns . . ns lecta compared to T-Iso at all food Intercepts .. n s concentrations. P. margaritifera had (d) Comparison between T-Iso and D. prirnolecta fed on by P. maxima higher abs.eff. when feeding on D. PI-i- Slopes .. . ns ns ns molecta compared with T-Iso, except lntercepts ns .. ns at food concentrations below about 2 mg I-'. 7 6 Mar Ecol Prog Ser 171: 71-84, 1998 food: T-ISO 0 ++ P. margaritifera .- -0.. P. maxima food: D. primolecta 0 2 4 6 8 10 Food concentration (mg I-') Fig. 2. Pinctada margaritifera and P. maxima. Pseudofaecal production ("Lof total food filtered) versus food concentration for oysters feeding on Tahitian Isochrysis sp. (T-Iso) (top) and Food concentration (mg I-') Dunaliella primolecta (bottom). Each data point is the rate for a single oyster, standardised to 10 g dry tissue wt. Regression Fig. 3. Pinctada margan'tifera and P. maxima. Absorption equations are in Table 2 efficiency versus food concentration for oysters feeding on Tahitian Isochrys~ssp. (T-Iso) (top) and Dunaliella primolecta (bottom). Each data point is the rate for a single oyster, stan- Absorbed energy (AE) dardised to 10 g dry tissue wt. Regression equations are in Table 2 Relationships between AE and FC were best ex- pressed by fourth-power polynomial regressions (Fig. 4). Pinctada margantifera(T-Iso) Predicted mean values of AE and 95% confidence AE = 32.2 + 589.6FC limits (95%CL) corresponding to 1 to 10 mg FC 1-Lare + (-253.2)FC2+ 37.3FCR+ (-1.85)FC4 (1) shown in Table 4 Both pearl oysters feeding on T-Iso (r2= 0.82,n = 49, p < 0.001) and Dunaliella prirnolecta displayed maximum values P. margaritifera(Dunaliella primolecta) of AE within the range 1 to 3 mg 1-'. The 95 O/oCL val- AE = 38.6 + 364.OFC ues show significant effects of food species concentra- + (-20.43)FC2+ 39.0FC3 + (-2.49)FC4 (2) tion on AE of both pearl oysters. These effects were: (r2= 0.76, n = 45, p < 0.001) (1) at food concentrations of 0.5 to 4.5 mg 1-' (Pinctada P. maxima (T-Iso) margantifera)and 0.5 to 6.0 mg 1-I (P. maxima),pearl AE = 97.8 + 403.6FC + (-121.0)FC2 oysters feeding on T-Iso had higher AE values than + 12.5FC3+ (-0.45)FC4 (3) those feeding on D. prirnolecta, and (2)P. maxima had (r2= 0.81, n = 43, p < 0.001) higher AE at 2.5 to 6.0 mg I-' (T-Iso)and 1 to 4.5 mg 1-' P. maxima (D.pnrnolecta) (D.primolecfa) than P. margantifera.Except for these AE = 88.9 + 322.2FC food concentration ranges, there were no significant + (-125.0)FC2+ 16.1.6FC3+ (-0.70)FC4 (4) differences in AE values between oyster species or (r2= O,??,n = 33, p < 0.001) food species. Yukihira et al.: Effect of food on oyster energy budgets 7 7 RE and 95 % CL of predicted mean RE for P. maxima the comparison between microalgal diets. To compare RE and 9500 CL between the oyster species feeding on the same food, the following regressions for Pinc- tada margaritiferawere used: T-ISO R = 2.80 (+ 0.496) + 0.264 (+ 0.136)FC (7) Dunal~ellaprimolecta 600 R = 1.81 (i 0.406) + 0.238 (k 0.084)FC (8) Q) P. margaribfera P. maxima Calculated respired energy (RE, J h-') 500- D. primolecta - D. primolecta 2 and 95 % CL are shown in Table 4. 0a 400- Excretion Relationships between excretion rate (E, mg h-') and food concentration were expressed by linear functions (Table 2). I'I11'l11' 02468100246810 E varied considerably, but ,increased Food concentration (mg I-') significantly with increasing food con- centration (Fig. 6). However, neither Fig. 4. Pinctada margaritifera and P. maxima. Relationships (regression slopes nor intercepts of the regressions curves and 95% conf~dencecurves) between absorbed energy and food of E on FC varied significantly between concentration for oysters feeding on Tah~tianIsochrysis sp. (T-Iso) (top) and Dunallella primolecta (bottom). Each data point is the rate for a oyster species nor between microalgal single oyster, standard~sedto 10 g dry tissue wt. Regress~onequations diet (Table 3). Therefore, all data were are in Table 2 pooled and a common regression was determined: Respiration E = 0.306 + O.11OFC (r2= 0.42, n = 133, p < 0.001) There were linear relationships between respiration (R,m1 O2 h-') and FC (Table 2). Respiration rate of Excreted energy (EE, J h-') was calculated using this Pinctada margaritiferaincreased significantly with equation (Table 4). increasing food concentration (Fig. 5, Table 5), but respiration rate of P. maxinla was not significantly affected. Therefore, the mean R values for P. maxima Scope for Growth were compared between the microalgal diets. P. max- ima had significantly higher R when feeding on T-Iso Scope for Growth (SFG)values for Pinctadamargari- than on Dunaliella primolecta (Table 5, ANOVA, p tifera and P, maxlma feeding on T-Iso and Dunaliella 0.01). These mean values of R were used to calculate primolecta were determined from calculated AE, RE RE (J h-') and 95 S:)CL values for P. maximain Table 4. and EE values (Table 4). Considering 95 % CL for Slopes of regression lines of R versus FC for Pinctada AE and RE, P. maximafeeding on T-Iso and D. primo- margaritiferawere not significantly different for the lecta had distinctly higher SFG than P. margaritifera 2 diets, but intercepts were significantly different throughout ration levels 3 to 6 mg 1-' T-Iso and 2 to 4 my (ANCOVA, p c 0.01). Therefore relationships between 1-l D. pr-imolecta,respectively. P. maryaritiferaand P. R and FC for P. margaritiferawere re-expressed as maximafeeding on T-Iso had higher SFG than when follows: feeding on D. primolecta over food concentration T-ISO ranges 1 to 4 mg 1-' and 2 to 6 mg I-', respectively. P. margar~tiferaand P. maxima feeding on T-Iso had R = 2.80 (k0.496) + 0.247FC, (5) 2.1 times (387,183 J h') and 1.5 times (423,280 J h-') Dunaliellapnmolecta higher maximum SFG values, respectively, than those R = 1.81 (* 0.406) + 0.247FC, (6) feeding on D. primolecta.The highest SFGs of P. mar- where figures in parenthesis are 95 % confidence lim- garjtiferaand P. maximafeeding on the 2 diets were at its (95 ?4 CL). These regressions were used to calculate approximate1.y the following food concentrations: Table 4. Pinctada rnargilrit~f~raand P maxima. Predicted mean values of absorbed energy (AE),respired energy (RE),excreted energy (EE)corresponding to different food concentrations (1 to 10 rng l l) and food specles, Isnchrysis sp. Tah~tlan(T-lso) and Dunaliella primolecta, and resultant scope for growth [SFG - ,\E - (RE + EE)].95'K confi- l dence lin~~ts(95'%, CL) are also shown lor AE dnd RE. There was no s~gnificantdifference in EE between pearl oyster species or w~thfood species. Significant differences in SFG values are lnd~catedby: "between oyster species on T-[so, "between oyster species feeding on D. prlmolecla; 'between food species for P. margdrjtifef-a;"between species for P. maxima Pard- Species Source Food concentration rneter 1rngI' 2 mg l'.' 3rngI' 4mgI' T-lso D. pr~molecta T-lso D, prjmolecta T-Iso D, pri~rlolecta T-lso D. pr~nlolecta - AE P r~~argar~tlferaEqs. (1)& (2) 404 235 467 222 379 143 253 84 (J h '1 95% CL (370,430) (213, 254) (430, 501) (195, 244) (330, 420) (111, 173) (200, 302) (48, 114) P. maxlnla Eqs (3)& (4) 392 302 514 351 521 310 461 233 95% CL (353, 429) (270, 329) (465, 562) (317, 384) (480, 569) (263, 358) (423, 499) (177. 287) RE P margaritlfeld 1 Ecls. (5)& (6) (RE1) 62 42 67 47 72 52 77 57 (J h ') 95% CL (52, 72) (34. 50) (57, 77) (39, 55) (61, 82) (44, 60) (67, 87) (49, 65) P ~nargarrlifera2 Eqs. (7) & (8)(RE2) 62 42 68 47 73 5 1 78 56 95% CL (49, 75) (32, 52) (52, 83) (35, 58) (55, 91) (38,65) (57, 100) (47, 71) P. rlldsrnla From 'Table S 81 58 8 1 58 8 1 58 81 58 95':L C:L (71,92) (49,67) (71. 92) (49,67) (71, 92) (49, 67) (71, 92) (49, 67) E E Both sl)c.c~es 10 10 13 13 16 16 19 19 (J h 'l SFG P margaritilera SFG = 4E - RE1 - EE 332' (J h '1 SFG = I\E - RE2 - EE 331 P n~axima SFG: 4E-RE-EE 301 Food concentration 5 mcJ I-' 6 my I-' 7 mg 1.' 8 mg 1.' 9 mg I-' 10 111y 1- I T-Iso D. pr-imolecta T-Iso D. prjrnolecta T-lso D. prirnolecla T-lso D. primolecta T-Iso D. primolecla T-lso D. primolecta l56 7 0 114 65 105 64 (82, 217) (21. 109) (-5, 204) (17, 96) (-20, 185) (-45, 114) 372 157 280 105 20 1 8 1 139 34 (329, 421) (102, 210) (235, 336) (48, 159) (155, 266) (-3, 149) (95, 224) (3, 165) 8 2 62 87 67 92 72 97 77 107 87 (72, 92) (54, 70) (77, 97) (59,75) (82, 102) (64, 80) (87, 107) (69, 85) (97. 117) (79. 95) 84 61 89 66 95 7 1 100 76 111 85 (60, 108) (44, 78) (63. 116) (47, 84) (65. 124) (50, 91) (68, 132) (54, 98) (73, 148) (60, 111) 58 81 58 81 58 8 1 58 81 58 1 7 (49, 67) (l2 (49, 67) (71, 92) (49, 67) (71, 92) (49, 67) (71,921 (49,67) 2 1 2 1 24 24 27 27 30 30 35 35 53 - 13 3 -26 -14 -62 51" -13 l" -25 -17 -65 269cLC1 78" 1 7 5~3,tI 23" 93 -3 29 -24 -83 l Yukihira et al.: Effect of food on oyster energy budgets 7 9 2 1 food: T-lso food: T-lso + P. margaritifera -0.- P. maxima -e- P. margaritifera P. maxima C ? 2 ." ." food: D. primolecta 2 food: D. primolecta a, 'G l 0 2 4 6 8 10 Food concentration (mg I-') Food concentration (mg I-') Fig 5. Pinctada margaritifera and P maxima Respiration rate Fig. 6, Pjnctada ~nargaritifera and P maxima. Excretion rate versus food concentration for oysters feeding on Tahit~an versus food concentration for oysters feeding on Tahitian lsochrysis sp. (T-Iso) (top)and Dunaliella pnmolecta (bottom). Isochrj~s~ssp. [T-Iso) (top)and Dunaljella primolecta (bottom). Each data point is the rate for a single oyster, standardised to Each data point is the rate for a single oyster, standardised to 10 g dry tissue wt. Regression equations are in Table 2 10 g dry tissue wt. Regression equations are in Table 2 P. margaritifera: 2 mg 1-l (T-Iso),1 mg 1-' (D.primolecta) Thus, Pinctada n~axima maintained positive SFG P. maxima: 3 mg 1-I (T-Iso), 2 mg I-' (D. primolecta) over a wider range of food concentration than P. mar- garitifera. Above these peaks, SFG declined to below zero with increasing food ratlon level. The approximate upper threshold concentrations beyond which SFG values DISCUSSION became negative were: Effects of food concentration on energetics P. margaritifera: 7 mg 1-' (T-Iso)and 5 mg I-' (D.primolecta) P,n7ama: 9 mg 1-' (T-Iso)and 7 mg l-' (D.primolecta) At high algal concentrations, suspension-feeding bi- valves generally decrease clearance rates (Winter 1978, Table 5. Pinctada maxima. Mean respiration rates (R,m1 0, Griffiths 1980) and absorption efficiency (Van Wee1 h-') and 95'!Kj confidence limits (CL) of oysters consuming 1961, Thompson & Bayne 1972, Griffiths & King 1979, various concentrations of Tahitian Isochrysis sp. (T-Iso) and Dunal~ella prjlnolecta Food species has a signif~cant effect Griffiths 1980, Bayne et al. 1989, van Erkom Schurink & on R (ANOVA,p < 0.01) Griffiths 1992), and increase pseudofaeces production (Foster-Smith 1975, Bayne & Worrall 1980). This study Food species Food concentration n R (CL) of 2 tropical pearl oysters demonstrated similar trends (mgI-') (Figs. 1, 2 & 3). Consequently, their absorbed energy (AE) was also strongly affected by increasing food T- SO 0-31.4 28 4.00 (* 0.513) D. pnmolecta 0-10.9 22 2.86 (+ 0.458) concentration (Fig. 4).Both Pinctada margarjtifera and P. maxima controlled the total amount of material in- Mar Ecol Prog Ser 171. 71-84, 1998 gested in varying food environments by a combination Pinctada margaritifera. D. primolecta was not as good of altering thelr clearance rates and the amount of a food for pearl oysters as T-Iso at any ration level and material rejected in pseudofaeces. This agrees with ob- the disparity increased at higher ration levels (Table 4). servations for the sub-tropical pearl oyster Pinctada These effects of the microalgal species on the pearl imbricata (Ward & MacDonald 1996). oysters' feeding and metabolism were similar to other Pinctada margaritifera and P. maxima have distinctly studies that demonstrated effects of diet on feeding different patterns of feeding and energy budgets. Yuki- in bivalves. Tenore & Dunstan (1973b), for example, hira et al. (1998) demonstrated that P. maxima had demonstrated that clearance rate of Crassostrea vir- higher absorption efficiency (abs.eff.)than P. margari- ginica was influenced by different microalgal diets tifera at low food concentration (0.5mg 1-' T-Iso).There and especially depressed by high concentrations of was no difference in clearance rate (CR) at this food Dunaliella tertiolecta (cf. F1.g I),while Le Pennec & level. The present study found that, at higher food con- Range1 (1985) reported that ingestion and digestion centrations, P. maxima had significantly higher abs.eff. of D. primolecta by Pecten maximus were low and and CR than P. margaritifera, regardless of algal diet Isochrysis galbana was among the best algal diets. (Figs. 1 & 3, Table 3a, b). Due to this and the lower Particle retention efficiency is about 100% in deter- pseudofaecal wastage of potential food particles in P. mination~of CR for bivalves filtering particles greater maxima, this species had higher SFG at food concentra- than ca 4 pm diameter (Bayne et al. 1985). This has tions of 3 to 6 mg 1-I (T-Iso) and 2 to 4 mg 1-' (D.primo- been confirmed for Pinctada margaritifera and P. max- lecta) (Table 4).Thus, it would appear that P. maxima ima (Yukihira et al. 1998). Since average diameters of is better adapted to maximise energy gain at higher T-Iso and Dunaliella primolecta are ca 4.5 pm and food concentrations compared with P. margaritifera. 7.0 pm, respectively, the size difference is unlikely to Winter (1978) showed that increases in food concen- influence filtration by the pearl oysters. There may be tration promote growth rates of bivalves only up to an other factors affecting feeding upon different types of optimum food concentration beyond which growth food, e.g. chemical stimulants on the surface of food rates decline. In terms of maximisation of growth particles. Dwivedy (1973) reported the presence of potentiality, optimal concentrations for P. marganti- chemoreceptors, sensitive to different tastes, on the fera and P, maxima are 1 to 2 mg 1-l T-Iso (ca l0 000 to labial palps of the American oyster Crassostrea vir- 20 000 ce1.l~ml-l) and 2 to 3 mg I-' T-Iso (ca 20000 to ginica, and Newell & Jordan (1983) inferred chemo- 30000 cells ml-l), respectively, as indicated by mea- selection of particles by C. virginica. Energy used in sured SFG (Table 4). These ration levels are in the digesting and absorbing energy from ingested food range of algal concentrations generating the highest may be important (Thompson & Bayne 1972, Bayne & SFG or growth rates recorded for other suspension- Scullard 1977). feeding bivalves (Table 6). The effects of food species on CR, abs.eff. and R resulted In substantial differences in SFG between pearl oysters feeding on the 2 microalgal diets. T-Iso Effects of food species on energetics contains 1.3 times more energy than Dunaliella primo- lecta (20.3 and 15.1 J mg-l, respectively), but oysters The 2 microalgae species used in this study. T-Iso feeding on T-Iso had 1.5 to 2.1 times higher maxi- and Dunaliella primolecta, significantly influenced the mum SFG values than those feeding on D. primolecta CR, abs.eff. and respiration rate of both pearl oyster (Table 4). This was in spite of higher respired energy species (Table 3), and the pseudofaeces production of (RE) for oysters feeding on T-Iso. (The higher oxygen Table 6. Food levels used for highest Scope for Growth or highest recorded growth rates for filter-feeding bivalves l Species Food level Food species Source Pinctada margaritifera 1-2 rng I-',ca 10 000-20000 cells ml-' Tahitian lsochrysis sp. Ths study Pinctada maxima 2-3 mg I'', ca 20000-30 000 cells ml-' Tahitian lsochrysis sp. Ths study Argopecten irradians 6000 cells ml-l Tahitian Isochrys~ssp. Cahalan et al. ( t 989) Aulacomya ater ca 3 mg 1.' Dunaliella primolecta Griffiths & King (1979) Chorom,~~tilusmeridionalis ca 2 mg 1-' Dunaliella primolecta Griffiths 11980) Mytilus chilensis ca 15 000 cells ml-' Dunaliella marina Navarro & Winter (1982) Mytilus edulis ca 12 000 cells ml' Tetraselmis sueclca Thompson & Bayne (1974) Ostrea edulis (juveniles) 200 000 crlls ml-' Isochrysis gaibana Beiras et al. (1994) Venrwpispullastra (juveniles) 300 000 cells ml-' Isochrysis galbana Beiras et al. (1993) Yukihira et al.:Effect of food on oyster energy budgets 81 consumption in pearl oysters feeding on T-Iso at all ca 30 000 cells ml-') and Olithodiscus sp. (3.8%, at food concentrations [Table 51 may be due to higher ca 5000 cells ml") (Hayashi 1983). mechanical and physiological costs relating to higher pumping [CR] and also to higher assimilation costs.) The higher energy gain on T-Iso was mainly due to Broodstock conditioning significantly higher CR on T-Iso (Table 3c, d). For the same reason, SFG upper thresholds for D. priniolecta, Physiological energetics are a valuable tool for pre- i.e. food concentrations beyond which SFG fell below dicting long-term growth performance under specific zero, were lower than those for T-Iso in both pearl environmental conditions (Beiras et al. 1994).Thus. the oysters (Table 4). These results show the importance of present study is relevant to a major aspect of pearl oys- energy-rich, ingestible and highly digestible food ter farming, i.e. the maturation of broodstock in tanks particles for the energy gain of pearl oysters and other using microalgal diets. Hayashi (1980) tested the suspension feeders. broodstock maturation of Punctada fucata martensii The food particles, however, must not only provide in static indoor tanks using 2 different diets, homo- the energy needs, but also the nutritional requirements genised rice starch powder and Pavlova lutheri, at of the pearl oyster. Okauchi (1990) found that, while 50000 to 60000 particles or cells ml-' d-'. Hayashi T-Iso has higher energy and total nitrogen content reported better maturation of pearl oysters feeding on than Isochrysis galbana and Chaetoceros gracilis, it P, lutheri. However, fully mature individuals were not was the poorest food species for supporting growth in produced in this trial and the feasibility of artificial Pinctada fucata martensii spat. The spat showed poor- broodstock conditioning was not demonstrated. est growth when feeding on T-Iso compared to feeding There is no published study on broodstock condi- on C. gracilis and I. galbana. Okauchi suggested that tioning of Pinctada margaritifera and P. maxima. How- the low content in T-Iso of eicosapentaenoic acid ever, our study suggests the potential for using opti- (EPA),a potentially essential lipid, may be the dietary mum ration levels (i.e. 1 to 2 mg I-' for P. margaritifera factor limiting its value for oyster growth (see also Pils- and 2 to 3 mg 1-' for P. maxima) of nutritionally rlch bury 1985, Helm & Laing 1987). For culture of bivalves, microalgae, such as a 'balanced' diet containing T-Iso, T-Iso is generally used in combination with other for broodstock conditioning. If these rations are con- microalgal species to achieve a diet without nutritional tinuously fed to adult pearl oysters in an appropriate deficiencies. This is currently practised when using static or flow-through system, they should support T-Iso as food for culturing bivalve larvae, including P. gonadal development provided other conditions favour margaritjfera and P. maxima larvae (e.g.Rose & Baker gametogenesis, e.g. temperature regime. 1994, Southgate & Beer 1997). Other studies have also demonstrated differences between microalgae species in their ability to support Habitat differences growth of pearl oyster larvae and spat, and differences between microalgae species in the rate at which they Jargensen (1990, 1996) concluded that the capacity are filtered by pearl oysters. Wada (1973) demon- for water processing in bivalves is an adaptation to the strated that Pinctada fucata martensi~ larvae feeding concentrations of suspended food that prevail in their on pure diets of Pavlova lutheri and Chaetoceros calci- biotope during the productive seasons of the year. Our trans or on a mixture of these 2 algae (1 to 2 X 104 cells studies on comparative feeding ecology of 2 species ml-l) had higher growth rates than larvae feeding on a of tropical pearl oyster support this. Since Pinctada pure diet of Chlorella sp. or on mixed diets of Chlorella maxima processes more water than P. margaritifera sp. with P lutheri or C. calcitrans. Nishimura (1980) when feeding in the high particulate range (Fig. l), assessed the influence of P. lutheri and Nitzschia P. maxima should be better adapted to waters with closterium and ration (20, 50 and 100 X 103 cells ml-' higher particulate and productivity levels. d-') on growth of pearl oyster spat. Better growth rates Both pearl oyster species occur in the Great Barrier were obtained with P. luthen, especially at 20 000 cells Reef region (GBR), northeast coast of Australia (Hynd ml-I during the first 20 d, but there were no clear 1955, Dayton et al. 1989), but they occur in different differences in growth at Day 28. Another study of P. habitats, as outlined in the 'Introduction'. Pinctada fucata martensii demonstrated higher filtration rates margantifera tends to occur on coral reefs offshore from (percentage of cells removed) when oysters were feed- the mainland, whereas P. maxima occurs on substrates ing on C. calcitrans (72.6%, at ca 50 000 cells m1 '), ranging from mud to sand and gravel, but not on coral C. gracilis (69.1(X, at ca 20000 to 30 000 cells ml-l) and reefs. P. maxima tends to occur in the waters of the in- P. lutheri (56.1 to 68.1 %, at ca 40000 cells ml-l) than ner and middle shelf, where there are greater nutrient when oysters were feeding on Chlorella sp. (48.4 %, at inputs and higher productivity levels than in coral reef Mar Ecol Prog Ser 171: 71-84, 1998 habitats. The habitats of P. margaritiferaare charac- (1991),and review by Jsrgensen (1996).Thus, a further terised by low levels of suspended particulate matter development of this study will deal with the feeding and (SPM):SPM declines significantly from the inner to the energetics of Pinctada margaritiferaand P. maxima outer continental shelf of the GBR (Oliver et al. 1995). supplied with natural suspended particles. Insofar as field data for SPM are available, and one can extrapolate these laboratory energetics data to the field Acknowledgements. We thank Mr Michael Crimp of Indo- (see below), the optimal food concentrations for P. mar- Pacific Pearl and Mr Bruce Stevens of Reefarm for providing some of the pearl oyster specimens. We are grateful to Dr Paul garitifera(1 to 2 mg 1-') are equivalent to SPM concen- Southgate of JCU for constructive criticism of the manuscript. trations found in waters of the GBR continental shelf This study was supported in part by an Internal Research where coral, reefs occur (Oliver et al. 1995, Yukihira Allowance and a Meritorious Research Grant from JCU. H.Y unpubl.). For example, the average annual SPM con- gratefully acknowledges financial support from the Japan International Cooperation Agency IIIMS contribution num- centration was 1.47 mg 1.' (range: 1 .l8 to 1.72 mg 1-', ber 927 n = 21; Yukihira unpubl.) near a fringing coral. reef In Pioneer Bay, Orpheus Island (18" 37' S, 146" 30' E), where P. margaritiferais common. The low food con- LITERATURE CITED centrations corresponding with the upper threshold of Bayne BL, Brown DA, Burns K, Dixon DR, Ivanovici A, negative SFG of P. margaritifera(e.g. 5 mg I-' for Livingstone DR. Lowe DM. Moore MN, Stebbing ARD, Dunaliellaprimolecta 1-' and 7 mg 1-' for T-Iso) help to Widdows J (1985) The effects of stress and pollution on explain why this species is excluded from turbid water marine animals, Chap 1 (Physiological measurements) SPM or equivalent data are not available for GBR habi- and 7 (Physiological procedures). Praeger Press, New tats specifically inhabited by Pinctadamaxima. How- York, p 4-45, 161-171. Bayne BL,Hawkins AJS, Navarro E, lgles~asIP (1989) Effects ever, its terrigenous sediment habitats in the inner to of seston concentration, on feeding, digestion and growth middle shelf region are characterised by turbid water in the mussel Mytilus edulis.Mar Ecol Prog Ser 55:47-54 and the SPM concentratlons will fluctuate substantially Bayne BL, Newell RC (1983)Physiological energetics of m.arine due to river discharge and wlnd-driven re-suspension of molluscs. In: Wilbur KM et al. (ed) The Molluscs, Vol 4, Physiology. Part 1. Academic Press, New York, p 407-515 sediment (Furnas et al. 1990, Furnas et al. 1995, Oliver et Bayne BL, Scullard C (1977)An apparent scientific dynamic ac- al. 1995). Reflecting this, at a near-shore site of the inner tion in Mytilus edulis (L.).J Mar Biol Assoc UK 57:371-378 shelf at Cape Ferguson, the average annual SPM con- Bayne BL, Worrall CM (1980) Growth and production of mus- centration was 12.22 mg 1-' (range: 1.95 to 60.37 mg 1-'; sels, Mytilus edulis from two populations. Mar Ecol Prog n = 72; Yukihira unpubl.). Although P. maximahas not Ser 3:317-328 Beiras R, Perez-Camacho A, Albentosa M (1993) Influence of been recorded from this site, it indicates the kind of food concentration on energy balance and growth perfor- conditions that this species may encounter at its most mance of Venerupispullastra seed reared in an open-flow inshore distributions. Its higher optimum SFG concen- system. Aquaculture 116:353-365 tration (2 to 3 mg 1-l) and upper threshold for negative Beiras R, Perez-Camacho A, Albentosa M (1994) Comparison of the scope for growth with the growth performance of SFG (7 or 9 mg 1-l) are largely below these field SPM Ostrea edulis seed reared at different food concentrations levels, but th.ey are more in accord with these conditions In an open-flow system. Mar Biol 1.19:22?-233 than are the equivalent parameters for P. margaritifera. Cahalan JA, Siddall SE, Luckenback MW (1989) Effects of On the other hand, P. maxima may experience lower flow velocity, food concentration and particle flux on growth rates of juvenile bay scallops Arqopecten irra- levels of SPM in its offshore, deepwater habitats. It is also dians. J ExpMar Biol Ecol 129:45-60 well adapted to maintaining a positive SFG at low SPWI Conover RJ (1966) Assimilation of organic matter by zoo- levels (Table 4, Yukihira et al. 1998).Thus, P. maximais plankton. 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Mar Ecol Arca zebra):responses to an acute increase in suspended Prog Ser 170:119-130 Editorial responsibilil)~:Otto Knne (Editor), Submitted: Apnl 15, 1998; Accepted: July 7, 1998 Oldendorf/Luhe, Germany Proofs received from author(s):September 16, 1998