The effect of temperature on clearance rate and oxygen consumption of scallops, Chlamys farreri.

ABSTRACT Rates of particle clearance and oxygen consumption were measured over full natural ranges of seawater temperature (1[degrees]C to 30[degrees]C) experienced by the scallop Chlamys farreri cultured in Shandong Province, People's Republic of China, comparing both acclimated and non-acclimated responses. Particle clearance rate varied in hyperbolic relation with acclimated temperature of maximal values of 10 to 15 L [h.sup.-1] [g.sup.-1] dry wt, occurring in acclimated scallops between 20[degrees]C and 25[degrees]C, with significant reductions at temperatures above about 26[degrees]C, particularly in non-acclimated scallops (P < 0.001). Oxygen consumption rate increased throughout the range of temperature. Based in part on responses defined here, a dynamic model of physiology and growth predicts that net energy balance becomes negative with short-term adjustments in seawater temperature from 15[degrees]C to above 26[degrees]C, when soft tissue wasting may be as much as 3.5% per day at 30[degrees]C. These predictions are consistent with the loss of condition reported by farmers under such conditions, and help to establish that similar naturally occurring transient increases in temperature have at least in part has been responsible for high coincident mortalities observed in cultured C. farreri during recent years.

KEY WORDS: scallop, Chlamys farreri, clearance rate, oxygen consumption rate, temperature, net energy balance, mortality

INTRODUCTION

Chlamys farreri is one of the main species of shellfish cultivated in China (Guo et al. 1999). However, since the 1990s, a sharp increase in mortality has compromised production, and seems linked with both abrupt temperature fluctuations and high temperature maxima in recent years (Wang & Yang 1994, Shao et al. 1996, Li & Mou 1999, Zhang & Yang 1999). The effects of environmental variables on physiologic components of growth have often been studied in bivalve molluses (Bayne 1976, Hawkins & Bayne 1992, Albentosa et al. 1994, Espina & Buckle-Ramirez 1994, Navarro & Iglesias 1995, Urrutia et al. 1996). Whereas this includes work on scallops, effects of temperature change are poorly documented in C. farreri and other species (Wang et al. 1999, Yuan et al. 2000).

In China, as in several other regions, the combination of a rapidly developing mariculture industry and the increasing impact of human activities on the coastal environment emphasizes the need for predicting and monitoring the carrying capacity for shellfish culture. Carrying capacity assessment, particularly in areas practicing polyculture, is a complex issue that needs to address the interaction of many variables throughout the year or growing period. Fisheries managers are increasingly looking to models of physiologic processes and growth in cultured species (e.g., Pouvreau et al. 2000, Solidoro et al. 2000, Ren & Ross 2001, Hawkins et al. 2002), for integration within ecosystem models (e.g., Nunes et al. 2003, Bacher et al. in press; Duarte et al. in press), to help them form strategies for production and development.

In this study, we describe thermal responses in rates of particle clearance and oxygen consumption in both acclimated and nonacclimated C. farreri. These responses have been used in the associated development of a dynamic model of responsive feeding, metabolism, and growth in C. farreri cultured in Sanggou Bay (Hawkins et al. 2002). Here, to better understand the high mortalities observed during recent years (refer to earlier), we also used that model to simulate net energy balance under a range of culture scenarios, which include abrupt changes in temperature within the range of those known to occur naturally.

MATERIALS AND METHODS

Animal Collection, Maintenance, and Treatment

Cultured Chlamys farreri were collected from lantern nets suspended within Sanggou Bay, Shandong Province, P.R. China (37.1[degrees]N, 122.5[degrees]E). Scallops were maintained in a 20 L aquarium in which 10 L of water were changed and about 1 x [10.sup.9] cells of Phaeodactylum tricornutum were added daily. The size, weight, and treatment of scallops are summarized in Table 1. In this study, 60 scallops were used in experiments on clearance rate, and 30 for determination of oxygen consumption rate.

Acclimation and Temperature Control

In the acclimation experiments the temperature of the water was adjusted by 1[degrees]C each day to reach the desired temperature and kept at each experimental temperature for 3 d before measuring clearance rates. Temperature changes were therefore gradual, to better approximate nature, when we assumed a final (standardized) period of 3 d acclimation, which we acknowledge may not have been complete. In nonacclimated comparisons, changes in temperature were made by decreasing or increasing from 15[degrees]C directly to the other temperatures, as detailed in Table 1. Additionally, animals were also subjected to an instantaneous decrease from 30[degrees]C to 23[degrees]C, and in this case measurements were taken after 24 h and 96 h.

Physiological Measurements

Clearance Rate

Individual clearance rates (CR; liters of water cleared of particles >2 [micro]m diameter [h.sup.-1]) were measured using a static system. Ten to 15 individuals were individually placed in separate beakers each containing 3 L of filtered seawater at a constant temperature. An additional 3-L beaker without a scallop was used as a control. The water was mixed by gentle aeration to avoid any physical disturbance. After a period of 15 min, to allow the animals to open their shell valves and to resume pumping, algal cells were added to minimal concentrations of 15,000 cells [ml.sup.-1], but algal cells did not exceed 25,000 cells [ml.sup.-1], thereby avoiding pseudofaeces production and inhibition of clearance rate (Hawkins et al. 2001). In February 2000, scallops were fed Phaeodactylum tricornutum, whereas in June 2000 scallops were fed Isochrysis galbana. This was necessary, given that the optimal temperature for growth of P. tricornutum is between 15[degrees]C and 20[degrees]C, but higher for I. galbana. Average diameters of P. tricornutum and I. galbana are almost identical (5.2 to 5.5 [micro]m). To test for any effects of different algal species, CR was compared in acclimated scallops feeding on either species of alga at 15[degrees]C.

After a 5-min period to allow thorough mixing of the algal cells, a 20-mL sample was taken from each beaker. Four subsequent 20-mL samples were taken at 30 min intervals over a period of 2 h. Cell concentrations in each sample were determined using a Coulter Multisizer II With a 100-[micro]m aperture tube.

The clearance rate by individual animals was calculated as follows (Coughlan 1969):

Clearance rate (1 [h.sup.-1]) = V x(ln[C.sub.o]-ln[C.sub.t])/t

Where [C.sub.o] and [C.sub.t] were the cell concentrations at the beginning and end of each time increment, V is volume of water, t is the time between [C.sub.o] and [C.sub.t]. The maximum clearance rate of each scallop was calculated based on the greatest decline in cell concentration over a 1-h period. This avoids the inclusion of periods when individuals may be totally or partially closed.

Oxygen Consumption Rate

Following the measures of CR, scallops were transferred to closed glass vessels containing 5 L of filtered (0.45 [micro]m) seawater, each with a magnetic stirrer. Three scallops were put into each vessel, which was sealed and placed in a temperature-controlled oven. Dissolved oxygen (DO) was measured using an oxygen meter (YSI-556). Twenty minutes were allowed for the scallops to acclimate, after which their siphons were open. Oxygen uptake was measured over the next hour. Prior to each DO reading, the stirrer was operated for 20 sec. Oxygen concentration was not allowed to fall below 70% of saturation. Rates of oxygen consumption (OCR; [micro]mol [h.sup.-1]) were measured in Chlamys farreri acclimated to 3[degrees]C, 5[degrees]C, 8[degrees]C, and 15[degrees]C, and 1 day after transfer when fully acclimated from 15[degrees]C to 23[degrees]C, 25[degrees]C, and 27[degrees]C. At each temperature, declines in oxygen concentration were corrected for that consumed by the oxygen meter, using values measured in a control vessel without scallops. At the end of the experiments the dry weight of each individual animal was determined after drying at 60[degrees]C for 48 h.

Weight Corrections

To standardize findings, rates were corrected for an equivalent individual of 1 g dry soft tissue using [Y.sub.s] = [([W.sub.s]/[W.sub.e]).sup.b][Y.sub.e], where [Y.sub.s] is physiologic rate of activity of a standard animal, [W.sub.s] is the dry weight of standard animal (1g in this study), [W.sub.e] is the dry weight of the experimental individual, [Y.sub.e] is the uncorrected rate. B-values of 0.62 and 0.75 were used for CR and OCR, respectively, according to previous measures that confirm theoretical expectations in C. farreri (Lu et al. 2000, Hawkins et al. 2001).

Statistical Analyses

Weight-corrected CR and OCR were analyzed by ANOVA (one-way analysis of variance), with temperature as the independent variable. Pair-wise comparisons of the clearance rate at different temperatures were compared using Tukey's HSD multiple comparison test.

Model Predictions

Our dynamic model of responsive feeding, metabolism and growth in C. farreri cultured in Sanggou Bay (Hawkins et al. 2002) was adapted using findings presented here to further elucidate the effects of temperature on growth and possible mortality. As described by Hawkins et al. (2001), the correction factor used in this model for temperature effects on acclimated filtration rate (TEF; fraction) was derived from the Gaussian curve describing how CR varied with temperature that we document below (refer Results), as follows:

TEF = (234.7 / (7.174 x [(6.283).sup.0.5])) x EXP(-0.5 x ([(-22.214) / 7.174).sup.2]) / (234.7 / (7.174 x [(6.283).sup.0.5])) x EXP(-0.5 x ([(12 - 22.214) / 7.174).sup.2]).

Here, to predict responses in nonacclimated scallops, we instead implemented a modified TE[F.sub.NA] based upon both the Gaussian and polynomial curves reported later (refer Results), describing how CR varied with temperature in both acclimated and nonacclimated scallops, respectively, as follows:

TE[F.sub.NA] = ((234.7 / (7.17 x [(6.283).sup.0.5])) - EXP(-0.5 x [((Water_temperature - 22.2) / 7.17).sup.2])) / ((234.7 / (7.17 x [(6.283).sup.0.5])) x EXP(-0.5 x [((12 x 22.2) / 7.17).sup.2])) x ((-18.059 + (3.078 x Water_temperature) + (0.084 x Water_temperature x Water_temperature)) / (-18.059 + (3.078 x 15) + (-0.084 x 15 x 15))).

To predict effects on metabolism in scallops subjected to abrupt increases in temperature, we continued to use the existing model correction factor reflecting a positive logarithmic dependence of oxygen consumption upon temperature as documented later (refer Results), and which confirms a similar relation established previously at temperatures of up to 30[degrees]C (Lu et al. 2000, Hawkins et al. 2002).

The model with revised TE[F.sub.NA] was run for 1 day, starting on Julian day 133 when the natural seawater temperature observed in Sanggou Bay was 15[degrees]C. Repeated simulations imposed stepwise increments in seawater temperature, each from 15[degrees]C, at 1[degrees]C intervals that ranged up to 30[degrees]C. Each of those runs used the same initial values of dry soft tissue weight (0.09 g), shell dry weight (0.64 g), shell energetic content (188 joules), and soft tissue energetic content (1717 joules), as had been predicted and validated for acclimated scallops, including the same data describing food availability and composition. By these means, we have predicted nonacclimated growth responses using our fully dynamic model in scallops subjected to abrupt stepwise increases in temperature from 15[degrees]C at 1[degrees]C intervals up to 30[degrees]C.

RESULTS

Comparison of CR When Feeding Upon Different Algal Species

Results from all experimental measures of CR (1 [h.sup.-1] [g.sup.-1]), as outlined in Table 1, are illustrated in Figure 1. Average CRs in C. farreri feeding on different algal species Isochrysis galbana (10.5 L [h.sup.-1] [g.sup.-1]) or Phaeodactylum tricornutum (8.0 L [h.sup.-1] [g.sup.-1]) at 15[degrees]C were not statistically significant (F = 3.31, df = 29, P > 0.05). All measures derived for each algal species were therefore combined.

[FIGURE 1 OMITTED]

Effects of Temperature Change on Clearance Rate

In acclimated scallops, average CR increased with temperature from practically zero at 1[degrees]C to a measured maximum of 16.3 1 [h.sup.-1] [g.sup.-1] at 25[degrees]C, decreasing to around 7 l [h.sup.-1] [g.sup.-1] at temperatures from 27[degrees]C to 30[degrees]C, but with greater individual variation. This increased variation in CR between individual scallops was because some animals had virtually ceased to feed at the higher temperatures.

The line of best fit describing CR in C. farreri that had been fully acclimated under standardized conditions of food availability varied with temperature (T; [degrees]C) was a Gaussian curve illustrated in Figure 1 and described by the following equation:

CR = (234.7 / (7.17 x [(6.283).sup.0.5])) x EXP(-0.5 x [((T - 22.14) + 7.174).sup.2]),

where adjusted [r.sup.2] = 0.85, residual df = 9 and P < 0.000001 (from Hawkins et al. 2002).

Compared with acclimated scallops, there was little difference in average CR among nonacclimated animals that had been subjected to abrupt changes in temperature from 15[degrees]C to either 20[degrees]C (F = 0.88, df = 29, P > 0.05) or 23[degrees]C (F = 0.23, df = 29, P > 0.05) (see Fig. 1). However, average CR in nonacclimated scallops decreased significantly at temperatures both above and below this range, as represented by a polynomial curve illustrated in Figure 1 and described by the following equation:

CR = -18.055 + (3.077 x T) - (0.084 x [T.sup.2]),

where adjusted [r.sup.2] = 0.76, residual df = 23 and P < 0.01.

The result was that average CRs at 25[degrees]C and above were significantly lower in nonacclimated than acclimated scallops (e.g., at 30[degrees]C, F = 9.84, df = 23, P < 0.01).

In scallops that had been acclimated at 30[degrees]C, and then transferred to 23[degrees]C, the average CRs determined after 1 and 4 days at 23[degrees]C (4.76 [+ or -] 1.90 and 6.51 [+ or -] 4.79 L [h.sup.-1] [g.sup.-1] respectively) were similar (F = 0.12, df = 16, P > 0.05), but significantly lower than among scallops acclimated at 23[degrees]C (10.19 [+ or -] 5.16 L [h.sup.-1] [g.sup.-1]) (F = 7.65, df = 18, P < 0.05; and F = 8.29, df = 17, P < 0.05; respectively).

Effects of Temperature Change on Oxygen Consumption

Average rates of oxygen consumption (OCR; [micro]mol [h.sup.-1] [g.sup.-1]) in scallops acclimated at 3[degrees]C, 5[degrees]C, 8[degrees]C, and 15[degrees]C, and in nonacclimated animals transferred from 15[degrees]C to 23[degrees]C, 25[degrees]C, and 27[degrees]C, are illustrated in Figure 2. Whether in acclimated or in nonacclimated scallops, temperature had significant positive effects on OCR, which rose from 19.4 [micro]mol [h.sup.-1] [g.sup.-1] at 3[degrees]C to 37.5 [micro]mol [h.sup.-1] [g.sup.-1] at 15[degrees]C (F = 38.65, df = 9, P < 0.01), and then from 37.5 [micro]mol [h.sup.-1] [g.sup.-1] at 15[degrees]C to a maximum of 88.1 [micro]mol [h.sup.-1] [g.sup.-1] at 27[degrees]C (F = 62.76, df = 9, P < 0.01). Overall sensitivity of OCR to combined temperature increases as represented by [Q.sub.10] value according to Bayne and Newell (1983) was [Q.sub.10] = [(88.1/ 19.4).sup.(10+(27-3))] = 1.9. These findings are consistent with [Q.sub.10] values of about 2, indicating approximate logarithmic increases in OCR with temperature reported in C. farreri and other shellfish species (e.g. Widdows 1973, Bayne &amp; Newell 1983, Lu et al. 2000).

[FIGURE 2 OMITTED]

Effects of Temperature Change on Net Energy Balance

Figure 3 illustrates average seasonal changes in seawater temperature and suspended chlorophyll a ([micro]g [1.sup.-1]) measured at seven sampling sites throughout Sanggou Bay, China, and presents scallop growth both in terms of shell length (cm) and net energy balance (NEB; J [h.sup.-1] [g.sup.-1]), as predicted by our dynamic model simulating the traditional culture scenario. It shows how predicted shell length increased from 2 cm following seeding onto longlines in April to reach marketable sizes of more than 6 cm during the following October, according to historical practice and records (Hawkins et al. 2002). These predictions are for fully acclimated scallops, when NEB only becomes negative from December onwards, at a time when food availability measured as chlorophyll a abundance is low, and when temperatures fall below 8[degrees]C (see Fig. 3).

[FIGURE 3 OMITTED]

Figure 4 illustrates output from our revised model, predicting NEB in scallops 1 day after being subjected to a range of increased temperatures, where scallops had previously been acclimated at 15[degrees]C, and those increases in temperature were at 1[degrees]C intervals from 15[degrees]C up to 30[degrees]C. Our simulations indicate that maximal NEB would occur following exposure to 20[degrees]C, becoming negative following exposure to temperatures above 26[degrees]C. Energy losses of 60 J [d.sup.-1] predicted following exposure to 30[degrees]C in scallops of this size (2 cm SL containing 1717 J within soft tissues) are equivalent to 3.5% of their soft tissue energy [d.sup.-1].

[FIGURE 4 OMITTED]

DISCUSSION

Bivalve feeding and metabolism is highly responsive to environmental conditions that include food availability (Newell & Shumway 1993, Iglesias et al. 1992, Hawkins et al. 1996, Hawkins et al. 2001) and temperature (e.g., Bayne & Newell 1983, Navarro et al. 2000). An ability to acclimate to temperature change has been widely reported (Schulte 1975, Widdows et al. 1979, Bayne & Newell 1983. Navarro et al. 2000, Wang et al. 1999). In respect of feeding, this is confirmed for C. farreri by the differences observed here (see Fig. 1). Further, despite being uncertain that scallops were fully acclimated following each temperature change, our findings confirm a hyperbolic relation between acclimated CR and temperature, as reported in other species (e.g., Bougrier et al. 1995) (see Fig. 1). Significant reductions in CR were observed towards the extremes of temperature studied here, particularly when the change was made abruptly. This is of particular ecological significance for C. farreri in northern China, where the natural range of seawater temperature in areas used for the culture of scallops is much broader (1[degrees]C to 30[degrees]C) than most other regions of the world (Saxby 2002).

Our findings indicate that approximately 20[degrees]C to 25[degrees]C is the optimal temperature range for feeding, temperatures above this resulting in reduced rates of feeding and thus, by inference, the general health of scallops both in the short and long-term. This is borne out by our model predictions, suggesting that maximal NEB may occur at around 20[degrees]C, and that temperatures above 26[degrees]C, particularly if experienced abruptly, lead to reduced feeding, increased oxygen consumption and negative NEB (see Figs. 2, 3, 4). CR in animals acclimated above 26[degrees]C was not only reduced, but also variable between individuals (see Fig. 1). This may be interpreted as either a short-term survival strategy to reduce energy expenditure, or a differing susceptibility to the high temperatures causing some individuals to cease feeding completely. Further to this, CR in scallops acclimated at 30[degrees]C and then transferred to 23[degrees]C, did not recover to values in animals acclimated at 23[degrees]C, for at least 4 d. Further experiments are needed to confirm whether physiologic competence in respect of CR would have recovered over a longer period. If not, we might conclude that although exposure to temperatures of 27[degrees]C to 30[degrees]C was not lethal in the short-term, irreparable physiologic harm may have resulted in reduced fitness.

Our weight-corrected oxygen consumption rates of between approximately 20 and 100 [micro]mol [g.sup.-1] [h.sup.-1] cannot easily be compared with previously published values in C. farreri; due to differences in methodology and units, previous values being expressed per individual, or in terms of wet weight (Wang et al. 1997, Wang et al. 1999, Yuan et al. 2000). However, rates reported here seem broadly comparable with those in previous studies, including those for other shellfish species (Haure et al. 1998, Bougrier et al. 1995, Aldridge et al. 1995, Taylor et al. 1995, Gunasingh et al. 2002, Gouletquer et al. 1999, Martinez et al. 1995).

Instead of calculating NEB using the simpler traditional measure of "scope for growth" according to Bayne and Newell (1983), we used our dynamic growth model for the scallop Chlamys farreri, thereby taking into account functional interrelations such as the influence of feeding rate upon absorption efficiency and a dependence of energy losses upon absorption rate (Hawkins et al. 2002). This model has been validated through both direct observations and records of growth as described by Hawkins et al. (2001). Simulations illustrated here indicate that in scallops acclimated to natural measured variations in temperature in Sanggou Bay, negative growth may occur from December onwards, when food availability is low, and temperatures are less than 8[degrees]C (see Fig. 3).

However, adaptation of that model in this study has shown that in nonacclimated scallops subjected to a major change in temperature from 15[degrees]C to 25[degrees]C and above, CR may decrease dramatically, associated with increased OCR and negative NEB. These sublethal changes in temperature may occur naturally in Sanggou Bay during summer when temperatures above 25[degrees]C are common. For example, in recent summers, high temperatures of approximately 27[degrees]C lasted for several days along the coast of Shandong Province, especially in 1997. It has also been reported that the El-hint phenomenon elevated near-shore seawater temperatures abruptly by from 2[degrees]C to 5[degrees]C to as high as 29[degrees]C (Gao & Wang 1998, Li & Mou 1999, Shao et al. 1996, Shang et al. 1998). These high temperatures or large changes in temperature may contribute significantly to severe physiologic stress. When compounded with other adverse environmental conditions, such as low food availability, pollution, toxic algal blooms or, a disease vector made more abundant or virulent by high temperature, increased mortality will inevitably result.

TABLE 1.

Sizes, weights and experimental treatments for measures of clearance
rate in Chlamys farreri.

 Date of      Treatment/
 Scallop      Temperature     Mean Shell Length     Tissue Dry Weight
Collection   ([degrees]C)    (mm) ([+ or -] SD)     (g) ([+ or -] SD)

February,    Acclimated at   54.18 [+ or -] 4.04   1.182 [+ or -] 0.271
  2000         1, 3, 5,
               10, 15
February,    Non-acclima-    55.22 [+ or -] 3.91   0.773 [+ or -] 0.196
  2000         ted: 15 to
               8, 20, 23,
               26, 27.5,
               30 and from
               30 to 23
               (measured
               after 24
               and 96 h)
June, 2000   Acclimated at   40.46 [+ or -] 9.49   0.145 [+ or -] 0.088
               23, 25, 27,
               28, 29, 30

ACKNOWLEDGMENTS

The authors thank two anonymous referees for their helpful suggestions.

LITERATURE CITED

Albentosa, M., R. Beiras & A. P. Camachl. 1994. Determination of optimal thermal conditions for growth of clam (Venerupis pullastra) seed. Aquaculture 126:31-32.

Aldridge, D. W., B. S. Payne & A. C. Miller. 1995. Oxygen consumption, nitrogenous excretion, and filtration rates of Dreissena polymorpha at acclimation temperatures between 20 and 32[degrees]C. Can. J. Fish. Aquat. Sci. 52:1761-1767.

Bacher, C., J. Grant, A. J. S. Hawkins, J. Fang, M. Zhu & M. Besnard. Modelling the effect of food depletion on scallop growth in Sungo Bay (China). Aquatic Living Resources (In Press).

Bayne, B. L. 1976. Marine mussels. Their ecology and physiology. London and New York: Cambridge Univ. Press.

Bayne, B. L. & R. G. Newell. 1983. Physiological energetics of marine molluscs. In: A. M. S. Salenddin & K. M. Wilbur, editors. The Mollusca, Vol. 4: Physiology, Part 1. Academic Press, New York, pp. 407-515.

Bougrier, S., P. Geairon, J. M. Deslous-Paoli, C. Bacher & G. Jonquieres. 1995. Allometric relationships and effects of temperature on clearance and oxygen consumption rates of Crassostrea gigas (Thunberg). Aquaculture 134:143-154.

Coughlan, J. 1969. The extermination of filtering rate from the clearance of suspensions. Mar. Biol. 2:356-358.

Duarte, P., R. Meneses, A. J. S. Hawkins, M. Zhu & J. Fang. Mathematical modelling to assess the carrying capacity for multi-species culture within coastal waters. Ecological Modelling. (in press).

Espina, S. & L. F. Buckle-Ramirez. 1994. Scope for growth as function of temperature, salinity and body weight in Tivela stultorum (Mollusca. Lamellibranchia). J. Applied Aquacult. 4:91-100.

Gao, X. Q. & X. L. Wang. 1998. EL-nino phenomenon and it's effect on biology. Journal of Biology (Chinese) 15:47.

Goulletquer, P., M. Wolowicz, A. Latala, P. Geairon, A. Huvet & P. Boudry. 1999. Comparative analysis of oxygen consumption rates between cupped oyster spat of Crassostrea gigas of French, Japanese, Spanish and Taiwanese origins. Aquat. Living Resour. 12:271-277.

Gunasingh, M. J., K. Nandakumar, K. S. Jesudoss, J. Azariah, K. K. Satapathy & K. V. K. Nair. 2002. Influence of temperature on the physiological responses of the bivalve Brachidontes striatulus and its significance in fouling control. Marine Environmental Research. 53: 51-63.

Guo, X., S. E. Ford & F. Zhang. 1999. Molluscan aquaculture in China. J. Shellfish Res. 18:19-31.

Haure, J., C. Penisson, S. Bougrier & J. P. Baud. 1998. Influence of temperature on clearance and oxygen consumption rates of the flat oyster Ostrea edulis: determination of allometric coefficients. Aquaculture 169:211-224.

Hawkins, A. J. S. & B. L. Bayne. 1992. Physiological processes, and the regulation of production. In: E. Gosling, editor, The mussel Mytilus: ecology, physiology, genetics and culture. Amsterdam: Elsevier Science Publishers B.V. pp. 171-222.

Hawkins, A. J. S., R. F. M. Smith, B. L. Bayne & M. Heral. 1996. Novel observations underlying fast growth of suspension-feeding shellfish in turbid environments: Mytilus edulis. Mar. Ecol. Prog. Ser. 131:179-190.

Hawkins, A. J. S., J. G. Fang, P. L. Pascoe, J. H. Zhang, X. L. Zhang & M. Y. Zhu. 2001. Modelling short-term responsive adjustments in particle clearance rate among bivalve suspension-feeders: separate unimodal effects of seston volume and composition in the scallop Chlamys farreri. J. Exp. Mar. Biol. Ecol. 262:61-73.

Hawkins, A. J. S., P. Duarte, J. G. Fang, P. L. Pascoe, J. H. Zhang, X. L. Zhang & M. Zhu. 2002. A functional simulation of responsive filter-feeding and growth in bivalve shellfish, configured and validated for the scallop Chlamys farreri during culture in China. J. Exper. Mar. Bio. Ecol. 281 : 1340.

Iglesias, J. I. P., E. Navarro, P. Alvarez Jorna & I. Armentia. 1992. Feeding, particle selection and absorption in cockles Cerastoderma edule (L.) exposed to variable conditions of food concentration and quality. J. Exp. Mar. Biol. Ecol. 162:177-198.

Li, Y. C. & H. N. Mou. 1999. Analysis on the reason and measure of the death of scallop in the seashore. Chin. HeBei Fisheries. 104:38.

Lu, R., R. Ji, Y. Zou, B. Xia, R. Li & M. Zhu. 2000. A study on the feeding of three bivalves. Acta Oceanol. Sinica 22:306-312.

Martinez, G., L. A. Caceres, E. Uribe & M. A. Diaz. 1995. Effects of different feeding regiments on larval growth and the energy budget of juvenile Chilean scallops, Argopecten purpuratus Lamarck. Aquaculture 132:313-323.

Navarro, E. & J. I. P. Iglesias. 1995. Energetics of reproduction related to environmental variability in bivalve mollusks. Haliotis 24:43-55.

Navarro, J. M., G. E. Leiva, G. Martinez & C. Aguilera. 2000. Interactive effects of diet and temperature on the scope for growth of the scallop Argopecten purpuratus during reproductive conditioning. J. Exp. Mar. Biol. Ecol. 147:67-83.

Nunes, J. P., J. G. Ferreira, F. Gazeau, J. Lencart-Silva, X. L. Zhang, M. Y. Zhu & J. G. Fang. 2003. A model for sustainable management of shellfish polyculture in coastal bays. Aquaculture 219:257-277.

Pouvreau, S., C. Bacher & M. Heral. 2000. Ecophysiological model of growth and reproduction of the black pearl oyster, Pinctada margaritifera: potential applications for pearl farming in French Polynesia. Aquaculture 186:117-144.

Ren, J. S. & A. H. Ross. 2001. A dynamic energy budget model of the Pacific oyster Crassostrea gigas. Ecol. Mod. 142:105-120.

Saxby, S. A. 2002. A review of food availability, sea water characteristics and bivalve growth performance at coastal culture sites in temperate and warm temperate regions of the world. Fisheries Research Report (Western Australia), No. 132.

Schulte, E. H. 1975. Influence of algal concentration and temperature on the filtration rate of Mytilus edulis. Mar. Biol. 30:331-341.

Shang, Z. Q., Y. E. Zhang & Z. B. Sun. 1998. Discussion on the reason and prevention of mortality in scallop Chlamys farreri. Chinese Fisheries. 12:36-37.

Shao, M. K., H. R. Wang, Y. G. Zhang, M. Xin, D. L. Zhao, Y. Fen & P. J. Li. 1996. Analysis on the reason of large-scale area death of scallop Chlamys farreri in Haiyang City. Shandong Fisheries (China) 13: 19.

Solidoro, C., R. Pastres, D. Melaku Canu, M. Pellizzato & R. Rossi. 2000. Modelling the growth of Tapes philippinarum in North Adriatic lagoons. Mar. Ecol. Prog. Ser. 199:137-148.

Taylor, A. C., J. Davenport & J. A. Allen. 1995. Anoxic survival, oxygen consumption and haemocyanin characteristics in the protobranch bivalve Nucula sulcata Bronn. Comp. Biochem. Physiol. 112A(2):333-338.

Urrutia, M. B., J. I. P. Iglesias, E. Navarro & J. Prou. 1996. Feeding and absorption in Cerastoderma edule under environmental conditions in the Bay of Marennes-Oleron (Western France). J. Mar. Biol. Ass. U. K. 76:431-450.

Wang Yuanlong & X. Y. Yang. 1994. Study on the reason of high mortality and its prevention in scallop. Chin. Shandong Fisheries (China) 11:34-36.

Wang, F., S. L. Dong & S. Zhang. 1997. Study on the respiration and excretion on scallop Chlamys farreri and clam Ruditapes philippinarum. J. Fisheries of China. 21:252-257.

Wang, J., Z. H. Jiang, B. Zhang, Y. Sun & Q. S. Tang. 1999. Study on energy budget of farrerid scallop (Chlamys farreri). Mar. Fish. Res. 20:71-75.

Widdows, J. 1973. The effects of temperature on the metabolism and activity of Mytilus edulis. Neth. J. Sea Res. 7:387-398.

Widdows, J., P. Fieth & C. M. Worrall. 1979. Relationships between seston, available food and feeding activity in the common mussel Mytilus edulis. Mar. Biol. 50:195-207.

Yuan, Y. X., K. M. Qu, J. F. Chen, B. J. Chen, F. Guo, Q. F. Li & Y. Cui. 2000. Adaptability of Chlamys farreri to environment--Effects of temperature on survival, respiration, ingestion and digestion. J. Fish. Sci. China. 7:24-27.

Zhang, F. S. & H. S. Yang. 1999. Analysis of the causes of mass mortality of farming Chlamys farreri in summer in coastal areas of Shandong, China. Marine Sciences (China) 1:44-47.

ZHANG JIHONG, (1) J. G. FANG, (1) * A. J. S. HAWKINS (2) AND P. L. PASCOE (2)

(1) Yellow Sea Fisheries Research Institute, 106 Nanjing Road, 266071 Qingdao, People's Republic of China; (2) Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth, PL1 3DH, United Kingdom

* Corresponding author. E-mail: [e-mail]

This work was funded in part by a European Community INCO-DC project ERBIC18CT980291 entitled "Carrying capacity and impact of aquaculture on the environment in Chinese bays," a Core Strategic Research Project entitled "Scaling Biodiversity, and the consequences of change" of the Plymouth Marine Laboratory, and The Chinese National Science Foundation project (no. 30271021) entitled "Study on Interaction between Intensive Bivalves culture and Environment in Coastal waters" and National Key Basic Research Program (G1999012012).