ELSEVIER Aquaculture 134 (1995) 143-154
Allometric relationships and effects of temperature
on clearance and oxygen consumption rates of
Crassostrea gigas (Thunberg)
S. Bougrier ‘**, P. Geairon, J.M. Deslous-Paoli 2, C. Bather 3,
G. Jonquikres 4
IFREMER, LABElM, BP 133.17390 La Tremblade. France
Accepted 22 February 1995
Clearance and oxygen consumption rates of Crassosfrea gigas were investigated with animals of
5-200 g total wet weight (0.1-3 g dry tissue weight), and at different temperatures (5--32”(Z) after
10 days acclimation. During this period significant mortalities were observed at 32”C, which may be
close to the upper thermal limit for this species. For each temperature, allometric relationships between
physiological rates and the dry weight (DW, g) of the animal were estimated. Clearance rate (CR,
1. h-l) was maximal at 19°C; oxygen consumption rate (VO*, mg Oz. h-‘) increased over the range
of experimental temperatures (T, “C). Two statistical models are proposed: CR= [a - (b * (T-
c) *) ] * DWd and VO1 = [a + (b * cT) ] * DWd. However, neither model is appropriate during the
Keywords: Clearance rate; Oxygen; Allometry; Temperature; Crassostrea gigas
Studies of bivalve ecosystem dynamics require an understanding of the trophic structure
of the productive area, the stocks of natural and cultivated molluscs and their impact on the
nutritional potentialities of the system. Modelling of such dynamics requires linked physical
* Corresponding author. Present addresses:
’ CNRS-IFREMER, CREMA, BP 5, 17137 L’Houmeau, France.
* IFREMER, DEL, I Rue Jean VILAR, 34200 S&e, France.
’ IFREMER, MERHA. BP 1049.44037 Nantes C&lex 01, France.
4 IFREMER, COP, BP 7004, TARAVAO, Tahiti, French Polynesia.
0044-8486/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved
144 S. Bougrier et al. /Aquaculrure I34 (1995) 143-154
and biological approaches. The relevant biological models are often based upon consider-
ation of the animal’s energetics, related to fluctuations in the biotic and abiotic conditions
within the water column. An understanding of food acquisition (i.e. clearance rate) and
metabolic loss (i.e. oxygen consumption rate) is therefore essential. These indices of energy
acquisition and energy loss would define the minimum needs for growth, and are therefore
critical to choosing potential cultivation areas. These physiological functions, when inte-
grated into an ecosystem model, would allow predictive modelling of shellfish production
of a bay.
Clearance and oxygen consumption rates are dependent on both exogenous and endog-
enous factors (Percy et al., 1971; Winter, 1973; Foster-Smith, 1975; Schulte, 1975; Shum-
way, 1982; Shumway and Koehn, 1982; Gerdes 1983a, b; Fiala-M&.lioni et al., 1985).
Studies (Bayne and Newell, 1983) have shown that size and temperature are two important
factors determining energy balance. The aim of this study was to establish statistical descrip-
tions of clearance and oxygen consumption rates of Crassostrea gigas related to two factors:
dry weight and temperature.
2. Materials and methods
C. gigas of 5-200 g total wet weight were collected from the Marennes-Oleron basin
(Fig. 1) in September 1988, February 1989 and September 1990. Natural temperatures and
salinities at the time of collection were 16°C and 32%0 ( 1988)) 6°C and 30%0 ( 1989)) and
23°C and 35%0 ( 1990), respectively.
In 1988 and 1989, animals were acclimated in the laboratory to the following tempera-
tures: 5, 10, 15, 20 and 25”C, which are representative of the thermal cycle of the basin. In
1990, animals were acclimated to higher temperatures (20, 23, 26, 29 and 32”C), which
are representative of the summer temperatures in the holding ponds (Marennes-O&on) or
of the French Mediterranean coast.
‘For each experimental temperature, 38 oysters were maintained in 3 tanks of 20 litres of
1 pm filtered seawater. Each day, 10 litres was changed, and the waste material was removed
from the tank. The temperature and salinity were measured twice a day. Each day, a mixture
of 12.5 ml (concentration of 4. 106. ml- ‘) of Zsochrysis galbana (Tahititian close T. Iso)
and 8.3 ml (concentration of 6. 106. ml- ‘) of Chaetoceros calcitrans (in September 1988),
25 ml of T. Iso (February 1989), and 125 ml of T. Iso (September 1990) was added per
oyster. The rate of change from the initial temperature to the experimental temperatures
was 1°C per day (0.5”C a.m. and 0.5”C p.m.). Feeding was stopped 1 day prior to each
measurement as suggested by Weigert (1968). Animals were thus acclimated for 10 days
to stabilized experimental temperature, but fed for only 9 days.
Significant mortalities occurred at 32°C in September 1990, with only 17 oysters surviving
at the end of the acclimation period.
Individual dry tissue weight was measured after freeze-drying for 72 h.
Individual clearance rates were estimated by measuring the consumption of algae, added
to 0.22 pm filtered seawater in a flow-through system as described (Anonymous, 1987) :
CR= [(Z-@/Z] *F
S. Bougrieret al. /Aquaculture 134 (1995) 143-154 145
Fig. 1. The Marennes-Ol&on basin.
where I and 0 are, respectively, the algal concentration of the inflow (measured at the exit
of a sedimentation control tank) and outflow, and F (1. h- ‘) is the flow inside the meas-
urement chamber. Algal concentrations were estimated by using a Multisizer (Coulter,
Coultronics, Margency, France).
The rate of oxygen consumption was measured in a closed chamber of 500 or loo0 ml,
according to the size of each animal. These chambers contained 0.22 pm filtered seawater,
without addition of food. Salinities were natural salinities: 32% ( 1988), 30% ( 1989) or
35% ( 1990). Oxygen consumption was estimated as the rate of decrease of oxygen con-
centration inside the measurement chamber, as recorded by oxymeter probes (Orbsiphere
Laboratories, Orbisphere France, Maurepas, France).
Linear regression was used to describe the allometric relationship. Temperature and
season effects were tested with a two-factor ANOVA analysis. Non-linear regression was
used to establish statistical models:
V02= [a+(b*cr)] *DWd
where CR (1. h-‘) is the clearance rate, VOZ (mg 0,. h-‘) is the oxygen consumption, T
(“C) is the temperature, DW (g) is the dry tissue weight and a, b, c, d are constants.
146 S. Bougrier et al. /Aquaculture 134 (1995) 143-154
Allometric relationships with body size were established for each temperature and for
each experimental period (Tables 1 and 2). An exponent value of b < 1 was confirmed for
this species. The intercepts, or a values, representing clearance rates of an animal with 1 g
dry tissue weight, increased with temperature from 5°C (2.0 1. h- ‘) to 20°C (4.8 1. hh ‘),
and then decreased to 32°C (2.5 1. h- ’ ) . No significant difference (P > 0.05) was observed
between November 1988 and February 1989, suggesting that for a given temperature, the
season, outside of the reproductive period, had no effect on the clearance rate of the animal.
On the other hand, the effect of temperature was significant (P < 0.05).
Rates of oxygen consumption increased significantly with temperature from 5°C (0.2 mg
0,. hh’) to 32°C ( 1.9 mg 0,-h-‘). However, the changes in a values with increases in
temperature were different between seasons (P < 0.05). When the experimental tempera-
tures were lower than natural initial temperature, values decreased in an irregular way. In
September, an increase in oxygen consumption was observed between lO-15°C and 20-
25’C, meanwhile values were similar for 5°C and lo’%, and for 15°C and 20°C. On the
other hand, a change to a higher temperature than the initial (February 1989 and September
1990)) induced a gradual increase in the rate of oxygen consumption.
Descriptive statistical models of clearance rate (Fig. 2) and oxygen consumption (Fig.
3) for C. gigas related to dry tissue weight and temperature were estimated from non-linear
CR= [a- (b* (T-c)‘)] *DWd,
with a=4.825 f0.089, b=0.013 +O.OOl, c= 18.954kO.396, d=0.439f0.030, n=328,
Allometric relationships for clearance rate (CR = aW b, for different temperatures ( T) and seasons in C. gigas
Seasons T a b n r
September 1988 5 2.170
February 1989 5 2.014
September 1990 20 3.365
0.364 28 0.669 l
0.311 28 0.609 l
0.535 28 0.726’
0.326 28 0.505 *
0.640 21 0.888’
0.348 12 0.321
0.539 26 0.621.
0.312 29 0.540’
0.695 32 0.736’
0.190 22 0.577 *
0.707 12 0.595 *
0.422 13 0.595’
0.670 20 0.753’
0.663 16 0.514’
0.585 13 0.693 *
n = number of animals, r = correlation coefficient.
*Significant (P < 0.05) ANOVA for the model.
S. Bougrieret al. /Aquaculture 134 (1995) 143-154 147
Allometric relationships for oxygen consumption ( VOz = a W b, for different temperatures ( T) and seasons in C.
Seasons T a b n r
0.771 19 0.827’
0.823 30 0.871’
0.775 30 0.943’
0.945 27 0.901 l
0.865 26 0.957’
0.546 20 0.717’
0.949 32 0.845 *
0.715 26 0.741.
0.605 35 0.812’
0.905 35 0.875 *
0.811 22 0.870’
0.576 23 0.822’
0.863 23 0.858’
0.811 17 0.797 *
0.693 10 0.816’
n = number of animals, r = correlation coefficient.
‘Significant (P<O.O5) ANOVA for the model.
o 0 ! 1 1 I I I 1
I I I I I I 1
o 1 2 3 4 5 6 7 8
Predicted clearance rate (lb’)
Fig. 2. Predicted and observed clearance rates for C. gigas (observations = predictions is represented by the line).
VO,= [a+ (b*?)] *DWd,
witha= -0.432+0.219, b=0.613f0.200,c=1.042_+0.007,d=0.800f0.029,n=380,
A 3-D representation of these models is given in Figs. 4 and 5.
148 S. Bougrieret nl. /Aquaculture 134 (199s) 143-154
0.0 0.0 0.5 1.0 1.5 2.0 2.5 3.0
Predicted oxygen consumption (mg Or-h-‘)
Fig. 3. Predicted and observed oxygen consumption rates for C. &a~ (observations = predictions is represented
by the line).
Fig. 4.3-Drepresentationofclearancerate model for C. gigas: CR= 14.825 - (0.013* CT- 18.954)‘) 1 * JIWO.~~‘.
S. Bougrier et al. /Aquaculture 134 (1995) 143-154 149
Fig. 5.3-D representation of oxygen consumption rate model for C. gigas:
VOz = [ - 0.432 + (0.613 + 1.042=) ] * Dw800.
Rates of clearance and oxygen consumption for C. gigas were related to dry tissue weight,
by allometric relationships. In bivalve molluscs, these relationships are usually characterized
by an allometric coefficient less than unity, indicating that animals of small size filter and
consume oxygen proportionally more than animals of larger size. This may be explained
( 1) by a surface/mass exchange relationship [indeed, Hughes ( 1969) reported filtration
rates to the gill area, and Foster-Smith ( 1975, 1976 to total gill ostial area] ; (2) by the
difference of growth rates during the life of the animal. Hamburger et al. (1983) showed
b-values of oxygen consumption similar for the pelagic larval and juvenile stages, but
different for the adult. In fact, in C. gigas, in the first year energy needs are solely allocated
to somatic growth of the animal (Deslous-Paoli and H&al, 1988). Later, metabolism is
mainly directed to gamete maturation and spawning (Rodhouse, 1978; Bayne and Newell,
1983). The reproductive effort is responsible for an 18% energy loss for yearling oysters,
and about 63% during the second year (Deslous-Paoli and Heral, 1988).
The rates of both clearance and oxygen consumption depend on seawater temperature.
Clearance rates increased when the temperature increased up to a maximum of 19°C beyond
which the clearance rate decreased. On the other hand, oxygen consumption increased over
the entire range of temperatures tested.
Two types of response to changes of temperature have been described in the literature
for variously acclimated or experimentally treated bivalves. A gradual increase of clearance
rate with temperature has been noted by Walne ( 1972) in Mytilus edulis, by Walne ( 1972))
150 S. Bougrier et al. /Aquaculture 134 (1995) 143-154
Rodhouse ( 1978) and Hutchinson and Hawkins ( 1992) in Ostrea edulis, by Walne ( 1972),
Bernard ( 1974) and Kusuki ( 1978) in C. gigas, and for oxygen consumption by Widdows
(1973) in M. edulis, by Newell et al. (1977) and Rodhouse ( 1978) in 0. edulis, by Dame
(1972) in C. uirginicu, and by Bernard (1974) and Kim (1980) in C. gigas. The second
type of response is an increase of these functions to an optimum of temperature: Schulte
( 1975) and Widdows (1978) in M. edulis, Goulletquer et al. ( 1989) in Ruditupes philip-
pinurum, Newell et al. (1977) in C. virginicu, Le Gall and Raillard ( 1988) in C. gigus for
clearance rate, and Hutchinson and Hawkins ( 1992) in M. edulis, Goulletquer et al. ( 1989)
in R. philippinurum, Le Gall and Raillard ( 1988) in C. gigus, for oxygen consumption.
M. edulis and C. gigus results seem to be confused. This may be explained by: ( 1) Some
studies are based on natural acclimation, others on experimental acclimation for various
duration. Moreover, Widdows ( 1976) showed that immediate, short or long acclimation
induced different responses by mussels according to the natural thermal variations of the
rearing area. (2) The range of temperature in most of the studies quoted was insufficient to
show a possible optimum of temperature; the maximum tested in Walne ( 1972) was 2O”C,
which is the optimum for C. gigus in the results reported here.
Raillard et al. ( 1993) established a model of clearance rate for C. gigus, as a function of
dry tissue weight and seston load. Doering and Oviatt ( 1986) described for Merceruzriu
mercenariu a model combining temperature and length of the animal. Rodhouse ( 1978)
presented a model combining the dry tissue weight and temperature effects after a 6 days
acclimation in 0. edulis
In the model proposed here, the u-parameter (4.8) represents the clearance rate of an
individual of 1 g dry tissue weight at an optimum temperature of 19°C (c-parameter). The
relatively large b-value (0.013) shows the concavity of the symmetric curve, due to marked
parabolic effects of temperature ( [ T- c] *) , above and below the optimum c-value which
caused the maximal clearance rate. This value of approximately 19°C is considered to be
the minimal critical temperature inducing spawning in C. gigus (Gras et al., 197 1) . The d-
parameter represents the allometric coefficient related to dry tissue weight. Its value of
0.439 is similar to that reported for other bivalves (Thompson and Bayne, 1974; Schulte,
1975; Rodhouse, 1978; Widdows, 1978).
Concerning oxygen consumption related to dry tissue weight and temperature, twomodels
have been proposed in the literature: a linear model (Dame, 1972) for C. virginicu, and a
model for C. gigus (Kim, 1980)) in which the allometric coefficient was a function of
temperature. However, this latter model predicted higher oxygen consumption than is
observed in the Marennes-Ol&on basin, especially for high temperatures (Fig. 6). More-
over, in Kim’s study the effect of dry tissue weight seemed to be of little importance,
contrary to what is normally accepted.
The difference in oxygen consumption rates by the oysters in this study caused by changes
of temperature indicates that 10 days of acclimation was probably not enough to regulate
their metabolism. These differences may be related to the effect of temperature on the rate
of enzymatic activity involved in normal metabolism. Indeed, from an initial situation of
low enzyme activity (low metabolism in February at 6”C), the increased enzymatic activity
would be synchronous with the increase of temperature. On the other hand, when the activity
was high (September 1988), a decline of temperature would not induce immediate depres-
sion of enzymatic activity. However, observed oxygen consumption obtained in the field in
S. Bougrieret al. /Aquaculture 134 (1995) 143-154 151
-.- 0.5 g
5 8 11 14 17 20 23 26 29 32
Fig. 6. Oxygen consumption model rate for C. gigas proposed here, and that of Kim (1980) for 3 values of dry
natural acclimated oysters is in agreement with the model proposed here, based on experi-
mental acclimated animals (Bougrier, unpublished data).
In contrast, a model based on animals acclimated to temperatures higher than the initial
temperature was very similar to that obtained with all the animals. The model reported here
can be written: VOz = [a + be’“‘*] DWd. The natural logarithm (In) of c is analogous to the
QIO, which often indicates a doubling in metabolic rate for every 10°C rise in temperature.
In such a model, oxygen consumption is divided into two terms: aDWd + be’“cTDWd. Only
the second term is a function of temperature, doubling at 18°C. This value is close to the
temperature ( 19°C) inducing the maximal clearance rate. The term a + b indicates the
oxygen consumption rate for a 1 g dry tissue weight oyster at 0°C ( VOz = 0.18 mg . h- ’ ) .
The d-parameter is the allometric coefficient. Its value of 0.8 is similar to that generally
reported for bivalves (Bayne and Newell, 1983).
In aquaculture, the areas for rearing are chosen based on the nutritional potential of the
system and the energy needs of the animals. A knowledge of the physiological functions of
food acquisition and metabolic loss could provide information, although incomplete, on the
probable success of rearing such species in that area. The surface response of the ratio of
oxygen consumption/ingestion, expressed in term of energy, for different diets can give
such information. Indeed, assimilated energy should represent about 80% of the ingested
energy (Thompson and Bayne, 1974; Winter, 1978). It means that for no net production,
at which catabolism (loss of energy = respiration = oxygen consumption) and anabolism
(tissue acquisition of energy = assimilation = 0.8 *ingestion) are equal, the ratio, in terms
of energy, oxygen consumption/ingestion (VO,/I) would be 0.8. In that case, the energy
needs for a 1 g dry weight oyster, at no net production and under the pseudofaeces threshold
hypothesis (ingestion = clearance rate * food availability), were about 3 J. l- ’ for 5°C
and 13 J. l-‘, nearly 4 times greater, for 32°C (Fig. 7). Thus, the animal will grow (Fig.
8, white area, VO,/I < 0.7), survive (Fig. 8, black area, 0.8 < VOz/I > 0.7) or die (Fig. 8,
grey area, VO,/I > 0.8) depending on the combined effect of temperature and food avail-
ability, as did half of the oysters during the 32°C acclimation experiment. This temperature
S. Bougrier et al. /Aquaculture 134 (1995) 143-154
Fig. 7. Relationship of clearance rate, oxygen consumption (circles) and necessary diet (squares) for no net
production (VO& = 0.8; see text) for a 1 g dry tissue weight C. gigas related to temperature (5-32°C).
5 7 9 11 13 15 17 19 21 23 25 27 29 31
Fig. 8. Values of the ratio VO,/l, (0.1-1.2) for a 1 g dry tissue weight C. gigas for different temperatures and
would be the upper thermal limit for C. gigas, confirming the observations of Le Gall and
Raillard ( 1988) who estimated it at 30°C.
Relationships reported here are for animals outside of their reproductive period. The
models are probably not applicable during the reproductive period. Bensch et al. ( 1991),
modelling the growth of R. philippinurum in an experimental system, could not relate their
S. Bougrier et al. /Aquaculture 134 (1995) 143-154 153
results to data collected just after spawning. Deslous-Paoli et al. ( 1987) reported an increase
in the clearance rate during the period of gamete maturation. On the other hand, lower
values for oxygen consumption and clearance rates than predicted by the model were
observed at the end of gamete maruration (Soletchnik, personal communication).
The authors are indebted to Drs. Brian L. Bayne, David J. Wildish, two anonymous
reviewers and the Editor, Robert P. Wilson, for their criticism, suggestions and aid in
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