- Email: [email protected]
Effects of different feeding regimens on larval growth and the energy budget of juvenile Chilean scallops, Argopecten purpuratus Lamarck
Aquaculture ELSEVIER
Aquaculture 132 (1995) 313-323
Effects of different feeding regimens on larval growth and the energy budget of juvenile Chilean scallops, Argopecten purpuratus Lamarck G. Martinez*, L.A. Caceres, E. Uribe, M.A. Diaz Facultad de Ciencias de1 Mar, Universidad Catdlica de1 None, Casilla I1 7, Coquimbo, Chile
Accepted 15 November 1994
Abstract Effects of continuous and discontinuous feeding regimens on growth and survival of Argopecren purpurarus larvae and the partitioning of energy in juveniles are presented. Larvae from a single cohort were cultured under three feeding regimens: ( 1) fed once a day, (2) fed twice a day and (3) fed continuously, while keeping the total daily amount of food equal for each treatment. Larvae cultured under the continuous feeding regimen had faster growth and higher survival than those fed discontinuously. Early juveniles from a single cohort of larvae wereculturedunder the same conditions as larvae. Organic weight, energy content, filtration rate, oxygen consumption and excretion rate were measured after 16 days under these regimens. Maximal increase in shell length and in ash-free dry weight was attained by those juveniles fed continuously. No significant difference in energy content was found between the three groups of individuals. Juveniles fed continuously showed a higher metabolic rate than those fed once or twice a day. Ingestion rate and ammonia excretion did not differ significantly among individuals in the three feeding regimens. Results indicate there is better assimilation of food in both larvae and juveniles under a continuous feeding regimen. Keywords: Arg’“pectenpurpuratus; Feeding and nutrition -
molluscs; Growth-molluscs; Assimilation efficiency
1. Introduction
Successful hatchery culture of larval and juvenile bivalves requires detailed knowledge of conditions needed to produce maximum growth and to ensure quality. Among these factors, food availability is important (Winter, 1977; Griffiths and King, 1979; Bayne and Newell, 1983), however, growth is influenced not only by the total amount of food but also * Correspondingauthor. Fax (56-5 1) 3 11287. 0044.8486/95/$09.50
0 1995 Elsevier Science B.V. All rights reserved
SSDlOO44-8486(94)00359-9
314
G. Martinez et al. /Aquaculture
132 (1995) 313-323
by the feeding regimen (Langton and McKay, 1976; Winter, 1977). In nature, suspension feeders are dependent on water movements to bring food to them. Water flow and food concentration interact to determine the supply of food, and contribute to the rate and efficiency of particle capture (Cahalan et al., 1989). We investigated conditions for optimum development and growth of larvae and juveniles of the Chilean scallop, Argopecten purpuratus Lamarck ( 1819). Martinez et al. ( 1992) showed that early juvenile A. purpuratus held under hatchery conditions had slower growth rates than animals held in the ocean. Dfaz and Martinez (1992) showed that maximum growth of larvae and juveniles of this species was obtained when they were fed a mixture of Isochrysis galbana (T-iso), Chaetoceros calcitrans and Nannochloropsis oculata. However, in both studies, the feeding regimen was discontinuous (twice a day). This paper describes studies of the effect of continuous and discontinuous feeding regimens on growth and survival of A. purpuratus larvae, together with an analysis of the partitioning of energy in juveniles when fed under the different regimens. The partitioning of available energy resources into growth and maintenance requirements was used to provide an index by which environmental effects can be evaluated directly (Johns, 1982).
2. Materials and methods Larval experiments Mature adult scallops (Argopectenpurpuratus) (8-10 mm shell length) from Herradura Bay, Coquimbo, Chile, were induced to spawn. Fertilization and larval rearing were carried out according to the method of DiSalvo et al. ( 1984). When larvae developed to the straight hinge stage, feeding began using a mixture of Isochrysis galbana (T-iso), Chaetoceros calcitrans and Nannochloropsis oculata. Three feeding regimens were studied: once-a-day feeding, twice-a-day feeding and continuous feeding. The total amount of microalgae added to each tank was the same on any one day for the three feeding regimens. Experimental tanks were maintained under constant aeration and held at 18 f 1°C. Every second day the tanks were cleaned, live larvae counted and the water volume adjusted in order to maintain similar larval densities in each tank and to assure equal amounts of food to the larvae. Shell dimensions, in both dimensions (anteriorposterior and dorsal-ventral) of a random sample of 70 larvae were measured with a Zeiss adjustable ocular micrometer to determine growth rate. As a good correlation (r = 0.99, P < 0.01) between both dimensions was found, size was expressed as a function of anteriorposterior length. The experiment was carried out twice, in March (Expt. 1) and in September 1992 (Expt. 2)) under identical conditions. Since the initial number of larvae was higher in the second experiment than in the first, much care was taken to maintain the same larval density in both studies. Post-larval experiments Early juvenile A. purpuratus (post-larvae) were obtained from a single batch of larvae cultured according to the method of DiSalvo et al. ( 1984) and fed a mixture of 1. galbana, C. calcitrans and N. oculata once a day.
G. Martinez et al. /Aquaculture
132 (1995) 313-323
315
When the juveniles were about 700 pm shell length, a sample was taken to determine the ash-free dry weight and energy content. The remaining juveniles were divided into three groups and subjected to the same three feeding regimens as used in the larval experiments. After 16 days, a sample of about 200 juveniles from each group was measured for anteriorposterior shell length (using an optical micrometer), washed with isotonic ammonium formate, dried to constant weight and placed in a muffle furnace at 500°C for 5 h to determine the ash content. From these values the ash-free dry weight (a.f.d.w.) was calculated (referred to as “organic matter” or “organic weight”). Another sample of individuals of each group was ignited in an OSK calorimeter to determine their energy content. The remaining individuals of the same groups were used to measure the physiological processes involved in the utilization of energy budget considering that: C=P+R+U+F Absorption Assimilation
= C-F = P + R (Bayne and Newell, 1983; Crisp, 1984)
where C = total intake of food or energy; P = portion of assimilated food that is incorporated into the biomass (production) ; R = portion of assimilated energy used for metabolic expenditure via respiration; U = that part of the consumption that is absorbed and later passed out of the body as secreted material, e.g., in the urine; F = portion of energy consumed that was not absorbed. but voided as feces. Consumption (C) was determined by ingestion rate assuming that ingestion rate = filtration rate X particle concentration (Sprung, 1984b), Filtration rate was determined by the indirect method, measuring removal of suspended particles from a known volume of water per unit time (Winter, 1977). In order to express consumption as amount of organic matter ingested, ash-free dry weight was obtained after ashing a sample of the microalgae mixture in a muffle furnace at 500°C. Production (P) was calculated as the difference between the ash-free dry weight of juveniles at the beginning and end of the experimental period. At each sampling, a group of individuals was washed with isotonic ammonium formate, dried to constant weight, ashed at 500°C and reweighed. Respiration (R) was determined by oxygen consumption using a Warburg constantpressure respirometer. The rates quoted were: ~1 O2 .individual-’
‘h-i.
Excretion (U) rate was calculated as the difference between the ammonia content of water in flasks with and without animals and was considered as pg NH: and converted to heat loss using the energy equivalent 0.00737 joules per ug NH: (Logan and Epifanio, 1978). Ammonia content was determined using the method of Solorzano ( 1969). EfJiciencies With the data on growth, food uptake and respiration, the following efficiencies were estimated. Assimilation efSiciency. Considered as that part of the ingested food that is retained for physiological purposes, namely for production and respiration, excluding excreta (F and U) (Bayne 1983; Sprung, 1984d; Crisp, 1984). It was calculated by:
316
G. Martinez et al. /Aquaculture
E = ( (Respiration
132 (1995) 313-323
rate + Growth rate) /Ingestion
rate) X 100
Respiration rate was expressed as the equivalent of organic weight considering 1 mg per 1.2 ml of O2 consumed (Laing and Millican, 1986). Growth rate was expressed as the organic biomass increase and ingestion rate as the organic weight of microalgae consumed in the unit time. Gross growth efficiency. As the proportion of the organic weight consumed converted into organic biomass, gross growth efficiency was calculated as: K, =Z/C (Sprung,
1984d).
Net growth ejficiency. Considered as the proportion of the assimilated converted to growth, net growth efficiency was calculated as:
K2 =Zl(I+R)
that was
(Sprung,
food which is
1984d)
3. Results Larval experiments Growth Larval growth, as measured by increases in shell length, under the three different feeding regimens is shown in Fig. 1. In both experiments (March and September, 1992), analysis of covariance of the fitted lines showed that the slopes were significantly different (F2,m = 24.9 1, P < 0.00 1 for Expt. 1 and F2,939= 8.73, P < 0.001 for Expt. 2). A test a posteriori showed that larvae under the continuous feeding regimen had faster growth rates than those fed twice or once a day. Yet, in Experiment 1, larvae fed twice a day had faster growth rates than those fed once a day (Neumann-Keuls test, P < 0.01; Zar, 1974). Survival In spite of having used different numbers of larvae in Experiment 1 than in Experiment 2, the results of both studies showed that continuous feeding resulted in higher survival of larvae than the other two feeding regimens (Table 1) . Post-larval experiments Final length, organic matter and energy content An analysis of variance showed that size and organic content (ash-free dry weight) of juvenile A. purpuratus were affected by feeding regimen (Table 2). Juveniles fed continuously attained a larger size and had a higher content of organic components than individuals in the other two feeding regimens (Table 3). In the two groups of juveniles fed discontinuously, those fed twice a day showed larger final length than those fed once a day (Tukey’s
G. Martinez et al. /Aquaculture
317
0
Exp. 1
ZlO-
132 (1995) 313-323
5.3-
D .
0 .. .
,.
5.1
-
4.9
-
170-
130-
t 4.7l
E a.
. _
90
= I
I
!
I
I
I
I
: vr aI
5
Exp. 2
180-
=
5.1
-
.p
0 (I 150-
.
:
D
4.9-
’
: 120-
D
4.7
-
* . so
I 4
, 2
I 6
I 8
Days
.
ODES
x
twice
0
continuous
4.5
I1 12
, 10
I 2
14
after
1 4
I 6
1 8
1 10
I 12
1 14
fertilization
a dry a da!
__
o”ce
-----
twice
a day a day
continuous
Fig. 1. Argopecten purpurufus larval shell length on different days after fertilization and fed under three different feeding regimens. Each point is the mean of 60 (Expt. 1) or 45 measurements (Expt. 2). The lines fitted to these points are represented on the right side of the figure.
test, P < 0.05). No significant difference fed the different feeding regimens. Physiological
processes
was found between energy content of juveniles
implied in the energy budget
Analysis of ingestion, oxygen consumption, ammonia excretion and production rate (expressed as increase in organic weight), showed that oxygen consumption and production rate were affected significantly by the feeding regimen in juvenile A. purpuratus (Table 4). Coincident with a higher growth rate, those juveniles fed continuously spent a higher amount of energy for metabolic demands than juveniles fed twice a day (Tukey test, P < 0.05). We
G. Martinez et al. /Aquaculture I32 (1995) 313-323
318
Table 1 Number of live Argopecten purpuratus larvae remaining regimens Expt.
Final number of larvae Percentage
1 2 1 2
of survival
when cultured for 15 days under three different feeding
Feeding regimens Once a day
Twice a day
Continuous
28 000 888 000 1.0 6.9
118 500 1 240 000 4.3 9.6
369 000 1990 000 13.3 15.4
Total amount of microalgae fed was the same for each regimen, 52.5 cells/$/day. for each group of larvae and for both experiments.
Larval density was the same
Table 2 Analysis of variance of final shell length, organic matter and energy content ofjuveniles of Argopectenpurpuratus from a single batch of larvae when cultured for 16 days under three different feeding regimens Source of variation
Degrees of freedom
Length Between groups Within groups
2 609
Organic matter Between groups Within groups
2 15
Energy content Between groups Within groups
2 12
Sum of squares
14.9794 53.0279
3426.33 5309.66
0.38449 11.51037
F-ratio
P
86.02
< 0.001
4.84
< 0.05
0.21
> 0.05
Table 3 Final shell length, organic weight and energy content of juveniles of Argopecten purpurarus from a single batch of larvae when cultured for 16 days under three different feeding regimens
Once a day Length
1.46 f 0.03
(mm) Organic weight
71.00 f 7.78
(pg/ind.) Energy content
2.75 f 0.65
(J/ind.) Values are means f s.d.
Twice a day 1.63 f 0.02 72.16rt6.62 2.54 f 0.28
Continuous 1.84kO.03 100.83 *8.51 2.36 kO.23
G. Martinez et al. /Aquaculture
132 (1995) 313-323
319
Table 4 Physiological processes involved in the utilization of energy by juveniles of Argopectenpurpuratus of 16 days when cultured under three different feeding regimens Feeding regimen
Once a day Twice a day Continuous
over a period
Ingestion rate (cell/h/ind.)
Respiration rate (~1 O,/h/ind.)
Ammonia excretion (pg NH.Jh/ind.)
Production
127 (63 86 (63 72 (22
0.2821 (0.087) 0.2442 (0.082) 0.3339 (0.086)
1.31 x10-a (0.95 x 10-a) 2.86x 10-s (2.29~ 10-a) 4.32~ lo-* (2.03x IO-*)
0.1121 (0.027) 0.1175 (0.024) 0.1921 (0.031)
955 899) 385 899) 724 701)
Analysis of variance for respiration
and production
(kg MO/h/ind.)
rate
Source of variation
Degrees of freedom
Sum of squares
Respiration Between groups Within groups
2 33
0.0487177 0.2419615
3.32
0.0485
Production Between groups Within groups
2 15
0.024007 1 0.0347372
5.18
0.0194
F-
P
ratio
Values are means (sd.). Table 5 Assimilation efficiencies (AR), gross growth efficiencies (K,) and net growth efficiencies (Kz) calculated from data of Table 4, transformed to organic weight equivalent, of juveniles of Argopecten purpuratus cultured under three different feeding regimens Feeding regimen
AE (%)
Ki (%)
Kz (%)
Once a day Twice a day Continuous
19.07 26.31 45.64
6.19 9.6 18.65
32.5 36.6 40.87
expressed this rate as oxygen consumed per mg ash-free dry weight, and then respiratory rate of juvenile scallops fed continuously did not differ from that of the other two groups of animals (3.51 ~1 as opposed to 3.52 ~1 O,/h/mg a.f.d.w. for animals fed twice a day and 4.15 ,zl O*/h/mg a.f.d.w. for animals fed once a day). Efficiencies estimated from data of ingestion, oxygen consumption and production showed that juveniles fed continuously had a higher assimilation efficiency than those individuals that received the same amount of food but supplied as one or two portions (Table 5). The best gross and net growth efficiency was obtained when juveniles were fed continuously.
320
G. Martinez et al. /Aquaculture I32 (1995) 313-323
4. Discussion
The faster growth and higher survival observed in A. purpuratus larvae fed continuously probably reflects better utilization of food. Growth and survival of bivalve larvae depend on several factors including an adequate food supply (Sprung, 1984a; Widdows, 1991). Previous studies on larval and juvenileA.purpuratus have shown that good growth occurred when they were fed a mixture of three species of algae (Diaz and Martinez, 1992). However, an adequate food supply does not only mean food quality but also appropriate availability. There is a food concentration level below which particles cannot be collected at maximum rates (Bayne, 1983; Pechenik, 1987). Rates of larval development tend to increase with increasing food concentration until a critical cell density is attained. Above this density a decline in growth may occur for several reasons: clogging of the feeding apparatus (Pechenik, 1987); larvae may become entangled in a net of pseudofeces (Sprung, 1984b); and larvae may react negatively to dissolved substances such as algal metabolites (Sprung, 1984b). When food is supplied in one or two portions per day, cell density is higher for an initial period of time than when the same total amount of microalgae is provided continuously. When cell density exceeds the upper critical level, the food provided to larvae will not be filtered and ingested efficiently. Results obtained in this study for juvenile A. purpuratus are similar to those described by Winter (1977) for juvenile Myths edulis. He showed that when the same amount of food was fed continuously to juvenile mussels, the increase in dry tissue weight was approximately twice as high as when animals were fed discontinuously. Langton and McKay ( 1976) found the opposite when they fed juvenile Crassostrea gigas at two food levels and four feeding regimes. Discontinuous feeding gave faster growth than continuous feeding. The difference between their results and those in the present study may be due to the fact that C. gigas is an intertidal mollusc and adapted to a discontinuous food supply while A. purpuratus is a subtidal bivalve adapted to a continuous food supply. That juveniles which attained the largest size and the highest content of organic components did not have a higher energy content but rather a lower (although not significant) content than the other individuals, may look surprising. Energy is not the only factor that is necessary for good growth. The heat released by juveniles in a calorimeter reflects their biochemical composition. A high energy content may mean a higher proportion of lipid. It is known that the the combustion of 1 g of lipid produces about twice caloric energy than 1 g of protein or carbohydrate. Lipids, and secondly proteins, have been suggested as the major energy reserves for bivalve larvae development and metamorphosis (Holland and Spencer, 1973; Gabbott, 1983; Mann and Gallager, 1985a). After metamorphosis there is a transition from this lipid-protein based energy metabolism to a carbohydrate-protein metabolism in the juvenile and adult stages (Gabbott, 1983; Mann and Gallager, 1985b; Moss Lane, 1986). Fidalgo et al. ( 1994) studying the food value of different microalgal diets to juvenile Myths galloprouincialis, have shown a significant positive correlation between growth rate and body lipid. Similar results had been obtained by Laing and Millican ( 1986) with cultured Ostrea edulis spat. Martinez et al. ( 1992) found that early juveniles of A. purpuratus held in the ocean during 40 days attained a larger size and contained less lipid than a group of individuals of the same brood, reared in the hatchery. The energy
G. Martinez
et al. /Aquaculture
132 (1995) 313-323
321
content, calculated from their biochemical composition, gave a higher value for the second group of juveniles. Although all individuals were supplied daily with the same food, animals that are fed discontinuously may be loosing a percentage of an essential component needed for growth. Then, those animals that grow more slowly may be lacking enough of some specific nutrient (different from lipid) that is essential for growth. The importance of this specific nutrient might not be in supplying energy, but rather it might be an essential precursor for macromolecules: e.g., some amino acid or vitamin. Kreeger and Langdon (1993) have shown that growth of juvenile Myfilus trossulus can be limited by dietary protein level. One must keep in mind that the scallops used in the present study correspond to early juveniles of less than 40 days after metamorphosis. Whyte et al. (1992) found a 58.3% decline in total energy of juveniles of the scallop, Cvussadoma gigunteu, during the transition of larvae to juveniles for 25 days after settlement. Holland and Spencer (1973) found a similar decrease in energy content in Ostrea edulis from pre-metamorphic larvae to early juveniles (in both cases, there was a good increase in the size of individuals). In our previous study, when different mixtures of microalgae were fed to growing early juvenile A. purpurutus, the mixture that produced the best growth was not that which produced the highest energy content (Diaz and Martinez, 1992). Juveniles of A. purpuratus fed under a continuous feeding regimen showed a better growth rate than individuals that were supplied the same daily amount of food in one or two portions. Growth studies under different food concentrations have shown that, above critical food densities, the growth rate declines (Thompson and Bayne, 1974; Winter, 1977; Griffiths and King, 1979; Widdows et al., 1979; Bayne, 1983; Cahalan et al., 1989). High particle concentrations increase the production of feces and pseudofeces (Widdows et al., 1979) and this may result in a significant loss of nutrients and consequent decreased growth (Cahalan et al., 1989). A decline in absorption efficiency has been commonly observed in laboratory experiments with increasing ration of microalgae (Thompson and Bayne, 1972, 1974; Navarro et al., 1991). The digestive system has functional capacity limits to the net uptake of nutrients. This determines a negative relationship between the amount of food that may be processed per unit time (ingestion rate) and the time it takes to traverse the digestive tube (Navarro and Iglesias, 1993). Bayne et al. ( 1989) have shown this negative relationship between ingestion rate and gut passage time for M. edulis fed a mixed algal and silt diet. In the present study, feces could not be collected, hence absorption efficiency could not be measured, but assimilation efficiency was calculated from growth rate and respiration rate data according to Sprung ( 1984d). Bayne (1983) distinguished between absorption and assimilation efficiency; the latter represents the part of cleared food that is effectively used to increase biomass. The greatest assimilation efficiency was obtained for those scallops that received the food in a continuous regimen. A continuous feeding regime permits a more or less steady food intake and improves digestion and assimilation of nutrients (Winter, 1977). Filter feeding activity has a metabolic cost (Sprung 1984~) and following a period of starvation this cost is higher than when feeding is continuous (Bayne and Scullard, 1977). Hence a continuous food supply may require a lower metabolic activity for filtering than a discontinuous feeding regime. The higher assimilation efficiency together with the higher gross and net growth efficiencies in animals fed continuously confirms our conclusion that under this feeding regimen
322
G. Martinez et al. /Aquaculture 132 (1995) 313-323
there is better utilization of the food. This is an important when juvenile bivalves are produced in hatcheries.
factor that must be considered
Acknowledgements We wish to express our thanks to Dr. Neil Bourne for his kind assistance in reviewing the manuscript. We are indebted to Dr. John Himmelman and two anonymous reviewers for helpful suggestions to improve the manuscript. Our acknowledgments to Mr. Raul Vera, Mr. Carlos Solar and the staff of the Unidad de Production of Facultad de Ciencias de1 Mar, Universidad Catolica de1 Norte, for their technical assistance. This study was partly funded by FDP-CORFO, Chile.
References Bayne, B.L., 1983. Physiological ecology of marine molluscan larvae. In: N.H. Verdonk, J.A.M. van den Biggelaar and AS. Tompa (Editors), The Mollusca, Vol. 3, Development. Academic Press, Orlando, FL, pp. 299-343. Bayne, B.L. and Newell, R.C., 1983. Physiological energetics of marine molluscs. In: A.S M. SaIeuddin and K.M. Wilbur (Editors), The Mollusca. Vol. 4, Physiology, Part I. Academic Press, New York, NY, pp. 407-5 15. Bayne, B.L. and Scullard, C., 1977. An apparent specific dynamic action in Myrilus edulis L. J. Mar. BioI. Assoc. UK, 57: 371-378. Bayne, B.L., Hawkins, A.J.S., Navarro, E. and Iglesias, I.P., 1989. Effects of seston concentration on feeding, digestion and growth in the mussel Mytilus edulis. Mar. Ecol. Prog. Ser., 55: 47-54. CahaIan, J.A., SiddaII, S.E. and Luckenbach, M.W., 1989. Effects of flow velocity, food concentration and particle flux on growth rates ofjuvenile bay scallops Argopecfen irradians. J. Exp. Mar. BioI. Ecol., 129: 45-60. Crisp, D.J., 1984. Energy flow measurements. In: N.A. HoIme and A.D. McIntyre (Editors), Methods for the Study of Marine Benthos, 2nd edn. Blackwell Publications, Oxford, pp. 284-372. Dfaz, M.A. and Martinez, G., 1992. Efecto de diferentes dietas sobre e1 balance energetic0 en juveniles de Argopectenpurpuratus L. Rev. BioI. Mar., 27(2): 163-173. DiSaIvo, L.H., Alar&, E., Martinez, E. and Uribe, E., 1984. Progress in mass culture of Chlamys (Argopecren) purpuruta (1819) with notes on its natural history. Rev. ChiI. Hist. Nat., 57: 3545. Fidalgo, J.P., Cid, A., Lopez-Mufioz, I., Abalde, J. and Herrero, C., 1994. Growth and biochemical profile of juvenile mussels (Mvzilus galloprouincialis Lmk) fed on different algal diets. J. Shell. Res., 13(I): 67-75. Gabbott, P.A., 1983. Developmental and seasonal metabolic activities in marine molluscs. In: P.W. Hochachka (Editor), The MoIIusca, Vo1.2, Environmental Biochemistry and Physiology. Academic Press, New York, NY, pp. 165-217. Griffiths, CL. and King, J.A., 1979. Some relationships between size, food availability and energy balance in the ribbed mussel Aulacomya uter. Mar. Biol., 51: 141-149. Holland, D.L. and Spencer, B.E., 1973. Biochemical changes in fed and starved oysters, Ostrea edulis L. during larval development, metamorphosis and early spat growth. J. Mar. Biol Assoc. UK, 53: 287-298. Johns, D.M., 1982. Physiological studies on Cancer irroratus larvae. III. Effects of temperature and salinity on the partitioning of energy resources during development. Mar. EcoI. Prog. Ser., 8: 75-85. Kreeger, D.A. and Langdon, C.J., 1993. Effect of dietary protein content on growth of juvenile mussels, Mytilus trossulus (Gould 1850). BioI. Bull., 185: 123-139. Laing, I. and Millican, P.F., 1986. Relative growth and growth efficiency of Ostrea edulis L. spat fed various algal diets. Aquaculture, 54: 245-262. Langton, R.W. and McKay, G.U., 1976. Growth of Crassostrea gigm (Thunberg) spat under different feeding regimes in a hatchery. Aquaculture, 7: 225-233. Logan, D.I. and Epifanio, C.E., 1978. A laboratory energy balance for the larvae and juveniles of the American lobster Homarus americanus. Mar. Biol.. 47: 381-389.
G. Martinez et al. /Aquaculture
132 (1995) 313-323
323
Mann, R. and Gallager, S.M., 1985a. Physiological and biochemical energetics of larvae of Teredo nmalis L. and Eat&a gouldi (Bartsch) (Bivalvia: Teredinidae). J. Exp. Mar. Biol. Ecol., 85: 21 l-228. Mann, R. and Gallager, SM., 1985b. Growth, morphometry and biochemical composition of the wood boring molluscs Teredo naualis L., Bar&a gouldi (Bartsch), and Nototeredo knoxi (Bartsch) (Bivalvia: Teredinidae). J. Exp. Mar. Biol. Ecol., 85: 229-251. Martinez, G., Torres, M., Uribe, E., Dfaz, M.A, and Perez, H., 1992. Biochemical composition of broodstock and early juvenile Chilean scallops, Argopecten purpuratus Lamarck, held in two different environments. J. Shell. Res., ll(2): 307-313. Moss Lane, J., 1986. Allometric and biochemical studies on starved and unstarved clams, Rangia cuneata (Sowerby, 1831). J. Exp. Mar. Biol.Ecol.,95: 131-143. Navarro, E. and lglesias, J.I.P., 1993. Infaunal filter-feeding bivalves and the physiological response to short-term fluctuations in food availability and composition. In: R.F. Dame (Editor), NATO AS1 Series, Vol. G 33, Bivalve Filter Feeders in Estuarine and Coastal Ecosystem Processes. Springer-Verlag. Berlin-Heidelberg. Navarro, E., Iglesias, J.I.P., Perez Camacho, A., Labarta, U. and Beiras, R., 1991. The physiological energetics of mussels (Mytilus galloprouincialis Lmk) from different cultivation rafts in the Ria de Arosa (Galicia, N.W. Spain). Aquaculture, 94: 197-212. Pechenik, J.A., 1987. Environmental influences on larval survival and development. In: A.C. Giese, J.S. Pearse and V.B. Pearse (Editors), Reproduction of Marine Invertebrates, Vol. IX. Blackwell Scientific Publications, Palo Alto, CA, pp. 551608. Solorzano, L., 1969. Determination of ammonia in natural seawaters by the phenolhypochlorite method. Limnol. Oceanogr., 14: 799-801. Sprung, M., 1984a. Physiological energetic of mussel larvae (Mvtilus edulis). I. Shell growth and biomass. Mar. Ecol. Prog. Ser., 17: 283-293. Sprung, M., 1984b. Physiological energetic of mussel larvae (Mytilus edulis). Il. Food uptake. Mar. Ecol. Prog. Ser., 17: 295-305. Sprung, M., 1984~. Physiological energetic of mussel larvae (Mytilus edulis). III. Respiration. Mar. Ecol. Prog. Ser., 18: 171-178. Sprung, M., 1984d. Physiological energetic of mussel larvae (Myths edulis). IV. Efficiencies. Mar. Ecol. Prog. Ser., 18: 179-186. Thompson, R.J. and Bayne, B.L., 1972. Active metabolism associated with feeding in the mussel Mytilus edulis L. J. Exp. Mar. Biol. Ecol., 9: 111-124. Thompson, R.J. and Bayne, B.L., 1974. Some relationships between growth, metabolism and food in the mussel, Mytilus edulis. Mar. Biol., 27: 317-326. Whyte, J.N.C., Bourne, N., Ginther, N.G. and Hodgson, CA., 1992. Compositional changes in the larva to juvenile development of the scallop Crassadoma gigantea (Gray). J. Exp. Mar. Biol. Ecol., 163: 13-29. Widdows, J., 1991. Physiological ecology of mussel larvae. Aquaculture, 94: 147-163. Widdows, P., Fieth, P. and Worrall, C.M., 1979. Relationship between seston, available food and feeding activity in the common mussel Mytilus edulis. Mar. Biol., 50: 195-207. Winter, J.E., 1977. Suspension-feeding in lamellibranquiate bivalves, with particular reference to Aquaculture. Medio Ambiente, 3( 1): 48-69. Zar, J.H. 1974. Biostatistical Analysis. Prentice Hall, Inc., Englewood Cliffs, NY, 619 pp.
Aquaculture 132 (1995) 313-323
Effects of different feeding regimens on larval growth and the energy budget of juvenile Chilean scallops, Argopecten purpuratus Lamarck G. Martinez*, L.A. Caceres, E. Uribe, M.A. Diaz Facultad de Ciencias de1 Mar, Universidad Catdlica de1 None, Casilla I1 7, Coquimbo, Chile
Accepted 15 November 1994
Abstract Effects of continuous and discontinuous feeding regimens on growth and survival of Argopecren purpurarus larvae and the partitioning of energy in juveniles are presented. Larvae from a single cohort were cultured under three feeding regimens: ( 1) fed once a day, (2) fed twice a day and (3) fed continuously, while keeping the total daily amount of food equal for each treatment. Larvae cultured under the continuous feeding regimen had faster growth and higher survival than those fed discontinuously. Early juveniles from a single cohort of larvae wereculturedunder the same conditions as larvae. Organic weight, energy content, filtration rate, oxygen consumption and excretion rate were measured after 16 days under these regimens. Maximal increase in shell length and in ash-free dry weight was attained by those juveniles fed continuously. No significant difference in energy content was found between the three groups of individuals. Juveniles fed continuously showed a higher metabolic rate than those fed once or twice a day. Ingestion rate and ammonia excretion did not differ significantly among individuals in the three feeding regimens. Results indicate there is better assimilation of food in both larvae and juveniles under a continuous feeding regimen. Keywords: Arg’“pectenpurpuratus; Feeding and nutrition -
molluscs; Growth-molluscs; Assimilation efficiency
1. Introduction
Successful hatchery culture of larval and juvenile bivalves requires detailed knowledge of conditions needed to produce maximum growth and to ensure quality. Among these factors, food availability is important (Winter, 1977; Griffiths and King, 1979; Bayne and Newell, 1983), however, growth is influenced not only by the total amount of food but also * Correspondingauthor. Fax (56-5 1) 3 11287. 0044.8486/95/$09.50
0 1995 Elsevier Science B.V. All rights reserved
SSDlOO44-8486(94)00359-9
314
G. Martinez et al. /Aquaculture
132 (1995) 313-323
by the feeding regimen (Langton and McKay, 1976; Winter, 1977). In nature, suspension feeders are dependent on water movements to bring food to them. Water flow and food concentration interact to determine the supply of food, and contribute to the rate and efficiency of particle capture (Cahalan et al., 1989). We investigated conditions for optimum development and growth of larvae and juveniles of the Chilean scallop, Argopecten purpuratus Lamarck ( 1819). Martinez et al. ( 1992) showed that early juvenile A. purpuratus held under hatchery conditions had slower growth rates than animals held in the ocean. Dfaz and Martinez (1992) showed that maximum growth of larvae and juveniles of this species was obtained when they were fed a mixture of Isochrysis galbana (T-iso), Chaetoceros calcitrans and Nannochloropsis oculata. However, in both studies, the feeding regimen was discontinuous (twice a day). This paper describes studies of the effect of continuous and discontinuous feeding regimens on growth and survival of A. purpuratus larvae, together with an analysis of the partitioning of energy in juveniles when fed under the different regimens. The partitioning of available energy resources into growth and maintenance requirements was used to provide an index by which environmental effects can be evaluated directly (Johns, 1982).
2. Materials and methods Larval experiments Mature adult scallops (Argopectenpurpuratus) (8-10 mm shell length) from Herradura Bay, Coquimbo, Chile, were induced to spawn. Fertilization and larval rearing were carried out according to the method of DiSalvo et al. ( 1984). When larvae developed to the straight hinge stage, feeding began using a mixture of Isochrysis galbana (T-iso), Chaetoceros calcitrans and Nannochloropsis oculata. Three feeding regimens were studied: once-a-day feeding, twice-a-day feeding and continuous feeding. The total amount of microalgae added to each tank was the same on any one day for the three feeding regimens. Experimental tanks were maintained under constant aeration and held at 18 f 1°C. Every second day the tanks were cleaned, live larvae counted and the water volume adjusted in order to maintain similar larval densities in each tank and to assure equal amounts of food to the larvae. Shell dimensions, in both dimensions (anteriorposterior and dorsal-ventral) of a random sample of 70 larvae were measured with a Zeiss adjustable ocular micrometer to determine growth rate. As a good correlation (r = 0.99, P < 0.01) between both dimensions was found, size was expressed as a function of anteriorposterior length. The experiment was carried out twice, in March (Expt. 1) and in September 1992 (Expt. 2)) under identical conditions. Since the initial number of larvae was higher in the second experiment than in the first, much care was taken to maintain the same larval density in both studies. Post-larval experiments Early juvenile A. purpuratus (post-larvae) were obtained from a single batch of larvae cultured according to the method of DiSalvo et al. ( 1984) and fed a mixture of 1. galbana, C. calcitrans and N. oculata once a day.
G. Martinez et al. /Aquaculture
132 (1995) 313-323
315
When the juveniles were about 700 pm shell length, a sample was taken to determine the ash-free dry weight and energy content. The remaining juveniles were divided into three groups and subjected to the same three feeding regimens as used in the larval experiments. After 16 days, a sample of about 200 juveniles from each group was measured for anteriorposterior shell length (using an optical micrometer), washed with isotonic ammonium formate, dried to constant weight and placed in a muffle furnace at 500°C for 5 h to determine the ash content. From these values the ash-free dry weight (a.f.d.w.) was calculated (referred to as “organic matter” or “organic weight”). Another sample of individuals of each group was ignited in an OSK calorimeter to determine their energy content. The remaining individuals of the same groups were used to measure the physiological processes involved in the utilization of energy budget considering that: C=P+R+U+F Absorption Assimilation
= C-F = P + R (Bayne and Newell, 1983; Crisp, 1984)
where C = total intake of food or energy; P = portion of assimilated food that is incorporated into the biomass (production) ; R = portion of assimilated energy used for metabolic expenditure via respiration; U = that part of the consumption that is absorbed and later passed out of the body as secreted material, e.g., in the urine; F = portion of energy consumed that was not absorbed. but voided as feces. Consumption (C) was determined by ingestion rate assuming that ingestion rate = filtration rate X particle concentration (Sprung, 1984b), Filtration rate was determined by the indirect method, measuring removal of suspended particles from a known volume of water per unit time (Winter, 1977). In order to express consumption as amount of organic matter ingested, ash-free dry weight was obtained after ashing a sample of the microalgae mixture in a muffle furnace at 500°C. Production (P) was calculated as the difference between the ash-free dry weight of juveniles at the beginning and end of the experimental period. At each sampling, a group of individuals was washed with isotonic ammonium formate, dried to constant weight, ashed at 500°C and reweighed. Respiration (R) was determined by oxygen consumption using a Warburg constantpressure respirometer. The rates quoted were: ~1 O2 .individual-’
‘h-i.
Excretion (U) rate was calculated as the difference between the ammonia content of water in flasks with and without animals and was considered as pg NH: and converted to heat loss using the energy equivalent 0.00737 joules per ug NH: (Logan and Epifanio, 1978). Ammonia content was determined using the method of Solorzano ( 1969). EfJiciencies With the data on growth, food uptake and respiration, the following efficiencies were estimated. Assimilation efSiciency. Considered as that part of the ingested food that is retained for physiological purposes, namely for production and respiration, excluding excreta (F and U) (Bayne 1983; Sprung, 1984d; Crisp, 1984). It was calculated by:
316
G. Martinez et al. /Aquaculture
E = ( (Respiration
132 (1995) 313-323
rate + Growth rate) /Ingestion
rate) X 100
Respiration rate was expressed as the equivalent of organic weight considering 1 mg per 1.2 ml of O2 consumed (Laing and Millican, 1986). Growth rate was expressed as the organic biomass increase and ingestion rate as the organic weight of microalgae consumed in the unit time. Gross growth efficiency. As the proportion of the organic weight consumed converted into organic biomass, gross growth efficiency was calculated as: K, =Z/C (Sprung,
1984d).
Net growth ejficiency. Considered as the proportion of the assimilated converted to growth, net growth efficiency was calculated as:
K2 =Zl(I+R)
that was
(Sprung,
food which is
1984d)
3. Results Larval experiments Growth Larval growth, as measured by increases in shell length, under the three different feeding regimens is shown in Fig. 1. In both experiments (March and September, 1992), analysis of covariance of the fitted lines showed that the slopes were significantly different (F2,m = 24.9 1, P < 0.00 1 for Expt. 1 and F2,939= 8.73, P < 0.001 for Expt. 2). A test a posteriori showed that larvae under the continuous feeding regimen had faster growth rates than those fed twice or once a day. Yet, in Experiment 1, larvae fed twice a day had faster growth rates than those fed once a day (Neumann-Keuls test, P < 0.01; Zar, 1974). Survival In spite of having used different numbers of larvae in Experiment 1 than in Experiment 2, the results of both studies showed that continuous feeding resulted in higher survival of larvae than the other two feeding regimens (Table 1) . Post-larval experiments Final length, organic matter and energy content An analysis of variance showed that size and organic content (ash-free dry weight) of juvenile A. purpuratus were affected by feeding regimen (Table 2). Juveniles fed continuously attained a larger size and had a higher content of organic components than individuals in the other two feeding regimens (Table 3). In the two groups of juveniles fed discontinuously, those fed twice a day showed larger final length than those fed once a day (Tukey’s
G. Martinez et al. /Aquaculture
317
0
Exp. 1
ZlO-
132 (1995) 313-323
5.3-
D .
0 .. .
,.
5.1
-
4.9
-
170-
130-
t 4.7l
E a.
. _
90
= I
I
!
I
I
I
I
: vr aI
5
Exp. 2
180-
=
5.1
-
.p
0 (I 150-
.
:
D
4.9-
’
: 120-
D
4.7
-
* . so
I 4
, 2
I 6
I 8
Days
.
ODES
x
twice
0
continuous
4.5
I1 12
, 10
I 2
14
after
1 4
I 6
1 8
1 10
I 12
1 14
fertilization
a dry a da!
__
o”ce
-----
twice
a day a day
continuous
Fig. 1. Argopecten purpurufus larval shell length on different days after fertilization and fed under three different feeding regimens. Each point is the mean of 60 (Expt. 1) or 45 measurements (Expt. 2). The lines fitted to these points are represented on the right side of the figure.
test, P < 0.05). No significant difference fed the different feeding regimens. Physiological
processes
was found between energy content of juveniles
implied in the energy budget
Analysis of ingestion, oxygen consumption, ammonia excretion and production rate (expressed as increase in organic weight), showed that oxygen consumption and production rate were affected significantly by the feeding regimen in juvenile A. purpuratus (Table 4). Coincident with a higher growth rate, those juveniles fed continuously spent a higher amount of energy for metabolic demands than juveniles fed twice a day (Tukey test, P < 0.05). We
G. Martinez et al. /Aquaculture I32 (1995) 313-323
318
Table 1 Number of live Argopecten purpuratus larvae remaining regimens Expt.
Final number of larvae Percentage
1 2 1 2
of survival
when cultured for 15 days under three different feeding
Feeding regimens Once a day
Twice a day
Continuous
28 000 888 000 1.0 6.9
118 500 1 240 000 4.3 9.6
369 000 1990 000 13.3 15.4
Total amount of microalgae fed was the same for each regimen, 52.5 cells/$/day. for each group of larvae and for both experiments.
Larval density was the same
Table 2 Analysis of variance of final shell length, organic matter and energy content ofjuveniles of Argopectenpurpuratus from a single batch of larvae when cultured for 16 days under three different feeding regimens Source of variation
Degrees of freedom
Length Between groups Within groups
2 609
Organic matter Between groups Within groups
2 15
Energy content Between groups Within groups
2 12
Sum of squares
14.9794 53.0279
3426.33 5309.66
0.38449 11.51037
F-ratio
P
86.02
< 0.001
4.84
< 0.05
0.21
> 0.05
Table 3 Final shell length, organic weight and energy content of juveniles of Argopecten purpurarus from a single batch of larvae when cultured for 16 days under three different feeding regimens
Once a day Length
1.46 f 0.03
(mm) Organic weight
71.00 f 7.78
(pg/ind.) Energy content
2.75 f 0.65
(J/ind.) Values are means f s.d.
Twice a day 1.63 f 0.02 72.16rt6.62 2.54 f 0.28
Continuous 1.84kO.03 100.83 *8.51 2.36 kO.23
G. Martinez et al. /Aquaculture
132 (1995) 313-323
319
Table 4 Physiological processes involved in the utilization of energy by juveniles of Argopectenpurpuratus of 16 days when cultured under three different feeding regimens Feeding regimen
Once a day Twice a day Continuous
over a period
Ingestion rate (cell/h/ind.)
Respiration rate (~1 O,/h/ind.)
Ammonia excretion (pg NH.Jh/ind.)
Production
127 (63 86 (63 72 (22
0.2821 (0.087) 0.2442 (0.082) 0.3339 (0.086)
1.31 x10-a (0.95 x 10-a) 2.86x 10-s (2.29~ 10-a) 4.32~ lo-* (2.03x IO-*)
0.1121 (0.027) 0.1175 (0.024) 0.1921 (0.031)
955 899) 385 899) 724 701)
Analysis of variance for respiration
and production
(kg MO/h/ind.)
rate
Source of variation
Degrees of freedom
Sum of squares
Respiration Between groups Within groups
2 33
0.0487177 0.2419615
3.32
0.0485
Production Between groups Within groups
2 15
0.024007 1 0.0347372
5.18
0.0194
F-
P
ratio
Values are means (sd.). Table 5 Assimilation efficiencies (AR), gross growth efficiencies (K,) and net growth efficiencies (Kz) calculated from data of Table 4, transformed to organic weight equivalent, of juveniles of Argopecten purpuratus cultured under three different feeding regimens Feeding regimen
AE (%)
Ki (%)
Kz (%)
Once a day Twice a day Continuous
19.07 26.31 45.64
6.19 9.6 18.65
32.5 36.6 40.87
expressed this rate as oxygen consumed per mg ash-free dry weight, and then respiratory rate of juvenile scallops fed continuously did not differ from that of the other two groups of animals (3.51 ~1 as opposed to 3.52 ~1 O,/h/mg a.f.d.w. for animals fed twice a day and 4.15 ,zl O*/h/mg a.f.d.w. for animals fed once a day). Efficiencies estimated from data of ingestion, oxygen consumption and production showed that juveniles fed continuously had a higher assimilation efficiency than those individuals that received the same amount of food but supplied as one or two portions (Table 5). The best gross and net growth efficiency was obtained when juveniles were fed continuously.
320
G. Martinez et al. /Aquaculture I32 (1995) 313-323
4. Discussion
The faster growth and higher survival observed in A. purpuratus larvae fed continuously probably reflects better utilization of food. Growth and survival of bivalve larvae depend on several factors including an adequate food supply (Sprung, 1984a; Widdows, 1991). Previous studies on larval and juvenileA.purpuratus have shown that good growth occurred when they were fed a mixture of three species of algae (Diaz and Martinez, 1992). However, an adequate food supply does not only mean food quality but also appropriate availability. There is a food concentration level below which particles cannot be collected at maximum rates (Bayne, 1983; Pechenik, 1987). Rates of larval development tend to increase with increasing food concentration until a critical cell density is attained. Above this density a decline in growth may occur for several reasons: clogging of the feeding apparatus (Pechenik, 1987); larvae may become entangled in a net of pseudofeces (Sprung, 1984b); and larvae may react negatively to dissolved substances such as algal metabolites (Sprung, 1984b). When food is supplied in one or two portions per day, cell density is higher for an initial period of time than when the same total amount of microalgae is provided continuously. When cell density exceeds the upper critical level, the food provided to larvae will not be filtered and ingested efficiently. Results obtained in this study for juvenile A. purpuratus are similar to those described by Winter (1977) for juvenile Myths edulis. He showed that when the same amount of food was fed continuously to juvenile mussels, the increase in dry tissue weight was approximately twice as high as when animals were fed discontinuously. Langton and McKay ( 1976) found the opposite when they fed juvenile Crassostrea gigas at two food levels and four feeding regimes. Discontinuous feeding gave faster growth than continuous feeding. The difference between their results and those in the present study may be due to the fact that C. gigas is an intertidal mollusc and adapted to a discontinuous food supply while A. purpuratus is a subtidal bivalve adapted to a continuous food supply. That juveniles which attained the largest size and the highest content of organic components did not have a higher energy content but rather a lower (although not significant) content than the other individuals, may look surprising. Energy is not the only factor that is necessary for good growth. The heat released by juveniles in a calorimeter reflects their biochemical composition. A high energy content may mean a higher proportion of lipid. It is known that the the combustion of 1 g of lipid produces about twice caloric energy than 1 g of protein or carbohydrate. Lipids, and secondly proteins, have been suggested as the major energy reserves for bivalve larvae development and metamorphosis (Holland and Spencer, 1973; Gabbott, 1983; Mann and Gallager, 1985a). After metamorphosis there is a transition from this lipid-protein based energy metabolism to a carbohydrate-protein metabolism in the juvenile and adult stages (Gabbott, 1983; Mann and Gallager, 1985b; Moss Lane, 1986). Fidalgo et al. ( 1994) studying the food value of different microalgal diets to juvenile Myths galloprouincialis, have shown a significant positive correlation between growth rate and body lipid. Similar results had been obtained by Laing and Millican ( 1986) with cultured Ostrea edulis spat. Martinez et al. ( 1992) found that early juveniles of A. purpuratus held in the ocean during 40 days attained a larger size and contained less lipid than a group of individuals of the same brood, reared in the hatchery. The energy
G. Martinez
et al. /Aquaculture
132 (1995) 313-323
321
content, calculated from their biochemical composition, gave a higher value for the second group of juveniles. Although all individuals were supplied daily with the same food, animals that are fed discontinuously may be loosing a percentage of an essential component needed for growth. Then, those animals that grow more slowly may be lacking enough of some specific nutrient (different from lipid) that is essential for growth. The importance of this specific nutrient might not be in supplying energy, but rather it might be an essential precursor for macromolecules: e.g., some amino acid or vitamin. Kreeger and Langdon (1993) have shown that growth of juvenile Myfilus trossulus can be limited by dietary protein level. One must keep in mind that the scallops used in the present study correspond to early juveniles of less than 40 days after metamorphosis. Whyte et al. (1992) found a 58.3% decline in total energy of juveniles of the scallop, Cvussadoma gigunteu, during the transition of larvae to juveniles for 25 days after settlement. Holland and Spencer (1973) found a similar decrease in energy content in Ostrea edulis from pre-metamorphic larvae to early juveniles (in both cases, there was a good increase in the size of individuals). In our previous study, when different mixtures of microalgae were fed to growing early juvenile A. purpurutus, the mixture that produced the best growth was not that which produced the highest energy content (Diaz and Martinez, 1992). Juveniles of A. purpuratus fed under a continuous feeding regimen showed a better growth rate than individuals that were supplied the same daily amount of food in one or two portions. Growth studies under different food concentrations have shown that, above critical food densities, the growth rate declines (Thompson and Bayne, 1974; Winter, 1977; Griffiths and King, 1979; Widdows et al., 1979; Bayne, 1983; Cahalan et al., 1989). High particle concentrations increase the production of feces and pseudofeces (Widdows et al., 1979) and this may result in a significant loss of nutrients and consequent decreased growth (Cahalan et al., 1989). A decline in absorption efficiency has been commonly observed in laboratory experiments with increasing ration of microalgae (Thompson and Bayne, 1972, 1974; Navarro et al., 1991). The digestive system has functional capacity limits to the net uptake of nutrients. This determines a negative relationship between the amount of food that may be processed per unit time (ingestion rate) and the time it takes to traverse the digestive tube (Navarro and Iglesias, 1993). Bayne et al. ( 1989) have shown this negative relationship between ingestion rate and gut passage time for M. edulis fed a mixed algal and silt diet. In the present study, feces could not be collected, hence absorption efficiency could not be measured, but assimilation efficiency was calculated from growth rate and respiration rate data according to Sprung ( 1984d). Bayne (1983) distinguished between absorption and assimilation efficiency; the latter represents the part of cleared food that is effectively used to increase biomass. The greatest assimilation efficiency was obtained for those scallops that received the food in a continuous regimen. A continuous feeding regime permits a more or less steady food intake and improves digestion and assimilation of nutrients (Winter, 1977). Filter feeding activity has a metabolic cost (Sprung 1984~) and following a period of starvation this cost is higher than when feeding is continuous (Bayne and Scullard, 1977). Hence a continuous food supply may require a lower metabolic activity for filtering than a discontinuous feeding regime. The higher assimilation efficiency together with the higher gross and net growth efficiencies in animals fed continuously confirms our conclusion that under this feeding regimen
322
G. Martinez et al. /Aquaculture 132 (1995) 313-323
there is better utilization of the food. This is an important when juvenile bivalves are produced in hatcheries.
factor that must be considered
Acknowledgements We wish to express our thanks to Dr. Neil Bourne for his kind assistance in reviewing the manuscript. We are indebted to Dr. John Himmelman and two anonymous reviewers for helpful suggestions to improve the manuscript. Our acknowledgments to Mr. Raul Vera, Mr. Carlos Solar and the staff of the Unidad de Production of Facultad de Ciencias de1 Mar, Universidad Catolica de1 Norte, for their technical assistance. This study was partly funded by FDP-CORFO, Chile.
References Bayne, B.L., 1983. Physiological ecology of marine molluscan larvae. In: N.H. Verdonk, J.A.M. van den Biggelaar and AS. Tompa (Editors), The Mollusca, Vol. 3, Development. Academic Press, Orlando, FL, pp. 299-343. Bayne, B.L. and Newell, R.C., 1983. Physiological energetics of marine molluscs. In: A.S M. SaIeuddin and K.M. Wilbur (Editors), The Mollusca. Vol. 4, Physiology, Part I. Academic Press, New York, NY, pp. 407-5 15. Bayne, B.L. and Scullard, C., 1977. An apparent specific dynamic action in Myrilus edulis L. J. Mar. BioI. Assoc. UK, 57: 371-378. Bayne, B.L., Hawkins, A.J.S., Navarro, E. and Iglesias, I.P., 1989. Effects of seston concentration on feeding, digestion and growth in the mussel Mytilus edulis. Mar. Ecol. Prog. Ser., 55: 47-54. CahaIan, J.A., SiddaII, S.E. and Luckenbach, M.W., 1989. Effects of flow velocity, food concentration and particle flux on growth rates ofjuvenile bay scallops Argopecfen irradians. J. Exp. Mar. BioI. Ecol., 129: 45-60. Crisp, D.J., 1984. Energy flow measurements. In: N.A. HoIme and A.D. McIntyre (Editors), Methods for the Study of Marine Benthos, 2nd edn. Blackwell Publications, Oxford, pp. 284-372. Dfaz, M.A. and Martinez, G., 1992. Efecto de diferentes dietas sobre e1 balance energetic0 en juveniles de Argopectenpurpuratus L. Rev. BioI. Mar., 27(2): 163-173. DiSaIvo, L.H., Alar&, E., Martinez, E. and Uribe, E., 1984. Progress in mass culture of Chlamys (Argopecren) purpuruta (1819) with notes on its natural history. Rev. ChiI. Hist. Nat., 57: 3545. Fidalgo, J.P., Cid, A., Lopez-Mufioz, I., Abalde, J. and Herrero, C., 1994. Growth and biochemical profile of juvenile mussels (Mvzilus galloprouincialis Lmk) fed on different algal diets. J. Shell. Res., 13(I): 67-75. Gabbott, P.A., 1983. Developmental and seasonal metabolic activities in marine molluscs. In: P.W. Hochachka (Editor), The MoIIusca, Vo1.2, Environmental Biochemistry and Physiology. Academic Press, New York, NY, pp. 165-217. Griffiths, CL. and King, J.A., 1979. Some relationships between size, food availability and energy balance in the ribbed mussel Aulacomya uter. Mar. Biol., 51: 141-149. Holland, D.L. and Spencer, B.E., 1973. Biochemical changes in fed and starved oysters, Ostrea edulis L. during larval development, metamorphosis and early spat growth. J. Mar. Biol Assoc. UK, 53: 287-298. Johns, D.M., 1982. Physiological studies on Cancer irroratus larvae. III. Effects of temperature and salinity on the partitioning of energy resources during development. Mar. EcoI. Prog. Ser., 8: 75-85. Kreeger, D.A. and Langdon, C.J., 1993. Effect of dietary protein content on growth of juvenile mussels, Mytilus trossulus (Gould 1850). BioI. Bull., 185: 123-139. Laing, I. and Millican, P.F., 1986. Relative growth and growth efficiency of Ostrea edulis L. spat fed various algal diets. Aquaculture, 54: 245-262. Langton, R.W. and McKay, G.U., 1976. Growth of Crassostrea gigm (Thunberg) spat under different feeding regimes in a hatchery. Aquaculture, 7: 225-233. Logan, D.I. and Epifanio, C.E., 1978. A laboratory energy balance for the larvae and juveniles of the American lobster Homarus americanus. Mar. Biol.. 47: 381-389.
G. Martinez et al. /Aquaculture
132 (1995) 313-323
323
Mann, R. and Gallager, S.M., 1985a. Physiological and biochemical energetics of larvae of Teredo nmalis L. and Eat&a gouldi (Bartsch) (Bivalvia: Teredinidae). J. Exp. Mar. Biol. Ecol., 85: 21 l-228. Mann, R. and Gallager, SM., 1985b. Growth, morphometry and biochemical composition of the wood boring molluscs Teredo naualis L., Bar&a gouldi (Bartsch), and Nototeredo knoxi (Bartsch) (Bivalvia: Teredinidae). J. Exp. Mar. Biol. Ecol., 85: 229-251. Martinez, G., Torres, M., Uribe, E., Dfaz, M.A, and Perez, H., 1992. Biochemical composition of broodstock and early juvenile Chilean scallops, Argopecten purpuratus Lamarck, held in two different environments. J. Shell. Res., ll(2): 307-313. Moss Lane, J., 1986. Allometric and biochemical studies on starved and unstarved clams, Rangia cuneata (Sowerby, 1831). J. Exp. Mar. Biol.Ecol.,95: 131-143. Navarro, E. and lglesias, J.I.P., 1993. Infaunal filter-feeding bivalves and the physiological response to short-term fluctuations in food availability and composition. In: R.F. Dame (Editor), NATO AS1 Series, Vol. G 33, Bivalve Filter Feeders in Estuarine and Coastal Ecosystem Processes. Springer-Verlag. Berlin-Heidelberg. Navarro, E., Iglesias, J.I.P., Perez Camacho, A., Labarta, U. and Beiras, R., 1991. The physiological energetics of mussels (Mytilus galloprouincialis Lmk) from different cultivation rafts in the Ria de Arosa (Galicia, N.W. Spain). Aquaculture, 94: 197-212. Pechenik, J.A., 1987. Environmental influences on larval survival and development. In: A.C. Giese, J.S. Pearse and V.B. Pearse (Editors), Reproduction of Marine Invertebrates, Vol. IX. Blackwell Scientific Publications, Palo Alto, CA, pp. 551608. Solorzano, L., 1969. Determination of ammonia in natural seawaters by the phenolhypochlorite method. Limnol. Oceanogr., 14: 799-801. Sprung, M., 1984a. Physiological energetic of mussel larvae (Mvtilus edulis). I. Shell growth and biomass. Mar. Ecol. Prog. Ser., 17: 283-293. Sprung, M., 1984b. Physiological energetic of mussel larvae (Mytilus edulis). Il. Food uptake. Mar. Ecol. Prog. Ser., 17: 295-305. Sprung, M., 1984~. Physiological energetic of mussel larvae (Mytilus edulis). III. Respiration. Mar. Ecol. Prog. Ser., 18: 171-178. Sprung, M., 1984d. Physiological energetic of mussel larvae (Myths edulis). IV. Efficiencies. Mar. Ecol. Prog. Ser., 18: 179-186. Thompson, R.J. and Bayne, B.L., 1972. Active metabolism associated with feeding in the mussel Mytilus edulis L. J. Exp. Mar. Biol. Ecol., 9: 111-124. Thompson, R.J. and Bayne, B.L., 1974. Some relationships between growth, metabolism and food in the mussel, Mytilus edulis. Mar. Biol., 27: 317-326. Whyte, J.N.C., Bourne, N., Ginther, N.G. and Hodgson, CA., 1992. Compositional changes in the larva to juvenile development of the scallop Crassadoma gigantea (Gray). J. Exp. Mar. Biol. Ecol., 163: 13-29. Widdows, J., 1991. Physiological ecology of mussel larvae. Aquaculture, 94: 147-163. Widdows, P., Fieth, P. and Worrall, C.M., 1979. Relationship between seston, available food and feeding activity in the common mussel Mytilus edulis. Mar. Biol., 50: 195-207. Winter, J.E., 1977. Suspension-feeding in lamellibranquiate bivalves, with particular reference to Aquaculture. Medio Ambiente, 3( 1): 48-69. Zar, J.H. 1974. Biostatistical Analysis. Prentice Hall, Inc., Englewood Cliffs, NY, 619 pp.