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Basic growth relations in experimental rearing of early juvenile cuttlefish Sepia officinalis L. (Mollusca: Cephalopoda)
Journal of Experimental Marine Biology and Ecology 265 Ž2001. 75–87 www.elsevier.comrlocaterjembe
Basic growth relations in experimental rearing of early juvenile cuttlefish Sepia officinalis L. žMollusca: Cephalopoda/ N. Koueta) , E. Boucaud-Camou Laboratoire de Biologie et Biotechnologies Marines, UniÕersite´ de Caen, 14032 Caen Cedex, France Received 13 March 2001; received in revised form 15 June 2001; accepted 9 July 2001
Abstract Basic growth relations were studied in experimental rearing of juvenile cuttlefish during 40 days. Eleven different rations of food were offered in order to establish the maintenance, optimum, and maximum rations during the early life of these animals. The maintenance ration, 2–3.5% of body weight, decreased with age. The optimum rations were, respectively, 16.2%, 14% and 9% during 10, 20 and 40 days of rearing. The maximum rations were, respectively, 40%, 31% and 10% of body weight after 10, 20 and 40 days of rearing. The correlation between conversion rate and growth rate was low, but increased after 20 days of rearing. These data allow determination of the exact quantity and the period of food adjustment during the early life of juvenile cuttlefish and, hence, wasting of food can be avoided. These observations are essential in the development of aquaculture and in experimental rearing of early juvenile cuttlefish. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Cuttlefish; Conversion rate; Growth; Maintenance ration; Maximum ration; Optimum ration
1. Introduction For the development of aquaculture of any species, the formulation of a growth model is essential. In growth studies, it is necessary to be able to understand how biotic and abiotic factors influence growth functions. These studies must be conducted in experimental rearing conditions that are controlled and standardized. The culture of
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Corresponding author. Tel.: q33-231-56-55-96; fax: q33-231-56-53-46. E-mail address: [email protected] ŽN. Koueta..
0022-0981r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 2 2 - 0 9 8 1 Ž 0 1 . 0 0 3 1 9 - 7
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cephalopods has recently become a very important area due to their rapid growth ŽForsythe and Heukelem, 1987., their increased market price ŽNavarro and Villanueva, 2000., and since their organs and cells are increasingly used in electrophysiology, biomedical and environmental sciences and endocrinology ŽHanlon and Messenger, 1996; Dickel et al., 1997; Koueta et al., 1995; Koueta and Boucaud-Camou, 1999; Henry et al., 1999.. The success of extensive rearing for market and experimental rearing for fundamental investigations depends on knowledge of the quantity and quality of food used during growth. The quantity and the quality of food offered to paralarvae and juveniles are crucial for their survival during initial and future stages of growth. For Sepia officinalis, many studies have investigated the effect of the quality or type of food on growth, but clear data concerning the quantity of food are lacking. This basic growth relation, well established in many species of fish, is not yet well known in cephalopods. Our previous investigations have shown that during the early stages of development, S. officinalis needs more food, but the ration decreases quickly during the first month of their life ŽKoueta and Boucaud-Camou, 1999.. During recent years, a number of studies involving cuttlefish cultures have been conducted ŽRichard, 1971; Yim and Boucaud-Camou, 1980; Boucaud-Camou et al., 1985; Toll and Strain, 1988; Boletzky, 1989; DeRusha et al., 1989; Castro, 1991; Lee et al., 1991; Castro et al., 1993, Forsythe et al., 1994; Hanley et al., 1998., but in these studies, the food was offered ad libitum. Some studies have been conducted involving only juvenile cuttlefish in order to investigate biochemical indices of growth and the quantity and the quality of the food offered ŽClarke et al., 1989; Koueta et al., 2000, in press.. In young animals, it appears necessary to establish experimentally a growth model to optimize future rearing and profitable aquaculture by examining the full growth curve over a wide range of environmental factors. In the formulation of a growth model for salmonids, Stauffer Ž1973. suggested that any attempt at modelling must include at least the three factors; ration, animal size and temperature as the most important variables. In this study, the temperature was stable and only the quantity of food offered varied. The basic growth relations in juvenile cuttlefish, i.e. maintenance ration, growthrration curve, optimum ration and maximum ration were studied.
2. Materials and methods 2.1. Experimental animals All the eggs were laid in the laboratory by females trawled off the Normandy coast and maintained in a large tank receiving water from the sea. The eggs were placed on floating sieves distributed in tanks connected to the semi-closed system as previously described ŽKoueta and Boucaud-Camou, 1999.. As hatching lasted several days, hatchlings were placed in small tanks of 707 cm2 in groups of 10 animals according to their age and fed ad libitum on live mysids or live young shrimps.
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2.2. Rearing system The semi-closed system limits the presence of particles and mud, which cause turbidity of the water in the Bay of Seine. Furthermore, this system allows the renewal of seawater in the tanks per day, thus avoiding problems of evaporation, loss of water due to cleaning of the tanks, changes of salinity and pH, and also of nitrate, nitrite, and ammonium concentrations. In this system, these different parameters are therefore the same as in open seawater and do not require any temporal adjustment when animal density is kept low ŽKoueta and Boucaud-Camou, 1999.. The base of the rearing system consists of a 1000-l reservoir tank containing a heating system. This tank is also filled with oyster shells as biological filters. Following this, the water is driven back into a skimmer by an automatic pump. The skimmer removes a maximum of dissolved organic material, then sends seawater back to the superior tray containing the filters. The pH of the seawater was 8, salinity 35.5‰, and the concentration of O 2 measured with an electronic oxygen meter was optimal Ž8.9–9.7 mgrl corresponding to a saturating rate.. NH 4q measurements made with a colorimetric kit revealed - 0.5 mgrl and, hence, the NH 3 concentration was - 0.02 mgrl at the pH of rearing. For nitrites and nitrates, the concentrations measured with a colorimetric kit were - 0.1 and - 10 mgrl, respectively. Physical and chemical parameters were maintained constant by continual renewal of fresh seawater, by avoiding overpopulation, and by removing dead cuttlefish, dead prey, and food remains. Before entering the system, the natural seawater, which was used to renew the circuit, ran through a system of UV lamps with a flow rate of 60 lrh Ž93% renewal per day.. The mechanical filters, which consist of foam and synthetic fibres, were cleaned daily with seawater Žto avoid lethal osmotic shock to the nitrite bacteria.. The temperature of seawater was maintained between 19.5 and 20.5 8C by the heating elements in the conditioning tank. The rearing system received 12 h of lightr24 h. 2.3. Feeding methodology A total of 132 juvenile cuttlefish of maximum 4 days old were divided into 11 homogenous groups of 12 animals, each group receiving a different quantity of food. The amount of food offered was, respectively, 0%, 1%, 3%, 5%, 10%, 20%, 25%, 30%, 35%, 40%, and 50% of their body weight per day per group. The diet was live mysids Ž Mesopodosis labberi and Schistomysis sp.. or very young shrimps Ž Crangon crangon.. The prey were offered once each day at 10 a.m. In the groups, each animal was separated from the others and grown in individual chambers ŽKoueta and BoucaudCamou, 1999.. The daily amount of food offered was recalculated according to animal weight after 5 days during 40 days of rearing. 2.4. Weight measurement A Sartorius balance with a precision of 0.1 mg was used to weigh all animals at the beginning of the experiment and then every 5 days thereafter during the study.
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2.5. Growth and food conÕersion rate analysis The amount of food ingested by the specimen in each container was measured by weighing each day the food remaining in the individual tanks. The feeding rate ŽFR. was expressed as FR Ž%body weight. s ŽFIrmean W = 100., where FI is the weight of food ingested, W the weight of each animal. The conversion efficiency Ž%. was calculated as growth weightrweight of food ingested= 100. Weight measurements were as described by Koueta and Boucaud-Camou Ž1999.. Weight increase Žmg. s final weighty initial weight. Relative weight gain Ž%. s weight increase= 100rinitial weight. Growth rate was expressed as Ainstantaneous relative growth rateB ŽIGR.: IGR Ž%body weightrday. s ŽLn W2 y Ln W1 .100rt, where W2 and W1 are, respectively, final and initial weight Žmg. of each animal, and t is the duration of the experiment in days. 2.6. Statistical analysis The statistical analysis were carried out in the computer using Statgraphics Plus. The results of different variables measured were compared between groups Ž10, 20, and 40 days of rearing. using ANOVA followed by multiple a posteriori comparisons employing the Tukey test ŽTukey honestly significant differences. ŽSokal and Rohlf, 1981.. The multiple-range tests tell us which means are significantly different from which others.
3. Results 3.1. SurÕiÕal The group of starved cuttlefish Ž12 animals. died progressively up to 21 days. Of the 120 juvenile cuttlefish used in other groups during the experiment, four were dead after 10 days and a further two after 30 days of rearing. The rate of survival was 95%. 3.2. Relation between growth and ration 3.2.1. Maintenance ration During the first 10 days of rearing, the starved juvenile cuttlefish did not grow while those animals fed on a ration of 1–2% body weightrday had a growth rate of 0.5%. When the animals received, respectively, a ration of 2.82% and 4.9%, the growth rate remained low, 1.03 and 1.25. After 20 days of rearing, starved juvenile cuttlefish growth was negative Žgrowth rate y1.37%., while the animals fed with a ration of 1% had no growth Žgrowth rate 0.06%.. The growth rate obtained for the rations of 2.61% and
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4.89% were low Žgrowth rate 0.2% and 0.8%.. After 40 days, the maintenance ration was 2% and induced a growth rate of 0.15% ŽFig. 1.. 3.2.2. Optimum ration After 10 days, the optimum ration was 16.2% for a growth rate of 8.5% of body weightrday. At day 20, the optimum ration decreased to 13.9% of body weight for a growth rate of 8.86% of body weight. After 40 days of rearing, the optimum ration was only 10% of the body weight for a growth rate of 7.09%. Therefore, the optimum ration changed for 10, 20 or 40 days Ž p - 0.05.. The correlation between optimum ration and optimum growth was R s 0.90 during the rearing ŽFigs. 1 and 2.. 3.2.3. Maximum ration After 10 days of rearing, a ration of 40% of body weight induced a growth rate of 12.8% of body weightrday in juvenile cuttlefish. At this age, the animals’ food intake increased to 46% of their body weight for a best growth rate of 13.15%. After 20 days of rearing, the maximum ration decreased to 31% of the body weight for a growth rate of 10.8%. At day 40 of the rearing, the maximum ration always decreased and was 10% for a growth rate of 8.2%. Therefore, the maximum ration changed for 10, 20 or 40 days
Fig. 1. Relation between ration Ž%weightrday. and growth rate Ž%weightrday. during juvenile cuttlefish rearing Ž R10 s 0.96; R 20 s 0.95; R 40 s 0.94..The curves were a function of power. The growth rate was low when the rations were under 5% of the body weightrday. Vertical bar: standard deviation.
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Fig. 2. Changes of optimum ration Ž%., growth rate Ž%. and conversion rate Ž%. with the age Ždays. of the juvenile cuttlefish. The curves were exponential, negative for optimum ration and optimum growth rate, positive for optimum conversion rate. Vertical bar: standard deviation.
of rearing Ž p - 0.05.. The correlation between maximum ration and maximum growth was 0.93 during the rearing. The correlations between ration and growth were R s 0.95; R s 0.96 and R s 0.93, respectively, for 10, 20 and 40 days of rearing. During the rearing, the maximum growth changed for 10, 20 and 40 days Ž p - 0.05. ŽFigs. 1 and 3.. 3.3. Relation between conÕersion rate and growth Before 20 days, the conversion rate was low. The conversion rate was more correlated with growth when juvenile cuttlefish were more than 20 days old. The correlations were R s 0.73; R s 0.85; R s 0.83, respectively, after 10, 20 and 40 days of rearing ŽFig. 4.. 3.4. Relation between conÕersion rate and ration With rations between 1% and 5%, the conversion rate was low and stable, between 20% and 22% ŽFig. 5.. The conversion rate then increased up to optimum ration. Thus, at day 10, 20 and 40 of rearing, the optimum conversion rate was, respectively, 45.03%,
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Fig. 3. Changes of maximum ration Ž%. maximum growth Ž%. and conversion rate Ž%. with the age Ždays. of the juvenile cuttlefish. The curves were exponential, negative for maximum growth and maximum growth rate, positive for maximum conversion rate. Vertical bar: standard deviation.
Fig. 4. Relation between conversion rate Ž%. and growth rate Ž%weightrday. during juvenile cuttlefish rearing Ž R10 s 0.70; R 20 s 0.80; R 40 s 0.82.. The curves were a function of power. The conversion rate were low when growth rate was under 2% of the body weightrday. Vertical bar: standard deviation.
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Fig. 5. Relation between conversion rate Ž%. and ration Ž%weightrday. during juvenile cuttlefish rearing. The curves were a function of power. The conversion rate were low when rations were under 5% of the body weightrday. Vertical bar: standard deviation.
46.72% and 48.09% Ž R s 0.99.. The optimum conversion rates were different for 10, 20 and 40 days Ž p - 0.05.. For maximum ration, the conversion rate during 10, 20 and 40 days of rearing was, respectively, 34.10%, 36.20% and 38.15% Ž R s 0.93.. The maximum conversion rates were different for 10, 20 and 40 days Ž p - 0.05. ŽFigs. 2 and 3..
4. Discussion 4.1. Maintenance ration The maintenance ration during juvenile cuttlefish rearing is above 2% of body weight per day. Only the animals receiving a ration of more than 2.3% of their body weight reached 40 days of rearing; the others died. The weight of starved animals decreased after 10 days of rearing. These observations suggest that the maintenance ration for juvenile cuttlefish rearing must be between 2.5% and 3% of their body weight. Under this ration, the animals lost weight and finally died. During the first 10 days of rearing, the animals are most resistant to starvation, due to the presence of yolk reserves used by young animals. Smith et al. Ž1986. suggested that juvenile walleye pollock ŽTheragra chalcogramma. have higher maintenance rations than adult pollock. During this investigation, our observations were similar, with a decrease in the maintenance ration from 3% to 2.2% during rearing from 20 to 40 days.
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4.2. Changes of optimum ration and maximum ration with age of juÕenile cuttlefish The optimum ration is high during the first 10 days of rearing Ž16.2%., subsequently decreasing progressively until 40 days Ž10%.. The maximum rations were 46% and 13%, respectively, for 10- and 40-day-old animals. These changes are due to the fast growth of juvenile cuttlefish, their appetite being stimulated by the presence of prey. Young and Davis Ž1990. found that maximum ration in larvae of Thunnus maccoyii was between 25% and 50% of larval body weight. In flounder larvae, Marioka et al. Ž1987. suggested that daily food requirement was 20–45% of body weight. Smith et al. Ž1986. have shown that in juvenile walleye pollock ŽT. chalcogramma., the maximum ration is three to four times higher than maintenance ration. Lagardere ` Ž1987. demonstrated that daily food consumption of juvenile common sole, Solea Õulgaris, was 8–11% of the body weight, similar to that of young plaice Pleuronectes platessa ŽBasimi and Grove, 1985. during the intense feeding periods Ž10–12% of the body weight.. These rations observed in different fish species are lower than that observed in our experiment. In juvenile cuttlefish, the maximum ration is 12 times higher than maintenance ration, due to the high conversion rate and fast growth of the cephalopods. Forsythe Ž1984., in a detailed study of growth of Octopus joubini, has shown that maximum food intake was 24%, 11.5% and 9% for, respectively, 15, 29 and 51 days of rearing. Growth rate was highest during the first 4 weeks with an overall mean of 7.4% of body weightrday at 23 8C. Hanlon and Forsythe Ž1985. studied food intake and growth in five species of Octopus and suggested that the growth rate during the exponential phase was 7% of body weightrday and the food intake was 20% of body weightrday. Segawa Ž1990. studied food consumption, food conversion and growth rates of the oval squid Sepiotheuthis lessoniana in laboratory experiments and showed that during the early life of the animal, the maximum ration was 32.5% of the body weightrday and the daily growth rate 12.9% of body weightrday. Clarke et al. Ž1989. studied a relation between food intake and growth in juvenile cuttlefish of 50 days old and suggest 90 mg of food Žthree mysids of 30 mg. as maximum ration. In comparison with this work, their juvenile animals were small Ž67.4 mg for 35 days old. and the maximum ration very low. Some preliminary results established by Choe Ž1966. showed that at the fast growing stage of S. subaculenta and Sepiella maindroni, daily rates of feeding were, respectively, 30.8% and 34.7% of their body weightrday. Cephalopods food intake, like their growth rate, is higher than in many fish. 4.3. Changes of conÕersion rate with age of juÕenile cuttlefish During rearing, the conversion rate remained stable when the ration was a maximum of 5% of body weight. For the ration up to 5%, the conversion rate increased with the age of the juvenile cuttlefish Ž p - 0.05.. This observation also suggests that in juvenile cuttlefish, the maintenance ration is high during early life and decreases with age, as also observed by Smith et al. Ž1986.. The correlations between maximum growth rate
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and maximum conversion rate Ž R s y0.91. and between optimum growth rate and optimum conversion rate Ž R s y0.88. were negative ŽFigs. 2 and 3.. 4.4. Changes of conÕersion rate with ration of juÕenile cuttlefish When the juvenile cuttlefish were more than 20 days old, the conversion rate was well correlated with ration up to the optimum ration. Above the optimum ration, the conversion rate decreased, becoming inversely proportional to the ration ŽFig. 5.. As suggested by Pascual Ž1978., Mangold Ž1983., Van Heukelem Ž1983., Hanlon and Forsythe Ž1985., Segawa Ž1990., and Hanlon and Messenger Ž1996., the conversion rate is very high in cephalopods and 30–60% of food ingested is used for growth. Our observations in this investigation suggest that after 20 days of rearing, hypertrophic growth is more important. Boletzky Ž1983. and Nixon and Mangold Ž1998. suggested that early juvenile cuttlefish have a conversion rate of 35–50%. These data are in agreement with our investigation when animals are more than 20 days old. Thus, growth rate was very high compared to other invertebrates or vertebrates as previously observed by Hanlon and Forsythe Ž1985. in Octopus. These investigations confirm our previous data; the ration decreased with age in young animals, a high quantity of food stimulated the capture of food, and the capabilities of young animals to assume the maintenance ration with yolk absorption in temporal starvation ŽVecchione, 1987.. In nature, these capabilities allow juvenile animals to learn how to capture prey and to survive when prey are scarce. Nevertheless, a maximum ration of 13% of body weightrday after 40 days of rearing confirm our previous data ŽKoueta and Boucaud-Camou, 1999.. This value seems low, but an explanation may be the isolation of the animals. Warnke Ž1994. suggested that cuttlefish reared in a rich environment in groups, with enough food and sand in the aquarium, capture more food than others reared in a poor environment, isolated and without sand. In this investigation, the isolation of the animals was essential to determine clearly the basic growth relations, such as maintenance ration, growthrration, optimum and maximum rations. The availability of sufficient food in early life stages is a major determinant of recruitment success. Knowledge of the feeding ecology of the larvae is essential for understanding their early life history and recruitment variability ŽYoung and Davis, 1990.. All these data would allow us to conduct a comparison between animals reared in a rich environment and in the conditions we used in our experiment. We can thus study a wide range of environment factors during the early life of juvenile cuttlefish and investigate biochemical indices, which are correlated with growth during longer time periods, as suggested by Koueta et al. Ž2000.. All results could then be extended to young cephalopods collected in the field and used to predict recruitment.
5. Conclusion Our results were obtained in particular conditions in experimental rearing where juvenile cuttlefish were isolated from each other. These investigations for the first time
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have permitted establishment of the fundamental basic growth relations like maintenance ration, growthrration curve, growthrconversion rate in cephalopods. The knowledge of optimum ration and maximum ration is essential to the better digestion of food during rearing, and this study provides important fundamental data for the aquaculture of Cephalopods. In this investigation, for the first time, changes in conversion rate, the growthrration curve, and the output of growth during early juvenile cuttlefish life have been studied. The increase of the conversion rate with age indicates the starting up of catabolic processes, such as digestive enzymes, and anabolic processes, such as protein synthesis, which are related to the fast growth during the first 2 months of juvenile cephalopod life. The study of some anabolic and catabolic process during juvenile cuttlefish growth appears essential to elucidate digestive capabilities, growth processes and their physiological regulation by hormones or growth factors. Such investigations present a great interest for fundamental research and aquaculture of cephalopods. Our future investigations will therefore focus on the evolution of digestive enzymes during growth and their physiological regulation.
Acknowledgements This work was supported by the Conseil Regional de Basse Normandie and conducted in CREC at Luc sur Mer. We wish to thank I. Probert for his help in English editing and P. Grosjean for daily technical verifications of the rearing system. [SS]
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Warnke, K., 1994. Some aspects of social interaction during feeding in Sepia officinalis ŽMollusca: Cephalopoda. hatched and reared in the laboratory. Vie Milieu 44 Ž2., 125–131. Young, J.W., Davis, T.O., 1990. Feeding ecology of larvae of southern bluefin, albacore and skipjack tunas ŽPisces: Scombridae. in the easten Indian Ocean. Mar. Ecol.: Prog. Ser. 61, 17–20. Yim, M., Boucaud-Camou, E., 1980. Etude cytologique du developpement post-embryonnaire de la glande ´ digestive de Sepia officinalis L. Mollusque Cephalopode. Arch. Anat. Microsc. Morphol. Exp. 69, 57–59. ´
Basic growth relations in experimental rearing of early juvenile cuttlefish Sepia officinalis L. žMollusca: Cephalopoda/ N. Koueta) , E. Boucaud-Camou Laboratoire de Biologie et Biotechnologies Marines, UniÕersite´ de Caen, 14032 Caen Cedex, France Received 13 March 2001; received in revised form 15 June 2001; accepted 9 July 2001
Abstract Basic growth relations were studied in experimental rearing of juvenile cuttlefish during 40 days. Eleven different rations of food were offered in order to establish the maintenance, optimum, and maximum rations during the early life of these animals. The maintenance ration, 2–3.5% of body weight, decreased with age. The optimum rations were, respectively, 16.2%, 14% and 9% during 10, 20 and 40 days of rearing. The maximum rations were, respectively, 40%, 31% and 10% of body weight after 10, 20 and 40 days of rearing. The correlation between conversion rate and growth rate was low, but increased after 20 days of rearing. These data allow determination of the exact quantity and the period of food adjustment during the early life of juvenile cuttlefish and, hence, wasting of food can be avoided. These observations are essential in the development of aquaculture and in experimental rearing of early juvenile cuttlefish. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Cuttlefish; Conversion rate; Growth; Maintenance ration; Maximum ration; Optimum ration
1. Introduction For the development of aquaculture of any species, the formulation of a growth model is essential. In growth studies, it is necessary to be able to understand how biotic and abiotic factors influence growth functions. These studies must be conducted in experimental rearing conditions that are controlled and standardized. The culture of
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Corresponding author. Tel.: q33-231-56-55-96; fax: q33-231-56-53-46. E-mail address: [email protected] ŽN. Koueta..
0022-0981r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 2 2 - 0 9 8 1 Ž 0 1 . 0 0 3 1 9 - 7
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cephalopods has recently become a very important area due to their rapid growth ŽForsythe and Heukelem, 1987., their increased market price ŽNavarro and Villanueva, 2000., and since their organs and cells are increasingly used in electrophysiology, biomedical and environmental sciences and endocrinology ŽHanlon and Messenger, 1996; Dickel et al., 1997; Koueta et al., 1995; Koueta and Boucaud-Camou, 1999; Henry et al., 1999.. The success of extensive rearing for market and experimental rearing for fundamental investigations depends on knowledge of the quantity and quality of food used during growth. The quantity and the quality of food offered to paralarvae and juveniles are crucial for their survival during initial and future stages of growth. For Sepia officinalis, many studies have investigated the effect of the quality or type of food on growth, but clear data concerning the quantity of food are lacking. This basic growth relation, well established in many species of fish, is not yet well known in cephalopods. Our previous investigations have shown that during the early stages of development, S. officinalis needs more food, but the ration decreases quickly during the first month of their life ŽKoueta and Boucaud-Camou, 1999.. During recent years, a number of studies involving cuttlefish cultures have been conducted ŽRichard, 1971; Yim and Boucaud-Camou, 1980; Boucaud-Camou et al., 1985; Toll and Strain, 1988; Boletzky, 1989; DeRusha et al., 1989; Castro, 1991; Lee et al., 1991; Castro et al., 1993, Forsythe et al., 1994; Hanley et al., 1998., but in these studies, the food was offered ad libitum. Some studies have been conducted involving only juvenile cuttlefish in order to investigate biochemical indices of growth and the quantity and the quality of the food offered ŽClarke et al., 1989; Koueta et al., 2000, in press.. In young animals, it appears necessary to establish experimentally a growth model to optimize future rearing and profitable aquaculture by examining the full growth curve over a wide range of environmental factors. In the formulation of a growth model for salmonids, Stauffer Ž1973. suggested that any attempt at modelling must include at least the three factors; ration, animal size and temperature as the most important variables. In this study, the temperature was stable and only the quantity of food offered varied. The basic growth relations in juvenile cuttlefish, i.e. maintenance ration, growthrration curve, optimum ration and maximum ration were studied.
2. Materials and methods 2.1. Experimental animals All the eggs were laid in the laboratory by females trawled off the Normandy coast and maintained in a large tank receiving water from the sea. The eggs were placed on floating sieves distributed in tanks connected to the semi-closed system as previously described ŽKoueta and Boucaud-Camou, 1999.. As hatching lasted several days, hatchlings were placed in small tanks of 707 cm2 in groups of 10 animals according to their age and fed ad libitum on live mysids or live young shrimps.
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2.2. Rearing system The semi-closed system limits the presence of particles and mud, which cause turbidity of the water in the Bay of Seine. Furthermore, this system allows the renewal of seawater in the tanks per day, thus avoiding problems of evaporation, loss of water due to cleaning of the tanks, changes of salinity and pH, and also of nitrate, nitrite, and ammonium concentrations. In this system, these different parameters are therefore the same as in open seawater and do not require any temporal adjustment when animal density is kept low ŽKoueta and Boucaud-Camou, 1999.. The base of the rearing system consists of a 1000-l reservoir tank containing a heating system. This tank is also filled with oyster shells as biological filters. Following this, the water is driven back into a skimmer by an automatic pump. The skimmer removes a maximum of dissolved organic material, then sends seawater back to the superior tray containing the filters. The pH of the seawater was 8, salinity 35.5‰, and the concentration of O 2 measured with an electronic oxygen meter was optimal Ž8.9–9.7 mgrl corresponding to a saturating rate.. NH 4q measurements made with a colorimetric kit revealed - 0.5 mgrl and, hence, the NH 3 concentration was - 0.02 mgrl at the pH of rearing. For nitrites and nitrates, the concentrations measured with a colorimetric kit were - 0.1 and - 10 mgrl, respectively. Physical and chemical parameters were maintained constant by continual renewal of fresh seawater, by avoiding overpopulation, and by removing dead cuttlefish, dead prey, and food remains. Before entering the system, the natural seawater, which was used to renew the circuit, ran through a system of UV lamps with a flow rate of 60 lrh Ž93% renewal per day.. The mechanical filters, which consist of foam and synthetic fibres, were cleaned daily with seawater Žto avoid lethal osmotic shock to the nitrite bacteria.. The temperature of seawater was maintained between 19.5 and 20.5 8C by the heating elements in the conditioning tank. The rearing system received 12 h of lightr24 h. 2.3. Feeding methodology A total of 132 juvenile cuttlefish of maximum 4 days old were divided into 11 homogenous groups of 12 animals, each group receiving a different quantity of food. The amount of food offered was, respectively, 0%, 1%, 3%, 5%, 10%, 20%, 25%, 30%, 35%, 40%, and 50% of their body weight per day per group. The diet was live mysids Ž Mesopodosis labberi and Schistomysis sp.. or very young shrimps Ž Crangon crangon.. The prey were offered once each day at 10 a.m. In the groups, each animal was separated from the others and grown in individual chambers ŽKoueta and BoucaudCamou, 1999.. The daily amount of food offered was recalculated according to animal weight after 5 days during 40 days of rearing. 2.4. Weight measurement A Sartorius balance with a precision of 0.1 mg was used to weigh all animals at the beginning of the experiment and then every 5 days thereafter during the study.
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2.5. Growth and food conÕersion rate analysis The amount of food ingested by the specimen in each container was measured by weighing each day the food remaining in the individual tanks. The feeding rate ŽFR. was expressed as FR Ž%body weight. s ŽFIrmean W = 100., where FI is the weight of food ingested, W the weight of each animal. The conversion efficiency Ž%. was calculated as growth weightrweight of food ingested= 100. Weight measurements were as described by Koueta and Boucaud-Camou Ž1999.. Weight increase Žmg. s final weighty initial weight. Relative weight gain Ž%. s weight increase= 100rinitial weight. Growth rate was expressed as Ainstantaneous relative growth rateB ŽIGR.: IGR Ž%body weightrday. s ŽLn W2 y Ln W1 .100rt, where W2 and W1 are, respectively, final and initial weight Žmg. of each animal, and t is the duration of the experiment in days. 2.6. Statistical analysis The statistical analysis were carried out in the computer using Statgraphics Plus. The results of different variables measured were compared between groups Ž10, 20, and 40 days of rearing. using ANOVA followed by multiple a posteriori comparisons employing the Tukey test ŽTukey honestly significant differences. ŽSokal and Rohlf, 1981.. The multiple-range tests tell us which means are significantly different from which others.
3. Results 3.1. SurÕiÕal The group of starved cuttlefish Ž12 animals. died progressively up to 21 days. Of the 120 juvenile cuttlefish used in other groups during the experiment, four were dead after 10 days and a further two after 30 days of rearing. The rate of survival was 95%. 3.2. Relation between growth and ration 3.2.1. Maintenance ration During the first 10 days of rearing, the starved juvenile cuttlefish did not grow while those animals fed on a ration of 1–2% body weightrday had a growth rate of 0.5%. When the animals received, respectively, a ration of 2.82% and 4.9%, the growth rate remained low, 1.03 and 1.25. After 20 days of rearing, starved juvenile cuttlefish growth was negative Žgrowth rate y1.37%., while the animals fed with a ration of 1% had no growth Žgrowth rate 0.06%.. The growth rate obtained for the rations of 2.61% and
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4.89% were low Žgrowth rate 0.2% and 0.8%.. After 40 days, the maintenance ration was 2% and induced a growth rate of 0.15% ŽFig. 1.. 3.2.2. Optimum ration After 10 days, the optimum ration was 16.2% for a growth rate of 8.5% of body weightrday. At day 20, the optimum ration decreased to 13.9% of body weight for a growth rate of 8.86% of body weight. After 40 days of rearing, the optimum ration was only 10% of the body weight for a growth rate of 7.09%. Therefore, the optimum ration changed for 10, 20 or 40 days Ž p - 0.05.. The correlation between optimum ration and optimum growth was R s 0.90 during the rearing ŽFigs. 1 and 2.. 3.2.3. Maximum ration After 10 days of rearing, a ration of 40% of body weight induced a growth rate of 12.8% of body weightrday in juvenile cuttlefish. At this age, the animals’ food intake increased to 46% of their body weight for a best growth rate of 13.15%. After 20 days of rearing, the maximum ration decreased to 31% of the body weight for a growth rate of 10.8%. At day 40 of the rearing, the maximum ration always decreased and was 10% for a growth rate of 8.2%. Therefore, the maximum ration changed for 10, 20 or 40 days
Fig. 1. Relation between ration Ž%weightrday. and growth rate Ž%weightrday. during juvenile cuttlefish rearing Ž R10 s 0.96; R 20 s 0.95; R 40 s 0.94..The curves were a function of power. The growth rate was low when the rations were under 5% of the body weightrday. Vertical bar: standard deviation.
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Fig. 2. Changes of optimum ration Ž%., growth rate Ž%. and conversion rate Ž%. with the age Ždays. of the juvenile cuttlefish. The curves were exponential, negative for optimum ration and optimum growth rate, positive for optimum conversion rate. Vertical bar: standard deviation.
of rearing Ž p - 0.05.. The correlation between maximum ration and maximum growth was 0.93 during the rearing. The correlations between ration and growth were R s 0.95; R s 0.96 and R s 0.93, respectively, for 10, 20 and 40 days of rearing. During the rearing, the maximum growth changed for 10, 20 and 40 days Ž p - 0.05. ŽFigs. 1 and 3.. 3.3. Relation between conÕersion rate and growth Before 20 days, the conversion rate was low. The conversion rate was more correlated with growth when juvenile cuttlefish were more than 20 days old. The correlations were R s 0.73; R s 0.85; R s 0.83, respectively, after 10, 20 and 40 days of rearing ŽFig. 4.. 3.4. Relation between conÕersion rate and ration With rations between 1% and 5%, the conversion rate was low and stable, between 20% and 22% ŽFig. 5.. The conversion rate then increased up to optimum ration. Thus, at day 10, 20 and 40 of rearing, the optimum conversion rate was, respectively, 45.03%,
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Fig. 3. Changes of maximum ration Ž%. maximum growth Ž%. and conversion rate Ž%. with the age Ždays. of the juvenile cuttlefish. The curves were exponential, negative for maximum growth and maximum growth rate, positive for maximum conversion rate. Vertical bar: standard deviation.
Fig. 4. Relation between conversion rate Ž%. and growth rate Ž%weightrday. during juvenile cuttlefish rearing Ž R10 s 0.70; R 20 s 0.80; R 40 s 0.82.. The curves were a function of power. The conversion rate were low when growth rate was under 2% of the body weightrday. Vertical bar: standard deviation.
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Fig. 5. Relation between conversion rate Ž%. and ration Ž%weightrday. during juvenile cuttlefish rearing. The curves were a function of power. The conversion rate were low when rations were under 5% of the body weightrday. Vertical bar: standard deviation.
46.72% and 48.09% Ž R s 0.99.. The optimum conversion rates were different for 10, 20 and 40 days Ž p - 0.05.. For maximum ration, the conversion rate during 10, 20 and 40 days of rearing was, respectively, 34.10%, 36.20% and 38.15% Ž R s 0.93.. The maximum conversion rates were different for 10, 20 and 40 days Ž p - 0.05. ŽFigs. 2 and 3..
4. Discussion 4.1. Maintenance ration The maintenance ration during juvenile cuttlefish rearing is above 2% of body weight per day. Only the animals receiving a ration of more than 2.3% of their body weight reached 40 days of rearing; the others died. The weight of starved animals decreased after 10 days of rearing. These observations suggest that the maintenance ration for juvenile cuttlefish rearing must be between 2.5% and 3% of their body weight. Under this ration, the animals lost weight and finally died. During the first 10 days of rearing, the animals are most resistant to starvation, due to the presence of yolk reserves used by young animals. Smith et al. Ž1986. suggested that juvenile walleye pollock ŽTheragra chalcogramma. have higher maintenance rations than adult pollock. During this investigation, our observations were similar, with a decrease in the maintenance ration from 3% to 2.2% during rearing from 20 to 40 days.
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4.2. Changes of optimum ration and maximum ration with age of juÕenile cuttlefish The optimum ration is high during the first 10 days of rearing Ž16.2%., subsequently decreasing progressively until 40 days Ž10%.. The maximum rations were 46% and 13%, respectively, for 10- and 40-day-old animals. These changes are due to the fast growth of juvenile cuttlefish, their appetite being stimulated by the presence of prey. Young and Davis Ž1990. found that maximum ration in larvae of Thunnus maccoyii was between 25% and 50% of larval body weight. In flounder larvae, Marioka et al. Ž1987. suggested that daily food requirement was 20–45% of body weight. Smith et al. Ž1986. have shown that in juvenile walleye pollock ŽT. chalcogramma., the maximum ration is three to four times higher than maintenance ration. Lagardere ` Ž1987. demonstrated that daily food consumption of juvenile common sole, Solea Õulgaris, was 8–11% of the body weight, similar to that of young plaice Pleuronectes platessa ŽBasimi and Grove, 1985. during the intense feeding periods Ž10–12% of the body weight.. These rations observed in different fish species are lower than that observed in our experiment. In juvenile cuttlefish, the maximum ration is 12 times higher than maintenance ration, due to the high conversion rate and fast growth of the cephalopods. Forsythe Ž1984., in a detailed study of growth of Octopus joubini, has shown that maximum food intake was 24%, 11.5% and 9% for, respectively, 15, 29 and 51 days of rearing. Growth rate was highest during the first 4 weeks with an overall mean of 7.4% of body weightrday at 23 8C. Hanlon and Forsythe Ž1985. studied food intake and growth in five species of Octopus and suggested that the growth rate during the exponential phase was 7% of body weightrday and the food intake was 20% of body weightrday. Segawa Ž1990. studied food consumption, food conversion and growth rates of the oval squid Sepiotheuthis lessoniana in laboratory experiments and showed that during the early life of the animal, the maximum ration was 32.5% of the body weightrday and the daily growth rate 12.9% of body weightrday. Clarke et al. Ž1989. studied a relation between food intake and growth in juvenile cuttlefish of 50 days old and suggest 90 mg of food Žthree mysids of 30 mg. as maximum ration. In comparison with this work, their juvenile animals were small Ž67.4 mg for 35 days old. and the maximum ration very low. Some preliminary results established by Choe Ž1966. showed that at the fast growing stage of S. subaculenta and Sepiella maindroni, daily rates of feeding were, respectively, 30.8% and 34.7% of their body weightrday. Cephalopods food intake, like their growth rate, is higher than in many fish. 4.3. Changes of conÕersion rate with age of juÕenile cuttlefish During rearing, the conversion rate remained stable when the ration was a maximum of 5% of body weight. For the ration up to 5%, the conversion rate increased with the age of the juvenile cuttlefish Ž p - 0.05.. This observation also suggests that in juvenile cuttlefish, the maintenance ration is high during early life and decreases with age, as also observed by Smith et al. Ž1986.. The correlations between maximum growth rate
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and maximum conversion rate Ž R s y0.91. and between optimum growth rate and optimum conversion rate Ž R s y0.88. were negative ŽFigs. 2 and 3.. 4.4. Changes of conÕersion rate with ration of juÕenile cuttlefish When the juvenile cuttlefish were more than 20 days old, the conversion rate was well correlated with ration up to the optimum ration. Above the optimum ration, the conversion rate decreased, becoming inversely proportional to the ration ŽFig. 5.. As suggested by Pascual Ž1978., Mangold Ž1983., Van Heukelem Ž1983., Hanlon and Forsythe Ž1985., Segawa Ž1990., and Hanlon and Messenger Ž1996., the conversion rate is very high in cephalopods and 30–60% of food ingested is used for growth. Our observations in this investigation suggest that after 20 days of rearing, hypertrophic growth is more important. Boletzky Ž1983. and Nixon and Mangold Ž1998. suggested that early juvenile cuttlefish have a conversion rate of 35–50%. These data are in agreement with our investigation when animals are more than 20 days old. Thus, growth rate was very high compared to other invertebrates or vertebrates as previously observed by Hanlon and Forsythe Ž1985. in Octopus. These investigations confirm our previous data; the ration decreased with age in young animals, a high quantity of food stimulated the capture of food, and the capabilities of young animals to assume the maintenance ration with yolk absorption in temporal starvation ŽVecchione, 1987.. In nature, these capabilities allow juvenile animals to learn how to capture prey and to survive when prey are scarce. Nevertheless, a maximum ration of 13% of body weightrday after 40 days of rearing confirm our previous data ŽKoueta and Boucaud-Camou, 1999.. This value seems low, but an explanation may be the isolation of the animals. Warnke Ž1994. suggested that cuttlefish reared in a rich environment in groups, with enough food and sand in the aquarium, capture more food than others reared in a poor environment, isolated and without sand. In this investigation, the isolation of the animals was essential to determine clearly the basic growth relations, such as maintenance ration, growthrration, optimum and maximum rations. The availability of sufficient food in early life stages is a major determinant of recruitment success. Knowledge of the feeding ecology of the larvae is essential for understanding their early life history and recruitment variability ŽYoung and Davis, 1990.. All these data would allow us to conduct a comparison between animals reared in a rich environment and in the conditions we used in our experiment. We can thus study a wide range of environment factors during the early life of juvenile cuttlefish and investigate biochemical indices, which are correlated with growth during longer time periods, as suggested by Koueta et al. Ž2000.. All results could then be extended to young cephalopods collected in the field and used to predict recruitment.
5. Conclusion Our results were obtained in particular conditions in experimental rearing where juvenile cuttlefish were isolated from each other. These investigations for the first time
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have permitted establishment of the fundamental basic growth relations like maintenance ration, growthrration curve, growthrconversion rate in cephalopods. The knowledge of optimum ration and maximum ration is essential to the better digestion of food during rearing, and this study provides important fundamental data for the aquaculture of Cephalopods. In this investigation, for the first time, changes in conversion rate, the growthrration curve, and the output of growth during early juvenile cuttlefish life have been studied. The increase of the conversion rate with age indicates the starting up of catabolic processes, such as digestive enzymes, and anabolic processes, such as protein synthesis, which are related to the fast growth during the first 2 months of juvenile cephalopod life. The study of some anabolic and catabolic process during juvenile cuttlefish growth appears essential to elucidate digestive capabilities, growth processes and their physiological regulation by hormones or growth factors. Such investigations present a great interest for fundamental research and aquaculture of cephalopods. Our future investigations will therefore focus on the evolution of digestive enzymes during growth and their physiological regulation.
Acknowledgements This work was supported by the Conseil Regional de Basse Normandie and conducted in CREC at Luc sur Mer. We wish to thank I. Probert for his help in English editing and P. Grosjean for daily technical verifications of the rearing system. [SS]
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