The Journal of Nutrition Vol. 128 No. 1 January 1998, pp. 123-129

Metabolic Requirements of Red Drum, Sciaenops ocellatus, for Protein and Energy Based on Weight Gain and Body Composition^1,2,3

Bruce B. McGoogan and Delbert M. Gatlin III⁴

Department of Wildlife and Fisheries Sciences and Faculty of Nutrition, Texas A & M University, College Station, TX 77843-2258

	ABSTRACT

Abstract Introduction Methods Results Discussion References

Precise formulation of diets that meet but do not greatly exceed nutritional requirements should assist in lowering feed costs for commercial aquaculture of red drum, Sciaenops ocellatus. In this study, protein and energy requirements of red drum for maintenance and maximum gain were determined by feeding a diet containing digestible protein (DP) at 36.5% and 14.2 kJ digestible energy (DE) per gram at various rates for 8 wk in two separate experiments. Changes in weight and whole-body energy and protein were measured and regressed against protein or energy fed using a nonlinear procedure. In the first experiment, juvenile fish [~ 3.4 g initial body weight (BW)] were either starved or fed at one of the following g/(100 g BW·d): 0.5, 1, 2, 4, 6, or 8. The second experiment utilized larger red drum (~5.5 g initial weight), fed 0.75, 1.5, 3, 5, 5.5, 6, 6.5 or 7 g/(100 g BW·d) to confirm and refine results from the first experiment. Based on maintenance of body weight in both experiments, red drum had a protein maintenance requirement of 1.5 and 2.5 g DP/(kg BW·d) whereas estimates based on maintenance of whole-body protein were 0.5 and 2.2 g DP/(kg BW·d). Energy requirements for maintenance of weight and body energy ranged from 58 to 93 and 92 to 97 kJ DE/(kg BW·d), respectively. Protein requirements for maximum weight gain and change in body protein ranged from 20 to 25 g DP/(kg BW·d), whereas energy requirements for maximum weight gain and whole-body deposition ranged from 776 to 958 and 914 to 985 kJ DE/(kg BW·d), respectively. These requirements for maintenance and maximum gain of red drum should assist in formulation of diets for a variety of desired feeding strategies.

	INTRODUCTION

Abstract Introduction Methods Results Discussion References

Red drum, Sciaenops ocellatus, is a species with demonstrated aquacultural potential, but experimental assessments have concluded that the economic feasibility of commercial red drum aquaculture could be strengthened with lower production costs (Sandifer et al. 1993). Enhancement of dietary efficiency (diet utilization for growth) should assist in lowering these costs; however, more precise nutritional information concerning the red drum is required for this to be achieved. Nutritional information regarding red drum has increased significantly in recent years but is still incomplete (Gatlin 1995, Robinson 1991).

Energy and protein are classified as two of the most important nutritional components for the culture of animals. The failure to include adequate quantities of protein and energy in the diet results in reduced growth, whereas excessive quantities of energy result in undesirable fat deposition or reduced feed consumption (NRC 1993). Use of protein for energy is generally undesirable because of the high cost of protein relative to carbohydrate and lipid, as well as its preferential utilization for tissue synthesis and growth. Although fish typically have lower energy requirements than other animals, the contribution of protein to meet these requirements has been estimated to be higher (Kaushik and Médale 1994). In aquaculture, it is generally desirable to minimize dietary protein concentration without reducing growth of the fish. This not only reduces feed costs but also decreases the protein that potentially may result in undesirable nitrogenous waste production.

View larger version (16K): [in this window] [in a new window]   Fig 1. Changes in body weight (BW) and whole-body protein of red drum fed graded levels of digestible protein (DP) for 8 wk in Experiment 1. Values are means ± SEM. Values for whole-body changes represent differences between mean values of 10 fish at the start of the experiment subtracted from the mean of five fish from each of three replicate groups for each treatment at the end of 8 wk.

View larger version (15K): [in this window] [in a new window]   Fig 3. Changes in body weight (BW) and whole-body protein of red drum fed graded levels of digestible protein (DP) for 8 wk in Experiment 2. Values are means ± SEM. Values were obtained using the same procedure as described in Figure 1 except that values for whole-body change were based upon three fish from each of three replicate groups.

Protein and energy requirements have been studied in a number of fish species (NRC 1993) including red drum. Daniels and Robinson (1986) concluded that a minimum of 35% protein and 17 kJ estimated digestible energy per gram of diet was required for rapid growth and acceptable body composition. In addition, that study reported that between 15.4 and 17.2 kJ/g diet was required when the diet contained 44% protein. Another study found the protein requirement of red drum for maximum growth to be ~40% of dry diet, and lipid was more efficiently utilized as an energy source than carbohydrate (Serrano et al. 1992). The minor difference in the results of these two studies may be explained by differences in conditions that affect dietary requirements such as size of fish and water temperature (Wilson and Halver 1986) as well as diet composition (NRC 1993).

Maintenance requirements, or those levels of nutrients and energy that are required for maintaining body functions (Cho and Bureau 1995), have not been investigated in red drum. The determination of maintenance requirements may provide insight into basic metabolic needs, and knowledge of these requirements may be applied for sustenance feeding of fish during adverse culture conditions or maintenance of fish at marketable size. Dietary requirements for maximum gain must be known for economical fish production and may be measured as the point at which the desired growth indicator reaches a plateau in a regression of indicator against intake.

There are inherent problems in quantifying requirements as pointed out by Cowey (1992). If weight gain is measured as the response (growth indicator) to increasing levels of intake, it would require the assumption of constant composition of gain, which is most likely not the case. In addition, if net protein utilization or protein efficiency ratio is used as a growth indicator, accurate measurements of intake are required, but these are somewhat difficult to obtain with aquatic animals. Measurements that reflect metabolic effects of dietary protein and energy intake may provide more precise predictions of dietary requirements. Therefore, it appears that differences between nitrogen (protein) and energy retention in relation to nitrogen and energy intake are appropriate measures to use for assessing protein and energy requirements. This study was conducted to determine the protein and energy requirements of red drum for maintenance and maximum gain based upon weight gain as well as whole-body protein and energy retention.

	MATERIALS AND METHODS

Abstract Introduction Methods Results Discussion References

Experimental diets.  Two separate experiments were conducted in which a single diet (Table 1) was fed at various percentages of body weight per day (BW⁵·d) to juvenile red drum for 8 wk. The diet was formulated to contain 40% crude protein, 7% lipid and 13.4 kJ estimated digestible energy/g diet (Serrano et al. 1992) on the basis of proximate composition of ingredients (AOAC 1990). Red drum muscle was used to provide all of the dietary protein, because it was considered to have the optimum amino acid balance for red drum and, ideally, would not inflate estimates of protein requirements as a result of imbalances of individual amino acids. Procedures for diet preparation and storage were as previously described (Nematipour and Gatlin 1993). Digestible protein and energy contents of the test diet were determined by replacing 0.5% cellulose with chromic oxide and conducting a digestibility trial with advanced red drum juveniles (100-200 g) in four 650-L tanks using established procedures (Gaylord and Gatlin 1996, McGoogan and Reigh 1996). On the basis of those determinations, the test diet contained digestible protein (DP) at 36.5% and 14.2 kJ digestible energy (DE)/g.

Feeding experiments.  Red drum in both experiments were produced from captive broodstock maintained at the Aquacultural Research and Teaching Facility of the Texas A&M University System. The juvenile fish were cultured in aquaria containing ~75 L of artificial seawater maintained at a salinity of 5-6 g/L. Aquaria were connected to common biological and mechanical filters, which recirculated water at a rate of 0.5 L/min and maintained ammonia, nitrite, pH and dissolved oxygen within acceptable ranges. Water temperature was maintained at 25.3 ± 1.1 and 25.6 ± 0.6°C in Experiments 1 and 2, respectively. A 12 h:12 h light:dark cycle was provided by fluorescent lighting controlled by timers. Fish were subjected to a 1-wk acclimation period in aquaria before beginning each 8-wk experiment. Dietary treatments were assigned to triplicate aquaria using a completely randomized design with each aquaria constituting a statistical unit. Fish in each aquarium were collectively weighed weekly, and these weights were used to compute weekly feed quantities.

In the first experiment, 15 red drum initially averaging (± SD) 51.8 ± 2.5 g/group were stocked in each of 21 aquaria. Treatments in the first experiment consisted of the aforementioned diet fed at the following g/(100 g BW·d): 0.5, 1, 2, 4, 6 and 8. Another group of fish was starved in this experiment. Fish fed 0.5-2 g/(100 g BW·d) were fed the entire ration in the morning, whereas, at all other feeding rates, rations were divided equally between the morning and evening. This strategy was implemented to maximize availability of feed to fish fed at the lowest rates.

For the second experiment, 15 red drum initially averaging 82.3 ± 4.2 g/group were stocked into each of 24 aquaria. Treatment levels were concentrated around predicted requirement ranges from the first experiment to confirm and refine these requirements. Thus, in the second experiment the same diet as in the first experiment was fed at the following g/(100 g BW·d): 0.75, 1.5, 3, 5, 5.5, 6, 6.5 and 7. Fish fed 0.75 and 1.5 g/(100 g BW·d) were fed the entire ration in the morning, whereas all other rations were divided equally between a morning and afternoon feeding. Procedures used in this study with regard to animal care and sample collection were approved by the Texas A&M University Laboratory Animal Care Committee.

Sample collection and analysis.  At the conclusion of the feeding trials, five fish per aquarium in Experiment 1 and three fish per aquarium in Experiment 2 were killed by a blow to the head. For treatments in which feed rate was < 2 g/(100 g BW·d), fish that died during the 8-wk period due to apparent nutritional deficiency also were subjected to whole-body analysis. Initial samples of 10 fish were collected before the start of each experiment. Fish were stored frozen (20°C) until body indices could be determined. Indices measured included: relative liver weight (RLW = liver weight × 100/fish weight); intraperitoneal fat (IPF) ratio (IPF ratio = IPF weight × 100/fish weight); and muscle ratio (MR = skeletal muscle weight × 100/fish weight). Individual fish were then homogenized and subsamples of the homogenate were analyzed in duplicate for dry matter, protein and energy according to established procedures (AOAC 1990, Gaylord and Gatlin 1996). Mean values for whole-body protein and energy within each group were applied to corresponding final fish weight for computation of final average whole-body protein and energy. The initial fish samples were analyzed for whole-body protein and energy and those values were multiplied by the initial average fish weight. These values were subtracted from the final values for estimates of the change in whole-body protein and energy. Whole-body measurements, as well as weight gain, were regressed against protein and energy intake, and a nonlinear procedure was used to estimate requirements for maximum gain (Robbins et al. 1979, SAS 1985). Maintenance requirements were predicted from best-fit lines that were regressed to zero.

	RESULTS

Abstract Introduction Methods Results Discussion References

Effects of protein and energy intake on body indices in the first experiment.  Red drum fed various quantities of protein and energy showed marked differences in body condition indices. Fish exhibited increasing RLW up to a feed rate of ~4 g/(100 g BW·d), the point at which this index began to reach a plateau (Table 2). Additionally, a minimum RLW of 0.2 was observed in the starved fish. Intraperitoneal fat was unmeasurable until feed rate was 4 g/(100 g BW·d) and reached a plateau at 6 g/(100 g BW·d) (Table 2). Muscle ratio showed a trend similar to RLW, increasing at each feed rate until reaching an asymptote at ~4 g/(100 g BW·d).

Effects of protein and energy intake on weight gain, feed efficiency and whole-body composition in the first experiment.  Weight gain and feed efficiency of red drum progressively increased as feeding rate increased up to 6 g/(100 g BW·d) or ~22 g DP/(kg BW·d) (Table 2). A similar response also was observed for whole-body protein (Fig. 1). Even though the slope of whole-body protein began to decrease substantially at this same feeding rate, there was a slight increase in whole-body protein at the next highest level. This observation resulted in the decision not to estimate a protein requirement for maximum protein gain from these data. However, protein requirements for maintenance were estimated at 2.5 and 2.2 g DP/(kg BW·d) on the basis of maintenance of weight and whole-body protein, respectively, whereas the requirement for maximum gain was 25 g DP/(kg BW·d) solely on the basis of weight gain.

Weight gain and whole-body energy similarly increased with increasing levels of energy intake before reaching a plateau at ~850 kJ DE/(kg BW·d) (Fig. 2). Nonlinear regression analysis provided maintenance energy estimates of 93 and 97 kJ DE/(kg BW·d) on the basis of body weight and energy retention, respectively, with requirements for maximum weight gain and deposition of ~958 and 914 kJ DE/(kg BW·d).

View larger version (17K): [in this window] [in a new window]   Fig 2. Changes in body weight (BW) and whole-body energy of red drum fed graded levels of digestible energy (DE) for 8 wk in Experiment 1. Values are means ± SEM. Values were obtained as described in Figure 1.

Effects of protein and energy intake on body indices in the second experiment.  Red drum fed increasing quantities of protein and energy showed a steady increase in RLW until the feeding rate was ~3-5 g/(100 g BW·d) (Table 3). Intraperitoneal fat ratio was unmeasurable until a feeding rate of 5 g/(100 g BW·d) and then leveled off at 6.5 g/(100 g BW·d) (Table 3). Muscle ratio quickly increased to a plateau at 1.5 g/(100 g BW·d) (Table 3).

Effects of protein and energy intake on weight gain, feed efficiency and whole-body composition in the second experiment.  Weight gain and feed efficiency reached a plateau at a feeding rate of 5.5 g/(100 g BW·d) or ~20 g DP/(kg BW·d) (Table 3). Whole-body protein retention also responded similarly (Fig. 3). Maintenance protein requirements were estimated to be 1.5 and 0.5 g DP/(kg BW·d) on the basis of static weight and whole-body protein, respectively. The requirement for maximum gain was 20 g DP/(kg BW·d) on the basis of both weight and whole-body protein measurements.

Whole-body energy retention of red drum in the second experiment displayed a similar trend to that observed for protein. Weight gain and energy retention of red drum began to reach a plateau in fish fed ~750 kJ DE/(kg BW·d) and greater (Fig. 4). The largest increase in weight and whole-body energy was observed in fish fed 994 kJ DE/(kg BW·d). Nonlinear regression analysis predicted maintenance energy requirements of 58 and 92 kJ DE/(kg BW·d) on the basis of static weight and whole-body energy, respectively. Requirements for maximum weight gain and energy deposition were 776 and 985 kJ DE/(kg BW·d), respectively.

View larger version (16K): [in this window] [in a new window]   Fig 4. Changes in body weight (BW) and whole-body energy of red drum when fed increasing levels of digestible energy (DE) for 8 wk in Experiment 2. Values were obtained as described in Figure 3.

	DISCUSSION

Abstract Introduction Methods Results Discussion References

On the basis of the results of both experiments, this study determined the average maintenance requirements of red drum to be 0.5-2.5 g DP and 58-97 kJ DE/(kg BW·d), with requirements for maximum weight gain at 20-25 g DP and 776-985 kJ DE/(kg BW·d). These requirement estimates should allow more accurate formulation and substitution of various feedstuffs in diets for red drum, because digestibility coefficients of a number of practical ingredients have been determined for this species (Gaylord and Gatlin 1996, McGoogan and Reigh 1996). In addition, these requirement estimates should allow feeding regimens to be adjusted to meet specific production goals.

Protein requirement estimates based on weight gain and protein gain were more similar than energy requirement estimates based on weight gain and body energy. It therefore appears likely that either weight or protein gain are appropriate measures for predicting requirements for maximum gain. However, in both experiments, protein requirements for maintenance were higher on the basis of weight gain compared with protein gain.

The fact that energy requirements for maximum weight gain were so different with the use of this response criterion compared with whole-body energy gain likely stems from the fact that once weight gain begins to plateau, energy density may continue to increase with lipid deposition. This belief is supported by large increases in IPF deposition at the highest feeding rates. These observations suggest that weight gain may be the more appropriate measure to use in predicting energy requirements for greatest production efficiency because higher levels of fat deposition are generally undesirable.

It is difficult to compare results from this study with dietary protein and energy requirements determined in other studies in which diets of various protein or energy concentrations were fed and requirements expressed as a dietary concentration of protein or energy necessary for maximum gain. In contrast, the requirements in this study were assessed as physiological requirements based on daily intake per unit of body weight.

Gatlin et al. (1986) conducted a study with channel catfish (Ictalurus punctatus) using the same methodology as that employed in this study whereby weight gain as well as whole-body protein and energy changes were considered in predicting daily requirements. Results from that study indicated that channel catfish required 1.3 g protein and 63 kJ/(kg BW·d) for maintenance and 8.8 g protein and 414 kJ/(kg BW·d) for maximum gain. Although these maintenance requirements are fairly similar to those determined for red drum, channel catfish appear to require substantially lower levels of protein and energy for maximum gain. This might be expected because of the tendency for red drum to grow more rapidly and consume greater quantities of feed than channel catfish cultured at similar temperatures. Additionally, red drum are generally perceived to be carnivorous (Boothby and Avault 1971) and thus dependent upon more dense nutrient and energy intake than that of the omnivorous channel catfish.

It is also of interest to compare results of this study with those obtained in other studies with red drum. The requirement estimates determined in this study can easily be expressed as a dietary concentration based upon a desired feeding rate, or conversely expressed as a feeding rate that will meet requirements given known dietary protein and energy concentrations. If we consider a reasonable feeding rate of 5-6 g/(100 g BW·d) for fish of the initial size (3-6 g) used in this study, metabolic requirements for maximum gain would be met by a diet containing DP at 36-44% and 15.1-18.2 kJ DE/g diet. These values are within the range suggested for red drum by other authors. Daniels and Robinson (1986) reported that a diet with a minimum of 35% protein and 17 kJ estimated digestible energy/g was required for rapid growth and acceptable body composition of red drum, but that energy needs were 15.4-17.2 kJ/g when protein was increased to 44% of diet. Similarly, Serrano et al. (1992) determined the protein requirement for maximum growth of red drum to be 40% of dry diet. Although most studies have expressed the determined requirements as a percentage of the diet, Bowen (1987) converted published dietary protein requirements of several species to requirements expressed per kilogram BW per day. In fact, the 22 g DP/(kg BW·d) estimated in this study for maximum weight gain of red drum appears to be similar to gross protein requirements determined for juveniles of other carnivorous fish species including Morone saxatilis [19 g/(kg BW·d)] and Micropterus dolomieu [21 g/(kg BW·d)] (Bowen 1987).

There are no reported data concerning the maintenance requirements of red drum with which to compare the current findings, but indications are that red drum, in addition to the previously discussed channel catfish, have maintenance requirements similar to rainbow trout. The maintenance energy requirement of relatively large rainbow trout (300 g initial weight) was found to be ~41 kJ DE/(kg BW·d) (Storebakken et al. 1991). This requirement appears to be similar, but somewhat lower, than the estimate of 58-97 kJ DE/(kg BW·d) determined for red drum in this study, with smaller initial fish size of red drum likely contributing to the higher requirement. The maintenance protein requirement presently determined for red drum of 1.5-2.5 g DP/(kg BW·d) is similar to the requirement previously found for rainbow trout of 2.6 g DP/(kg BW·d) (Kaushik and Gomes 1988).

In summary, requirements for maximum gain determined in this study, when expressed as a dietary concentration, are similar to those determined in previous studies with red drum despite differences in methodology. However, the methodology currently employed and the expression of requirements in terms of daily metabolic needs seem to offer the possibility of manipulating formulations and feeding strategies to meet specific production purposes.

	ACKNOWLEDGMENTS

We thank Gary Jones and Dow Chemical Company of Freeport, TX for providing access to wild red drum that were filleted and lyophilized for use in experimental diets. Additionally, we thank Jane Crowther (Zapata Haynie, Reedville, VA) for providing menhaden oil for the diets.

	FOOTNOTES

Manuscript received 11 June 1997. Initial reviews completed 16 July 1997. Revision accepted 10 September 1997.

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