Effects of starvation on energy reserves in young juveniles of abalone Haliotis discus hannai Ino.ABSTRACT Effects of various degrees of starvation (0-, 5-, 10-, 15-, 20- and 25-day fasted) on tissue protein, lipid, total carbohydrate, glycogen glycogen (glī`kəjən), starchlike polysaccharide (see carbohydrate) that is found in the liver and muscles of humans and the higher animals and in the cells of the lower animals. and ash contents, as well as the ratio of soft-tissue to shell weight, were investigated in young juvenile abalone abalone (ăbəlō`nē), popular name in the United States for a univalve gastropod mollusk of the genus Haliotis, members of which are also called ear shells, or sea ears, as their shape resembles the human ear. , Haliotis discus hannai Ino (initial shell length: 4.8 [+ or -] 0.6 mm, initial live weight: 15.0 [+ or -] 1.3 mg). Results showed that after 25-day starvation, tissue protein, lipid, total carbohydrate, and ratios of soft-tissue to shell weight decreased significantly, whereas the glycogen level remained constant, and ash content increased significantly. During the 25-day starvation, juvenile abalone lost 23.4% of protein, 19.8% of lipid, and 13.3% of total carbohydrate. The corresponding energy depletions were 226.5, 81.3, and 3.0 kJ/100 g dry body weight, respectively. The variation of energy depletion among the energy components is probably evidence of selective utilization of energy reserves by juvenile abalone, and partly a reflection of the predominance of energy components in juvenile tissues. KEY WORDS: abalone, Haliotis discus hannai, young juvenile, starvation, energy reserves INTRODUCTION In abalone hatcheries, benthic ben·thos n. 1. The collection of organisms living on or in sea or lake bottoms. 2. The bottom of a sea or lake. [Greek. diatoms diatoms a series of unicellular algae, microscopic in size, with cell walls containing silica. Members of the family Diatomaceae. Their remains accumulate as geological deposits and are mined. See diatomaceous earth. have traditionally been used as initial foods for young juveniles. During the stage when young juveniles are at 5-10 mm of shell length, weaning weaning, n the period of transition from breast feeding to eating solid foods. weaning the act of separating the young from the dam that it has been sucking, or receiving a milk diet provided by the dam or from artificial sources. on to macroalgae or artificial diet, the supply of diatoms has been identified as a major obstacle in abalone nutrition, owning to problems relating to relating to relate prep → concernant relating to relate prep → bezüglich +gen, mit Bezug auf +acc the quality and quantity of diatoms (McCormick & Hahn 1983, Ebert & Houk 1984, Hahn 1989, Knauer et al. 1996). Starvation often occurs when juveniles are not able to ingest in·gest tr.v. in·gest·ed, in·gest·ing, in·gests 1. To take into the body by the mouth for digestion or absorption. See Synonyms at eat. 2. sufficient optimal diatoms, which is probably one of the key factors accounting for the high mortality in many abalone hatcheries all over the world. Starvation is not an uncommon circumstance for marine invertebrates (Carefoot et al. 1993). During starvation, an organism's normal energy mobilization and metabolism is altered, and energy reserves (mainly tissue protein, lipid, and carbohydrate) are catabolized and oxidized oxidized having been modified by the process of oxidation. oxidized cellulose see absorbable cellulose. to supply basal metabolism basal metabolism: see metabolism. . Therefore, starvation must have profound effects on the organism's physiologic condition and tissue chemical content. Many researchers have conducted studies to investigate the effect of starvation on energy reserves in marine gastropods and bivalves. Results show that tissue protein, lipid, and carbohydrate play different roles in different species of marine invertebrates. Most studies on larval larval 1. pertaining to larvae. 2. larvate. larval migrans see cutaneous and visceral larva migrans. bivalves showed that lipid acted as the main energy reserves (Millar & Scott 1967, Corner & Cowey 1968, Holland & Spencer 1973, Whyte et al. 1987). Rodriguez et al. (1990) found that larval oyster, Ostrea edulis, consumed protein as the main energy source. In gastropods, available data shows that carbohydrates acted as the main energy reserves (Martin 1961, Goddard & Martin 1966). Carefoot et al. (1993) studied the effect of starvation on tissue glycogen in the northern abalone, Haliotis kamtschatkana of ~100-150 g live weight, and results showed that glycogen reserves in the digestive gland digestive gland n. A gland, such as the liver or pancreas, that secretes into the alimentary canal substances necessary for digestion. and foot muscle were depleted de·plete tr.v. de·plet·ed, de·plet·ing, de·pletes To decrease the fullness of; use up or empty out. [Latin d . However, there was no information on the changes of protein and lipid content during starvation. This study is conducted to investigate the effects of starvation on the energy reserves in young juveniles of H. discus hannai at weaning stage, from which we can get some useful information on the energy metabolism and nutritional requirement of abalone during this stage. MATERIALS AND METHODS Young Juvenile Culture and Sample The experiment was conducted in the Mashan Sea-product abalone hatchery hatchery a commercial establishment dedicated to the hatching of bird eggs to provide day old chicks and poults to the poultry industry. hatchery liquid the contents of unfertilized eggs. Used in petfood manufacture. in Shandong Province, People's Republic of China. All the young juveniles used had been settled and grown on diatoms for 2 mo, and showed excellent performance both in growth and survival. At the beginning of the experiment, 150 young juveniles were randomly collected as the sample of Day 0, and initial shell length and live weight were measured. Three PVC PVC: see polyvinyl chloride. PVC in full polyvinyl chloride Synthetic resin, an organic polymer made by treating vinyl chloride monomers with a peroxide. hatchery tanks (50 x 40 x 30 cm) were set up as three replicates. Each tank was stocked with 500 young juveniles on black corrugated plastic plates (45 x 30 cm), and covered with a 1.5 mm mesh. To minimize the possibility of diatom diatom (dī`ətŏm', -tōm'), unicellular organism of the kingdom Protista, characterized by a silica shell of often intricate and beautiful sculpturing. Most diatoms exist singly, although some join to form colonies. growth contributing food for the larvae Larvae, in Roman religion Larvae: see lemures. , seawater seawater Water that makes up the oceans and seas. Seawater is a complex mixture of 96.5% water, 2.5% salts, and small amounts of other substances. Much of the world's magnesium is recovered from seawater, as are large quantities of bromine. used was filtered twice with 10-[micro]m meshes, and the corrugated plastic plates and the tanks were thoroughly scrubbed daily. During the experimental period, water temperature ranged from 21[degrees]C to 25[degrees]C and the salinity from 31[per thousand] to 33[per thousand]. At Day 5 and thereafter, 50 young juveniles from each tank were randomly sampled every 5 days until Day 25, and stored at -20[degrees]C for subsequent analyses. Six samples (Days 0, 5, 10, 15, 20 and 25) were achieved altogether. Methods of Analysis Samples were freeze-dried, and then soft-tissue was separated from the shell. The contents of protein, lipid, total carbohydrate, glycogen, and ash in soft-tissue were determined, and the ratio of soft-tissue to shell weight of each sample was calculated. Tissue protein content (N x 6.25) was calculated from the determination of total N by Kjeldahl analysis. Ash content was calculated by gravimetric analysis gravimetric analysis n. The determination of the quantities of the constituents of a compound. following loss of mass on ignition at 550[degrees]C for 24 h in a muffle furnace. Extraction of lipid was carried out by the method of Bligh & Dyer (1959), and the lipid levels were determined gravimetrically. Total carbohydrate content was determined by the methods of Dubois et al. (1956), and modified by Towle and Giese (1966). D-glucose was used as a calibration standard. Thirty milligrams of soft-tissue were boiled for 10 min with 3 mL 15% TCA TCA 1. trichloroacetic acid. 2. tricarboxylic acid cycle (Krebs cycle). TCA Tricyclic antidepressant, see there , then the mixture was centrifuged at 3,500 rpm for 10 min. TCA (15%) was added to the supernatant supernatant /su·per·na·tant/ (-na´tant) the liquid lying above a layer of precipitated insoluble material. supernatant the liquid lying above a layer of precipitated insoluble material. to the total volume of 10 mL. Two milliliter milliliter /mil·li·li·ter/ (mL) (-le?ter) one thousandth (10-3) of a liter. mil·li·li·ter n. Abbr. of this mixture was mixed with 1 mL 5% phenol phenol (fē`nōl), C6H5OH, a colorless, crystalline solid that melts at about 41°C;, boils at 182°C;, and is soluble in ethanol and ether and somewhat soluble in water. and 5 mL concentrated sulfuric acid sulfuric acid, chemical compound, H2SO4, colorless, odorless, extremely corrosive, oily liquid. It is sometimes called oil of vitriol. Concentrated Sulfuric Acid (p = 1.84). The mixture was allowed to stand for 10 min and then was shaken and placed in a water bath at 30[degrees]C for 15 min. The absorbance absorbance /ab·sor·bance/ (-sor´bans) 1. in analytical chemistry, a measure of the light that a solution does not transmit compared to a pure solution. Symbol . 2. at 490 nm was measured spectrophotometrically. Total carbohydrate content was calculated as amount of released glucose (mg) per mg soft-tissue x 100. Glycogen content was measured by the method of Handel (1965), and glycogen was used as a calibration standard. Fifteen milligrams of soft-tissue were boiled with 1 ml 30% KOH KOH The chemical formula for potassium hydroxide, which is used to perform the KOH test. The tests is also called a potassium hydroxide preparation. Mentioned in: KOH Test KOH potassium hydroxide. for 1 h. The mixture was precipitated with 95% ethanol and glycogen determined by the anthrone method. Tissue glycogen content was calculated as amount of released glycogen (mg) per mg soft-tissue x100. Statistical analysis Data from each sample were subjected to one-way ANOVA anova see analysis of variance. ANOVA Analysis of variance, see there and Duncan test to determine difference in means. Prior to analysis, data on percentages were transformed using squared root of arcsine, to make the variance independent of the mean; alpha levels for all tests were set at 0.05. Statistical analysis was performed using Systat package. RESULTS Shell length, live weight, and tissue chemical composition of juvenile abalone are shown in Table 1. Shell length maintained almost the same within the first 15 days, then there was a slight increase in shell length. Meanwhile, live weight showed a declining trend. However, these changes in shell length and live weight during the 25-day starvation were not statistically different. Tissue protein content decreased dramatically from 53.8 to 41.2% during starvation, and there was a significant difference between the batches of Day 0-5 and the batches of Day 10-25 (P < 0.05). After Day 10, protein content kept almost constant. The decreased protein content at Day 25 amounts to 23.4% of the initial tissue protein (Day 0). Tissue lipid content decreased continuously from 11.6% to 9.3% during the starvation period. After Day 15, tissue lipid was significantly lower than the initial value (P < 0.05). Lost lipid in the juvenile abalone at Day 25 amounts to 19.8% of the initial content (Day 0). Total carbohydrate content also declined significantly from 12.9% to 11.2%. In the early period of starvation (from Day 0 to 5), there were no significant changes in total carbohydrate content. At Day 10, however, the total carbohydrate content declined significantly (P < 0.05), and after that time it remained almost the same. The decline in total carbohydrate by Day 25 amounted to 13.3% of the initial value (Day 0). A slight declining trend, from 4.8% to 4.6%, was observed in the tissue glycogen during the experimental period, but there was no overall significant difference (P > 0.05). Tissue ash content increased significantly from 12.7% to 24.1% with the prolonged time of starvation (P < 0.05). Ash content in larvae of Day 20 and 25 nearly doubled that of Day 0. The ratio of soft-tissue to shell weight decreased significantly from 0.26 to 0.12 (P < 0.05). And the amount declined during Day 0 to Day 10 was larger than that happened in the period from Day 15 to 25. DISCUSSION In the present study, almost the same shell length was maintained within the first 15 days, then there was a slight increasing trend, though this change did not have any statistical significance. This means either that the juvenile abalone might be still able to obtain limited nutrients from the environment to support shell growth, or that shell could grow using the limited nutrients stored in abalone tissues. Meanwhile, live weight showed a more obvious decreasing trend during the 25-day starvation, though the change in live weight was not statistically different either. The significant losses of organic matters (protein, lipid, and carbohydrate) in abalone tissues demonstrated that the young juveniles obtained, very little nutrients from the environment. The loss of live weight, due to organic matter decrease, was probably compensated by water refilling in tissues. Hence, the results and conclusions in this study were not significantly affected by exogenous nutrients. The tissue organic matter decreased continuously with the time of starvation suggesting that the energy reserves (protein, lipid, and total carbohydrate) were catabolized and oxidized to supply the energy required for metabolism. The decreases of tissue reserves mainly occurred during the first 15 days (protein), or 20 days (lipid and carbohydrate), and then the declines were at slower and more constant rates. Previous studies also showed that the decline of energy reserves was most rapid during the first few days during starvation in some marine invertebrates (von Brand et al. 1957, Duerr 1965, Carefoot et al. 1993). During the period of starvation, tissue protein, lipid and total carbohydrate content declined significantly, but there was little change in glycogen content. Taking the mean values of protein, lipid, and total carbohydrate content lost by the juveniles after 25 days of starvation, and converting to joule equivalents (Beukema & de Bruin 1979), it is apparent that juvenile abalone obtained more energy from protein (226.5 kJ/100 g dry weight) than lipid (81.3 kJ/100 g dry weight) and total carbohydrate (3.0 kJ/100 g dry weight). The constant content of glycogen indicated either that glycogen was not in great demand or that it was resynthesized from other constituents by glyconeogenesis. Further studies into glycogen metabolism in juvenile abalone should be carried out. The variation of energy from different substrates probably means that juvenile abalone have selective utilization of energy reserves during starvation. However, the higher energy lost from protein may be partly due to its predominance in young juveniles. There have been different results of energy reserve usage elicited by different researchers, even from the studies on the same species of invertebrates. A number of studies on energy reserves in larval oysters, Ostrea edulis, during metamorphosis showed that lipid acted as the major energy supplier (Millar & Scott 1967, Holland & Spencer 1973). Results from Bartlett (1979) and Rodriguez et al. (1990) indicated that in Ostrea edulis and Crassostrea gigas, tissue protein supplied most of the energy during metamorphosis. The disagreement of these results can possibly be attributed to the different experimental conditions, and the nutritional status nutritional status, n the assessment of the state of nourishment of a patient or subject. , of oyster larvae. Furthermore, Millar & Scott (1967) pointed out that the role of energy reserves in energy metabolism varies with the developmental stages of animals. Results of the present study differed from that of Carefoot et al. (1993), which showed that tissue glycogen acted as the main energy supplier during starvation. Available evidence suggests that energy metabolism of abalone is based on the utilization of carbohydrates, because their natural diet is rich in carbohydrates (Painter 1983), and similarly, abalone tissue contains rich stores of glycogen (Webber 1970, Knauer et al. 1994). In larval abalone, however, energy metabolism may differ largely from that in the adult. In general, juvenile animals require more protein per unit of body weight because their growth rate is higher than that of older individuals (Mercer et al. 1993). In the wild, larval and juvenile abalone might ingest diatoms with high levels of protein, because the protein content of benthic diatoms ranges widely from 3.5% to 47% (Ansell et al. 1964, Darley 1977). In juvenile abalone, there are higher contents of tissue protein and lipid than in older individuals (Mai et al. 1995), but lower glycogen content. There is probably a relationship between the initial biochemical composition and the role of various energy reserves during starvation.
TABLE 1.
Tissue chemical composition in juvenile abalone Haliotis
discus hannai Ino under different starvation.
Day 0 Day 5
Mean shell length
(mm) * 4.79 (0.64) 4.81 (0.57)
Mean live weight
(mg) * 15.0 (1.33) 16.0 (3.18)
Tissue protein (%) [53.83.sup.b] (3.42) [49.98.sup.b] (1.37)
Tissue lipid (%) [11.64.sup.c] (0.54) [11.06.sup.bc] (0.34)
Total carbohydrate (%) [12.89.sup.b] (0.22) [12.62.sup.b] (0.58)
Tissue glycogen (%) 4.81 (0.27) 4.84 (0.31)
Ash content (%) [12.69.sup.a] (1.43) [15.15.sup.ab] (1.70)
Soft-tissue to shell
weight [0.26.sup.d] (0.03) [0.20.sup.c] (0.01)
Day 10 Day 15
Mean shell length
(mm) * 4.79 (0.36) 4.81 (0.28)
Mean live weight
(mg) * 14.9 (2.46) 13.00 (1.85)
Tissue protein (%) [43.02.sup.a] (4.18) [41.75.sup.a] (1.62)
Tissue lipid (%) [10.65.sup.bc] (0.59) [10.00.sup.ab] (0.21)
Total carbohydrate (%) [11.52.sup.a] (0.48) [11.99.sup.ab] (0.44)
Tissue glycogen (%) 4.83 (0.13) 4.73 (0.35)
Ash content (%) [16.96.sup.ab] (2.56) [17.75.sup.ab] (0.84)
Soft-tissue to shell
weight [0.17.sup.bc] (0.01) [0.15.sup.ab] (0.015)
Day 20 Day 25
Mean shell length
(mm) * 4.92 (0.19) 5.07 (0.57)
Mean live weight
(mg) * 14.00 (2.04) 13.6 (1.79)
Tissue protein (%) [42.03.sup.a] (2.15) [41.22.sup.a] (1.87)
Tissue lipid (%) [9.36.sup.a] (0.96) [9.33.sup.a] (0.92)
Total carbohydrate (%) [11.27.sup.a] (0.63) [11.17.sup.a] (0.78)
Tissue glycogen (%) 4.61 (0.27) 4.66 (0.13)
Ash content (%) [20.24.sup.b] (0.93) [24.12.sup.b] (2.58)
Soft-tissue to shell
weight [0.15.sup.ab] (0.02) [0.12.sup.a] (0.015)
* Values of shell length and live weight represent mean (SEM). n = 60.
Other values represent mean (SEM) (n = 3).
([dagger]) Means in each row sharing the same letter are not
significantly different based on Duncan (P > 0.05).
ACKNOWLEDGMENTS The authors thank Mashan Sea-product Company for providing the larval abalone and the experimental facilities. LITERATURE CITED Ansell, A. D., J. Coughlan & K. F. Lander. 1964. Studies on the mass culture of Phaeodactylum. IV Production and nutrient utilization in outdoor mass culture. Limol. Oceanogr. 9:334-342. Bartlett, B. R. 1979. Biochemical changes biochemical changes (bī·ō·keˈmik· in the Pacific oyster Crassostrea gigas (Thunberg, 1795) during larval development and metamorphosis. Proc. Nam. Shellfish. Ass. 69:202. Beukema, J. J. & W. D. Bruin. I979. Calorific values of the soft parts of the tellinid bivalve bivalve, aquatic mollusk of the class Pelecypoda ("hatchet-foot") or Bivalvia, with a laterally compressed body and a shell consisting of two valves, or movable pieces, hinged by an elastic ligament. Macoma baltheca (L) as determined by two methods. J. Exp. Mar. Biol. Ecol. 37:19-30. Bligh, E. G. & W. J. Dyer. 1959. 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Webber, H. H. 1970. Changes in metabolic composition during the reproductive cycle reproductive cycle n. The cycle of physiological changes that begins with conception and extends through gestation and parturition. of the abalone Haliotis cracheroidii (Gastropoda: Prosobranchiata). Physiol. Zool. 43:213-231. Whyte, J. N. C., N. Bourne Bourne, town (1990 pop. 16,064), Barnstable co., SE Mass., crossed by Cape Cod Canal; settled 1627, inc. 1884. Bourne Bridge (1935), across the canal, made the town an entry point to Cape Cod and a resort and commercial center. & C. A. Hodgson. 1987. Assessment of biochemical composition and energy reserves in larvae of the scallop scallop or pecten, marine bivalve mollusk. Like its close relative the oyster, the scallop has no siphons, the mantle being completely open, but it differs from other mollusks in that both mantle edges have a row of steely blue "eyes" and Patinopecten yessoensis. J. Exp. Mar. Biol. Ecol. 113:113-124. SHAOBO DU AND KANGSEN MAI * The Key Laboratory of Mariculture mariculture marine aquaculture. (Ministry of Education), Ocean University of China, Qingdao 266003, People's Republic of China * Corresponding author. E-mail: kmai@ouc.edu.cn |
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