Changes in biochemical composition of newly spawned eggs, prehatching embryos and newly hatched larvae of the blue crab Callinectes sapidus.
KEY WORDS: blue crab, Callinectes sapidus, biochemical composition, embryonic development
Blue crab (Callinectes sapidus) is distributed mainly along the eastern coast of North America (Holthuis 1961), inhabiting estuaries (Mangum & Amend 1972, Lynch et al. 1973, Cameron 1978). The blue crab supports one of the largest and most successful commercial and recreational fisheries in the Chesapeake Bay and elsewhere in its range (Cronin 1998, Rugolo et al. 1998). Although crabs fetch good market prices (Mehmet et al. 2004), global crab fisheries have declined continuously during the past decade (Food and Agriculture Organization 2002). As an alternative, crab aquaculture has advanced, with production technologies for various species of portunid crabs such as swimming crab (Portunus trituberculatus and Portunus pelagicus) (Hamasaki 1996) and mud crab (Scylla serrata and Scylla spp.) (Keenan & Blackshaw 1999). As for C. sapidus, mass production of it is still under experimental evaluation. Most cultured portunid crabs go through only 5 (e.g., the mud crab, S. serrata) or 4 (e.g., P. pelagicus) zoeal larval stages (Hamasaki 1998, Takeuchi 2000, Suprayudi et al. 2002), whereas blue crabs experience 8 zoeal stages and megalops in a larval development that is shorter in duration than development in other species (Costlow & Bookhout 1959).
Blue crab embryos develop over a period of 10-13 days at 28[degrees]C, and the embryos are dependent nutritionally on lipids and lipoproteins stored in yolk. The principal component of blue crab yolk is lipovitellin, a water-soluble lipoprotein composed of similar amounts of lipids and proteins.
Phospholipids play an important role in the structure of the cell membrane whereas triglycerides (TGs) provide energy for physiological processes. The quantity and composition of lipids in decapod crustacean larvae change continuously during development in response to various biotic and abiotic factors (Anger & Harms 1990, Montano & Navarro 1996, Anger 1998, Muhlebach et al. 1999, Hasek & Felder 2005).
In the current study, the composition and lipid profile during three developmental stages of blue crabs were investigated. The aim of this study was to provide insights into the biochemical dynamics during development.
MATERIALS AND METHODS
Sample Collection and Processing
Ovigerous blue crab specimens were sampled by crab traps in the lower Chesapeake Bay, VA, during their reproductive season (June and July 2006 in this study). The live blue crabs were transferred to the laboratory to measure the following variables: carapace length and width, wet body weight, gonadosomatic index (GSI), hepatosomatic index (HSI), and muscle index (MI). Carapace width was measured with dial calipers (0.1 mm), and body wet weight (WW; 0.1 g) was determined with a top-loading balance. Each crab was dissected to determine the WW of ovary and hepatopancreas tissue (0.0001 g) using an analytical balance. Embryos were removed from females and weighed. All tissues were blotted lightly with tissue paper to wipe surface water prior to weighing. The GSI was equal to the ovary WW divided by the total body WW, then multiplied by 100. The HSI for females was equivalent to the WW of hepatopancreas divided by the total body WW, then multiplied by 100.
Developmental Stage Determination
The developmental stages were determined by embryo color and developmental characteristics. In general, newly formed embryos (stage I) were brown-red and embryonic cell division could be observed using a microscope. Prehatching embryos (stage II) were gray and their heartbeat exceeded 100 beats/min. Ovigerous crabs approaching the point of hatching were monitored closely until the larvae emerged (stage III), and the sampling was performed immediately.
Water Content, Protein, and Carbohydrate Analyses
The analyses of water content, crude protein (Kjeldahl method, using a 6.25 N-to-protein conversion factor) were conducted according to the procedures of the Association of Official Analytical Chemists (Association of Official Analytical Chemists 1984). Total carbohydrates were determined by the phenol-sulfuric acid method (Kochert 1978).
Total lipid was extracted with chloroform-methanol (2:1, v/v) according to the method described by Folch et al. (1957).
Fatty Acid Analysis
Fatty acid methyl esters were prepared by transesterification with 0.4 M KOH--methanol, and were verified analytically by flame ionization detection after injecting the sample into an Agilent 6890 gas chromatograph fitted with an HP-5.5% Phenyl Methyl Siloam Capillary Column (30.0 m x 25 mm; Agilent 19091J-413). Injector and detector temperatures were set at 300[degrees]C. The column temperature was held initially at 60[degrees]C for 2 min, followed by an increase at a rate of 20[degrees]C/min to 150[degrees]C, then at a rate of 4[degrees]C/min to 280[degrees]C, maintained until all fatty acid methyl esters had been eluted. The carrier gas was helium with a flow rate at 40 mL/min. Peaks were identified by comparing retention times with known standards (Sigma Chemical Co.)
Lipid Class Analysis
Lipid class was identified and quantified using an Iatroscan MK-5 TLC-FID Analyser. The Iatroscan MK-5 incorporated thin-layer chromatography with flame ionization detection. One microliter of each lipid extract was spotted on a 15 cm x 0.9 mm Chromarod with a sintered silica and ceramic coating. The Chromarods were grouped into 10 sets in a rod holder, thus allowing several samples to be analyzed simultaneously. Chromarods were developed in hexane:diethyl ether:formic acid (42:28:0.3, v:v:v) for 10 cm to determine the lipid composition. After developing, Chromarods were dried at 60[degrees]C for 5 min and then scanned in the flame ionization detector of the Iatroscan (hydrogen flow rate, 160 mL/min; airflow rate, 2 L/min; and scanning speed, 30 sec/rod).
All statistical analyses were performed using SPSS 13.0. Data were expressed as mean [+ or -] SD. Homogeneity of variance was analyzed with Levene's test. Arcsine square root or logarithmic transformation was performed prior to analysis when necessary. Prior to statistical analysis, percentage compositions were arcsine transformed. Statistical analyses were conducted using 1-way analysis of variance and were compared with Duncan's multiple range test. When a normal distribution and/or homogeneity of the variances was not achieved, data were subjected to the Kruskal-Wallis H nonparametric test, followed by the Games-Howell nonparametric multiple comparison test (Sokal & Rohlf 1995). P < 0.05 was regarded as a statistically significant difference.
Body Parameters of Ovigerous Blue Crab
Body parameters of sampled ovigerous blue crabs were similar for newly spawned and prehatching groups, except that the wet weights of newly spawned females were greater than prehatching females (Table 1).
Water, Protein, Lipid, and Carbohydrate Composition
Biochemical composition per embryo or larva varied among the 3 developmental stages (Tables 2 and 3). Protein, lipid, and carbohydrate contents decreased significantly whereas water content increased throughout development.
Fatty Acid Composition
The fatty acid composition of blue crabs in 3 developmental stages is shown in Table 4. The predominant fatty acids included palmitic (16:0), palmitoleic (16:1n7), stearic (18:0), oleic (18:1 n9), eicosapentaenoic (20:5n3, EPA), and docosahexaenoic (22:6n3, DHA) acids, with each of these lipid classes accounting for more than 5% of total fatty acids. The level of total saturated fatty acid increased significantly from stage I to stage II (P < 0.05), and then decreased to stage I levels during stage III. However, total monounsaturated fatty acid, n3/n6, and DHA/EPA contents during stage I decreased significantly compared with those in stage II (P < 0.05); during stage III, these levels stabilized. Total polyunsaturated fatty acid, polyunsaturated fatty acid/saturated fatty acid, and n3 did not differ among the 3 developmental stages. The level of n6 polyunsaturated fatty acid increased significantly from stage I to stage II (P < 0.05), then stabilized during stage III.
Lipid Class Composition
Lipid class profiles from stage I to stage III are presented as content weight per individual embryo or larva (Fig. 1) and as a percentage by weight per individual embryo or larva (Fig. 2). Lipid class analysis revealed that the percentage of TG decreased significantly (P < 0.05) from stage I (0.18 [micro]g or 33.96%) to stage III (0.02 [micro]g or 4.72%), whereas cholesterin showed a reverse change (stage I, 0.03 [micro]g or 4.48%; stage III, 0.07 [micro]g or 16.01%). Free fatty acids (FFAs) showed a remarkable 4-fold increase from stage I (0.02 [micro]g or 4.48%) to stage II (0.17 [micro]g or 16.01%), and then decreased significantly (P < 0.05) from stage II (0.17 [micro]g or 35.09%) to stage Ill (0.13 [micro]g or 27.72%). The phospholipid level decreased significantly from stage I (0.37 lag or 57.81%) to stage II (0.18 [micro]g or 32.66%; P < 0.05), and then return to stage I levels during stage III (from 0.18-0.28 [micro]g or from 32.66-51.55%).
Throughout the early development of blue crab, the embryos use lipid and, to a lesser degree, protein to build tissue, and the total amount of these components decrease from stage I to stage III. In some crustaceans, by contrast, these biochemical components show different patterns during embryonic development. In Macrobrachium nipponense, protein seems to act as the main structural substance, whereas lipid mainly provides energy (Zhao et al. 2007). The primary constituents of blue crab yolk are lipovitellin and lipid droplets. The lipovitellin provides the developing blue crab embryos with lipids and amino acids for protein synthesis in nutritional needs of newly formed embryos (Richard & Thomas 1995, Walker et al. 2006).
Throughout the course of embryogenesis of Artemia, proteins are degraded into amino acids and peptides by proteases (Chaffoy de Courcelles & Kondo 1980, Ezquieta & Vallejo 1985). Also, in Emerita, lipids from lipovitellin and droplets are hydrolyzed by lipases (Subramoniam 1991). These biochemical reactions provide energy and components for the development of blue crab embryo. Thus, both protein and lipid contents decreased significantly during embryonic development of blue crab. Carbohydrates also decreased during blue crab development, but carbohydrates probably contribute little to the embryonic structural development of blue crab (Tables 2 and 3).
In newly spawned eggs of blue crab, the content of lipid was 0.72 [micro]g, significantly lower than that in two other portunid crab species, Scylla serrata (1.94 [micro]g) (Cheng et al. 1999) and Portunus trituberculatus (4.14 [micro]g) (Chen et al. 2007). Higher lipid content indicates that there is sufficient lipid reserve after hatching to meet the need by the newly hatching larvae during development, and which allows them to survive a longer period of starvation before the first feeding (Nates & McKenney 2000). This is also a trait of embryos in species that go through fewer zoeal stages, as seen in these other portunid genera (John & Soundarapandian 2009).
During blue crab embryonic development, the content of arachidonic acid (C20:4) increased significantly, nearly doubling from 2.13% (stage I) to 3.93% (stage III). At the physiological level, C20:4 is a precursor in the synthesis of prostaglandins (Lilly & Bottino 1981), which are potent substances that have effects on reproduction, digestion, and respiratory systems, and control the permeability of ions through membranes and restrain fat dissolution (Ying et al. 2006). C20:4 is relevant to the repression of dissolving of fat (Ying et al. 2006), but its function in developing blue crabs has not been studied.
Stage I embryos not only contained more lipids, but also displayed a greater proportion of TG than stages II and III, suggesting that much TG was used for hatching and excess fatty acids were released (Nates & McKenney 2000). Although a decrease in TG was concomitant with an increase in FFAs, the polar lipid fraction remained relatively stable during stages I and III, and decreased during stage II alone, suggesting that the prehatching stage consumes more energy than other stages. During stage III, the phospholipid fraction increased significantly, indicating that more FFAs were transformed and incorporated into polar lipids rather than into neutral lipids (Dall et al. 1993). The excess FFAs could be diverted for growth purpose at any point in development. Thus, these pathways of fatty acid conversion appear to provide flexibility for development.
Decapod larvae generally exhibit a limited ability to introduce double bonds into the n6 and n3 position of C18, C20, and C22 fatty acids (Teshima et al. 1992), and the higher proportion of EPA and DHA in decapods reflects that larval development is supported mainly by lipid material derived from yolk. Throughout the course of embryonic development of Callinectes sapidus, the levels of C14:0, C16:1n7, and C22:5n3 decreased significantly, whereas EPA increased significantly, suggesting that the former group acts mainly as an energy source, whereas the latter serves primarily as structural substance. C16:0, C16:1n7, and C18:1n9 were the major fatty acids in 3 developmental stages of blue crab embryos, which is consistent with other crustaceans (Teshima & Kanazawa 1983, Gonzalez-Baro & Pollero 1988, Jeckel et al. 1989, Teshima et al. 1989, Mourente et al. 1994).
It is generally considered that EPA and DHA are essential fatty acids for decapod crustaceans, and these components have important functions for fertilization and hatching (Catacutan 1991), and degrade during these key events. In our study, the EPA level increased significantly, but the DHA content decreased significantly from stage I to stage III in blue crab embryos. These findings suggest that the functions of EPA and DHA in blue crab development may differ from other decapods. In general, the increase in long-chain fatty acids is implemented by the elongation of short-chain fatty acids. During embryonic development, no exogenous fatty acids are supplied, so changes in fatty acids are likely to be the reaction of dehydration and transition among the fatty acids originally stored in yolk (Wang et al. 2007).
This research was supported, in part, by grants to A. H. H. from NOAA through the Blue Crab Advanced Research Consortium, Smithsonian Marine Science Network, and Smithsonian Environmental Sciences Program.
Anger, K. 1998. Patterns of growth and chemical composition in decapod crustacean larvae. Invert. Rep. Dev. 33:159-176.
Anger, K. & J. Harms. 1990. Elemental (CHN) and proximate biochemical composition of decapod crustacean larvae. Comp. Biochem. Physiol. 97B:69-80.
Association of Official Analytical Chemists. 1984. Official methods of analysis of the Association of Official Analytical Chemists, 14th edition. Association of Official Analytical Chemists Inc., Arlington, VA: 114 pp.
Cameron, J. N. 1978. NaCl balance in blue crabs, Callinectes sapidus, in fresh water. J. Comp. Physiol. B 123:127-135.
Catacutan, M. R. 1991. Growth and fatty acid composition of Penaeus mondon juveniles fed various lipids. Isr. J. Aquacult. 43: 47-56.
Chaffoy de Courcelles, D. D. & M. Kondo. 1980. Lipovitellin from the crustacean, Artemia salina: biochemical analysis of lipovitellin complex from the yolk granules. J. Biol. Chem. 255:6727-6733.
Chen, S., X. Wu, Y. X. Cheng, C. Wan, D. Zhu, B. Zhou, J. Wan & L. Gong. 2007. Changes of proximate biochemical composition and energy source during embryonic development of swimming crab, Portunus trituberculatus. J. Fish. Sci. Chn. 2:229-235. (in Chinese).
Cheng, Y. X., S. J. Li, X. L. Chen & G. Z. Wang. 1999. The changes of lipid composition of the crab Scylla serrata during the embryonic development. Presented at the Fifth International Symposium on the Efficient Allocation and Preservation of Marine Biological Resources. Yosu National University press, Yosu, Korea. 79-90.
Costlow, J. D., Jr. & C. G. Bookhout. 1959. The larval development of Callinectes sapidus Rathbun in the laboratory. Biol. Bull. 116:373-396.
Cronin, L. E. 1998. Early days of crabbing and a brief history for the Chesapeake Bay. J. Shellfish Res. 17:379-382.
Dall, W., A. Chandumpai & D. M. Smith. 1993. The fate of some [sup.14]C-labelled dietary lipids in the tiger prawn Penaeus esculentus. Mar. Biol. 115:39-45.
Ezquieta, B. & C. G. Vallejo. 1985. The trypsin-like proteinase of Artemia: yolk localization and developmental activation. Comp. Biochem. Physiol. B 82:731-736.
Folch, H., M. Less & H. A. Stanley. 1957. A simple method for isolation and purification of total lipids from animal tissues. J. Biochem. 226:497-499.
Food and Agriculture Organization. 2002. The state of world fisheries and aquaculture 2002. http://www.fao.org/sof/sofia/ index_ en.htm.
Gonzalez-Baro, M. R. & R. J. Pollero. 1988. Lipid characterization and distribution among tissues of the freshwater crustacean Macrobrachium borellii during annual cycle. Comp. Biochem. Physiol. 91B:711-715.
Hamasaki, K. 1996. Study on the reproduction and the development of the swimming crab Portunus trituberculatus. PhD diss., Japan Sea-Farming Association (JAFSA), Kyushu University. pp. 153.
Hamasaki, K. 1998. Dietary value for larval swimming crab Portunus trituberculatus of marine rotifer Brachionus rotundiformis cultured with several feeds. Nippon Suisan Gakkaishi 64:841-846.
Hasek, B. E. & D. L. Felder. 2005. Biochemical composition of ovary, embryo, and hepatopancreas in the grapsoid crabs Armases cinereum and Sesarma nr. reticulatum (Crustacea, Decapoda). Comp. Biochem. Physiol. B 140:455-463.
Holthuis, L. B. 1961. Report on the collection crustacean Decapoda and Stomatopoda from Turkey and Balkans. Zool. Verb. 47:1-67.
Jeckel, W. H., J. E. Aizpum & V. J. Moreno. 1989. Biochemical composition, lipid classes and fatty acids in the ovary of the shrimp Pleoticus muelleri Bate. Comp. Biochem. Physiol. 92B:271-276.
John, N. S. & P. Soundarapandian. 2009. Embryonic development of commercially important portunid crab Portuns sanguinolentus (Herbst). Int. J. Anim. Vet. Adv. 1:32-38.
Keenan, C. P. & A. Blackshaw. 1999. Mud crab aquaculture and biology. In: Proceedings of an international scientific forum held in Darwin, Australia, April 21 24, 1997, ACIAR Proceedings, vol. 78. C. P. Keenan and A. Blackshaw, eds., Darwin. Watson Ferguson & Co., Brisbane, Australia. pp. 116.
Kochert, A. G. 1978. Carbohydrate determination by the phenolsulfuric acid method. In: J. A. Hellebust & J. S. Craigie, editors. Handbook of phycolocical methods: physiological and biochemical methods. London, UK: Cambridge University Press. pp. 95-97.
Lilly, M. L. & N. R. Bottino. 1981. Identification of arachidonic acid in Gulf of Mexico shrimp and degree of biosynthesis in Penaeus setiferus. Lipids 16:871-875.
Lynch, M. P., K. L. Webb & W. A. Van Engel. 1973. Variations in serum, constituents of the blue crab Callinectes sapidus: chloride and osmotic concentrations. Comp. Bioehem. Physiol. 44A:719-734.
Mangum, C. P. & L. M. Amende. 1972. Blood osmotic concentration of the blue crab (Callinectes sapidus Rathbun) found in freshwater. Chesap. Sci. 13:318-320.
Mehmet, C., T. Canan & M. Celik. 2004. Fatty acid composition of the blue crab (Callinectes sapidus Rathbun, 1896) in the north eastern Mediterranean. Food Chem. 88:271-273.
Montano, M. & J. C. Navarro. 1996. Fatty acids of wild and cultured Penaeus pannamei larvae from Ecuador. Aqua. 142:259-268.
Mourente, G., A. Medina, S. Gonzalez & A. Rodriguez. 1994. Changes in lipid class and fatty acid contents in the ovary and midgut gland of the female fiddler crab Uca tangeri during maturation. Mar. Biol. 121:182-194.
Muhlebach, A., C. Albers & G. Kattner. 1999. Differences in the sterol composition of dominant Antarctic zooplankton. Lipids 34:45-51.
Nates, S. F. & C. L. McKenney, Jr. 2000. Ontogenetic changes in biochemical composition during larval and early postlarval development of Lepidophthalmus louisianensis, a ghost shrimp with abbreviated development. Comp. Biochem. Physiol. B 127:459-468.
Richard, F. L. & N. Thomas. 1995. Effect of reproductive toxicants on lipovitellin in female blue crabs, Callinectes sapidus. Mar. Environ. Res. 39:151-154.
Rugolo, L., K. S. Knotts & A. M. Lange. 1998. Historical profile of the Chesapeake Bay blue crab (Callinectes sapidus) fishery. J. Shellfish Res. 17:383-394.
Sokal, R. R. & F. J. Rohlf. 1995. Biometry: the principles and practice of statistics in biological research, 3rd edition. New York: W. H. Freeman. 937 pp.
Subramoniam, T. 1991. Yolk utilization and esterase activity in the mole crab Emerita asiatica (Milne Edwards). In: A. Wenner & A. Kuris, editors. Crustacean egg production. Rotterdam: A.A. Balkema. pp. 19-29.
Suprayudi, M. A., T. Takeuchi, K. Hamasaki & J. Hirokawa. 2002. The effect of n-3 HUFA content on the development and survival of mud crab, Scylla serrata, larvae. Suisan Zoshoku 50:205-212.
Takeuchi, T. 2000. A review of studies on the effect of dietary n-3 highly unsaturated fatty acids on larval swimming crab Portunus trituberculatus and mud crab Scylla tranquebarica. In: The Proceedings of the JSPS-DGHE International Symposium on Fisheries Science in Tropical Areas, August 21-25, 2000, vol. 10. Odang Carman, Tokyo, Japan Society for the Promotion of Science. pp. 244-247.
Teshima, S. & A. Kanazawa. 1983. Variation in lipid compositions during the ovarian maturation of the prawn. Bull. Jpn Soc. Sci. Fish. 49:957-962.
Teshima, S., A. Kanazawa & S. Koshio. 1989. Lipid metabolism of the prawn P. japonicus during maturation: variation in lipid profiles of the ovary and hepatopancreas. Comp. Biochem. Physiol. 92B:45-49.
Teshima, S., A. Kanazawa & S. Koshio. 1992. Ability for bioconversion of n-3 fatty acids in fish and crustaceans. Oceanis 18:67-75.
Walker, A., S. Ando, G. D. Smith & R. F. Lee. 2006. The utilization of lipovitellin during blue crab (Callinectes sapidus) embryogenesis. Comp. Biochem. Physiol. B 143:201-208.
Wang, G. Z., X. H. Kong, K. J. Wang & S. J. Li. 2007. Variation of specific proteins, mitochondria and fatty acid composition in gill of Scylla serrata (Crustacea, Decapoda) under low temperature adaptation. J. Exp. Mar. Biol. Ecol. 352:129-138.
Ying, X. Y., W. X. Yang & Y. P. Zhang. 2006. Comparative studies on fatty acid composition of the ovaries and hepatopancreas at different physiological stages of the Chinese mitten crab. Aqua. 256:617-623.
Zhao, Y. M., Y. L. Zhao & C. Zeng. 2007. Morphogenesis and variations in biochemical composition of the eggs of Macrobrachium nipponense (De Haan, 1849) (Decapoda, Caridea, Palaemonidae) during embryonic development. Crustac. 9:1057-1070.
SHUGUO LI, (1,2) YONGXU CHENG, (1) * BO ZHOU (1) AND ANSON H. HINES (3)
(1) Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, No 999 Huchenghuan Road, Lingang New District, Shanghai 201306, China; (2) College of Animal Science and Technology, Inner Mongolia University for the Nationalities, Tongliao, 028000, China; (3) The Smithsonian Environment Research Center, PO Box 28, Edgewater, MD 21037
* Corresponding author. E-mail: email@example.com
TABLE 1. Parameters of sampled ovigerous blue crabs. Carapace length Crab type Wet weight (g) (cm) Newly spawned 190.34 [+ or -] 30.75 6.08 [+ or -] 0.35 Prehatched 146.67 [+ or -] 17.65 5.73 [+ or -] 0.40 Carapace width Hepatosomatic Crab type (cm) index Newly spawned 15.45 [+ or -] 1.31 3.93 [+ or -] 0.93 Prehatched 15.09 [+ or -] 1.24 3.98 [+ or -] 0.99 Crab type Gonadosomatic index Muscle index Newly spawned 5.24 [+ or -] 1.96 28.41 [+ or -] 2.32 Prehatched 5.37 [+ or -] 1.93 29.34 [+ or -] 1.21 TABLE 2. Biochemical composition by weight of 3 developmental stages of blue crab (micrograms per individual; n = 5). Developmental Proteins Lipids stage Stage I 2.32 [+ or -] 0.19 (a) 0.72 [+ or -] 0.1 l (a) Stage II 2.26 [+ or -] 0.18 (b) 0.50 [+ or -] 0.07 (b) Stage III -- 0.44 [+ or -] 0.10 (b) Developmental Carbohydrates Water content stage Stage I -- 10.38 [+ or -] 0.79 (a) Stage II 0.10 [+ or -] 0.02 (b) 12.80 [+ or -] 0.36 (b) Stage III 0.04 [+ or -] 0.02 (c) -- Data are expressed as mean [+ or -] SD. Within the same column, values with different superscript letters are significantly different (P < 0.05); values with the same superscript letters are not significantly different (P > 0.05). --, no data. TABLE 3. Biochemical composition by percentage of 3 embryonic stages of blue crab (percentage of wet weight; n = 6). Developmental Proteins Lipids Stage Stage I 16.58 [+ or -] 0.88 (a) 4.87 [+ or -] 1.19 (a) Stage II 13.78 [+ or -] 0.72 (b) 2.94 [+ or -] 0.37 (b) Stage III -- 1.11 [+ or -] 0.22 (c) Developmental Carbohydrates Water Content Stage Stage I -- 73.90 [+ or -] 1.13 (a) Stage II 0.54 [+ or -] 0.14 (b) 79.26 [+ or -] 1.43 (b) Stage III 0.12 [+ or -] 0.05 (c) -- Data are expressed as mean t SD. Within the same column, values with different superscript letters are significantly different (P < 0.05). --, no data. TABLE 4. Fatty acid (FA) profile of blue crab 3 three developmental stages (percentage of total FA). FA Stage I Stage II C14:0 1.79 [+ or -] 0.07 (a) 1.18 [+ or -] 0.13 (b) C15:0 0.87 [+ or -] 0.11 (a) 0.72 [+ or -] 0.13 (b) C16:0 21.42 [+ or -] 1.11 (a) 22.97 [+ or -] 0.99 (a) C17:0 0.88 [+ or -] 0.19 1.12 [+ or -] 0.28 C18:0 5.62 [+ or -] 0.43 (a) 8.86 [+ or -] 0.59 (b) [SIGMA] SFA 30.57 [+ or -] 1.19 (a) 34.85 [+ or -] 1.17 (b) C14:1n7 0.32 [+ or -] 0.07 (a) 0.23 [+ or -] 0.11 (a) C16:1 n5 2.09 [+ or -] 0.50 2.03 [+ or -] 0.42 C16:1n7 10.08 [+ or -] 2.21 (a) 7.25 [+ or -] 0.92 (b) C17:1 0.69 [+ or -] 0.21 (a) 0.50 [+ or -] 0.07 (b) C18:1n7 3.44 [+ or -] 1.07 3.21 [+ or -] 0.49 C18:1 n9 12.19 [+ or -] 0.89 11.74 [+ or -] 2.00 C20:1n7 2.40 [+ or -] 0.44 (a) 1.80 [+ or -] 0.54 (a b) C20:1n9 2.73 [+ or -] 0.50 (a) 2.00 [+ or -] 0.47 (b) [SIGMA] MUFA 33.94 [+ or -] 1.56 (a) 28.77 [+ or -] 1.80 (b) C18:2n6 1.49 [+ or -] 0.40 1.91 [+ or -] 1.07 C20:2n6 1.19 [+ or -] 0.39 1.31 [+ or -] 0.61 C22:2n6 0.36 [+ or -] 0.11 (a) 0.23 [+ or -] 0.02 (b) C18:3n3 - 0.35 [+ or -] 0.18 (b) C18:3n4 1.10 [+ or -] 0.24 (a) 0.71 [+ or -] 0.19 (b) C20:3n3 0.38 [+ or -] 0.10 (a) 0.28 [+ or -] 0.04 (a b) C203n6 0.36 [+ or -] 0.08 (a) 0.30 [+ or -] 0.05 (a b) C18:4n3 0.86 [+ or -] 0.34 0.43 [+ or -] 0.17 C20:4n3 0.83 [+ or -] 0.17 (a) 0.45 [+ or -] 0.15 (b) C20:4n6 2.13 [+ or -] 0.38 (a) 3.40 [+ or -] 0.67 (b) C20:5n3 7.71 [+ or -] 0.69 (a) 10.14 [+ or -] 1.03 (b) C22:5n3 1.31 [+ or -] 0.36 (a) 0.82 [+ or -] 0.15 (b) C22:6n3 12.19 [+ or -] 1.37 (a) 10.02 [+ or -] 1.30 (b) [SIGMA] PUFA 29.89 [+ or -] 2.13 30.34 [+ or -] 3.09 PUFA/SFA 0.98 [+ or -] 0.09 0.87 [+ or -] 0.11 [SIGMA] n3 23.27 [+ or -] 1.33 22.49 [+ or -] 2.18 [SIGMA] n6 5.52 [+ or -] 0.88 (a) 7.14 [+ or -] 1.23 (b) n3/n6 4.29 [+ or -] 0.59 (a) 3.21 [+ or -] 0.53 (b) DHA/EPA 1.60 [+ or -] 0.29 (a) 0.99 [+ or -] 0.12 (b) Unknown 5.59 [+ or -] 0.90 6.04 [+ or -] 1.23 FA Stage III C14:0 0.96 [+ or -] 0.21 (c) C15:0 0.64 [+ or -] 0.12 (b) C16:0 19.74 [+ or -] 1.45 (b) C17:0 1.04 [+ or -] 0.18 C18:0 8.85 [+ or -] 1.06 (b) [SIGMA] SFA 31.23 [+ or -] 2.12 (a) C14:1n7 4.31 [+ or -] 0.92 (b) C16:1 n5 2.06 [+ or -] 0.34 C16:1n7 4.78 [+ or -] 0.83 (c) C17:1 0.46 [+ or -] 0.07 (b) C18:1n7 3.71 [+ or -] 0.56 C18:1 n9 11.57 [+ or -] 1.45 C20:1n7 1.61 [+ or -] 0.28 (b) C20:1n9 1.80 [+ or -] 0.30 (b) [SIGMA] MUFA 30.31 [+ or -] 1.78 (b) C18:2n6 1.72 [+ or -] 0.75 C20:2n6 1.59 [+ or -] 0.59 C22:2n6 - C18:3n3 0.78 [+ or -] 0.19 (c) C18:3n4 0.74 [+ or -] 0.27 (b) C20:3n3 0.25 [+ or -] 0.06 (b) C203n6 0.24 [+ or -] 0.06 (b) C18:4n3 0.27 [+ or -] 0.05 C20:4n3 0.35 [+ or -] 0.11 (b) C20:4n6 3.93 [+ or -] 0.93 (c) C20:5n3 11.46 [+ or -] 1.01 (c) C22:5n3 0.50 [+ or -] 0.17 (c) C22:6n3 9.60 [+ or -] 1.21 (c) [SIGMA] PUFA 31.44 [+ or -] 1.92 PUFA/SFA 1.01 [+ or -] 0.13 [SIGMA] n3 23.21 [+ or -] 1.89 [SIGMA] n6 7.48 [+ or -] 1.08 (b) n3/n6 3.17 [+ or -] 0.59 (b) DHA/EPA 0.84 [+ or -] 0.11 (b) Unknown 7.02 [+ or -] 0.89 Data are expressed as mean [+ or -] SD. Within the same row, values with different superscript letters are significantly different (P < 0.05); values with the same superscript letters are not significantly different (P> 0.05). DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid; SFA, saturated fatty acid.
|Printer friendly Cite/link Email Feedback|
|Author:||Li, Shuguo; Cheng, Yongxu; Zhou, Bo; Hines, Anson H.|
|Publication:||Journal of Shellfish Research|
|Date:||Dec 1, 2012|
|Previous Article:||Seasonal variation in brood size of the spiny lobster Panulirus gracilis (decapoda: palinuridae) in Mexican waters of the gulf of California.|
|Next Article:||Growth and longevity of Glycymeris nummaria (Linnaeus, 1758) from the eastern Adriatic, Croatia.|