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Changes in biochemical composition of newly spawned eggs, prehatching embryos and newly hatched larvae of the blue crab Callinectes sapidus.

ABSTRACT Changes in biochemical composition during the transition from eggs to larvae in the blue crab Callinectes sapidus were documented. The amounts of proteins, lipids, and carbohydrates decreased from newly formed embryos (stage I) through prehatching embryos (stage II) to newly hatched larvae (stage III; P < 0.05), but the water content increased significantly from stage I to stage II (P < 0.05). Total saturated fatty acid increased significantly from stage I to stage II (P < 0.05), then the content of total saturated fatty acid in stage III decreased to a level similar to that in stage I. In contrast, total monounsaturated fatty acid, n3/n6, and docosahexaenoic acid-to-eicosapentaenoic acid ratios decreased significantly from stage I to stage II (P < 0.05), whereas these variables remained unchanged in stage III. The level of n6 polyunsaturated fatty acid increased significantly from stage I to stage II (P < 0.05) and then stabilized subsequently during stage III. Lipid class analysis revealed that the percentage of triglyceride decreased significantly from stage I to stage III, whereas the proportion of cholesterin increased (P < 0.05). Phospholipids decreased significantly from stage I to stage II (P < 0.05), then returned to stage I levels during stage III. These data suggest that the embryos in stage II and stage III required more energy compared with those in stage I.

KEY WORDS: blue crab, Callinectes sapidus, biochemical composition, embryonic development

INTRODUCTION

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.

Sample Analysis

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).

Lipid extraction

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).

Statistical Analysis

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.

RESULTS

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%).

DISCUSSION

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).

ACKNOWLEDGMENTS

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.

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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: yxcheng@shou.edu.cn

DOI: 10.2983/035.031.0405

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.
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Article Details
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Author:Li, Shuguo; Cheng, Yongxu; Zhou, Bo; Hines, Anson H.
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:1USA
Date:Dec 1, 2012
Words:5022
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