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Highlights in BioScience             

ISSN: 2682-4043 

DOI:10.36462/H.BioSci.20210                                                                                                          
 

 

Highlights in BioScience                                                                                                                                                                           July 2020| Volume 3 

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Research Article 

 

 

Open Access 

 
 

 

 

 

 

1University of Tunis El Manar, Faculty of 

Sciences of Tunis, Laboratory of Ecology, 

Biology and Physiology of aquatic organisms, 

2092 Tunis, Tunisia 

 

 

Contacts of Authors  

 

 

* To whom correspondence should be 

addressed: Imene Chetoui 

 

Citation: Chetoui I, Bejaoui S, Ghribi F, El 

Cafsi M (2020). Annual variation of the 

biochemical composition, energy reserves and 

physiological indices in Mactra stultorum 

tissues from the Tunisian coasts. Highlights in 

BioScience Volume 3. Article ID 20210. 

dio:10.36462/ H.BioSci.20210 

 

Received:  May 23, 2020 

 

Accepted:  July 9, 2020 

 

Published: July 12, 2020 

 
 

Copyright: © 2020 Chetoui et al. This is an 

open access article distributed under the terms 

of the Creative Commons Attribution License, 

which permits unrestricted use, distribution, 

and reproduction in any medium, provided the 

original author and source are credited. 

 

 

Data Availability Statement: All relevant data 

are within the paper and supplementary 

materials 

 

 

 

Funding: The authors have no support or 

funding to report. 

 

 

Competing interests: The authors declare that 

they have no competing interests. 

Annual variation of the biochemical composition, energy 

reserves and physiological indices in Mactra stultorum 

tissues from the Tunisian coasts 

 
Imene Chetoui

1
*, Safa Bejaoui

1
, Feriel Ghribi

1
 and M'hamed El Cafsi

1
  

 

Abstract 

        The present study assessed the consequences of 

environmental changes on the biochemical quality and the 

physiological condition of the whole body and others organs 

Mactra stultorum collected from the north coast of Tunisia. 

Significant variations in the biochemical components, PE and CI 

have shown between seasons. The depletion of glycogen in all tissues 

was recorded during spawning periods (late spring and summer). Lipid 

accumulation in gonad–visceral mass during the early and late 

gametogenesis stages was associated with the increase in CI and GSI. 

However, decreases in lipid and protein contents were recorded in all the 

tested organs during summer when the animals are in the spawning 

period, suggesting that clams could accumulate proteins and lipids. 

Regarding the environmental factors, a negative and a significant 

correlation was recorded between glycogen, lipid contents and water 

temperature. Based on these results and as M. stultorum is 

appreciated by the consumers, we suggest that the harvesting of M. 

stultorum should be concentrated on February to June when the 

whole body was characterized by an important amount of the 

biochemical composition when the seafood is at its highest nutritive 

value as compared to August to January. Because of its high nutritive 

value especially it’s richness by some important and essentials fatty 

acids, M. stultorum seems to be considered as   an important commercial 

species in many countries and in Tunisia particularly. We suggest that 

harvesting of M. stultorum should be concentrated on the period when 

the seafood is at its highest nutritive value. survivability rates from 

malignancy. The greatest variations in the mortality ratios existed within 

the European countries.  

 

Keywords: Mactra stultorum, Seasonal variations, Biochemical composition, 

Percentage edibility, Condition index and Gonado-somatic index. 

 

Introduction  

Over the last few decades, mollusk bivalves became a high nutritious food 

source in the human diet. They are considered highly nutritional with interesting 

dietetic properties because of their valuable biochemical constituents such as 

proteins, glycogen, lipids, fatty acids and minerals. Research on the biochemical 

and energy reserves of bivalve species was launched in the 19
th

 century. Several 

authors have studied the seasonal variation of the biochemical compounds of 

bivalves, the storage cycle of their energy reserves relative to the reproduction of 

the species and the environmental fluctuations of the environment [1-3].

https://creativecommons.org/licenses/by/4.0/


 

 

Chetoui et al., 2020                                                                                                               Annual dynamic of the biochemical compositions on M. stultorum 

 

 

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In bivalves, glycogen constitutes the most prominent 

reserve, especially during the processes of gametogenesis  

[4, 5]. Glycogen is a good supplying energy demand during 

the formation of gametes [6].  Due to their high caloric 

content, lipids serve as energy storage under critical 

nutritional conditions [7]. They play an important role in 

metabolic pathways in the formation of gametes and are 

considered as the major reserve of oocytes [8, 9]. Protein, 

one of the abundant biochemical components in bivalves, 

can be serving also serve as an energy reserve during 

gametogenesis when other reserves are exhausted [10]. 

Certain exogenous factors, such as the 

temperature of the water and the availability of food 

in the surrounding environment as well as some 

endogenous conditions such as the reproductive cycle 

play a key role in the variation of the physiological 

fitness of many marine organisms [11, 12]. So it has 

been demonstrated that there is an important and 

broad relationship between the percentage edibility, 

the condition index and organic content. Additionally, 

the condition index, which supported as the health 

index, considered as a good index to determine the 

evolution of the physiological processes in relation to 

the reproduction, growth, mortality, parasitic and 

other contagions factors [13, 14]. 

The bivalve Mactra stultorum is a benthic species 

inhabiting sandy beaches of the lower infra-littoral zone. It 

is widely distributed along the north and south coasts of the 

Mediterranean Sea, the Black Sea, Senegal and Europe [15]. 

In Tunisia, it has been reported from the North coasts and 

from the South in the Gulf of Gabes [16]. Because of its 

high nutritive value especially it’s richness by some 

important and essentials fatty acids such as eicosapentanoic 

(EPA, 20:5n-3) and docosahexanoic (DHA, 22:6n-3) acids 

[17], M. stultorum seems to be considered as an important 

commercial species in many countries such as in Manche 

(Atlantic coast) [18]. Recently, the reproductive cycle of M. 

stultorum has been determined by Chetoui et al. [19]. The 

assessment of histological studies indicated that its 

reproductive cycle is synchronous for both sexes.  The 

gametogenesis process is initiated in January. The 

maturation phase is extended from April to July and the 

partial spawning started in spring to reach its peak in late 

summer, indicating a prolonged reproductive activity. To the 

best of our knowledge, the biochemical composition of M. 

stultorum from the Mediterranean coasts in relation to 

various endogenous (reproductive cycle…etc) and 

exogenous conditions (temperature, salinity, food 

accessibility…etc) have not yet been studied. 

The goal of the present work is to investigate the 

annual dynamic of the biochemical composition (including 

macromolecules and glycogen) of the whole soft tissue and 

different organs of M. stultorum collected from northern 

Tunisian coasts and to assess its percentage of edibility (PE) 

and the condition index (CI) in relation to the total 

reproductive period and environmental parameters. 

Materials and Methods 

Sampling site and collection 

Specimens of Mactra stultorum were collected during 

12 months (from June 2008 until May 2009) from the sandy 

beach of station Kalaat El Andalous located at the Gulf of 

Tunis (37°03’73’’N and 10°10’67’’E). The current North-

South is reduced in this range through advanced Sidi Ali 

Mekki. Thus, these waters are usually calm and the bottom 

consists mainly of fine sand deposited on the front of the 

delta plain of Oued Medjerda (Figure 1). 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Figure 1. Maps of sampling area in Tunisia (The black full 

star in the Gulf of Tunis shows the sampling site: Kalaât El 

Andalous). 

Kalaât El Andaous 

Lake  of Medgerda  

GULF OF TUNIS  



 

 

Chetoui et al., 2020                                                                                                               Annual dynamic of the biochemical compositions on M. stultorum 

 

 

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Environmental parameters were measured monthly. 

Surface seawater temperature and salinity were carried out 

in situ depth of 30cm using a mercury thermometer and a 

salinometer, respectively. Chlorophyll a was extracted using 

Whatman GF/F filters with 90% methanol in the laboratory 

and concentration was evaluated according to the protocol 

of Aminot and Chaussepied [20]. Samples of M. 

stultorum were transferred to the laboratory for 

acclimation in filtered seawater in order to eliminate all 

types of nutrients from their digestive glands. After 72 h, 

clams of similar size (30 and 57mm) were selected for 

experimentation. The total Wight and shell dry weight of 

all M. stultorum were analyzed using 0.001 g electronic 

precision balance. The biometric measurements such as shell 

length (SL), height (SH) and width (SW) were measured 

with a digital caliper (0.1mm). 

Experimental analysis  

After sacrifice, separate organs such as mantle (MT), 

adductor muscle (AM), foot (FT), gonad-visceral mass (GV) 

and rest (RE) were dissected for the first group and for the 

second group we selected the body whole. All selected 

animals were kept in a freezer at -30 ° C for biochemical 

analysis. The gonad and visceral mass are taken as a single 

organ (GV) due to the difficulty of their separation. For 

biochemical analysis, each month six replicates were used to 

produce the means with 6–8 M. stultorum pooled in each 

replicate. Total protein content was determined by the 

method of Lowry et al. [21] using the Bovine serum albumin 

(BSA) as a standard range. Samples were homogenized in a 

Tris-HCl buffer (20 mM; pH=7.4), then, centrifuged at 

10.000 × g for 20 min (4°C). Supernatants were stored in 

Eppendorf tubes at -80°C for subsequent analyses. A 

volume of 10 µL supernatants was dissolved in 400 µL of 

water solution to which we added a 2ml of a mixture 

composed of three solutions: sodium carbonate hydrate 

dissolved in a solution of NaOH (0.1N), copper sulfate 

dissolved in water and sodium hydrate dissolved in water. 

To the last mixture we added 200 µL of Folin Reagent, then, 

incubated for 30 min at the darkness. The proteins were 

quantified using the spectrometric method at 540 nm.  

The total glycogens were determined by the enzymatic 

potocol of Dubois et al. [22]. The glycogen was released 

from the tissues by heating 0.5 g of fresh tissue in the 

presence of 2 ml of alkaline solution (KOH, 300 g / l) for 2 

min in a water bath at 100 ° C. Glycogen was precipitated 

by the addition of ethanol 95°C. This precipitate was 

recovered after cooling the tubes in ice and centrifugation at 

3000 rpm for 10 min. It was dissolved in 10 ml of water. 

Then, 1 ml of the last glycogen solution was hydrolyzed by a 

hydrochloric acid HCl (1.2mol / L) in a bath at 100°C for 2 

h.  Then, this hydrolyzate was neutralized by the addition of 

sodium hydroxide solution NaOH (0.4 N) until the color 

changes to pink. Finally, the glucose oxidase reagent was 

added to these last mixtures, which were subsequently 

incubated in a bath at 37 °C for 15 min. The optical density 

was measured at 520 nm. 

Total lipids (TL) were extracted using the method of 

Folch et al. [23]. The flesh was crushed with a solution of 

chloroform: methanol (2:1, v:v) including 0.01% Butyl-

hydroxy-toluene (BHT) as an antioxidant. The extraction 

volume was estimated by 30 ml of extraction solvent per g 

of tissue. The mixture of the extract volume and 2 ml of 

NaCl solution (15%) were centrifuged at 3000 x g for 15 

min.  The chloroform phase was recovered and evaporated 

to dryness by Rotavapor® R-300. Finally, the residue was 

diluted in 2 ml of chloroform solution. The levels of total 

lipid, glycogen and protein are expressed as mg / g Dry 

Weight (mg/g DW). The percentage edibility (PE), the 

condition index (CI) and the gonado-somatic index (GSI) 

were assessed monthly from May 2008 to Jun 2009. A 

total of 30 clams were selected each month for the analysis 

of each index.  The flesh and shells of each clam were 

dried in an oven at 60°C for up to 72 h to determine the 

constant dry tissue and shell weight. For each index, 30 

individuals were collected each month. According to 

Deslou-Paoli et al. [24], the CI was calculated as equation 1 

and the GSI was expressed by equation 2: Equation 1: CI= 

(dry weight of the soft parts/dry weight of shell) *100; 

Equation 2: GSI= (dry weight of the gonad-visceral 

mass/dry weight of shell) *100. The percentage edibility 

(PE) was calculated using Anibal et al. method [25] and 

was estimated using equation 3: Equation 3: PE= (wet 

meat weight (g)/Total wet weight including shell (g)) 

*100.  

Statistical analysis  

Data analysis was performed using the software 

Statistica version 5.0. The biochemical composition of each 

separate tissue and whole body was compared between 

months.  Normality was assessed for all datasets using the 

Shapiro-Wilcoxon test. The significant differences between 

variables were analyzed using one-way analysis of variance 

(ANOVA) followed by posthoc Tukey's test (p<0.05). When 

the conditions for ANOVA were not satisfied, 

nonparametric Kruskal–Wallis's test was used (p<0.05). The 

differences between samples were deemed to be significant 

at p<0.05. Pearson correlation matrix and principal 

component analysis (PCA) were used to exhibit the 

association between biochemical, biological indices, 

percentage ediblity and environmental factors among the 

studied periods 

Results 

Environmental parameters  

The temperature of the seawater varied between 8°C in 

January to 28 °C in July and August. Salinity was highest 

(38.2 psu) in July, dropping to <35psu from December to 



 

 

Chetoui et al., 2020                                                                                                               Annual dynamic of the biochemical compositions on M. stultorum 

 

 

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March with a minimum value noted in January (31 psu). 

This decrease in salinity is generally due to the relatively 

high pluviometry (84.14mm in January) and to discharge 

from the river Medjerda. Chlorophyll a values ranged from 

1.28 mg/l (November) to 6.35mg/l (April) (Figure 2). 

 

 
Figure 2. Physicochemical parameters of Kalaât El 

Andalous during the sampling period (Jun 2008–May 2009). 

 

Biometric analyses 

The biometric data (shell length, height and width) are 

elucidated in Table 1. The shell length (SL) ranged from 

32.68 to 47.82 mm; the shell height (SL) ranged from 25.72 

to 39.83mm, the shell width (SW) varied from 12.88 to 

25.58 mm and the shell dry weight ranged from 3.57 to 

10.5g. 

Table1: Biometric measurements of Mactra stultorum 

during one year. 
 

Month  
SL (mm) SH (mm) SW (mm) SDW (g) 

Mean SD Mean SD Mean SD Mean SD 

J(08) 40.15 6.39 33.81 7.67 20.94 4.35 5.69 1.7 

J(08) 47.52 4.04 39.41 4.81 25.22 2.68 10.5 2.43 

A(08) 46.25 3.16 38.09 3.84 24.52 2.2 8.73 2.21 

S(08) 47.97 2.84 39.2 3.44 25.48 2.1 9.16 2.31 

O(08) 43.55 4.83 36.3 5.9 23.54 3.9 8.08 2.26 

N(08) 40.95 3.68 33.69 4.88 21.83 4.02 5.31 1.99 

D(08) 36.82 3.32 30.8 3.86 19.32 2.38 3.57 1.41 

J(09) 32.68 7.04 25.72 7.79 12.88 5.64 6.34 2.5 

F(09) 46.71 5.64 39.35 6.59 25.56 3.78 8.18 1.74 

M(09) 45.49 4.56 37.99 5.63 24.31 3.22 7.03 2.47 

A(09) 46.97 3.49 39.83 6.22 25.58 3.8 9.78 2.07 

M(09) 40.54 8.08 33.63 9.1 19.8 7.02 9.46 2.85 

Results are given as mean ± SD. n=50 individuals each month.  

SL: shell length; SH: shell height; SW: shell width and SDW: 

shell dry weight. 

 

Biochemical composition 

Seasonal variations in the protein, glycogen and total 

lipid contents of different body parts (foot, gonad-visceral 

mass, mantle, adductor muscle and rest) are shown in (Table 

2). The biochemical constituents showed a significant 

variation between seasons and tissues (p<0.001). In all 

tissues, the highest protein content (235.±8.42 mg/g 

DW) was noted in the foot, while, the minimal amount 

of protein (31.2±3.4 mg/g DW) was noted in the 

adductor muscle. Using to HSD Tukey’s tests (F=3.35, p 

= 0.001), significant differences were recorded for a protein 

of foot which varied from 140 to 235 mg/g DW (p <0.05). It 

marked by tow peaks in September (220.78±10.20 mg/g 

DW) and December (175.07±11.53 mg/g DW).In the 

gonad-visceral mass, the seasonal evolution of protein has 

shown a significant variation throughout the year.  

The minimum level was observed in July (54.18±19.97 

mg/g DW), then; increased significantly to reach two peaks 

in September (231.84±23.13mg/g DW) and April 

(250.94±22.60 mg/g DW). For the mantle, the level was 

relatively stable from June to December, then it dropped in 

January (39.67 ± 9.38 mg/g DW) and enhanced in March 

(126.84 ± 14.48mg/g DW). The protein level in the adductor 

muscle remained stable between 120 and 130mg /g DW 

throughout the study year except October (31.17 ± 8.38 

mg/g DW) and February (60.41 ± 9.40 mg/g DW) in which 

protein level decreased significantly. The protein content in 

the rest part was comprised between 24.3± 0.37 mg/g DW in 

January to 144.9± 1.35 mg/g DW in March. 

The gradient of the glycogen content in M 

stultorum body parts has shown that the FT tissue has the 

high level, followed by those in the tissues from the 

AM, MT and GV. In contrast, lower glycogen content 

was recorded in the RE tissues. The glycogen contents 

varied similarly in the four examined tissues (foot, gonad-

visceral mass, mantle, adductor muscle). They were lower 

from July to September (<20 mg/g DW) and peaked in 

April, and then declined considerably in May.  The lowest 

values of glycogen in the rest part (RE) were detected during 

autumn and winter in particular in November and January 

with (3.54±1.17mg/g DW) and (4.94±1.28 mg/g DW). 

However, similar to other parts of the body, the quantity of 

glycogen peaked in April (17.64±3.9 mg/g DW) One-way 

ANOVA analysis (HSD Tukey’s tests, F=6.51, p = 0) 

indicated that glycogen levels in all examined tissues 

showed significant monthly variations. 

Total lipids contents are unevenly distributed between 

tissues of M. stultorum and varied significantly (p<0.05) 

between seasons except for foot, which varied from 14 to 22 

mg/g. In the gonad-visceral mass, TL content started at 

(50.38± 8.58 mg/g DW) in June and decreased in August 

(25.16± 8.78 mg/g DW). Then, it gradually increased in 

autumn and stabilized in winter. 



 

 

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Table 2.  Seasonal variations in the contents of total protein, glycogen and lipids (mg/g DW) of the body parts and whole body of clam Mactra stultorum. 

 

 
Total protein contents in mg/g dry weight tissue 

 J(08) J(08) A(08) S(08) O(08) N(08) D(08) J(09) F(09) M(09) A(09) M(09) 

FT 150±9.48be 142±8.65 ab 152.1±9.80 bc 221±12 f 170±8.07de 147±11.2abc 175.1±10.8 e 138±10.1ab 130.4±11.41 a 142.3±7.828 ab 162.9±12.62dca 235±8.42 f 

GV 112±10.1b 54.2±9.99 a 164±10.77c 232±11.6 e 117±11.1 bd 97±10.9 b 157±10.94 c 146±12.3 cd 95.2±11.36b 177.8±10.21 c 250.9±11.3 c 172±10.9 c 

MT 96.8±6.14 d 83.4±8.55 be 70.82±13.65 b 77.2±9.66 b 79.6±6.35 b 81±10.6 b 77.82±5.7 b 39.7±5.0 a 96.22±7.27 ad 126.8±5.35 f 97.92±8.47 de 97.6±10. ce 

AM 136±8.21 f 137±7.57 f 142.5±6.63 f 126±3.7 ed 31.2±3.4 a 73.9±3.8c 135±8.19 ef 138±9.7 f 60.43±6.36 b 70.6±6.6 bc 121.4±6.9 d 134±4.58 ef 

RE 93.4±3.08 c 83.8±4.01c 79.76±1.075 c 97.9±2.3 d 53.9±4.08 b 57.5±7.87 b 98.11±1.71 d 24.3±0.37 a 84.37±5.52 c 144.9±1.35 f 121.2±1.38 e 97.2±2.1 d 

WB 114±4.89 c 97.4±9.2 b 114.8±3.9 c 142±9.2e 84.2±6.7 a 85.8±4.5a 123.5±5.56d 85.2±2.52 a 91.84±6.16ab 134.6±3.11 f 145.9±2.98e 139±2.11 ef 

 

 
Total glycogen contents in mg/g dry weight tissue 

 J(08) J(08) A(08) S(08) O(08) N(08) D(08) J(09) F(09) M(09) A(09) M(09) 

FT 14.6±1.96 cd 10.06±1.5 acd 6.45±1.56 ab 5.15±1 a 15.4±1.49 d 11.5±1.64 bca 28.84±2 ef 26.8±1.41 eg 29.7±2.82 ef 33.4±1.17 fh 35.5±3 h 23±2.4g 

GV 9.04±2.93 bc 6.22±1.06 b 3.47±1.68 a 4.18±1.02 ab 11.88±1 cd 16.56±1.89 de 20.05±2.96 eg 14.84±1.02 df 18.5±1.9 ef 23.81±1.1 g 35.46±1.2 h 8.53±0.81 ab 

MT 14.11±1.57 c 9.51±1.05 b 8.37±0.75 a 7.55±2.03 b 8.86±1.83 b 10.45±1.51 bc 22.37±1.4 d 12±1.31 bc 10.25±1.28 c 24.78±2.21d 27.71±1.5 e 20.54±1.34 d 

AM 12.71±0.92 b 10.54±1.1 a 6.03±1.25 a 7.01±1.76 a 10.81±1.61 ab 19.84±2.36 ab 17.20±0.82 bc 19.55±1.35 cd 21.61±2.09 cd 33.8±1.9 e 34.55±1.5 e 22.47±2.3d 

RE 7.07±1.17 c 10.8±1.78 d 7.71±1.44 c 6.24±0.6b 5.77±1.43b  3.54±1.17a 8.94±2.3 f 4.94±1.28b 13.69±3.8 e 17.64±3.9 f 10.94±2.5 d 5.21±1.3 b 

WB 10.8±3.97 be 10±2.91 be 6.12±2.54 a 5.73±2.44 a 11.6±3.71 cd 12.7±4.57 cd 21.05±5.41f 13.8±4.67 d 18.65±5.86e 25.19±5.91g 27.34±5.42g 15.6±3.7d 

 

 
Total lipid contents in mg/g dry weight tissue 

 J(08) J(08) A(08) S(08) O(08) N(08) D(08) J(09) F(09) M(09) A(09) M(09) 

FT 14.7±0.93 16.4±1.67 16.8±1.80  19±0.93  17.2±2.03  18.9±1.15  20.89±1.95 21.4±1.14  20.13±2.08  21.12±1.13  22.62±1.9  20.2±2.7  

GV 50.4±17.8 e 45.2±12.6 d 25.17±8.78 a 28.9±8.58 a 43.7±5.25 cd 43.8±5.15 cd 40.58±5.64 c 43.9±16.5 cd 34.47±12.02 b 57.07±11.42f 72.46±14.64 h 64±7.8 g 

MT 36.6±7.8 b 32.1±4.57 acd 30.84±8.5 ac 35.1±6.42 bd 30.9±3.44 a 35.5±8.63 bd 35.56±9.87 bd 36.1±6.13 bd 28.27±8.89 a 35.35±3.3b 41.25±3.25 e 283.23 a 

AM 13.8±2.4ab 14.6±4.97 b 9.82±2.02 a 24.1±7.82 c 25.4±3.51 c 30.8±4.68d 32.86±8.16e 28±3.43 cde 26.06±5.64 c 16.51±3.63 b 15.25±5.52b 13.6±2.3 ab 

RE 55.5±4.38 f 44.9±4.94 d 31.64±3.47cb 34.3±3.63 cb 24.2±3.09 b 55.6±3.94 f 58.33±3.57 f 24.3±2.6 b 28.24±3.352 b 39.73±4.48 d 25.22±3.7 b 20.3±3.3a 

WB 37.8±8.2 c 33±7.61 c 24.32±6.12 a 29.3±6.93 b 30.9±4.56 b 40.1±6.44 d 41.09±7.2 d 28.8±6.99 b 28.07±7.55 b 34.92±7.2 c 33.67±6.86 c 27.7±5.4 b 

Results are given as mean ± SD. n=8 replicates each month.  FT: foot. GV: gonad-visceral mass. MT: mantle. AM: adductor muscle. RE: rest. WB: whole body. Different letters indicate 

significant monthly difference for each organ (HSD Tukey’s tests. p < 0.05).



 

 

Chetoui et al., 2020                                                                                                               Annual dynamic of the biochemical compositions on M. stultorum 

 

 

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TL in the gonad-visceral mass reached a maximum 

value during April (72.45 ± 5.73 mg/g DW). In mantle, TL 

content presented low values in October (30.86 ± 3.44 mg/g 

DW) and February (28.27± 8.89mg/g DW). For adductor 

muscle, the content of lipids seems to be low from Jun to 

August and from March to May (below 20mg/g DW). 

However, the high values were observed in autumn and 

winter in order of 25 and 32 mg/g DM, respectively. In the 

rest part the TL contents fluctuated between 20.3 mg/g DW 

and 58 mg/g DW throughout the study year. One-way 

ANOVA analysis (HSD Tukey’s tests, F=18.11, p = 0) 

indicated that the TL contents in GV, AM, MT and RE 

showed significant monthly variations. Seasonal variations 

in the content of proteins, total lipids and glycogen of the M. 

stultorum whole body are shown in (Table 2) expressed as 

mg per g of dry weight. Protein content was the major 

biochemical compound and underwent significant variations 

during the experimental period (HSD Tukey’s tests, F 

=146.42, p = 0). It was in minimum value (84.2±6.7 mg/g 

DW) in October and reached a maximum (145.9±2.98mg/g 

DW) in April. The total lipid contents, which are the second 

major biochemical constituents in the whole body, it were 

comprised between 24 and 37 mg/g DW during the 

experimental period. Glycogen content varied in a similar 

way to that observed in GV. It was in a lowest value during 

August and September and increased gradually during 

winter and spring to reach a maximum in April. This 

compound has demonstrated significant changes among 

month (HSD Tukey’s tests, F =270.20, p = 0).    

Condition index (CI) and gonado-somatic (GSI) index  

The CI and GSI indexes showed a synchronous 

evolution.  Lowest values of CI (4.43 ± 1.24%) and of GSI 

(1.26±0.32%) were recorded in August (08). However, high 

percent of CI and GSI were observed in April with values of 

(14.41± 2.09%) and (3.97±0.52%) respectively. These 

indexes have shown significant differences among months 

(ANOVA, (p< 0.05) (Figure 3). 

 

 
Figure 3: Seasonal variation of the condition index (CI) and 

gonado-somatic index (GSI) of Mactra stultorum   

throughout the study period.Results are given as mean ± SD, 

n=30 replicates each month. Different letters indicate 

significant monthly difference for each index (HSD Tukey’s 

tests, p < 0.05). 

Percentage edibility (PE) 

During the reproductive cycle, the percentage of 

edibility showed a significant fluctuation from 25%-

60%, with a sharp enhancement in the percentage 

edibility during April (59.64±1.93%). During the 

summer, autumn and winter, it decreased considerably, 

with the lowest of the edibility percent (25.34±0.71%) 

being noted in August (Figure 3). The percentage 

edibility has shown significant differences among months 

(ANOVA, (p< 0.05) (Figure 4).  

 

 
Figure 4: Seasonal variation of percentage edibility (%) in 

Mactra stultorum throughout the study period. Results are 

given as mean ± SD, n=30 replicates each month. Different 

letters indicate significant monthly difference for PE (HSD 

Tukey’s tests, p < 0.05). 

 

Statistical analyses  

The interaction between biochemical compositions in 

each separate tissue and in the whole body of M. stultorum 

(1); environmental parameters (water temperature, salinity 

and chlorophyll a) (2); reproductive indices of M. stultorum 

(CI and GSI) (3), percentage edibility (4) and seasons 

(5) was tested using Principal components analysis (PCA) 

and a Pearson correlation (Figure 5 and Table 3). 

Results of PCA allowed us to retain the first two 

factorial axes that explain 57.32% of the total variance. 

Factor 1 displayed 41.30% of the total variance, defined by  

CI; GSI;  PE and different biochemical’s compounds in each 

organ and whole body except the LIPWB; LIPMA; LIPRE; 

PROMT; PROFT, which characterized factor 2 (14.5%). In 

addition, the environmental parameters (T °C, S, and Chlo 

a) described the factor 2 (Figure 5A). Analyze of 

biochemical’s composition reveled significant seasonal 

fluctuations marked by two phases the first one is the 

storage phase and the second is the depletion of reserves. 

During late winter and spring, glycogen was accumulated in 

high quantities in all tissues and whole body, which was 

positively and highly correlated with CI and GSI (Table 3). 

 

 



 

 

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Figure 5. Principal analysis component (PCA) represented by two factors F1 and F2 and produced by the biochemical 

parameters and reproductive indices of Mactra stultorum and the environmental condition. Projection of the variables on the 

factor-plane (1-2) (A) and projection of the cases on the factor-plane (1-2) (B) PRO: protein, GLY: glycogen, LIP: total lipid, 

FT : foot , GV: gonad-visceral mass, MT: mantle, AM : adductor muscle, RE: rest, BW: whole body, CI:  condition index, 

GSI: gonado-somatic index, T°C: water  temperature, Chlo a: chlorophyll a, S: salinity. 

 

This reserve seems to be lower during summer when 

the temperature is higher which presented a negative 

correlation with GLYGV and GLYFT. The total lipid in 

GV, MT, FT increased significantly especially during spring 

when the CI, GSI and PE are higher (positive correlation 

with LIPGV). While the AM deplete their lipid reserves 

during this same period and when the water temperature 

increased (negative correlation).In other hand the position of 

LIPWB in the middle of the two factors of PCA can be 

explained by the insignificant correlation with all parameters 

except with LIPRE. The major biochemical compound in all 

tissues, proteins significantly fluctuated with seasons and 

varied with tissues.   

Additionally, the protein in the gonad-visceral mass 

was negatively correlated with chlorophyll a, especially 

during autumn and winter when CI and Chlo a   values were 

lower (p <0.05). PE showed a positive and high correlation 

with the accumulation of protein and carbohydrate 

(glycogen) in the tissue of M. stultorum and with CI and GSI 

when increased. Only the accumulation of lipid in GV is 

positively correlated with PE index of physiological 

fitness. The salinity did not correlate with the biochemical 

compound of M. stultorum. A synergy affirmed by a positive 

correlation was observed between seasonal evolutions of 

glycogen contents of body parts and those of total lipid 

levels in foot and gonad-visceral mass of M. stultorum. 

Nevertheless, the changes in protein contents of M. 

stultorum did not demonstrate a significant correlation with 

the biochemical compounds (lipid and glycogen) except for 

PRORE. The projection of individuals (each sample from 

each month) on the same factorial plan (1:2) showed that the 

different cases could be clustered into three groups. It has 

been demonstrated that are an interactions between groups 1 

and 2, which each individuals accumulated high levels of 

biochemical’s compounds in each tissue during winter and 

spring corresponding to gametogenetic and maturity stages 

and they are characterized by a high level of PE. The third 

group represents the animals how depleted their reserve 

when environmental parameters such as sea water 

temperature and chlorophyll a increased signaling to 

spawning period (Figure 5B). 

Discussion 

This study provides new data about the seasonal 

evolution of the biochemical composition on the surf clam 

M. stultorum from Tunisian coasts. Previous studies on 

marine invertebrates such as bivalves showed that the 

changes in their biochemical composition are mostly 

affected by endogenous factors (the reproductive cycle) and 

exogenous factors (environmental conditions) [1, 26]. 

Glycogen is considered as the major energy reserve in 

bivalves. It may be used concurrently as an energy source 

for growth and also stored in specific cells as an energetic 

reserve during gametogenesis process when the energy 

demands are high [27, 28]. In our study, the glycogen 

content in all tissues and the whole body of M. stultorum 

was lower during summer corresponding with the spawning 

phase. This compound increased gradually during winter 

and during spring and reached a maximum in April 

coinciding with the maturation of gonads. However, in May, 

they decreased considerably when 40% of the populations 

are partially spawned.  The seasonal variation of glycogen 

seems to be related to the reproductive cycle of M. 

stultorum, as mentioned previously by Chetoui et al. [19], 

which was also confirmed by a positive correlation with CI 

and GSI physiological indices. 



 

 

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Table 3: Correlation matrix of the biochemical parameters and reproductive indices of Mactra stultorum and the environmental condition. 

 PROFT PROGV PROMT PROAM PRORE GLYFT GLYGV GLYMT GLYAM GLYRE LIPFT LIPGV LIPMT LIPAM LIPRE PROWB GLYWB LIPWB CI GSI PE T (°C) Chlo a 

PROGV ns                       

PROMT ns ns                      

PROAM ns ns ns                     

PRORE ns ns 0,85 ns                    

GLYFT ns ns ns ns ns                   

GLYGV ns ns ns ns ns 0,85                  

GLYMT ns ns ns ns 0,66 0,86 0,82                 

GLYAM ns ns ns ns ns 0,87 0,88 0,88                

GLYRE ns ns ns ns 0,63 0,59 ns ns ns               

LIPFT ns ns ns ns ns 0,78 0,73 0,69 0,76 ns              

LIPGV ns ns ns ns ns 0,61 0,62 0,80 0,77 ns ns             

LIPMT ns ns ns ns ns ns ns ns ns ns ns ns            

LIPAM ns ns ns ns ns ns ns ns ns ns ns ns ns           

LIPRE ns ns ns ns ns ns ns ns ns ns ns ns ns ns          

PROWB 0,60 0,81 ns ns 0,81 ns ns ns ns ns ns ns ns ns -0,09         

GLYWB ns ns ns ns ns 0,94 0,93 0,93 0,93 0,65 0,75 0,68 ns ns -0,06 ns        

LIPWB ns ns ns ns ns ns ns ns ns ns ns ns ns ns 0,83 ns ns       

CI ns ns ns ns ns 0,82 0,74 0,80 0,91 ns 0,70 0,82 ns ns -0,41 ns 0,79 ns      

GSI ns ns ns ns ns 0,71 0,66 0,77 0,87 ns ns 0,88 ns ns -0,35 ns 0,72 ns 0,97     

PE ns ns 0,71 ns 0,61 0,76 0,77 0,80 0,83 ns ns 0,73 ns ns ns ns 0,83 0.75 0,84 0,85    

T (°C) ns ns ns ns ns -0,69 -0,61 ns ns ns -0,81 ns ns -0,72 0,04 ns ns ns ns ns ns   

Chlo a ns ns ns ns ns ns ns ns ns ns ns ns ns ns -0,48 ns ns ns ns ns ns ns  

S ns ns ns ns ns ns ns ns ns ns ns ns ns ns 0,20 ns ns ns ns ns ns 0,60 ns 

Correlation coefficients statistically significant (p <0.05); ns: not significant (p <0.05); the positive correlation is presented with yellow color and the negative one is presented with red 

color. PRO: protein, GLY: glycogen, LIP: total lipid, FT : foot , GV: gonad-visceral mass, MT: mantle, AM : adductor muscle, RE: rest, BW: whole body, CI:  condition index, GSI: 

gonado-somatic index, T°C: water  temperature, Chlo a: chlorophyll a, S: salinity.



 

 

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We suggested that the accumulation of glycogen at the 

end of the cycle (autumn) serves as energy for the start of a 

new reproductive cycle in winter and support the essential 

metabolic maintenance during this season food scarcity. 

Likewise, during gametogenesis development (in winter) 

and the maturation phase (in spring), the storage of glycogen 

can be used as precursors for lipid synthesis needed for the 

formation of gametes for mollusks [6] and as an immediate 

available energy source during spawning period [29, 30].  

Similar results were recorded for M. veneriformis [31]. 

However, some authors demonstrated that glycogen levels in 

M. chinensis and R. decussatus decreased considerably 

during the sexual maturity process [11, 32]. 

The biochemical composition of bivalve seems to be 

affected by many environmental parameters such as 

temperature, salinity and food accessibility [33]. A negative 

correlation between glycogen content in M. stultorum and 

the water temperature can be related to the direct or indirect 

effects of the energy reserves fluctuations (storage and 

exploitation) [34]. However, the accumulation of glycogen 

in gonad-visceral mass of M. stultorum, especially during 

March and April, could be explained by its positive 

correlation with food availability expressed by the peak of 

the chlorophyll a [31].  For that reason, the glycogen content 

represents a good characteristic of nutritional conditions 

[35]. 

Our results showed that protein was the major 

compound in all organs and whole body of M. stultorum. In 

the gonad-visceral mass of M. stultorum, the content of 

protein was higher during ripening (March and April) and 

during spawning (July and August). By contrast, this 

compound in other organs (FT, AM and MT) decreased 

during the same periods. From another point, the whole 

body seems to accumulate this organic constituent during 

the same periods. It should be noted that probably M. 

stultorum used protein in the mantle and foot as a source of 

energy during the ripening phase and partially the spawned 

and those of adductor muscles during spawning phase. 

Furthermore, the glycogen quantity of these muscular organs 

decreased considerably when gametes are released. Our 

result can be interpreted by the main role of protein to serve 

as an energy reserve in adult bivalves in periods of reduced 

glycogen levels [9, 10] and particularly to support the end of 

gametogenesis [3, 30]. The negative correlation between 

chlorophyll a and protein level in gonad-visceral mass of M. 

stultorum during autumn and winter suggested that the 

deficiency of food availability (low levels of chlorophyll a) 

has reduced the protein levels [9]. Unuma et al. [32] and Qi 

et al. [36] have suggested  that the lower level of protein 

during the same period was interpreted by its role as a 

nutrient source for the proliferation and differentiation of 

cell germ in the gametogenesis process (in particularly 

during spermatogenesis of M. chinensis and 

Pseudocentrotus depressus). 

The total lipid in M. stultorum gonad-visceral mass 

was higher than in the other organs, suggesting that GV is 

the major lipid storage site [31, 32]. Based on the 

reproductive cycle of M. stultorum, the lipid content of the 

gonad-visceral mass presented a positive correlation with CI 

and GSI. They begin to accumulate progressively during the 

earlier and late developmental stages, reached a high level 

when the gametes mature during the ripening stage (March 

and April) and finally decreased considerably when the 

spawning occurred from May to August. It is necessary to 

mention that the total lipid accumulated in GV has been 

considered as good indicators of oocyte value and larva 

viability (1).  In this context, it may be admitted as a good 

index of gonad maturity [34]. Our results are in concordance 

with those found for M. chinensis, Ruditapes philippinarum 

and Scapharca broughtonii [27, 32].  

Although mantle and adductor muscles were not really 

considered as lipid organs storage. In the present study, the 

lipid reserves stocked in mantle decreased during spawning 

stage. Nevertheless, those of adductor muscle declined 

dramatically during the ripening and spawning periods.  

These decreases indicate that the conversion of lipids 

accumulated in these tissues could be used to provide the 

necessary energy for the gametogenesis process of M. 

stultorum. However, the total lipid of foot did not show any 

changes throughout the year which was affirmed by a 

positive correlation with CI and a negative correlation with 

water temperature. It can be suggested that the lipid located 

in this tissue did not contribute to the energy conversion 

utilization process of M. stultorum. Comparable results have 

been observed in M. veneriformis during sexual maturity 

and spawning periods [31]. However, dissimilar results were 

also described by Qiaozhen and Qi, [32] and Qi et al. [31]. 

With regards to the annual changes in total lipid of whole 

body, it showed significant alterations with seasons. 

Bayne, [37] has described two reproductive patterns of 

marine bivalves based on the relationship between energy 

storage and gonad development cycles.  In a conservative 

pattern, gametogenesis used the energy stored in various 

organs in forms of lipids and glycogen. However, in an 

opportunistic pattern, gametogenesis occurs using the energy 

supplied by the nutrients when the food in water is abundant. 

Therefore, we can suggest that M. stultorum adopts an 

intermediate pattern closer to M. veneriformis [31]. They 

used at the beginning of their reproductive cycle during the 

winter the energy reserves stored previously. Nevertheless, 

during the spring season, they exploited at the same time the 

energy stored and energy provided by food availability. 

Several studies have demonstrated that PE and CI are the 

main tools for the commercialization of bivalves, which 

varied seasonally and geographically, depending 

generally on exogenous and endogenous conditions 

such as food accessibility and the gametogenic cycle, 

respectively [11, 38]. 



 

 

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The percentage edibility showed significant 

differences among seasons. It seems to be higher during 

early summer (08) and during spring (09) which 

corresponds to the beginning of the gametogenetic 

cycle. In this period the animals accumulate biochemical’s 

constituents for their gamete development when food in 

water is available and/ or abundant. Therefore, this index of 

physiological fitness was positively correlated firstly with 

accumulation of protein and carbohydrate (glycogen) in all 

tissues of M. stultorum; secondly with the CI and GSI 

indexes and thistly with lipid contents in GV. While, during 

late summer, autumn and early winter, it decreased 

considerably, with the lowest value recorded in 

August. Some decline in PE coincided with spawning 

and inactive periods. M. stultorum during the last 

periods has depleted their reserve during the spawning 

process. Our results are in agreement with those in 

clams R. decussatus and Paphia malabarica [25, 39]. 

Moreover, CI is considered as a good tool widely 

used to measure the physiological state and to identify 

the spawning seasons of bivalves [13]. This indirect 

method of analysis [40] is necessarily confirmed by 

histological sectioning and microscopic evaluation of 

the gonads [41].  Our data of seasonal variation of CI in 

M. stultorum during the period (Jun 2008 to May 2009) 

was studied and confirmed by the determination of 

different stages of the gametogenic cycle of M. 

stultorum [19]. According to Chetoui et al. [19], CI 

increased from winter to spring. These seasons 

represent the start of gametogenic development and ripe 

periods for both sexes [19]. However, the decrease of 

CI coincides with spawning and inactive stages [19]. CI 

was positively correlated with other reproductive index 

as gonad-somatic index which was specific for the 

assessment of physiological state of gonad. 

In the Mediterranean Sea, mainly in Tunisia, bivalves 

are considered as a rich food source and a healthy 

proportionate diet [3, 42]. Since, they are known for their 

nutritious and essential energy reserves (e.g., protein, 

vitamins and minerals). In addition, bivalves are the best 

source of polyunsaturated fatty acids n-3 family 

(PUFA (n-3)) mainly the two essentials fatty acids 

EPA and DHA which play crucial roles in human nutri-

tion and health [43].These elements present a dissimilar 

organization and concentration depending on the 

bivalve tissues that can be commonly associated with 

external climate fluctuations. The variation of the 

nutritional value could be assessed using percentage 

of edibility and the condition index; however, 

information about them is crucial for the cultivation 

and harvesting strategy of bivalves [44]. In other 

hand, not only the biochemical compounds, PE and CI 

have influences on the flesh quality during cultivation 

and harvesting process. The supplement information’s 

about the feeding strategy and the quality of the food 

in aquaculture are crucial for to keep the good 

nutritional value of the animals flesh as well for human 

consumption as for manufacturing animal foodstuff. 

Consequently, all these data allow adopting a good 

management of the breeding cost of bivalves. 

Conclusion 

In conclusion, this study reported, at the first time, the 

assessment of the biochemical composition in several organs 

and the whole body of M. stultorum in relation to the 

environmental conditions and the reproductive cycle. A 

decrease of glycogen levels in all tissues during the 

spawning periods (from May to August) suggesting it 

important role as energy in the gametogenesis process. Lipid 

and protein varied significantly and played an important role 

as fuel for gametogenesis when stored glycogen was 

exhausted and to support the basic metabolic maintenance 

cost in periods of food insufficiency. Additionally, the 

best nutritive season for M. stultorum was noted during 

the beginning of gametogenic cycle and ripe periods 

(from February to Jun) associated with the highest 

contents of the biochemical composition, percentage 

of edibility and condition index and when the food 

availability was abundant. However, from July to 

January, it is not advisable to consume it due to its 

lowest nutritional value represented by low levels of the 

organic constituents and the percentage edibility.  

Based on these results, we suggest that the 

harvesting of M. stultorum should be concentrated on 

the period when the seafood is at its highest nutritive 

value. The percentage of edibility and the condition 

index are very important tools in physiological studies 

providing valuable information required for assessing larvae 

development and promoting successful restocking actions in 

aquaculture management. Further studies of other 

aquaculture parameters such as food quality and 

pathological tests seem to be necessary in order to avoid 

disease and increase the larva growth and bivalve’s quality. 

Acknowledgments     

This study was supported by the Tunis University of 

Sciences and the research laboratory.   

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