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Using of chitosan nanoparticles (CsNPs), Spirulina as a feed additives under intensive culture system for black tiger shrimp (Penaeus monodon)
⁎Corresponding author at: Department of Zoology, College of Science, King Saud University, 2455, Riyadh 11541, Saudi Arabia. awarith@ksu.edu.sa (Abdel-Wahab A. Abdel-Warith)
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Received: ,
Accepted: ,
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.
Peer review under responsibility of King Saud University.
Abstract
Study conducted to evaluate the impact of dietary incorporation of chitosan nanoparticles (CsNPs) bio-synthesis and Spirulina platensis on the growth performance and body composition of intensive cultured fingerling of black tiger shrimp (Penaeus monodon) in addition to the effect of the diets on heavy metals concentrations in water of culture cages. Six diets were prepared to contain approximately 44% crude protein and 499 k cal./100 g diet and supplemented by S. platensis and chitosan as follow: T1: control, T2: 0.05% S. platensis, T3: 0.1% S. platensis, T4: 1 ml chitosan, T5: 1 ml chitosan and 0.05% S. platensis and T6: 1 ml chitosan and 0.1% S. platensis. Shrimp fingerlings (1.24 ± 0.01 g) were randomly distributed in 12 hapas at stocking density of 20 fingerlings for each. The hapas were divided into 6 replicate groups and placed in cages. Each group received a kind of the experimental diet twice daily at feeding rate of 5% shrimp biomass for 12 weeks. The results indicated that, the growth parameters; final body weight (FBW g), weight gain (WG g), specific growth rate (SGR%) and survival rate (SR%) were improved significantly all trials compared to the control group. The best values for these parameters were recorded in the group of T5 and T6 without significant differences between them. Shrimp body composition showed the highest protein and fat contents for the group of T5 and T6 with significant differences (P < 0.05) among all treatments. No significant differences were noted for the heavy metals concentrations between all treatments. In conclusion, the incorporation of chitosan nanoparticles (CsNPs) and S. platensis attained considerable improvement in growth performance of black tiger shrimp and further investigations are recommended to optimize the level of incorporation in the diets for shrimp species.
Keywords
S. platensis
Chitosan nanoparticles
Growth performance
Chemical composition P. monodon
1 Introduction
Although there are over than 3,000 shrimp species worldwide, only 40 groups are commercially exploited (Whetsone et al., 2002). Shrimp farming is based on a sub-species, mainly selected from the Penaeidae family for their good reproductive and growth potential. The P. monodon is the second most cultured shrimp species in the world following the white leg shrimp (Litopenaeus vannamei) (FAO, 2010). The P. monodon species is naturally distributed in the Indo-Pacific region including the eastern coast of Africa, the Arabian Peninsula, south-east Asia, the Sea of Japan, and northern Australia (Holthuis, 1980).
Microalgae consist of high protein and essential amino acid when compared with other reference food proteins (Becker, 2007). For example Spirulina platensis has highly protein content (60–70%), and it has been receiving concern as an animal food source and it has also contain a good source of vitamins, minerals, essential fatty acids and antioxidant pigments such as carotenoids. Investigations have been conducted to use Spirulina as a diets supplementation for fish and crustaceans (Jaime-Ceballos et al., 2007; Silva-Neto et al., 2012) and also as a partial substitution for fishmeal in tilapia (Abdel-Warith and Elsayed, 2019), carp and sturgeon (Nandeesha et al., 2001; Palmegiano et al., 2008). In addition, Many researchers (Richmond, 2004; Abdel-Warith and Elsayed, 2019) have investigated the microalgae utilization in aquaculture diets. Zooplankters that are commonly used include rotifers (Brachionus sp.), copepods (Tigriopus sp.), cladocerans (Daphnia sp., Moina sp.), and brine shrimp (Artemia sp.) (De Pauw and Persoone, 1992). Therefore, diets containing algae may be influenced on growth and the rate of survival (Cohen et al., 1993).
Nanotechnologies have wide range applications in the fishery industry, such as water treatment, sterilization, nano-feed for feeding the fish, and controlling of aquatic diseases. It is thought that nanoparticles of some elements like selenium and iron supplemented in diet could enhance growth of fish and crustacean (Can et al., 2011). Therefore, nanotechnologies can be practically use to create fish ponds that are safe from disease and pollution in addition to providing for the fast growth of fish and Crustaceans including crab, lobster, shrimp, or barnacle (Can et al., 2011). This study aimed to evaluate the effect of chitosan nanoparticles (CsNPs) biosynthesis and S. platensis in diets on growth performance and chemical composition of intensive cultured fingerlings black tiger shrimp, Penaeus monodon in addition its effect on heavy metals concentration in the aquariums
2 Materials and methods
2.1 Experimental design
Fingerling of Penaeus monodon were obtained from a private farm in Burullus, and then transported to the cages in plastic bags filled with water and oxygen. Twelve hapas (1 × 2.5 × 1 m3) were placed in cages and divided into six replicate groups (T1 to T6). Twenty fingerlings (1.24 ± 0.01 g) of the black tiger shrimp P. monodon were stocked in each hapa (15 fingerlings/m3). The shrimp fingerlings were fed on sinking pellets diet (2 mm) at feeding rate of 5% of total biomass twice daily for six days per week. Every two weeks, shrimp fingerlings of all groups were weighed and the amount of feed was adjusted according to the changes in body weight throughout the experimental period. The experiments lasted for 12 weeks and at the end of the experimental period five of the P. monodon from each hapa were collected. The chemical composition of their whole body was assessed using the methods described by AOAC (2016).
2.2 Diet formulation
The Spirulina platensis meal was collected from the algae unit at the National Research Center chitosan (CS) and sodium tri polyphosphate (STPP) was used as a crosslinking agent both were purchased from Sigma-Aldrich (St. Louis, MO, USA). Chitosan was used as a carrier and STPP was used as a crosslinking agent. Chitosan nanoparticles (CsNPs) were prepared by using the ionic gelation method according to Masarudin et al. (2015). Six diets were prepared (Table 1) to provide 44% protein and 499 kcal/100 g diet and supplemented by S. platensis and chitosan as follows: Each 40 g contains
Feed ingredients
Experimental diets
T1 (Control)
T2
T3
T4
T5
T6
Fish meal (C.P.70%)
48.5
48.5
48.5
48.5
48.5
48.5
Soybean meal (C.P.44%)
20
20
20
20
20
20
Yellow corn meal (C. P. 7%)
10
9.95
9.9
9.9
9.85
9.8
Rice bran (C.P. 14%)
11.5
11.5
11.5
11.5
11.5
11.5
Fish oil
6
6
6
6
6
6
Chitosan (g/kg)
0
0
0
0.1
0.1
0.1
S. platensis (g/kg)
0
0.05
0.1
0
0.05
0.1
Vit*& Min premix**
4
4
4
4
4
4
Total
100
100
100
100
100
100
Proximate analysis (dry matter basis)
Dry matter
92.16
91.98
93.07
92.55
91.62
91.619
Crude protein
43.79
43.65
43.91
43.22
43.19
43.57
Ether extract (EE)
13.29
13.77
13.91
13.43
13.39
13.58
Ash
10.88
10.79
10.91
10.77
10.82
10.74
Metabolizable energy (Kcal)/100 g
499.2
491.9
492.4
489.9
490.7
494.7
T1: control, T2: 0.05% S. platensis, T3: 0.1% S. platensis, T4: 1 ml chitosan nanoparticles.
T5: 1 ml chitosan nanoparticles and 0.05% S. platensis, T6: 1 ml chitosan nanoparticles and 0.1% S. platensis.
Dietary ingredients were mixed in a food mixer (Legacy, USA) with water (at around 50 °C) to produce a 2 mm pellet. The moist pellets were then oven dried at 105 °C and stored frozen at −20 °C until use. The diets were analyzed for determining their chemical composition (Table 1) according to the methods as described by AOAC (2016).
2.3 Assessment of water quality:
Water temperature was adjusted at the range and checked daily at 9 am. Dissolved oxygen (DO) was checked at 7 am by YSI model (YSI CO., Yellow Springs, Ohio, USA). Total ammonia, nitrate, and nitrite were assessed using a DREL, 2000 spectrophotometer (Hash CO., USA). pH values were estimated daily by Orion pH meter (Texas, USA). Generally, all measures of water quality (temperature, pH value, DO, etc.) were in suitable range for black tiger shrimp (Boyd, 1990).
2.4 Assessment of heavy metals in water of culture hapas
Water samples were collected weekly from various places in each treatment by a PVC tube column sampler at a half meter depth from the water surface. The samples of each treatment were mixed in a plastic bucket and then 1 L was kept in a polyethylene bottle, which was refrigerated and transported to the laboratory for determine the heavy metals concentrations (Fe, Cu, Pb, and Mn) ppm Metals were extracted with concentrated HCl and preserved in a refrigerator until subjected to analysis. The concentrations of the heavy metals as µg/l were assessed using Atomic Absorption Spectrophotometer with air-acetylene mixture as fuel (APHA. 1998).
2.5 Statistical analysis
Results were statistically analyzed by applying the computer program (SAS) ANOVA procedure Statistical Analysis System (SAS, 1996) and Dunncan’s (1955). Multiple Range Test were utilized to look at variations between means. Impacts of treatment were viewed as huge at P < 0.05.
3 Results and discussion
The average values of initial body weight (IBW), final body weight (FBW), weight gain, specific growth rate (SGR%) and survival rate (SR%) (mean ± SE) of P. monodon are presented in Table 2. The results indicated no significant differences in the IBW while, significant differences (P < 0.05) were noted in the FBW of shrimp fed various experimental diets (T2–T6) except the average of FBW recorded in T5 and T6. The highest value of FBW (18.49 ± 0.2 g) was observed in shrimp fed on T6 (1 ml chitosan and 0.1% S. platensis) and the lowest FBW (12.62 ± 0.17 g) was shown in shrimp fed the control diet. Values in the same column with the same superscript are not significantly different (P > 0.05).
Treatments
IBW1
FBW2
WG3
SGR%4/day
SR%5
T1
1.24 ± 0.002a
12.62 ± 0.17e
11.37 ± 0.0018e
2.76 ± 0.017e
57.32 ± 1.06c
T2
1.25 ± 0.0034a
15.28 ± 0.1d
14.03 ± 0.001d
2.98 ± 0.01d
68.07 ± 1.73b
T3
1.25 ± 0.01a
15.97 ± 0.14c
14.72 ± 0.002c
3.03 ± 0.014c
68.17 ± 1.73a
T4
1.24 ± 0.004a
17.83 ± 0.23b
16.58 ± 0.002b
3.17 ± 0.014b
71.01 ± 2.082a
T5
1.24 ± 0.004a
18.48 ± 0.2a
17.24 ± 0.002a
3.21 ± 0.012a
74.19 ± 1.52a
T6
1.25 ± 0.004a
18.49 ± 0.2a
17.25 ± 0.002a
3.21 ± 0.011a
73.22 ± 3.51a
Data of the present study are in agreement with results obtained by Abdulrahman and Ameen (2014) who showed that, combined dried S. platensis had a potential impact on growth at an optimum level of 5 g/kg for white shrimp (Litopenaeus vannamei). The mean value of the group receiving 5.0 g/kg was highly significant difference for all the assessed parameters which indicating that the suitable amount in diet of chitosan nanoparticles using S. platensis for green tiger shrimp is 5.0 g/kg during the study period. Ibrahem et al. (2013) reported that feed additives with chitosan particles for chlorella enhanced the weight, length, and growth for striped jack, Pseudocaranx dentex, and Oreochromis niloticus. On the other hand, Badawy et al. (2008) investigated the algae mixture (S. platensis and chitosan nanoparticles) as supplemental feeds, results observed that growth performance of O. niloticus (FBW, BWG, DWG, RWG, and SGR) increased significantly (P < 0.05) when increased with one or both of S. platensis and chitosan. Moreover, these data were in accordance with the finding by Abdel-Warith and Elsayed (2019) who found that the possibility of adding A. platensis as a protein source fed to O. niloticus improves the overall feed utilization, growth performance, survival rate and body composition.
The highest value of WG (17.25 ± 0.002 g) was found in shrimp fed on diet T6 while the lowest WG (11.37 ± 0.0018 g) were shown by shrimp of the control group (Table 2). The analysis of variance for the averages weight gain was highly significant (P < 0.05) among all trails except the mean WG in trials T5 and T6. Ghaeni et al. (2011) stated that green tiger shrimp (Penaeus semisulcatus) fed diets containing S. platensis powder showed highly significant (P < 0.05) growth and weight gain when compared to shrimp were fed the control diet. Similar to our results, Carnevali et al. (2006) found that weight gain for black tiger shrimp was significantly higher for the treated groups compared to the control group when S. platensis were treated by chitosan nanoparticles and used for 70 days. Al-Dohail et al. (2009) also indicated that African catfish Clarias gariepinus fed the combination of S. platensis with chitosan showed better growth performance compared to the control fish group. Similarly, application of chitosan nanoparticles and S. platensis was found to improve the growth performance of O. niloticus (Wang et al., 2008) and Silurus glanis (Bogut et al., 2000).
The effect of chitosan nanoparticles biosynthesis and S. platensis on SGR is recoded in Table 2. T5 (1 ml chitosan and 0.05% S. platensis) and T6 (1 ml chitosan and 0.1% S. platensis) showed the highest SGR values (3.21 ± 0.011%/day for both), while shrimp fed on T1 (control) showed the lowest SGR values (2.76 ± 0.017%/day) and the differences between the means were significant (P < 0.05). These might be related to the chitosan nanoparticles and S. platensis which might be enhance the digestive enzymes such as protease, amylase, and lipase, which has the potential to increase the value of digestive enzymes in the gut and/or its effect for also improving digestive activity by synthesis of vitamins and co-factors or enzymatic improvement for WG and SGR (Gatesoupe, 1999). Also, Bauer et al. (2012) indicated that L. vannamei which fed on diet supplementation by microbial floc showed highly significant differences of all growth parameters including WG, SGR, survival rate and feed utilization when compared to the control group. In addition, Abdel-Warith and Elsayed (2019) found that diets containing Arthrospira platensis enhanced the biochemical and hematological parameters and these might be improve immune system and reflect on overall growth parameters.
Survival rate (SR) of P. monodon as affected by chitosan nanoparticles biosynthesis using S. platensis is presented in Table 2. Penaeus monodon of T5 (1 ml chitosan and 0.05% S. platensis) and T6 (1 ml chitosan and 0.1% S. platensis) recorded the highest SR values (74.19 ± 1.52 and 73.22 ± 3.51%) respectively, whereas, those of T1 (control) showed the lowest value being 57.32% as illustrated in Table 2 with significantly difference (P < 0.05) among treatment groups. These results are in accordance with Moe (2011) who noted that growth performance and the average of survival rate of Litopenaeus vannamei fed with 0.05% dietary S. platensis and chitosan was higher (100%) than the control group (80%). Jana et al. (2014) also found that Spirulina improves the survival rate of Pangus fish Pangasius sutchi it was found to be 94% and 80% survival rate, respectively, for the fodder impregnated with spirulina and chitosan at the end of the experiment.
Heavy metals were assessed in the water of black tiger shrimp (P. monodon) rearing in hapas placed in three different cages in the same area were recorded in Table 3. The total mean values of iron (Fe) concentrations in water were 0.413 ± 0.01, 0.43 ± 0.012, 0.42 ± 0.01, 0.403 ± 0.003, 0.413 ± 0.003, and 0.3 ± 0.12 ppm for the six different treatments, respectively. The mean values of copper) Cu) concentration ranged from 0.009 to 0.01. The average lead (Pb) concentration was 0.1 ppm for all treatments. The concentration of manganese (Mn) was 0.2 ppm for all trials. The statistical analysis showed that no significant differences (P > 0.05) in concentration of all estimated metals (Fe, Cu, Pb and Mn) among different treatments despite of the variations in the ratio of Chitosan nanoparticles and S. platensis added to the diets. Values in the same column with the same superscript are not significantly different (P > 0.05).
Treatments
Fe ppm
Cu ppm
Pb ppm
Mn ppm
T1
0.413 ± 0.01a
0.01 ± 0.0003 a
0.1 ± 0.003 a
0.2 ± 0.003 a
T2
0.43 ± 0.012 a
0.01 ± 0.001 a
0.1 ± 0.003 a
0.2 ± 0.01 a
T3
0.42 ± 0.01 a
0.01 ± 0.0003 a
0.1 ± 0.01 a
0.2 ± 0.010 a
T4
0.403 ± 0.003 a
0.009 ± 0.001 a
0.1 ± 0.003 a
0.2 ± 0.0145 a
T5
0.413 ± 0.003 a
0.010 ± 0.001 a
0.1 ± 0.01 a
0.2 ± 0.003 a
T6
0.3 ± 0.12 a
0.001 ± 0.0003 a
0.1 ± 0.003 a
0.2 ± 0.01 a
In this study, results indicate that there were significant differences (P < 0.05) in body composition of black tiger shrimp (P. monodon) among various treatments of biosynthesis of chitosan nanoparticles and S. platensis (Table 4). The moisture content was slightly lower for shrimp fed on T6 (70.9 ± 0.02%) when compared to shrimp fed on the control diet that had higher moisture content (74.44 ± 0.012%). The crude protein content was higher for T6 (40.70 ± 0.05%) while the lower protein content (38.27 ± 0.034%) was recorded with the control group. In the same way, crude lipid value was also differ among groups, representing the higher amount of lipid in T6 (12.10 ± 0.1%) compared to the other groups. The total ash content was higher (22.75 ± 0.198%) for the control group whereas low ash content (22.01 ± 0.17%) was recorded for T3 where the diet contained 0.1% S. platensis. Analysis of variance showed that body composition was significantly (P < 0.05) affected by chitosan nanoparticles biosynthesis using S. platensis diets for all incorporation ratios. Values in the same column with the same superscript are not significantly different (P > 0.05).
Treatments
Moisture
Protein
Lipid
Ash
T1
74.44 ± 0.012a
38.27 ± 0.034f
10.14 ± 0.08c
22.75 ± 0.198a
T2
71.38 ± 0.027d
39.20 ± 0.04e
11.42 ± 0.11b
22.22 ± 0.16b
T3
71.76 ± 0.02b
39.40 ± 0.034d
11.53 ± 0.058b
22.01 ± 0.17bc
T4
71.53 ± 0.012c
39.90 ± 0.02c
11.90 ± 0.19a
21.80 ± 0.2c
T5
71.11 ± 0.023e
40.34 ± 0.034b
12.01 ± 0.19a
21.40 ± 0.11d
T6
70.90 ± 0.02f
40.70 ± 0.05a
12.10 ± 0.1a
21.22 ± 0.13d
Sriraman (1998) reported that protein content was higher for the younger individuals compared to adults for Penaeus monodon. The high content of protein for younger individuals might be related to increase the protein structure during the active growth phase as it has been showed for Penaeus monodon (Moreno et al., 2015; Mehta and Nayak, 2017). Results of the current study are in accordance with data reported by Hoa (2009), Ambar et al. (2017), and Nesara and Anand (2018) for Penaeus monodon and Mahbub (2016) for major prawn and shrimp.
4 Conclusion
Based on results obtained, it can be concluded that microalgae might be a precious, cost effective means of CsNPs for P. monodon growth. It can also be concluded that feeding of P. monodon on diets containing 44% protein and supplemented with S. platensis and chitosan nanoparticles can lead to an increase in shrimp growth performance and improve the body composition of P. monodon especially the protein and lipid content thereby improving their production and nutritional value. In addition, results of the current study highlight the possibility of using S. platensis and chitosan nanoparticles in P. monodon enhanced feed utilization and survival rate. Therefore, the use of S. platensis and chitosan nanoparticles in crustacean diets can be included for the large-scale culture of crustacean, particularly for shrimp. The optimum inclusion levels of the S. platensis and chitosan nanoparticles in crustacean diets require further investigation to determine its desirable impact on growth, feed utilization, immune response, and infection resistance.
Acknowledgment
Authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through research group No. (RGP-VPP-304). In addition, the authors would like to thank the Researchers Support Services Unit for their technical support.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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