Advertisement

International Aquatic Research

, Volume 9, Issue 1, pp 11–24 | Cite as

Evaluation of dietary soybean meal as fish meal replacer for juvenile whiteleg shrimp, Litopenaeus vannamei reared in biofloc system

  • Hyeonho Yun
  • Erfan Shahkar
  • Ali Hamidoghli
  • Seunghan Lee
  • Seonghun Won
  • Sungchul C. Bai
Open Access
Original Research

Abstract

Different levels of dietary soybean meal (SBM) as a fish meal (FM) replacer, with and without amino acid supplementation, for whiteleg shrimp, Litopenaeus vannamei reared in the biofloc system was examined in eight weeks of feeding trial. Eight experimental diets consisted of a basal diet with 0% FM replacement by SBM provided in clear sea water without biofloc system (S0SW), four diets replacing FM at 0% (S0), 33% (S33), 67% (S67) and 100% (S100) by SBM, and three diets replacing FM at 33% (S33A), 67% (S67A) and 100% (S100A) by SBM supplemented with amino acids (methionine and lysine) in the seawater biofloc system. Results of water quality analyses showed significantly lower total suspended solids and nitrate for S0SW group than all other treatments. Diets S0 and S33A resulted in higher weight gain and specific growth rate among all groups, with no significant differences with S33 group. In addition, whole-body protein and amino acid compositions of shrimp fed S0SW were lower than most biofloc groups. Haemolymph parameters showed significant differences in total protein, cholesterol and triglyceride between groups S0 and S0SW. Also, superoxide dismutase activity showed a decreasing trend with increasing replacement level. In conclusion, based on these results, SBM could replace up to 33% of FM with or without amino acid supplementation in juvenile whiteleg shrimp diets reared in the biofloc system.

Keywords

Biofloc technology Fish meal Soybean meal Amino acid 

Introduction

The “biofloc technology” is a sustainable technique used in minimum or zero water exchange shrimp culture systems (Avnimelech 2008; Crab et al. 2009; De Schryver et al. 2008). In this system, heterotrophic microorganisms are employed to manage chemical quality of water by converting inorganic material to organic compounds such as conversion of ammonium into bacterial biomass (Avnimelech 2006; Crab et al. 2007). With the development of microbial community, biofloc (microbial flocs) is formed containing heterogeneous mixture of organisms and organic material (Hargreaves 2006; De Schryver et al. 2008). Biofloc that is promoted in the culture water can beneficially control the quantity of ammonium and nitrite. Moreover, it is available as a source of food supplement for cultured shrimp (Hari et al. 2004; Arnold et al. 2009; Ballester et al. 2010), and offer essential in situ nutrients, such as protein (Emerenciano et al. 2012), lipid (Wasielesky et al. 2006), amino acids (Ju et al. 2008) and fatty acids (Izquierdo et al. 2006; Ekasari et al. 2010). Biofloc biomass in the culture system that is consumed by cultured shrimp and digested, may compensate a significant amount of protein demand, and consequently reduce the quantity of fish meal (FM) required (Burford et al. 2004; Crab et al. 2010; Hari et al. 2004; Wasielesky et al. 2006; Xu and Pan 2012; Xu et al. 2012).

Fish meal (FM) has generally been a major ingredient in shrimp diets because of its high protein quality, desirable amino acid profile, excellent palatability and digestibility, low carbohydrate content and minimum anti-nutritional factors (Zhou et al. 2004). However, FM is also overpriced, comparing to other ingredients, in formulated shrimp diets (Lee and Bai 1997; FAO 2013). Recently, the price of fish meal has been increasing due to excessive demand and static supply (FAO 2014). It has been stated that the success and sustainability of the shrimp aquaculture industry will depend partly on the reduction of FM usage in shrimp feeds (Yue et al. 2012). For this reason, many studies have aimed to replace or reduce FM inclusion in diets by less expensive alternative protein sources, such as algae (Kiron et al. 2012), bacteria (Aas et al. 2006), plants (Gatlin et al. 2007), invertebrates (Barrows and Frost 2014) and by-products (Fowler 1991). Meanwhile, soybean meal (SBM) is known to be one of the most successful replacers of FM, because of its favorable protein content and amino acid profile (McGoogan and Gatlin 1997; Kikuchi 1999), less expensive price than FM and availability (Hardy 2006). However, one of the potential problems associated with the use of SBM is the deficient levels of indispensable amino acids (viz. lysine and methionine), that is limiting their use in shrimp feed as an alternative to FM (Yue et al. 2012). In addition, SBM contains some anti-nutritional components (for example, protease inhibitors, saponins tannins, phytic acid, lectins, alkaloids and non-starch polysaccharides) that negatively influence the digestion or absorption of nutrients and cause the dysfunction of vitamins (Gatlin et al. 2007; Krogdahl et al. 2010).

Whiteleg shrimp, Litopenaeus vannamei, is the most globally cultured shrimp species. It is mostly cultured in China, India and Thailand and the worldwide production has increased from 1.32 million tons (mt) in 2004 to 3.28 mt in 2013 due to high market demand (FAO 2014). Considering the high level of FM (25–50%) in the diet of this species, L. vannamei is perhaps one of the biggest consumers of FM in the world (Olsen and Hasan 2012). Therefore, this study was undertaken to investigate the benefits of biofloc system in shrimp culture while replacing FM by SBM; to reduce the amount of FM used in the diet of L. vannamei. In addition, this study aimed to identify the optimum level of dietary SBM with/without amino acids (lysine and methionine) supplementation as a FM alternative and effects on growth performance, whole-body proximate, amino acids compositions and haemolymph indices of juvenile whiteleg shrimp, L. vannamei, reared under biofloc conditions.

Materials and methods

Experimental design

The feeding trial was carried out at the National Fisheries Research and Development Institute (NFRDI), Taean, Republic of Korea. The shrimp used in this study were produced from specific pathogen free (SPF) L. vannamei broodstock imported from Hawaii, USA. Prior to the start of the feeding trial, juvenile whiteleg shrimp were kept in indoor fiberglass tank (6 m2, 5 t) containing aerated clean water for a period of 7 days at 28.3 ± 1.7 °C. In this period, shrimp were fed a commercial feed (DongA One, Busan, Republic of Korea), two time per day. At the beginning of the feeding trial, a total of 1320 juvenile whiteleg shrimp (average initial weight 0.9 ± 0.05 g) were carefully selected from the stock tank and directly distributed into 24 fiberglass tanks with a water volume of 200 L each (55 shrimp for each tank). Eight groups of shrimp were fed using each of the formulated diets. The feeding rate was 7% of body weight per day at beginning of experiment that gradually deceased to 5% at the end of experiment. After every 2 weeks, total weight in each tank was measured and daily feed was equally divided into four parts and given at 09:00, 13:00, 17:00 and 21:00 to all of the tanks. During 8 weeks of the feeding trial, biofloc was supplied from the stock tanks at the NFRDI and aeration for all tanks was applied using air-stones that were connected to an air pump (Resun LP-60 Pond Air Pump, China), and 20% of the water was exchanged daily in all the biofloc and clear water tanks.

Throughout the experiment, dissolved oxygen, salinity, temperature (°C), and pH (YSI Model 85, YSI Incorporated, Yellow Springs, OH, USA) were measured daily in both the biofloc and clear water tanks. Water samples (500 mL) were collected from each tank at 2 weeks intervals (0, 2, 4, 6, and 8 weeks). Half of this amount of water was analyzed using a spectrophotometer for total ammonia nitrogen (TAN), nitrite nitrogen (NO2 -N) and nitrate nitrogen (NO3 -N) using the standard methods for marine environmental analysis (MLTM 2010); the other half was filtered using vacuum pressure passing through Whatman GF/C filter paper that were pre-dried and pre-weighed. The filter paper containing suspended materials was dried at 105 °C in an oven until sustained weight, and the dried sample was weighed to 0.01 mg. The weight difference was calculated and total suspended solids (TSS) were obtained (Avnimelech and Kochba 2009).

Experimental diets

Eight experimental diets were formulated to replace FM using SBM at 0% in seawater without biofloc system (S0SW) as a control diet. Four diets replaced 0% (S0), 33% (S33), 67% (S67) and 100% (S100) of FM without amino acid supplementation and three diets replaced 33% (S33A), 67% (S67A) and 100% (S100A) of FM with supplementation of l-Methionine and l-Lysine in seawater biofloc system (Table 1). The amino acid profiles of the major feed ingredients (fish meal, soybean meal, wheat flour and wheat gluten) and diets are listed in Tables 2 and 3, respectively. For carbohydrate, lipid and non-nutritive bulk, ingredients, such as wheat flour and wheat gluten meal, fish oil and cellulose were used, respectively. Other nutrients were added to meet the nutritional requirements of L. vannamei (Hu et al. 2008), and were kept in the same levels in all diets.
Table 1

Ingredients and proximate composition of the test diets (% of DM basis)

Ingredients

S0SW

S0

S33

S33A

S67

S67A

S100

S100A

Fish meala

39.0

39.0

26.0

26.0

13.0

13.0

0.00

0.00

Soybean mealb

0.00

0.00

15.9

15.9

32.2

32.2

48.1

48.1

Wheat flourb

46.6

46.6

40.4

40.4

34.2

34.4

28.3

28.4

Wheat gluten mealb

3.60

3.60

4.60

4.50

5.40

5.00

6.30

5.70

l-Methioninec

0.00

0.00

0.00

0.10

0.00

0.15

0.00

0.20

l-Lysinec

0.00

0.00

0.00

0.00

0.00

0.10

0.00

0.30

Fish oild

3.60

3.60

4.50

4.50

5.30

5.30

6.10

6.10

Lecithinb

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

Calcium phosphatec

2.00

2.00

2.00

2.00

2.00

2.00

2.00

2.00

Cholesterolc

0.20

0.20

0.20

0.20

0.20

0.20

0.20

0.20

Vitamin premixe

2.00

2.00

2.00

2.00

2.00

2.00

2.00

2.00

Mineral premixf

2.00

2.00

2.00

2.00

2.00

2.00

2.00

2.00

Cellulosec

0.00

0.00

1.40

1.40

2.70

2.70

4.00

4.00

Chemical analysis (% DM)

 Protein

36.1

34.8

35.6

35.3

36.2

35.1

35.8

35.7

 Lipid

8.27

8.03

8.34

8.16

7.80

8.10

8.35

7.97

 Ash

10.92

10.60

10.37

10.29

9.11

8.91

7.62

7.17

 Moisture

7.30

7.33

7.30

9.10

7.93

7.26

7.34

7.44

 Digestible energy (kJ g−1)

4143

4143

4143

4143

4143

4142

4142

4142

aChilean standard grade steam-dried fish meal, Suhyup feed C. Uiryeong, Republic of Korea

bSuhyup feed C. Uiryeong, Republic of Korea

cSigma-Aldrich Korea Yongin, Republic of Korea

dJeil feed Co. Hamma n, Republic of Korea

eContains (as mg/kg in diets): Ascorbic acid, 300; dl-Calcium pantothenate, 150; Choline bitartrate, 3000 l Inositol, 150; Menadione, 6; Niacin, 150; Pyridoxine · HCl, 15; Riboflavin, 30; Thiamine mononitrate, 15; dl-α-Tocopherol acetate, 201; Retinyl acetate, 6; Biotin, 1.5; Folic acid, 5.4; Cobalamin, 0.06

fContains (as mg/kg in diets): NaCl, 437.4; MgSO4·7H2O, 1379.8; ZnSO4·7H2O, 226.4; Fe-Citrate, 299; MnSO4, 0.016; FeSO4, 0.0378; CuSO4, 0.00033; Calcium iodate, 0.0006; MgO, 0.00135; NaSeO3, 0.00025

Table 2

Amino acid composition of the major feed ingredients (% of as is basis)

Amino acidsa

Fish meal

Soybean meal

Wheat flour

Wheat gluten

EAA

 Threonine

2.96

2.11

0.29

2.09

 Valine

3.25

2.52

0.43

3.13

 Isoleucine

2.71

2.45

0.51

3.15

 Leucine

4.94

4.10

0.70

5.38

 Phenylalanine

2.62

2.70

0.49

3.98

 Histidine

2.29

1.89

0.29

2.08

 Lysine

4.75

3.20

0.21

1.32

 Arginine

4.09

3.75

0.39

2.81

 Methionine

1.41

0.58

0.14

1.04

NEAA

 Aspartic

6.63

6.36

0.43

3.23

 Serine

3.20

2.75

0.49

3.76

 Glutamic

9.00

10.03

3.53

29.57

 Proline

2.98

2.67

1.12

9.32

 Glycine

4.41

2.17

0.35

2.63

 Alanine

3.93

2.27

0.29

1.97

 Tyrosine

2.01

1.56

0.27

2.28

 Cysteine

0.88

1.00

0.34

2.22

aAmino acid sample were analyzed at Feeds and Foods Nutrition Research Center, Pukyong National University. Values are means of triplicate samples

Table 3

Amino acid composition of the test diets (% of DM basis)

Amino acidsa

S0SWb

S0

S33

S33A

S67

S67A

S100

S100A

EAA

 Threonine

1.01

1.01

1.03

1.02

1.23

1.22

1.21

1.23

 Valine

1.74

1.75

1.73

1.66

1.54

1.52

1.58

1.57

 Isoleucine

1.46

1.46

1.51

1.46

1.43

1.41

1.96

1.48

 Leucine

2.47

2.45

2.49

2.38

2.50

2.48

2.57

2.56

 Phenylalanine

1.38

1.44

1.53

1.44

1.62

1.59

1.73

1.72

 Histidine

1.03

0.94

0.93

0.96

1.08

1.04

1.06

1.09

 Lysine

1.88

1.80

1.75

1.77

1.51

1.71

1.52

1.70

 Arginine

1.86

1.72

1.86

1.81

2.03

1.98

2.07

2.12

 Methionine

0.30

0.28

0.32

0.35

0.22

0.33

0.20

0.31

NEAA

 Aspartic

2.58

2.49

2.69

2.69

3.09

3.14

3.17

3.39

 Serine

0.86

0.90

0.98

1.04

1.70

1.66

1.72

1.76

 Glutamic

6.87

6.98

7.24

7.14

7.95

7.60

8.30

8.22

 Proline

2.30

2.36

2.51

2.48

2.41

2.26

2.29

2.48

 Glycine

1.81

1.88

1.62

1.54

1.48

1.49

1.33

1.33

 Alanine

1.61

1.58

1.46

1.40

1.35

1.36

1.28

1.28

 Tyrosine

0.64

0.69

0.85

0.69

1.00

1.05

1.12

1.18

 Cysteine

0.75

0.73

0.84

0.85

0.73

0.77

0.75

0.71

aAmino acid sample were analyzed at Feeds & Foods Nutrition Research Center, Pukyong National University. Values are means of triplicate samples

bFor experimental diets refer to Table 1

Methods for preparation of diets were pursued according to the research done by Bai and Kim (1997). At first, all dry ingredients were mixed (HYVM-1214, Hanyoung Food Machinery, Republic of Korea) thoroughly and the experimental diets were prepared. After that, according to formulation table, fish oil and water were added to the diets. A screw-type pelleting machine (SFD-GT, Shinsung, Republic of Korea) was used to form the pellets by passing the dough through. After the pelletizing process, the pellets were air dried for approximately 48 h and were broken up, sieved into the proper pellet size, sealed, and stored at −20 °C until utilization.

Biofloc collection and shrimp sampling

Biofloc samples were collected at the beginning and the middle of the feeding period by passing the water through a 10-μm mesh size nylon bag. Biofloc samples were dried in an oven at 60 °C until constant weight and preserved at −20 °C for proximate composition that is shown in Table 4. At the end of the feeding trial, feeding was denied for 24 h, and the total number and weight of shrimp in each tank were determined. Growth performance parameters, such as weight gain (WG), specific growth rate (SGR), protein efficiency ratio (PER), feed conversion ratio (FCR) and survival were calculated according to the formulas described by Mohanty (1999).
$$\begin{aligned} & {\text{Weight gain (WG)}} = ({\text{final weight}} - {\text{initial weight}}) \times 100/{\text{initial weight}}. \\ & {\text{Specific growth rate (SGR)}} = 100 \times ({\text{ln final weight}} - {\text{ln initial weight}}) /{\text{days}}. \\ & {\text{Feed conversion ratio (FCR)}} = {\text{total dry feed intake}},{\text{ g}}/{\text{total wet weight gain}},{\text{ g}} \\ & {\text{Protein efficiency ratio (PER)}} = {\text{wet weight gain}},{\text{ g}}/{\text{protein intake}},{\text{ g}}. \\ \end{aligned}$$
Table 4

Proximate composition (% dry weight basis) of the outdoor biofloc-based culture pond water at the beginning and the middle of the feeding trial

Parametersa

Beginning

Middle

Pooled SEMb

Crude protein (%)

26.9

27.4

0.07

Crude lipid (%)

0.34

0.37

0.02

Crude Ash (%)

47.6

48.6

0.11

Moisture (%)

86.3

86.7

0.09

aBiofloc samples were analyzed at Feeds & Foods Nutrition Research Center, Pukyong National University. Values are means of triplicate samples

bPooled standard error of means: SD/√n

Ten intact shrimp per tank (30 individuals per treatment group) were randomly selected and kept at −20 °C for whole-body proximate and amino acid compositions. Five shrimp were randomly selected from each tank and about 0.3 ml of haemolymph was taken from the ventral sinus in the first pleomere using a 1-ml syringe that had a hypodermic needle with 2 mm of thickness. About 0.2 ml of an anticoagulant substance (113 mM glucose, 27.2 mM sodium citrate, 2.8 mM citric acid and 71.9 mM NaCl) was passed through each syringe. Haemolymph samples were centrifuged at 5000×g for 10 min and the plasma was separated and stored at −70 °C for determination of haemolymph biochemical parameters, including plasma total protein, cholesterol, triglyceride and glucose. The same shrimp were used for another set of haemolymph samples, this time anticoagulant was not used and after 30 min haemolymph was clot at room temperature. Then, using a centrifuge (at 5000×g) for 10 min the serum was divided and kept at −70 °C for the analysis of non-specific immune responses such as superoxide dismutase (SOD) and trypsin activities.

The tested diets, shrimp whole-body and amino acid compositions from each dietary treatment, and biofloc samples were analyzed according to the standard methods of AOAC (2005). Moisture content of samples was estimated by drying oven at 135 °C for 2 h to constant weight. Crude protein was determined using the Kjeldahl method (N× 6.25) after acid digestion. Soxhlet extraction was used to evaluate crude lipid using the Soxtec system 1046 (Tacator AB, Hoganas, Sweden), and a muffle furnace was used to determine ash of dried samples by combustion at 550 °C for 6 h. Ninhydrin method (Sykam Amino Acid Analyzer S433; Sykam, Eresing, Germany) was used to analyze amino acids.

The concentrations of triglyceride, total protein, cholesterol, and glucose levels of plasma were determined by a chemical analyzer Fuji DRI-CHEM 3500i (Fuji Photo Film Ltd., Tokyo, Japan). SOD Assay Kit (Sigma-Aldrich, 19160) was used to measure the activity of SOD by inhibition rate of enzyme with WST-1 (Water Soluble Tetrazolium dye) and xanthine oxidase according to instructions of manufacturer. Each assay was observed at absorbance of 450 nm after 20 min of reaction at 37 °C. The inhibition percent was assigned by mg protein and the values were known as SOD activity. The trypsin activity of shrimp was measured in the serum using a commercial kit (BioVision, CA, USA).

Statistical analysis

One-way ANOVA was used to analyze data for the effects of the dietary treatments. When significant differences were found, a least significant difference (LSD) test used to identify differences among experimental groups. The significance level of P < 0.05 was used to compare differences. SAS version 9.0 (SAS Institute, Cary, NC, USA) application was used for statistical analyses.

Results

Water quality parameters

The results for water quality parameters and biofloc development in term of total suspended solids (TSS) are shown in Table 5. The measured water quality in all experimental groups remained within recommended levels for shrimp culture. TSS levels almost stabilized in the biofloc tanks with average level of around 202.4 mg L−1 throughout the experimental period, but with significant differences with the clear water tanks. There were also significant differences in the amount of NO3-N between all biofloc tanks and clear water tanks (P < 0.05).
Table 5

Average water quality parameters of different experimental diets for 8 weeks

Parameters

S0SWa

S0

S33

S33A

S67

S67A

S100

S100A

Pooled SEMb

Salinity (g L−1)

31.8

32.2

32.0

32.0

32.2

32.1

32.1

32.1

0.01

DO (mg L−1)

5.9

5.8

5.8

5.8

5.8

5.7

5.8

5.8

0.02

pH

7.9

7.6

7.6

7.6

7.6

7.6

7.6

7.3

0.01

TAN (mg L−1)

0.56

0.44

0.32

0.38

0.31

0.33

0.35

0.42

0.08

NO2 -N (mg L−1)

0.64

0.49

0.66

0.65

0.57

0.51

0.58

0.59

0.02

NO3 -N (mg L−1)

18.7v

3.08u

3.13u

3.16u

3.12u

3.23u

3.34u

3.35u

8.00

TSS (mg L−1)

36.4v

206u

191u

192u

196u

209u

215u

208u

7.36

Values in same row with different superscript are significantly different at P < 0.05

DO dissolved oxygen, TAN total ammonia nitrogen, TSS total suspended solids

aFor experimental diets refer to Table 1

bPooled standard error of means: SD/√n

Growth performance

At the end of the feeding trial, WG and SGR of shrimp fed S0 and S33A diets were significantly higher than those of shrimp fed the other diets with no significant differences with S33 group (Table 6). FCR gradually increased among biofloc groups by addition of dietary SBM with significant differences between S0 group and S67A, S100 and S100A groups. There were also significant differences in FCR between S0SW and S0 groups. PER of shrimp fed S0 diet were significantly higher than those of shrimp fed S67, S67A, S100, S100A and S0SW diets. Survival of shrimp fed S0SW diet was significantly lower (P < 0.05) than those of shrimp fed the other diets, except the S0 group.
Table 6

Growth performance of juvenile whiteleg shrimp fed different experimental diets for 8 weeks

Parameters

S0SWa

S0

S33

S33A

S67

S67A

S100

S100A

Pooled SEMb

WG (%)c

539y

901w

834wx

891w

773x

800x

540y

544y

28.2

SGR (% day−1)d

3.49z

4.34w

4.21wxy

4.33w

4.09y

4.14xy

3.50z

3.51z

0.07

FCRe

1.46x

1.06z

1.09yz

1.08yz

1.17yz

1.18y

1.59w

1.54wx

1.07

PERf

1.91z

2.71w

2.58wx

2.61wx

2.38y

2.43yz

1.76z

1.83z

0.04

Survival rate (%)

75.8x

84.2wx

89.1w

89.7w

89.7w

84.8w

86.7w

91.5w

1.12

Values in same row with different superscript are significantly different at P < 0.05

aFor experimental diets refer to Table 1

bPooled standard error of means: SD/√n

cWeight gain (WG) = (final weight − initial weight) × 100/initial weight

dSpecific growth rate (SGR) = 100 × (ln final weight − ln initial weight)/days

eFeed conversion ratio (FCR) = total dry feed intake, g/total wet weight gain, g

fProtein efficiency ratio (PER) = wet weight gain, g/protein intake, g

Whole-body proximate composition

Crude protein and crude lipid contents of shrimp fed S0SW diet were significantly lower and higher, respectively, than shrimp fed the other diets (Table 7). Crude ash content of shrimp fed S100 and S100A diets was significantly higher than those of shrimp fed the other diets. Moisture percentage of shrimp fed S100A diet was significantly higher (P < 0.05) than the shrimp fed other diets among biofloc groups.
Table 7

Whole-body proximate composition (% dry weight basis) of juvenile whiteleg shrimp fed different experimental diets for 8 weeks

Composition

S0SWa

S0

S33

S33A

S67

S67A

S100

S100A

Pooled SEMb

Crude protein (%)

77.1v

80.1u

80.2u

80.2u

79.6u

79.5u

80.3u

79.5u

2.44

Crude lipid (%)

4.10u

2.70wxy

2.98wx

3.50v

3.10vw

2.59xyz

2.38yz

2.22z

0.11

Crude Ash (%)

10.8wxy

10.7xy

11.5w

11.0wx

10.0y

12.8v

14.1u

14.0u

0.28

Moisture (%)

77.6uv

75.2y

75.7x

75.8x

77.3v

76.6w

77.3v

77.7u

0.15

Values in same row with different superscript are significantly different at P < 0.05

aFor experimental diets refer to Table 1

bPooled standard error of means: SD/√n

Whole-body amino acid composition

The whole-body amino acid composition of shrimp is shown in Table 8. The total essential amino acids of S0SW group were significantly lower than all other groups that were cultured in biofloc system except for the S0 group (P < 0.05). Meanwhile, the whole-body non-essential amino acids of shrimp fed the S0SW and S0 diets were significantly lower than the shrimp fed on diets S33A, S67, S67A, S100 and S100A (P < 0.05).
Table 8

Whole-body amino acid composition (mg 100 mg−1) of juvenile whiteleg shrimp fed different experimental diets for 8 weeks

Amino acids

S0SWa

S0

S33

S33A

S67

S67A

S100

S100A

Pooled SEMb

Threonine

2.60w

2.62w

2.63vw

2.70uv

2.73u

2.73u

2.72u

2.71uv

0.01

Valine

3.11wxy

3.11xy

3.07y

3.24uv

3.30u

3.21uvw

3.20uvwx

3.11wxy

0.02

Isoleucine

2.69wx

2.70x

2.64x

2.82uv

2.89u

2.81uvw

2.81uvw

2.74vwx

0.02

Leucine

4.66w

4.78vw

4.75vw

4.96u

4.98u

4.96u

4.96u

4.87uv

0.03

Phenylalanine

2.97

2.99

3.00

3.10

3.12

3.06

2.47

3.04

0.06

Histidine

4.24vw

4.29vw

4.59v

4.09w

4.10w

4.33vw

5.16u

4.58v

0.07

Lysine

4.68w

4.95vw

4.93v

5.19u

5.03uv

5.00uv

5.21u

4.96v

0.03

Arginine

4.50x

5.29w

5.23w

5.32w

5.40vw

5.26w

5.81u

5.57v

0.06

Methionine

0.91wx

0.80x

1.12vw

1.41u

1.45u

1.42u

1.45u

1.32uv

0.05

Essential

30.4y

31.5xy

32.0wx

32.8vw

33.0uv

32.8vw

33.8u

32.9uv

0.24

Aspartic

7.69uv

7.64v

7.86uv

8.11u

8.11u

8.05uv

7.88uv

8.05uv

0.05

Serine

2.66x

2.75wx

2.77vw

2.79vw

2.79uvw

2.82uv

2.83uv

2.86u

0.01

Glutamic

10.5vw

10.5w

10.3w

10.8uv

10.9u

10.9u

11.0u

10.7uvw

0.06

Proline

4.59

4.76

4.78

5.09

4.87

5.04

4.68

4.59

0.06

Glycine

5.09x

5.42wx

5.52vw

5.54vw

5.77v

5.70v

6.20u

6.10u

0.07

Alanine

4.02y

3.98xy

4.06wx

4.14vwx

4.25uv

4.18uvw

4.24uv

4.27u

0.03

Tyrosine

2.21

2.13

2.18

2.11

2.10

2.12

2.16

2.15

0.01

Cysteine

1.27vw

1.25w

1.37vw

1.51u

1.53u

1.50u

1.54u

1.42uv

0.03

Non-essential

38.0w

38.6w

38.9vw

40.1uv

40.4u

40.3u

40.5u

40.1uv

0.25

Total

68.4w

70.1vw

70.8v

72.9u

73.4u

73.1u

74.3u

73.0u

0.47

Values in same row with different superscript are significantly different at P < 0.05

aFor experimental diets refer to Table 1

bPooled standard error of means: SD/√n

Haemolymph parameters

Plasma protein values of shrimp fed S0 and S33 diets were significantly higher than those of shrimp fed S100A and S0SW diets (Table 9). Moreover, plasma glucose value of shrimp fed S100 and S100A diets was significantly higher than those of shrimp fed S33 diet. Significantly higher (P < 0.05) plasma cholesterol and triglyceride values were found in shrimp fed S0SW diet compared to the other diets.
Table 9

Haemolymph parameters of juvenile whiteleg shrimp fed different experimental diets for 8 weeks

Parameters

S0SWa

S0

S33

S33A

S67

S67A

S100

S100A

Pooled SEMb

Total protein (g dL−1)

4.67v

8.40u

8.47u

6.73uv

7.13uv

5.60uv

6.80uv

4.80v

0.33

Glucose (mg dL−1)

1518uv

1437uv

1412v

1476uv

1466uv

1498uv

1542u

1547u

13.2

Cholesterol (mg dL−1)

38.0u

19.3vw

20.7v

18.7vwx

19.3vw

16.0vwx

10.7wx

10.0x

1.58

Triglyceride (mg dL−1)

81.3u

52.0vw

57.3v

48.0vw

48.0vw

40.7vw

37.3vw

32.7w

3.10

Values in same row with different superscript are significantly different at P < 0.05

aFor experimental diets refer to Table 1

bPooled standard error of means: SD/√n

Non-specific immune responses

The results for non-specific immune response activity showed significantly higher serum superoxide dismutase (SOD) in shrimp fed S0 diet compared to those of shrimp fed the other diets, except for shrimp fed S33A and S0SW diets (Fig. 1a). Significantly higher levels of trypsin activity was obtained in shrimp fed S0 diet compared to those of shrimp fed S100 and S100A diets (P < 0.05; Fig. 1b).
Fig. 1

Serum superoxide dismutase (a) and trypsin (b) activities of juvenile whiteleg shrimp fed different experimental diets for 8 weeks. Values are mean ± SD of three replicate tanks per sampling time in each group

Discussion

During this experiment, water quality parameters in biofloc system were in favorable condition and had no significant effect on survival of whiteleg shrimp. However, significant differences were observed in the amount of total suspended solids (TSS) and nitrate (NO 3 - ) between clear water and biofloc system. Changes in the amount of TSS in culture water, over time, shows the development of the system. Hence, TSS is considered to be an indicator for quantitative evaluation of culture system (De Schryver et al. 2008). It has been reported that the optimal amount of TSS for shrimp culture is approximately between 200 and 400 mg L−1 (Plínio et al. 2015; Xu et al. 2016) and further increases in TSS level could cause gill irritation of organisms and biological oxygen demand (BOD) creates more stresses in shrimp (Beveridge et al. 1991; Hargreaves 2006; Brune et al. 2003; Ray et al. 2010), whereas lower amounts of TSS could cause growth reduction of shrimp (Samocha et al. 2004a; Ekasari et al. 2016). Proper management of TSS level could be useful for both shrimp and biofloc system (Cohen et al. 2005; Ebeling et al. 2006; De Schryver et al. 2008; Ray et al. 2010). In our experiment, nitrate, nitrite and TAN were in safe levels for whiteleg shrimp culture that is in accordance with findings of Van Wyk and Scarpa (1999). Nitrate is the final compound in the nitrification process, although it is not highly toxic for shrimp, it is recommended to be kept lower than 100 mg L−1 in culture water. Higher amounts of nitrate could cause stress for shrimp and reduce the growth (Plínio et al. 2015; Samocha et al. 2004a, b). These results suggest that by application of biofloc system for shrimp culture the water quality parameters could be effectively controlled in a more favorable trend (Xu et al. 2016).

The dietary protein of feed in the present study was formulated to contain 35–36% crude protein based on the requirement of whiteleg shrimp (Xia et al. 2010; Shahkar et al. 2014). In addition, the reference diet (control) contained 39% of fish meal (FM), because commercial shrimp feeds usually contain 25–50% of FM (Dersjant-Li 2002; Tacon and Barg 1998). The results illustrated for WG, SGR, FCR, PER and survival rate clearly indicate the benefits of shrimp culture in biofloc system in comparison to clear water. This is in agreement with previous studies that have proven growth and immunity enhancement of shrimp that were cultured in biofloc system (Kim et al. 2014). The observation for growth performance also showed that up to 33% of the FM in a practical diet for whiteleg shrimp, reared in biofloc system, could be effectively substituted by the soybean meal (SBM). Previously, numerous studies have been conducted to evaluate the suitability of various feed ingredients as alternative protein sources for FM; as partial or even total replacement of FM by plant ingredients in the diet of L. vannamei has been reported by several authors (Amaya et al. 2007; Suárez et al. 2009; Olmos et al. 2011; Ye et al. 2011; Liu et al. 2012; Yue et al. 2012; Gu et al. 2013; Sá et al. 2013; Sookying et al. 2013; Kuhn et al. 2016; Xie et al. 2016). In the present study, application of methionine and lysine in the diet did not significantly influence the growth performance. Probably the EAA requirements of shrimp may have been met without the additional amino acids and excess amino acids in the diet did not result in higher growth. This might be related to the nutritional quality of bioflocs, as they are known to have considerable amount of protein, lipid, carbohydrate and ash content as an aquatic feed (Crab et al. 2010). In contrast to our results, Yue et al. (2012) found that using lysine and methionine in the diet of L. vannamei more amounts of FM could be replaced by SBM, although it should be considered that in their experiment shrimp were not cultured in biofloc system. According to our results, the higher growth performance of shrimp that were cultured in biofloc in comparison to the clear water group is in agreement with previous findings (Ray et al. 2011; Irshad et al. 2016). Valle et al. (2015), replaced fish meal with biofloc flour and protein hydrolysate in the diet of L. vannamei and indicated that biofloc flour is a potential ingredient that can be used as substitute for fishmeal. In our study, whole-body proximate composition was not affected much by the FM substitution with SBM. Although, higher whole-body protein level in shrimp that were cultured in biofloc system, in comparison to shrimp that were cultured in clear water, indicates the positive influence of biofloc in increasing the whole-body protein content. Similar observation has been reported in a study on whiteleg shrimp by Xu et al. (2012). Khatoona et al. (2016), reported that 50% biofloc in the diet of L. vannamei could increase the whole-body protein content, compared to the diets without biofloc inclusion. This shows the positive contribution of bioflocs in increasing the whole-body protein level in shrimp.

As a plant protein source, SBM is widely used as a partial or complete substitute for animal protein (Hertrampf and Pascual 2000). Several nutritionists have investigated the feasibility of SBM in aquafeeds, and the results are contradictory, because the levels of SBM that can be used without causing growth reduction are highly species-specific and influenced by culture systems (Yue et al. 2012). For instance, Markey (2007) reported that 58% of SBM is being used in grow out culture of whiteleg shrimp. Lim and Dominy (1990) demonstrated that 40% level of a marine mixed protein could be replaced by solvent extracted SBM, whereas higher levels exerted reduced growth performance of L. vannamei. It was also reported that 80% FM could be replaced by co-extruded soybean and poultry by-product meal supplemented with egg in indoor recirculating water system (Davis and Arnold 2000). Likewise, other researchers suggested different inclusion levels of FM in the diet of whiteleg shrimp culture in different conditions (Samocha et al. 2004a; Browdy et al. 2006; Patnaik et al. 2006; Amaya et al. 2007). This is while in marine shrimp diets, higher levels of dietary SBM usually resulted in lower growth (Akiyama 1990; Floreto et al. 2000). Likewise, Yue et al. (2012) suggested that FM inclusion can be reduced to approximately 200 g kg−1 diet of whiteleg shrimp when SBM and peanut meal are included instead. Reduced growth performance and increased FCR in L. vannamei fed different diets that gradually replace FM by SBM could be because of anti-nutritional factors, such as saponins, phytoestrogens, allergens, phytate (myo-inositol-1,2,3,4,5,6-hexakisphosphate), protease inhibitors, trypsin inhibitors, lectins and antivitamins (Francis et al. 2001). For example, trypsin inhibitors and lectins prevent the proper activity of digestive enzymes (Gemede and Ratta 2014). The other limitation in application of SBM in fish diet is the improper amino acid composition that does not meet the nutritional requirements of fish (Floreto et al. 2000). In addition, n-3 lipid composition of SBM is much lower comparing to FM, and thus high inclusion levels of SBM in the diet may result in reduced growth performance (Sharawya et al. 2016).

According to the results obtained for whole-body amino acid composition of shrimp in this study, higher essential and non-essential amino acids were observed in biofloc cultured shrimp comparing to clear water cultured shrimp. In addition, higher amounts of FM seem to have negative effect of the amino acid composition. This might be partly related to the higher digestibility of amino acids in FM comparing to SBM (Liu et al. 2013; Yang et al. 2009). Similar results were observed by Xie et al. (2016), while replacing FM by soy protein concentrate and soybean meal based protein blend for juvenile white shrimp. Moreover, more investigations are required for clarifying the mechanism.

Haemolymph metabolites in crustaceans represent the physiological, nutritional and immunological stress indicators (Becerra-Dorame et al. 2012). In this study, plasma protein was higher in lower substitute level of SBM which means high FM containing diet resulted in high total protein content in haemolymph of whiteleg shrimp and this was according to the results obtained by Rosas et al. (2000). Furthermore, in the present study, plasma cholesterol and triglyceride levels have decreasing trend among the dietary treatments. In other studies, same decreasing trend of cholesterol was found in rainbow trout, Oncorhynchus mykiss (Kaushik et al. 1995) and gilthead sea bream, Sparus aurata (Venou et al. 2006) due to inclusion of SBM in the diet. This might have happened because of the hypocholesterolemic effect of SBM (Davis and Morris 1997; Yue et al. 2012). The plasma glucose levels in whiteleg shrimp increased with increasing substitute level of SBM among the experimental diets. These results are probably related to higher inclusion level of plant protein (SBM) in the diet, which is definitely followed by the increment of carbohydrate source in the diet.

Trypsin is a protease enzyme that is excreted by the pancreas and plays a great role in the digestion of proteins (Erlanger et al. 1961). The results of the present study showed that the 100% replacement level of FM, with no regard to the inclusion of amino acids, had negative effects on the activity of trypsin. This might be related to the trypsin inhibitory properties of SBM (Francis et al. 2001). There are several natural trypsin inhibitors, also known as serine protease inhibitors, and SBM is one of the most important ones. SBM controls the activation and catabolism of proteins by the inhibition of serine proteases (Silverman et al. 2001). Thus, at 100% replacement level, SBM will act as trypsin inhibitor for juvenile whiteleg shrimp. Previously, it was shown that biofloc contain several extracellular enzymes such as protease and amylase (Yu et al. 2009). The extracellular enzymes that are synthesized by the microorganisms attached to the biofloc would release to the digestive tract of the host organism after being ingested. These enzymes would take part along with the total enzymes activities of the body. In addition, the bioactive compounds present in the biofloc may possibly improve digestive enzyme activities of the shrimp (Xu et al. 2012). Observation with the trypsin activity suggested an improved efficiency of whiteleg shrimp to digest SBM diet reared in biofloc system as compared to those shrimp reared in clear water fed diets with 100% FM. The superoxide dismutase (SOD) is an antioxidant enzyme that functions by removing damaging reactive oxygen species (ROS) from the cell. The mechanism is by catalyzing the segregation of the superoxide (O2−) radicals to ordinary molecules such as oxygen or hydrogen peroxide (Fattman et al. 2003; Lin et al. 2010). In the present study, SOD activity was reduced when the FM substitution level exceeded 33% of diet. The results of this study demonstrated that shrimp fed diets with up to 33% replacement level were in better physiological and health condition compared to higher inclusion rates. In conclusion, this study showed that up to 33% FM in the diets of juvenile whiteleg shrimp reared in biofloc system could be replaced by SBM with or without supplementation of methionine and lysine.

Notes

Acknowledgements

This experiment was a part of the project ‘The Environmental-friendly Aquaculture Technology using biofloc’ (RP-2012-AQ-008) of the National Fisheries Research and Development Institute (NFRDI), Incheon, Republic of Korea, and Feeds and Foods Nutrition Research Center (FFNRC), Pukyong National University, Busan, Republic of Korea.

References

  1. Aas TS, Grisdale-Helland B, Terjesen BF, Helland SJ (2006) Improved growth and nutrient utilization in Atlantic salmon (Salmo salar) fed diets containing a bacterial protein meal. Aquaculture 259:365–376CrossRefGoogle Scholar
  2. Akiyama DM (1990) The use of soybean meal to replace white fish meal in commercially processed. Penaeus monodon Fabricus feeds in Taiwan. In: Takeda M, Watanabe T (eds) Feeding and nutrition in fish: the current status of fish nutrition in aquaculture. Proceedings of 3rd international symposium, Toba, Japan, pp 289–299Google Scholar
  3. Amaya E, Davis DA, Rouse DB (2007) Replacement of fish meal in practical diets for the Pacific white shrimp, Litopenaeus vannamei, reared under pond conditions. Aquaculture 262:393–401CrossRefGoogle Scholar
  4. AOAC (2005) Official methods of analysis, 18th edn. Association of Official Analytical Chemists, GaithersburgGoogle Scholar
  5. Arnold SJ, Coman FE, Jackson CJ, Groves SA (2009) High-intensity, zero water exchange production of juvenile tiger shrimp, Penaeus monodon: an evaluation of artificial substrates and stocking density. Aquaculture 293:42–48CrossRefGoogle Scholar
  6. Avnimelech Y (2006) Bio-filters: the need for a new comprehensive approach. Aquac Eng 34:172–178CrossRefGoogle Scholar
  7. Avnimelech Y (2008) Sustainable land-based aquaculture—rational utilization of water, land and feed. Mediterr Aquacult J 1:45–55Google Scholar
  8. Avnimelech Y, Kochba M (2009) Evaluation of nitrogen uptake and excretion by tilapia in bio floc tanks, using 15 N tracing. Aquaculture 287:163–168CrossRefGoogle Scholar
  9. Bai SC, Kim KW (1997) Effects of dietary animal protein sources on growth and body composition in Korean rockfish, Sebastes schlegeli. Aquaculture 10:77–85Google Scholar
  10. Ballester ELC, Abreu PC, Cavalli RO, Emerenciano M, Abreu L, Wasielesky W (2010) Effect of practical diets with different protein levels on the performance of Farfantepenaeus paulensis juveniles nursed in a zero exchange suspended microbial flocs intensive system. Aquac Nutr 16:163–172CrossRefGoogle Scholar
  11. Barrows FT, Frost J (2014) Evaluation of modified processing waste from the nut industry, algae and an invertebrate meal for rainbow trout, Oncorhynchus mykiss. Aquaculture 434:315–324CrossRefGoogle Scholar
  12. Becerra-Dorame MJ, Martinez-Cordova LR, Martinez-Porchas M, Hernandez-Lopez J, Lopez-Elias JA, Mendoza-Cano F (2012) Effect of using autotrophic and heterotrophic microbial-based-systems for the pre-grown of Litopenaeus vannamei, on the production performance and selected haemolymph parameters. Aquac Res 45:944–948CrossRefGoogle Scholar
  13. Beveridge MCM, Phillips MJ, Clarke RM (1991) A quantitative and qualitative assessment of wastes from aquatic animal production. In: Brune DE, Tomasso JR (eds) Advances in world aquaculture: aquaculture and water quality. World Aquaculture Society, Baton Rouge, pp 506–533Google Scholar
  14. Browdy C, Seaborn G, Davis DA, Bullis RA, Samocha TM, Wirth E, Leffler JW (2006) Comparison of pond production efficiency, fatty acid profiles and contaminants in Litopenaeus vannamei fed organic certifiable, plant-based and fishmeal-based grow-out diets. J World Aquac Soc 37:437–451CrossRefGoogle Scholar
  15. Brune DE, Schwartz G, Eversole AG, Collier JA, Schwedler TE (2003) Intensification of pond aquaculture and high rate photosynthetic systems. Aquac Eng 28:65–86CrossRefGoogle Scholar
  16. Burford MA, Thompson PJ, McIntosh RP, Bauman RH, Pearson DC (2004) The contribution of flocculated material to shrimp (Litopenaeus vannamei) nutrition in a high-intensity, zero exchange system. Aquaculture 232:525–537CrossRefGoogle Scholar
  17. Cohen J, Samocha TM, Fox JM, Gandy RL, Lawrence AL (2005) Characterization of water quality factors during intensive raceway production of juvenile L. vannamei using limited discharge and biosecure management tools. Aquac Eng 32:425–442CrossRefGoogle Scholar
  18. Crab R, Avnimelech Y, Defoirdt T, Bossier P, Verstraete W (2007) Nitrogen removal techniques in aquaculture for a sustainable production. Aquaculture 270:1–14CrossRefGoogle Scholar
  19. Crab R, Kochva M, Verstraete W, Avnimelech Y (2009) Bioflocs technology application in over-wintering of tilapia. Aquac Eng 40:105–112CrossRefGoogle Scholar
  20. Crab R, Chielens B, Wille M, Bossier P, Verstraete W (2010) The effect of different carbon sources on the nutritional value of bioflocs, a feed for Macrobrachium rosenbergii postlarvae. Aquac Res 41:559–567CrossRefGoogle Scholar
  21. Davis DA, Arnold CR (2000) Replacement of fish meal in practical diets for the Pacific white shrimp, Litopenaeus vannamei. Aquaculture 185:291–298CrossRefGoogle Scholar
  22. Davis SJ, Morris PC (1997) Influence of multiple amino acid supplementations on the performance of rainbow trout, Oncorhynchus mykiss (Walbaum), fed soya based diets. Aquac Res 28:65–74CrossRefGoogle Scholar
  23. De Schryver P, Crab R, Defoirdt T, Boon N, Verstraete W (2008) The basics of bioflocs technology: the added value for aquaculture. Aquaculture 277:125–137CrossRefGoogle Scholar
  24. Dersjant-Li Y (2002) The use of soy protein in aquafeeds. In: Cruz-Suárez LE, Ricque-Marie D, Tapia-Salazar M, Gaxiola-Cortez MG, Nuno S (eds) Avances en Nutrición Acuícola Volumen VI. Memorias del VI Simposio Internacional de Nutrición Acuícola. Universidad Autónoma de Nuevo León, Monterrey, Nuevo León México, pp 541–558Google Scholar
  25. Ebeling JM, Timmons MB, Bisogni JJ (2006) Engineering analysis of the stoichiometry of photoautotrophic, autotrophic, and heterotrophic removal of ammonia–nitrogen in aquaculture systems. Aquaculture 257:346–358CrossRefGoogle Scholar
  26. Ekasari J, Crab R, Verstraete W (2010) Primary nutritional content of bio-flocs cultured with different organic carbon sources and salinity. HAYATI J Biosci 17:125–130CrossRefGoogle Scholar
  27. Ekasari J, Suprayudi MA, Wiyoto W, Hazanah RF, Lenggara GS, Sulistiani R, Alkahfi M, Zairin M (2016) Biofloc technology application in African catfish fingerling production: the effects on the reproductive performance of broodstock and the quality of eggs and larvae. Aquaculture 464:349–356CrossRefGoogle Scholar
  28. Emerenciano M, Ballester ELC, Cavalli RO, Wasielesky W (2012) Biofloc technology application as a food source in a limited water exchange nursery system for pink shrimp, Farfantepenaeus brasiliensis (Latreille, 1817). Aquac Res 43:447–457CrossRefGoogle Scholar
  29. Erlanger B, Kokowsky N, Cohen W (1961) The preparation and properties of two new chromogenic substrates of trypsin. Arch Biochem Biophys 95:271–278CrossRefGoogle Scholar
  30. FAO (2013) Food and Agriculture Organization of the United Nations commodity prices. Website. http://www.fao.org/economic/est/prices. Accessed 5 March 2013
  31. FAO (2014) The state of world fisheries and aquaculture. FAO Fisheries and Aquaculture, Food and Agriculture Organization of the United Nations, Rome, ItalyGoogle Scholar
  32. Fattman CL, Schaefer LM, Oury TD (2003) Extracellular superoxide dismutase in biology and medicine. Free Radic Biol Med 35:236–256CrossRefGoogle Scholar
  33. Floreto EAT, Bayer RC, Brawn PB (2000) The effects of soybean-based diets, with and without amino acid supplementation, on growth and biochemical composition of juvenile American lobster, Homarus americanus. Aquaculture 189:211–235CrossRefGoogle Scholar
  34. Fowler LG (1991) Poultry by-product meal as a dietary protein source in fall chinook salmon diets. Aquaculture 99:309–321CrossRefGoogle Scholar
  35. Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227CrossRefGoogle Scholar
  36. Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl A, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579CrossRefGoogle Scholar
  37. Gemede HF, Ratta N (2014) Antinutritional factors in plant foods: potential health benefits and adverse effects. GARJFST 3:103–117Google Scholar
  38. Gu M, Zhang WB, Bai N, Mai KS, Xu W (2013) Effects of dietary crystalline methionine or oligo-methionine on growth performance and feed utilization of white shrimp (Litopenaeus vannamei) fed plant protein-enriched diets. Aquac Nutr 19:39–46CrossRefGoogle Scholar
  39. Hardy RW (2006) Worldwide fish meal production outlook and the use of alternative protein meals for aquaculture. In: VIII international symposium on aquaculture nutrition, Nov 15–17, Universidad Autonoma de Leon, Monterry, Leon, MexicoGoogle Scholar
  40. Hargreaves JA (2006) Photosynthetic suspended-growth systems in aquaculture. Aquac Eng 34:344–363CrossRefGoogle Scholar
  41. Hari B, Kurup BM, Varghese JT, Schrama JW, Verdegem MCJ (2004) Effects of carbohydrate addition on production in extensive shrimp culture systems. Aquaculture 241:179–194CrossRefGoogle Scholar
  42. Hertrampf JW, Pascual FP (2000) Handbook on ingredients for aquaculture feeds. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  43. Hu Y, Tan B, Mai K, Zheng S, Cheng K (2008) Growth and body composition of juvenile white shrimp, Litopenaeus vannamei, fed different ratios of dietary protein to energy. Aquac Nutr 14:499–506CrossRefGoogle Scholar
  44. Irshad AH, Verma AK, Rani AMB, Rathore G, Saharan N, Gora AH (2016) Growth, non-specific immunity and disease resistance of Labeo rohita against Aeromonas hydrophila in biofloc systems using different carbon sources. Aquaculture 457:61–67CrossRefGoogle Scholar
  45. Izquierdo M, Forster I, Divakaran S, Conquest L, Decamp O (2006) Effect of green and clear water and lipid source on survival, growth and biochemical composition of Pacific white shrimp Litopenaeus vannamei. Aquac Nutr 12:192–202CrossRefGoogle Scholar
  46. Ju ZY, Forster I, Conquest L, Dominy W (2008) Enhanced growth effects on shrimp, Litopenaeus vannamei from inclusion of whole shrimp floc or floc fractions to a formulated diet. Aquac Nutr 14:533–543CrossRefGoogle Scholar
  47. Kaushik SJ, Cravedi JP, Lalles JP, Sumpter J, Fauconnea B, Laroche M (1995) Partial to total replacement of fish meal by soybean protein on growth, protein utilization, potential estrogenic or antigenic effects, cholesterolemia and flesh quality in rainbow trout Oncorhynchus mykiss. Aquaculture 133:257–274CrossRefGoogle Scholar
  48. Khatoona H, Banerjeeb S, Yuanb GTG, Harisa N, Ikhwanuddina M, Ambaka MA, Endut A (2016) Biofloc as a potential natural feed for shrimp postlarvae. Int Biodeter Biodegr 113:304–309CrossRefGoogle Scholar
  49. Kikuchi K (1999) Use of defatted soybean meal as a substitute for fish meal in diets Japanese flounder (Paralichthys olivaceus). Aquaculture 179:3–11CrossRefGoogle Scholar
  50. Kim SK, Pang Z, Seo HC, Cho YR, Samocha T, Jang IK (2014) Effect of bioflocs on growth and immune activity of Pacific white shrimp, Litopenaeus vannamei postlarvae. Aquac Res 45:362–371CrossRefGoogle Scholar
  51. Kiron V, Phromkunthong W, Huntley M, Archibald I, De Scheemaker G (2012) Marine microalgae from biorefinery as a potential feed protein source for Atlantic salmon, common carp and whiteleg shrimp. Aquac Nutr 18:521–531CrossRefGoogle Scholar
  52. Krogdahl Å, Penn M, Thorsen J, Refstie S, Bakke AM (2010) Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquac Res 41:333–344CrossRefGoogle Scholar
  53. Kuhn DD, Lawrence AL, Crockett J, Taylor D (2016) Evaluation of bioflocs derived from confectionary food effluent water as a replacement feed ingredient for fishmeal or soy meal for shrimp. Aquaculture 454:66–71CrossRefGoogle Scholar
  54. Lee KJ, Bai SC (1997) Hemoglobin powder as a dietary fish meal replacer in juvenile Japanese eel, Anguilla japonica. Aquac Res 28:509–516CrossRefGoogle Scholar
  55. Lim C, Dominy W (1990) Evaluation of soybean meal as a replacement for marine animal protein in diets for shrimp (Penaeus vannamei). Aquaculture 87:53–63CrossRefGoogle Scholar
  56. Lin K, Huang H, Lin C (2010) Cloning, expression and physiological analysis of broccoli catalase gene and Chinese cabbage ascorbate peroxidase gene under heat stress. Plant Cell Rep 29:575–593CrossRefGoogle Scholar
  57. Liu XH, Ye JD, Wang K, Kong JH, Yang W, Zhou L (2012) Partial replacement of fish meal with peanut meal in practical diets for the Pacific white shrimp, Litopenaeus vannamei. Aquac Res 43:745–755CrossRefGoogle Scholar
  58. Liu X, Ye J, Kong J, Wang K, Wang A (2013) Apparent digestibility of 12 protein-origin ingredients for Pacific white shrimp Litopenaeus vannamei. N Am J Aquac 75:90–98CrossRefGoogle Scholar
  59. Markey JC (2007) Replacement of poultry-by-product meal in production diets for the pacific white shrimp (Litopenaeus vannamei). Master’s Thesis. Auburn University. Auburn, AlabamaGoogle Scholar
  60. McGoogan BB, Gatlin DM (1997) Effects of replacing fish meal with soybean meal in diets for red drum Sciaenops ocellatus and potential for palatability enhancement. J World Aquac Soc 28:374–385CrossRefGoogle Scholar
  61. MLTM (Ministry of Land Transport and Maritime Affairs) (2010) Standard methods for marine environmental analysis. Ministry of Land, Transport and Maritime Affairs, SeoulGoogle Scholar
  62. Mohanty RK (1999) Growth performance of Penaeus monodon at different stocking densities. J Inland Fish Soc India 31:53–59Google Scholar
  63. Olmos J, Ochoa L, Paniagua-Michel J, Contreras R (2011) Functional feed assessment on Litopenaeus vannamei using 100% fish meal replacement by soybean meal, high levels of complex carbohydrates and Bacillus probiotic strains. Mar Drugs 9:1119–1132CrossRefGoogle Scholar
  64. Olsen RL, Hasan MR (2012) A limited supply of fishmeal: impact on future increases in global aquaculture production. Trends Food Sci Technol 27:120–128CrossRefGoogle Scholar
  65. Patnaik S, Samocha TM, Davis DA, Bullis RA, Browdy CL (2006) The use of HUFA rich algae meals in diets for Litopenaeus vannamei. Aquac Nutr 12:395–401CrossRefGoogle Scholar
  66. Plínio SF, Luis HP, Wilson W (2015) The effect of different alkalinity levels on Litopenaeus vannamei reared with biofloc technology (BFT). Aquac Int 23:345–358CrossRefGoogle Scholar
  67. Ray JA, Lewis BL, Browdy CL, Leffler JW (2010) Suspended solids removal to improve shrimp, Litopenaeus vannamei, production and an evaluation of a plant-based feed in minimal exchange, super intensive culture systems. Aquaculture 299:89–98CrossRefGoogle Scholar
  68. Ray JA, Dillon KS, Lotz JM (2011) Water quality dynamics and shrimp (Litopenaeus vannamei) production in intensive, mesohaline culture systems with two levels of biofloc management. Aquac Eng 45:127–136CrossRefGoogle Scholar
  69. Rosas C, Cuzon G, Gaxiola G, Arena L, Lemaire P, Soyez C, Van Wormhoudt A (2000) Influence of dietary carbohydrate on the metabolism of juvenile Litopenaeus stylirostris. J Exp Mar Biol Ecol 24:181–198CrossRefGoogle Scholar
  70. Sá M, Sabry Neto H, Cordeiro Júnior E, Nunes A (2013) Dietary concentration of marine oil affects replacement of fish meal by soy protein concentrate in practical diets for the white shrimp, Litopenaeus vannamei. Aquac Nutr 19:199–210CrossRefGoogle Scholar
  71. Samocha TM, Davis DA, Saoud PI, De Bault K (2004a) Substitution of fishmeal by co-extruded soybean poultry by-product meal in practical for the Pacific white shrimp, Litopenaeus vannamei. Aquaculture 231:197–203CrossRefGoogle Scholar
  72. Samocha TM, Lawrence AL, Collins CA, Castille FL, Bray WA, Davies CJ, Lee PG, Wood GF (2004b) Production of the Pacific white shrimp, Litopenaeus vannamei, in high-density greenhouse-enclosed raceways using low salinity groundwater. J Appl Aquac 15:1–19CrossRefGoogle Scholar
  73. Shahkar E, Yun H, Park G, Jang IK, Kim S, Katya K, Bai SC (2014) Evaluation of optimum dietary protein level for juvenile whiteleg shrimp, Litopenaeus vannamei. J Crustac Biol 34:552–558CrossRefGoogle Scholar
  74. Sharawya Z, Godab AMA-S, Hassaan MS (2016) Partial or total replacement of fish meal by solid state fermented soybean meal with Saccharomyces cerevisiae in diets for Indian prawn shrimp, Fenneropenaeus indicus. Postlarvae 212:90–99Google Scholar
  75. Silverman GA, Bird PI, Carrell RW, Church FC, Coughlin PB, Gettins PG, Irving JA, Lomas DA, Luke CJ, Moyer RW, Pemberton PA, Remold-O’Donnell E, Salvesen GS, Travis J, Whisstock JC (2001) The serpins are an expanding superfamily of structurally similar but functionally diverse Proteins. J Biol Chem 276:33293–33296CrossRefGoogle Scholar
  76. Sookying D, Davis DA, Soller Dias Da Silva F (2013) A review of the development and application of soybean-based diets for Pacific white shrimp Litopenaeus vannamei. Aquac Nutr 19:441–448CrossRefGoogle Scholar
  77. Suárez JA, Gaxiola G, Mendoza R, Cadavid S, Garcia G, Alanis G, Suárez A, Faillace J, Cuzon G (2009) Substitution of fish meal with plant protein sources and energy budget for white shrimp Litopenaeus vannamei (Boone, 1931). Aquaculture 289:118–123CrossRefGoogle Scholar
  78. Tacon AGJ, Barg UC (1998) Major challenges to feed development for marine and diadromous finfish and crustacean species. In: De Silva SS (ed) Tropical mariculture. Academic, San Diego, pp 171–208CrossRefGoogle Scholar
  79. Valle BCS, Dantas EM, Silva JFX, Bezerra RS, Correia ES, Peixoto SRM, Soares RB (2015) Replacement of fishmeal by fish protein hydrolysate and biofloc in the diets of Litopenaeus vannamei postlarvae. Aquac Nutr 21:105–112CrossRefGoogle Scholar
  80. Van Wyk P, Scarpa J (1999) Water quality and management. In: Van Wyk P (ed) Farming marine shrimp in recirculating freshwater systems. Florida Department of Agriculture and Consumer Services, Tallahassee, pp 128–138Google Scholar
  81. Venou B, Alexis MN, Fountoulaki E, Haralabous J (2006) Effects of extrusion and inclusion level of soybean meal on diet digestibility, performance and nutrient utilization of gilthead sea bream (Sparus aurata). Aquaculture 261:343–356CrossRefGoogle Scholar
  82. Wasielesky W, Atwood H, Stokes A, Browdy CL (2006) Effect of natural production in a zero exchange suspended microbial floc based super-intensive culture system for white shrimp, Litopenaeus vannamei. Aquaculture 258:396–403CrossRefGoogle Scholar
  83. Xia S, Li Y, Wang W, Rajkumar M, Paramasivam K, Vasagam K, Wang H (2010) Influence of dietary protein on growth, digestibility, digestive enzyme activity and stress tolerance in white leg shrimp, Litopenaeus vannamei (Boone, 1931), reared in high-density tank trials. Aquac Res 411:1845–1854CrossRefGoogle Scholar
  84. Xie S, Liu Y, Zeng S, Niu J, Tian L (2016) Partial replacement of fish-meal by soy protein concentrate and soybean meal based protein blend for juvenile Pacific white shrimp, Litopenaeus vannamei. Aquaculture 464:296–302CrossRefGoogle Scholar
  85. Xu WJ, Pan LQ (2012) Effects of bioflocs on growth performance, digestive enzyme activity and body composition of juvenile Litopenaeus vannamei in zero-water exchange tanks manipulating C/N ratio in feed. Aquaculture 356–357:147–152Google Scholar
  86. Xu WJ, Pan LQ, Zhao DH, Huang J (2012) Preliminary investigation into the contribution of bioflocs on protein nutrition of Litopenaeus vannamei fed with different dietary protein levels in zero-water exchange culture tanks. Aquaculture 350–353:147–153Google Scholar
  87. Xu W, Timothy CM, Tzachi MS (2016) Effects of C/N ratio on biofloc development, water quality, and performance of Litopenaeus vannamei juveniles in a biofloc-based, high-density, zero-exchange, outdoor tank system. Aquaculture 453:169–175CrossRefGoogle Scholar
  88. Yang Q, Zhou X, Zhou Q, Tan B, Chi S, Dong X (2009) Apparent digestibility of selected feed ingredients for white shrimp Litopenaeus vannamei, Boone. Aquac Res 41:78–86CrossRefGoogle Scholar
  89. Ye JD, Wang K, Li FD, Sun YZ, Liu XH (2011) Incorporation of a mixture of meat and bone meal, poultry by-product meal, blood meal and corn gluten meal as a replacement for fish meal in practical diets of Pacific white shrimp Litopenaeus vannamei at two dietary protein levels. Aquac Nutr 17:337–347CrossRefGoogle Scholar
  90. Yu GH, He PJ, Shao LM, Zhu YS (2009) Enzyme extraction by ultrasound from sludge flocs. J Environ Sci 21:204–210CrossRefGoogle Scholar
  91. Yue YR, Liu YJ, Tian LX, Gan L, Yang HJ, Liang GY (2012) Effects of replacing fish meal with soybean meal and peanut meal on growth, feed utilization and haemolymph indexes for juvenile white shrimp, Litopenaeus vannamei, Boone. Aquac Res 43:1687–1696CrossRefGoogle Scholar
  92. Zhou QC, Tan BP, Mai KS, Liu YJ (2004) Apparent digestibility of selected feed ingredients for juvenile cobia, Rachycentron canadum. Aquaculture 241:441–451CrossRefGoogle Scholar

Copyright information

© The Author(s) 2017

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Hyeonho Yun
    • 1
  • Erfan Shahkar
    • 2
  • Ali Hamidoghli
    • 2
  • Seunghan Lee
    • 2
  • Seonghun Won
    • 2
  • Sungchul C. Bai
    • 2
  1. 1.Department of Life, Food and IngredientsCJ Cheiljedang CenterSeoulRepublic of Korea
  2. 2.Department of Marine Bio-materials and Aquaculture/Feeds and Foods Nutrition Research CenterPukyong National UniversityBusanRepublic of Korea

Personalised recommendations