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Citation of this paper

Impact of substituting soybean meal with organic acid treated shrimp waste meal on the performance and egg quality of laying hens

Md. Aliar Rahman and Rakhi Chowdhury

Department of Animal Nutrition, Faculty of Animal Husbandry, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh
rakhich03_bau@bau.edu.bd

Abstract

This study aimed to assess the consequences of replacing soybean meal (SBM) with shrimp waste meal (SWM) in laying hens diets, with an emphasis on the performance and egg quality. Two hundred and fifty LOHMANN Brown laying hens were randomly assigned to diets containing formic acid treated SWM (FSWM) at the levels of 0%, 25%, 50%, 75% and 100% in place of SBM for 11 weeks (25 to 36 weeks of age). As the levels of FSWM in diet increased, feed intake, hen-day egg production, egg weight and egg mass decreased (p<0.01) linearly; the best and worst outcomes were revealed in the 0% and 100% FSWM diets, respectively(p<0.01). A similar trend was observed for feed conversion ratio (p<0.01). Nevertheless, there was no significant difference in these variables between 0%, 25% and 50% FSWM (p>0.05). Interestingly, eggshell weight and thickness increased with increasing FSWM levels; however, there was no substantial difference between 50%, 75% and 100% FSWM levels. The yolk color became deeper with the increasing levels of dietary FSWM. Thus, it appears possible to use formic acid treated SWM in place of SBM up to 50%, or around 12%, of the total diet while maintaining laying ability and enhancing egg quality.

Key words: formic acid, production, eggshell, yolk color, soybean meal, shrimp waste meal


Introduction

Soybean meal (SBM) is the primary plant-based source of amino acids used as a common feed ingredient in the chicken diet. The dietary inclusion of it is contingent upon its nutritional value, market accessibility, costs and other factors (Pope et al 2024). The growing demand for SBM and its environmental impact have prompted increased efforts to explore alternative feedstuffs for chicken’s diet (Van and Oonincx 2017). Consequently, the use of agro-industrial protein rich by-products from local sources has received special attention. The potential of adding by-products such sunflower meals, brewer’s dry grain and wheat middlings to chickens diet have been shown in a number of earlier experiments (Rao et al 2006; Adedokun et al 2015; Adams et al 2022; Such et al 2024). However, because they have less lysine and methionine and more fiber than SBM, their use is restricted (Saleh et al 2021; Lannuzel et al 2023; Njeri et al 2023) in chickens’ diet. Alternatively, shrimp by-product, considered also as shrimp waste (head and hull) are nutrient-rich, especially in protein, which is comparable to quality fishmeal or better than SBM and relatively cheap in price (Ababor et al 2023).

It is well known that shrimp are among the most widely consumed seafoods in the world. However, 40% of each shrimp is discarded (AlFaris et al 2022), which is either openly disposed of in landfills or released into the ocean, leading to environmental pollution that impacts both the economy and the livelihoods of local communities. It is worth noting that this shrimp waste is rich in crude protein, with an approximate content of 48-52%; however, the presence of a comparatively large amount of ash (16-23%) and an anti-nutritional factor chitin (12-16%), limits its use in animal feed in high amount, especially in chickens feed (Rahman and Koh 2014). Chitin can interfere with the activity of digestive enzymes responsible for breaking down proteins, leading to decreased digestibility when shrimp waste meal (SWM) is included in diets (Khempaka et al 2006b). In response, various strategies have been explored to enhance the nutritional value and safety of the use of SWM in chickens’ diet. The digestibility and nutritional content of SWM were reported to have significantly improved following chemical treatment with either acids or alkali (Fox et al 1994; Oduguwa et al 1998; Rahman and Koh 2016a) and biological treatment with either beneficial bacteria or fungi (Abun et al 2022; Djunaidi et al 2009); and led to significant improvement in chickens performance when treated SWM was added to the diet, rather than the untreated one (Septinova et al 2010; Jegede et al 2006). When it comes to safety and health concerns, organic acids are better to employ in chicken diets than inorganic ones; and among the commonly used organic acids formic acid is European Union approved feed additive for use in feed for all animal species and its use in animal nutrition is environmentally safe (EFSA 2014; Chowdhury et al 2024).).

Findings, however, vary, particularly when it comes to the nutritional improvement of SWM after treatment and suggested level of SWM for optimum performance of chickens. Additionally, there is limited information available regarding the use of treated SWM in laying hens diet. Consequently, this study was carried out preliminarily to know the nutritional changes that occurred in SWM after treatment using organic acid (formic acid) and, most importantly, to assess the impact of using this formic acid treated SWM (FSWM) as a substitute for SBM taking into account the laying performances and egg quality.


Materials and methods

The experimental protocol for laying hen handling and sample collection was approved by the Ethical Standards of the Research Committee (ESRC) at the Bangladesh Agricultural University Research System (BAURES), BAU, Mymensingh, Bangladesh (BAURES/ESRC/AH/44).

Collection of shrimp waste and preparation of shrimp waste meal

Sun dried shrimp waste (Photo 1) consist of head and hulls of available shrimp in Bangladesh called as “Chaka Shrimp”, scientific name Penaeus indicus, was purchased and screened for the presence of foreign particles, to avoid the adulteration. Before treatment, samples of the purchased shrimp waste was kept separately and grinded for the chemical analysis, which was considered as untreated SWM (Photo 2) and used for the determination of chemical composition. Later, the collected shrimp waste was treated by using an organic acid, namely formic acid following the method described by Rahman and Koh (2016a) with slight modification. Briefly, 100 g shrimp waste was suspended in 300 ml of 5% formic acid solution at room temperature for 30 minutes, then filtered by using a cheese cloth and wasted with distilled water to adjust the pH. After that, the solid residue was collected, properly sun dried and grinded to pass through 1.0 mm mesh screen, which was then considered as FSWM (Photo 2).

Photo 1. Untreated shrimp waste Photo 2. Untreated and formic acid-treated shrimp waste meal
Diets and experimental procedure

Corn-SBM based basal diet was formulated to fulfil the nutrient requirement of laying hens during the experimental period following the guideline of LOHMANN TIERZUCHT GmbH, Germany. The SBM in basal diet was replaced by different levels (0%, 25%, 50%, 75% and 100%) of FSWM. Two hundred and fifty LOHMANN Brown Laying hen strain were randomly assigned to diets consisting of FSWM at different levels for a period of 11 weeks (from 25 to 36 weeks of age); the first week was devoted to diet adaptation, while the following ten weeks were used to gather data. Diets and water were provided on ad libitum basis throughout the whole period.

Daily records were kept of egg number, weight and hens mortality (if any), as well as feed consumption (feed supplied against feed orts). Eggs were examined for quality determination such as, eggshell weight and thickness was measured using electronic balance and screw gauge, respectively. Haugh unit was measured using a formula (Rahman et al 2021). Yolk color was measured using Roche Yolk Color Fan.

Table 1. Ingredients and chemical composition of experimental diets

Ingredients (%)

% FSWM1

0

25

50

75

100

Corn

57.80

58.50

59.00

59.50

60.00

Soybean meal

24.00

18.0

12.00

6.00

0.00

FSWM

0.00

6.00

12.00

18.00

24.00

Limestone

8.90

8.40

8.00

7.50

7.00

Di-calcium phosphate2

1.60

1.40

1.30

1.30

1.30

Protein concentrate

2.40

2.40

2.40

2.40

2.40

Rice polish

3.00

3.00

3.00

3.00

3.00

Oil

1.30

1.30

1.30

1.30

1.30

Lysine

0.10

0.10

0.10

0.10

0.10

Methionine

0.20

0.20

0.20

0.20

0.20

Layer premix3

0.22

0.22

0.22

0.22

0.22

Common salt

0.25

0.25

0.25

0.25

0.25

Coccidiostat

0.10

0.10

0.10

0.10

0.10

Toxin binder

0.10

0.10

0.10

0.10

0.10

Phytase

0.02

0.02

0.02

0.02

0.02

Salmonella killer

0.01

0.01

0.01

0.01

0.01

Chemical composition (% on DM basis)

Crude protein

16.11

16.12

16.10

16.08

16.05

Lysine4

0.88

0.96

1.04

1.12

1.19

Methionine4

0.44

0.54

0.63

0.73

0.83

Linolenic acid4

1.41

1.53

1.57

1.62

1.67

Crude fiber

4.42

4.84

5.23

5.62

6.02

Calcium

3.51

3.74

4.02

4.29

4.56

Available phosphorus4

0.37

0.38

0.41

0.45

0.50

ME (Kcal/Kg feed)4

2723

2719

2721

2724

2717

10% formic acid treated-shrimp waste meal (FSWM): 24% SBM + 0% FSWM, 25% FSWM: 18% SBM + 6.0% FSWM, 50% FSWM: 12% SBM + 12.0% FSWM, 75% FSWM: 6% SBM + 18.0 % FSWM, 100% FSWM: 0% SBM + 24.0 % FSWM.218% granular phosphate and 23% calcium.3Vitamin A 12,000 IU, vitamin D3 3,200 IU, vitamin E 40 mg, vitamin B 1 2 mg, vitamin B 2 5 mg, vitamin B12 0.02 mg, niacin 40 mg, biotin 0.075 mg, folic acid 2 mg, pantothenic acid 12 mg, manganese 100 mg, zinc 600 mg, iron 30 mg, copper 10 mg, iodine 1 mg, selenium 0.2 mg.4Calculated value.
Calculation, chemical and statistical analysis

Egg mass, feed conversion ratio (FCR), hen-day egg production (HDEP) were calculated using the following formula mentioned by Rahman et al (2021). Untreated and treated SWM and diets were analyzed for the proximate composition following the standard methods (AOAC 2005). Chitin content was measured according to the method of Ghanem et al (2003). Data obtained from chemical analysis and experimental periods were analyzed by SPSS 22 via one way ANOVA. Statistical significance among the treatment groups were determined using Tukey's multiple comparison tests at a significant level of 5% while orthogonal polynomial contrasts were used to evaluate linear and quadratic effects of different levels of FSWM. The results were reported as mean and overall p-values and statistical significance was taken at p<0.05.


Results

Nutritional value of untreated and formic acid-treated SWM

When SWM was treated with 5% formic acid, the quantity of crude fiber (CF), ash and chitin decreased (Figure 1). Comparing FSWM to untreated SWM, the reduction percentages for CF, ash and chitin were approximately 16%, 28% and 15%, respectively. It is noteworthy that FSWM had roughly 13% more crude protein (CP) than untreated SWM.

Figure 1. Nutritional value of untreated and formic acid-treated shrimp waste meal


Figure 2. Effect of feeding formic acid treated shrimp waste meal (FSWM) replacing soybean meal on egg production per day of laying
hens 0% FSWM (Control): 24 kg SBM + 0 kg FSWM; 25% FSWM: 18 kg SBM + 6.0 kg FSWM; 50% FSWM: 12 kg
SBM + 12 kg FSWM; 75% FSWM: 6 kg SBM + 18 kg FSWM; 100% FSWM: 0 kg SBM + 24 kg FSWM
Performance

HDEP, feed intake, egg mass and egg weight all declined with increasing the levels (0%, 25%, 50%, 75% and 100%) of FSWM in diets; the worst results were observed at the 100% FSWM level (p<0.01; Table 2). Though hens fed 0%, 25% and 50% FSWM diets showed almost similar HDEP (p>0.05), the production dropped sharply (p<0.05) in 75% and 100% FSWM added diets (Figure 2). The maximum acceptable level for egg weight was found to be 25% FSWM inclusion by replacing SBM (Figure 3), while the optimum inclusion level for feed intake, egg mass and egg weight were observed to be 50% FSWM inclusion by replacing SBM with no discernible difference with 0% and 25% replacement (p>0.05). Increases in FSWM levels in laying hen diets resulted in poor FCR; the diets with 0% and 100% FSWM had the best and worst FCR values, respectively (p<0.01). The FCR value of 50% FSWM was statistically similar to that of 25% FSWM and 0% FSWM (p>0.05).

Table 2. Effect of feeding replacing soybean meal (SBM) with shrimp waste meal formic acid-treated shrimp waste meal (FSWM) on performance of laying hens

Variables (g/h/d)

% FSWM

p-value

0

25

50

75

100

% Egg production, h/d

91.44a

91.11a

90.78a

85.45b

81.11c

<0.01

Feed intake

115a

114a

113a

108b

104c

<0.01

Egg weight

65.22a

64.05a

62.83ab

60.5bc

58.32c

<0.01

Egg mass

59.62a

58.35a

57.05a

51.74b

47.31c

<0.01

FCR (egg basis)

1.93a

1.96a

1.98a

2.09b

2.20c

<0.01

0% FSWM (Control): 24 kg SBM + 0 kg FSWM; 25% FSWM: 18 kg SBM + 6.0 kg FSWM; 50% FSWM: 12 kg SBM + 12 kg FSWM; 75% FSWM: 6 kg SBM + 18 kg FSWM; 100% FSWM: 0 kg SBM + 24 kg FSWM;abcMeans different superscripts in the same column showed significantly different results (p<0.05); g: gram; h: hen; d: day; FCR: feed conversion ratio.


Figure 3. Effect of feeding formic acid treated shrimp waste meal (FSWM) replacing soybean meal on egg weight of laying
hens 0% FSWM (Control): 24 kg SBM + 0 kg FSWM; 25% FSWM: 18 kg SBM + 6.0 kg FSWM; 50% FSWM: 12 kg
SBM + 12 kg FSWM; 75% FSWM: 6 kg SBM + 18 kg FSWM; 100% FSWM: 0 kg SBM + 24 kg FSWM
Egg quality

The different levels of FSWM in the diets of laying hens had a significant impact on the external quality of the eggs (shell weight and thickness); however, internal quality (Haugh unit) remained unaffected (data not shown, Table 3). Shell thickness (mm), weight (g & %) increased (p<0.01) depending on the FSWM levels. Although there were no significant differences between the 50%, 75% and 100% FSWM diets, the 100% FSWM diet had the highest values for these variables. The most interesting finding was that the yolk color value rose (p<0.01) as FSWM levels in diets increased. Hens given 50% and 100% FSWM diets had nearly 18% and 34% higher yolk color value, respectively, than those fed 0% FSWM diet.

Table 3. Effect of feeding replacing soybean meal (SBM) with shrimp waste meal formic acid-treated shrimp waste meal (FSWM) on egg quality of laying hens

Variables

% FSWM

p -value

0

25

50

75

100

Shell thickness (mm)

0.33c

0.35b

0.37ab

0.38a

0.38a

<0.01

Shell weight (g)

6.95c

7.25b

7.38a

7.40a

7.43a

<0.01

Shell weight (%)

10.66c

11.32b

11.76ab

12.24a

12.75a

<0.01

Yolk color

5.32d

6.15c

6.31bc

6.51b

7.14a

<0.01

0% FSWM (Control): 24 kg SBM + 0 kg FSWM; 25% FSWM: 18 kg SBM + 6.0 kg FSWM; 50% FSWM: 12 kg SBM + 12 kg FSWM; 75% FSWM: 6 kg SBM + 18 kg FSWM; 100% FSWM: 0 kg SBM + 24 kg FSWM;abcdMeans different superscripts in the same column showed significantly different results (p<0.05)


Discussion

According to the present study, the nutritional quality of SWM was improved by organic acid treatment and the improvement was observed through the lower levels of crude fiber, ash and chitin in FSWM when compared to the untreated one. The reduction of chitin content was one of the main purposes of this study, since chitin was found to impair the overall performance of commercial chicken. However, the introduction of formic acid-treated SWM to the diet, instead of untreated SWM, restored the declining performance (Rahman and Koh 2016b). Notably, chitosan extraction from SWM chitin is currently receiving more industrial attention. According to a study by Islam et al (2016) chitin and chitosan can be recovered from SWM using chemical techniques like alkali (sodium hydroxide) and acid (hydrochloric acid). This means that treating SWM with either acid or alkali dilutes the complex structure of chitin and releases it along with other molecules, increasing the availability of nutrients and its overall digestibility. The higher CP content compared to the corresponding value in the untreated SWM in current study exhibits the efficiency of organic acid in releasing CP from the protein-minerals complex in the shrimp exoskeleton structure. The decreased ash content in FSWM may provide credible evidence of mineral matter leaching during the acid treatment of SWM. Rahman and Koh (2014) suggest that treating SWM using either organic or inorganic acids could enhance its nutritional content; however, the rate of improvement was higher for organic acids than for inorganic ones. It was also reported that bioprocessing, or treating SWM with microorganisms, improved the quality of SWM by raising its CP and lowering its CF level (Abun et al 2021; Septinova et al 2010). The nutritional composition of SWM is related to the shrimp species studied and mainly the proportions of head and shell (Dang et al 2018). However, it was observed that efficiency of organic acid treatment to improve the nutritional quality of SWM was better than inorganic acid treatment and comparable to microorganism treatment.

In the present study, feed intake was decreased by 1%, 2%, 8% and 10% in hens given 25%, 50%, 75% and 100% FSWM added diets, respectively, compared with diets contained 0% FSWM. It is mentionable that diets with higher levels of FSWM (75% and 100%) possess a higher percentage of chitin, which may be the most considerable reason for this decreased feed intake in laying hens along with the strong smell of shrimp in the diets. The decreased feed intake resulted in lower egg weight, egg mass and poor FCR values in laying hens given 75% and 100% FSWM diets. This might be explained by the fact that diets with high levels of FSWM contain a high percentage of chitin, which reduces the diet's digestibility and raise FCR. The results of Orthogonal Polynomial revealed that feed intake and egg weight decreased linearly with the increasing levels of FSWM (p<0.01). A similar trend was found in case of egg mass and FCR values; however, these two parameters also experienced significant quadratic effect (p=0.01). Poor growth performance and nutrient digestibility of broilers fed chitin or SWM were previously reported and it was also mentioned that the performance and digestibility became worse with the increasing level of shrimp meal and chitin (Kempaka et al 2006a). In another report Abun et al (2022) mentioned that adding fermented shrimp waste products to feed up to 10% in the diet can help native chickens grow and achieve a high carcass weight. In hens fed 75% and 100% FSWM diets, HDEP dropped by roughly 7% and 11%, respectively, but in hens fed 50% FSWM diet, it dropped by less than 1%. According to the performance variable results of the current study, it may be possible to replace up to 50% of SBM with FSWM, or roughly 12% of the diet, in order to achieve the optimal production results from laying hens.

The use of FSWM at different levels showed a significant influence (p<0.01) on egg quality in terms of eggshell thickness, weight and yolk color. The Orthogonal Polynomial test revealed that while the egg yolk color was significantly impacted linearly, the thickness and weight of the shell were significantly impacted quadratically. Substitution of SBM with FSWM caused an approximate 6%–15% increase in eggshell thickness, a 4%–7% rise in eggshell weight and a 15%–34% high yolk color intensification. While some researchers have observed good benefits of processed shrimp waste on egg quality (Abun et al 2022; Fileto et al 2022; Carranco-Jáuregui et al 2006), there is still debate about how much of it may be used in a diet. According to the current study the best outcomes are obtained when FSWM is used at a 50% substitution rate for SBM or 12% dietary intake in relation to egg quality in laying hens.

It might be feasible to lessen the reliance on SBM in chicken diets by using quality SWM. Additionally, this also has environmental and social benefits, as it is well known that the deposition of shrimp waste into the environment increases the biochemical oxygen demand and its degradation produces a strong odor (Abuzar et al 2023). Proper utilization of shrimp waste may also help to reduce the burden on the earth and decrease environmental pollution.


Conclusions


Acknowledgement

The authors gratefully acknowledge the Ministry of Science and Technology (MoST) Bangladesh, for providing financial support for this research (Project ID: SRG-221059/2022-23). The authors also extend their appreciation to the Department of Animal Nutrition, Bangladesh Agricultural University, for its valuable assistance.


References

Ababor S, Tamiru M, Alkhtib A, Wamatu J, Kuyu C G, Teka T A, Terefe L A and Burton E 2023 The use of biologically converted agricultural byproducts in chicken nutrition. Sustainability, 15, 14562. https://doi.org/10.3390/su151914562 .

Abun A, Widjastuti T and Haetami K 2021 The effect of fermented shrimp waste in the ration on the performance of local chickens. Global Academic Journal of Agriculture and Bio Sciences, 3, 6, 85-91. https://doi.org/10.36348/gajab.2021.v03i06.001.

Abun A, Haetami K and Widjastuti T 2022 The effect of feed containing fermented shrimp waste on the conversion of protein, carcass weight and abdominal fat of native chicken. World Journal of Biology Pharmacy and Health Sciences, 9, 1, 46-53. https://doi.org/10.30574/wjbphs.2022.9.1.0027.

Abuzar, Sharif H R, Sharif M K, Arshad R, Rehman A, Ashraf W, Karim A, Awan K A, Raza H, Khalid W and Asar T O 2023 Potential industrial and nutritional applications of shrimp by-products: a review. International Journal of Food Properties, 26, 2, 3407-3432. https://doi.org/10.1080/10942912.2023.2283378.

Adams C B, Souza O, Agilar J C, Muller G, Rodrigues B and Stefanello C 2022 Energy values of brewer’s grains and olive pomace waste for broiler chickens determined using the regression method. Agriculture, 12, 444. http://dx.doi.org/10.3390/agriculture12040444.

Adedokun S A, Jaynes P, Payne R L and Applegate T J 2015 Standardized ileal amino acid digestibility of corn, corn distillers’ dried grains with solubles, wheat middlings and bakery by-products in broilers and laying hens. Poultry Science, 94, 10, 2480-2487. https://doi.org/10.3382/ps/pev226.

AlFaris N A, Alshammari G M, AlTamimi J Z, AlMousa L A, Alagal R I, AlKehayez N M, Aljabryn D H, Alsayadi M M and Yahya M A 2022 Evaluating the effects of different processing methods on the nutritional composition of shrimp and the antioxidant activity of shrimp powder. Saudi Journal of Biological Sciences, 29, 1, 640-649. https://doi.org/10.1016/j.sjbs.2021.09.029.

Association of Official Analytical Chemists (AOAC) 2005 Official methods of analysis, 18th ed. Arlington (VA).

Carranco-Jáuregui M E, Sanginés-García L, Morales-Barrera E, Carrillo-Domínguez S, Ávila-González E, Ramírez-Poblano M and Pérez-Gil Romo F 2006 Shrimp head meal in laying hen rations and its effects on fresh and stored egg quality. Interciencia, 31, 11, 822-827.

Chowdhury R, Rahman M A, Islam K M S and Al-Mamun M 2024 A comparative study on the effects of fungal and bacterial phytase with or without citric acid on growth performance, serum mineral profile, bone quality and nutrient retention in broilers. Journal of Advanced Veterinary and Animal Research, 11, 2, 376-383. https://doi.org/10.5455/javar.2024.k786.

Dang T T, Gringer N, Jessen F, Olsen K, Bøknæs N, Nielsen P L and Orlien V 2018 Emerging and potential technologies for facilitating shrimp peeling: A review. Innovative Food Science & Emerging Technologies, 45, 228-40. http://dx.doi.org/10.1016/j.ifset.2017.10.017.

Djunaidi I H, Yuwanta T and Nurcahyanto M 2009 Effects of inclusion Aspergillus niger fermented shrimp waste meal in broiler diets on live performance and digestive organ weight. Indonesian Journal of Animal and Veterinary Sciences, 14, 2, 104-109.

EFSA (The European Food Safety Authority) Panel on Additives and Products or Substances used in Animal Feed 2014 Scientific Opinion on the safety and efficacy of formic acid when used as a technological additive for all animal species. EFSA Journal, 12, 10, 3827.

Fileto J B, Freitas E R, Nepomuceno R C, Gomes T R, Silva V S, dos Santos E O, de Souza O F, Watanabe G C and de Oliveira P J 2022 Nutritional evaluation of shrimp waste and its inclusion in laying diet for European quails. Research Square, 1. https://doi.org/10.21203/rs.3.rs-2199393/v1.

Fox C J, Blow P, Brown J H and Watson I 1994 The effect of various processing methods on the physical and biochemical properties of shrimp head meals and their utilization by juvenile Penaeus monodon Fab. Aquaculture, 122, 3, 209-226. https://doi.org/10.1016/0044-8486(94)90511-8.

Ghanem A, Ghaly A E and Chaulk M 2003 Effect of shrimp processing procedures on the quality and quantity of extracted chitin from the shells of northern shrimp Pandalus borealis. Journal of Aquatic Food Product Technology, 12, 4, 63-79. http://dx.doi.org/10.1300/J030v12n04_05.

Islam S Z, Khan M and Alam A K M N 2016 Production of chitin and chitosan from shrimp shell wastes. Journal of Bangladesh Agricultural University, 14, 2, 253-259. https://doi.org/10.3329/bjsir.v45i4.7330.

Jegede A V, Oduguwa O O, Fanimo A O, Bamgbose A M and Agunbiade J A 2006 Effect of processing methods on the utilization of shrimp waste by broiler chickens. Nigerian Journal of Animal Production, 33, 1, 23-39. https://doi.org/10.51791/njap.v33i1.1487.

Khempaka S, Koh K and Karasawa Y 2006a Effect of shrimp meal on growth performance and digestibility in growing broilers. The Journal of Poultry Science, 43, 3, 250-254. https://doi.org/10.2141/jpsa.43.250.

Khempaka S, Mochizuki M, Koh K and Karasawa Y 2006 Effect of chitin in shrimp meal on growth performance and digestibility in growing broilers. The Journal of Poultry Science, 43, 4, 339-343. https://doi.org/10.2141/jpsa.43.339.

Lannuzel C, Smith A, Mary A L, Della Pia E A, Kabel M A and De Vries S 2022 Improving fiber utilization from rapeseed and sunflower seed meals to substitute soybean meal in pig and chicken diets: A review. Animal Feed Science and Technology, 285, 115213. https://doi.org/10.1016/j.anifeedsci.2022.115213.

Njeri F M, Patterson R, Gachuiri C K and Kiarie E G 2023 Effects of pretreating wheat middlings and sunflower meal with fiber degrading enzymes on components solubilization and utilization in broiler chickens. Translational Animal Science, 7, 1, txad108. https://doi.org/10.1093/tas/txad108.

Oduguwa O O, Fanimo A O, Iyayi E A, Kalejaiye O O and Oyekola O A 1998 Preliminary studies on the effects of different processing methods on the nutritive value of shrimp waste meal. Nigerian Journal of Animal Production, 25, 2, 139-144. https://doi.org/10.51791/njap.v25i2.2184.

Pope M, Boyd R D, Holzgraefe D, Monaco H and Sifri M 2024 Economic value and environmental impact of soybean meal in poultry and swine diets. Journal of Applied Poultry Research, 33, 3, 100449. https://doi.org/10.1016/j.japr.2024.100449.

Rahman M and Koh K 2014 Nutritional quality and in vitro digestibility of shrimp meal made of heads and hulls of black tiger (Penaeus monodon), white leg (Litopenaeus vannamei) and argentine red (Pleoticus muelleri) shrimps. The Journal of Poultry Science, 51, 4, 411-415. https://doi.org/10.2141/jpsa.0140002.

Rahman M and Koh K 2016a Improvement in nutritional quality of shrimp meal with autoclave and chemical treatments: an in vitro study. The Journal of Poultry Science, 53, 2, 124-127. https://doi.org/10.2141/jpsa.0150128.

Rahman M and Koh K 2016b Effects of formic acid-treated shrimp meal on growth performance and nutrient digestibility in broilers.The Journal of Poultry Science, 53, 3, 208-212. https://doi.org/10.2141/jpsa.0160015.

Rahman MA, Ray D, Redoy MRA and Al-Mamun M 2021 Dose titration of herbs mixture powder supplementation on laying performance and egg quality in commercial layer chicken. Livestock Research for Rural Development, 33, 1. https://www.lrrd.org/lrrd33/1/aliar3313.html.

Rama Rao SV, Raju MV, Panda AK and Reddy MR 2006 Sunflower seed meal as a substitute for soybean meal in commercial broiler chicken diets. British Poultry Science, 47, 5, 592-598. https://doi.org/10.1080/00071660600963511.

Saleh A A, El-Awady A, Amber K, Eid Y Z, Alzawqari M H, Selim S, Soliman M M and Shukry M 2021 Effects of sunflower meal supplementation as a complementary protein source in the laying hen’s diet on productive performance, egg quality and nutrient digestibility. Sustainability, 13, 6, 3557. https://doi.org/10.3390/su13063557.

Septinova D, Kurtini T and Tantalo S 2010 Evaluation the usage of treated shrimp waste as protein source in broiler diet. Animal Production, 12, 1, 1-5.

Such N, Mezőlaki Á, Tewelde K G, Pál L, Horváth B, Poór J and Dublecz K 2024 Feeding sunflower meal with pullets and laying hens even at a 30% inclusion rate does not impair the ileal digestibility of most amino acids. Frontiers in Veterinary Science, 11, 1347374. https://doi.org/10.3389/fvets.2024.1347374.

Van Huis A and Oonincx D G 2017 The environmental sustainability of insects as food and feed. A review. Agronomy for Sustainable Development, 37, 43, 1-4. https://doi.org/10.1007/s13593-017-0452-8.