Assessment of Conventional and Low Gossypol Cottonseed Meal as Alternative Protein Sources in Low-Fishmeal Diets of Hybrid Grouper (Epinephelus fuscoguttatus♀× Epinephelus lanceolatus♂): Growth, Feed Utilization, Gut Histology, and Immunity
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethics
2.2. Experimental Diets
2.3. Growth Trial and Zootechnic Performance
2.4. Sampling and Analysis
2.4.1. Whole Body, White Muscle Composition, and Somatic Indices
2.4.2. Serum IgM and LZM Concentrations
2.4.3. Histological Analyses
2.4.4. Molecular Analysis (Real-Time Quantitative PCR Analysis of IGF-1)
2.5. Calculations
2.6. Statistical Analysis
3. Results
3.1. Survival and Zootechnic Performances
3.2. Somatic Indices
3.3. Whole-Body and White Muscle Compositions
3.4. Gut Histology
3.5. Expression of Hepatic IGF-1
3.6. Serum IgM and LZM Concentrations
4. Discussion
4.1. Zootechnic Performances
4.2. Whole-Body and White Muscle Compositions
4.3. Gut Micromorphology
4.4. Serum LZM and IgM Concentrations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Miles, R.D.; Chapman, F.A. The Benefits of Fish Meal in Aquaculture Diets. EDIS 2006. [Google Scholar] [CrossRef]
- Hossain, S.; Koshio, S.; Ishikawa, M.; Yokoyama, S.; Sony, N.M.; Islam, J.; Maekawa, M.; Fujieda, T. Substitution of dietary fishmeal by soybean meal with inosine administration influences growth, digestibility, immunity, stress resistance and gut morphology of juvenile amberjack Seriola dumerili. Aquaculture 2018, 488, 174–188. [Google Scholar] [CrossRef]
- Zarantoniello, M.; Pulido Rodriguez, L.F.; Randazzo, B.; Cardinaletti, G.; Giorgini, E.; Belloni, A.; Secci, G.; Faccenda, F.; Pulcini, D.; Parisi, G.; et al. Conventional feed additives or red claw crayfish meal and dried microbial biomass as feed supplement in fish meal-free diets for rainbow trout (Oncorhynchus mykiss): Possible ameliorative effects on growth and gut health status. Aquaculture 2022, 554, 738137. [Google Scholar] [CrossRef]
- Hill, J.C.; Alam, M.S.; Watanabe, W.O.; Carroll, P.M.; Seaton, P.J.; Bourdelais, A.J. Replacement of Menhaden Fish Meal by Poultry By-Product Meal in the Diet of Juvenile Red Porgy. N. Am. J. Aquac. 2019, 81, 81–93. [Google Scholar] [CrossRef] [Green Version]
- Randazzo, B.; Zarantoniello, M.; Cardinaletti, G.; Cerri, R.; Giorgini, E.; Belloni, A.; Contò, M.; Tibaldi, E.; Olivotto, I. Hermetia illucens and Poultry by-Product Meals as Alternatives to Plant Protein Sources in Gilthead Seabream (Sparus aurata) Diet: A Multidisciplinary Study on Fish Gut Status. Animals 2021, 11, 677. [Google Scholar] [CrossRef]
- Zhou, Z.; Yao, W.; Ye, B.; Wu, X.; Li, X.; Dong, Y. Effects of replacing fishmeal protein with poultry by-product meal protein and soybean meal protein on growth, feed intake, feed utilization, gut and liver histology of hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂) juveniles. Aquaculture 2020, 516, 734503. [Google Scholar] [CrossRef]
- Robinson, E.H.; Tiersch, T.R. Effects of Long-Term Feeding of Cottonseed Meal on Growth, Testis Development, and Sperm Motility of Male Channel Catfish Ictalurus punctatus Broodfish1. J. World Aquac. Soc. 1995, 26, 426–431. [Google Scholar] [CrossRef]
- Romano, G.B.; Scheffler, J.A. Lowering seed gossypol content in glanded cotton (Gossypium hirsutum L.) lines. Plant Breed. 2008, 127, 619–624. [Google Scholar] [CrossRef]
- Duodu, C.P.; Adjei-Boateng, D.; Edziyie, R.E.; Agbo, N.W.; Owusu-Boateng, G.; Larsen, B.K.; Skov, P.V. Processing techniques of selected oilseed by-products of potential use in animal feed: Effects on proximate nutrient composition, amino acid profile and antinutrients. Anim. Nutr. 2018, 4, 442–451. [Google Scholar] [CrossRef]
- Alam, M.S.; Watanabe, W.O.; Carroll, P.M.; Gabel, J.E.; Corum, M.A.; Seaton, P.; Wedegaertner, T.C.; Rathore, K.S.; Dowd, M.K. Evaluation of genetically-improved (glandless) and genetically-modified low-gossypol cottonseed meal as alternative protein sources in the diet of juvenile southern flounder Paralichthys lethostigma reared in a recirculating aquaculture system. Aquaculture 2018, 489, 36–45. [Google Scholar] [CrossRef]
- Anderson, A.D.; Alam, M.S.; Watanabe, W.O.; Carroll, P.M.; Wedegaertner, T.C.; Dowd, M.K. Full replacement of menhaden fish meal protein by low-gossypol cottonseed flour protein in the diet of juvenile black sea bass Centropristis striata. Aquaculture 2016, 464, 618–628. [Google Scholar] [CrossRef]
- Sullivan, J.A.; Reigh, R.C. Apparent digestibility of selected feedstuffs in diets for hybrid striped bass (Morone saxatilis ♀ × Morone chrysops ♂). Aquaculture 1995, 138, 313–322. [Google Scholar] [CrossRef]
- Cook, R.L.; Zhou, Y.; Rhodes, M.A.; Davis, D.A. Evaluation of various cottonseed products on the growth and digestibility performance in Florida pompano Trachinotus carolinus. Aquaculture 2016, 453, 10–18. [Google Scholar] [CrossRef]
- Hassaan, M.S.; El-Sayed, A.I.M.; Soltan, M.A.; Iraqi, M.M.; Goda, A.M.; Davies, S.J.; El-Haroun, E.R.; Ramadan, H.A. Partial dietary fish meal replacement with cotton seed meal and supplementation with exogenous protease alters growth, feed performance, hematological indices and associated gene expression markers (GH, IGF-I) for Nile tilapia, Oreochromis niloticus. Aquaculture 2019, 503, 282–292. [Google Scholar] [CrossRef]
- Su, J.; Hou, H.; Wang, C.; Luo, Y. Effects of replacing soybean meal with cottonseed meal on growth, muscle amino acids, and hematology of juvenile common carp, Cyprinus carpio. Aquac. Int. 2019, 27, 555–566. [Google Scholar] [CrossRef]
- Gómez-Requeni, P.; Mingarro, M.; Calduch-Giner, J.A.; Médale, F.; Martin, S.A.M.; Houlihan, D.F.; Kaushik, S.; Pérez-Sánchez, J. Protein growth performance, amino acid utilisation and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream (Sparus aurata). Aquaculture 2004, 232, 493–510. [Google Scholar] [CrossRef]
- Moriyama, S.; Ayson, F.G.; Kawauchi, H. Growth regulation by insulin-like growth factor-I in fish. Biosci. Biotechnol. Biochem. 2000, 64, 1553–1562. [Google Scholar] [CrossRef]
- Irm, M.; Taj, S.; Jin, M.; Timothée Andriamialinirina, H.J.; Cheng, X.; Zhou, Q. Influence of dietary replacement of fish meal with fish soluble meal on growth and TOR signaling pathway in juvenile black sea bream (Acanthopagrus schlegelii). Fish Shellfish Immunol. 2020, 101, 269–276. [Google Scholar] [CrossRef]
- Kumar, S.; Sándor Zs, J.; Nagy, Z.; Fazekas, G.; Havasi, M.; Sinha, A.K.; De Boeck, G.; Gál, D. Potential of processed animal protein versus soybean meal to replace fish meal in practical diets for European catfish (Silurus glanis): Growth response and liver gene expression. Aquac. Nutr. 2017, 23, 1179–1189. [Google Scholar] [CrossRef]
- Xu, M.; Wang, T.; Wang, J.; Wan, W.; Wang, Z.; Guan, D.; Sun, H. An evaluation of mixed plant protein in the diet of Yellow River carp (Cyprinus carpio): Growth, body composition, biochemical parameters, and growth hormone/insulin-like growth factor 1. Fish Physiol. Biochem. 2019, 45, 1331–1342. [Google Scholar] [CrossRef]
- Minghetti, M.; Drieschner, C.; Bramaz, N.; Schug, H.; Schirmer, K. A fish intestinal epithelial barrier model established from the rainbow trout (Oncorhynchus mykiss) cell line, RTgutGC. Cell Biol. Toxicol. 2017, 33, 539–555. [Google Scholar] [CrossRef] [Green Version]
- Estensoro, I.; Ballester-Lozano, G.; Benedito-Palos, L.; Grammes, F.; Martos-Sitcha, J.A.; Mydland, L.T.; Calduch-Giner, J.A.; Fuentes, J.; Karalazos, V.; Ortiz, Á.; et al. Dietary Butyrate Helps to Restore the Intestinal Status of a Marine Teleost (Sparus aurata) Fed Extreme Diets Low in Fish Meal and Fish Oil. PLoS ONE 2016, 11, e0166564. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Torrecillas, S.; Caballero, M.J.; Mompel, D.; Montero, D.; Zamorano, M.J.; Robaina, L.; Rivero-Ramírez, F.; Karalazos, V.; Kaushik, S.; Izquierdo, M. Disease resistance and response against Vibrio anguillarum intestinal infection in European seabass (Dicentrarchus labrax) fed low fish meal and fish oil diets. Fish Shellfish Immunol. 2017, 67, 302–311. [Google Scholar] [CrossRef]
- Bian, F.; Zhou, H.; He, G.; Wang, C.; Peng, H.; Pu, X.; Jiang, H.; Wang, X.; Mai, K. Effects of replacing fishmeal with different cottonseed meals on growth, feed utilization, haematological indexes, intestinal and liver morphology of juvenile turbot (Scophthalmus maximus L.). Aquac. Nutr. 2017, 23, 1429–1439. [Google Scholar] [CrossRef]
- Liu, H.; Dong, X.; Tan, B.; Du, T.; Zhang, S.; Yang, Y.; Chi, S.; Yang, Q.; Liu, H. Effects of fish meal replacement by low-gossypol cottonseed meal on growth performance, digestive enzyme activity, intestine histology and inflammatory gene expression of silver sillago (Sillago sihama Forsskál) (1775). Aquac. Nutr. 2020, 26, 1724–1735. [Google Scholar] [CrossRef]
- Cai, C.; Li, E.; Ye, Y.; Krogdahl, A.; Jiang, G.; Wang, Y.; Chen, L. Effect of dietary graded levels of cottonseed meal and gossypol on growth performance, body composition and health aspects of allogynogenetic silver crucian carp, Carassius auratus gibelio ♀ × Cyprinus carpio ♂. Aquac. Nutr. 2011, 17, 353–360. [Google Scholar] [CrossRef]
- Ye, G.; Dong, X.; Yang, Q.; Chi, S.; Liu, H.; Zhang, H.; Tan, B.; Zhang, S. Low-gossypol cottonseed protein concentrate used as a replacement of fish meal for juvenile hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂): Effects on growth performance, immune responses and intestinal microbiota. Aquaculture 2020, 524, 735309. [Google Scholar] [CrossRef]
- Wang, T.; Xu, M.; Wang, J.; Wan, W.; Guan, D.; Han, H.; Wang, Z.; Sun, H. A combination of rapeseed, cottonseed and peanut meal as a substitute of soybean meal in diets of Yellow River carp Cyprinus carpio var. Aquac. Nutr. 2020, 26, 1520–1532. [Google Scholar] [CrossRef]
- Yildirim, M.; Lim, C.; Wan, P.J.; Klesius, P.H. Growth performance and immune response of channel catfish (Ictalurus puctatus) fed diets containing graded levels of gossypol–acetic acid. Aquaculture 2003, 219, 751–768. [Google Scholar] [CrossRef]
- Holland, M.C.; Lambris, J.D. The complement system in teleosts. Fish Shellfish Immunol. 2002, 12, 399–420. [Google Scholar] [CrossRef] [Green Version]
- Anderson, D.P. Immunostimulants, adjuvants, and vaccine carriers in fish: Applications to aquaculture. Annu. Rev. Fish Dis. 1992, 2, 281–307. [Google Scholar] [CrossRef]
- Kiron, V. Fish immune system and its nutritional modulation for preventive health care. Anim. Feed Sci. Technol. 2012, 173, 111–133. [Google Scholar] [CrossRef]
- Wei, J.; Yu, N.; Tian, W.; Zhang, F.; Wu, Q.; Li, E.; Zhang, M.; Du, Z.; Qin, J.; Chen, L. Dietary vitamin B12 requirement and its effect on non-specific immunity and disease resistance in juvenile Chinese mitten crab Eriocheir sinensis. Aquaculture 2014, 434, 179–183. [Google Scholar] [CrossRef]
- Prager, E.M.; Jollès, P. Animal lysozymes c and g: An overview. Exs 1996, 75, 9–31. [Google Scholar] [CrossRef]
- Bag, M.R.; Makesh, M.; Rajendran, K.V.; Mukherjee, S.C. Characterization of IgM of Indian major carps and their cross-reactivity with anti-fish IgM antibodies. Fish Shellfish Immunol. 2009, 26, 275–278. [Google Scholar] [CrossRef]
- Mohd Faudzi, N.; Yong, A.S.K.; Shapawi, R.; Senoo, S.; Biswas, A.; Takii, K. Soy protein concentrate as an alternative in replacement of fish meal in the feeds of hybrid grouper, brown-marbled grouper (Epinephelus fuscoguttatus) × giant grouper (E. lanceolatus) juvenile. Aquac. Res. 2018, 49, 431–441. [Google Scholar] [CrossRef]
- Bunlipatanon, P.; U-taynapun, K. Growth performance and disease resistance against Vibrio vulnificus infection of novel hybrid grouper (Epinephelus lanceolatus × Epinephelus fuscoguttatus). Aquac. Res 2017, 48, 1711–1723. [Google Scholar] [CrossRef]
- Arrokhman, S.; Wijayanti, N.; Soegianto, A. Survival and osmoregulation of juvenile of hybrid grouper (Epinephelus fuscoguttatus × Epinephelus lanceolatus) during acclimation in calcium-supplemented freshwater. Aquac. Int. 2016, 25, 693–704. [Google Scholar] [CrossRef]
- Rahimnejad, S.; Bang, I.C.; Park, J.-Y.; Sade, A.; Choi, J.; Lee, S.-M. Effects of dietary protein and lipid levels on growth performance, feed utilization and body composition of juvenile hybrid grouper, Epinephelus fuscoguttatus × E. lanceolatus. Aquaculture 2015, 446, 283–289. [Google Scholar] [CrossRef]
- Jiang, S.; Wu, X.; Luo, Y.; Wu, M.; Lu, S.; Jin, Z.; Yao, W. Optimal dietary protein level and protein to energy ratio for hybrid grouper (Epinephelus fuscoguttatus × Epinephelus lanceolatus) juveniles. Aquaculture 2016, 465, 28–36. [Google Scholar] [CrossRef]
- Ye, G.; Dong, X.; Yang, Q.; Chi, S.; Liu, H.; Zhang, H.; Tan, B.; Zhang, S. Dietary replacement of fish meal with peanut meal in juvenile hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂): Growth performance, immune response and intestinal microbiota. Aquac. Rep. 2020, 17, 100327. [Google Scholar] [CrossRef]
- Bo, Y.; Min, X.; Xiufeng, W.; Xiaoyi, W.; Xiao, W.; Lei, M.; Wei, M.; Lina, G.; Qinxiao, C.; Lu, Z.; et al. Replacing poultry by-product meal protein with soybean protein isolate in low fishmeal diets for juvenile hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂). Aquac. Nutr. 2021, 27, 2405–2415. [Google Scholar] [CrossRef]
- Zhou, Z.; Wu, X.; Gatlin, D.M.; Wang, X.; Mu, W.; Ye, B.; Ma, L. Dietary valine levels affect growth, protein utilisation, immunity and antioxidant status in juvenile hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂). Br. J. Nutr. 2021, 125, 408–419. [Google Scholar] [CrossRef]
- Escaffre, A.-M.; Kaushik, S.; Mambrini, M. Morphometric evaluation of changes in the digestive tract of rainbow trout (Oncorhynchus mykiss) due to fish meal replacement with soy protein concentrate. Aquaculture 2007, 273, 127–138. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
- Sun, H.; Tang, J.-W.; Yao, X.-H.; Wu, Y.-F.; Wang, X.; Liu, Y.; Lou, B. Partial substitution of fish meal with fermented cottonseed meal in juvenile black sea bream (Acanthopagrus schlegelii) diets. Aquaculture 2015, 446, 30–36. [Google Scholar] [CrossRef]
- Wang, J.; Clark, G.; Ju, M.; Castillo, S.; Gatlin, D.M. Effects of replacing menhaden fishmeal with cottonseed flour on growth performance, feed utilization and body composition of juvenile red drum Sciaenops ocellatus. Aquaculture 2020, 523, 735217. [Google Scholar] [CrossRef]
- Lim, S.-J.; Lee, K.-J. Partial replacement of fish meal by cottonseed meal and soybean meal with iron and phytase supplementation for parrot fish Oplegnathus fasciatus. Aquaculture 2009, 290, 283–289. [Google Scholar] [CrossRef]
- Chen, G.; Yin, B.; Liu, H.; Tan, B.; Dong, X.; Yang, Q.; Chi, S.; Zhang, S. Effects of fishmeal replacement with cottonseed protein concentrate on growth, digestive proteinase, intestinal morphology and microflora in pearl gentian grouper (♀ Epinephelus fuscoguttatus × ♂ Epinephelus lanceolatu). Aquac. Res. 2020, 51, 2870–2884. [Google Scholar] [CrossRef]
- He, Y.; Guo, X.; Tan, B.; Dong, X.; Yang, Q.; Liu, H.; Zhang, S.; Chi, S. Replacing fishmeal with cottonseed protein concentrate in feed for pearl gentian groupers (Epinephelus fuscoguttatus ♀ × E. lanceolatus ♂): Effects on growth and expressions of key genes involved in appetite and hepatic glucose and lipid metabolism. Aquac. Rep. 2021, 20, 100710. [Google Scholar] [CrossRef]
- Council, N.R. Nutrient Requirements of Fish and Shrimp; The National Academies Press: Washington, DC, USA, 2011; p. 392. [Google Scholar] [CrossRef]
- Duan, C.; Ren, H.; Gao, S. Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: Roles in skeletal muscle growth and differentiation. Gen. Comp. Endocrinol. 2010, 167, 344–351. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Wang, H.; Zhang, J.; Lin, B.; Chen, L.; Wang, Q.; Li, G.; Deng, J. Assessment of rapeseed meal as fish meal alternative in diets for juvenile Asian red-tailed catfish (Hemibagrus wyckioides). Aquac. Rep. 2020, 18, 100497. [Google Scholar] [CrossRef]
- Niklasson, L.; Sundh, H.; Fridell, F.; Taranger, G.L.; Sundell, K. Disturbance of the intestinal mucosal immune system of farmed Atlantic salmon (Salmo salar), in response to long-term hypoxic conditions. Fish Shellfish Immunol. 2011, 31, 1072–1080. [Google Scholar] [CrossRef]
- Wei, L.; Wu, P.; Zhou, X.-Q.; Jiang, W.-D.; Liu, Y.; Kuang, S.-Y.; Tang, L.; Feng, L. Dietary silymarin supplementation enhanced growth performance and improved intestinal apical junctional complex on juvenile grass carp (Ctenopharyngodon idella). Aquaculture 2020, 525, 735311. [Google Scholar] [CrossRef]
- Saurabh, S.; Sahoo, P.K. Lysozyme: An important defence molecule of fish innate immune system. Aquac. Res. 2008, 39, 223–239. [Google Scholar] [CrossRef]
- Magnadottir, B.; Lange, S.; Gudmundsdottir, S.; Bøgwald, J.; Dalmo, R.A. Ontogeny of humoral immune parameters in fish. Fish Shellfish Immunol. 2005, 19, 429–439. [Google Scholar] [CrossRef]
- Kiron, V.; Puangkaew, J.; Ishizaka, K.; Satoh, S.; Watanabe, T. Antioxidant status and nonspecific immune responses in rainbow trout (Oncorhynchus mykiss) fed two levels of vitamin E along with three lipid sources. Aquaculture 2004, 234, 361–379. [Google Scholar] [CrossRef]
- Burrells, C.; Williams, P.D.; Southgate, P.J.; Crampton, V.O. Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins. Vet. Immunol. Immunopathol. 1999, 72, 277–288. [Google Scholar] [CrossRef]
- Kolkovski, S.; Tandler, A. The use of squid protein hydrolysate as a protein source in microdiets for gilthead seabream Sparus aurata larvae. Aquac. Nutr. 2000, 6, 11–15. [Google Scholar] [CrossRef]
Ingredients | Dietary Treatments | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
PBMP | CCMP 20 | CCMP 40 | CCMP 60 | CCMP 80 | CCMP 100 | LGCMP 20 | LGCMP 40 | LGCMP 60 | LGCMP 80 | LGCMP 100 | |
Fish-meal (Anchovy) 1 | 18.53 | 18.53 | 18.53 | 18.53 | 18.53 | 18.53 | 18.53 | 18.53 | 18.53 | 18.53 | 18.53 |
Poultry by-product meal 2 | 46.15 | 36.92 | 27.69 | 18.46 | 92.3 | 0.00 | 36.92 | 27.69 | 18.46 | 9.23 | 0.00 |
Conventional cottonseed proteome 3 | 0.00 | 9.68 | 19.37 | 29.05 | 38.74 | 48.42 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 |
Low-gossypol cottonseed proteome 4 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 9.56 | 19.11 | 28.67 | 38.23 | 47.78 |
Chile fish oil (Salmon) | 0.00 | 1.17 | 2.34 | 3.50 | 4.67 | 5.84 | 1.17 | 2.34 | 3.50 | 4.67 | 5.83 |
Vitamin premix | 1. | 1. | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
Mineral premix | 0.5 | 0.5 | 0.5 | 0.5 | 0.5 | 0.5 | 0.5 | 0.5 | 0.5 | 0.5 | 0.5 |
Corn starch | 19.24 | 19.24 | 19.24 | 19.24 | 19.24 | 19.24 | 19.24 | 19.24 | 19.24 | 19.24 | 19.24 |
L-Alanine | 0.03 | 0.28 | 0.28 | 0.21 | 0.11 | 0.01 | 0.30 | 0.33 | 0.25 | 0.17 | 0.08 |
L-Arginine | 0.24 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 |
L-Phenylalanine | 0.24 | 0.13 | 0.03 | 0.00 | 0.00 | 0.00 | 0.13 | 0.03 | 0.00 | 0.00 | 0.00 |
L-Methionine | 0.55 | 0.60 | 0.65 | 0.69 | 0.74 | 0.79 | 0.60 | 0.65 | 0.72 | 0.77 | 0.82 |
L-Isoleucine | 0.12 | 0.17 | 0.23 | 0.28 | 0.34 | 0.39 | 0.15 | 0.18 | 0.21 | 0.24 | 0.27 |
Carboxymethyl cellulose sodium | 2.00 | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 |
Cellulose | 11.40 | 9.77 | 8.15 | 6.53 | 4.91 | 3.29 | 9.90 | 8.41 | 6.92 | 5.43 | 3.93 |
Proximate compositions | |||||||||||
Dry matter | 92.68 | 91.89 | 91.99 | 92.06 | 92.47 | 92.91 | 93.07 | 92.88 | 92.55 | 92.49 | 91.86 |
Crude protein (%, dry matter) | 45.85 | 45.68 | 46.38 | 46.19 | 45.59 | 45.66 | 44.99 | 45.43 | 46.11 | 46.28 | 45.97 |
Crude lipid (%, dry matter) | 8.59 | 8.49 | 8.55 | 8.39 | 8.25 | 8.33 | 8.42 | 8.61 | 8.44 | 8.50 | 8.47 |
Ingredients | Dietary Treatments | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
PBMP | CCMP 20 | CCMP 40 | CCMP 60 | CCMP 80 | CCMP 100 | LGCMP 20 | LGCMP 40 | LGCMP 60 | LGCMP 80 | LGCMP 100 | |
Essential amino acids | |||||||||||
Lysine | 3.32 | 3.29 | 3.28 | 3.26 | 3.24 | 3.23 | 3.21 | 3.25 | 3.26 | 3.28 | 3.29 |
Arginine | 2.86 | 2.65 | 2.70 | 2.74 | 2.79 | 2.83 | 2.75 | 2.73 | 2.74 | 2.82 | 2.88 |
Methionine | 1.69 | 1.81 | 1.85 | 1.91 | 1.93 | 1.90 | 1.76 | 1.82 | 1.85 | 1.93 | 1.92 |
Histidine | 1.83 | 2.12 | 2.09 | 2.07 | 2.04 | 2.01 | 2.22 | 2.09 | 2.01 | 2.05 | 2.01 |
Leucine | 1.96 | 2.05 | 2.13 | 2.21 | 2.29 | 2.38 | 2.05 | 2.13 | 2.21 | 2.29 | 2.38 |
Isoleucine | 3.28 | 3.57 | 3.61 | 3.66 | 3.71 | 3.76 | 3.49 | 3.55 | 3.68 | 3.74 | 3.78 |
Valine | 1.93 | 2.09 | 2.21 | 2.32 | 2.43 | 2.54 | 2.15 | 2.20 | 2.31 | 2.36 | 2.44 |
Phenylalanine | 2.18 | 2.30 | 2.34 | 2.38 | 2.41 | 2.45 | 2.32 | 2.34 | 2.35 | 2.45 | 2.46 |
Threonine | 1.41 | 1.41 | 1.43 | 1.46 | 1.48 | 1.51 | 1.40 | 1.44 | 1.45 | 1.46 | 1.52 |
Non-essential amino acids | |||||||||||
Glutamic acid | 4.06 | 4.39 | 4.60 | 4.81 | 5.02 | 5.23 | 4.35 | 4.60 | 4.81 | 5.02 | 5.23 |
Serine | 1.82 | 2.22 | 2.25 | 2.28 | 2.31 | 2.34 | 2.21 | 2.25 | 2.28 | 2.31 | 2.34 |
Aspartic acid | 5.75 | 6.79 | 7.08 | 7.38 | 7.67 | 7.96 | 6.59 | 7.08 | 7.38 | 7.67 | 7.96 |
Tyrosine | 2.89 | 3.87 | 3.52 | 3.17 | 2.83 | 2.48 | 3.89 | 3.58 | 3.19 | 2.93 | 2.49 |
Alanine | 3.51 | 3.22 | 2.99 | 2.76 | 2.54 | 2.31 | 3.25 | 2.95 | 2.79 | 2.59 | 2.41 |
Cystine | 0.42 | 0.40 | 0.36 | 0.31 | 0.26 | 0.22 | 0.41 | 0.36 | 0.31 | 0.26 | 0.22 |
Glycine | 1.36 | 1.53 | 1.60 | 1.68 | 1.76 | 1.84 | 1.45 | 1.65 | 1.69 | 1.78 | 1.86 |
Proline | 2.18 | 2.84 | 2.75 | 2.66 | 2.57 | 2.48 | 2.75 | 2.78 | 2.65 | 2.56 | 2.47 |
Dietary Treatments | Type of Cottonseed Meal Proteome | Levels of Replacement | WG% | FCR | DFI | PER | Survival |
---|---|---|---|---|---|---|---|
PBMP | 0 | 1068 ± 17 b | 0.91 ± 0.00 cd | 1.45 ± 0.01 cd | 2.38 ± 0.01 bc | 100 | |
CCMP 20 | CCMP | 20 | 876 ± 9 d | 0.91 ± 0.00 cd | 1.45 ± 0.00 cd | 2.38 ± 0.01 bc | 100 |
CCMP 40 | CCMP | 40 | 907 ± 6 d | 0.92 ± 0.00 cd | 1.45 ± 0.00 cd | 2.37 ± 0.01 bc | 100 |
CCMP 60 | CCMP | 60 | 1000 ± 19 c | 0.91 ± 0.00 cd | 1.45 ± 0.00 cd | 2.38 ± 0.00 bc | 100 |
CCMP 80 | CCMP | 80 | 1166 ± 7 a | 0.90 ± 0.00 cd | 1.42 ± 0.01 cd | 2.43 ± 0.01 ab | 100 |
CCMP 100 | CCMP | 100 | 809 ± 10 e | 1.04 ± 0.01 a | 1.65 ± 0.02 a | 2.10 ± 0.02 e | 100 |
LGCMP 20 | LGCMP | 20 | 902 ± 8 d | 0.93 ± 0.00 c | 1.47 ± 0.01 c | 2.35 ± 0.01 c | 100 |
LGCMP 40 | LGCMP | 40 | 1211 ± 15 a | 0.89 ± 0.00 d | 1.41 ± 0.01 d | 2.45 ± 0.01 a | 100 |
LGCMP 60 | LGCMP | 60 | 1017 ± 8 bc | 0.91 ± 0.00 cd | 1.43 ± 0.01 cd | 2.40 ± 0.01 abc | 100 |
LGCMP 80 | LGCMP | 80 | 908 ± 16 d | 0.98 ± 0.01 b | 1.57 ± 0.01 b | 2.21 ± 0.01 d | 100 |
LGCMP 100 | LGCMP | 100 | 758 ± 14 e | 1.02 ± 0.02 a | 1.62 ± 0.02 a | 2.13 ± 0.03 e | 100 |
Means of main effects 1 | 100 | ||||||
CCMP | 951 | 0.93 B | 2.97 B | 2.33 A | |||
LGCMP | 959 | 0.94 A | 3.00 A | 2.30 B | |||
20 | 889 c | 0.92 c | 2.91 c | 2.37 b | |||
40 | 1059 a | 0.90 c | 2.87 c | 2.41 a | |||
60 | 1009 b | 0.91 c | 2.89 c | 2.39 ab | |||
80 | 1037 ab | 0.94 b | 2.98 b | 2.32 c | |||
100 | 783 d | 1.03 a | 3.27 a | 2.11 d | |||
Analysis of variance (p-value) | |||||||
Type of cottonseed meal proteome | 0.321 | 0.023 | 0.017 | 0.006 | |||
Levels of replacement | 0.000 | 0.000 | 0.000 | 0.000 | |||
Interaction | 0.000 | 0.000 | 0.000 | 0.000 |
Dietary Treatments | Type of Cottonseed Meal Proteome | Levels of Replacement | HSI | CF | IPF |
---|---|---|---|---|---|
PBMP | 0 | 2.10 ± 0.10 | 1.98 ± 0.04 | 2.11 ± 0.07 | |
CCMP 20 | CCMP | 20 | 2.19 ± 0.09 | 1.91 ± 0.05 | 1.96 ± 0.14 |
CCMP 40 | CCMP | 40 | 2.25 ± 0.10 | 2.04 ± 0.06 | 1.85 ± 0.15 |
CCMP 60 | CCMP | 60 | 2.33 ± 0.18 | 2.05 ± 0.04 | 1.76 ± 0.16 |
CCMP 80 | CCMP | 80 | 2.44 ± 0.11 | 2.14 ± 0.05 | 1.86 ± 0.11 |
CCMP 100 | CCMP | 100 | 1.98 ± 0.12 | 1.99 ± 0.03 | 1.74 ± 0.15 |
LGCMP 20 | LGCMP | 20 | 1.86 ± 0.19 | 2.02 ± 0.04 | 1.66 ± 0.09 |
LGCMP 40 | LGCMP | 40 | 1.94 ± 0.15 | 2.00 ± 0.04 | 1.55 ± 0.16 |
LGCMP 60 | LGCMP | 60 | 2.16 ± 0.12 | 2.10 ± 0.06 | 1.49 ± 0.10 |
LGCMP 80 | LGCMP | 80 | 2.22 ± 0.13 | 2.10 ± 0.04 | 1.59 ± 0.11 |
LGCMP 100 | LGCMP | 100 | 2.40 ± 0.06 | 2.12 ± 0.03 | 1.70 ± 0.14 |
Means of main effects 1 | |||||
CCMP | 2.24 | 2.24 | 1.84 A | ||
LGCMP | 2.12 | 2.12 | 1.60 B | ||
20 | 2.03 | 2.03 | 1.81 | ||
40 | 2.09 | 2.09 | 1.70 | ||
60 | 2.25 | 2.25 | 1.63 | ||
80 | 2.33 | 2.33 | 1.73 | ||
100 | 2.19 | 2.19 | 1.72 | ||
Analysis of variance (p-value) | |||||
Type of cottonseed meal proteome | 0.074 | 0.131 | 0.010 | ||
Levels of replacement | 0.228 | 0.132 | 0.738 | ||
Interaction | 0.446 | 0.037 | 0.827 |
Dietary Treatments | Type of Cottonseed Meal Proteome | Levels of Replacement | Whole-Body Composition | White Muscle Composition | ||||
---|---|---|---|---|---|---|---|---|
Moisture | Protein | Lipid | Moisture | Protein | Lipid | |||
PBMP | 0 | 70.1 ± 0.1 | 17.8 ± 0.0 | 7.44 ± 0.06 a | 76.8 ± 0.0 | 19.6 ± 0.3 c | 1.61 ± 0.19 | |
CCMP 20 | CCMP | 20 | 70.6 ± 0.1 | 17.8 ± 0.1 | 7.13 ± 0.02 b | 76.2 ± 0.1 | 19.8 ± 0.1 bc | 1.42 ± 0.07 |
CCMP 40 | CCMP | 40 | 70.4 ± 0.1 | 17.7 ± 0.1 | 6.85 ± 0.02 c | 76.6 ± 0.1 | 19.8 ± 0.2 abc | 1.34 ± 0.09 |
CCMP 60 | CCMP | 60 | 70.7 ± 0.1 | 18.0 ± 0.1 | 6.56 ± 0.02 d | 76.5 ± 0.1 | 19.9 ± 0.2 abc | 1.25 ± 0.10 |
CCMP 80 | CCMP | 80 | 71.2 ± 0.0 | 18.2 ± 0.1 | 6.28 ± 0.01 e | 77.3 ± 0.1 | 20.0 ± 0.0 bc | 1.32 ± 0.01 |
CCMP 100 | CCMP | 100 | 71.5 ± 0.1 | 17.9 ± 0.3 | 6.09 ± 0.03 f | 77.2 ± 0.3 | 19.7 ± 0.2 abc | 1.00 ± 0.08 |
LGCMP 20 | LGCMP | 20 | 70.5 ± 0.2 | 18.1 ± 0.2 | 7.03 ± 0.03 bc | 76.0 ± 0.2 | 20.2 ± 0.2 ab | 1.40 ± 0.30 |
LGCMP 40 | LGCMP | 40 | 70.6 ± 0.1 | 18.3 ± 0.1 | 6.85 ± 0.02 c | 76.5 ± 0.1 | 20.3 ± 0.1 a | 1.63 ± 0.18 |
LGCMP 60 | LGCMP | 60 | 70.6 ± 0. | 18.3 ± 0.1 | 6.58 ± 0.02 d | 76. 9 ± 0.1 | 20.0 ± 0.2 abc | 1.27 ± 0.18 |
LGCMP 80 | LGCMP | 80 | 70.4 ± 0.1 | 18.2 ± 0.1 | 6.33 ± 0.02 e | 76.6 ± 0.8 | 20.0 ± 0.1 abc | 1.21 ± 0.22 |
LGCMP 100 | LGCMP | 100 | 71.1 ± 0.1 | 18.1 ± 0.1 | 76.9 ± 0.1 | 19.9 ± 0.2 abc | 1.03 ± 0.10 | |
Means of main effects 1 | ||||||||
CCMP | 70.87 | 17.93 B | 6.58 | 76.91 A | 19.85 B | 1.27 | ||
LGCMP | 70.77 | 18.12 A | 6.59 | 76.66 B | 20.08 A | 1.31 | ||
20 | 70.35 c | 17.97 | 7.08 a | 76.10 d | 20.00 | 1.41 a | ||
40 | 70.62 bc | 18.01 | 6.85 b | 76.62 c | 20.07 | 1.49 a | ||
60 | 70.75 bc | 17.96 | 6.57 bc | 76.83 bc | 19.95 | 1.26 ab | ||
80 | 70.89 b | 18.20 | 6.31 c | 77.05 ab | 19.87 | 1.26 ab | ||
100 | 71.48 a | 18.00 | 6.15 d | 77.34 a | 19.95 | 1.02 b | ||
Analysis of variance (p-value) | ||||||||
Type of cottonseed meal proteome | 0.242 | 0.030 | 0.548 | 0.002 | 0.000 | 0.491 | ||
Levels of replacement | 0.000 | 0.383 | 0.000 | 0.000 | 0.215 | 0.000 | ||
Interaction | 0.051 | 0.295 | 0.148 | 0.752 | 0.019 | 0.276 |
Dietary Treatments | Type of Cottonseed Meal Proteome | Levels of Replacement | Foregut (μm) | Midgut (μm) | Hindgut (μm) | |||
---|---|---|---|---|---|---|---|---|
hF | hMV | hF | hMV | hF | hMV | |||
PBMP | 0 | 448 ± 5 c | 3.0 ± 0.1 b | 385 ± 9 def | 2.5 ± 0.1 c | 423 ± 5 ef | 2.7 ± 0.1 fg | |
CCMP 20 | CCMP | 20 | 451 ± 11 c | 2.9 ± 0.1 bcd | 387 ± 5 def | 2.6 ± 0.1 bc | 433 ± 5 cdef | 2.7 ± 0.1 efg |
CCMP 40 | CCMP | 40 | 465 ± 5 bc | 2.7 ± 0.0 d | 408 ± 3 bcd | 2.6 ± 0.1 bc | 439 ± 7 bcde | 2.8 ± 0.1 cdef |
CCMP 60 | CCMP | 60 | 470 ± 5 bc | 2.9 ± 0.0 bcd | 439 ± 14 a | 2.8 ± 0.1 ab | 459 ± 3 ab | 2.9 ± 0.0 bc |
CCMP 80 | CCMP | 80 | 517 ± 9 a | 3.2 ± 0.1 a | 427 ± 6 ab | 2.8 ± 0.1 ab | 473 ± 7 a | 3.3 ± 0.0 a |
CCMP 100 | CCMP | 100 | 456 ± 11 bc | 2.8 ± 0.0 cd | 395 ± 7 de | 2.7 ± 0.1 abc | 445 ± 7 bcd | 2.9 ± 0.0 cde |
LGCMP 20 | LGCMP | 20 | 460 ± 7 bc | 3.0 ± 0.1 bc | 366 ± 9 f | 2.6 ± 0.0 bc | 414 ± 11 f | 2.6 ± 0.0 g |
LGCMP 40 | LGCMP | 40 | 513 ± 7 a | 3.3 ± 0.1 a | 424 ± 12 abc | 2.9 ± 0.1 a | 476 ± 12 a | 3.0 ± 0.1 ab |
LGCMP 60 | LGCMP | 60 | 478 ± 8 b | 3.0 ± 0.1 bc | 401 ± 6 cde | 2.8 ± 0.1 ab | 449 ± 2 bc | 2.9 ± 0.1 cd |
LGCMP 80 | LGCMP | 80 | 466 ± 4 bc | 2.9 ± 0.0 bc | 382 ± 11 ef | 2.7 ± 0.0 abc | 433 ± 6 cdef | 2.7 ± 0.0 defg |
LGCMP 100 | LGCMP | 100 | 459 ± 15 bc | 2.8 ± 0.1 bcd | 369 ± 6 f | 2.6 ± 0.0 bc | 425 ± 9 def | 2.5 ± 0.1 h |
Means of main effects 1 | ||||||||
CCMP | 472.32 | 2.90 B | 411.49 A | 2.69 | 450.38 A | 2.93 A | ||
LGCMP | 475.61 | 3.00 A | 388.78 B | 2.69 | 439.78 B | 2.79 B | ||
20 | 456.13 c | 2.91 bc | 376.63 c | 2.58 b | 423.99 b | 2.70 b | ||
40 | 489.41 ab | 3.02 ab | 416.62 ab | 2.73 a | 458.11 a | 2.96 a | ||
60 | 474.21 b | 2.93 bc | 420.43 a | 2.76 a | 454.46 a | 2.93 a | ||
80 | 492.03 a | 3.08 a | 404.85 b | 2.72 a | 453.26 a | 3.00 a | ||
100 | 458.05 c | 2.81 c | 382.17 c | 2.66 ab | 435.60 b | 2.70 b | ||
Analysis of variance (p-value) | ||||||||
Type of cottonseed meal proteome | 0.327 | 0.001 | 0.000 | 0.768 | 0.001 | 0.000 | ||
Levels of replacement | 0.000 | 0.000 | 0.000 | 0.004 | 0.000 | 0.000 | ||
Interaction | 0.000 | 0.000 | 0.000 | 0.002 | 0.000 | 0.000 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Irm, M.; Ye, B.; Wu, X.; Geng, L.; Cai, Q.; Zhang, L.; Zhai, H.; Zhou, Z. Assessment of Conventional and Low Gossypol Cottonseed Meal as Alternative Protein Sources in Low-Fishmeal Diets of Hybrid Grouper (Epinephelus fuscoguttatus♀× Epinephelus lanceolatus♂): Growth, Feed Utilization, Gut Histology, and Immunity. Animals 2022, 12, 1906. https://doi.org/10.3390/ani12151906
Irm M, Ye B, Wu X, Geng L, Cai Q, Zhang L, Zhai H, Zhou Z. Assessment of Conventional and Low Gossypol Cottonseed Meal as Alternative Protein Sources in Low-Fishmeal Diets of Hybrid Grouper (Epinephelus fuscoguttatus♀× Epinephelus lanceolatus♂): Growth, Feed Utilization, Gut Histology, and Immunity. Animals. 2022; 12(15):1906. https://doi.org/10.3390/ani12151906
Chicago/Turabian StyleIrm, Misbah, Bo Ye, Xiaoyi Wu, Lina Geng, Qinxiao Cai, Lu Zhang, Haoyun Zhai, and Zhiyu Zhou. 2022. "Assessment of Conventional and Low Gossypol Cottonseed Meal as Alternative Protein Sources in Low-Fishmeal Diets of Hybrid Grouper (Epinephelus fuscoguttatus♀× Epinephelus lanceolatus♂): Growth, Feed Utilization, Gut Histology, and Immunity" Animals 12, no. 15: 1906. https://doi.org/10.3390/ani12151906
APA StyleIrm, M., Ye, B., Wu, X., Geng, L., Cai, Q., Zhang, L., Zhai, H., & Zhou, Z. (2022). Assessment of Conventional and Low Gossypol Cottonseed Meal as Alternative Protein Sources in Low-Fishmeal Diets of Hybrid Grouper (Epinephelus fuscoguttatus♀× Epinephelus lanceolatus♂): Growth, Feed Utilization, Gut Histology, and Immunity. Animals, 12(15), 1906. https://doi.org/10.3390/ani12151906