Growth Performance, Apparent Ileal Digestibility, and Nutrient Transporter Gene Expressions of Broilers Fed Seaweed-Supplemented Diets
Abstract
Seaweed provides macro-, micro-nutrients, and biological bioactive components that may improve broiler production. The study aimed to evaluate the effects of various levels of brown seaweed (BS) and green seaweed (GS) on growth performance, carcass characteristics, apparent ileal digestibility (AID), and hepatic growth and nutrient transporter gene expressions. The study followed a completely randomized design (CRD) (twelve treatments, six replicates, and seven birds per replicate). The dietary treatments contained: basal diet [negative control (NC)], basal diet + vitamin E (100 mg/kg feed) [positive control (PC)], basal diet + 0.25%, 0.50%, 0.75%, 1.0%, and 1.25% BS and GS, respectively. The data were analyzed using the General Linear Model (GLM) of the statistical analysis system (SAS 9.4) by one-way ANOVA. Duncan’s Multiple Range Test was used to assess the significant differences between treatment groups at p<0.05. Various levels of BS and GS (p<0.05) improved body weight (BW), body weight gain (BWG), and feed intake (FI) at the starter phase. No significant effects were observed in the carcass characteristics. The AID of crude protein (CP), organic matter (OM), and dry matter (DM) during the starter phase were significantly improved. The hepatic growth hormone receptor (GHR) gene had increased expression in birds fed 0.50% and 0.75% of GS-contained diets. Similarly, birds fed 0.50% of BS and 0.25%, 0.50%, and 0.75% of GS had higher (p<0.05) expression of the hepatic Insulin-like growth factor-1 (IGF-1) gene. Furthermore, there were no significant effects on the intestinal nutrient transporters genes, including aminopeptidase (APN), glucose transporter (SGLT5), and oligopeptide transporter (PepT1) at the jejunum tissue. It was therefore concluded that different levels of BS and GS in the broiler chickens’ diet improved the starter period growth performance and nutrient digestibility.
References
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Garcia-Vaquero, M., & M. Hayes. 2016. Red and green macroalgae for fish and animal feed and human functional food development. Food Reviews International 32:15–45. https://doi.org/10.1080/87559129.2015.1041184
Hayes, M. 2012. Marine Bioactive Compounds: Sources, Characterization and Applications (M Hayes, Ed.). 1st ed. Springer US, Dublin 15, Ireland. https://doi.org/10.1007/978-1-4614-1247-2
Heim, G., A. M. Walsh, T. Sweeney, D. N. Doyle, C. J. O’Shea, M. T. Ryan, & J. V. O’Doherty. 2014. Effect of seaweed-derived laminarin and fucoidan and zinc oxide on gut morphology, nutrient transporters, nutrient digestibility, growth performance and selected microbial populations in weaned pigs. Br. J. Nutr. 111:1577–1585. https://doi.org/10.1017/S0007114513004224
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Association Official Analytical Chemistry. 1995. Association of Official Analytical Chemistry: Official Methods of Analysis. VA, USA.
Azizi, M. N., T. C. Loh, H. L. Foo, H. Akit, W. I. Izuddin, N. Shazali, E. L. T. Chung, & A. A. Samsudin. 2021a. Chemical compositions of brown and green seaweed, and effects on nutrient digestibility in broiler chickens. Animals 11:2147. https://doi.org/10.3390/ani11072147
Azizi, M. N., T. C. Loh, H. L. Foo, & E. L. T. Chung. 2021b. Is palm kernel cake a suitable alternative feed ingredient for poultry? Animals 11:1–15. https://doi.org/10.3390/ani11020338
Azizi, M. N., T. C. Loh, H. L. Foo, H. Akit, W. I. Izuddin, & D. Yohanna. 2023. Brown and green seaweed antioxidant properties and effects on blood plasma antioxidant enzyme activities, hepatic antioxidant genes expression, blood plasma lipid profile, and meat quality in broiler chickens. Animals 13:1582. https://doi.org/10.3390/ani13101582
Balasubramanian, B., S. Shanmugam, S. Park, N. Recharla, J. S. Koo, I. Andretta, & I. H. Kim. 2021. Supplemental impact of marine red seaweed (Halymenia palmata) on the growth performance, total tract nutrient digestibility, blood profiles, intestine histomorphology, meat quality, fecal gas emission, and microbial counts in broilers. Animals 11:1244. https://doi.org/10.3390/ani11051244
Beckman, B. R. 2011. Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes. Gen. Comp. Endocrinol. 170:233–252. https://doi.org/10.1016/j.ygcen.2010.08.009
Bhatia, S., P. Rathee, K. Sharma, B. B. Chaugule, N. Kar, & T. Bera. 2013. Immuno-modulation effect of sulphated polysaccharide (porphyran) from Porphyra vietnamensis. Int. J. Biol. Macromol. 57:50–56. https://doi.org/10.1016/j.ijbiomac.2013.03.012
Bonos, E., A. Kargopoulos, I. Nikolakakis, P. Florou Paneri, & E. Christaki. 2017. The seaweed Ascophyllum nodosum as a potential functional ingredient in chicken nutrition. Journal Oceanography Marine Research 04:1–5. https://doi.org/10.4172/2572-3103.1000140
Cherry, P., C. O’hara, P. J. Magee, E. M. Mcsorley, & P. J. Allsopp. 2019. Risks and benefits of consuming edible seaweeds. Nutr. Rev. 77:307–329. https://doi.org/10.1093/nutrit/nuy066
Choi, Y. J., S. R. Lee, & J. W. Oh. 2014. Effects of dietary fermented seaweed and seaweed fusiforme on growth performance, carcass parameters and immunoglobulin concentration in broiler chicks. Asian-Australas. J. Anim. Sci. 27:862–870. https://doi.org/10.5713/ajas.2014.14015
Corino, C., S. C. Modina, A. Di Giancamillo, S. Chiapparini, & R. Rossi. 2019. Seaweeds in pig nutrition. Animals 9:1–26 Available at https://www.mdpi.com/2076-2615/9/12/1126. https://doi.org/10.3390/ani9121126
Del Vesco, A. P., E. Gasparino, A. R. Oliveira Neto, S. E. F. Guimarães, S. M. M. Marcato, & D. M. Voltolini. 2013. Dietary methionine effects on IGF-I and GHR mRNA expression in broilers. Genet. Mol. Res. 12:6414–6423. https://doi.org/10.4238/2013.December.10.2
Diyana, S., A. Aziz, N. U. R. F. Jafarah, S. Sabri, M. As, W. A. D. Abdul, Z. Norhana, & B. Yusof. 2019. Antifungal activity of dichloromethane and hexane extracts of four Malaysian seaweed species against Ganoderma boninense. Malays. Appl. Biol. 48:189–196.
El-Deek, A. A., M. A. Al-Harthi, A. A. Abdalla, & M. M. Elbanoby. 2011. The use of brown algae meal in finisher broiler. Egypt. Poult. Sci 31:767–781.
El-Sabrout, K., M. R. T. Dantas, & J. B. F. Souza-Junior. 2023. Herbal and bee products as nutraceuticals for improving poultry health and production. Worlds Poul. Sci. J. 79:223–242. https://doi.org/10.1080/00439339.2021.1960238
Ferraces-Casais, P., M. A. Lage-Yusty, A. R. B. de Quirós, & J. López-Hernández. 2012. Evaluation of Bioactive compounds in fresh edible seaweeds. Food Anal. Methods 5:828–834. https://doi.org/10.1007/s12161-011-9321-2
Garcia-Vaquero, M., & M. Hayes. 2016. Red and green macroalgae for fish and animal feed and human functional food development. Food Reviews International 32:15–45. https://doi.org/10.1080/87559129.2015.1041184
Hayes, M. 2012. Marine Bioactive Compounds: Sources, Characterization and Applications (M Hayes, Ed.). 1st ed. Springer US, Dublin 15, Ireland. https://doi.org/10.1007/978-1-4614-1247-2
Heim, G., A. M. Walsh, T. Sweeney, D. N. Doyle, C. J. O’Shea, M. T. Ryan, & J. V. O’Doherty. 2014. Effect of seaweed-derived laminarin and fucoidan and zinc oxide on gut morphology, nutrient transporters, nutrient digestibility, growth performance and selected microbial populations in weaned pigs. Br. J. Nutr. 111:1577–1585. https://doi.org/10.1017/S0007114513004224
Holdt, S. L. & S. Kraan. 2011. Bioactive compounds in seaweed: Functional food applications and legislation. J. Appl. Phycol. 23:543–597. https://doi.org/10.1007/s10811-010-9632-5
Humam, A. M., T. C. Loh, H. L. Foo, A. A. Samsudin, N. M. Mustapha, I. Zulkifli, & W. I. Izuddin. 2019. Effects of feeding different postbiotics produced by Lactobacillus plantarum on growth performance, carcass yield, intestinal morphology, gut microbiota composition, immune status, and growth gene expression in broilers under heat stress. Animals 9:644. https://doi.org/10.3390/ani9090644
Khalifah, A., S. Abdalla, M. Rageb, L. Maruccio, F. Ciani, & K. El-Sabrout. 2023. Could insect products provide a safe and sustainable feed alternative for the poultry industry? A comprehensive review. Animals 13:1534. https://doi.org/10.3390/ani13091534
Kidgell, J. T., M. Magnusson, R. de Nys, & C. R. K. Glasson. 2019. Ulvan: A systematic review of extraction, composition and function. Algal Res. 39:101–422. https://doi.org/10.1016/j.algal.2019.101422
Kim, S. K. 2011. Handbook of Marine Macroalgae: Biotechnology and Applied Phycology. Wiley-Blackwall publishing, Oxford. https://doi.org/10.1002/9781119977087
Kulshreshtha, G., M. T. Hincke, B. Prithiviraj, & A. Critchley. 2020. A review of the varied uses of macroalgae as dietary supplements in selected poultry with special reference to laying hen and broiler chickens. J. Mar. Sci. Eng. 8:536–564. https://doi.org/10.3390/jmse8070536
Lahaye, M. & A. Robic. 2007. Structure and function properties of Ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–1774. https://doi.org/10.1021/bm061185q
Livak, K. J. & T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Loh, T. C. 2017. Animal Feed the way forward. University Putra Malaysia, Selangor. Inaugural lecture. http://psasir.upm.edu.my/id/eprint/66849
MacArtain, P., C. I. R. Gill, M. Brooks, R. Campbell, & I. R. Rowland. 2007. Nutritional value of edible seaweeds. Nutr. Rev. 65:535–543. https://doi.org/10.1111/j.1753-4887.2007.tb00278.x
Marcu, A., I. Vacaru-opri, G. Dumitrescu, L. Petculescu, A. Marcu, M. Nicula, I. Pe, D. Dronca, B. Kelciov, & C. Mari. 2013. The influence of genetics on economic efficiency of broiler chickens growth. Anim. Sci. Biotechnol. 46:339–346.
Matanjun, P., S. Mohamed, N. M. Mustapha, K. Muhammad, & C. H. Ming. 2008. Antioxidant activities and phenolics content of eight species of seaweeds from north Borneo. J. Appl. Phycol. 20:367–373. https://doi.org/10.1007/s10811-007-9264-6
Mohammadigheisar, M., V. L. Shouldice, J. S. Sands, D. Lepp, M. S. Diarra, & E. G. Kiarie. 2020. Growth performance, breast yield, gastrointestinal ecology and plasma biochemical profile in broiler chickens fed multiple doses of a blend of red, brown and green seaweeds. Br. Poult. Sci. 61:590–598. https://doi.org/10.1080/00071668.2020.1774512
Montagne, L., J. R. Pluske, & D. J. Hampson. 2003. A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Anim. Feed Sci. Technol. 108:95–117. https://doi.org/10.1016/S0377-8401(03)00163-9
NRC. 1994. Nutrient Requirements of Poultry. 9th rev ed. Washington (DC): National Academy Press.
Øverland, M., L. T. Mydland, & A. Skrede. 2019. Marine macroalgae as sources of protein and bioactive compounds in feed for monogastric animals. J. Sci. Food Agric. 99:13–24. https://doi.org/10.1002/jsfa.9143
Peng, J., J. P. Yuan, C. F. Wu, & J. H. Wang. 2011. Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: Metabolism and bioactivities relevant to human health. Mar. Drugs 9:1806–1828. https://doi.org/10.3390/md9101806
Rao, P. V. S., C. Periyasamy, K. S. Kumar, A. S. R. And, & P. Anantharaman. 2018. Seaweeds: Distribution, Production and Uses. Pages 59–78 in Bioprospecting of Algae. M. M. Noor, S. K. B. and S. K. S., ed. Society for Plant Research.
Rizk, Y. S., I. I. Ismail, S. H. A. Hafsa, A. A. Eshera, & F. A. Tawfeek. 2017. Effect of dietary green tea and dried seaweed on productive and physiological performance of laying hens during late phase of production. Egypt. Poult. Sci. J. 37:685–706. https://doi.org/10.21608/epsj.2017.7534
Sadh, P. K., S. Duhan, & J. S. Duhan. 2018. Agro-industrial wastes and their utilization using solid state fermentation: A review. Bioresour. Bioprocess. 5:1–15. https://doi.org/10.1186/s40643-017-0187-z
Short, F. J., P. Gorton, J. Wiseman, & K. N. Boorman. 1996. Determination of titanium dioxide added as an inert marker in chicken digestibility studies. Anim. Feed Sci. Technol. 59:215–221. https://doi.org/10.1016/0377-8401(95)00916-7
ShuBai, W., J. YuHui, W. LiHua, Z. FengHua, & L. YingTing. 2013. Enteromorpha prolifera supplemental level: Effects on laying performance, egg quality, immune function and microflora in feces of laying hens. Chinese Journal Animal Nutrition 25:1346–1352.
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Authors
AziziM. N., LohT. C., FooH. L., & IzuddinW. I. (2024). Growth Performance, Apparent Ileal Digestibility, and Nutrient Transporter Gene Expressions of Broilers Fed Seaweed-Supplemented Diets. Tropical Animal Science Journal, 47(3), 333-342. https://doi.org/10.5398/tasj.2024.47.3.333
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