Abstract
Marine algae contain large amounts of bioactive compounds and dietary fiber; thus, when used as feed for poultry, they could be an alternative to improve intestinal integrity and reduce lipid serum concentrations. Few studies have assessed the prebiotic properties of this marine resource. The objective of this study was to evaluate the prebiotic effects of different concentrations of the green alga Ulva rigida as feed additive to enhance the morphology of intestinal villi and reduce total cholesterol and triglyceride levels in chickens. One hundred and forty-one-day-old Arbor Acres broilers were randomized to one of four treatments: 0, 2, 4, and 6% Ulva meal, respectively, including seven replicates of five broilers each, in a completely randomized design. The assay was run for 6 weeks. Body weight gain and carcass percentage were not affected by the treatment, but feed intake, feed conversion ratio, and mortality showed significant differences (p < 0.05). Width, height, and contour length of intestinal villi were higher (p < 0.05) in all U. rigida meal treatments compared to the control group. The highest (p < 0.05) intestinal villus height and contour length were recorded with 2% Ulva. Serum total cholesterol and triglyceride levels were significantly lower in Ulva treatments vs. control (p < 0.05). The addition of U. rigida to broilers meal improved the growth of intestinal villi and reduced serum total cholesterol and triglyceride levels, thus confirming that it could be considered as a prebiotic that can enhance the broiler health.




Similar content being viewed by others
References
Abudabos AM, Okab AB, Aljumaah RS, Samara EM, Abdoun KA, Al-Haidary AA (2013) Nutritional value of green seaweed (Ulva lactuca) for broiler chickens. Ital J Anim Sci 12:177–181
Águila-Ramírez R, Casas-Valdez M, Hernández-Guerrero CJ, Marín-Alvarez A (2005) Biomasa de Ulva spp. (Chlorophyta) en tres localidades del Malecón de La Paz, Baja California Sur, México. Rev Biol Mar Ocean 40:55–61
Aguilera-Morales M, Casas-Valdez M, Carrillo-Domínguez S, González-Acosta B, Pérez-Gil F (2005) Chemical composition and microbiological assays of marine algae Enteromorpha spp., as a potential food source. J Compos Anal 18:79–88
AOAC (2000) Official methods of analysis. AOAC International, Washington, D.C.
Arce-Menocal J, Ávila-González E, López C, García EA, García GF (2005) Efecto de paredes celulares (Saccharomyces cerevisiae) en el alimento de pollo de engorda sobre los parámetros productivos. Téc Pecu Méx 43:155–162
Arce-Menocal J, Ávila-González E, López C (2008) Comportamiento productivo y cambios morfológicos en vellosidades intestinales del pollo en engorda a 21 días de edad con el uso de paredes celulares de Saccharomyces cerevisiae. Vet Mex 39:223–228
Awad WA, Ghareeb K, Abdel-Raheem S, Böhm J (2009) Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult Sci 88:49–56
Bradbury EJ, Wilkinson SJ, Cronin GM, Walk CL, Cowieson AJ (2012) The effect of marine calcium source on broiler leg integrity. In: Proc 23rd Annual Australian Poultry Science Symposium, Sydney NSW, Australia 19-22 February pp 85–88
Buclaw M (2016) The use of inulin in poultry feeding: a review. J Anim Physiol Anim Nutr 100:1015–1022
Cabrita ARJ, Maia MRG, Oliveira HM, Sousa-Pinto I, Almeida AA, Pinto E, Fonseca AJM (2016) Tracing seaweeds as mineral sources for farm-animals. J Appl Phycol 28:3135–3150
Carrillo S, Casas-Valdez M, Ramos F, Pérez-Gil F, Sánchez-Rodríguez I (2002) Algas Marinas de Baja California Sur, México: Valor nutricional. Arch Latinoam Nutr 52:400–405
Carrillo S, Bahena A, Casas-Valdez M, Carranco M, Calvo C, Ávila E, Pérez-Gil F (2012) The alga Sargassum spp. as alternative to reduce egg cholesterol content. Cuban J Agri Sci 46:181–186
Cervantes-Duarte R, Aguirre-Bahena F, Reyes-Salinas A, Valdez-Holguín JE (2001) Caracterización hidrológica de una laguna costera de Baja California Sur, México. Oceánides 16:93–105
Chávez S, García-Martínez J, Delgado-Ramos L, Pérez-Ortín JE (2016) The importance of controlling mRNA turnover during cell proliferation. Curr Genet 62:701–710
Chávez-Sánchez T, Piñón-Gimate A, Serviere-Zaragoza E, Sánchez-González A, Hernández-Carmona G, Casas-Valdez M (2017) Recruitment in Ulva blooms in relation to temperature, salinity and nutrients in a subtropical bay of the Gulf of California. Bot Mar 60:257–270
Chávez-Sánchez T, Piñón-Gimate A, Melton JT III, López-Bautista JM, Casas-Valdez M (2018) Ulva blooms in the southwestern gulf of California: reproduction and biomas. Estuar Coast Shelf Sci 200:202–2011
Cortes-Cuevas A, Ávila GE, Casaubon HT, Carrillo DS (2000) El efecto del Bacillus toyoi sobre el comportamiento productivo en pollos de engorda. Vet Mex 31:301–308
Cruz-Ayala MB, Núñez-López RA, López GE (2001) Seaweeds in the southern gulf of California. Bot Mar 44:187–197
Cruz-Suarez LE, Ricque-Marie D, Tapia-Salazar M, Guajardo-Barbosa C (2000) Uso de la harina de kelp (Macrocystis pyrifera) en alimentos para camarón. In: Cruz-Suarez LE, Ricque-Marie D, Tapia-Salazar M, Olvera-Novoa MA, Civera-Cerecedo R (eds) Avances en Nutrición Acuícola V. Memorias del V Simposium Internacional de Nutrición Acuícola, pp 227–266
Cuervo M, Gómez C, Romero H (2002) Efecto de la utilización de un suplemento nutricional hidratado en pollos de engorde recién nacidos. Rev Colombiana Cien Pecuarias 15:319–329
El-Deek AA, Al-Harthi MA, Abdalla AA, Elbanoby MM (2011) The use of brown algae meal in finisher broiler diets. Egypt Poult Sci J 31:767–781
Evans FD, Critchely AT (2014) Seaweeds for animal production use. J Appl Phycol 26:891–899
Ferrini G, Manzanilla EG, Menoyo D, Esteve-Garcia E, Baucells MD, Barroeta AC (2010) Effects of dietary n-3 fatty acids in fat metabolism and thyroid hormone levels when compared to dietary saturated fatty acids in chickens. Livestock Sci 131:287–291
Foster GG, Hodgson AN (1998) Consumation and apparent dry matter digestibility of six intertidal macroalgae by Turbo sarmaticus (Mollusca:Vegigastropoda: Turbinidae). Aquaculture 167:211–227
Frikha F, Kammoun M, Hammami N, Mchirgui RA, Belbahri L, Gargouri Y, Miled N, Ben-Rebah F (2011) Chemical composition and some biological activities of marine algae collected in Tunisia. Cienc Mar 37:113–124
Gopal GS, Pal R (2011) Biochemical composition and lipid characterization of marine green alga Ulva rigida- a nutriotional approach. J Algal Biomass Utln 2:10–13
Hassan S, El-Twab SA, Hetta M, Mahmoud B (2011) Improvement of lipid profile and antioxidant of hypercholesterolemic albino rats by polysaccharides extracted from the green alga Ulva lactuca Linnaeus. Saudi J Biol Sci 18:333–340
Hu X, Wang T, Li W, Jin F, Wang L (2013) Effects of NS Lactobacillus strains on lipid metabolism of rats fed a high-cholesterol diet. Lipids Health Dis 12:67
Irkin LC, Erdugan H (2014) Chemical composition of Ulva rigida C. Agardh from the Canakkae Strait (Dardanelles), Turkey. J Black Sea/Mediterr Environ 20:114–121
Itzá-Ortiz MF, López-Coello C, Ávila-González E, Gómez-Rosales S, Arce-Menocal J, Velásquez-Madrazo PA (2008) Efecto de la fuente energética y el nivel de energía sobre la longitud de las vellosidades intestinales, la respuesta inmune y el rendimiento productivo en los pollos de engorda. Vet Mex 39:357–376
James O, Godwin E, Otini I (2013) Ulvaria chamae (Annonaceae) plant extract neutralizes some biological effects of Naja nigricollis snake venom in rats. Br J Pharmacol Toxicol 4:41–50
Jaramillo ÁH (2012) Evaluación de la mezcla de un ácido orgánico y un prebiótico en los parámetros productivos y alométricos de pollos de engorde con alimentación controlada. Rev Colombiana Cienc Anim 5:52–66
Koth TS, Im JT, Park IK, Lee HJ, Choi DY, Choi CJ, Lee HG, Choi YJ (2005) Effect of dietary brown seaweed levels on the protein and energy metabolism in broiler chicks activated acute phase response. J Anim Sci Tech (Kor) 47:379–390
Kulshreshtha G, Rathgeber B, Stratton G, Thomas N, Evans F, Critchley A, Hafting J, Prithiviraj B (2014) Immunology, health, and disease: feed supplementation with red seaweeds, Chondrus crispus and Sarcodiotheca gaudichaudii, affects performance, egg quality, and gut microbiota of layer hens. Poult Sci 93:2991–3001
Lee W, Koh E, Woh J, Kim M, Park J, Lee K (2005) Obesity: the role of hypothalamic AMP-activated protein kinase in body weight regulation. Int J Biochem Cell Biol 37:2254–2259
Li Q, Luo J, Wang C, Tai W, Wang H, Zhang X, Liu K, Jia Y, Lyv X, Wang L, He H (2018) Ulvan extracted from green seaweeds as new natural additives in diets for laying hens. J Appl Phycol 30:2017–2027
Makkar HPS, Tran G, Heuzé V, Giger-Reverdin S, Lessire M, Lebas F, Ankers P (2016) Seaweeds for livestock diets: a review. Anim Feed Sci Technol 212:1–17
Marinho-Sorino E, Fonseca PC, Carneiro MAA, Moreira WSC (2006) Seasonal variation in the chemical composition of two tropical seaweeds. Bioresour Technol 97:2402–2406
Markovic R, Šefer D, Krstic M, Petrujkic B (2009) Effect of different growth promoters on broiler performance and gut morphology. Arch Med Vet 41:163–169
NCR (1994) Nutrient requirements of poultry, 9th edn. National Academic Press, Washingthon, DC
Osorio JH, Flórez JD, Pérez JE (2012) Evaluación de los métodos directo, precipitado y Friedewald para la cuantificación de colesterol LDL y HDL en pollos de engorde. Rev Med Vet 24:85–90
Qadri SSN, Biswas A, Mandal AB, Kumawat M, Saxena R, Nasir AM (2019) Production performance, immune response and carcass traits of broiler chickens fed diet incorporated with Kappaphycus alvarezii. J Appl Phycol 31:753–760
Raghavendran HRB, Sathivel A, Devaki T (2005) Effect of Sargassum polycystum (Phaeophyceae)-sulphated polysaccharide extract against acetaminophen-induced hyperlipidemia during toxic hepatitis in experimental rats. Molec Cell Biochem 276:89–96
Rebolé A, Ortiz LT, Rodríguez M, Alzueta C, Treviño J, Velasco S (2010) Effects of inulin and enzyme complex, individually or in combination, on growth performance, intestinal microflora, cecal fermentation characteristics, and jejunal histomorphology in broiler chickens fed a wheat-and barley-based diet. Poult Sci 89:276–286
Rehman H, Böhm J, Zentek J (2007) Effects of differentially fermentable carbohydrates on the microbial fermentation profile of the gastrointestinal tract of broilers. J Anim Physiol Anim Nutr 92:471–480
Robic A, Bertrand D, Sassi JF, Lerat Y, Lahaye M (2009) Determination of the chemical composition of ulvan, a cell wall polysaccharide from Ulva spp. (Ulvales, Chlorophyta) by FT-IR and chemometrics. J Appl Phycol 21:451–456
SAGARPA (2016) 4to Informe de Labores 2015-2016. Secretaría de Agricultura, Ganadería, Pesca y Desarrollo Alimentario, México 154 pp
Sall J, Lee C, Lehman A (2007) JMP® star statistic: a guide to statistic and data analysis using JMP®, 4th edn. SAS Institute, Cary
Sun J, Song HL, Zhao J, Xiao Y, Qi R, Lin YT (2010) Effects of different dietary levels of Enteromorpha prolifera on nutrient availability and digestive enzyme activities of broiler chickens. Chin J Anim Nutr 22:1658–1664
Taboada C, Millán R, Míguez I (2010) Composition, nutritional aspects and effect on serum parameters of marine algae Ulva rigida. J Sci Food Agric 90:445–449
Tietz N (2006) Clinical guide to laboratory test. In: Tietz N (ed) A Guide, 4th edn. WB Saunders Co, Philadelphia
Velasco S, Rodríguez ML, Alzuela MC, Rebolé A, Ortiz LT (2010) Los prebióticos tipo inulina en alimentación aviar. I: Características y efectos a nivel intestinal. Rev Complutense Cien Vet 4:87–104
Ventura MR, Castañón JIR, McNab JM (1994) Nutritional value of seaweed (Ulva rigida) for poultry. Anim Feed Sci Technol 49:87–92
Wang SB, Shi XP, Zhou CF, Lin YT (2013) Entermorpha prolifera: effects on performance, carcass quality and small intestinal digestive enzyme activities of broilers. Chin J Anim Nutr 25:1332–1337
Xu ZR, Hu CH, Xia MS, Zhan XA, Wang MQ (2003) Effects of dietary fructo oligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult Sci 82:1030–1036
Zar JH (2010) Biostatistical analysis, 5th edn. Prentice-Hall Inc, Upper Saddle River
Acknowledgments
The authors are grateful to Efrain Flores Montaño for his help in field sampling, and to Diego Armando Falcón Vidal for his collaboration during the experiment. Alma Ribera Camacho assisted in the histological analysis; María Elena Sánchez and Diana Fischer provided editorial services. Thanks also to the person in charge of the Poultry Area of the Posta Zootécnica at the Universidad Autónoma de Baja California Sur for facilitating the conduct of the experiment. Casas-Valdez and Piñón-Gimate authors thank Estímulo al Desempeño de la Investigación (EDI), Comisión de Fomento a las Actividades Académicas (COFAA), and Cañedo-Castro scholarship granted by CONACYT and Beca al Estímulo Institucional de Formación de Investigadores (BEIFI), Instituto Politécnico Nacional (IPN).
Funding
This study was funded by the project Instituto Politécnico Nacional-SIP20161094.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The experiment was run in compliance with the Mexican standard NOM-069-200-1999. Also, the experimental procedures were performed in accordance with the Guidelines and Rules for Animal Experimentation and the Animal Ethics Committee, Universidad Autonoma de Baja California Sur, Mexico.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cañedo-Castro, B., Piñón-Gimate, A., Carrillo, S. et al. Prebiotic effect of Ulva rigida meal on the intestinal integrity and serum cholesterol and triglyceride content in broilers. J Appl Phycol 31, 3265–3273 (2019). https://doi.org/10.1007/s10811-019-01785-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-019-01785-x