The effects of L-arginine (Arg) and L-citrulline (Cit) supplementations in an Arg-deficient reduced-protein diet on tibia morphology and mineral composition were investigated in broilers maintained at the thermo-neutral (NT) and cyclic warm temperature (WT). Seven hundred and twenty Ross 308 male broilers were brooded together for the first 7 days and randomly assigned to four dietary treatments with 12 replicates of 15 birds each from days 8 to 35. The dietary treatments were standard protein diet (SP) with 22.3% and 20.9% crude protein in grower and finisher, respectively, an Arg-deficient reduced-protein diet with 2.5% lower protein (RP), and RP added with Arg (RP-Arg) or Cit (RP-Cit) at 0.28%. Dietary treatments were fed from day 8 with average bird’s body weights of 177±3.25 g. Cyclic warm temperature (33 °C ± 1 °C for 6 h per day) was applied in one of the climate-controlled rooms during the finisher phase (21 to 35 day), resulting in a 2 × 4 factorial arrangement of treatments with the factors were the dietary treatment and temperature. Birds fed the RP diet had lower tibia breaking strength (day 28), ash (day 35), and diameter (days 21 and 28) compared to those offered the SP diet (p<0.05). Birds fed the RP diet had lower serum K and tibia B and higher tibia Mn level on day 21; higher serum Ca, P, and Mg, and lower tibia B level on day 28 compared to the SP-fed birds (p<0.05). Supplementation with Arg or Cit compensated for the adverse effects of the RP diet on these traits (p<0.05). Interactions showed tibia diameter decreased in birds fed the SP diet compared to the RP and RP-Cit diets only when raised under cyclic WT on day 35 (p<0.05). Thus, supplementation of Arg or Cit to the RP diet was necessary to support bone morphology and mineralisation under normal and warm temperatures.
Attia, Y. A., R. A. Hassan, A. E. Tag El‐Din, & B. M. Abou‐Shehema. 2011. Effect of ascorbic acid or increasing metabolizable energy level with or without supplementation of some essential amino acids on productive and physiological traits of slow‐growing chicks exposed to chronic heat stress. J. Anim. Physiol. Anim. Nutr. 95:744-755. https://doi.org/10.1111/j.1439-0396.2010.01104.x
Aviagen. 2014a. Ross 308 Broiler Management Handbook. Ross Breeders Limited, Newbridge, Midlothian, Scotland, UK.
Aviagen. 2014b. Ross 308 Broiler Nutrition Specification. Ross Breeders Limited, Newbridge, Midlothian, Scotland, UK.
Belhadj, S. I., T. Najar, A. Ghram, & M. Abdrrabba. 2016. Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J. Anim. Physiol. Anim. Nutr. 100:401-412. https://doi.org/10.1111/jpn.12379
Belloir, P., B. Méda, W. Lambert, E. Corrent, H. Juin, M. Lessire, & S. Tesseraud. 2017. Reducing the CP content in broiler feeds: impact on animal performance, meat quality and nitrogen utilization. Animals. 11:1881-1889. https://doi.org/10.1017/S1751731117000660
Brickett, K. E., J. P. Dahiya, H. L. Classen, C. B. Annett, & S. Gomis. 2007. The impact of nutrient density, feed form, and photoperiod on the walking ability and skeletal quality of broiler chickens. Poult. Sci. 86:2117-2125. https://doi.org/10.1093/ps/86.10.2117
Castro, F. L. S., H. Y. Kim, Y. G. Hong, & W. K. Kim. 2019a. The effect of total sulfur amino acid levels on growth performance, egg quality, and bone metabolism in laying hens subjected to high environmental temperature. Poult. Sci. 98:4982-4993. https://doi.org/10.3382/ps/pez275
Castro, F. L. S., S. Su, H. Choi, E. Koo, & W. K. Kim. 2019b. L-arginine supplementation enhances growth performance, lean muscle, and bone density but not fat in broiler chickens. Poult. Sci. 98:1716-1722. https://doi.org/10.3382/ps/pey504
Chrystal, P. V., A. F. Moss, A. Khoddami, V. D. Naranjo, P. H. Selle, & S. Y. Liu. 2020. Effects of reduced crude protein levels, dietary electrolyte balance, and energy density on the performance of broiler chickens offered maize-based diets with evaluations of starch, protein, and amino acid metabolism. Poult. Sci. 99:1421-1431. https://doi.org/10.1016/j.psj.2019.10.060
Cowieson, A. J., R. Perez-Maldonado, A. Kumar, & M. Toghyani. 2020. Possible role of available phosphorus in potentiating the use of low protein diets for broiler chicken production. Poult. Sci. 99:6954-6963. https://doi.org/10.1016/j.psj.2020.09.045
Dao, H. T., N. K. Sharma, E. J. Bradbury, & R. A. Swick. 2021a. Response of meat chickens to different sources of arginine in low‐protein diets. J. Anim. Physiol. Anim. Nutr. 105:731-746. https://doi.org/10.1111/jpn.13486
Dao, H. T., N. K. Sharma, E. J. Bradbury, & R. A. Swick. 2021b. Effects of L-arginine and L-citrulline supplementation in reduced protein diets for broilers under normal and cyclic warm temperature. Anim. Nutr. 7:927-938. https://doi.org/10.1016/j.aninu.2020.12.010
Dao, H. T., N. K. Sharma, E. J. Bradbury, & R. A. Swick. 2021c. Response of laying hens to L-arginine, L-citrulline and guanidinoacetic acid supplementation in reduced protein diet. Anim. Nutr. 7:460-471. https://doi.org/10.1016/j.aninu.2020.09.004
del Barrio, A. S., W. D. Mansilla, A. Navarro-Villa, J. H. Mica, J. H. Smeets, L. A. den Hartog, & A. I. García-Ruiz. 2020. Effect of mineral and vitamin C mix on growth performance and blood corticosterone concentrations in heat-stressed broilers. J. Appl. Poult. Res. 29:23-33. https://doi.org/10.1016/j.japr.2019.11.001
Esser, A. F. G., D. R. M. Gonçalves, A. Rorig, A. B. Cristo, R. Perini, & J. I. M. Fernandes. 2017. Effects of guanidionoacetic acid and arginine supplementation to vegetable diets fed to broiler chickens subjected to heat stress before slaughter. Rev. Bras. Cienc. Avic. 19:429-436. https://doi.org/10.1590/1806-9061-2016-0392
Farag, M. R. & M. Alagawany. 2018. Physiological alterations of poultry to the high environmental temperature. J. Therm. Biol. 76:101-106. https://doi.org/10.1016/j.jtherbio.2018.07.012
Fouad, A. M., H. K. El-Senousey, X. J. Yang, & J. H. Yao. 2013. Dietary L-arginine supplementation reduces abdominal fat content by modulating lipid metabolism in broiler chickens. Animals. 7:1239-1245. https://doi.org/10.1017/S1751731113000347
Heaney, R. P. & D. K. Layman. 2008. Amount and type of protein influences bone health. Am. J. Clin. Nutr. 87:1567S-1570S. https://doi.org/10.1093/ajcn/87.5.1567S
Hilliar, M., N. Huyen, C. K. Girish, R. Barekatain, S. Wu, & R. A. Swick. 2019. Supplementing glycine, serine, and threonine in low protein diets for meat type chickens. Poult. Sci. 98:6857-6865. https://doi.org/10.3382/ps/pez435
Hosseini, S. M. & M. Afshar. 2017. Effect of diet form and enzyme supplementation on stress indicators and bone mineralisation in heat-challenged broilers fed wheat-soybean diet. Ital. J. Anim. Sci. 16:616-623. https://doi.org/10.1080/1828051X.2017.1321973
Jahanian, R. 2009. Immunological responses as affected by dietary protein and arginine concentrations in starting broiler chicks. Poult. Sci. 88:1818-1824. https://doi.org/10.3382/ps.2008-00386
Khattak, F. M., T. Acamovic, N. Sparks, T. N. Pasha, M. H. Joiya, Z. Hayat, & Z. Ali. 2012. Comparative efficacy of different supplements used to reduce heat stress in broilers. Pak. J. Zool. 44:31-41.
Kurtoğlu, F., V. Kurtoğlu, I. Celik, T. Kececi, & M. Nizamlioğlu. 2005. Effects of dietary boron supplementation on some biochemical parameters, peripheral blood lymphocytes, splenic plasma cells and bone characteristics of broiler chicks given diets with adequate or inadequate cholecalciferol (vitamin D3) content. Br. Poult. Sci. 46:87-96. https://doi.org/10.1080/00071660400024001
Kvidera, S. K., E. A. Horst, E. J. Mayorga, J. T. Seibert, M. A. Al-Qaisi, J. W. Ross, R. P. Rhoads, & L. H. Baumgard. 2016. 0995 Effect of supplemental citrulline on thermal and production parameters during heat stress in growing pigs. J. Anim. Sci. 94:477. https://doi.org/10.2527/jam2016-0995
Lips, P. 2012. Interaction between vitamin d and calcium. Scand. J. Clin. Lab. Invest. 72:60-64.
Liu, F., E. M. de Ruyter, R. Z. Athorn, C. J. Brewster, D. J. Henman, R. S. Morrison, R. J. Smits, J. J. Cottrell, & F. R. Dunshea. 2019. Effects of L‐citrulline supplementation on heat stress physiology, lactation performance and subsequent reproductive performance of sows in summer. J. Anim. Physiol. Anim. Nutr. 103:251-257. https://doi.org/10.1111/jpn.13028
Luo, J., J. Song, L. Liu, B. Xue, G. Tian, & Y. Yang. 2018. Effect of epigallocatechin gallate on growth performance and serum biochemical metabolites in heat-stressed broilers. Poult. Sci. 97:599-606. https://doi.org/10.3382/ps/pex353
Mosleh, N., T. Shomali, F. Nematollahi, Z. Ghahramani, M. S. A. Khadi, & F. Namazi. 2018. Effect of different periods of chronic heat stress with or without vitamin C supplementation on bone and selected serum parameters of broiler chickens. Avian Pathol. 47:197-205. https://doi.org/10.1080/03079457.2017.1401212
NHMRC. 2013. Australian Code of Practice for the Care and Use of Animals for Scientific Purposes. 8th Ed. The National Health and Medical Research Council, Australia.
Oliveira, M. C., U. M. Arantes, & J. H. Stringuini. 2010. Efeito do balanco eletrolitico da racao sobre parametros osseos e da cama de frango. Biotemas. 23:203-209. https://doi.org/10.5007/2175-7925.2010v23n1p203
Onderci, M., N. Sahin, K. Sahin, T. A. Balci, M. F. Gursu, V. Juturu, & O. Kucuk. 2006. Dietary arginine silicate inositol complex during the late laying period of quail at different environmental temperatures. Br. Poult. Sci. 47:209-215. https://doi.org/10.1080/00071660600611052
Patience, J. F. 1990. A review of the role of acid-base balance in amino acid nutrition. J. Anim. Sci. 68:398-408. https://doi.org/10.2527/1990.682398x
Seedor, J. G., H. A. Quartuccio, & D. D. Thompson. 1991. The biophosphonate alendronate (MK - 217) inhibits bone loss due to ovariectomy in rats. J. Bone Miner. Res. 6:339-346. https://doi.org/10.1002/jbmr.5650060405
Sgavioli, S. C. H. F. Domingues, E. T. Santos, T. C. O. de Quadros, L. L. Borges, R. G. Garcia, M. J. Q. L. Louzada, & I. C. Boleli. 2016. Effect of in-ovo ascorbic acid injection on the bone development of broiler chickens submitted to heat stress during incubation and rearing. Rev. Bras. Cienc. Avic. 18:153-162. https://doi.org/10.1590/18069061-2015-0075
Silva, L. M. G. S., A. E. Murakami, J. I. M. Fernandes, D. Dalla Rosa, & J. F. Urgnani. 2012. Effects of dietary arginine supplementation on broiler breeder egg production and hatchability. Rev. Bras. Cienc. Avic. 14:267-273. https://doi.org/10.1590/S1516-635X2012000400006
Su, C. L. & R. E. Austic. 1999. The recycling of L-citrulline to L-arginine in a chicken macrophage cell line. Poult. Sci. 78:353-355. https://doi.org/10.1093/ps/78.3.353
Talaty, P. N., M. N. Katanbaf, & P. Y. Hester. 2009. Life cycle changes in bone mineralisation and bone size traits of commercial broilers. Poult. Sci. 88:1070-1077. https://doi.org/10.3382/ps.2008-00418
Wu, S. B., R. A. Swick, J. Noblet, N. Rodgers, D. Cadogan, & M. Choct. 2019. Net energy prediction and energy efficiency of feed for broiler chickens. Poult. Sci. 98:1222-1234. https://doi.org/10.3382/ps/pey442
Zaman, Q. U., T. Mushtaq, H. Nawaz, M. A. Mirza, S. Mahmood, T. Ahmad, M. E. Babar, & M. M. H. Mushtaq. 2008. Effect of varying dietary energy and protein on broiler performance in hot climate. Anim. Feed Sci. Technol. 146:302-312. https://doi.org/10.1016/j.anifeedsci.2008.01.006
Zanu, H. K., S. K. Kheravii, N. K. Morgan, M. R. Bedford, & R. A. Swick. 2020. Interactive effect of dietary calcium and phytase on broilers challenged with subclinical necrotic enteritis: 3. serum calcium and phosphorus, and bone mineralization. Poult. Sci. 99:3617-3627. https://doi.org/10.1016/j.psj.2020.04.012
Zemel, M. B. 1988. Calcium utilization: effect of varying level and source of dietary protein. Am. J. Clin. Nutr. 48:880-883. https://doi.org/10.1093/ajcn/48.3.880
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Authors submitting manuscripts should understand and agree that copyright of manuscripts of the article shall be assigned/transferred to Tropical Animal Science Journal. The statement to release the copyright to Tropical Animal Science Journal is stated in Form A. This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License (CC BY-SA) where Authors and Readers can copy and redistribute the material in any medium or format, as well as remix, transform, and build upon the material for any purpose, but they must give appropriate credit (cite to the article or content), provide a link to the license, and indicate if changes were made. If you remix, transform, or build upon the material, you must distribute your contributions under the same license as the original.