Abstract

This study aimed to assess the effects of environmental temperature and age of broilers on the energy value of corn. A total of 288 Cobb 500 chicks were distributed in a complete randomized design with a split-plot arrangement and six replications of six chicks each. The main plot consisted of three temperatures (cold: 18 ºC; thermoneutral: 25 ºC; and hot: 33 ºC), while the secondary plot consisted of age (initial: 11 to 14 days; growing: 25 to 28 days; and final: 39 to 42 days). The basal diet was based on corn and soybean meal. The test diet was produced by replacing the basal diet for test food: 40% corn + 60% basal diet. The mean values of AMEn observed for broiler chicks under cold, thermoneutral, and hot temperatures were 3322, 3279, and 3233 kcal/kg of natural matter, respectively, and 3215, 3218, and 3400 kcal/ kg of natural matter for the initial, growing, and final phases, respectively. Overall, the metabolizable energy values of corn and the balance and coefficients of metabolizability of nutrients in the test diet increased with the broiler age, but the true metabolizable energies of corn were not affected by environmental temperature. The balance and coefficients of metabolizability of nutrients in the test diet decreased due to heat exposure during the growing and final phases.

Keywords:
nitrogen balance; metabolizable energy; heat stress; cold stress; metabolizability of nutrients

Resumo

O objetivo deste trabalho foi determinar o efeito da temperatura ambiente e da idade da ave sobre o valor energético do milho. Foram utilizados 288 pintos de corte, da linhagem Cobb 500, distribuídos em delineamento experimental inteiramente casualizado em esquema de parcelas subdivididas no tempo, sendo as parcelas as três temperaturas de criação (fria: 18 ºC; termoneutra: 25 ºC e quente: 33 ºC) e as subparcelas as três idades de avaliação (inicial: 11 a 14; crescimento: 25 a 28 e final: 39 a 42 dias), com seis repetições de seis aves cada. A dieta basal foi composta por milho e farelo de soja. A dieta teste foi produzida substituindo a dieta basal pelo alimento teste: 40% de milho + 60% da dieta basal. Encontraram-se valores médios de energia metabolizável aparente, corrigida pelo balanço de nitrogênio (EMAn) do milho, para aves criadas em 18 ºC; 25 ºC e 33 ºC de 3322, 3279 e 3233 kcal/kg de matéria natural, respectivamente, e para as fases de 11 a 14; 25 a 28 e 39 a 42 dias de 3215, 3218 e 3400 kcal/kg de matéria natural, respectivamente. De um modo geral, os valores de energia metabolizável do milho, os balanços e os coeficientes de metabolizabilidade dos nutrientes da dieta teste aumentam com a idade do frango de corte, porém as energias metabolizáveis verdadeiras do milho não foram afetadas pela temperatura ambiente. Os balanços e os coeficientes de metabolizabilidade dos nutrientes da dieta teste foram reduzidos em estresse por calor para aves na fase de crescimento e final.

Palavras-chave:
balanço de nitrogênio; energia metabolizável; estresse por calor; estresse por frio; metabilizabilidade de nutrientes

Introduction

The nutritional composition of ingredients and their respective energy values must be as accurate as possible in feed formulation, justifying the determination of the chemical composition and metabolizable energy values of national foods commonly used in animal nutrition.

The update of nutrient requirements in feed formulations is important because of the productivity and maintenance of broilers, which are altered due to genetic improvement and other factors, such as age, sex, lines, and environmental temperature,¹1 Saeeda M, Abbasc G, Alagawanyd M, Kambohe AA, El-Hackd MEA, Khafagaf AF, Chaoa S. Heat stress management in poultry farms: A comprehensive overview. Journal of Thermal Biology [Internet]. 2019 [cited 2021 January 06]; 84, 414-425, Available from: https://www.sciencedirect.com/science/article/pii/S0306456519300658?via%3Dihub. English.
https://www.sciencedirect.com/science/ar... which modify the use of energy and protein.

Corn is the main energy ingredient in poultry feed, but it also contributes a good part to dietary protein. It is responsible for approximately 25% of the total crude protein in chicken diets,²2 Bertechini AG, Fassani EJ, Fialho ET. Utilização do milho QPM (quality protein maize) para aves. Ciência e Agrotecnologia, v. 23, n. 2, p. 434-440, 1999. Portuguese. with its greatest limitation, as a source of nutrients, the low content of the amino acids lysine and tryptophan.

The determination of the metabolizable energy values of ingredients considering the age may contribute to the caloric adequacy of diets. The digestive capacity of the poultry increases as their age advances, with increased use of nutrients due to the development of accessory organs and the digestive system.³3 Murawska D. The Effect of Age on Growth Performance and Carcass Quality Parameters in Different Poultry Species. In: Manafi M. editor. Poultry Science. [Internet]. 2017 [cited 2021 January 05]; 33-50. Available from: https://www.intechopen.com/books/poultry-science/the-effect-of-age-on-growth-performance-and-carcass-quality-parameters-in-different-poultry-species. English.
https://www.intechopen.com/books/poultry... Thus, the formulation using the metabolizable energy values of the food adjusted to the poultry age can lead to a higher optimization in the formulation and less waste of nutrients in the feed, improving feed conversion and, consequently, decreasing the food cost.

In general, the recommendations on nutrition and feeding of broilers are carried out at an environmental temperature within the comfort range of growing poultry, which is not adequate to meet their energy requirements in a heat or cold stress environment, which may be one of the causes for the decrease in broiler performance.

Considering that poultry voluntarily reduce food intake as the environmental temperature rises above the thermal comfort range,⁴4 Syafwan S, Wermink GJD, Kwakkel RP, Verstegen MWA. Dietary self-selection by broilers at normal and high temperature changes feed intake behavior, nutrient intake, and performance. Poultry Science [Internet]. 2012 March [cited 2019 Dec 10]; 91(3): 537-549. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119402162. English.
https://www.sciencedirect.com/science/ar... a feed formulated for thermoneutral conditions would not be adequate to meet their energy requirements in a heat-stress environment.

This study was developed to determine the effect of the environmental temperature and broiler age on the energy value of corn.

Material and methods

The experiment was conducted at the School of Veterinary Medicine and Animal Science, UNESP, campus of Botucatu, at the Laboratory of Poultry Nutrition, according to the ethical principles in animal experimentation approved by the Committee on Ethics in Animal Experimentation (Protocol No. 160/2007-CEEA). A total of 288 male Cobb 500 broiler chicks were used. The experimental design was completely randomized in a split-plot scheme in time, with the plots consisting of three temperatures (18, 25, and 33 ºC) and the subplots consisting of three ages of assessment (initial: 11 to 14 days; growth: 25 to 28 days; and final: 39 to 42 days), with six replications of six animals.

A total of 216 out of the 288 broiler chicks were distributed in 36 galvanized wire cages, measuring 0.50 m high, 0.50 m wide, and 0.60 m deep, distributed in three temperature-controlled chambers (hot, thermoneutral, and cold) with the cages arranged in two batteries of two floors each, totaling 12 cages/chamber. The remaining 72 broiler chicks were used in an extra treatment (fasting for 72 hours) to assess endogenous and metabolic losses at each age of assessment within the three climatic chambers to determine a correction factor to estimate the true metabolizable energy of corn.⁵5 Sakomura NK, Rostagno HS. Métodos de pesquisa em nutrição de monogástricos. Jaboticabal: Funep, 2007, 283p.

The basal diet was formulated based on corn and soybean meal, and the food composition and nutritional requirements were obtained from Rostagno et al.⁶6 Rostagno, HS, Albino LFT, Donzele JL, Gomes PC, Oliveira R FM, Lopes DC, Ferreira AJP, Toledo Barreto SL. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. 2 st ed. Viçosa: UFV; 2005. 186p. Portuguese. (Table 1). The test diet was obtained by replacing part of the basal diet with the test food (40% corn + 60% basal diet).

All animals remained in a hot chamber until six days of age in order not to compromise their initial performance. Then, they were randomly distributed in the three chambers (cold, thermoneutral, and hot). The values of environmental temperature, relative air humidity, and temperature-humidity index (THI), determined in the climatic chambers during the experimental period, are shown in Table 2. The values of environmental temperature and relative air humidity were collected using a thermo-hygrometer, and a globe thermometer was used to calculate THI. The equipment remained inside the climatic chambers throughout the experimental period. Data collection was carried out in the morning and at the end of the day.

Three metabolic tests with four days of adaptation (7 to 10, 21 to 24, and 35 to 38 days of age) and four days of total excreta collection (11 to 14, 25 to 28, and 39 to 42 days of age) were performed to assess the use of metabolizable energy and the metabolization of corn nutrients with increasing age.

Samples of feed and excreta were stored frozen (−16 ºC) for the analyses of dry matter (DM), nitrogen (N), and ether extract (EE), according to the methodology described by Silva & Queiroz.⁸8 Silva DJ, Queiroz AC. Análise de alimentos: Métodos químicos e biológicos. 3 st ed. Viçosa: UFV; 2002. 235p. Portuguese. The results allowed calculating the coefficients of apparent and true metabolizability of dry matter (CMDM and CMDMT), ether extract (CMEE and CMEET), and nitrogen (CMN and CMNT) of the test diet.

The gross energy values of diets and excreta were obtained using an Ika Works C-200 calorimeter, which allowed calculating the apparent and true metabolizable energy (AME and TME), subsequently corrected by the nitrogen balance (AMEn and TMEn) in the natural matter using the equations proposed by Matterson et al.⁹9 Matterson LD, Potter LM, Stutz NW, Singsen EP. The metabolizable energy of feeds ingredients for chickens. Storrs, Connecticut : University of Connecticut - Agricultural Experiment Station; 1965. p. 3-11. (Research Report, 7). The metabolizability coefficients of food energy were determined based on the values of gross energy, AME, AMEn, TME, and TMEn.

Statistical analyses were performed using analysis of variance by the software SAEG.¹⁰10 Saeg - Sistema de análises estatísticas e genéticas: user guide [CD-ROM] Version 9.1: Universidade Federal de Viçosa, UFV, 2007. Significant differences between the means of treatments were verified using the Tukey test (5% probability).

Results and discussion

The chemical composition of corn in the natural matter used in the experiment was 87.84% dry matter, 7.5% crude protein, 3.4% ether extract, and 3968 kcal/kg of crude energy. The protein value obtained for corn was lower than those found by Rodrigues et al.¹¹11 Rodrigues PB, Rostagno HS, Albino LFT, Gomes PC, Barboza WA, Santana RT. Valores Energéticos do Milheto, do Milho e Subprodutos do Milho, Determinados com Frangos de Corte e Galos Adultos. Revista Brasileira de Zootecnia [Internet]. 2001 Nov [cited 2019 oct 12]; 30(6): 1767-1778. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-35982001000700015&lng=en&nrm=iso&tlng=pt. Portuguese.
https://www.scielo.br/scielo.php?script=... of 8.07%, Mello et al.¹²12 Mello HHC, Gomes PC, Rostagno HS, Albino LFT, Souza RM, Calderano AA. Valores de energia metabolizável de alguns alimentos obtidos com aves de diferentes idades. [Metabolizable energy values of feedstuffs obtained from poultry at different ages] Revista Brasileira de Zootecnia [Internet]. 2009 May [cited 2019 oct 12]; 38(5): 863-868. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-35982009000500012&lng=en&nrm=iso. Portuguese.
https://www.scielo.br/scielo.php?script=... of 7.91%, and Kato et al.¹³13 Kato KR, Bertechini AG, Fassani EJ, Brito JAG, Castro SF. Metabolizable energy of corn hybrids for broiler chickens at different ages. [Energia metabolizável de milhos híbridos para frangos de corte em diferentes idades] Ciência Agrotécnica [Internet]. 2011 Dec [cited 2019 July 22]; 35(6): 1218-1226. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-70542011000600024. English.
https://www.scielo.br/scielo.php?script=... from 8.60 to 9.60%, and higher than those mentioned by D’Agostini et al.¹⁴14 D’Agostini P, Gomes PC, Albino LFT, Rostagno HS, Sá LM. Valores de composição química e energética de alguns alimentos para aves. [Values of chemical and energy composition of some feedstuffs for broiler chicks]. Revista Brasileira de Zootecnia [Internet]. 2004 Jan [cited 2019 july 21];33(1): 128-134. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119411760?via%3Dihub. Portuguese.
https://www.sciencedirect.com/science/ar... of 7.33% and Nery et al.¹⁵15 Nery LR, Albino LFT, Rostagno HS, Campos AMA, Silva CR. Valores de energia metabolizável de alimentos determinados com frangos de corte. [Metabolizable energy values of feedstuffs obtained from poultry at different ages] Revista Brasileira de Zootecnia [Internet]. 2007 Sept [cited 2019 oct 12]; 36(5): 1354-1358. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-35982007000600018&lng=en&nrm=iso&tlng=pt. Portuguese.
https://www.scielo.br/scielo.php?script=... of 7.26%. The frequency of nitrogen fertilization can influence the crude protein content of the grain.¹³13 Kato KR, Bertechini AG, Fassani EJ, Brito JAG, Castro SF. Metabolizable energy of corn hybrids for broiler chickens at different ages. [Energia metabolizável de milhos híbridos para frangos de corte em diferentes idades] Ciência Agrotécnica [Internet]. 2011 Dec [cited 2019 July 22]; 35(6): 1218-1226. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-70542011000600024. English.
https://www.scielo.br/scielo.php?script=... The gross energy was higher than that found by Nery et al.¹⁵15 Nery LR, Albino LFT, Rostagno HS, Campos AMA, Silva CR. Valores de energia metabolizável de alimentos determinados com frangos de corte. [Metabolizable energy values of feedstuffs obtained from poultry at different ages] Revista Brasileira de Zootecnia [Internet]. 2007 Sept [cited 2019 oct 12]; 36(5): 1354-1358. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-35982007000600018&lng=en&nrm=iso&tlng=pt. Portuguese.
https://www.scielo.br/scielo.php?script=... of 3939 kcal/kg and lower than the result of D’Agostini et al.¹⁴14 D’Agostini P, Gomes PC, Albino LFT, Rostagno HS, Sá LM. Valores de composição química e energética de alguns alimentos para aves. [Values of chemical and energy composition of some feedstuffs for broiler chicks]. Revista Brasileira de Zootecnia [Internet]. 2004 Jan [cited 2019 july 21];33(1): 128-134. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119411760?via%3Dihub. Portuguese.
https://www.sciencedirect.com/science/ar... of 4089 kcal/kg and Mello et al.¹²12 Mello HHC, Gomes PC, Rostagno HS, Albino LFT, Souza RM, Calderano AA. Valores de energia metabolizável de alguns alimentos obtidos com aves de diferentes idades. [Metabolizable energy values of feedstuffs obtained from poultry at different ages] Revista Brasileira de Zootecnia [Internet]. 2009 May [cited 2019 oct 12]; 38(5): 863-868. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-35982009000500012&lng=en&nrm=iso. Portuguese.
https://www.scielo.br/scielo.php?script=... of 4009 kcal/kg. These differences occur because soil fertility, climate, genetics, storage, and processing are factors that interfere with the chemical composition of food.¹⁶16 Butolo JE. Qualidade de ingredientes na alimentação animal. Campinas: J.E Butolo, 2002. 430p.

An interaction was observed between environmental temperature and raising phase for AME, AMEn, TME, and TMEn (Table 3). Broilers at the growing phase (25 to 28 days of age) raised in the cold chamber used the energy from corn better when compared to animals raised under thermoneutral temperature (AME) (P=0.0315) and better than animals raised under thermoneutral and hot temperature after correction by the nitrogen balance (P=0.048). The correction of endogenous losses (TME and TMEn) canceled the differences between temperatures, with no differences in the metabolizable energies assessed within the raising phases.

Geraert et al.¹⁷17 Geraert PA, Guillaumin S, Zuprizal LM. Effect of high ambient temperature on dietary ME value in genetically lean and fat chickens. Poultry Science [Internet]. 1992 Dec [cited 2019 Nov 14]; 71(12): 2113-2116. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119337812. English.
https://www.sciencedirect.com/science/ar... and Faria Filho et al.¹⁸18 Faria Filho DE, Campos DMB, Afonso-Torres KA, Vieira BS, Rosa PS, Vaz AM, Macari M, Furlan RL. Protein levels for heat-exposed broilers: performance, nutrient digestibility, and protein and energy metabolism. International Journal of Poultry Science [Internet]. 2007 [cited 2019 oct 29]; 6(3): 187-194. Available from: https://pdfs.semanticscholar.org/206b/453009848a1c221a8a193c72723655c1f99f.pdf. English.
https://pdfs.semanticscholar.org/206b/45... found that the metabolizable energy content of the feed is not changed by the exposure of chickens to heat, while Keshavarz & Fuller¹⁹19 Keshavarz K, Fuller HL. The influence of widely fluctuating temperatures on heat production and energetic efficiency of broilers. Poultry Science [Internet]. 1980 Sept [cited 2019 Dec 10]; 59(9): 2121-2128. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119356536. English.
https://www.sciencedirect.com/science/ar... observed higher energy levels and Yamazaki & Zi-yi²⁰20 Yamazaki M, Zi-Yi Z. A note on the effect of temperature on true and apparent metabolizable energy values of a layer diet. British Poultry Science [Internet]. 1982 Nov [cited 2019 Nov 14]; 23(1): 447-450. Available from: https://www.tandfonline.com/doi/pdf/10.1080/00071688208447977?needAccess=true. English.
https://www.tandfonline.com/doi/pdf/10.1... found reduced energy levels (12-month-old Leghorn roosters) with increasing temperature. These different results can be attributed to the specific experimental conditions of each study, such as line, nutritional levels, ingredients, sex, and assessment period (age).

An explanation for these findings was proposed by Hai et al.²¹21 Hai L, Rong D, Zhang Z-Y. The effect of environment on the digestion of broilers. Journal of Animal Physiology and Animal Nutrition [Internet]. 2001 Dec [cited 2019 July 22]; 83(2): 57-64. Available from: https://www.researchgate.net/publication/229449543_The_effect_of_thermal_environment_on_the_digestion_of_broilers. English.
https://www.researchgate.net/publication... , who compared the effect of temperature (5, 21, and 32 ºC) on the digestive process of broilers and found that the enzymatic activity of trypsin and amylase decreased due to heat, not being influenced by low temperature. The pair-feeding approach of this experiment allowed the authors to conclude that, although at a low intensity, the food restriction imposed by exposure to heat improved the digestibility of all nutrients in the diet. The occurrence of these antagonistic effects is one of the justifications for the difficulty in finding and accurately predicting the response of broilers to the thermal challenge, in addition to being the cause of many of the discrepant results presented in the literature.

The mean values of the temperature-humidity index (THI) for the thermal comfort range of poultry are between 71 and 76.²²22 Silva MAN, Barbosa Filho AD, Rosário MF, Silva CJM, Silva IJO, Savino VJM, Coelho AAD. Fatores de estresse associados à criação de linhagens de avós de frangos de corte. [Environmental influence on the performance of parental lines of broiler chicken] Revista Brasileira de Zootecnia [Internet]. 2007 June [cited 2019 oct 12]; 36(3): 652-659. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-35982007000300019&lng=en&nrm=iso&tlng=pt. Portuguese.
https://www.scielo.br/scielo.php?script=... Therefore, the THI value of 82.19 (Table 2) for the hot chamber shows that the animals were stressed by heat, but it was not enough to affect the use of corn energy. The lower relative humidity (RH) in the hot chamber during the experiment may have reduced the effect of stress.

Another cause of the absence of the effect of heat stress on ME may be due to the low percentage of protein in the diet with 40% corn (mean of 15% CP), which promoted a reduction in the caloric increase, usually caused by protein-rich diets.²³23 Mcleod MG. Effects of amino acid balance and energy: protein ratio on energy and nitrogen metabolism in male broiler chicken. British Poultry Science. 1997; 38:405-411. However, even the high-energy feed (3250 kcal) under a heat stress environment did not impede for the broilers to maintain the same feed intake and weight gain adequate at 35 and 42 days of age.²⁴24 Melo FVST, Souza ARL, Cruz Neto MA, Mendes DB, Melo JFB. Níveis de energia metabolizável para frangos de corte em estresse térmico. [Metabolisable energy levels for stress broilers under thermal stress] Revista Brasileira de Saúde e Produção Animal [Internet]. 2020 [cited 2021 January 05]; 21: 01-13. Available from: https://www.scielo.br/scielo.php?script=sci_abstract&pid=S1519-99402020000100800&lng=en&nrm=iso&tlng=pt. Portuguese.
https://www.scielo.br/scielo.php?script=...

The absence of a sanitary challenge in the experiment may also have assisted in maintaining the use of ME even under heat stress. Broilers infected by Salmonella and raised at a temperature of 31 ºC from 35 to 41 days of age presented lower weight gain and feed intake and worse feed conversion.²⁵25 Quinteiro Filho WM, Gomes AVS, Pinheiro ML, Ribeiro A, Ferraz de Paula V, Astolfi Ferreira CS, Ferreira AJP, Palermo Neto J. Heat stress impairs performance and induces intestinal inflammation in broiler chickens infected with Salmonella Enteritidis. Avian Pathology [Internet]. 2012 [cited 2021 January 05]; 41:5, 421-427, Available from: https://www.researchgate.net/publication/230695770_Heat_stress_impairs_performance_and_induces_intestinal_inflammation_in_broiler_chickens_infected_with_Salmonella_Enteridis. English.
https://www.researchgate.net/publication...

Animals raised in the cold chamber showed no difference between ages (Table 3) for all calculated energies. The results of the thermoneutral and hot chambers showed that older animals (final phase) had better use of the energy from corn than the other ages in the initial and growing phases (P<0.001). This result may be related to the maturation of the gastrointestinal tract, which, according to Uni et al.,²⁶26 Uni, Z.; Ganot, S.; Sklan, D. Posthatch development of mucosal function in the broiler small intestine. Poultry Science [Internet]. 1998 January [cited 2019 Dec 10]; 77(1): 75-82. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119407700?via%3Dihub#! English.
https://www.sciencedirect.com/science/ar... is established at 16 days of age in broilers.

The determination of the metabolizable energy of feed ingredients before 14 days of age may present lower values than those obtained with older birds, and the metabolizable energy values determined in older broilers may overestimate the availability of energy for younger birds.²⁷27 Yang Z, Pirgozliev VR, Rose SP, Woods P, Yang HM, Wang ZY, Bedford DMR. Effect of age on the relationship between metabolizable energy and digestible energy for broiler chickens. Poultry Science [Internet]. 2020 January [cited 2020 April 29]; 99(1): 320-330. Available from: https://pdfs.semanticscholar.org/206b/453009848a1c221a8a193c72723655c1f99f.pdf. English.
https://pdfs.semanticscholar.org/206b/45...

Sakomura et al.²⁸28 Sakomura NK, Del Bianchi M, Pizauro Jr JM, Café MB, Freitas ER. Efeito da idade dos frangos de corte na atividade enzimática e digestibilidade dos nutrientes do farelo de soja e da soja integral. [Effect of age on enzyme activity and nutrients digestibility for broilers fed soybean meal and full fat soybean] Revista Brasileira de Zootecnia [Internet]. 2004 July [cited 2019 oct 12]; 33(4): 924-935. Available from: https://www.scielo.br/scielo.php?pid=S1516-35982004000400013&script=sci_arttext&tlng=en. Portuguese.
https://www.scielo.br/scielo.php?pid=S15... found a linear increase in the activity of amylase, trypsin, and lipase with the advancing age of broilers (1 to 7, 8 to 14, 15 to 21, and 22 to 28 days), and the phase of the highest increase occurred between the first and second weeks of age, coinciding with the maximum allometric growth of pancreas.

Batal & Parsons²⁹29 Batal AB, Parsons CM. Utilization of various carbohydrate sources as affected by age in the chick. Poultry Science [Internet]. 2004 July [cited 2019 Oct 10];83(7): 1140-1147. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119426667. English.
https://www.sciencedirect.com/science/ar... studied the effect of age on carbohydrate digestibility and found that the AMEn values of corn increased from 12 to 15% with age. In the current study, the increase in AMEn in broilers at 14 days for 42 days of age was around 5.5%. Mello et al.¹²12 Mello HHC, Gomes PC, Rostagno HS, Albino LFT, Souza RM, Calderano AA. Valores de energia metabolizável de alguns alimentos obtidos com aves de diferentes idades. [Metabolizable energy values of feedstuffs obtained from poultry at different ages] Revista Brasileira de Zootecnia [Internet]. 2009 May [cited 2019 oct 12]; 38(5): 863-868. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-35982009000500012&lng=en&nrm=iso. Portuguese.
https://www.scielo.br/scielo.php?script=... found no differences in the metabolizable energy of corn with increasing age in metabolic assays with broilers from 10 to 17, 26 to 33, and 40 to 47 days of age and 25-week old Leghorn roosters.

The results of AMEn found for corn were lower than those presented by the Brazilian Tables for Poultry and Swine³⁰30 Rostagno HS, Albino LFT, Hannas MI, Donzele JL, Sakomura NK, Perazzo FG, Saraiva A, Teixeira ML, Rodrigues PB, Oliveira RF, Barreto SLT, Brito CO. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. 4st ed. Viçosa: UFV; 2017. 488p. Portuguese. (corn with 7.86% protein and 3364 kcal/kg in the natural matter), except for broilers raised at cold and thermoneutral temperatures at the final phase (3379 and 3459 kcal/kg) for AMEn. However, the values found by Rostagno et al.³⁰30 Rostagno HS, Albino LFT, Hannas MI, Donzele JL, Sakomura NK, Perazzo FG, Saraiva A, Teixeira ML, Rodrigues PB, Oliveira RF, Barreto SLT, Brito CO. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. 4st ed. Viçosa: UFV; 2017. 488p. Portuguese. are compilations of studies with broilers at different ages and roosters. This study showed lower values for heat stress temperature than those found by Rostagno et al.³⁰30 Rostagno HS, Albino LFT, Hannas MI, Donzele JL, Sakomura NK, Perazzo FG, Saraiva A, Teixeira ML, Rodrigues PB, Oliveira RF, Barreto SLT, Brito CO. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. 4st ed. Viçosa: UFV; 2017. 488p. Portuguese. and, therefore, feed formulation for broilers under stress based on metabolizable energy values acquired at thermoneutral temperature can cause a reduction in the animal performance.

Several studies have assessed the energy value of corn. D’Agostini et al.¹⁴14 D’Agostini P, Gomes PC, Albino LFT, Rostagno HS, Sá LM. Valores de composição química e energética de alguns alimentos para aves. [Values of chemical and energy composition of some feedstuffs for broiler chicks]. Revista Brasileira de Zootecnia [Internet]. 2004 Jan [cited 2019 july 21];33(1): 128-134. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119411760?via%3Dihub. Portuguese.
https://www.sciencedirect.com/science/ar... found mean values of AME and AMEn of 3246 and 3235 kcal/kg in the natural matter, respectively, for corn. Vieira et al.³¹31 Vieira RO, Rodrigues PB, Freitas RTF, Nascimento GAJ, Silva EL, Hespanhol R. Composição química e energia metabolizável de híbridos de milho para frangos de corte. [Chemical composition and metabolizable energy of corn hybrids for broilers] Revista Brasileira de Zootecnia [Internet]. 2007 July [cited 2019 oct 12]; 36(4): 832-838. Available from: https://www.scielo.br/scielo.php?pid=S1516-35982004000400013&script=sci_arttext&tlng=en. Portuguese.
https://www.scielo.br/scielo.php?pid=S15... also found that the apparent metabolizable energy, corrected for the mean of corn hybrids, reached 3744 kcal/kg, ranging from 3405 to 4013 kcal/kg of DM. Generoso et al.³²32 Generoso RAR, Gomes PC, Rostagno HS, Albino LFT, Barreto SLT, Brumano G. Composição química e energética de alguns alimentos para frangos de corte em duas idades. [Chemical and energy composition of some feeds for broiler chicks and two ages] Revista Brasileira de Zootecnia [Internet]. 2008 July [cited 2019 oct 12]; 37(7): 1251-1256. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-35982008000700016&lng=en&nrm=iso&tlng=pt. Portuguese.
https://www.scielo.br/scielo.php?script=... found mean values of apparent metabolizable energy, corrected by the nitrogen balance of corn, of 3351 and 3524 kcal/kg in the natural matter determined in broilers at the growing (21 to 30 days of age) and final phases (41 to 50 days), respectively.

The AME values were higher than the AMEn values in all treatments due to the positive nitrogen balance. This characteristic is normal when ME values are determined in growing broilers, as this phase presents higher retention of nitrogen for the deposition of protein tissue. This difference is more pronounced when the correction for endogenous and metabolic losses is performed.¹⁵15 Nery LR, Albino LFT, Rostagno HS, Campos AMA, Silva CR. Valores de energia metabolizável de alimentos determinados com frangos de corte. [Metabolizable energy values of feedstuffs obtained from poultry at different ages] Revista Brasileira de Zootecnia [Internet]. 2007 Sept [cited 2019 oct 12]; 36(5): 1354-1358. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-35982007000600018&lng=en&nrm=iso&tlng=pt. Portuguese.
https://www.scielo.br/scielo.php?script=...

The TME values of corn were, on average, 5.3% higher than the AME values for broilers raised in the hot chamber, a difference higher than that of the other chambers, that is, 3.3 and 4.5% for the cold and the thermoneutral chambers, respectively. The methodology consisted of total excreta collection, with the animals fed ad libitum and no interference in the intake volume. Consequently, the AME and TME values were similar. However, the reduction in intake due to heat stress in the hot chamber overestimated the result of TME, increasing the difference between AME and TME.

An interaction (P<0.001) was observed between environmental temperature and age of broilers for the apparent and true nitrogen (NB and TNB) and ether extract (EEB and TEEB) balance of the test diet (Table 4). The results at the initial phase (11 to 14 days of age) showed no interference of the environmental temperature for the evaluated variables (NN, TNB, EEB, and TEEB). The apparent and true nitrogen balances were higher for broilers stressed by cold at the growing (P<0.001) and final phases (P<0.001). The worst nitrogen balance for broilers under heat stress has occurred due to the lower efficiency of nitrogen retention, with protein metabolization reduced by heat, regardless of sex and diet.¹⁸18 Faria Filho DE, Campos DMB, Afonso-Torres KA, Vieira BS, Rosa PS, Vaz AM, Macari M, Furlan RL. Protein levels for heat-exposed broilers: performance, nutrient digestibility, and protein and energy metabolism. International Journal of Poultry Science [Internet]. 2007 [cited 2019 oct 29]; 6(3): 187-194. Available from: https://pdfs.semanticscholar.org/206b/453009848a1c221a8a193c72723655c1f99f.pdf. English.
https://pdfs.semanticscholar.org/206b/45... ^,3333 Faria Filho DE, Rosa OS, Figueiredo DF, Dahlke F, Macari M, Furlan RL. Dietas de baixa proteína no desempenho de frangos criados em diferentes temperaturas. [Low-protein diets on broilers performance reared under different temperatures]. Pesquisa Agropecuária Brasileira [Internet]. 2006 Jan [cited 2019 june 03];41(1): 101-106. Available from: https://www.scielo.br/scielo.php?script=sci_arttext&pid=S0100-204X2006000100014&lng=en&nrm=iso&tlng=pt. Portuguese.
https://www.scielo.br/scielo.php?script=... ^,3434 Temim S, Chagneau AM, Guillaumin S, Michel J, Peresson R, Geraert PA, Tesseraud S. Effects of chronic heat exposure and protein intake on growth performance, nitrogen retention and muscle development in broiler chickens. Reproduction, Nutrition, Development [Internet]. 1999 [cited 2019 Oct 10]; 39(1): 145-156. Available from: https://hal.archives-ouvertes.fr/hal-00900289/document. English.
https://hal.archives-ouvertes.fr/hal-009... ^,3535 Zuprizal ML, Chagneau AM, Geraert PA. Influence of ambient temperature on true digestibility of protein and amino acid of rapeseed and soybean meals in broilers. Poultry Science [Internet]. 1993 February [cited 2019 Dec 10]; 72(2): 289-295. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119338337#!. English.
https://www.sciencedirect.com/science/ar...

A similar result was observed for EEB and TEEB, with a worse balance for animals under heat stress. However, broilers raised under thermoneutral temperature at the growing phase had no differences compared to animals raised under hot temperature. Broilers exposed to heat have higher water intake, which can cause less digestibility of nutrients by increasing the feed passage rate.³⁶36 Bonnet S, Geraert PA, Lessire M, Carre B, Guillaumin S. Effect of high ambient temperature on feed digestibility in broiler. Poultry Science [Internet]. 1997 June [cited 2019 july 10];76(6): 857-863. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119411760?via%3Dihub. English
https://www.sciencedirect.com/science/ar... Heat is also responsible for reducing the size of organs³⁷37 Savory CJ. Influence of ambient temperature on feeding activity parameters and digestive function in domestic fowls. Physiology Behavior [Internet]. 1986 [cited 2019 Dec 10]; 38(3): 353-357. Available from: https://www.sciencedirect.com/science/article/pii/003193848690106X. English.
https://www.sciencedirect.com/science/ar... and the surface of intestinal villi.³⁸38 Mitchell MA, Carlisle AJ. The effects of chronic exposure to elevated environmental temperature on intestinal morphology and nutrient absorption in the domestic fowl (Gallus domesticus). Comparative Biochemestry and Physiology Part A: Physiology [Internet]. 1992 Jany [cited 2019 Dec 10]; 101(1): 137-142. Available from: https://www.sciencedirect.com/science/article/pii/0300962992906413?via%3Dihub. English.
https://www.sciencedirect.com/science/ar...

The effect of broiler age within the climatic chambers was better for NB (P<0.001) and the TNB (P<0.001) at all temperatures and the growing phase (25 to 28 days of age). Proteins are essential in the nutritional and metabolic aspects for broilers, as they are related to body processes such as the formation of structural tissues (muscle). Protein deposition in skeletal muscles in growing animals contributes about 65% of all protein deposited daily.³⁹39 Macari M, Furlan RL, Gonzales E. Fisiologia Aviária: Aplicada a frangos de corte. 2st ed., Jaboticabal: FUNEP; 2002. 375p. Portuguese.

Older broilers had the highest EEB and TEEB (cold and thermoneutral temperature), not differing from the growing phase for heat-stressed broilers. The presence of substrate in the digestive tract in young broilers seems to induce a higher production of enzymes. Thus, the activity of digestive enzymes, both pancreatic and membrane, increases with the broiler age, reaching higher levels at 10 days of age, on average.⁴⁰40 Noy Y, Sklan D. Posthatch development of poultry. Journal of Applied Poultry Research [Internet]. 1997 Oct [cited 2019 Dec 10]; 6(3): 344-354. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119356536. English.
https://www.sciencedirect.com/science/ar... Rapid changes in the digestive tract enable an increase in feed intake and alter nutrient digestibility.⁴4 Syafwan S, Wermink GJD, Kwakkel RP, Verstegen MWA. Dietary self-selection by broilers at normal and high temperature changes feed intake behavior, nutrient intake, and performance. Poultry Science [Internet]. 2012 March [cited 2019 Dec 10]; 91(3): 537-549. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119402162. English.
https://www.sciencedirect.com/science/ar... The higher ether extract balance obtained in broilers at the final phase was probably due to the higher production of enzymes for digesting lipids compared to the young animals.

A significant interaction between temperature and age was observed for the variables CMDM (P=0.0130), CMDMT (P=0.0150), CMN (P<0.001), CMNT (P<0.001), and CMEE (P<0.001), except for CMEET, which presented an exclusive effect of the raising phase (P=0.0404) (Table 5).

The best metabolization of dry matter in the feed at the initial phase was observed for broilers under thermoneutral temperature, but broilers under cold stress showed better results with the increase of age, not differing from the thermoneutral temperature at the final phase. The temperature did not affect the results of broilers at the initial phase when CMDM was corrected for endogenous losses (CMDMT), with the best coefficients for birds raised in the thermoneutral chamber at the final phase, not differing from the cold chamber at the growing phase.

The use of nitrogen (CMN) showed an interference of temperature only for older broilers, in which heat stress reduced nitrogen use. A temperature effect was observed for all age phases when endogenous losses (CMNT) were removed. Broilers at the initial phase showed better coefficients when raised under cold stress, not differing from the thermoneutral temperature at the growing phase. Heat or cold stress in older broilers reduced nitrogen uptake.

The ability of broilers to deal with oxidative stress gradually decreases as the environmental temperature increases.⁴¹41 Wang Y, Xia L, Guo T, Cheng C, Jiang L, Wang D, Wang J, Li K, Zhan X. Metabolic changes and physiological responses of broilers in the final stage of growth exposed to different environmental temperatures. Poultry Science [Internet]. 2020 April [cited 2020 April 29]; 99(4): 2017-2025. Available from: https://pdfs.semanticscholar.org/206b/453009848a1c221a8a193c72723655c1f99f.pdf. English.
https://pdfs.semanticscholar.org/206b/45... These negative effects also interfere with the intake of feed and nutrients⁴4 Syafwan S, Wermink GJD, Kwakkel RP, Verstegen MWA. Dietary self-selection by broilers at normal and high temperature changes feed intake behavior, nutrient intake, and performance. Poultry Science [Internet]. 2012 March [cited 2019 Dec 10]; 91(3): 537-549. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119402162. English.
https://www.sciencedirect.com/science/ar... and, consequently, nutrient use is reduced.

CMEE was not influenced by the temperature at the growing phase (P=0.5316). Cold stress for young broilers caused a reduction in the coefficient, with the best results for older broilers (final phase) raised at thermoneutral temperature. When CMEE was corrected by endogenous losses (CMEET), only the age effect influenced this variable, confirming better use of the ether extract by older broilers.

Garcia et al.⁴²42 Garcia RG, Mendes AA, Klink UP, Almeida Paz ICL, Takahashi SE, Pelícia K, Komiyama M, Quinteiro RR. Digestibilidade de rações contendo sorgo com e sem tanino em frangos de corte colostomizados submentidos a três temperaturas ambiente. [Digestibility of feeds containing sorghum, with and without tannin, forcolostomyzed broiler chickens submitted to three room temperature] ARS Veterinária [Internet].2005[cited 2019 june 17]; 21(2): 257-264. Available from: https://www.researchgate.net/publication/277120596_DIGESTIBILIDADE_DE_RACOES_CONTENDO_SORGO_COM_E_SEM_TANINO_EM_FRANGOS_DE_CORTE_COLOSTOMIZADOS_SUBMETIDOS_A_TRES_TEMPERATURAS_AMBIENTE. Portuguese.
https://www.researchgate.net/publication... worked with the digestibility of diets containing sorghum with low or high tannin for colostomized (removal of the colon via surgery and collection of feces and uric acid separately) broilers raised at three environmental temperatures (14, 25, and 32 ºC) and found that the coefficients of digestibility of dry matter and ether extract were higher in the hot chamber and lower in the cold. These higher values were associated with the lower intake observed at high temperatures, which led to a lower speed of transit of food in the digestive tract of broilers and, consequently, higher absorption of nutrients.⁴4 Syafwan S, Wermink GJD, Kwakkel RP, Verstegen MWA. Dietary self-selection by broilers at normal and high temperature changes feed intake behavior, nutrient intake, and performance. Poultry Science [Internet]. 2012 March [cited 2019 Dec 10]; 91(3): 537-549. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119402162. English.
https://www.sciencedirect.com/science/ar... This result occurred in the current study only for CMEE at the initial phase.

There was an effect of the broiler age for the studied temperatures. The best results for CMDM were observed in broilers at the final phase raised under thermoneutral and cold temperatures. Broilers in the hot chamber used the dry matter similarly, regardless of age. After correction (CMDMT), the results in the thermoneutral chamber were maintained, not differing between broilers at the growing and final phase in the cold chamber. Age also interfered with CMDMT for broilers in the hot chamber, with better results at the final stage.

Nitrogen metabolization (CMN) was better for broilers at the final phase in the thermoneutral chamber and growing and final phases in the cold chamber. The best coefficients under heat stress were observed in broilers at the growth phase (25 to 28 days of age). The correction for endogenous losses (CMNT) did not change the results inside the chambers, and broilers in the cold, thermoneutral, and hot chambers had the lowest coefficients at the initial phase, but the growing phase in the cold chamber had the best result.

The ether extract was better used by older broilers, regardless of the environmental temperature. Broiler age not only interfered with the metabolizable energy but also with the metabolizability of nutrients in the diet. Furthermore, heat stress reduced the metabolizability of nutrients in the test diet.

Bonnet et al.³⁶36 Bonnet S, Geraert PA, Lessire M, Carre B, Guillaumin S. Effect of high ambient temperature on feed digestibility in broiler. Poultry Science [Internet]. 1997 June [cited 2019 july 10];76(6): 857-863. Available from: https://www.sciencedirect.com/science/article/pii/S0032579119411760?via%3Dihub. English
https://www.sciencedirect.com/science/ar... conducted a performance experiment and metabolic test using broilers from 38 to 42 days of age raised under hot (32 ºC) and thermoneutral temperature (22 ºC), fed ad libitum, and pair-feeding (controlled feeding). The authors observed that, even with the same intake, broilers submitted to heat stress did not obtain the same growth rate as the animals under a thermoneutral environment. Also, a reduction in feed efficiency was observed during heat stress as a direct consequence of exposure to high temperature.

Conclusions

In general, the metabolizable energy values of corn, the balances, and coefficients of metabolizability of nutrients in the test diet increased with the broiler age, but the true metabolizable energy of corn was not affected by the environmental temperature. The balances and coefficients of metabolizability of nutrients in the test diet were reduced under heat stress for broilers at the growing and final phases.

Acknowledgments

To the São Paulo Research Foundation - FAPESP for financial support for conducting this research.

References

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