SciELO - Scientific Electronic Library Online

vol.9 número1Effect of the supplementation of vitamins and organic minerals on the performance of broilers under heat stressInfluence of sulfur amino acid levels in diets of broiler chickens submitted to immune stress índice de autoresíndice de assuntospesquisa de artigos
Home Pagelista alfabética de periódicos  

Serviços Personalizados




Links relacionados


Brazilian Journal of Poultry Science

versão impressa ISSN 1516-635Xversão On-line ISSN 1806-9061

Rev. Bras. Cienc. Avic. v.9 n.1 Campinas jan./mar. 2007 

Effects of the reduction of dietary heat increment on the performance, carcass yield, and diet digestibility of broilers submitted to heat stress1



Laganá CI; Ribeiro AMLII; Kessler AMII; Kratz LRIII; Pinheiro CCIII

IResearcher APTA Regional/PRDTA Leste Paulista
IIAssistant Professor, Dep. Zootecnia - UFRGS/ Porto Alegre, RS
IIILaboratório de Ensino Zootecnico - UFRGS/ Porto Alegre, RS

Mail Address




This experiment aimed at verifying the effect of different diets and thermal environments on the performance, carcass yield, and diet digestibility of 21 to 42-day-old broilers. A total number of 288 21-day-old male Ross broilers were distributed in a 2 x 2 + 2 factorial arrangement, with six replicates, including the following factors: two environments (TNE – thermoneutral: 21-25ºC and 73% RH; CHS – cyclic heat stress: 25-32ºC and 65%RH), and two diets (control: 2.4% soybean oil and 19.5% protein; summer: 4.0% soybean oil and 18.5% protein). In TNE, two additional treatments were included with feed restriction of birds fed both the control and summer diets (pair-feeding), thereby maintaining the same feed intake level for both types of diet. Diet did not influence performance, dry matter and protein digestibilities, or carcass and part yields. TNE birds had better performance (p<0.001) as compared to CHS birds, but FCR was not different. CHS birds had lower breast yield (p<0.0001), and higher thigh yield (p<0.02) than TNE birds. In the pair-feeding treatments, environment did not influence performance, but dry matter digestibility was significantly lower in CHS (p<0.03), whereas protein digestibility was not affected. The difference in feed intake was the main responsible factor for the variation in the performance of heat-stressed birds.

Keywords: Environment temperature, fat, poultry nutrition, protein, feed restriction.




Increases of protein and energy levels in broiler diets to compensate reduction in intake during hot weather are frequently recommended. The replacement of carbohydrates by fat as energy sources is recommended, as well as the supply of adequate amino acid profile. The use of oil in substitution of carbohydrates is justified by the fact that fats, among all ingredients, oil presents the lowest heat increment (9%), as compared to protein (26%) (Ribeiro & Laganá, 2002).

Dale & Fuller (1980) observed less harmful effects of high temperatures on weight gain when 27.5% of dietary metabolizable energy (ME) was replaced by fat (dietary addition of 8% vs. 2.25%). These authors found that, when birds were submitted to cyclic heat stress (CHS), growth rate improved when fat was added to the diet. However, fat had no effect when birds were submitted to chronic heat stress. One of the differences between continuously high temperatures (chronic heat stress) and cyclic heat stress is that, in CHS, birds are able to dissipate heat during the cooler night period, which is not possible when birds are maintained to constantly high temperatures. Therefore, birds submitted to heat stress ingest feed during the cooler periods, influencing nutritional requirements (Balnave & Oliva, 1990), response to feed supplements (Smith & Teeter, 1987), and compensatory weight gain (Ribeiro et al., 2001a).

As to dietary protein concentration, two strategies are suggested to minimize CHS effects on growth rate:

a) the use of low-protein diets in order to decrease heat increment, with some authors recommending lowering dietary protein content with the supplementation of essential amino acids (Waldroup, 1976; Austic, 1985; Cheng et al., 1997); and

b) the use of high-protein diets to compensate lower feed intake caused by heat, as recommended by Temim et al. (2000).

The latter used diets containing 10 to 33% crude protein (CP), and observed that 28 to 33% CP diets resulted in better weight gain and feed conversion ratio than the 20% CP diet fed to 4-6-week-old broilers maintained under continuous heat (32ºC). However, the authors stress that, in this case, only highly digestible protein sources should be used, as increasing dietary protein content through low digestibility ingredients would cause higher heat increment (HI), and therefore, the heat stress would be worsened.

Research studies showed that birds submitted to heat stress not only cause lower feed intake. Dale & Fuller (1980), using pair-feeding, observed that even when feed intake was the same, birds submitted to heat stress did not present the same growth rate as those kept in thermoneutral environment. These authors assert that feed efficiency is reduced during heat stress, which can be caused by lower feed digestion – first stage of nutrient utilization –, as well as to a higher energy requirement to maintain body temperature. Stress implies in an increase in energy needs, as there is high activity of the neural muscular system and other tissues. At the onset of stress, skeletal muscle tone increases by the action of catecholamines, preparing the individual for possible physical activity, which is equivalent to maintaining an alert state. Therefore, the body requires higher levels of glucose and other nutrients, such as amino acids, salts, and vitamins, which are essential to sustain an increase in activity (Cabral et al., 1997).

When submitting broilers to chronic stress at 32ºC and using pair-feeding, Bonnet et al. (1997) reported that dry matter, protein, fat, and starch digestibilities were lower as compared to birds submitted to a temperature of 22ºC.

The present study aimed at:

a) verifying if higher oil and lower protein (lower HI) diets benefited the metabolism, performance, and carcass traits of broilers submitted to cyclic heat stress (25-32ºC); and

b) verifying the direct effect of high environmental temperature on the performance and nutrient utilization, using pair-feeding technique.



The experiment was carried out in temperature-controlled rooms, called Cold Battery and Hot Battery, of the poultry sector of the Animal Science Laboratory (Laboratório de Ensino Zootécnico – LEZO), of the Federal University of Rio Grande do Sul, Brazil. A total number of 288 21-day-old male Ross broilers was housed in 0.72 m2 cages, equipped with metal trays for the collection of excreta. Birds were distributed in a 2 x 2 + 2 factorial arrangement, with six replicates of eight birds each. Birds were submitted to one of two environments: TNE (thermoneutral environment) or CHS (cyclic heat stress); and were fed one of two diets, control diet and summer diet, described in Table 1. Diets were formulated according to the recommendations of Rostagno et al. (2000). Under the TNE environment, two further treatments were applied: feed restriction, maintaining the same feed intake as birds submitted to CHS, for both diets (control and summer diets). In order to calculate the amount of food supplied, the feed intake of CHS birds, which feed was offered ad libitum, was measured daily, and the measured amount was offered to TNE birds on the next day. Therefore, treatments were: A – CHS, control diet; B – CHS, summer diet; C – TNE, control diet, ad libitum; D – TNE, summer diet, ad libitum; E – TNE, control diet, same intake as A; and F – summer diet, same intake as B.



The summer feed contained 1.6% more oil and 1% less CP than the control diet, but maintaining the same energy, lysine, and methionine+cystine levels. Vitamin and mineral supplementation was the same for both diets.

TNE room temperature was kept at 21-25ºC, and relative humidity at 65% until 28 days, and 81% from 28 to 42 days. In order to simulate cyclic heat stress environment, birds were submitted to daily cycles of 12 hours of thermoneutral temperature (25ºC), 3 hours of increasing temperature (25 to 32ºC), six hours at 32ºC, and 3 hours of decreasing temperature (32 to 25ºC). Relative humidity was kept at 65% during the entire experimental period.

Weight gain, feed intake, and feed conversion ratio were calculated weekly. Apparent digestibility was measured by total excreta collection, four days weekly, for three weeks. Birds were submitted to six hours before the beginning of the collection period and six hours before the end of collection to promote gastrointestinal emptying (Ribeiro et al., 2001a). Measures were obtained in the cages, and each experimental unit consisted of the group of birds in each cage. Excreta was daily collected during four days, weighed, homogenized, placed in duly identified plastic bags, and an aliquot (10%) was frozen (-10ºC) until analyses. After thawing, excreta were acidified to pH 4.0, dried until constant weight at 60ºC, and dry matter was analyzed (Ribeiro et al., 2001b). The kaolin added to the summer diet was discounted from feed intake and excreta for digestibility calculation, as recommended by Pucci et al. (2003).

Birds were slaughtered at 42 days of age. After weighing, birds were submitted to neck dislocation, bleeding, scalding, defeathering, evisceration, and chilling for 40 minutes, after which the carcass was cut up.

Analyses of variance were performed using the GLM (General Linear Models) procedure of SAS software package, and means were compared using LSMeans.



Table 2 shows the performance responses of birds fed ad libitum. There was no significant interaction between environment and diet for any parameter. Birds under CHS fed ad libitum presented lower feed intake (p<0.001) as compared to those under TNE. Feed intakes lower than those observed in the present experiment (11%) were reported by Austic (1985), Howlider & Rose (1987), Smith (1993), and Czarick & Tison (1990). These authors observed that the first response of the bird to heat stress is a reduction in intake, and as a result of not ingesting the necessary amounts of nutrients, performance and welfare are compromised, and mortality increases. A decrease in feed intake, in an attempt to generate less heat, was also observed by Teeter et al. (1984) and Bonnet et al. (1997). Under chronic heat stress, the bird significantly reduces feed intake, as compared to cyclic heat stress, which can be explained by the absence of a comfort period in case of continuous heat stress. The lower reduction in feed intake in the present experiment, as compared to the above mentioned studies, is linked to the magnitude, duration, and type of stress to which the birds were submitted, and which must be considered, as acclimation is associated to feed intake (Teeter et al., 1992).



Diet type did not influence feed intake, differently from Bonnet et al. (1997), who observed significant increase in feed intake in birds submitted to chronic heat stress of 32ºC and fed a summer diet (105 vs. 113 g/birds/day).

Birds under CHS also presented lower body weight (p<0.003) and weight gain (p<0.001) as compared to those under TNE due to the reduction in feed intake. At the end of the experiment, average weight of birds under CHS was 6% lower than those under TNE, which was also observed by Ribeiro et al. (2001a), who submitted birds to cyclic heat stress for a longer period (21 to 56 days of age). Oliveira Neto et al. (2000), Lana et al. (2000), and Howlider & Rose (1987) also found lower growth rates and final weight in CHS birds. Bonnet et al. (1997) reported a 50% reduction in weight gain of birds submitted to chronic stress at 32ºC as compared to birds kept in thermoneutral environment of 22ºC, after three weeks.

As to feed conversion ratio (FCR), no significant differences were observed due to environment or diet type. Bonnet et al. (1997) compared diets containing 11.6 or 8.1% fat for birds under CHS, and also did not observe differences in FCR. However, Dale & Fuller (1980) found better FCR with the dietary addition of 8% fat as compared to 2.25% in birds submitted to CHS. The lack of environmental effect found in the present study is consistent with Lana et al. (2000), who also did not find FCR differences in birds submitted to 31ºC as compared to those kept at 25ºC. This was attributed to the proportional drop in feed intake and weight gain.

Table 3 shows the comparison of performance under TNE and CHS when birds were fed the same intake levels, from 21 to 42 days of age. There was no significant effect of treatments on performance parameters. These results are different from those obtained by Dale & Fuller (1980), Geraert et al. (1996), and Bonnet et al. (1997), who equalized feed intake, and reported different growth rates between birds kept in TNE and under CHS.



After observing that birds submitted to did not present the same growth rate as those in thermoneutral environment, Dale & Fuller (1980) suggested that processes, such as panting and opening wings, to attempt to dissipate heat require extra energy expenditure, causing a reduction in feed utilization. Acclimation, on the other hand, may explain the positive results observed in the third week of heat in the present experiment. Wildeman et al. (1994) concluded that acclimated broilers may have higher feed intake. The increase in water consumption promoted by high temperatures may, up to a certain extent of heat stress, allow the bird to maintain constant feed intake (May et al., 1997).

Diet had no effect on performance

Table 4 shows that the environment influenced breast yield (p<0.01) and thigh yield (p<0.02) in birds fed ad libitum. TNE birds had higher breast yield, which is consistent with the findings of Smith (1993), whereas CHS birds presented higher thigh yield. Baziz et al. (1996) observed a reduction in breast yield, and increase in leg muscle (leg + thighs) yield in 4-7-week-old broilers kept under chronic heat stress (32ºC).



Diet had no influence on carcass yield

Table 5 shows carcass yield results of birds submitted to feed restriction. TNE birds presented higher breast yield (p<0.002) and thigh yield (p<0.01) as compared to CHS birds. These differences were observed in birds of similar weights, as two of the treatments applied feed restriction. The higher respiratory rate, as a function of panting, increases breast muscle activity, as well as the absence of diaphragm, may have promoted the lower breast yield of CHS birds. According to Meltzer (1987), tissue temperature increase accelerates chemical reactions, thereby increasing oxygen demand and heat production.



Dry matter digestibility (DMD) was lower (p<0.03) in CHS birds. This observation is consistent with Bonnet et al. (1997), as to a decrease in dry matter digestibility after a period of heat exposure. According to these authors, these results partially explain the lower performance of heat-stressed birds and partially by a reduction in feed efficiency in some cases (Benyi & Habi, 1998). Teeter et al. (1985) asserted that feed restriction may improve digestibility, as birds submitted to 25% feed restriction from 28 to 39 days of age, presented 5% higher diet digestibility.

Based on Sibbald (1979) and May et al. (1988), it is possible that the period of time feed-restricted birds remained with no feed may have contributed to improve diet digestibility, when restricted-fed CHS birds are compared with those fed ad libitum.

As to environment effect, literature information is controversial. May et al. (1988) observed birds under CHS presented reduced passage rate, and therefore, were able to improve diet digestibility. This response is associated to corticosterone, which would retain feed in the digestive tract longer, thereby favoring nutrient digestion and absorption. Washburn, (1991), Gordon & Roland, (1997) and Bonnet et al. (1997) observed that the increase in water consumption caused by high environmental temperatures, can increase feed passage rate, and therefore, it may decrease nutrient absorption.

As to diets, after correction for kaolin inclusion, no significant differences were found among treatments (p<0.56). Pucci et al. (2003) also did not find significant effect of higher oil inclusion in the feed on dry matter digestibility, when feed intake and excreta were corrected after kaolin withdrawal. On the other hand, Bonnet et al. (1997) e Vieira et al (2002) observed a reduction in dry matter digestibility in birds fed diets containing higher fat levels.



Environment and diet had no influence on protein digestibility, in agreement with the study with layers under CHS of Koelkebeck et al. (1998). These results were different from those of Bonnet et al. (1997) and Wallis & Balnave (1984), who, in studies with broilers in heat environments, showed a consistent decrease in protein and amino acid digestibilities in complete diets. Sibbald (1982) observed that the results of many studies associating digestibility with heat stress are not conclusive.



The summer diet, which contained more oil and less protein, did not influence performance, diet digestibility, or carcass and part yields of birds submitted to cyclic heat stress as compared to those kept under thermoneutral environment. Heat conditions worsened bird performance, and decreased breast yield; however, thigh yield improved. In the pair-feeding treatments, environment did not affect performance, and showed that the reduction in feed intake was the main responsible factor for the performance reduction in heat-stressed broilers. In addition, in the pair-feeding treatments, dietary dry matter digestibility was significantly lower in birds submitted to cyclic heat stress, whereas crude protein digestibility was not affected.



Austic RE. Feeding poultry in hot and cold climates. In: STRESS Physiology in Livestock. Boca Raton, FL: CRC; 1985. p.123-136.         [ Links ]

Balnave D, Oliva A. Responses of finishing broilers at high temperatures to dietary methionine source and supplementation levels. Australian Journal or Agricultural Research 1990; 41(3):557-564.         [ Links ]

Baziz HA, Geraert PA, Padilha JCF, Guillaumin S. Chronic heat exposure enhances fat deposition and modifies muscle and fat partition in broiler carcasses. Poultry Science 1996; 75(4):505-513.         [ Links ]

Benyi K, Habi H. Effects of food restriction during the finishing period on the performance of broiler chickens. British Poultry Science 1998; 39(3):423-425.         [ Links ]

Bizeray D, Leterrier C, Constantin P, Picard M, Faure JM. Early locomotor behavior in genetic stocks of chickens with different growth rates. Applied Animal Behaviour Science 2000; 68(3):231-241.         [ Links ]

Bonnet S, Geraert PA, Lessire M, Carre B, Guillaumin S. Effect of high ambient temperature on feed digestibility in broilers. Poultry Science 1997; 76(6):857-863.         [ Links ]

Cabral APT, Luna JF, Souza KN, Macedo LM, Mendes MGA, Medeiros PASM, Gomes RM, Souza FP. O estresse e as doenças psicossomáticas. Revista Piscofisiologia [periódico on-line] 1997 dez [capturado 2004 dez 18]; 1(1). Disponível em:        [ Links ]

Cheng TK, Hamre ML, Coon CN. Effect of environmental temperature, dietary protein and energy levels on broiler performance. Journal Applied Poultry Research 1997; 6(1):1-17.         [ Links ]

Czarick M, Tison BL. Reflective roof coatings on commercial laying houses. Transactions of ASAE 1990; 90:4512.         [ Links ]

Dale NM, Fuller HL. Effect of diet composition on feed intake and growth of chicks under heat stress. II. constant x cycling temperatures. Poultry Science 1980; 59(9):1431-1441.         [ Links ]

Ferreira RA, Oliveira RFM, Donzele JL, Soares RTRM, Abreu MLT, Moura AMA, Cella PS. Efeito da temperatura ambiente e da umidade relativa sobre o rendimento de carcaça e de cortes nobres de frangos de corte. In: Reunião Anual da Sociedade Brasileira de Zootecnia, 41; 2004; Campo Grande. Anais... p.1-4.         [ Links ]

Geraert PA, Padilha JCF, Guillaumin S. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: Growth performance, body composition and energy retention. British Journal of Nutrition 1996; 75(2):195-204.         [ Links ]

Gordon RW, Roland DA. The influence of environmental temperature on in vivo limestone solubilization, feed passage rate, and gastrointestinal pH in laying hens. Poultry Science 1997; 76(4):683688.         [ Links ]

Howlider MAR, Rose SP. Temperature and the growth of broilers. World¢s Poultry Science 1987; 43(2):228-237.         [ Links ]

Koelkebeck KW, Parsons CM, Wang X. Effect of acute heat stress on amino acid digestibility in laying hens. Poultry Science 1998; 77(9):13931396.         [ Links ]

Lana GEG, Rostagno HS, Albino LFT, Lana AMQ. Efeito da temperatura ambiente e da restrição alimentar sobre o desempenho e a composição da carcaça de frangos de corte. Revista Brasileira de Zootecnia 2000; 29(4):1117-1123.         [ Links ]

May JD, Branton SL, Deaton JW, Simmons JD. Effect of environmental temperature and feeding regimen on quality of digestive tract contents of broilers. Poultry Science 1988; 67(1):64-71.         [ Links ]

May JD, Lott BD, Simmons JD. Water consumption by broilers in high cyclic temperatures: bell versus nipple waterers. Poultry Science 1997; 76(7):944-947.         [ Links ]

Meltzer A. Acclimatization to ambient temperature and its nutritional consequences. World's Poultry Science 1987; 43(1):33-45.         [ Links ]

Oliveira Neto AR, Oliveira RFM, Donzele JL. Metabolizable energy level for broilers from 22 to 42 days of age maintained under thermoneutral environment. Revista Brasileira de Zootecnia 2000; 29(4):1132-1140.         [ Links ]

Pucci LEA, Rodrigues PB, Freitas RTF, Bertechini AG, Carvalho EM. Níveis de óleo e adição de complexo enzimático na ração de frangos de corte. Revista Brasileira de Zootecnia 2003; 32(4):909-917.         [ Links ]

Ribeiro AML, Penz AM, Teeter R. Effects of 2-hydroxy-4-(methylthio) butanoic acid and DL-Methionine on broiler performance and compensatory growth after exposure to two different environmental temperatures. Journal of Applied Poultry Research 2001a; 10(4):419-426.         [ Links ]

Ribeiro AML, Penz AM, Belay TK, Teeter R. Comparison of different drying techniques for nitrogen analysis of poultry excreta, feces, and tissue. Journal of Applied Poultry Research 2001b; 10(4):21-23.         [ Links ]

Ribeiro AML, Laganá C. Estratégias nutricionais para otimizar a produção de frangos de corte em altas temperaturas. In: Encontro Internacional dos Negócios da Pecuária; 2002; Cuiabá. Resumos... Cuiabá: ENIPEC; 2002. 1 CD-ROM.         [ Links ]

Rostagno HS, Albino LFT, Donzele JL, Gomes PC, Ferreira AS, Oliveira RF, Lopes DC. Tabelas Brasileiras para aves e suínos. Composição de alimentos e exigências nutricionais. Viçosa: UFV; 2000. 141p.         [ Links ]

Ruckebush LP, Phaneuf LP, Dunlop RF. Fisiologia de pequeñas y grandes espécies, México: Manual Moderno; 1994. 862p.         [ Links ]

Rutz F. Aspectos fisiológicos que regulam o conforto térmico das aves. In: Conferência Apinco de Ciencia e Tecnologia Avícolas; 1994; Santos. Anais... Campinas: FACTA; 1994:99-110.         [ Links ]

Rutz F. Impacto da nutrição vitamínica sobre a resposta imunológica das aves. In: Simpósio Brasil Sul de Avicultura, 3; 2002; Chapecó. Resumos... p.1-15.         [ Links ]

Sas Institute. User's guide (8.2). Statistical Analysis System Institute, Cary: NC; 2001.         [ Links ]

Sibbald JD. Passage of feed through the adult rooster. Poultry Science 1979; 58(2):446-459.         [ Links ]

Sibbald JD. Measurement of bioavaliable energy in poultry feedingstuffs: a review. Canadian Journal Animal Science 1982; 62(4):983-1048.         [ Links ]

Smith MO. Parts yield of broilers reared under cycling high temperatures. Poultry Science 1993; 72(10):1146-1150.         [ Links ]

Smith MO, Teeter RG. Potassium balance of the 5 to 8-week-old broiler exposed to constant heat of cycling high temperature stress and the effects of supplemental potassiumchloride on body weight gain and feed efficiency. Poultry Science 1987; 66(3):487–492.         [ Links ]

Teeter RG, Smith MO, Murray E. Force feeding methodology and equipment for poultry. Poultry Science 1984; 63(4):573-575.         [ Links ]

Teeter RG, Smith RO, Arp SC, Sangiah S, Breazile JE. Chronic heat stress and respiratory alkalosis: occurrence and treatment in broiler chicks. Poultry Science 1985; 64(9):1060-1064.         [ Links ]

Teeter RG, Smith MO, Wiernusz CJ. Broiler acclimation to heat distress and feed intake effects on body temperature in birds exposed to thermoneutral and high ambient temperatures. Poultry Science 1992; 71(9):1101-1104.         [ Links ]

Temim S, Chagneau AM, Guillaumin S, Michael J, Peresson R, Tesseraud S. Does excess dietary protein improve growth performance and carcass characteristics in heat-exposed chickens? Poultry Science 2000; 79(2):312-317.         [ Links ]

Vieira SL, Ribeiro AML, Kessler AM, Fernandes LM, Ebert AR, Eichner G. Utilização da energia de dietas para frangos de corte formuladas com óleo ácido de soja. Revista Brasileira de Ciência Avícola 2002; 4(2):127-139.         [ Links ]

Waldroup PW, Mitchell RJ, Peyne JR, Hazen KR. Performance of chicks fed diets formulated to minimize excess levels of essential amino acids. Poultry Science 1976; 55(1):243-253.         [ Links ]

Wallis IR, Balnave D, The influence of environmental temperature, age and sex on the digestibility of amino acids in growing broiler chickens. Poultry Science 1984; 25(3):401-407.         [ Links ]

Washburn KW. Efficiency of feed utilization and rate of feed passage through the digestive system. Poultry Science 1991; 70(3):447-452.         [ Links ]

Weeks CA, Danbury TD, Davies HC, Hunt P, Kestin SC. The behaviour of chickens and its modification by lameness. Applied Animal Behaviour Science 2000; 67(1):111-125.         [ Links ]

Wildeman RF, Ford BC, May JD, Lott BD. Acute heat acclimation and kidney function in broilers. Poultry Science 1994; 73(1):75-88.        [ Links ]



Mail Address
C Laganá
APTA/PRDTA Leste Paulista
Caixa Postal 01
13.910-000. Monte Alegre do Sul, SP, Brasil

Arrived: September / 2006
Approved: March / 2007



1 Part of the thesis presented by the first author to Universidade Federal do Rio Grande do Sul as one of the requisites to obtain the title of Ph.D. in Animal Science.

Creative Commons License Todo o conteúdo deste periódico, exceto onde está identificado, está licenciado sob uma Licença Creative Commons