DOI: https://doi.org/10.21203/rs.3.rs-667004/v1
The aim of this study is to determine the effects of feeding type (ad-libitum: AF and intermittent: IF) and water temperature (normal: NW and cold: CW) treatments on welfare status and meat quality in fast-growing broiler chickens reared under daily heat stress between 22-42 days of age. Panting rate and rectal temperature of the chickens were determined at 4, 5 and 6 weeks of age and twice a week in 3 female and 3 male chickens in each pen. Welfare traits such as foot pad dermatitis (FPD), hock burn (HB), breast burn (BB) and leg problems (LP) were examined individually at 42 days of age. At day 43, 3 male and 3 female chickens per pen were randomly selected and slaughtered after an 8-h fasting period, pH and color [lightness (L*), redness (a*) and yellowness (b*)] of breast and thigh meat were determined. AF×CW chickens had significantly higher panting rates at all ages compared to the other groups (P < 0.05). While FPD and LP were not affected by feeding type and water temperature treatments, interaction effects on HB and BB were found significant (P < 0.05). The HB and BB levels were the lowest in AF×NW chickens (P < 0.05). While treatments did not change to any color traits in breast meat (P > 0.05), interactions significantly affected the yellowness (b*) value in thigh (P < 0.05).
In conclusion, management practices such as IF and CW in fast-growing broilers could not completely reduce the detrimental effects of heat stress on some welfare and meat quality traits, and in some cases even caused more negativity.
Birds are under great challenge at high environmental temperatures due to the absence of sweat glands and the well-insulated feather coverage (Lara and Rostagno, 2013; Noubandiguim et al., 2021). High ambient temperatures in broiler production can cause detrimental effects on physiological, immunity, welfare, health, performance, meat quality, and serious economic losses (Hristov et al., 2018; Erensoy et al., 2020a). Numerous studies have been conducted on the sustainability of better growth and feed efficiency traits by reducing body heat production and providing better heat dissipation in hot environmental conditions (Cahaner et al., 1993; Sahraei, 2012; Park et al., 2013; Erensoy et al., 2020a). Modern broilers have become more sensitive to heat stress due to fast-growth selection (Erensoy et al., 2020a,b). Increased body weight has contributed to the development of some welfare problems such as foot pad dermatitis (FPD), hock burn (HB), and breast burn (BB), and leg problems (LP) (Dawkins et al., 2004; Haslam et al., 2007). It is also stated that heat stress can increase the incidence and severity of these problems (Mello et al., 2015). There were also many studies reporting that acute or chronic heat stress negatively affects the meat quality of broilers (Sandercock et al., 2001; Zaboli et al., 2019) and accelerates the development of PSE syndrome (pale, soft and exudative) in breast meat (Zhang et al., 2012; Shakeri et al., 2020). Among the various factors affecting meat quality, pH and color are the most widely accepted chemical indicators (El Rammouz et al., 2004; Le-Bihan-Duval et al., 1999; 2008; Berri et al., 2001). It has been reported that acute heat stress can reduce pH, redness, yellowness, and increase breast lightness in broiler chickens (Petracci et al., 2004; Akşit et al., 2006; Zaboli et al., 2019).
The accompanying heat stress to excessive live weight makes it challenging to manage in modern broilers, which are already vulnerable in many aspects such as physiological, welfare and health. In our previous study (Erensoy et al., 2020a) had already demonstrated the effects of feeding type and water temperature on performance and carcass traits. We hypothesized that these management tools could also improve some welfare and meat quality traits under heat stress conditions. This study aims to determine the effects of feeding type (AF and IF) and water temperature (NM and CW) treatments on welfare status and meat quality in broiler chickens reared under daily heat stress during 22–42 days of age.
Chicken and housing material
This study was carried out in the experimental farm of Ondokuz Mayıs University, Faculty of Agriculture, between June and August 2019. The chicken and feed material in this study were the same as in Erensoy et al. (2020a).
This study was started with a total of 320 Anadolu-T broiler chickens at 21 days of age. In the study, heat stress treatment and data collection procedures were carried out between 22 and 42 days of age. The experiment was carried out in a fully environmentally controlled house with automatic heating, ventilation, and lighting equipment. In order to eliminate the effects that may arise from the lighting on the treatments, 24-h continuous lighting was applied. All chickens were fed ad-libitum until 21 days of age. They were fed with standard broiler starter ration (3000 kcal/kg ME, 23% CP) during the first week, followed by chick feed (3100 kcal/kg ME, 22% CP) until 28 days of age, chicken feed (3100 kcal/kg ME, 21% CP) between 29 and 35 days, and finisher feed (3100 kcal/kg ME, 18% CP) until 42 days of age. Water was also given ad-libitum throughout the entire experimental period. The pen dimensions were 1.0×1.5 m and each with a 15 kg capacity round feeder and two nipple drinkers.
Experimental design
The experimental design of this study was in the same procedure as in Erensoy et al. (2020a) and designed as a 2x2 factorial design including two feeding systems (AL: ad-libitum feeding; IF: intermittent feeding) and two water temperature (NW: normal water; CW: cold water) treatments. A total of 320 broiler chickens were randomly distributed in each group (AF×NW, AF×CW, IF×NW, and IF×CW) at 21 days of age, with four replicates and 20 chickens. Stocking density was 13.3 chickens/m2. Broilers in the AL group were fed ad-libitum for 24-h and IF chickens were daily fasted for 6-h between 11-17 h during the experiment (between 22-42 days). NW chickens consumed tap water (avg. 24.9 °C), and CW chickens more chilled water (avg. 16.4 °C) freely for 24 h. The light intensity in all pens was approximately 20 and 25 lux. Heat stress was applied between 11-17 h every day between 22-42 days of age. Temperature and relative humidity values were 30 °C and 61.4%, 25.3 °C and 70.2%, respectively, during the hours with (11-17 h) and without (18-10 h) heat treatment.
Data collection
Heat stress indicators
At the end of the 3 weeks of age, all chickens were tagged with wing-band, individual live weights were taken, and ten males and ten females were randomly distributed to each pen. The birds' panting rate and rectal temperature were determined at 4, 5, and 6 weeks of age and twice a week in three female and three male broilers in each pen in the middle of the heat stress duration (at 14h). In order not to affect body temperature, firstly, the panting rate was determined in each observation. While the chicken was in the lying position, the number of panting movements for 1 min were counted by the same person and it was recorded as panting rate (panting count/1 min). Rectal temperature was measured in the same animals with a rectal thermometer with a sensitivity of 0.1 oC for 2 min and 2 cm inside the cloaca gently (Farghly et al., 2019; Erensoy et al., 2020a).
Welfare traits
A scale with 1 g precision (Jadever, JWQ-6 Digital Precision Scale, Northspring BizHub Industrial Building, Singapore) was used to determine individual live weights at 42 days of age. Welfare traits included foot pad dermatitis (FPD), hock burn (HB), breast burn (BB), and leg problems (LP) of all birds (10 male and 10 female from each group), and were determined using a visual scoring system between 0–3 scale (Welfare Quality, 2009; Yamak et al., 2014; de Jong et al., 2020). In the determination of LP, chickens were classified clinically by holding their wings and the leg bone tarsal joint according to Letterier and Nys (1992).
Meat quality traits
On day 43, three male and three female chickens in each pen were randomly selected and slaughtered after an 8-h fasting period. Semi-automated equipment was used for scalding (1 min at 56 °C), plucking, chilling (5 min at 1-5 °C), vent-opening, evisceration, and air-chilling (24 h at 4 °C). Following air-chilling, carcasses were cut into parts according to standard methods (Sarica et al., 2014). Meat pH was measured at 3 points on the left thigh and left breast (Model PC 510, Cyber Scan, Singapore), and meat color (L*: Lightness, a*: redness, b*: yellowness) was evaluated at 3 points on the left thigh and left breast (Fanatico et al., 2005) using a colorimeter (Konica Minolta Cr-400).
Litter quality
Litter moisture content was determined at 43 days of the experiment. Litter samples were collected from three different points in each pen and they were mixed. A 100 g of this mixture was dried at 60 oC for 48 h, and moisture content was measured according to Sarıca and Erensoy (2020).
Statistical analysis
This study was designed with a completely randomized design and a 2×2 factorial arrangement (feeding type × water temperature). The normality of the data was analyzed with the Shapiro-Wilk test. Panting rate, rectal temperature, and meat quality traits had normal distribution and they subjected to statistical analysis using the general linear model of the SPSS (Version 25.0) program. The means were also tested at the level of α = 0.05 by Duncan multiple comparison test. However, FPD, HB, BB, and LP traits had not normal distribution, so they were analyzed according to the Kruskal-Wallis and Mann-Whitney U procedure. Interactions were explained with figures when statistically significant (P < 0.05). The standard error of the mean (SEM) for the traits with the normally distributed data type and the median, minimum and maximum values were given in addition to the SEM for the non-normally distributed traits (Önder, 2018).
The effect of feeding type and water temperature on weekly rectal temperature change is given in Table 1. The treatment did not significantly affect the rectal temperatures at 4 and 6 weeks of age. However, at five weeks of age, rectal temperatures were significantly higher in IF chickens than AF and in NW chickens compared to CW (P < 0.05).
The panting rate of chickens under heat stress was significant at 4, 5, and 6 weeks of age, and interaction effects were also found significant (P < 0.05, Table 2). AF×CW broilers had significantly higher panting rates at all ages compared to the other groups (P < 0.05), and the other groups were found similar to each other (Fig. 1). AF×CW chickens showed panting behavior 71.5, 81.9, and 124.7 times per minute at 4, 5, and 6 weeks of age, respectively.
Treatments |
Week 4 |
Week 5 |
Week 6 |
---|---|---|---|
Feeding type |
|||
AF |
40.9 |
40.9b |
41.4 |
IF |
40.9 |
41.1a |
41.1 |
Water temp. |
|||
NW |
40.9 |
41.1a |
41.2 |
CW |
40.9 |
40.9b |
41.2 |
SEM |
0.06 |
0.05 |
0.07 |
p-values |
|||
Feeding type |
0.843 |
0.004 |
0.118 |
Water temp. |
0.560 |
0.050 |
0.916 |
Interaction |
0.079 |
0.375 |
0.787 |
AF: Ad-libitum feeding; IF: Intermittent feeding; NW: Normal water; CW: Cold water | |||
SEM: Standard error of means; Differences among the means were tested using Duncan’s multiple-comparison tests. Means in a column without a common lowercase letter significantly differ (P ≤ 0.05). |
Treatments1 |
Week 4 |
Week 5 |
Week 6 |
---|---|---|---|
Feeding type |
|||
AF |
63.7 (57.5: 37–132) |
75.9 (71.5: 34–134) |
114.2 (115: 62–170) |
IF |
55.3 (53: 40–98) |
63.9 (61.5: 34–129) |
104.7 (107: 37–166) |
Water temp. |
|||
NW |
55.0 (50: 37–98) |
66.8 (56: 34–134) |
104.3 (105.5: 37–166) |
CW |
64.0 (59: 41–132) |
74.0 (70.4: 34–130) |
114.6 (116: 44–170) |
SEM |
2.47 |
2.91 |
3.42 |
p-values |
|||
Feeding type |
0.079 |
0.002 |
0.090 |
Water temp. |
0.005 |
0.015 |
0.032 |
Interaction |
0.010 |
0.001 |
0.006 |
1 Values in parentheses: (median: min-max) | |||
AF: Ad-libitum feeding; IF: Intermittent feeding; NW: Normal water; CW: Cold water | |||
SEM: Standard error of means; Differences among the means were tested using Mann-Whitney U comparison test at 0.05 level. |
The effects of feeding type and water temperature on some welfare traits such as FPD, HB, BB, and LP are given in Table 3. The moisture content of CW chickens litter had significantly higher than NW’s and was 23.9 and 18.0%, respectively (P < 0.05). While FPD and LP were not affected by feeding type and water temperature treatments, interaction effects on HB and BB were found significant (P < 0.05). HB and BB levels were the lowest in AF×NW, and the other groups were similar (Fig. 2).
Treatments2 |
Litter moisture (%) |
FPD |
HB |
BB |
LP |
---|---|---|---|---|---|
Feeding type |
|||||
AF |
20.9 |
0.04 (0:0–1) |
0.63 (1:0–2) |
0.41 (0:0–2) |
0.04 (0:0–1) |
IF |
21.0 |
0.00 (0:0–0) |
0.70 (1:0–2) |
0.46 (0:0–1) |
0.05 (0:0–2) |
Water temp. |
|||||
NW |
18.0b |
0.01 (0:0–1) |
0.54 (1:0–2) |
0.33 (0:0–1) |
0.09 (0:0–2) |
CW |
23.9a |
0.03 (0:0–1) |
0.77 (1:0–2) |
0.53 (1:0–2) |
0.01 (0:0–1) |
SEM |
1.51 |
0.001 |
0.058 |
0.059 |
0.027 |
p-values |
|||||
Feeding type |
0.954 |
0.064 |
0.413 |
0.623 |
0.846 |
Water temp. |
0.018 |
0.635 |
0.005 |
0.015 |
0.066 |
Interaction |
0.954 |
0.299 |
0.002 |
0.023 |
0.300 |
1 Values in parentheses: (median: min-max) | |||||
2 AF: Ad-libitum feeding; IF: Intermittent feeding; NW: Normal water; CW: Cold water; FPD: Foot pad dermatitis; HB: Hock burn; BB: Breast burn; LP: Leg problem | |||||
SEM: Standard error of means; Differences among the FPD, HB, BB and LP means were tested using Mann-Whitney U comparison test at 0.05 level; Means in a column without a common lowercase letter significantly differ (P ≤ 0.05). |
The effect of feeding type and water temperature on color and pH traits of breast and thigh meat are given in Table 4. While main effects did not change to L*, a*, b* values in breast meat, and L * and a * values in thigh meat, interactions significantly affected the b * value in the thigh (P < 0.05, Fig. 3). The b* value was the highest (4.41) in the thigh meat of the IF×CW chickens and the lowest (2.34) in AF×NW chickens (P < 0.05). It was determined that breast meat pH did not change significantly according to the treatments. However, IF chickens (6.12) were lower than AF (6.20) and CW chickens (6.11) also showed lower thigh pH than NW (6.21) (P < 0.05).
Treatments1 |
Breast meat |
Thigh meat |
||||||
---|---|---|---|---|---|---|---|---|
L* |
a* |
b* |
pH |
L* |
a* |
b* |
pH |
|
Feeding type |
||||||||
AF |
57.65 |
1.34 |
2.54 |
5.90 |
59.58 |
4.10 |
3.32 |
6.20a |
IF |
58.70 |
1.09 |
2.59 |
5.89 |
60.31 |
3.85 |
3.37 |
6.12b |
Water temp. |
||||||||
NW |
57.93 |
1.37 |
2.67 |
5.92 |
59.59 |
3.92 |
2.96 |
6.21a |
CW |
58.42 |
1.06 |
2.46 |
5.87 |
60.30 |
4.02 |
3.73 |
6.11b |
SEM |
0.713 |
0.195 |
0.454 |
0.028 |
0.445 |
0.237 |
0.423 |
0.024 |
p-values |
||||||||
Feeding type |
0.306 |
0.386 |
0.932 |
0.863 |
0.257 |
0.462 |
0.929 |
0.045 |
Water temp. |
0.634 |
0.282 |
0.750 |
0.221 |
0.274 |
0.767 |
0.207 |
0.005 |
Interaction |
0.372 |
0.787 |
0.574 |
0.605 |
0.226 |
0.157 |
0.038 |
0.292 |
1 AF: Ad-libitum feeding; IF: Intermittent feeding; NW: Normal water; CW: Cold water; L*: Lightness, a*: Redness, b*: Yellowness | ||||||||
SEM: Standard error of means; Differences among the means were tested using Duncan’s multiple-comparison tests. Means in a column without a common lowercase letter significantly differ (P ≤ 0.05). |
In the last half-century, a significant increase in meat yield has been mainly (85–90%) achieved by genetic selection for rapid growth traits, nutrition, and management practices (Havenstein et al., 2003; Erensoy et al., 2020b). However, the thermoregulation ability of broilers could not develop simultaneously with their growth traits. This has made metabolic heat dissipation, which has become more difficult as a result of increased body weight and feed intake, especially in the last 2–3 weeks of the production period, even more, difficult in hot environmental conditions (Deeb et al., 2002; Zaboli et al., 2019). The presence of feathers and the absence of sweat glands in birds increase the sensitivity to high environmental temperatures (Lara Rostagno et al., 2013; Loyau et al., 2013) and negatively affect performance, welfare status, and meat quality traits (Akşit et al., 2006; Wang et al., 2013). In our study, IF and CW were given between 22–42 days of age to reduce the harmful effects of heat stress on some welfare and meat quality traits in broilers.
Approximately 4.5-5 oC higher temperature and 9–10% lower relative humidity levels were determined in the period when heat stress was applied (11–17 h) compared to the hours that were not applied. In our study, although 6-h of IF treatment under heat stress conditions provided a numerical decrease in rectal temperature, this was not at a significant level (as seen in Table 1). These results were found consistent with Farghly et al. (2018a) and inconsistent with the results of Özkan et al. (2003) and Farghly et al. (2018b). Marai et al. (1999), Abioja et al. (2011), and Park et al. (2015) reported that giving cold water suppressed the increase in body temperature of broiler chickens. In addition, it has been reported that drinking water at a lower temperature than the bird's body temperature will help to dissipate the body temperature more easily (Fairchild and Ritz, 2012). However, in the current study, CW treatment did not decrease the body temperature of broiler chickens at six weeks of age.
Panting is known to thermoregulate in many bird species (Steenfeldt et al., 2019). Syafwan et al. (2012) reported that rearing male broilers at 32°C during the day and at 25°C at night between 21–42 days did not change the panting rate. Abioja et al. (2011) and Farghly et al. (2018a) reported that CW intake reduces the panting rate in maintaining homeostasis in hot conditions in poultry. However, our study results showed that broilers in the AF×CW group under hot conditions showed the significantly highest panting rate at 4, 5, and 6 weeks of age in parallel (see Fig. 1). In previous studies, the effect of such an interaction on indicators of heat stress has not been tested before. While the panting rate is expected to decrease in broilers consuming CW (Farghly et al., 2018a), an unexpected effect occurred with AF×CW interaction. The fact that the body temperature of the AF chickens during heat stress hours (11–17 h) was 0.3 oC higher, although not at a significant level, may have caused more panting to remove metabolic heat from feed intake, in accordance with Farghly (2011). In addition, we speculated that consuming CW probably contributes to eliminating the harmful effects of heat stress on broilers and is consistent with Fairchild and Ritz (2012).
Broilers consuming CW had worse litter quality than those consuming NW (as seen in Table 3, P < 0.05). In the previous study we conducted on the same chicken materials (Erensoy et al., 2020a), it is known that IF and CW does not affect water consumption, so we speculated that the difference in water consumption does not cause the deterioration in the litter quality. However, chickens consuming CW showed more panting behavior at 4, 5, and 6 weeks of age (see Fig. 1). It is known that the duration of sitting or lying down (resting) behaviors increase with advancing age in broilers (Bessei, 2006). In addition, body weight increase as the growth period progress, so the floor area is almost completely covered by birds, making it difficult to ventilate the litter surface (Bessei, 2006). Although behaviors were not examined in our study, it is speculated that activity decreases with advancing age, possibly due to panting behavior, and that chickens consuming CW have more contact with relatively high moisture litter. Conversely, chickens in the AF×NW group showed less HB and BB (see Fig. 2). Water temperature treatment rather than feeding type seems more effective in the interaction effects for HB and BB, as shown in Table 3. In our study, more prolonged contact of the hock and breast with the litter increased the severity of HB and BB, consistent with Mench (2002) and Allain et al. (2009). However, the fact that FPD and LP were not significantly affected by this situation was not compatible with the general literature (Shepherd and Fairchild, 2010; Cengiz et al., 2011; Mello et al., 2015; Dunlop et al., 2016). In our study, both FPD and LP varied within minimal limits, and FPD was seen in only 3 chickens and LP in 5 chickens among all broilers (data not shown).
Pre-slaughter stress factors such as heat stress, fasting, handling, and water deprivation may affect meat quality (Mota-Rojas et al., 2006). One of our hypotheses for this study was that the negative effects of heat stress on meat quality could be reduced by management practices such as IF and CW treatments. However, it was seen that the results obtained partially supported our hypothesis. IF treatment decreased the panting rate compared to AF, but unexpectedly, the highest panting was observed in AF×CW broilers for all age periods (see Fig. 1). Panting behavior is a physiological response of birds to maintain thermal homeostasis under heat stress conditions, provide heat dissipation through respiration, and regulate body temperature (Yahav et al., 2005). The increase in the panting rate decreases the H + ions concentration in the blood plasma, causing a decrease in pH (respiratory alkalosis), and it becomes difficult to maintain body temperature balance (Sandercock et al., 2006; Zaboli et al., 2019). This mechanism results in a faster pH drop and lower ultimate pH in breast meat of broiler. PSE (pale, soft, and exudative) syndrome develops due to lower pH in breast meat, higher lightness (L*), lower redness (a*), and yellowness (b*) (Petracci et al., 2004; Akşit et al., 2006). However, in our study, IF and CW treatments were insufficient to significantly change the ultimate pH and color traits of breast meat compared to consuming AF and NW chickens (as seen in Table 4). These results were consistent with the report of Lippens et al. (2000) that IF does not affect the pH and color traits of breast meat. However, IF and CW treatments significantly decreased the ultimate pH of the thigh meat in broiler chickens. It is speculated that CW intake increases the panting rate and contributes to the decrease in ultimate pH of the thigh meat. In addition, the yellowness (b*) of thigh meat was also found the highest in IF×CW broilers (P = 0.038, see Fig. 3). Consistent with Lu et al. (2007), a further decrease in thigh meat pH of broilers in the CW group probably caused more yellowness (b*).
We concluded that management practices such as IF and CW in fast-growing broilers could not completely reduce the harmful effects of heat stress on some welfare and meat quality traits, and in some cases, even caused more negativity. When AF broilers consumed CW, the panting rate unexpectedly increased, and the severity of HB and BB increased. While IF and CW treatments did not affect the quality traits of breast meat, they decreased the ultimate pH value and increased the yellowness (b*) in thigh meat.
Acknowledgements
The authors would like to thank the technical and administrative staff working at the “Eskişehir Geçit Kuşağı Agricultural Research Institute”, where the study material was obtained and the breeding-selection practices of “Anadolu-T” broiler pure-lines were carried out.
Author contribution
All listed authors have made substantial contributions to the research design, analysis, or interpretation of data, and drafting the manuscript. All authors have approved the submitted version.
Funding
This study was supported by TAGEM of Republic of Turkey Ministry of Agriculture and Forestry (TAGEM/16/ARGE17) and Ondokuz Mayis University Project Office (PYO.ZRT.1901.18.014).
Data availability
Not applicable.
Code availability
Data were analyzed using SPSS (Version 25.0).
Ethical statement
All procedures for the rearing, management and slaughtering were approved by the Ondokuz Mayıs University Ethical Committee for Experimental Animals (30.06.2017; 2017/31).
Conflict of interest
The authors declare that they have no conflicts of interest.