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METABOLISM AND NUTRITION |
* CIISA – Faculdade de Medicina Veterinária, Pólo Universitário do Alto da Ajuda, Avenida da Universidade Técnica, 1300-477 Lisbon, Portugal; Fertiprado, 7450-250 Vaiamonte, Portugal; CECAV – Universidade de Trás-os-Montes e Alto Douro, Apartado 1013, 5000-911 Vila Real, Portugal; Instituto Superior de Agronomia, Tapada da Ajuda, 1349-017 Lisbon, Portugal; and || Estação Zootécnica Nacional, Instituto Nacional de Investigação Agrária e das Pescas, Fonte Boa, 2005-048 Vale de Santarém, Portugal
1 Corresponding author: cafontes{at}fmv.utl.pt
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Key Words: free-range broiler • pasture intake • broiler performance • meat quality
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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In the United States, small farmers have adopted a free-range poultry production method that promotes pasture intake, which has been termed the pastured poultry system (http://www.apppa.org). At 3 or 4 wk of age broilers are introduced into floorless portable pens that are moved daily to fresh pasture to encourage forage intake. Compared with conventional free-range and organic systems, the pastured poultry alternative is likely to induce considerably greater levels of pasture consumption, and thus it is an ideal system to evaluate the nutritional impact of pasture intake in broiler performance and meat quality. Pasture may constitute a source of energy and protein for growing broilers. In addition, the presence of a range of bioactive compounds in the forage, such as xanthophylls and several hypocholesterolemic and anticarcinogenic compounds, may lead to improvements in meat quality (Ponte et al., 2004a). However, the high fiber content of pasture biomass may limit nutrient utilization and could reduce growth rates and feed efficiency. To our knowledge, the effects of pasture intake in broiler performance and meat quality in free-range systems remain largely unknown.
Microbial cellulases and hemicellulases are widely used for supplementing poultry diets rich in nonstarch polysaccharides (Bedford, 2000; Fontes et al., 2004). Soluble arabinoxylans and β-glucans lead to a considerable increase in digesta viscosity, therefore interfering with the movement of particles and solutes across the intestinal lumen and reducing the access of the repertoire of digestive enzymes to their substrates (Edwards et al., 1988; Bedford et al., 1991). Endo-acting polysaccharide hydrolases added to the diets decrease the degree of polymerization of the recalcitrant nonstarch polysaccharides, leading to a considerable reduction in digesta viscosities (Bedford and Classen, 1992). In addition, breakdown of plant cell-wall polysaccharides improves the access of the digestive biocatalysts to the endosperm contents that were otherwise trapped (Chesson, 1993). However, it is unknown if cellulases and hemicellulases could contribute to improving the nutrient utilization of pasture biomass from free-range broilers. For this application polysaccharidases would have to contribute to a significant hydrolysis of the recalcitrant carbohydrates at the upper part of the gastrointestinal tract so that more energy could be absorbed in the small intestine and hindgut.
The objective of this study was to establish the impact of pasture intake on broiler performance and resulting meat quality. Free-range broilers were allowed access to subterranean clover (Trifolium subterraneum) or white clover (Trifolium repens) based pastures. Birds in a control group remained in the same site but without access to the pastures, to allow a rigorous identification of the effects of herbage intake. The capacity of cellulases and hemicellulases to improve the nutritive value of diets containing significant percentages of forage was investigated. In addition, the sensory attributes of meat derived from the described production systems were evaluated. Finally, a comprehensive characterization of the fatty acid profile and the contents in cholesterol, tocopherols, and tocotrienols of broiler meat derived from such treatments is presented in the companion paper (Ponte et al., 2008).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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. The cellulase and hemicellulase supplement was added to the cereal-based diet at a level of 0.41% (wt/wt) and consisted of a mixture of 1:10:30 of Roxazyme G (Roche Vitamins Ltd., Basel, Switzerland), Avizyme 1300 (Danisco Animal Nutrition, Wiltshire, UK), and Avizyme 1100 (Danisco Animal Nutrition). Roxazyme G contains a minimum of 1,600 U/g of cellulase, 3,600 U/g of endo-1,3(4)-β-glucanase and 5,200 U/g of endo-1,4-β-xylanase; Avizyme 1300 contains a minimum of 300 U/g of endo-1,4-β-xylanase, 300 U/g of endo-1,3(4)-β-glucanase, and 800 U/g protease; and Avizyme 1100 contains a minimum of 2,500 U/g of endo-1,4-β-xylanase and 800 U/g of protease. Although the Roxazyme G supplement was incorporated at the recommended level, the incorporation levels of Avizyme 1100 and 1300 were 4 and 1.3 times greater, respectively, than the recommended doses. This enzyme mixture was used in an attempt to hydrolyze at least part of the cellulose and the hemicelluloses fractions of the pasture. To promote forage intake, the portable pens of the treatments with access to pasture were moved daily so that birds could access fresh herbage every day. The 2 pastures used by the birds in these experiments were contiguous, to avoid climate variations, and were installed in the autumn of 2002. The white clover pasture was irrigated during the dry summer season (June–September). Pens of the NP treatment were located in a fixed position, in the same field, and access to the pasture was blocked in the initial days and throughout the experiment by adding new pine wood shavings to the ground.
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Analytical Procedures
Analyses for DM (method 934.01), crude fat (method 920.39), CP (method 954.01), neutral detergent fiber (method 2002.04) and acid detergent fiber/acid detergent lignin (method 973.18) were performed according to the methods specified by Association of Official Analytical Chemists (1980). Cellulase and xylanase assays were performed using carboxymethylcellulose and oat spelt xylan, respectively, according to the methods described by Fontes et al. (2000). Analysis of cellulase and xylanase activity in the digesta contents recovered from the various gastrointestinal compartments was assessed in agar plates, using the polysaccharides referred above at 0.1% (wt/vol) final concentration in 10 mM Tris HCl pH 7.0. Activity was detected after 16 h of incubation at 37°C through the Congo Red assay plate, as described in Ponte et al. (2004b) and Mourão et al. (2006).
Microbial Evaluation
Prevalence of Campylobacter and Salmonella spp. on farm was determined by monitoring the presence of both pathogens in feces, water, and the cereal-based feed. At the beginning and end of both experiments (birds at 28 and 56 d of age, respectively), samples of water and of the basal feed (25 g) were collected for microbial quantification (n = 5). In addition, 20 fecal samples were randomly collected from birds of the 6 treatments by cloacal swab using sterile cotton-tipped swabs. Campylobacter and Salmonella were detected and quantified following the methods described by Musgrove et al. (2001) and McCrea et al. (2006), respectively, which essentially follow the International Organisation for Standardization methods ISO/ FDIS 10272-1 (2005) and ISO 6579 (2002).
Skin Color
The color of breast skin was evaluated using a Minolta chromameter CR-300 (Osaka, Japan). The readings were taken on equivalent positions of the carcasses. The tip of the chromameter measuring head was placed flat against the surface of the skin. For each reading, 3 measurements were performed and the final value for each bird is the average of those readings. Skin color was expressed in the CIELAB dimensions of lightness (L), redness (a), and yellowness (b). Skin color evaluation was performed before the carcasses were frozen at –20°C.
Sample Preparation for Sensory and Shear Force Analysis
Approximately 4 wk after slaughtering, a consumer test was conducted on the breast meat at Estação Zootécnica Nacional kitchen/sensory facility (Vale de Sanatarém, Portugal). Carcasses were thawed at refrigerated temperature (4°C) and cooked for 40 min in a standard commercial oven at 200°C, such that the final internal temperature of the meat was 65°C (±5°C). From each carcass, half of the breast was used for sensory evaluation and the other half was prepared for shear force values by cutting two 1.9-cm-wide strips. Only pectoralis major muscle was used for shearing force evaluation using a Warner-Bratzler shear device, attached to a TA-tx2i Texture Analyser (Stable Micro Systems, Godalming, UK). The measurements of maximum shear force were taken on equivalent positions of the strip. Triplicate shear measurements were recorded on each breast and averaged.
Sensory Analysis
The sensory evaluation of meat samples from the spring experiment was performed by a sensory panel that was not screened for behavior such as poultry consumption habits or free-range poultry purchasing. The sensory panel consisted of 30 untrained consumers who had previously participated in similar sensory evaluations and were chosen from the staff of Estação Zootécnica Nacional. Panel members were not given any information about the meat or the experimental treatments and procedures. Serving sizes were half of a split breast piece served without the skin. Panelists were asked to evaluate liking of tenderness, juiciness, flavor, and overall appreciation of each meat sample individually, on a 1 to 5 scale (1 = very disagreeable; 2 = disagreeable; 3 = neither agreeable nor disagreeable; 4 = agreeable; 5 = very agreeable).
Statistical Analysis
Statistical analysis was conducted by ANOVA using SAS with the GLM procedure (SAS Institute, 2004). The experimental unit considered was the pen. In relation to the bird performance data, initially the model considered the effects of pasture intake, season, enzyme supplementation, and the interactions between the various effects. Because none of the interactions were found to be significant (P > 0.84), they were removed from the model. Unless otherwise stated, differences were considered significant when P < 0.05.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Although the nutritive value of the herbage changed according to the time of the year, both pastures displayed relatively high CP contents in both the spring and autumn, because of the predominance of leguminous species (Table 2
). However, DM percentages were always relatively low (see Table 2) and neutral detergent fiber was the main organic component of the pasture. Although chickens have been reported to feed on a wide range of macro-invertebrates living in the surface soil (Clark and Gage, 1996), the contribution of macro-invertebrates to the diet of free-range broilers was not quantified in these experiments.
Bird Performance
The results of the 2 experiments, expressed as final BW, BW gain, feed intake, and feed conversion ratios are summarized in Table 3. In both seasons, the final BW of birds consuming pasture were significantly greater than that of the control birds kept under the same environmental conditions but not allowed to forage. The differences in the final BW were related to the greater BW gains of grazing birds, which ranged from 75 to 150 g more BW compared with the nongrazing birds in the 4 wk of the experiment. The data suggest that, in general, pasture intake promoted an increase in the consumption of the cereal-based feed. In the spring experiment, consumption of the cereal-based feed showed a trend for increase in birds in the TrP group (P = 0.107) and this trend was also manifested for the birds in the TsP group, although the differences relative to the control birds were not significant (Table 3). Interestingly, in the autumn experiment, birds consuming forage always had greater intakes of the cereal-based feed compared with the nongrazing birds, although the intakes were even greater for the broilers in the TsP group. These data suggest that differences in the levels of cereal-based feed consumption may be related to the composition or the levels of pasture intake, or both. There were no differences between the feed conversion ratios of birds subjected to the 3 different grazing regimens, suggesting that bird performance primarily depends on the intake of the cereal-based feed rather than from an improvement in the efficiency of nutrient utilization per se. Finally, it is interesting to verify that, considering the theoretical suboptimal environmental conditions to which the free-range chicken were subjected compared with birds housed indoors, the growth rate achieved by the broilers in both the spring and autumn experiments is at the levels expected for the genotype RedBro Cou Nu x RedBro M (2,079 g of BW at d 56; Hubbard ISA management manual). However, feed conversion ratios were considerably greater than expected for this genotype (should be 2.1 to 2.2 at d 56), suggesting that birds can compensate growth at inappropriate temperatures, humidity, and light intensity by increasing feed intakes. The difference between our results for feed conversion and those in the Hubbard ISA management manual could also result from different energetic concentrations of diets: the cereal-based feed had 12.12 MJ of AME/kg instead 13.38 MJ of AME as recommended in the management manual.
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The capacity of a complex mixture of cellulases and hemicellulases to improve the nutritive value of diets of pasture broilers was evaluated. The data presented in Table 3 suggest that supplementation of the cereal-based feed with heavy doses of exogenous polysaccharidases was unable to significantly improve bird performance in both the spring and the autumn experiments. It is possible that the inability of polysaccharidases to improve the performance of free-range chickens results from enzyme inhibition or proteolysis in the gastrointestinal tract. To exclude this possibility, digesta samples were collected from the various gastrointestinal compartments and tested for cellulase and xylanase activity. The data (not shown) demonstrated that high levels of both cellulase and xylanase activities were present in the crop, duodenum, and jejunum of birds fed with the cereal-based feed supplemented with the plant cell-wall hydrolases. Under the same conditions, no enzyme was detected in the corresponding compartments of birds fed on the basal diet without exogenous enzymes. As expected, all birds (whether supplemented or not with the microbial enzymes) displayed high levels of polysaccharidase activity in the cecum (not shown). Together, the data suggest that the incapacity of enzymes to improve bird performance may result from the low intake of pasture material (2.5 to 4.5% on a DM basis). In addition, the complexity of pasture plant cell-wall polysaccharides may require greater enzyme doses eventually with different enzyme specificities acting for longer periods than that allowed from the short digestive transit period of chicken.
On-Farm Microbial Contamination
Campylobacter and Salmonella are the 2 leading sources of foodborne illness in Europe and the United States. The prevalence of infection is usually greater in free-range birds compared with birds in enclosed housing, because outdoor birds potentially have increased exposure to additional vectors of infection (McCrea et al., 2006). Therefore, during the field experiments the prevalence of Campylobacter and Salmonella on farm was determined. No positive samples were encountered in the water, cereal-based feed, or birds at the beginning or end of the experiments (data not shown), suggesting that birds were not contaminated at the start of the experiments and did not become infected during the 28-d outdoor trial. These data are unusual considering the considerable prevalence of both pathogens on free-range chicken farms as reported by other studies (Rivoal et al., 1999; Heuer et al., 2001; McCrea et al., 2006). Although the number of samples analyzed in each experiment might have been low (30 at the beginning and 30 at the end), it is possible that the on-site conditions were particularly favorable to avoid microbial contamination because the pastures had not previously been used for grazing chickens. Although the potential for the transmission of foodborne pathogens to humans through free-range poultry products is real, it is clear that the prevalence of the pathogens can be low and will vary widely with the on-farm conditions.
Meat Physical Properties
The influence of the production system, particularly pasture intake, in various aspects of the overall quality of poultry meat was investigated. In the companion paper (Ponte et al., 2007), we will describe aspects of the biochemical properties of broiler chicken meat derived from these experiments. In the present study, the influence of pasture intake in carcass yield, meat pH, texture, and skin color were evaluated. Because enzyme supplementation had no influence on broiler performance, experiments with meat samples were performed exclusively with meat samples of birds not supplemented with the exogenous enzymes. The data, presented in Table 4, showed that pasture intake had a positive effect on carcass yield in both experiments. This is unexpected because the expected greater activity of grazing birds is believed to improve the proportion of wings, thighs, and drum sticks, whereas foraging could increase the proportion of gastrointestinal tract tissues on the overall BW. However, Fanatico et al. (2005) found no differences in the carcass yield of indoor and outdoor birds. Therefore, it is possible that carcass yield may have been affected by 2 factors: birds with pasture had a more developed gastrointestinal tract (due to greater fiber intake and total feed intake) that reduced carcass yield but had greater BW that generated a trend to increase it.
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). This is surprising because several studies have indicated a decrease in the pH of meats from outdoor-reared pigs and chicken, reflecting better welfare conditions, reduced preslaughter stress, and thus reduced consumption of glycogen (Enfält et al., 1997; Castellini et al., 2002). Interestingly, meat from the older birds had consistently higher pH values. Tenderness is an important attribute for consumers and was measured by evaluating meat shear force values. Overall, the data demonstrated that pasture intake did not affect meat texture (Table 4): in the spring experiment, NP meat had a similar (P > 0.05) shear force to that observed in the TsP and TrP groups, whereas in the autumn experiment, shear force was similar (P > 0.10) in the 4 groups tested. However, conventional free-range chickens at 81 d of age were shown to have less tender meat, an observation that might be directly correlated with a greater proportion of cross-linked collagen in older birds.
Results of the colorimetric evaluation of breast skin are presented as the CIELAB values of L (lightness), a (redness), and b (yellowness) in Table 5. In general, pasture intake did not influence broiler skin color. However, in the spring experiment, birds in the TrP group displayed higher L scores, indicating a less deeply pigmented skin. Interestingly, in both experiments, birds from the nonpasture treatment displayed a considerable increase in the broiler carcass redness (a), showing that the usually undesirable pink and red tones in the skin were more developed. Overall, the data suggest that the skin from NP, TsP and TrP birds had higher b values compared with the commercial broilers, suggesting a greater efficacy of the cereal-based feed for pigmenting the carcasses with yellow tones, which may result from the high proportion of corn in the feed. This is supported by the observation that, although pasture contains carotenoid pigments (Toyopmizu et al., 2001), no improvement of the yellowness of the breast skin color was observed when diets contain a considerable proportion of corn (Schaible, 1970). In addition, the increased levels of cereal-based feed ingested by birds foraging on the clover-based pastures had no influence on the carcass yellowness, suggesting that pigments supplied by the corn-based feed were already present at a saturating level in nonforaging birds.
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suggest that the intake of TsP had no effect in meat tenderness, juiciness, and flavor. In addition, the panel was unable to discriminate meat originated from commercial, NP, and TsP birds in terms of juiciness and flavor. As expected, meat originating from conventional free-range chickens slaughtered at d 81 was classified as less tender compared with meat of birds from the fast-growing genotype (Ross) slaughtered at d 35, or meat from the NP and TsP birds of this study (slaughtered at d 56). In contrast, the younger age and fast-growing genotype of the Ross should have contributed to the classification of the meat as more tender. Differences in tenderness may be due to the fact that fast growth in birds leads to larger muscle fibers and differences in proteolytic potential (Dransfield and Sosnicki, 1999). However, it is possible that in some conditions differences in texture are subtle and not differentiated by the consumers.
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In conclusion, the supplementation of a cereal-based diet for pastured broilers with a heavy load of microbial cellulases and hemicellulases had no impact on broiler performance. In contrast, the data suggest that pasture intake promotes growth by improving the consumption of the cereal-based feed, although the levels of forage intake (on a DM basis) were low. Together, the data presented here and in the companion paper (Ponte et al., 2007) suggest that pasture intake improves meat sensory attributes, supporting the consumer assumption that poultry products derived from free-range pastured-based systems present greater standards of sensory quality.
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ACKNOWLEDGMENTS |
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Received for publication April 10, 2007. Accepted for publication September 8, 2007.
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