Introduction
In European countries and the Mediterranean area, people have consumed rabbit meat for a long time. Rabbit meat has lower cholesterol content and higher levels of protein with essential amino acids than meat from other animal species (Dalle Zotte and Szendro, 2011). In addition, rabbit meat can be regarded as a functional food because of its potential for improvement in state of health and reduction of disease risk (Dalle Zotte and Szendro, 2011). Rabbit meat provides consumers with rich nutritive and bioactive compounds such as PUFA, DHA, and selenium to improve physiological functions. In addition, the low n-6/n-3 ratio in rabbit meat helps control cardiovascular and other chronic diseases. In the past 50 years, rabbit meat production in the world has increased 2.5 fold; 1.6 million tons were produced in 2009. China, Italy, Spain and France are the main rabbit meat producers (FAOSTAT, 2010). In commercial rabbit breeding, acceptable meat quality standards are one of the most important limiting factors for the economic output of a farm unit (Rotolo et al., 2013). Color, intramuscular fat (IMF) content, and pH value are all typical meat quality parameters (Dalle Zotte, 2002).
Hyla is a productive breed that is widely used in crossbreeding programs around the world (Hamouda et al., 1990). Hyla is a breed that has fast growth and high feed conversion as well as large litter size and high survival rate. Champagne displayed a high growth rate in young rabbits and was the most productive among medium-sized breeds (Bolet et al., 2004). Champagne is famous for its special fur and high meat production. Tianfu Black is a Chinese indigenous breed developed by the Sichuan Agricultural University in 2001. Currently, Tianfu Black rabbits are popular among Chinese breeders, but it is not well-known elsewhere the world. No research comparing carcass and meat quality traits among these three mediumsize rabbit breeds currently exists in China. Thus, the objective of this research was to compare carcass and meat quality traits in longissimus dorsi and biceps femoris muscles in the Hyla, Champagne, and Tianfu Black rabbit breeds. Two muscles were considered in this research because pH levels and rates of metabolism have been found to be dissimilar in different rabbit muscles (Blasco et al., 1990; Ouhayoun et al., 1983, 1988; Vigneron et al., 1976).
Materials and methods
Animals
This study was carried out at the experimental rabbitry of the Institute of Animal Genetics and Breeding, Sichuan Agricultural University, China. A total of 340 rabbits (168 males and 172 females) were used in this study. The number of rabbits by breed was 130 Hyla, 130 Champagne and 80 Tianfu Black. Rabbits were reared in individual cages after weaning at 6 weeks of age and fed ad libitum with a commercial diet using standard feeding and management protocols (NRC, 1977).
Carcass traits
Rabbits were slaughtered at 10 wk of age. The slaughter and carcass dissection procedures followed the World Rabbit Science Association (WRSA) recommendations (Blasco and Ouhayoun, 1996). The slaughter weight, head, skin, thoracic viscera (heart, lungs, trachea, esophagus and thymus), liver, kidneys, commercial carcass (includes head, thoracic viscera, liver and kidneys), reference carcass (no head or viscera) was weighed. Percentages of head, thoracic viscera, liver, kidneys and dissectible fat were calculated relative to the commercial carcass weight. Percentage of skin relative to slaughter weight as well as percentages of commercial and reference carcass weights relative to slaughter weight (dressing percentage) were also computed (Peiretti et al., 2013).
Meat quality traits
Measurements of pH (pH0 h) and color (L*0 h, a*0 h, b*0 h) were taken within 15 min after slaughter. Subsequently, after carcasses had been chilled for 24 at 4℃ measurements were taken for pH (pH24 h), color (L*24 h, a*24 h, b*24 h), and intramuscular fat (IMF). Measurements of pH, IMF and color were taken from the biceps femoris and longissimus dorsi muscles. The pH measurements were taken with a probe using a pH meter (Model PH-STAR CPU, Meister®, Germany). The probe was inserted directly into the muscle to a depth of 3 mm. The objective color was measured by using a Konica Minolta colormeter modal (CR-400, Japan) and the CIELAB system. Color data were expressed in terms of Lightness (L*), redness (a*) and yellowness (b*). Lightness (L*) ranged from black (0) to white (100), redness (a*) ranged from green (-60) to red (+60) and yellowness (b*) ranged from blue (-60) to yellow (+60). The IMF was analyzed using the modified Soxhlet method (AOAC, 1980).
Statistical analysis
Carcass and meat quality traits were analyzed using the following linear model:
Yijk = μ + Bi + Sj + eijk
Where Yijk was a meat quality trait, μ was the overall mean for each trait, Bi was the breed effect, Sj was the fixed sex effect, and eijk was the random error. Least squares means and their standard errors were computed for each breed. Breed least squares means were compared using Bonferroni t-tests. Computations were carried out using the general linear model (GLM) procedure of SPSS 21 (IBM, USA).
Results and Discussion
Carcass traits
Least squares means for carcass traits and dressing percentages in three rabbit breeds are presented in Table 1. No significant differences in slaughter weight was found among the three rabbit breeds (p>0.05) which indicated that the two exotic breeds (Hyla and Champagne) or local breed (Tianfu Black) had similar growth rates under the feeding levels and handling techniques utilized in the present study.
Table 1.The data are expressed as least square means±standard errors (Means±SE). Values with different superscripts within the same row differ significantly at p<0.05 (a, b) and p<0.01 (A, B).
Tianfu Black rabbits had the highest head percentage, followed by Champagne, whereas Hyla had the lightest heads. In addition, skin percentage in Tianfu Black was significantly higher than in the other two breeds (p<0.01). Lighter skins in the Hyla and Champagne rabbits may have given them an advantage in heat dissipation (Zeferino et al., 2013) relative to Tianfu Black rabbits. The substantially higher head and skin percentages of Tianfu Black would help farmers easily distinguish these rabbits from other medium-size breeds.
Significant differences between the three rabbit breeds existed for visceral organs (Table 1). Tianfu Black rabbits had heavier thoracic viscera than Hyla and Champagne rabbits (p<0.05). Champagne and Tianfu Black had similar liver and kidney percentages which were higher than that of Hyla (p<0.05). Thoracic viscera, liver and kidney are important organs to ensure that an animal has a healthy body and high productivity. Pascual and Pla (2007) suggested that higher head and thoracic viscera percentages may be due to lower degree of maturity of an animal. Commercial carcasses of Tianfu Black rabbits were significantly heavier than those of the Hyla and Champagne rabbits (p<0.05; Table 1). However, there was no significant differences among these three rabbit breeds for reference carcass percentages.
Paci et al. (2012) reported different percentages of skin, head, liver, kidney and reference carcasses in a local rabbit breed and commercial hybrid rabbits in Italy. Similarly, differences in skin, thoracic viscera, liver, kidney, commercial and reference carcass percentages were found between Botucatu and New Zealand White × Botucatu breed groups under three stress temperatures (Zeferino et al., 2013) and in a local rabbit population in Tuscany (Italy) in indoor and outdoor housing systems (D'Agata et al., 2009). Slaughter trait differences were also found in various large, medium, and small rabbit breeds (Chiericato et al., 1994; Pla et al., 1996; Tùmová et al., 2010). However, Ortiz Hernández and Rubio Lozano (2001) reported that breed and sex had no influence on carcass muscle percentage in New Zealand, Californian, Chinchilla, and Rex breeds in Mexico.
Meat quality traits
Table 2 and 3 show least squares means for longissimus dorsi and biceps femoris meat quality traits. Tianfu Black rabbits had higher pH0 h for longissimus dorsi (p<0.009; Table 2) and biceps femoris (p<0.012; Table 3) than Hyla and Champagne rabbits). Conversely, Tianfu Black had lower pH24 h than Hyla and Champagne rabbits for longissimus dorsi (p<0.006; Table 2). In addition, the lower pH24 h for biceps femoris in Tianfu Black than in Hyla and Champagne rabbits was nearly significant (p<0.054; Table 3). Hyla and Champagne rabbits had similar pH0 h and pH24 h values for both muscles. Values of pH0 h were higher than values of pH24 h in Tianfu Black, Hyla and Champagne. Lastly, values of pH0 h and pH24 h in longissimus dorsi were similar to corresponding values in biceps femoris in these three breeds. Our pH24 h values were similar to those of Mazzone et al. (2010) who reported pH24 h in male rabbits subjected to smooth (pH24 h=5.79) and rough loading methods (pH24 h=5.81).
Table 2.The data are expressed as least square means±standard errors (Means±SE). Values with different superscripts within the same row differ significantly at p<0.05 (a, b) and p<0.01 (A, B).
Table 3.The data are expressed as least square means±standard errors (Means±SE). Values with different superscripts within the same row differ significantly at p<0.05 (a, b) and p<0.01 (A, B, C).
Muscles have been found to possess a variety of different chemical components. For example, slow red fibers are rich in oxidative enzymes, but rapid white fibers are rich in both glycogen and glycolytic enzymes. These enzymatic differences lead to differences in muscle fiber topology. This has been called muscular heterogeneity. Muscular heterogeneity would produce differences in acidification kinetics and the ultimate pH in different muscles (Blasco and Piles, 1990; Nath and Rao, 1985; Niedzwiadek et al., 1983; Osman, 1991; Renou et al., 1986). In our case, differences in pH found in the longissimus dorsi and biceps femoris muscles here suggest that the acidification process in these two muscles differed in the three breeds. The pH also affects the appearance of raw meat and the tenderness of cooked meat. On the other hand, muscle ultimate pH has an important influence on meat quality (Watanabe et al., 1996) and is related to the rate of glycogen breakdown and liberation of lactate post-slaughter. Thus, our goal was to achieve an ultimate pH a little lower than 6.0 by 24 h (Table 2, Table 3). This was considered to be essential for good product quality (Mach et al., 2008; Terlouw, 2005). A pH substantially lower than 6.0 (e.g., 5.0) would make the meat too firm and dry because the myofibrillary network would shrink and water holding capacity (WHC) would decrease.
Least squares means for longissimus dorsi (Table 2) showed that there were no significant differences among the three rabbit breeds for L*0 h and L*24 h. Values of a*0 h in Tianfu Black rabbits were significantly different from a*0 h values in Hyla and Champagne breeds (p<0.01), but there was no significant differences between Hyla and Champagne breeds (p>0.05). The value of a*24 h in Tianfu Black rabbits was significantly higher than that of Hyla rabbits (p<0.05), and Champagne rabbits had no significant differences with Tianfu Black and Hyla rabbits (p>0.05). Tianfu Black rabbits had a significantly higher b*0 hthan Hyla rabbits (p<0.05), and Champagne rabbits had no significant differences with Tianfu Black and Hyla rabbits (p>0.05). Champagne rabbits had significantly higher values of b*24 h than Hyla and Tianfu Black rabbits (p<0.01), but no significant differences were found between Hyla and Tianfu Black rabbits (p>0.05). Hyla rabbits had a significantly higher IMF than Champagne and Tianfu Black rabbits (p<0.01), and there was no significant differences between Champagne and Tianfu Black rabbits (p>0.05). Thus, a* (0 h and 24 h) and b* (0 h and 24 h) values in the longissimus dorsi muscle were significantly different among these three rabbit breeds (p<0.05).
Least squares means for biceps femoris (Table 3) showed that that no significant differences existed for L*24 h among the three rabbit breeds (p>0.05). The L*0 h, a*0 h and a*24 h values were significantly higher in Tianfu Black rabbits than in Hyla and Champagne rabbits (p<0.05). Tianfu Black rabbits had higher b*0 h values than Champagne rabbits (p<0.01), and b*0 h values in Champagne rabbits were higher than in Hyla rabbits (p<0.01).
Comparisons of meat color trait least squares means for longissimus dorsi muscle (Table 2) and biceps femoris muscle (Table 3) indicated that: 1) The value of L*24 h in the three rabbit breeds was higher than that of L*0 h in both longissimus dorsi and biceps femoris muscles. However, the biceps femoris muscle had somewhat higher L*0 h and L*24 h values than the longissimus dorsi muscle; 2) Values of a*0 h and a*24 h were larger in longissimus dorsi than in biceps femoris in the three rabbit breeds; and 3) Values of b*24 h were higher than those of b*0 h in the three rabbit breeds in the longissimus dorsi and biceps femoris muscles, and values of b*0 h and b*24 h were similar in both longissimus dorsi and biceps femoris muscles.
The meat color depends on the level of myoglobin, oxydo-reduction, the degree of oxidation of iron atoms, and on a possible denaturation of globin (Guidera et al., 1997; Monika et al., 2010; Newcom et al., 2004; Pla et al., 1996). Tianfu Black had the highest values for a*0 h and a*24 h indicating that meat from Tianfu Black rabbits had a darker red color than meat from the other two breeds. Higher a* values in Tianfu Black were likely related to higher pigment content (Renerre, 1990). Champagne rabbits had the highest b*24 h values in both longissimus dorsi and biceps femoris muscles. However, differences in b*24 h observed here among breeds were small, thus it is likely that consumers would be unable to distinguish differences in yellowness visually.
Pascual and Pla (2007) reported that selection for growth rate in rabbits would increase the oxidative metabolism route and change the meat color. However, Hernández et al. (2006) reported that selection for growth rate did not affect the main sensory characteristics of meat, such as tenderness, juiciness, and fibrousness, but it had a negative effect on aniseed odor, aniseed flavor, and liver flavor. Intense artificial selection for growth rate of meat-type birds has resulted in a higher incidence of abnormal conditions (e.g., PSE-like meat), however this has not been found in rabbit meat (Cavani et al., 2009). Several researchers reported that the pre-slaughter environment (e.g., housing temperature, rearing techniques, feeding regimens, transport conditions and time) influenced blood biochemical parameters and meat traits in rabbits (Combes et al., 2010; Corino et al., 2007; Sabuncuoglu et al., 2011), thus producers should offer rabbits suitable pre-slaughter environmental conditions to obtain high-quality meat.
Least squares means for longissimus dorsi (Table 2) indicated that Hyla rabbits had significantly higher IMF values than Champagne and Tianfu Black rabbits (p<0.01), and that there were no significant differences between Champagne and Tianfu Black rabbits (p>0.05). Similarly, least squares means for biceps femoris (Table 3) showed that Hyla had a far higher IMF than the other two breeds (p<0.01; Table 3). Thus, Hyla rabbits had substantially higher IMF values than other two breeds in both muscles. However, the biceps femoris IMF values were all larger than the corresponding longissimus dorsi IMF values for the three breeds. The IMF value here was far lower than the IMF value in lean meat (5.4±0.9) found in hybrid rabbits produced by crossing two SIKA genotype lines in Slovenia (Polak et al., 2013). These authors reported that lean meat IMF content differed by genotype line, sex and age at slaughter and that IMF increased with age. Ouhayoun (1988) found differences in hind leg fat content among seven breeds of large, medium and small size rabbits slaughtered at 11 wk of age; large size breeds had lower fat content than small size breeds. Compared to pig meat, rabbit meat has a lower intramuscular fat and this intramuscular fat has a high percentage of unsaturated fatty acids and a low cholesterol level (Cavani and Petracci, 2008; Hernández et al., 2006). These characteristics give rabbit meat an advantage over pork when attracting consumers intent on buying healthy meat.
Conclusions
This study found differences in carcass and meat quality traits among three rabbit breeds. Tianfu Black rabbits had higher commercial carcass, head, skin, and thoracic viscera percentages than Hyla and Champagne rabbits. Tianfu Black had the lowest pH at 24 h, the highest redness color values at 0 and 24 h post-mortem, and lower intramuscular fat percent than Hyla and Champagne. Conversely, Hyla rabbits had the highest pH values, lightness, and yellowness at 24 h as well as the highest intramuscular fat percentages. Based on results here, we recommend the Tianfu Black breed for commercial rabbit production.
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