Japanese quail meat quality: Characteristics, heritabilities, and genetic correlations with some slaughter traits

Japanese quail meat quality: Characteristics, heritabilities, and genetic correlations with some slaughter traits Dogan Narinc,* Tulin Aksoy,* 1 Emre Karaman,* Ali Aygun, Mehmet Ziya Firat,* and Mustafa Kemal Uslu * Faculty of Agriculture, Department of Animal Science, Akdeniz University, Antalya, 07100, Turkey; Faculty of Agriculture, Department of Animal Science, Selcuk University, Konya, 42075, Turkey; and Faculty of Engineering, Department of Food Engineering, Akdeniz University, Antalya, 07100, Turkey ABSTRACT The aim of this study was to evaluate the genetic parameters of several breast meat quality traits and their genetic relationships with some slaughter traits [BW, breast yield (BRY), and abdominal fat yield (AFY)]. In total, 1,093 pedigreed quail were slaughtered at 35 d of age to measure BRY, AFY, and breast meat quality traits [ultimate ph (ph U ), Commission Internationale d Eclairage color parameters (L*, lightness; a*, redness; and b*, yellowness), thawing and cooking loss (TL and CL, respectively), and Warner-Bratzler shear value (WB)]. The average ph U, L*, a*, and b* were determined to be 5.94, 43.09, 19.24, and 7.74, respectively. In addition, a very high WB average (7.75 kg) indicated the firmness of breast meat. High heritabilities were estimated for BW, BRY, and AFY (0.51, 0.49, and 0.35). Genetic correlations of BW between BRY and AFY were found to be high (0.32 and 0.58). INTRODUCTION Japanese quail (Coturnix coturnix japonica) is used as a model animal and also is one of the sources for eggs and meat, particularly for the niche market. Much research is conducted to improve growth because Japanese quail respond quickly to selection for BW (Anthony et al., 1986; Caron et al., 1990; Marks, 1996). In addition, some studies were carried out aiming to improve carcass composition (Lotfi et al., 2011) and feed conversion (Khaldari et al., 2010; Varkoohi et al., 2010). On the other hand, selection of meat-type chickens focuses not only on growth performance and On the other hand, the moderate negative relationship between BRY and AFY ( 0.24) implies that selection for breast yield should not increase abdominal fat. The ph U was found to be the most heritable trait (0.64), whereas the other meat quality traits showed heritabilities in the range of 0.39 to 0.48. Contrary to chickens, the genetic correlation between ph U and L* was low. The ph U exhibited a negative and high correlation with BW and AFY, whereas L* showed a positive but smaller relationship with these traits. Moreover, ph U exhibited high negative correlations ( 0.43 and 0.62) with TL and WB, whereas L* showed a moderate relationship (0.24) with CL. This genetic study confirmed that the multi-trait selection could be used to improve meat quality traits. Further, the ultimate ph of breast meat is a relevant selection criterion due to its strong relationships with either water-holding capacity and texture or low abdominal fatness. Key words: meat quality in Japanese quail, water-holding capacity, Warner-Bratzler, genetic parameter, Gibbs sampling 2013 Poultry Science 92 :1735 1744 http://dx.doi.org/10.3382/ps.2013-03075 2013 Poultry Science Association Inc. Received January 29, 2013. Accepted March 20, 2013. 1 Corresponding author: tulinaks@akdeniz.edu.tr carcass parts but also on improved meat quality because recently chicken meat is consumed as cuts or as processed products rather than as whole carcass (Le Bihan-Duval et al., 2008). The most important poultry meat quality attributes are appearance and texture because they most influence consumers initial selection and ultimate satisfaction with products. Moreover, one of the major contributing components of appearance is color (Fletcher et al., 2000). The author, taking into account the results of much research, concluded that the major factors affecting poultry meat color were heme pigment content of meat and also preslaughter, postslaughter, and slaughter factors. The best way to determine the texture of cooked meat is through the sensory analysis of experienced panelists, which is an expensive and demanding method. Warner-Bratzler (WB) shear test for toughness of cooked meat is the most widely used and primary method (Cavitt et al., 2005; Lee et al., 2008). 1735

1736 Narinc et al. In common with other species, variation in the rate and extent of rigor mortis development, and therefore the ultimate ph (ph U ), markedly affect the technological quality of poultry meat. However, as a result, the quality of meat is a product of complex interactions between the genotype of an animal and its environment (Le Bihan-Duval, 2004). Le Bihan-Duval et al. (2001) estimated the genetic parameters for meat quality traits in an experimental meat-type chicken line in which a long-term selection program was applied for high BW and breast yield (BRY) as well as low abdominal fat percentage (AFY). They reported moderate to high (range from 0.35 to 0.57) estimates of heritabilities for ph 15, ph U, L*, a*, b*, and drip loss. In another study on turkey, Le Bihan-Duval et al. (2003) obtained similar results. Duclos et al. (2007) reported that selection on high breast muscle development and low abdominal fat percentage results in decreased glycogen storage, which leads to a reduced postmortem acidification and water-holding capacity. Researchers also reported that there is no evidence of any antagonism between growth rate or muscle development and breast meat quality characteristics such as water-holding capacity and technological quality. Le Bihan-Duval et al. (2008) estimated genetic parameters for several meat quality traits (L*, a*, b*, drip loss, thawing-cooking loss, and WB shear force) and their genetic relationships with muscle characteristics (breast ph, glycolytic potential, and so on) in a heavy commercial line of broiler chickens. The authors concluded that the strong relation of ph U to meat color, water-holding capacity, and texture renders it a relevant selection criterion. There are only a few studies carried out on meat quality and its genetic components in Japanese quail. Remignon et al. (1998) investigated the effect of acute stress on some meat quality traits of quail. Genchev et al. (2008) presented the results of a study in which slaughter-carcass traits and chemical and quality characteristics of meat were examined. Oguz et al. (2004) estimated the heritabilities for BW, breast weight and yield, ph U, and breast meat color parameters in a random bred Japanese quail flock. Gevrekci et al. (2009) estimated the heritabilities for some production traits such as BW and breast weight and for some meat quality traits in a randombred Japanese quail flock. To our knowledge, there is no literature on genetic correlations among meat quality characteristics and their relationship between slaughter traits. This study was aimed to estimate the multi-trait genetic parameters (heritabilities and genetic correlations) for BW, BRY, AFY, and some meat quality traits via Bayesian methodology. Birds MATERIALS AND METHODS The experiment was conducted at the Animal Science Department, Akdeniz University. The care and use of animals were in accordance with laws and regulations of Turkey and approved by The Ethical Committee of Akdeniz University (decision number 09/69 02.14.2011). In this research, an experimental flock of 1,093 pedigreed quail was obtained on a single hatch from 160 male and 480 female breeders of a sire line where a selection was applied for one generation using multi-trait best linear unbiased prediction methodology considering 4 traits (BW, carcass yield, feed conversion ratio, and inflection point of age derived from Gompertz growth curve) was used. All chicks were wing banded after hatching and they were housed in brooding cages (82.56 cm 2 /quail) until sex determination at 21 d of age. Afterward, they were transferred to grower cages (150 cm 2 /quail). The diet containing 24% CP and 2,900 kcal of ME/kg was used for the first 21 d; the finisher ration had 21% CP and 2,800 kcal of ME/kg. Ad libitum feeding and a 18 h lighting program were applied from hatch to the end of the experiment. Measurements At 35 d of age, the BW of all male and female quail were determined 6 h after feed withdrawal and slaughtered in an experimental processing plant. The birds were stunned in an electrical water bath (average ± SD, 275 V ± 6.0, and 60 ma ± 0.15; applied for 4 s) as applied in Tserveni-Gousi et al. (1999), and then manually cut, bled out, scalded (55 C, 2 min), defeathered with equipment, manually eviscerated, and the abdominal fat pad (from the proventriculus surrounding the gizzard down to the cloaca) was taken, chilled in an ice-water tank, and drained. All carcasses were individually placed in plastic bags and stored in +4 C for a night. Next morning, after carcass dissection, breast with bone and the remaining abdominal fat on cold carcasses were weighed (in gram) using an electronic digital balance with a sensitivity of 0.01 g. Slaughter and dissection were performed by same experienced operators. Breast and total fat pad yields (BRY and AFY) were calculated in relation to BW at 35 d. After immediate carcass dissection (about 24 h postmortem), the ph U values were measured by directly inserting the glass electrode of the ph-meter (Testo 206-pH2, Testo Ltd., Istanbul, Turkey) into the anterior part of left pectoralis major muscle (Berri et al., 2001). Breast meat color was determined on the medial surface (bone-side) of each right breast fillet using a Minolta Chromameter (CR-300, ECS Ltd., Izmir, Turkey). The bone side was used to avoid colorations of the breast surface caused by scalding (Fletcher et al., 2000). The Commission Internationale d Eclairage L*a*b* system was used, where L* is the lightness of the meat, a* the redness, b* the yellowness (Swatland, 1985; Monnin, 1998). After measuring the color parameters, all of the right pectoralis major were trimmed to small particles and were individually weighted and placed in plastic bags.

At this time, the weight of each right fillet was recorded as the initial muscle weight. All packed right fillets were placed in 18 C for 28 d. At the end of storage period, breast samples were thawed in a refrigerator (+4 C) for 24 h, and then they were removed from bags, wiped with paper properly, and weighted (thawed weight). After this measuring, all muscle samples were placed in plastic bags in a water bath (80 C) until they reached an internal temperature of 70 C, and chilled to room temperature, wiped, and weighed (cooked weight) again (Jiang et al., 2011). Thawing loss (TL) was determined as percentage of weight loss after thawing to initial muscle weight. Cooking loss (CL) was calculated as the difference between the cooked and uncooked weights, which was expressed as a percentage of the uncooked weight (Northcutt et al., 2001; Lee et al., 2008). To determine the toughness of breast meat, a Texture Profile Analyzer (TA-XT plus Stuble Microsystems, Godalming, Surrey, UK) device with a WB shearing knife was used. The samples (1 2 0.5 cm) were vertically taken from the muscle fibers of cooked meat. These samples were cut with WB shearing knife and measured by shear force (WB) as kilograms. Piston head speed was fitted to 15 mm/s during the measurement, and it was initiated with 10 kg of contact power (Cavitt et al., 2005; Yalçin et al., 2010). Statistical Analyses GENETIC VARIABILITY OF MEAT QUALITY IN JAPANESE QUAIL Descriptive statistics and Kolmogorov-Smirnov normality tests of the traits were obtained using the UNI- VARIATE procedure of SAS software (SAS Institute, 2011). Because the normality was not held for the traits, they were transformed using Box-Cox transformation (Box and Cox, 1964), which resulted in normally distributed BRY, L*, and b* (Table 1). The nonparametric rank transformation (Aulchenko et al., 2007) was performed in R package (R Development Core Team, 2010) for the traits for which the Box-Cox transformation did not yield normally distributed traits. The analyses were performed by fitting the multitrait animal model, which can be written in matrix notation as y = Xβ + Zu + e, where y is a vector containing the phenotypic records of each trait for all animals, β is a vector of fixed effects, and u is a vector of random genetic effects. X and Z are known design matrices relating phenotypic records to β and u, respectively. Also, e is a vector of random errors. From these definitions, it is assumed that ( ) ( ) ( ) y ~ MVN Xβ, ZGZ + R I u ~ MVN 0, G A e ~ MVN 0, R I, where I is the identity matrix, A is the numerator relationship matrix, G is the additive genetic variance-covariance matrix, and R is the error variance-covariance matrix. For Bayesian analysis of the data, we assumed a noninformative prior for the fixed effects so that p ( β) constant. Also, the multivariate normal distribution assigned to u is viewed as prior distribution as well. The prior distribution assumed for G and R was also an inverted Wishart distribution: ( ) ( ) G v, V ~ IW v, V G G G G R v, V ~ IW v, V, R R R R and where v G, V G, v R, and V R are the parameters for the prior distributions (hyperparameters), and we used V G = V R = 0 and v G = v R = 10 in the analysis (Waldmann and Ericsson, 2006). Bayesian analyses were carried out using R package (R Development Core Team, 2010). A single sampling chain of 500,000 iterations was considered with a 50,000 cycles of burn-in and a thinning interval of 225 cycles to result 2,000 samples of parameters of interest in total. Genetic parameters, heritabilities, h 2 i, and genetic correlations, r gii ( ), were calculated from the posterior Table 1. Results of Kolmogorov-Smirnov normality test for slaughter and meat quality traits 1737 Trait 1 Original Box-Cox transformation Rank transformation BW 0.00 0.01 0.20 BRY 0.02 0.05 0.20 AFY 0.00 0.00 0.20 ph u 0.00 0.02 0.20 L* 0.01 0.31 0.20 a* 0.00 0.01 0.20 b* 0.02 0.11 0.20 TL 0.00 0.01 0.20 CL 0.02 0.04 0.20 WB 0.00 0.00 0.20 1 BW, g; BRY = breast yield, % of BW; AFY = abdominal fat yield, % of BW; ph U = ph at 24 h postmortem; L* = lightness; a* = redness; b* = yellowness; TL = thawing loss, %; CL = cooking loss, %; WB = Warner- Bratzler shear force, kg/cm 2.

1738 Narinc et al. means of variance and covariance parameters as follows: h 2 i = σ 2 σia 2 2 2 2 ia + σie ia ia σii a r = gii ( ) σ + σ, 2 where i and i represent the trait(s) of interest and σ ia and σ 2 ie are the diagonal elements of G and R matrices, respectively. In other words, the additive and error variance for the ith trait, respectively. Besides, σ ii a stands for the additive genetic covariance between the traits i and i. Basic Statistics RESULTS AND DISCUSSION The average BW at wk 5 was found to be 168.12 g (Table 2). This value is in good agreement with those reported by Toelle et al. (1991) and Sarı et al. (2011), and also higher than those presented by Aksit et al. (2003) and Oguz et al. (2004). Differences may occur among flocks in terms of BW for Japanese quail (Minvielle, 2004). The breast, which is economically important and the most valuable part of the carcass, was determined to be 27.45% of the BW (Table 2). In some studies in Japanese quail, the breast percentage was reported in the range of 25.75 to 27.21% (Aksit et al., 2003; Narinc et al., 2010b; Sarı et al., 2011). Percentage of abdominal fat (0.65%, Table 2) was found to be similar to those reported by Aksit et al. (2003) and Lotfi et al. (2011). The descriptive statistics of meat quality traits are presented in Table 2. Ultimate ph of breast meat was determined to be 5.94 on average. A similar value (5.92) was reported by some authors (Oguz et al., 2004; Gevrekci et al., 2009). On the other hand, some authors reported higher (6.17 and 6.00, respectively, Genchev et al., 2008 and 2010; and 6.38 by Karakaya et al., 2005) or lower (5.59 by Remignon et al., 1998) values of ph U Table 2. Descriptive statistics for slaughter and meat quality traits 1 in quail breast meat. According to one of the few studies in quail meat quality, the ph of meat declined rapidly within first 2 h following slaughter and leveled off after 4 h of aging in breast muscle as 5.8 to 5.9 (Singh and Verma, 1995). In general, broiler chicken meats with ph U between 5.7 and 6.1 are called normal and do not reveal any quality problems (Barbut, 1997; Zhang et al., 2005). The average ph determined in our study is coherent with the other findings in the literature for quail and broiler meat. The average L*, a*, and b* values of breast meat are 43.09, 19.24, and 7.74, respectively (Table 2). Oguz et al. (2004) and Gevrekci et al. (2009) reported the average L*, a*, and b* values of breast meat were 54.92, 9.70, and 5.59, and 54.87, 9.68, and 3.23, respectively. In another study about male quail, breast meat color parameters (L*, a*, and b*) were determined as 45.02, 5.47, and 12.66, respectively (Remignon et al., 1998). On the other hand, Imik et al. (2010) slaughtered the Japanese quail at 21 d of age to examine some antioxidant effects, and determined color parameters on the superficialis pectoralis major muscle as 40.07, 12.20, and 3.44, and 41.45, 12.02, and 5.63 in male and female control groups, respectively. In this research, the color parameters determined additionally on the deep of pectoralis major were 40.43, 13.40, and 3.39 in males and 39.15, 15.30, and 3.46 in females. Additionally, Riegel et al. (2004) measured those parameters as 38.9, 12.4, and 2.0 in male and 40.0, 10.9, and 2.5 in female quail s breast meat samples at 24 wk of age. The higher redness values determined in this study may be the fact that our measurements were obtained from the bottom side of the pectoralis major muscle to reduce the deviations because of high scalding temperature (Fletcher et al., 2000). According to the studies carried out on broiler chicken meat quality, ideal L* should be between 46 and 53 (Barbut, 1997; Zhang and Barbut, 2005), and meats with an L* value below 46 are called to be dark, firm, dry, which means they have a dark color, high waterholding capacity, and short shelf life. Previous litera- Item Mean SD CV (%) Minimum Maximum Slaughter trait BW, g 168.12 19.96 11.87 103.40 260.60 BRY, % 27.45 1.91 6.97 21.02 32.43 AFY, % 0.65 0.40 62.31 0.04 2.57 Meat quality trait ph U 5.94 0.17 2.89 5.30 6.58 L* 43.09 2.41 5.58 35.89 52.34 a* 19.24 1.92 10.00 10.04 23.89 b* 7.74 1.52 19.65 3.32 12.86 TL, % 9.09 3.64 40.06 1.40 29.48 CL, % 24.02 2.14 8.89 13.74 34.23 WB, kg 7.75 2.29 29.57 4.06 15.97 1 BRY = breast yield, % of BW; AFY = abdominal fat yield, % of BW; ph U = ph at 24 h postmortem; L* = lightness; a* = redness; b* = yellowness; TL = thawing loss, %; CL = cooking loss, %; WB = Warner-Bratzler shear force, kg/cm 2.

GENETIC VARIABILITY OF MEAT QUALITY IN JAPANESE QUAIL ture showed that the a* value of broiler chicken breast meat ranges between 0.96 and 4.50, and b* values were in the range of 6.7 to 13.5 (Le Bihan-Duval et al., 1999, 2001, 2008; Fletcher et al., 2000; Berri et al., 2001). It was also reported that the selection for meat yield results in a decrease in a* of meat in chickens (Berri et al., 2001), turkeys (Sante et al., 1991), and ducks (Baeza et al., 1997). High a* values (11 and 7.5) were determined on the breast meat of native chickens (Yue et al., 2010; Jiang et al., 2011). On the other hand, Smith et al. (1993) stated that redness value was higher for ducklings than chickens. Some researchers (Kisiel and Ksiazkiewicz, 2004; Ali et al., 2008; Haraf et al., 2009) reported that rather high a* values for duck breast meat range between 14.0 and 17.8. In parallel, a* value of geese pectoralis measured as about 17 and 20 by Gumulka et al. (2009) and Yakan et al. (2012), respectively. On the other hand, Yousefi et al. (2012) reported that a* parameters as between 14.26 and 16.45 in different sheep breeds. Furthermore, a* values of beef muscle ranged between 15.8 and 25.2 (Girolami et al., 2013). Consequently, one can conclude that the quail meat resembles both waterfowl and red meat in terms of color parameters, particularly the redness. From Table 2, it can be seen that the average TL after 4 wk of storage in breast meat samples is 9.09%. In broiler chickens, TL was determined as 7.47% at 0 C thawing temperature, but this loss was considerably higher than at +18 C (Yu et al., 2005). In our study, the meat samples were thawed at +4 C. Furthermore, breast meat CL was found to be 24.02% (Table 2). Karakaya et al. (2005) applied a similar cooking procedure and determined the CL of quail meat as 27.9%. On the contrary, Le Bihan-Duval et al. (2008), in broiler chickens, reported a very low value (14.6%) for the total of TL and CL. The WB shear value for breast meat samples was obtained as 7.75 kg on average (Table 2). A report on WB shear force in quail breast meat was not encountered. In a heavy commercial line of broilers, Le Bihan- Duval et al. (2008) reported the average breast meat shear force as 14.5 N (~1.48 kg), which is considerably lower than our finding. On the other hand, Yousefi et al. (2012) reported the WB shear value of sheep meat as 12 kg. Thus, it can be concluded that the toughness of quail meat is considerably higher than that of the broiler meat, and may be closer to red meat. Heritability Estimates Summary statistics for the posterior distributions of heritability estimates of slaughter and meat quality traits are presented in Table 3 along with their posterior densities in Figures 1, 2, and 3. In Bayesian approach, frequentist CI are replaced by Bayesian credible intervals (BCI). The interpretation of a 95% BCI is that the probability that the parameter falls into the given interval is 0.05. Also, the highest probability density interval (HPD), the shortest possible interval enclosing 95% of the posterior mass, is the choice if the posterior distribution is an asymptotic one (Waldmann and Ericsson, 2006). Both BCI and HPD of the heritabilities in Table 3 are almost identical and indicate the same interval for the parameters of interest. Heritability of BW at wk 5 was estimated to be 0.51. Also, similar to our findings, many researchers reported high heritability estimates for BW in Japanese quail (Toelle et al., 1991; Aksit et al., 2003; Narinc et al., 2010a; Sarı et al., 2011). Similarly, heritability estimate (0.49, Table 3) for BRY was found to be high. However, many researchers reported low heritability estimates (0.15 0.19) for BRY in quail (Vali et al., 2005; Narinc et al., 2010b; Lotfi et al., 2011). Parallel to our finding, heritability of BRY was reported as 0.35 by Oguz et al. (2004). On the other hand, heritability of BRY was estimated to be high (0.53 and 0.55) in broilers by Le Bihan-Duval et al. (1998, 2001), and 0.32 in turkeys by Le Bihan Duval et al. (2003). Estimated heritability for AFY (0.35) is moderate (Table 3). In other studies involving quail, moderate heritabilities (0.23 0.29) were also reported for the trait (Aksit et al., 2003; Narinc et al., 2010b; Lotfi et al., 2011). However, a rather higher heritability (0.63 0.84) for AFY was reported in chickens by Le Bihan Duval et al. (1998, 1999, 2001, 2008). Table 3. Posterior expectations, SD, credible intervals, and highest posterior density intervals of the heritabilities 1 Item Mean SD Median Mode BCI 2.5 BCI 97.5 HPDI 2.5 HPDI 97.5 1739 Slaughter trait BW 0.51 0.06 0.52 0.51 0.39 0.64 0.40 0.64 BRY 0.49 0.06 0.48 0.49 0.38 0.62 0.38 0.62 AFY 0.35 0.06 0.32 0.35 0.25 0.47 0.25 0.47 Meat quality trait ph U 0.64 0.05 0.62 0.64 0.54 0.73 0.54 0.73 L* 0.43 0.06 0.43 0.43 0.31 0.56 0.31 0.56 a* 0.45 0.06 0.43 0.45 0.33 0.58 0.32 0.57 b* 0.45 0.07 0.45 0.45 0.33 0.58 0.33 0.58 TL 0.39 0.06 0.40 0.39 0.28 0.51 0.28 0.50 CL 0.40 0.06 0.41 0.40 0.29 0.52 0.29 0.52 WB 0.48 0.06 0.45 0.48 0.37 0.59 0.37 0.59 1 BW, g; BRY = breast yield, % of BW; AFY = abdominal fat yield, % of BW; ph U = ph at 24 h postmortem; L* = lightness; a* = redness; b* = yellowness; TL = thawing loss, %; CL = cooking loss, %; WB = Warner-Bratzler shear force, kg/cm 2 ; BCI = Bayesian credible interval (2.5%, lower bound; 97.5%, upper bound); HPDI = highest posterior density interval (2.5%, lower bound; 97.5%, upper bound).

1740 Narinc et al. Figure 1. Posterior distributions of heritability of slaughter traits. BRY = breast yield; AFY = abdominal fat yield. According to our findings, ph U is the highest heritable meat characteristic (0.64; Table 3). Oguz et al. (2004) also reported a high estimation (0.48), whereas Gevrekci et al. (2009) determined a moderate heritability (0.24) with the REML method for ph U. The trait is also considered to be highly heritable in chicken due to the estimates ranging between 0.34 and 049 (Le Bihan-Duval et al., 1999, 2001, 2008), whereas rather low heritability estimates (0.16) were reported by Le Bihan-Duval et al. (2003) in turkey. As seen in Table 3, the estimated heritabilities of breast meat color characteristics (L*, a*, and b*) were 0.43, 0.45, and 0.45. These estimates have been reported as 0.23, 0.45, and 0.22 by Oguz et al. (2004), and 0.24, 0.35, and 0.15 by Gevrekci et al. (2009). According to Le Bihan Duval et al. (1999, 2001, 2008), breast meat color were significantly heritable, with heritability values ranging from 0.25 to 0.57 in broiler chickens. The TL, CL, and WB shear values were also highly heritable, and their heritability estimates were 0.39, 0.40, and 0.48 (Table 3). Heritability values of drip loss for raw broiler chicken meat were estimated as 0.39 and 0.26 by Le Bihan-Duval et al. (2001, 2008). In another study, Le Bihan-Duval et al. (2008) reported the heritabilities of thawing-cooking loss and WB shear force as 0.35 and 0.34. Genetic and Phenotypic Relationships As seen in Table 4, phenotypic and genetic correlations between BW and BRY are estimated to be 0.28 and 0.32, respectively. Oguz et al. (2004) also reported a positive phenotypic correlation between these traits (0.26). Vali et al. (2005) estimated the genetic correlation between BW and BRY in quail as 0.22. It is reported that there are positive genetic correlations (0.16 and 0.17) between these 2 characteristics of broiler chicken (Le Bihan-Duval et al., 1999, 2001) and also more strong genetic association between these characters in turkey as 0.25 (Le Bihan-Duval et al., 2003). In addition, a higher positive genetic correlation (0.65) was observed between BW at 42 d of age and breast muscle percentage in Japanese quail (Lotfi et al., 2011). Caron et al. (1990), who investigated the effect of mass selection for BW in Japanese quail, concluded that the selected lines with the highest BW were more fatty than the selected line for lower BW. Similarly, we estimated a high and positive genetic correlation (0.58) between BW and AFY (Table 4). However, Lotfi et al. (2011) estimated a lower genetic correlation (0.21). According to Le Bihan-Duval et al. (1999, 2001), genetic correlation between BW and AFY was only 0.19 in broilers. It can clearly be seen from Table 4 that the Figure 2. Posterior distributions of heritability of ultimate ph (ph U ) of breast meat and color parameters (L* = lightness; a* = redness; b* = yellowness).

GENETIC VARIABILITY OF MEAT QUALITY IN JAPANESE QUAIL 1741 Figure 3. Posterior distributions of heritability of water-holding capacity and shear force. TL = thawing loss; CL = cooking loss; WB = Warner-Bratzler. genetic correlation between BRY and AFY is 0.24. Narinc et al. (2010b) estimated the genetic correlation between 2 characteristics in quail as 0.34, and Le Bihan-Duval et al. (1999, 2001) reported the genetic correlations as 0.20 and 0.17 in broilers. It is well known that there is a very strong negative genetic relationship between ph U and L* ( 0.91 and 0.65) of breast meat in chickens (Le Bihan-Duval et al., 2001, 2008) and ( 0.53) turkeys (Le Bihan-Duval et al., 2003). The genetic relationship ( 0.16) determined between ph U and L* in our study was also negative and low (Table 4). Oguz et al. (2004) reported a negative phenotypic correlation ( 0.26) between ph U and L* in quail. Le Bihan-Duval et al. (2001) reported that the drip loss of raw meat, a measure of water-holding capacity, was highly genetically correlated with ph U ( 0.83) and also with L* (0.80). Increasing ph U (or decreasing L*) should contribute to the improvement of the waterholding capacity of chicken breast meat. A remarkable and negative genetic correlation ( 0.43) was estimated between TL and ph U, whereas the estimate of genetic correlation between TL with L* was inconsistently low (0.17; Table 4). In addition, contrary to the high genetic relationship ( 0.62) observed between ph U and WB value, a very low estimate (0.04) was obtained for L*- WB (Table 4). Le Bihan-Duval et al. (2008) reported a high and negative genetic correlation between ph U and WB shear force ( 0.81). Our results suggest that the ph U of quail meat is more highly associated with meat quality than with L* values, in a manner different in chicken. The color of the meat is related to ph U of the muscle (Fletcher et al., 2000), but it cannot be ignored that the iron content has been highly related to a* and L* of breast meat in broiler (Boulianne and King, 1998). Thus, Berri et al. (2001) reported that chickens selected for high BW and BRY showed higher L* and less a* breast meat than control lines. The authors explained this by the decrease in the heme pigment content in selected ones. Quail, which has not been selected extensively, showed a high a* value, probably due to the high heme pigment that may cause a low relationship between L* and meat quality properties. Considering the meat color, particularly the a* and L*, and the relationship between L* and ph U or waterholding capacity, it can be concluded that the quail meat is quite different from chicken and also turkey meat. For that reason, it seems to be difficult to benefit from the huge scientific literature about meat quality of chicken and turkey one-to-one. We believe that further Table 4. The genetic correlation estimates (below diagonal) and phenotypic correlations (above diagonal) for slaughter and meat quality traits 1 Item BW BRY AFY ph U L* a* b* TL CL WB BW 0.28* 0.44* 0.26* 0.11* 0.06 0.05 0.02 0.19* 0.11* BRY 0.32* 0.15* 0.02 0.06 0.03 0.01 0.04 0.22* 0.04 AFY 0.58* 0.24* 0.40* 0.19* 0.18* 0.02 0.14* 0.02 0.04 ph U 0.28* 0.08 0.41* 0.14* 0.22* 0.09 0.24* 0.19* 0.43* L* 0.19* 0.15* 0.26* 0.16* 0.11* 0.35* 0.12* 0.04 0.06* a* 0.17* 0.17* 0.20* 0.33* 0.15 0.49* 0.08* 0.13* 0.11* b* 0.06 0.07 0.08 0.18* 0.40* 0.54* 0.04 0.15* 0.03 TL 0.07 0.01 0.26* 0.43* 0.17* 0.10 0.14 0.02 0.12* CL 0.27* 0.27* 0.10 0.05 0.24* 0.20* 0.25* 0.05 0.21* WB 0.14 0.11 0.01 0.62* 0.04 0.15 0.01 0.21* 0.23* 1 BRY = breast yield, % of BW; AFY = abdominal fat yield, % of BW; ph U = ph at 24 h postmortem; L* = lightness; a* = redness; b* = yellowness; TL = thawing loss, %; CL = cooking loss, %; WB = Warner-Bratzler shear force, kg. *Correlation is statistically significant (P < 0.05).

1742 Narinc et al. scientific study is primarily necessary about the conversion of muscle to meat, the amount of decline in postmortem ph and their relationships between the factors to deal with the preslaughter and slaughter phases in quail. Heritability estimates for BW and BRY were high, whereas the estimated heritability for AFY was moderate. These findings together denote that the improvement in these characteristics is feasible through genetic selection, similar to many studies presented for quail, chicken, and turkey. In addition, the high genetic correlations observed between BW and BRY or AFY are higher than the values reported for chickens and turkeys. These high estimations indicate that the selection for BW will improve the breast percentage but also increase the fat pad yield. Moderate negative relationship between BRY and AFY implies that selecting for high breast yield should not increase the fatness of the bird, at least of the abdominal pad, in line with the reports for chicken (Le Bihan-Duval et al., 1998, 1999). According to our findings, the most heritable meat quality trait is ph U (0.64), whereas the others also have high heritabilities. Selection can, therefore, be used to improve the meat quality in quail and other poultry species. A remarkable result of this study is the estimated low genetic correlation between ph U and L* of breast meat, contrary to the chickens and turkeys. The L* value has positive relationships with BW, BRY, and AFY (0.19, 0.15, and 0.26), whereas ph U exhibited negative but high correlations with BW and AFY, except BRY. The selection for growth in quail can decrease the ph of the meat and can also slowly modify its color by increasing the L* and a* values. Many researchers have concluded that selection for rapid growth resulted in a higher L* but a lower a* in chicken breast meat (Le Bihan-Duval et al., 1999; Berri et al., 2001). This controversy between quail and chicken for the effect of selection on the redness of breast meat may be due to the heme pigment contents of the pectoralis major muscle of these species. It is well known that ph U and L* are strongly linked to and correlated with drip loss of the raw chicken meat. According to our results, TL showed a higher relationship with ph than L*. However, CL was found to be related with L* but not with ph U. On the other hand, an important indicator of texture, WB, is highly correlated with ph U, whereas its relation with L* is low. This study showed that the breast meat of quail has a fairly high WB value compared with chickens, denoting its relative firmness. Despite this difference, there are similarities due to the negative and high correlation between ph and WB in chickens (Le Bihan-Duval et al., 2008). Therefore, one can conclude that the selection for high ph U can lead to softening of quail meat. Lotfi et al. (2011) concluded that the quality of breast meat in Japanese quail was higher compared with broilers, due to the higher intramuscular fat content. In addition, their results indicated that the intramuscular fat is a heritable trait and selection for increased BW and decreased abdominal fat will improve breast meat quality. This study showed that the major contributing factors to meat quality were heritable in quail, and no genetic conflict was detected between meat quality and quantity. In addition, our results exhibit that the ph U of quail meat is also a relevant selection criterion because of its strong relationship with either meat quality traits such as water-holding capacity and texture or leanness. Further research is needed to define the optimum breeding strategy to improve meat quality as a result of specific differences in quail species. ACKNOWLEDGMENTS We thank the Scientific and Technological Research Council of Turkey (TUBITAK) for the financial support of this study with the project number of 111O413. This research with the project number of 2011.03.0121.005 is part of the first author s PhD thesis, financially supported by Akdeniz University Scientific Research Coordination Unit (Turkey). REFERENCES Aksit, M., I. Oguz, Y. Akbas, Y. Altan, and M. Ozdogan. 2003. Genetic variation of feed traits and relationships to some meat production traits in Japanese quail (Coturnix coturnix japonica). Arch. Geflugelkd. 67:76 82. Ali, M. S., H. S. Yang, J. Y. Jeong, S. H. Moon, Y. H. Hwang, G. B. Park, and S. T. Joo. 2008. Effect of chilling temperature of carcass on breast meat quality of duck. Poult. Sci. 87:1860 1867. Anthony, N. B., K. E. Nestor, and W. L. Bacon. 1986. Growth curves of Japanese quail as modified by divergent selection for 4-week body weight. Poult. Sci. 65:1825 1833. Aulchenko, Y. S., S. Ripke, A. Isaacs, and C. M. van Duijn. 2007. GenABEL: An R package for genome-wide association analysis. Bioinformatics 23:1294 1296. Baeza, E., H. De Carville, M. R. Marche, and B. Leclercq. 1997. Effects of selection, over three and four generations, on meat yield and fatness in Muscovy ducks. Br. Poult. Sci. 38:359 365. Barbut, S. 1997. Problem of pale soft exudative meat in broiler chickens. Br. Poult. Sci. 38:355 358. Berri, C., N. Wacrenier, N. Millet, and E. Le Bihan-Duval. 2001. Effect of selection for improved body composition on muscle and meat characteristics of broilers from experimental and commercial lines. Poult. Sci. 80:833 838. Boulianne, M., and A. J. King. 1998. Meat color and biochemical characteristics of unacceptable dark colored broiler chicken carcasses. J. Food Sci. 63:759 762. Box, G. E. P., and D. R. Cox. 1964. An analysis of transformations. J. R. Stat. Soc., B 26:211 252. Caron, N., F. Minvielle, M. Desmarais, and L. M. Poste. 1990. Mass selection for 45-day body weight in Japanese quail: Selection response, carcass composition, cooking properties, and sensory characteristics. Poult. Sci. 69:1037 1045. Cavitt, L. C., J. F. Meullenet, R. K. Gandhapuneni, G. W. Youm, and C. M. Owens. 2005. Rigor development and meat quality of large and small broilers and the use of Allo-Kramer shear, needle puncture, and Razor Blade shear to measure texture. Poult. Sci. 84:113 118. Duclos, M. J., C. Berri, and E. Le Bihan-Duval. 2007. Muscle growth and meat quality. J. Appl. Poult. Res. 16:107 112.

GENETIC VARIABILITY OF MEAT QUALITY IN JAPANESE QUAIL 1743 Fletcher, D. L., M. Qia, and D. P. Smith. 2000. The relationship of raw broiler breast meat color and ph to cooked meat color and ph. Poult. Sci. 79:784 788. Genchev, A., R. Mihaylov, S. Ribarski, A. Pavlov, and M. Kabakchiev. 2008. Slaughter analysis protocol in experiments using Japanese quails (Coturnix japonica). Trakia J. Sci. 6:66 71. Genchev, A., S. Ribarski, and G. Zhelyazkov. 2010. Physicochemical and technological properties of Japanese quail meat. Trakia J. Sci. 8:86 94. Gevrekci, Y., I. Oguz, M. Aksit, A. Onenc, D. Ozdemir, and O. Altan. 2009. Heritability and variance component estimates of meat quality in Japanese quail (Coturnix coturnix japonica). Turk. J. Vet. Anim. Sci. 33:89 94. Girolami, A., F. Napolitano, D. Faraone, and A. Braghieri. 2013. Measurement of meat color using a computer vision system. Meat Sci. 93:111 118. Gumulka, M., D. Wojtysiak, E. Kapkowska, K. Poltowicz, and A. Rabsztyn. 2009. Microstructure and technological meat quality of geese from conservation flock and commercial hybrids. Ann. Anim. Sci. 9:205 213. Haraf, G., J. Ksiazkiewicz, J. Woloszyn, and A. Okruszek. 2009. Characteristic of meat color of different duck populations. Arch. Tierzucht. 52:527 537. Imik, H., M. A. Atasever, M. Koc, M. A. Atasever, and K. Ozturan. 2010. Effect of dietary supplementation of some antioxidants on growth performance, carcass composition and breast meat characteristics in quails reared under heat stress. Czech J. Anim. Sci. 55:209 220. Jiang, R. R., G. P. Zhao, J. L. Chen, M. Q. Zheng, M. Q. Zhao, P. Li, J. Hu, and J. Wen. 2011. Effect of dietary supplemental nicotinic acid on growth performance, carcass characteristics and meat quality in three genotypes of chicken. J. Anim. Physiol. Anim. Nutr. (Berl.) 95:137 145. Karakaya, M., C. Saricoban, and M. T. Yilmaz. 2005. The effect of various types of poultry pre- and post-rigor meats on emulsification capacity, water-holding capacity and cooking loss. Eur. Food Res. Technol. 220:283 286. Khaldari, M., A. Pakdel, H. Mehrabani Yeganeh, J. A. Nejati, and P. Berg. 2010. Response to selection and genetic parameters of body and carcass weights in Japanese quail selected for 4-week body weight. Poult. Sci. 89:1834 1841. Kisiel, T., and J. M. Ksiazkiewicz. 2004. Comparison of physical and qualitative traits of meat of two Polish conservative flocks of ducks. Arch. Tierz. Dummerstorf 47:367 375. Le Bihan-Duval, E. 2004. Genetic variability within and between breeds of poultry technological meat quality. World s Poult. Sci. J. 60:331 340. Le Bihan-Duval, E., C. Berri, E. Baeza, N. Millet, and C. Beaumont. 2001. Estimation of the genetic parameters of meat characteristics and of their genetic correlations with growth and body composition in an experimental broiler line. Poult. Sci. 80:839 843. Le Bihan-Duval, E., C. Berri, E. Baeza, V. Sante, T. Astruc, H. Remignon, G. Le Pottier, J. Bentley, C. Beaumont, and X. Fernandez. 2003. Genetic parameters of meat technological quality traits in a grand-parental commercial line of turkey. Genet. Sel. Evol. 35:623 635. Le Bihan-Duval, E., M. Debut, C. M. Berri, N. Sellier, V. Santé- Lhoutellier, Y. Jégo, and C. Beaumont. 2008. Chicken meat quality: Genetic variability and relationship with growth and muscle characteristics. BMC Genet. 9:53. Le Bihan-Duval, E., S. Mignon-Grasteau, N. Millet, and C. Beaumont. 1998. Genetic analysis of a selection experiment on increased body weight and breast muscle weight as well as on limited abdominal fat weight. Br. Poult. Sci. 39:346 353. Le Bihan-Duval, E., N. Millet, and H. Remignon. 1999. Broiler meat quality: Effect of selection for increased carcass quality and estimates of genetic parameters. Poult. Sci. 78:822 826. Lee, Y. S., A. Saha, R. Xiong, C. M. Owens, and J. F. Meullenet. 2008. Changes in broiler breat fillets tenderness, water-holding capacity, and color attributes during long-term frozen storage. Food Engineering and Physical Properties 73:162 168. Lotfi, E., S. Zerehdaran, and M. Ahani Azari. 2011. Genetic evaluation of carcass composition and fat deposition in Japanese quail. Poult. Sci. 90:2202 2208. Marks, H. L. 1996. Long-term selection for body weight in Japanese quail under different environments. Poult. Sci. 75:1198 1203. Minvielle, F. 2004. The future of Japanese quail for research and production. World s Poult. Sci. J. 60:500 507. Monnin, G. 1998. Recent methods for predicting quality of whole meat. Meat Sci. 49:231 243. Narinc, D., T. Aksoy, and E. Karaman. 2010a. Genetic parameters of growth curve parameters and weekly body weights in Japanese quail. J. Anim. Vet. Adv. 9:501 507. Narinc, D., E. Karaman, and T. Aksoy. 2010b. Estimation of genetic parameters for carcass traits in Japanese quail using Bayesian methods. S. Afr. J. Anim. Sci. 40:342 347. Northcutt, J. K., R. J. Buhr, L. L. Young, C. E. Lyon, and G. O. Ware. 2001. Influence of age and postchill carcass aging duration on chicken breast fillet quality. Poult. Sci. 80:808 812. Oguz, I., M. Aksit, A. Onenc, Y. Gevrekci, D. Ozdemir, and O. Altan. 2004. genetic variability of meat quality characteristics in Japanese quail (Coturnix coturnix japonica). Arch. Geflügelk. 68:176 181. R Development Core Team. 2010. R: A language and environment for statistical computing, reference index version 2.12.1. R Foundation for Statistical Computing, Vienna, Austria. http:// www.r-project.org. Remignon, H., A. D. Mills, D. Guemene, V. Desrosiers, M. Garreau-Mills, M. Marche, and G. Marche. 1998. Meat quality traits and muscle parameters in high and low fear lines of Japanese quail Coturnix japonica subject to acute stress. Br. Poult. Sci. 39:372 378. Riegel, J., S. Maak, K. P. Behr, and M. Wicke. 2004. Investigations on meat quality of the Pectoralis superficialis in turkey depending on line and age. XXII. World s Poultry Congress, Istanbul. Sante, V., G. Bielicki, M. Renerre, and A. Lacourt. 1991. Postmortem evolution in the Pectoralis superficialis muscle from two turkey breeds: Relationship between ph and colour changes. Proceedings 37th International Congress of Meat Science and Technology, Kulmbach, Germany, vol. 1:465 468. Sarı, M., M. Tilki, and M. Saatci. 2011. Genetic parameters of slaughter and carcase traits in Japanese quail (Coturnix coturnix japonica). Br. Poult. Sci. 52:169 172. SAS Institute. 2011. SAS/STAT User s Guide. Version 9.2 ed. SAS Institute Inc., Cary, NC. Singh, R. P., and S. S. Verma. 1995. Effect of hot and cold deboning on the yield and meat quality of quail meat. J. Food Sci. Tech. 32:233 235. Smith, D. P., D. L. Fletcher, R. J. Buhr, and R. S. Beyer. 1993. Pekin duckling and broiler chicken pectoralis-muscle structure and composition. Poult. Sci. 72:202 208. Swatland, H. J. 1985. Development of rigor mortis in intact sides of pork measured with a portable rigorometer. J. Anim. Sci. 61:882 886. Toelle, V. D., G. B. Havenstein, K. E. Nestor, and W. R. Harvey. 1991. Genetic and phenotypic relationship in Japanese quail. Poult. Sci. 70:1679 1688. Tserveni-Gousi, A. S., A. B. M. Raj, and M. O Callaghan. 1999. Evaluation of stunning/killing methods for quail (Coturnix japonica): Bird welfare and carcase quality. Br. Poult. Sci. 40:35 39. Vali, N., M. A. Edriss, and H. R. Rahmani. 2005. Genetic parameters of body and some carcass trait in two quail strains. Int. J. Poult. Sci. 4:296 300. Varkoohi, S., M. M. S. Babak, A. Pakdel, A. N. Javaremi, M. Zaghari, and A. Kause. 2010. Response to selection for feed conversion ratio in Japanese quail. Poult. Sci. 89:1590 1598. Waldmann, P., and T. Ericsson. 2006. Comparison of REML and Gibbs sampling estimates of multi-trait genetic parameters in Scots pine. Theor. Appl. Genet. 112:1441 1451. Yakan, A., D. Aksu Elmalı, M. Elmalı, T. Şahin, S. Motor, and Y. Can. 2012. Carcass and meat quality characteristics of white and multicolor geese under local breeder conditions. Kafkas Univ. Vet. Fak. Derg. 18:663 670. Yalçin, S., H. Ozkul, S. Ozkan, R. Gous, I. Yasa, and E. Babacanoglu. 2010. Effect of dietary protein regime on meat quality traits and carcase nutrient content of broilers from two commercial genotypes. Br. Poult. Sci. 51:621 628.

1744 Narinc et al. Yousefi, A. R., H. Kohram, A. Zare-Shahneh, A. Nik-khah, and A. W. Campbell. 2012. Comparison of the meat quality and fatty acid composition of traditional fat-tailed (Chall) and tailed (Zel) Iranian sheep breeds. Meat Sci. 92:417 422. Yu, L. H., E. S. Lee, J. Y. Jeong, H. D. Paik, J. H. Choi, and C. J. Kim. 2005. Effects of thawing temperature on the physicochemical properties of pre-rigor frozen chicken breast and leg muscles. Meat Sci. 71:375 382. Yue, H. Y., L. Zhang, S. G. Wu, L. Xu, H. J. Zhang, and G. H. Qi. 2010. Effect of transport stress on blood metabolism, glycolytic potential, and meat quality in nest-type yellow-feathered chickens. Poult. Sci. 89:413 419. Zhang, A. W., B. D. Lee, S. K. Lee, K. W. Lee, G. H. An, K. B. Song, and C. H. Lee. 2005. Effects of yeast (Saccharomyces cerevisiae) cell components on growth performance, meat quality, and ileal mucosa development of broiler chicks. Poult. Sci. 84:1015 1021. Zhang, L., and S. Barbut. 2005. Rheological characteristics of fresh and frozen PSE, normal and DFD chicken breast meat. Br. Poult. Sci. 46:687 693.