Introduction
Turkey production is both an important and profitable agricultural industry and the investigation of factors that affect profitability is warranted, especially for a consumer-valued product such as turkey breast meat. Increasing the proportion of breast meat contributes to higher yields from the carcass and increases overall profitability as breast meat has the highest economic value relative to other carcass components and makes a large contribution to the gross margin. Consequently, breeding and management practices that optimise this trait should be identified and implemented. Sex, strain, and selection pressure affect final carcass yields. This inherited genetic potential interacts with environmental factors including nutrition, light, and temperature to determine the proportion of breast meat on the carcass. Breast meat accretion is influenced at all stages of production, including breeder, hatchery, and grow-out operations. This necessitates careful planning of management practices throughout all segments of the industry in order for a turkey to fulfil its full genetic potential. As a result, all segments of the turkey industry must be conscious of the impact their management decisions can have on the final breast meat yield.
Defining breast meat yield
Breast meat yield is most commonly defined as the proportion of breast meat relative to the weight of the processed carcass or as the weight of the breast relative to slaughter weight. The M. pectoralis superficialis (fillet) and the M. pectoralis profundus (tender) are the contributing muscles to breast meat and are considered in these definitions. However, the method of carcass dissection and muscle isolation is variable between processing plants and BMY analysis is often only relevant when comparing measurements taken at the same location. As a result, it would be beneficial to have a standard procedure for breast meat separation. This would enable a straight-forward comparison between carcass yield studies based on the evaluation of equivalent cuts. To this end, a review was published to illustrate methods of turkey carcass dissection (Hahn and Spindler, 2002). A regulated dissection procedure would ensure that the weight of the two breast muscles and carcass weight, which are required to calculate BMY, are comparable across studies.
Allometric growth
The relative body composition of a turkey changes throughout the growing phase because the body components do not increase in size at a uniform rate (Peng et al., Reference PENG, ADAMS, FURUMOTO, HESTER, LARSEN, PIKE and STADELMAN1985; Brenoe and Kolstad, 2000). This allometric growth results in a disproportionate increase in the size of the breast at later stages of the growth trajectory. The observed increase in the proportion of breast meat is primarily due to an accelerated increase in the depth of the breast, as the relative length and width remain fairly constant with increasing body size (Swatland, Reference SWATLAND1979, Reference SWATLAND1989b). M. pectoralis superficialis growth is primarily responsible for the relationship between breast and body size, as this muscle has a stronger and more consistent relationship with both body weight and age across strains and sexes (Barbour and Lilburn, 1995; Brake et al., Reference BRAKE, HAVENSTEIN, FERKET, RIVES and GIESBRECHT1995). A positive linear correlation between BMY and body weight reflects these phenotypic observations (Summers et al., Reference SUMMERS, JACKSON and SPRATT1989; Brake et al., Reference BRAKE, HAVENSTEIN, FERKET, RIVES and GIESBRECHT1995).
Similar to allometric growth between other body compartments, the various muscles within the breast grow at different rates. The proportion of the M. pectoralis superficialis is increased in growth selected lines (Wilson et al., Reference WILSON, NIEBERG, BUHR, KELLY and SHULTZ1990; Lilburn and Nestor, 1991). This suggests that selection to increase body size has a stronger impact on the growth rate of the M. pectoralis superficialis relative to the M. pectoralis profundus. The allometric growth of the turkey, therefore, results in unequal expansion of the breast relative to other body components and growth rates are also variable between the breast muscles. Consequently, the overall growth characteristics result in a linear increase in BMY as body size increases.
Muscle development
As a turkey's muscles develop, their increase in size can be attributed to an increase in both the number (hyperplasia) and the size (hypertrophy) of the muscle fibres. The relative influence of these two factors changes between the growing phases with hyperplasic and hypertrophic growth predominating pre- and post-hatch, respectively. The significance of post-hatch hypertrophy is indicated by the increase in protein and DNA content of the muscle during the growing phase (Kang et al., Reference KANG, SUNDE and SWICK1985; Swatland, Reference SWATLAND1989b; Mozdziak et al., Reference MOZDZIAK, SCHULTZ and CASSENS1994; Velleman, Reference VELLEMAN2007). Muscle development is consequently not a static process and the factors controlling breast growth shift throughout development from early hyperplasia to later hypertrophy.
The early stage of post-hatch hypertrophy is characterized by high satellite cell mitotic activity and a high rate of protein deposition, and this initial phase is followed by an increase in the cytoplasm to nucleus ratio of the fibres (Kang et al., Reference KANG, SUNDE and SWICK1985; Mozdziak et al., Reference MOZDZIAK, SCHULTZ and CASSENS1994; Moore et al., Reference MOORE, FERKET and MOZDZIAK2005). This pattern indicates that hypertrophy occurs initially by contributing new genetic material to the muscle fibres, and these new nuclei enable the expansion of muscle fibre size. The initial supply of new DNA is critical, and restricting satellite cell proliferation can decrease a muscle's capacity for growth, which can reduce the size of the mature muscles (Mozdziak et al., Reference MOZDZIAK, SCHULTZ and CASSENS1997, Reference MOZDZIAK, PULVERMACHER and SCHULTZ2000). The outcome of the hypertrophic growth is an increase in fibre width and in the size of the extracellular space, while decreasing the fibre density as the bird ages (Velleman et al., Reference VELLEMAN, COY, ANDERSON, PATTERSON and NESTOR2003b). It is evident that hypertrophic growth is a dynamic process and new genetic material must first be generated to provide the DNA required for the fibres to expand in size.
The muscle growth processes interact differently with the growth trajectories of each sex (Shaklee et al., Reference SHAKLEE, KNOX and MARSDEN1952; Chapuis et al., Reference CHAPUIS, TIXIER-BOICHARD, DELABROSSE and DUCROCQ1996). The linear relationship between BMY and body weight varies, and this is demonstrated by the different intercept and regression coefficient terms for toms and hens (Brake et al., Reference BRAKE, HAVENSTEIN, FERKET, RIVES and GIESBRECHT1995). These developmental differences are apparent physiologically where toms show an increased fibre diameter, increased number of muscle fibres, and increased rate of satellite cell differentiation compared to hens (Swatland, Reference SWATLAND1989a; Velleman et al., Reference VELLEMAN, XIAOSONG, NESTOR and MCFARLAND2000). Cumulatively, these studies indicate that male and female birds have different growth physiology related to both hypertrophy and hyperplasia.
Inheritance
Additive genetic factors affect BMY as a trait independent of the relationship between absolute breast weight and body size (Velleman et al., Reference VELLEMAN, COY, ANDERSON, PATTERSON and NESTOR2003b; Velleman and Nestor, Reference VELLEMAN and NESTOR2004). There are limited heritability estimates in the literature, but the few there are display moderate to high heritabilities (BMY h2 = 0.32, breast width h2 = 0.30 (Nestor et al., Reference NESTOR, BACON, HAVENSTEIN, SAIF and RENNER1988; Le Bihan-Duval et al., Reference LE BIHAN-DUVAL, BERRI, BAÉZA, SANTÉ, ASTRUC, RÉMIGNON, POTTIER, BENTLEY, BEAUMONT and FERNANDEZ2003)). This would indicate that selection based on BMY would result in relatively rapid genetic progress given a breeding objective developed with yield as an important component.
The patterns of inheritance and impact of selection on BMY have been studied by comparing lines that have been developed with different selection emphases on BMY. This has been done by contrasting experimental strains, developed by selecting for body weight alone, to commercial lines which are characteristically selected for both growth rate and BMY (Velleman et al., Reference VELLEMAN, COY, ANDERSON, PATTERSON and NESTOR2003b; Velleman and Nestor, 2004). Differences in BMY between lines can consequently be used to determine the impact of selection emphases on characteristics of the breast muscles, and to provide an indication of the level of genetic gain that can be achieved by including BMY in a breeding objective.
Phenotypic variation in BMY is related to changes in muscle morphology. These physiological differences can be attributed directly to increasing BMY and increases in growth rate. Increased body size in both growth-selected and commercial lines has been associated with a decrease in the width of the perimysial and endomysial spaces relative to random bred control lines (Velleman et al., Reference VELLEMAN, COY, ANDERSON, PATTERSON and NESTOR2003b; Velleman and Nestor., 2004). The proliferative capacity of satellite cells increases with selection for growth and the higher amount of genetic material is associated with larger numbers and size of the muscle fibres. Larger muscles are favoured by focusing selection pressure on BMY in commercial breeding objectives, as seen by an increase in fibre width and a decrease in fibre density (Swatland, Reference SWATLAND1989a; Wilson et al., Reference WILSON, NIEBERG, BUHR, KELLY and SHULTZ1990; Cherel et al., Reference CHEREL, HURTREL, GARDAHAUT, MERLY, MAGRAS-RESCH, FONTAINE-PERUS and WYERS1994; Merly et al., Reference MERLY, MAGRAS-RESCH, ROUAUD, FONTAINE-PERUS and GARDAHAUT1998; Velleman et al., Reference VELLEMAN, XIAOSONG, NESTOR and MCFARLAND2000). These divergent patterns in morphology are established early in development as differences in the extracellular space and fibre width are apparent in growth selected and commercial lines, respectively, in the embryo at 25 days of incubation (Velleman et al., Reference VELLEMAN, COY, ANDERSON, PATTERSON and NESTOR2002a). As a result of a selection emphasis on growth, the characteristics of the extracellular space are altered and increased selection pressure on BMY is associated with a change in the morphology of the muscle fibre.
In contrast to additive genetic variation, heterosis and maternal effects do not appear to have a significant effect on BMY. Line crosses do not consistently show heterotic effects, reportedly only being detected for one specific cross within one study (Velleman and Nestor, 2004). Similarly, in a maternal study, objective measurements were not significant when contrasts were made between F2 crosses and did not support differences detected in visual scores of muscle morphology (Velleman et al., Reference VELLEMAN, ANDERSON and NESTOR2003a; Velleman and Nestor, Reference VELLEMAN and NESTOR2004). These studies would indicate that additive genetic factors are the primary genetic contributor to variance in breast morphology, while maternal and heterotic effects have a lower impact on phenotypic differences.
Effect of strain
Muscle morphology and breast yields differ between genetic strains, indicating a divergence in additive genetic factors between genetic groups. There are primarily two genetic pools maintained in the turkey industry; Aviagen Turkeys and Hybrid Turkeys, with a number of small niche breeders supplying the balance of the world parent stock market (Wood et al., Reference WOOD, WOJCINSKI and BUDDIGER2006). Pure lines derived from nucleus breeding populations are crossed to create commercial strains and these genetic groups, as well as selection pressure within the crossed lines, results in varying BMY potential between strains (MacNeil and Buss, Reference MACNEIL and BUSS1968; Blair et al., Reference BLAIR, POTTER and HULET1989; Lilburn and Nestor, Reference LILBURN and NESTOR1991; Brake et al., Reference BRAKE, HAVENSTEIN, FERKET, RIVES and GIESBRECHT1995). As a result, the coefficients describing the linear relationship between BMY and body weight are specific to each strain (Brake et al., Reference BRAKE, HAVENSTEIN, FERKET, RIVES and GIESBRECHT1995).
Variation in breast growth between strains supports the distinct genetic parameters and relationships with body weight. Before 12 weeks of age, strain effects are most significant on the proportion of M. pectoralis superficialis (Barbour and Lilburn, Reference BARBOUR and LILBURN1996). The effect of strain shifts throughout the growing period to significantly affect M. pectoralis profundus yield at later ages (Lilburn et al., Reference LILBURN, RENNER and ANTHONY1992; Lilburn and Emmerson, Reference LILBURN and EMMERSON1993; Barbour and Lilburn, 1995; Roberson et al., Reference ROBERSON, RAHN, BALANDER, ORTH, SMITH, BOOREN, BOOREN, OSBURN and FULTON2003). It is apparent that the independent development of genetic resource pools has created turkey strains with differences in both the genetic potential for BMY as well as pattern of muscle development.
Hatchery effects
Management of the hatchery environment is important as hyperplasia occurs primarily in the embryo and an increase in the number of muscle fibres is associated with larger mature muscle size. Growth and commercially selected lines show significant variation in the number and size of muscle fibres pre-hatch by 20 days of incubation (Velleman et al., Reference VELLEMAN, COY, ANDERSON, PATTERSON and NESTOR2002b). The effect of incubation environment was tested by increasing incubation temperature for short periods between 0 and 12 days of incubation (Maltby et al., Reference MALTBY, SOMAIYA, FRENCH and STICKLAND2004). The result was an increase in the number of muscle fibres as well as density of nuclei, and this early increase in hyperplasia and hypertrophic mechanisms could contribute to a larger final muscle size in the birds at slaughter. The positive effect of increased temperature, however, was not apparent when temperature was increased after 24 days of incubation (Christensen et al., Reference CHRISTENSEN, WINELAND, GRIMES, OVIEDO, MOZDZIAK, ORT and MANN2007). While incubation temperature manipulation can impact BMY, varying oxygen levels has not been shown to have an effect on breast muscle development (Christensen et al., Reference CHRISTENSEN, WINELAND, GRIMES, OVIEDO, MOZDZIAK, ORT and MANN2007). This would indicate that temperature control throughout the early incubation period may contribute to higher BMY by stimulating both muscle hyperplasia and hypertrophy while varying oxygen levels would have no effect.
Nutrition is a key environmental factor post-hatch and the early feeding regime must be carefully managed for a poult to fulfil its genetic potential. Short and long term increases in the proportion of breast meat can be achieved by feeding poults immediately post-hatch (Noy and Sklan, Reference NOY and SKLAN1998; Reference NOY and SKLAN1999). In contrast, post-hatch starvation reduces the proportion of the M. pectoralis superficialis and overall BMY when birds are compared to those given nutrients (Mozdziak et al., Reference MOZDZIAK, WALSH and MCCOY2002; Moore, Reference MOORE2005). A decrease in satellite cell mitotic activity in the first 4 days post-hatch as well as a smaller fibre diameter and nuclear density were also observed in the starved birds. The association of smaller muscle fibres, lower DNA content, and reduced early satellite cell proliferation with decreased final muscle size indicates that post-hatch starvation could negatively impact final BMY. An alternative to feeding poults post-hatch is in-ovo delivery of nutrients to the embryo (Moore, Reference MOORE2005; Foye et al., Reference FOYE, UNI and FERKET2006; de Oliveira, Reference DE OLIVEIRA2007). Results were not supportive of a beneficial relationship with BMY as, regardless of the composition or delivery method, injection of nutrients into the egg did not have any impact on the rate of satellite cell proliferation or BMY. Providing nutrients to poults immediately post-hatch should, consequently, be considered as an effective way to reduce the negative effect that post-hatch starvation may have on BMY.
Nutrition
Nutrition throughout the growing phase has an effect on BMY and a feeding programme that produces the most profitable carcass while minimizing feed costs is required. To identify ways to increase production efficiency, a large number of studies have investigated the effect of diet on BMY. Research has primarily focused on the impact of total feed levels, dietary protein and energy content, and amino acid levels. Study results are summarised in Table 1.
Feed costs could be reduced by limiting the total quantity or nutrient content of feed. The effect of dietary restriction, however, relative to more expensive feeding regimes on carcass yields must be considered. As would be expected, severe feed restriction negatively impacts BMY (Crouch et al., Reference CROUCH, GRIMES, CHRISTENSEN and KRUEGER2002). On the contrary, dietary protein can be restricted by up to 10%, relative to NRC recommendations, without negatively impacting BMY (Blair et al., Reference BLAIR, POTTER and HULET1989; Clarke et al., Reference CLARKE, FERKET, ELKIN, MCDANIEL, FREED, MCMURTRY, KRUEGER and HESTER1993; Barbour and Lilburn, 1996; Kidd et al., Reference KIDD, KERR, ENGLAND and WALDROUP1997; Waibel et al., Reference WAIBEL, CARLSON, BRANNON and NOLL2000). The negative impact of protein restrictions in excess of 10% on final yield values is reduced when the diet limitation occurs before 6 weeks of age (Oju et al., Reference OJU, WAIBEL and NOLL1988; Ferket and Sell, 1989). This suggests that the time and length of the restriction period must also be considered. Feeding a diet supplemented to contain a 20% increase in protein, above NRC recommendations, after a protein restriction of greater than 10% can also help reduce the negative effect (Hester et al., Reference HESTER, KRUEGER and JACKSON1990). Potential for compensatory growth may therefore be higher in younger turkeys and may also be favoured by diets that contain excess protein after the restriction period. These studies indicate that there is potential for the protein content of turkey feed to be reduced to 90%, if all other nutrients are formulated to meet or exceed NRC recommendations, without negatively impacting BMY.
Reducing the total amino acid content, or a combination of essential amino acids (Lys, Met+Cys, Thr, Trp, Arg, His, Leu, Ile, Phe, and Val), has a negative impact on BMY (Waldroup et al., Reference WALDROUP, ADAMS and WALDROUP1993; Reference WALDROUP, ANTHONY and WALDROUP1998; Lemme et al., Reference LEMME, FRACKENPOHL, PETRI and MEYER2006). The effect of amino acid reduction becomes stronger later in the growing phase and with longer restriction periods (Lemme et al., Reference LEMME, FRACKENPOHL, PETRI and MEYER2006). This supports the increase in sensitivity to dietary restriction with age.
The effect of variation in dietary concentration of specific essential amino acids depends on the amino acid considered. Increasing threonine levels in a diet that meets basic protein requirements can improve the trait, however supplemented threonine does not have a positive effect on BMY when birds are fed a protein deficient diet (Kidd et al., Reference KIDD, KERR, ENGLAND and WALDROUP1997; Lehmann et al., Reference LEHMANN, PACK and JEROCH1997; Waibel et al., Reference WAIBEL, CARLSON, BRANNON and NOLL2000). Varying methionine levels can be ineffective, however there is a positive dietary effect when betaine is added with the methionine (Noll, Reference NOLL2002). This is a result of the interaction between betaine and both methionine and the lipid metabolic pathway. Alternatively, increasing lysine levels in turkey feed had a positive impact on BMY and this occurs independently of the relative proportion of dietary arginine (Lilburn and Emmerson, Reference LILBURN and EMMERSON1993; Lehmann et al., Reference LEHMANN, PACK and JEROCH1996; Kidd and Kerr, 1998; Veldkamp et al., Reference VELDKAMP, KWAKKEL, FERKET, KOGUT and VERSTEGEN2003). Cumulatively, these studies show that limitation of certain amino acids, including methionine and threonine, is possible without affecting BMY, however there is are positive correlations between BMY and total amino acid and lysine levels.
The addition of fat as an energy source has been used to improve growth performance, however increasing the dietary fat concentration has not significantly affected BMY (Salmon, Reference SALMON1974; Sell et al., Reference SELL, HASIAK and OWINGS1985; Halvorson et al., Reference HALVORSON, WAIBEL, OJU, NOLL and EL-HALAWANI1991; Sell, Reference SELL1993; Sell et al., Reference SELL, JEFFREY and KERR1994). If the level of protein to energy (fat) in the feed is not maintained, BMY can be reduced (Salmon, Reference SALMON1983). Increasing dietary fat levels, consequently, is not a viable option to reduce feed costs, as the relative level of protein must also be increased to maintain performance levels.
Antibiotics and feed additives have been considered as a means to improve growth performance. Results have shown a positive benefit of virginiamycin and ractopamine on both feed efficiency and body weight (Cervantes, Reference CERVANTES2009; Elanco Animal Health, Reference ELANCO ANIMAL HEALTH.2008; Ferket et al., Reference FERKET, PARKS and GRIMES2002; Waibel et al., Reference WAIBEL, HALVORSON, NOLL and HOFFBECK1991). While the increase in body weight caused by virginiamycin is not associated with an increase in BMY, cellular studies have indicated that ractopamine can increase the number, protein, and DNA content of muscle cells in the turkey (Parks et al., Reference PARKS, GRIMES and FERKET2005; Shappell et al., Reference SHAPPELL, FEIL, SMITH, LARSEN and McFARLAND2000). These cellular responses may have a positive effect on breast growth, however there is limited research on the effect of ractopamine on BMY and conclusions cannot be made. As a result, a reduction in dietary protein provides the most potential for reducing feed costs without impacting BMY. Caution should be taken to ensure the dietary amino acid and lysine levels are formulated to meet requirements if the concentration of other nutrients is altered.
Growing environment
Natural climatic fluctuations and controlled growing environments have been used to investigate the impact of rearing environment on BMY. Breast meat yield is negatively impacted by heat and increased environmental temperatures decrease BMY (Rose and Michie, Reference ROSE and MICHIE1987; Noll et al., Reference NOLL, STRANGELAND, SPEERS and BRANNON2001; Noll, Reference NOLL2002; Veldkamp et al., Reference VELDKAMP, KWAKKEL, FERKET and VERSTEGEN2005). Rearing environments with higher temperatures during light periods and lower temperatures during darkness produce intermediate BMY relative to consistently hot or cool environments (Halvorson et al., Reference HALVORSON, WAIBEL, OJU, NOLL and EL-HALAWANI1991). Altering the dietary electrolyte balance and nutrient levels has been attempted to reduce the negative impact of heat, however these manipulations were not effective (Veldkamp et al., Reference VELDKAMP, FERKET, KWAKKEL, NIXEY and NOORDHUIZEN2000a; Reference VELDKAMP, KWAKKEL, FERKET, SIMONS, NOORDHUIZEN and PIJPERS2000b).
Light cycling programmes involve alternating fixed-length light and dark periods each day. Alternatively, intermittent lighting involves exposing the birds to more frequent alternating light and dark periods during a 24 hour day. Light cycling has been shown to increase BMY and the effect has been significant if the light periods are substantially longer than the periods of dark (18L:6D) (Halvorson et al., Reference HALVORSON, WAIBEL, OJU, NOLL and EL-HALAWANI1991; Clarke et al., Reference CLARKE, FERKET, ELKIN, MCDANIEL, FREED, MCMURTRY, KRUEGER and HESTER1993). When light cycling is practiced, gradually decreasing the light exposure results in higher BMY when compared to gradually increasing light hours (Peng et al., Reference PENG, ADAMS, FURUMOTO, HESTER, LARSEN, PIKE and STADELMAN1985; Lilburn et al., Reference LILBURN, RENNER and ANTHONY1992). The effect seems to be most strongly correlated to the development of the M. pectoralis superficialis (Lilburn et al., Reference LILBURN, RENNER and ANTHONY1992). It is apparent that maintaining lower rearing temperatures as well as light cycling should be utilized to optimize BMY. These positive correlations are most likely due to the reduced biological stress and stimulation of bird activity that can be created by these management practices.
Conclusions
The processes regulating muscle growth are dynamic, and hyperplasia and hypertrophy both contribute to breast development. The physiological characteristics of the breast muscle, as well as total yields from the carcass, are under the influence of additive genetic factors and genetic potential can vary by sex and strain. This genetic component makes trait improvement possible by applying selection pressure to breast meat yield in a breeding programme. Management of the rearing environment, including nutrition, lighting, and temperature, all must be carefully considered for turkeys to fulfil their genetic potential. As a result of the combined impact of both genetics and environment on breast meat yield, all industry levels from the primary breeder to the commercial grower must consider the influence that they can have on final proportion of breast meat.
