Introduction
There are numerous growth path possibilities during early and later life that may influence productive characteristics of cattle. These different growth paths result from factors including climate, soil quality and pasture species, which contribute to variable pasture and nutrient quality and availability. Growth of the bovine foetus has well-studied consequences for survival (Holland and Odde, Reference Holland and Odde1992) and can be slowed during the latter half of gestation by restricted nutrition and/or inadequate placental development (Bell et al., Reference Bell, Greenwood and Ehrhardt2005). Similarly, influences of pre-weaning nutrition, most notably lactational performance of the dam, on growth to market weights of cattle are well characterised (Berge, Reference Berge1991). However, consequences of foetal calf growth for subsequent growth, and of foetal and neonatal calf growth for efficiency and carcass- and beef-quality characteristics, are less well understood.
Hence, this paper reviews research on consequences of cattle nutrition and growth during foetal and neonatal life for subsequent growth and efficiency, and for carcass and beef quality. It includes findings from our recent studies on consequences of maternal nutrition (commencing between days 30 and 90 of gestation) and growth during pregnancy and to weaning of cattle sired by bulls of extreme genotypes for muscle and intramuscular fat development (Cafe et al., Reference Cafe, Hearnshaw, Hennessy and Greenwood2006a and Reference Cafe, Hennessy, Hearnshaw, Morris and Greenwood2006b; Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006). Factors affecting growth and nutrition of the bovine foetus and milk-fed calf are also briefly described. The reader is also referred to reviews on consequences of prenatal development in livestock species by Bell (Reference Bell2006) and Symonds et al. (Reference Symonds, Stephenson, Gardner and Budge2007), and on consequences of bovine foetal, pre-weaning and early post-weaning growth and nutrition by Berge (Reference Berge1991) and Greenwood et al. (Reference Greenwood, Cafe, Hearnshaw and Hennessy2005).
Normal bovine conceptus growth and metabolism
During postnatal growth, energy and nutrient availability directly influence growth and body composition of cattle. However, environmental influences on foetal growth and development and, hence, birth characteristics are regulated via the dam, and by the placenta that functions as a nutritional conduit between the dam and the foetus.
Most growth of the bovine foetus occurs during the final 100 days or so of a gestation averaging approximately 280 days (Winters et al., Reference Winters, Green and Comstock1942; Lyne, Reference Lyne1960; Ferrell et al., Reference Ferrell, Garrett and Hinman1976; Prior and Laster, Reference Prior and Laster1979). Foetal nutrient uptake becomes a quantitatively important contributor to maternal nutrient requirements only after mid-gestation (Ferrell et al., Reference Ferrell, Ford, Prior and Christenson1983). Unlike the sheep, in which the placenta attains most of its mass of dry tissue, protein and DNA by mid-gestation (Ehrhardt and Bell, Reference Ehrhardt and Bell1995), the bovine placenta normally continues to increase in weight until near term (Prior and Laster, Reference Prior and Laster1979; Ferrell, Reference Ferrell1989). As a result, it has been suggested that placental growth may be less sensitive to nutritional deficiencies in cattle than in sheep. Placental weight and birth weight are highly correlated in cattle (Anthony et al., Reference Anthony, Bellows, Short, Staigmiller, Kaltenbach and Dunn1986b; Echternkamp, Reference Echternkamp1993; Zhang et al., Reference Zhang, Nakao, Moriyoshi, Nakada, Ohtaki, Ribadu and Tanaka1999); however, the functional capacity of the placenta is closely related to placental perfusion. Bovine uterine and umbilical blood flow increases exponentially during the second half of gestation, which equates to relatively constant rates of umbilical blood flow on a foetal weight-specific basis during this period (Reynolds et al., Reference Reynolds, Ferrell, Robertson and Ford1986). A more detailed account of placental function and metabolism in cattle is provided by Ferrell (Reference Ferrell1989), and of foetal macronutrient requirements and metabolism in cattle and sheep, and of placental function and metabolism, by Bell et al. (Reference Bell, Greenwood and Ehrhardt2005).
Intrauterine growth retardation
Maternal nutrition
Severe nutritional restriction for at least the last half to one-third of pregnancy is usually required to reduce bovine foetal growth. Significant reductions in birth weight were caused by prolonged underfeeding of heifers from weaning until parturition (Wiltbank et al., Reference Wiltbank, Bond, Warwick, Davis, Cook, Reynolds and Hazen1965), and underfeeding of heifers and cows for the second and third trimesters (Ryley and Gartner, Reference Ryley and Gartner1962; Hodge and Rowan, Reference Hodge and Rowan1970; Freetly et al., Reference Freetly, Ferrell and Jenkins2000; Cafe et al., Reference Cafe, Hennessy, Hearnshaw, Morris and Greenwood2006b) or late pregnancy only (Hight, Reference Hight1966; Tudor, Reference Tudor1972; Bellows and Short, Reference Bellows and Short1978; Kroker and Cummins, Reference Kroker and Cummins1979). The effect of nutritional restriction on birth weight was more pronounced in calves from heifers than those from cows when the period of restriction encompassed mid- and late gestation (Hennessy et al., Reference Hennessy, Hearnshaw, Greenwood, Harper and Morris2002) rather than late gestation only (Tudor, Reference Tudor1972). However, birth weight was not significantly affected by nutritional restriction of heifers from mating to 140 days gestation (Cooper et al., Reference Cooper, Morris and McCutcheon1998) or during the final 12 weeks of pregnancy (Hodge et al., Reference Hodge, Beasley and Stokoe1976), or of mature cows for the second trimester (Freetly et al., Reference Freetly, Ferrell and Jenkins2000).
During the final one-half to one-third of pregnancy, feed energy available to the dam appears to have more influence on birth weight than the availability of protein, although results are variable (Holland and Odde, Reference Holland and Odde1992). Variation in feed energy available to the dam during this period resulted in differences in birth weight, ranging from 0 to 8.2 kg (Dunn et al., Reference Dunn, Ingalls, Zimmerman and Wiltbank1969; Tudor, Reference Tudor1972; Laster, Reference Laster1974; Corah et al., Reference Corah, Dunn and Kaltenbach1975; Bellows and Short, Reference Bellows and Short1978; Kroker and Cummins, Reference Kroker and Cummins1979; Bellows et al., Reference Bellows, Short and Richardson1982). Similarly, variable protein supply of the diet during the third trimester may (Bellows et al., Reference Bellows, Carr, Patterson, Thomas, Killen and Milmine1978) or may not (Anthony et al., Reference Anthony, Bellows, Short, Staigmiller, Kaltenbach and Dunn1986a; Holland and Odde, Reference Holland and Odde1992) alter birth weight of calves, while restricted or supplemental dietary protein during early or mid-pregnancy had little effect on birth weights (Perry et al., Reference Perry, Norman, Owen, Daniel and Phillips1999 and Reference Perry, Norman, Daniel, Owens, Grant and Doogan2002). Furthermore, supplementation of grazing cows for 3 months pre-partum with 0.45 kg/day of 42% crude protein supplement did not affect calf birth weights (Stalker et al., Reference Stalker, Adams, Klopfenstein, Feuz and Funston2006). However, more chronic nutritional restriction of energy and/or protein of heifers from weaning until parturition resulted in birth weight differences of up to 10 kg due to energy supply and up to 7.3 kg due to protein supply (Wiltbank et al., Reference Wiltbank, Bond, Warwick, Davis, Cook, Reynolds and Hazen1965).
As described above, placental weight and birth weight are highly correlated in cattle. However, because the bovine placenta may continue to increase in mass until near term, it is less clear whether the placenta regulates bovine foetal growth to the same extent as it does in sheep (Ferrell, Reference Ferrell1989). Placental characteristics may be altered by nutrition during early and mid-pregnancy without significantly affecting foetal size (Rasby et al., Reference Rasby, Wettermann, Geisert, Rice and Wallace1990), and protein supplementation of cows during early or mid-pregnancy may also alter placental characteristics without necessarily affecting birth weight (Perry et al., Reference Perry, Norman, Owen, Daniel and Phillips1999 and Reference Perry, Norman, Daniel, Owens, Grant and Doogan2002).
Development and growth of vital organs precede development of bone, muscle and fat (Palsson, Reference Palsson1955), respectively; hence the mass of the relatively late maturing carcass tissues are generally considered more susceptible to the effects of nutrition during later pregnancy when nutrition impacts most on foetal growth. However, more subtle effects on organ and tissue development due to nutrition during early pregnancy may occur, with the potential for long-term consequences for health, as shown in sheep (Greenwood and Bell, Reference Greenwood and Bell2003; Bell et al., Reference Bell, Greenwood and Ehrhardt2005; Symonds et al., Reference Symonds, Stephenson, Gardner and Budge2007).
Thermal environment
Foetal growth in cattle was restricted (18% lower foetal weight) by chronic heat stress of pregnant cows, while provision of shade resulted in a 3.1 kg increase in birth weight (Collier et al., Reference Collier, Doelger, Head, Thatcher and Wilcox1982). In sheep, chronic heat stress in early to mid-gestation restricts placental development, thus imposing a limitation on subsequent foetal growth irrespective of nutrition later in pregnancy (Bell et al., Reference Bell, Wilkening and Meschia1987). This suggests that restricted foetal calf growth due to heat stress is probably a consequence of reduced placental development. Severe cold stress of cattle may also reduce foetal growth if inadequate nutrition is provided to meet the additional metabolic requirements of cows in addition to foetal requirements for growth and development (Andreoli et al., Reference Andreoli, Minton, Spire and Schalles1988), although in sheep, more moderate cold stress of ewes in late gestation increased birth weight by 15% (Thompson et al., Reference Thompson, Bassett, Samson and Slee1982). It is believed that temperature regulates blood flow to the periphery and lungs in order to preserve or dissipate body heat, resulting in increased or decreased blood flow and nutrient supply to the gravid uterus (Reynolds et al., Reference Reynolds, Ferrell and Nienaber1985).
Parity
Heifers give birth to smaller calves, on average, than cows (reviewed by Holland and Odde, Reference Holland and Odde1992) due at least in part to size and nutritional requirements for growth of heifers, limiting nutrient availability for placental and foetal growth. Severe maternal nutritional restriction may impact more on birth weights of calves of heifers than of cows, particularly among male calves and those of sires with inherently high birth weight of offspring (Hennessy et al., Reference Hennessy, Hearnshaw, Greenwood, Harper and Morris2002), presumably due to their greater requirements for nutrients compared with female calves and those of sires with inherently low birth weight of offspring. In adolescent sheep fed to attain excessive fatness prior to and during gestation, placental and foetal growth and birth weight are reduced (Wallace et al., Reference Wallace, Aitken and Cheyne1996 and Reference Wallace, Bourke and Aitken1999), although the extent to which over-nutrition of adolescent heifers influences birth weight is not clear.
Litter size
Twin calves and higher multiples are rare in cattle unless exogenous regulation of ovarian function or embryo transfer is practised. Individuals within litters have reduced foetal growth compared with singletons due to a reduced number of placentomes and mass of placenta per foetus (Hafez and Rajakoski, Reference Hafez and Rajakoski1964; Greenwood et al., Reference Greenwood, Slepetis and Bell2000b) and because of greater total nutrient requirements of the litter. On average, twin calves range from 7.4 to 9.8 kg lighter than singletons (Gregory et al., Reference Gregory, Echternkamp, Dickerson, Cundiff, Koch and Van Vleck1990 and Reference Gregory, Echternkamp and Cundiff1996; De Rose and Wilton, Reference De Rose and Wilton1991; Cummins, Reference Cummins1994; Wilkins et al., 1994). Restricted nutrition limits foetal growth earlier and more severely in twins or higher multiples than in singletons, although stocking rates of pregnant cows fed on pasture did not significantly influence the birth weight of twins (Wilkins et al., 1994).
Foetal and maternal genotype
Foetal genotype is most important in determining foetal growth during early and mid-pregnancy, whereas maternal genotype is more important in determining foetal growth during late pregnancy when most foetal growth normally occurs and foetal growth is increasingly subject to external influences mediated via the dam. The effect of foetal and maternal genotype on foetal growth has been most convincingly demonstrated in cattle by Ferrell (Reference Ferrell1991) who implanted Charolais (heavier birth weight) or Brahman (lighter birth weight) embryos into Charolais and Brahman cows. At 232 days of pregnancy, each foetal genotype was similar in size, irrespective of dam breed. However, by 274 days of gestation Charolais foetuses in Brahman cows were 7 kg lighter than those in Charolais cows. In contrast, Brahman foetuses in Charolais cows were only 2 kg heavier than those in Brahman cows. Similar results were obtained by Joubert and Hammond (Reference Joubert and Hammond1958) for birth weights for South Devon and Dexter cattle and their reciprocal crosses. In this regard, foetal growth capacity as influenced by sex and sire-genotype may also influence the nutritional status of the pregnant cow during late gestation (Greenwood et al., Reference Greenwood, Wolcott, Hearnshaw, Hennessy, Morris and Harper2002b), probably due to differences in foetal nutrient uptake, contributing to maternal nutrient requirements.
Growth and development from birth to weaning
Calves undergo a transition at birth from a diet comprising primarily glucose and amino acids to one that is quantitatively greater and is proportionately higher in fat. This is associated with maturation of the digestive, metabolic and endocrine systems. Evidence in sheep suggests severely growth-retarded newborns are immature with respect to energy metabolism and have more foetal-like metabolism than their well-grown counterparts (Greenwood et al., Reference Greenwood, Hunt, Slepetis, Finnerty, Alston, Beermann and Bell2002a; Rhoads et al., Reference Rhoads, Greenwood, Bell and Boisclair2000a and Reference Rhoads, Greenwood, Bell and Boisclair2000b).
The major nutritional factors affecting pre-weaning calf growth and composition at weaning are the lactational performance of the dam and the quality and availability of nutrients from pasture and/or supplementation prior to and following parturition. Most notably, maternal genotype, age and parity, nutrient availability and body condition and live weight of the dam, and capacity of the calf to grow and consume milk, interact to influence lactational output. Calves become increasingly dependent on forage-based diets that result in the production of volatile fatty acids that stimulate development and maturation of the rumen (Warner and Flatt, Reference Warner and Flatt1965) until weaning, when this dependence becomes complete.
Long-term consequences of altered growth during the early life of cattle
In this section, the long-term consequences of altered growth early in life for growth, feed efficiency, and carcass, yield, beef quality and myofibre characteristics are discussed first for altered foetal growth, and then for altered pre-weaning growth. Interactions between prenatal and pre-weaning growth are then discussed.
Consequences of foetal growth and nutrition
Postnatal growth
In our recent studies of consequences of foetal growth, which compared performance of calves differing by 10.2 kg or by 35% in birth weight (Table 1), capacity of low-birth-weight cattle to exhibit compensatory growth was limited. Cattle significantly growth retarded during foetal life due to severely restricted maternal nutrition from early pregnancy (commencing between day 30 and 90 of pregnancy) to parturition remained smaller during rearing on their dams and at any given postnatal age after weaning compared with their well-grown or better-nourished counterparts (Table 1). However, it remains speculative whether this represents a permanent stunting or simply a delay of attainment of mature size of cattle. Growth of low-birth-weight cattle was significantly slower than those of high birth weight at all stages of postnatal growth, although about half the difference in average daily gain (ADG) during feedlotting was explained by differences in weight at feedlot entry between the low- and high-birth-weight cattle (Table 1). However, when differences in birth weights were less-pronounced, post weaning and feedlot growth were not significantly affected by birth weight (Cafe et al., Reference Cafe, Hearnshaw, Hennessy and Greenwood2006a). These findings are consistent with those of Swali and Wathes (Reference Swali and Wathes2006) who found that small size at birth resulted in smaller cattle compared with high-birth-weight cattle at 15 months of age, while average-birth-weight cattle did not differ significantly in weight during postnatal growth compared with the low- or high-birth-weight groups.
Table 1 Consequences of growth in utero for growth and live-weight characteristics of beef cattle to 30 months of age (adapted from Greenwood et al., Reference Greenwood, Cafe, Hearnshaw and Hennessy2005 and Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006)Footnote †
Abbreviation is: ADG = average daily gain.
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex/year cohort, sire-genotype and their interactions.
† Maternal nutritional treatments commenced between days 30 and 90 of pregnancy (refer to Cafe et al. (Reference Cafe, Hennessy, Hearnshaw, Morris and Greenwood2006b) and Greenwood et al. (Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006) for details of pasture-based nutritional treatments and selection criteria for calves used to study long-term consequences of growth early in life).
‡ Predicted from mean ADG during backgrounding.
§ Predicted from mean ADG during background and mean feedlotting period.
In contrast to the above findings, artificially reared low-birth-weight male calves grew more rapidly to weaning than their high-birth-weight counterparts, although the opposite occurred for female calves (Tudor and O’Rourke, Reference Tudor and O’Rourke1980). Hence, it is important to recognise that an assessment of influences of foetal development on postnatal performance requires consideration of the consequences of nutrition during pregnancy on subsequent maternal performance when offspring remain on their dams to weaning, due to carry-over effects on the dam. In this regard, readers are referred to Greenwood et al. (Reference Greenwood, Hunt, Hermanson and Bell1998) for an example of a rearing system designed to uncouple prenatal and postnatal influences in ruminants varying in birth weight. The net effects of maternal nutrition during pregnancy on the calf remain of practical significance to livestock producers, and influences of nutrition during mid- and late pregnancy or late pregnancy only on calf weaning weight have been consistently shown (e.g. Hight, Reference Hight1966 and Reference Hight1968a; Cafe et al., Reference Cafe, Hennessy, Hearnshaw, Morris and Greenwood2006b; Stalker et al., Reference Stalker, Adams, Klopfenstein, Feuz and Funston2006), irrespective of effects on foetal growth.
In relation to potential interactions between prenatal and postnatal nutrition and growth, differences in weight of calves at birth following three levels of maternal nutrition during late pregnancy disappeared by weaning when postnatal nutrition was of high quality and availability (Hight, Reference Hight1968b). In this study, however, residual effects of the previous year’s nutrition influenced calf growth, with cows previously well nourished producing heavier calves, and vice versa (Hight, Reference Hight1968b). Similarly, effects of variable nutrition during mid- and/or late pregnancy on weight at birth were overcome by adequate nutrition post partum, resulting in no difference in body weight at 58 days of age (Freetly et al., Reference Freetly, Ferrell and Jenkins2000). While twin cattle are lighter at birth and grow more slowly on their dams to weaning (Hennessy and Wilkins, Reference Hennessy and Wilkins1997), they may grow more slowly (Gregory et al., Reference Gregory, Echternkamp and Cundiff1996), at a similar rate (De Rose and Wilton, Reference De Rose and Wilton1991) or more rapidly (Wilkins et al., 1994; Clarke et al., Reference Clarke, Cummins, Wilkins, Hennessy, Andrews and Makings1994; Hennessy and Wilkins, Reference Hennessy and Wilkins1997) post-weaning than singletons, depending on the rearing system and subsequent nutritional regimen.
Feed intake and efficiency
Slower feedlot growth by low-birth-weight calves was associated with the consumption of fewer nutrients in the feedlot but no difference in feed efficiency or residual feed intake compared with high-birth-weight calves at an equivalent age from 26 to 30 months (Table 2). When compared at equivalent feedlot entry live weights, differences in feed intake due to birth weight were no longer apparent, consistent with findings in twin cattle, which tended to consume less feed in feedlot than singletons, due primarily to their lower live weight (De Rose and Wilton, Reference De Rose and Wilton1991). Similarly, provision of supplement to cows for 3 months pre-partum had no significant post-weaning effects on ADG, feed intake and feed efficiency in steers (Stalker et al., Reference Stalker, Adams, Klopfenstein, Feuz and Funston2006) or heifers (Martin et al., Reference Martin, Vonnahme, Adams, Lardy and Funston2007) that were individually fed following weaning, although the heifers of supplemented cows tended to have greater absolute and residual feed intakes during individual feeding for 84 days post-weaning.
Table 2 Consequences of growth in utero for feed intake and efficiency of beef cattle during feedlotting from 26 to 30 months of age (L. M. Cafe and P. L. Greenwood, unpublished results)
Abbreviations are: ADG = average daily gain, DM=dry matter; LW=live weight.
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex/year cohort, sire-genotype and their interactions, with feedlot entry weight as a covariate (linear and, where significant, quadratic) to predict means at equivalent feedlot entry weight. Difference in significance of feedlot ADG between Tables 1 and 2 is due to the number of cohorts studied (three cohorts in Table 1v. two cohorts in Table 2) and the duration of the measurement period (average of 117 days in Table 1v. 70 days in Table 2).
† During 70-day period in feed intake pens.
‡ At mean metabolic live weight.
Body and carcass composition
Few studies have examined long-term consequences of foetal nutrition and growth for body and carcass characteristics in cattle (Tudor et al., Reference Tudor, Utting and O’Rourke1980) prior to our more recent studies (Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006). Our research has shown that a significant reduction in birth weight following severe maternal nutritional restriction did not influence indices of fatness, apart from P8 (rump) fat, in carcasses of Wagyu- or Piedmontese-sired steers and heifers at 30 months of age, beyond that normally attributable to differences in live or carcass weight (Table 3). Low-birth-weight cattle had a similar intramuscular fat content, retail yield, fat trim and bone content at equivalent carcass weight, suggesting little overall difference in carcass composition from their high-birth-weight counterparts. However, ossification score was higher in low- compared with high-birth-weight calves (Table 3), suggesting an impact of prenatal growth on calcification of bone and relative maturity. Similar to our findings, gross compositional differences were not evident in the whole body or in the carcass of Hereford steers or heifers grown to 370 to 400 kg live weight following restricted or adequate nutrition of their dams from 180 days of pregnancy to parturition with a resultant 22% or 6.8 kg difference in calf birth weight (Tudor et al., Reference Tudor, Utting and O’Rourke1980). Furthermore, pre-partum supplementation of cows had no effects on the carcass composition of offspring following feedlotting for 222 days post weaning (Stalker et al., Reference Stalker, Adams, Klopfenstein, Feuz and Funston2006).
Table 3 Consequences of growth in utero for carcass and yield characteristics of beef cattle at 30 months of age (adapted from Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006)
Abbreviation is: IMF = intramuscular fat.
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex/year cohort, sire-genotype and their interactions, with carcass weight as a covariate (linear and, where significant, quadratic) to predict means at equivalent carcass weight. Refer to Table 1 for growth characteristics of the cattle.
Research on twin cattle has also demonstrated that, despite significantly lower birth weights and reduced pre-weaning growth, compositional differences at equivalent slaughter weights or ages are small and not significant, with twins generally having similar or leaner carcasses than singletons (De Rose and Wilton, Reference De Rose and Wilton1991; Wilkins et al., 1994; Clarke et al., Reference Clarke, Cummins, Wilkins, Hennessy, Andrews and Makings1994; Gregory et al., Reference Gregory, Echternkamp and Cundiff1996).
Beef quality and myofibre characteristics
There were no adverse effects on objective measurements of beef quality including peak force, compression, cooking loss and colour in the longissimus (striploin) and semitendinosus (eye round) muscles at 30 months of age due to restricted growth in utero (Table 4).
Table 4 Consequences of growth in utero for objective measurements of m. longissimus (striploin) and m. semitendinosus (eye round) quality in beef cattle at 30 months of age (adapted from Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006)
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex, sire-genotype and their interactions. Refer to Tables 1 and 3 for growth and carcass characteristics of the cattle.
† Objective measures of texture, as defined by Perry et al. (Reference Perry, Shorthose, Ferguson and Thompson2001).
Myofibre characteristics including number and size of myofibres, and percentages and relative areas of myofibres in the m. longissimus lumborum (Table 5) and semitendinosus (results not shown) muscles at 30 months of age, were also unaffected by calf growth in utero (Table 5). In this regard, nutrition during pregnancy resulting in divergent foetal calf growth resulted in differences at birth in the percentages of type 1 (low 17.2 v. high 23.3%) and type 2A (28.2 v. 23.5%) myofibres, the ratio of fast to slow (4.8 v. 3.4) myofibres and the cross-sectional area of type 2X (673 v. 831 μm2) myofibres (Greenwood et al., Reference Greenwood, Hearnshaw, Kelly and Hennessy2004). However, differences in myofibre characteristics due to foetal growth were no longer evident by weaning (P. L. Greenwood, unpublished results). Within the present study, as with newborn lambs restricted in growth during mid- to late pregnancy (Greenwood et al., Reference Greenwood, Slepetis, Hermanson and Bell1999 and Reference Greenwood, Hunt, Hermanson and Bell2000a), apparent myofibre number was not affected by divergent growth in utero (Table 5).
Table 5 Consequences of growth in utero for longissimus lumborum myofibre characteristics of heifer beef cattle at 30 months of age (P. L. Greenwood and L. M. Café, unpublished results)
Abbreviation is: CSA = cross-sectional area.
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex, sire-genotype and their interactions.
Refer to Lehnert et al. (Reference Lehnert, Byrne, Reverter, Nattrass, Greenwood, Wang, Hudson and Harper2006) for myofibre classification and measurement methodology. Type 1, type 1 myosin heavy chain (MHC) ≡ slow oxidative; type 2C, intermediate between type 1 and type 2A; type 2A, type 2A MHC ≡ fast oxidative-glycolytic; type 2AX, intermediate between type 2A and type 2X; type 2X, type 2X MHC ≡ fast glycolytic.
Consequences of pre-weaning growth and nutrition
Postnatal growth
Consequences of nutritional restriction from birth to weaning for subsequent growth of cattle were reviewed by Allden (Reference Allden1970), Berge (Reference Berge1991) and Hearnshaw (Reference Hearnshaw1997). It is generally recognised that severe pre-weaning nutritional restriction limits the capacity of cattle to exhibit compensatory growth and achieve equivalent weight for age in later life. In reviewing a series of Australian studies on consequences of pre-weaning nutritional systems, Hearnshaw (Reference Hearnshaw1997) concluded that compensatory gain following pre-weaning growth restriction occurred most frequently when overall post-weaning growth rates were less than 0.6 kg/day, whereas at higher post-weaning growth rates compensation was less evident. However, in feedlot the differences in growth were in the opposite direction to differences in growth post-weaning, and when compensation did occur among cattle restricted prior to weaning, the gains were only small. In more recent studies, calves reared slowly (464 g/day) compared with those reared rapidly (872 g/day) from birth to weaning were 37 kg lighter at weaning, but 48 kg lighter following backgrounding due to a trend towards slower backgrounding growth among the previously restricted cattle, and remained 46 kg lighter at slaughter at 17 months of age (Hennessy and Morris, Reference Hennessy and Morris2003; Hennessy and Arthur, Reference Hennessy and Arthur2004).
In our recent studies, a difference in weaning weight of 73 kg resulted in a 40 kg difference in live weight and 24 kg in carcass weight at 30 months of age (Greenwood et al., Reference Greenwood, Cafe, Hearnshaw and Hennessy2005 and Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006; Table 6). The low weaning weight cattle grew more rapidly during backgrounding and at a similar rate in the feedlot, resulting in more rapid growth overall from weaning to 30 months of age. However, compensation in live weight remained incomplete by the conclusion of the study. Similarly, in steers restricted in growth from birth to weaning, then backgrounded to the same feedlot entry weight as cattle grown rapidly to weaning, some compensatory growth was observed during backgrounding but not in the feedlot (Cafe et al., Reference Cafe, Hearnshaw, Hennessy and Greenwood2006a). These studies have confirmed earlier findings that severe, chronic nutritional restriction to weaning limits compensatory growth, which only occurred prior to feedlot entry and not in the feedlot, resulting in smaller cattle and carcasses and less retail yield of beef at an equivalent age.
Table 6 Consequences of growth from birth to weaning for growth and live weight characteristics of beef cattle to 30 months of age (adapted from Greenwood et al., Reference Greenwood, Cafe, Hearnshaw and Hennessy2005 and Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006)Footnote †
Abbreviation is: ADG = average daily gain.
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex/year cohort, sire-genotype and their interactions, with feedlot entry weight as a covariate (linear and, where significant, quadratic) to predict means at equivalent feedlot entry weight.
† Refer to Cafe et al. (Reference Cafe, Hennessy, Hearnshaw, Morris and Greenwood2006b) and Greenwood et al. (Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006) for details of pasture-based nutritional treatments and selection criteria for calves used to study long-term consequences of growth early in life.
‡ Predicted from mean ADG during backgrounding.
§ Predicted from mean ADG during background and mean feedlotting period.
Feed intake and efficiency
During feedlotting from 26 to 30 months of age, feed intake was lower among cattle grown slowly to weaning than those grown rapidly; however, this effect of pre-weaning growth rate was not evident when assessed at the same feedlot entry weight (Table 7). Differences in feed efficiency or residual feed intake were not apparent on an age- or live-weight equivalent basis. Consistent with these findings, when variation in live weight that contributed to differences in energy requirements for maintenance and growth were accounted for, low pre-weaning growth rates did not influence measures of efficiency in the feedlot of cattle of equivalent age compared with those grown more rapidly prior to weaning (Hennessy and Arthur, Reference Hennessy and Arthur2004). Furthermore, effects of early post partum nutrition on growth, intake and efficiency of steers (Stalker et al., Reference Stalker, Adams, Klopfenstein, Feuz and Funston2006) and heifers (Martin et al., Reference Martin, Vonnahme, Adams, Lardy and Funston2007) in the feedlot soon after weaning were not evident. These results are consistent with earlier findings, reviewed by Berge (Reference Berge1991), that feed conversion efficiency is little affected in the long term by nutrition prior to weaning. However, following extremely severe postnatal nutritional restriction where calves were held near their birth weights for 200 days, compared with cattle well grown to weaning, feed efficiency was adversely affected in males during growth from 200 kg to about 400 kg live weight, whereas during the same period females were more efficient (Tudor and O’Rourke, Reference Tudor and O’Rourke1980).
Table 7 Consequences of growth from birth to weaning for feed intake and efficiency of beef cattle during feedlotting from 26 to 30 months of age (L. M. Cafe and P. L. Greenwood, unpublished results)
Abbreviations are: ADG = average daily gain, DM = dry matter, LW = live weight.
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex/year cohort, sire-genotype and their interactions, with feedlot entry weight as a covariate (linear and, where significant, quadratic) to predict means at equivalent feedlot entry weight. Difference in significance of feedlot ADG between Tables 6 and 7 is due to the number of cohorts studied (three in Table 6v. two in Table 7) and the duration of the measurement period (average of 117 days in Table 6v. 70 days in Table 7).
† During 70-day period in feed intake pens.
‡ At mean metabolic live weight.
Body and carcass composition
At equivalent carcass weight, there was more fat trim, less retail yield and there tended to be less bone in the carcass among the cattle grown rapidly compared with those grown slowly to weaning (Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006; Table 8). This suggests the greater fatness at weaning of the rapidly reared cattle persisted to 30 months of age. However, because of failure to compensate fully in weight, the carcasses from light weaners remained smaller and weight of retail beef was lower compared with the heavy weaners at the same age. When cattle grown rapidly or slowly to weaning were backgrounded to the same feedlot entry weight and slaughtered after 120 days in the feedlot, their carcasses did not differ in compositional and yield characteristics (Cafe et al., Reference Cafe, Hearnshaw, Hennessy and Greenwood2006a).
Table 8 Consequences of growth from birth to weaning for carcass characteristics of beef cattle at 30 months of age (adapted from Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006)
Abbreviation is: IMF = intramuscular fat.
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex/year cohort, sire-genotype and their interactions, with carcass weight as a covariate (linear and, where significant, quadratic) to predict means at equivalent carcass weight. Refer to Table 6 for growth characteristics of the cattle.
Earlier studies within pasture-based nutritional systems also failed to demonstrate substantial differences in body or carcass composition due to nutrition and growth from birth to weaning (Berge, Reference Berge1991; Hearnshaw, Reference Hearnshaw1997). These authors concluded that cattle from low pre-weaning nutrition groups generally have less fat than those from high pre-weaning nutrition groups, but if compared at a constant carcass weight, differences in fatness usually disappear. As a result, calves with lower weaning weights take longer to reach carcass specifications than heavier calves.
In contrast to the above findings, severe nutritional restriction to weaning that resulted in little growth post partum, followed by concentrate (high energy) feeding from weaning to slaughter resulted in greater fatness at the same live and carcass weights compared with cattle well nourished prior to weaning (Tudor et al., Reference Tudor, Utting and O’Rourke1980). Within the same study, cattle restricted or well nourished to weaning then grown on pasture to the same slaughter weight did not differ in composition. Factors likely to have contributed to increased fatness among the small compared with large weaners, which were subsequently fed concentrates, include the following: greater length of time on concentrate feed to reach the slaughter weight; greater weight-specific intake of nutrients following the nutritional restriction; a greater requirement for protein relative to energy at weaning and, hence, potential nutrient imbalance in the concentrate diet during the early post-weaning phase; and more limited capacity for lean tissue accretion post weaning in the small compared with large weaners.
Beef quality and myofibre characteristics
Differences in objective measurements of meat quality between cattle grown slowly or rapidly to weaning were not evident within our research (Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006; Table 9). Similarly, in earlier studies, objective measures of eating quality were not adversely affected by restricted nutrition prior to weaning (Hearnshaw, Reference Hearnshaw1997; Hennessy et al., Reference Hennessy, Morris and Allingham2001; Hennessy and Morris, Reference Hennessy and Morris2003). When they were affected, however, meat of cattle from low-nutrition groups was usually more tender than that of high-nutrition groups (Hearnshaw, Reference Hearnshaw1997; Hennessy et al., Reference Hennessy, Morris and Allingham2001). However, when compared at a constant carcass weight, in about half of the studies the meat quality differences became non-significant (Hearnshaw, Reference Hearnshaw1997). Despite these findings, meat quality may be compromised if the slow growth of cattle alter weaning results in them being at least 8 to 9 months older at slaughter weight (Loxton, Reference Loxton1997; Purchas et al., Reference Purchas, Burnham and Morris2002). It is unclear if similar age differences resulting from growth restriction earlier in life have similar effects.
Table 9 Consequences of growth from birth to weaning for objective measurements of m. longissimus (striploin) and m. semitendinosus (eye round) quality in beef cattle at 30 months of age (adapted from Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006)
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex, sire-genotype and their interactions. Refer to Tables 6 and 8 for growth and carcass characteristics of the cattle.
† Objective measures of texture, as defined by Perry et al. (Reference Perry, Shorthose, Ferguson and Thompson2001).
As with the above findings for meat quality, growth to weaning had little overall affect on myofibre characteristics in the longissimus lumborum muscle at 30 months of age, apart from a small increase in the relative area of type 1 myofibres in cattle grown slowly to weaning compared with those grown rapidly (Table 10). This is despite differences due to pre-weaning growth in the size of each myofibre type and the percentages and relative area of fast (type 2) myofibres at weaning (P. L. Greenwood, unpublished results).
Table 10 Consequences of growth from birth to weaning for longissimus lumborum myofibre characteristics of heifer beef cattle at 30 months of age (P. L. Greenwood and L. M. Cafe, unpublished results)
Abbreviation is: CSA = cross-sectional area.
Values are predicted means from residual maximum likelihood (REML) analyses including effects of birth weight, pre-weaning nutrition, sex, sire-genotype and their interactions. Refer to Lehnert et al. (Reference Lehnert, Byrne, Reverter, Nattrass, Greenwood, Wang, Hudson and Harper2006) for myofibre classification and measurement methodology. Type 1, type 1 myosin heavy chain (MHC) ≡ slow oxidative; Type 2C, intermediate between type 1 and type 2A; Type 2A, type 2A MHC ≡ fast oxidative-glycolytic; Type 2AX, intermediate between type 2A and type 2X; Type 2X, type 2X MHC ≡ fast glycolytic.
Interactions between in utero and pre-weaning growth
Among the numerous beef production characteristics that we investigated, the only interaction between growth in utero and growth prior to weaning was for the eye muscle (m. longissimus) cross-sectional area when compared at an equivalent carcass weight at 30 months of age (Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006). Cattle of low birth weight had a greater eye muscle area at slaughter than high-birth-weight cattle within the high pre-weaning growth group (91.1 v. 87.2 cm2), suggesting, perhaps, in conjunction with the results for subcutaneous fat depth, some long-term consequences of divergent foetal growth for distribution of carcass tissues. However, the eye muscle area did not differ due to birth weight within the animals that grew slowly to weaning (89.8 v. 90.5 cm2, respectively). Similarly, interactions between prenatal and pre-weaning nutrition for post-weaning growth, feed intake, feed efficiency and carcass characteristics were not evident in the study of Stalker et al. (Reference Stalker, Adams, Klopfenstein, Feuz and Funston2006).
Interactions between growth early in life and gender
There appear to be few studies of interactions between growth early in life and the gender of cattle on beef production characteristics. Growth of well nourished, artificially reared calves (Tudor and O’Rourke, Reference Tudor and O’Rourke1980) and feed efficiency after weaning have been shown to be influenced by gender following maternal nutritional restriction (Tudor and O’Rourke, Reference Tudor and O’Rourke1980). The results of Stalker et al. (Reference Stalker, Adams, Klopfenstein, Feuz and Funston2006) and Martin et al. (Reference Martin, Vonnahme, Adams, Lardy and Funston2007) also suggest differences between genders in the efficiency of nutrient utilisation following divergent maternal nutrition during late pregnancy. However, few interactions between gender and nutrition early in life have been demonstrated for subsequent body and carcass characteristics, with these relating mainly to bone growth (Tudor et al., Reference Tudor, Utting and O’Rourke1980). Within our recent studies, interactions between birth weight and gender/year cohorts were evident for carcass weight, eye muscle area, and weight of bones and retail beef at 30 months of age (Greenwood et al., Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006). However, while suggestive of interactions between sex and growth early in life, our experimental design did not allow for this interaction to be specifically tested.
Interactions between growth early in life and sire-genotype
A major objective of our research has been to determine the extent to which genotype may interact with nutrition early in life to influence subsequent growth, carcass, yield and beef-quality characteristics. To achieve this objective, our research included offspring of Piedmontese (a high muscling, high-birth-weight breed homozygous for a non-functional mutation in myostatin) and Wagyu (a high marbling and lower birth weight breed) bulls. Perhaps surprisingly, no interactions between sire-genotype and growth early in life were evident for any production parameters reported here or presented by Greenwood et al. (Reference Greenwood, Cafe, Hearnshaw, Hennessy, Thompson and Morris2006).
Conclusions
Severe, chronic growth retardation of cattle early in life is associated with reduced growth potential, resulting in smaller animals at any given age. The capacity for long-term compensatory growth diminishes as the age of onset of severe nutritional restriction resulting in prolonged growth retardation declines, such that more-extreme intrauterine growth retardation can result in slower growth throughout postnatal life. However, within the normal limits of beef production systems, neither restricted growth in utero nor from birth to weaning influences the efficiency of nutrient utilisation later in life.
Retail yield from cattle severely restricted in growth during pregnancy or from birth to weaning is reduced compared with cattle well grown early in life, when compared at the same age later in life. However, retail yield and carcass composition of low- and high-birth-weight calves are similar when compared at the same carcass weight.
At equivalent carcass weights, cattle that are grown slowly from birth to weaning have carcasses of similar or leaner composition than those grown rapidly. However, there is evidence to suggest that if high energy, concentrate feed is provided following severe growth restriction from birth to weaning, then at equivalent weights post weaning the slowly growing, small weaners may be fatter than their well-grown counterparts.
Restricted prenatal and pre-weaning nutrition and growth do not adversely affect measures of beef quality including shear force, compression, cooking loss and colour. Similarly, bovine myofibre characteristics are little affected in the long term by growth in utero or from birth to weaning, despite specific myofibre-type-related effects at birth and weaning, respectively.
Hence, economic benefits resulting from adequate maternal nutrition, especially during pregnancy, to optimise growth of offspring to market weights are primarily due to advantages in carcass weight and retail beef yield at a given age, reduced feed costs to reach a given market weight, stocking rates and subsequent reproductive rates of breeding cows, but not due to differences in beef-quality characteristics (Alford et al., 2007).
Interactions were not evident between prenatal and pre-weaning growth for subsequent growth, efficiency, carcass, yield and beef-quality characteristics, within our pasture-based production systems. Interactions between genotype and nutrition early in life studied using offspring of Piedmontese (a high muscling, higher birth weight breed, homozygous for a mutation that produces non-functional myostatin) and Wagyu (a high marbling, lower birth weight breed) sires mated to Hereford cows were not evident for any growth, efficiency, carcass, yield and beef-quality parameters.
We propose that within pasture-based production systems for beef cattle, the plasticity of the carcass tissues, particularly of muscle, allows animals that are growth-retarded early in life to attain normal carcass composition at equivalent weights in the long term, albeit at older ages. This may well relate to regulation of nutrient intake to a level appropriate for the size and lean tissue growth capacity of the animal, coupled with the capacity of the myosatellite cell population to generate myonuclei in support of muscle growth over a prolonged recovery period, as discussed previously (Greenwood et al., Reference Greenwood, Hunt, Hermanson and Bell1998, Reference Greenwood, Slepetis, Hermanson and Bell1999 and Reference Greenwood, Hunt, Hermanson and Bell2000a). However, the availability of feed and quality of nutrition during recovery from severe growth retardation early in life may be important in determining the subsequent composition of young, light-weight cattle relative to their heavier counterparts.
Finally, it needs to be emphasised that long-term consequences of more specific, acute environmental influences during specific stages of embryonic, foetal and neonatal calf development remain to be determined. This need for further research extends to consequences of nutrition and growth early in life for subsequent reproductive performance, which has been recently shown to be affected in heifers by nutrition of their dams during late pregnancy (Martin et al., Reference Martin, Vonnahme, Adams, Lardy and Funston2007), although neither reproductive or lactational performance were affected by birth weight (Swali and Wathes, Reference Swali and Wathes2006).
Acknowledgements
The contributions of Ms Helen Hearnshaw, Dr David Hennessy and Professor John Thompson in the conduct of research on consequences of growth and nutrition during early life of cattle described herein are most gratefully acknowledged. The financial and in-kind support of the Cooperative Research Centre for Cattle and Beef Quality, NSW Department of Primary Industries, CSIRO Livestock Industries and the University of New England is gratefully acknowledged. We also acknowledge the considerable efforts of research, technical and/or farm staff of NSW Department of Primary Industries Agricultural Research and Advisory Stations at Grafton and Glenn Innes and its Beef Industry Centre of Excellence in Armidale, at the Beef CRC ‘Tullimba’ Feedlot, at CSIRO Livestock Industries, Queensland Bioscience Precinct, St Lucia, and at the University of New England Meat Science Complex, in the conduct of the Beef CRC research described in this review.
