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Journal of Animal Science - Animal Physiology

Metabolic, endocrine, and reproductive responses of beef heifers submitted to different growth strategies during the lactation and rearing periods1

 

This article in JAS

  1. Vol. 93 No. 8, p. 3871-3885
     
    Received: Feb 09, 2015
    Accepted: May 26, 2015
    Published: July 24, 2015


    2 Corresponding author(s): jarodriguezs@aragon.es
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doi:10.2527/jas.2015-8994
  1. J. A. Rodríguez-Sánchez 2*,
  2. A. Sanz*,
  3. C. Tamanini and
  4. I. Casasús*
  1. * Unidad de Tecnología en Producción Animal. Centro de Investigación y Tecnología Agroalimentaria (CITA) de Aragón. Avda. Montañana, 930, 50059 Zaragoza, Spain
     Dipartimento di Scienze Mediche Veterinarie (DIMEVET), Università degli Studi di Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia (BO), Italy

Abstract

The effects of different feeding strategies (0.7 kg/d target ADG [LO] and 1.0 kg/d target ADG [HI] during the lactation period (LACT; 0–6 mo) and the rearing period (REAR; 6–15 mo; HI–HI, HI–LO, LO–HI, and LO–LO treatments) on the growth and reproductive parameters of beef heifers bred by fixed-time AI at 15 mo were analyzed. Animal weights were recorded weekly (from birth to 18 mo), and size measures were recorded at 6 and 15 mo. Heifers were bled to determine the onset of puberty and the metabolic and endocrine (IGF-I and leptin) status. During lactation, calves in the high lactation treatment (LactHI) had greater weight (P < 0.001), weight gain (P < 0.001), and body size (P < 0.001) than calves in the low lactation treatment (LactLO). The greater energy balance of LactHI heifers at weaning was reflected in greater concentrations of plasma glucose (P < 0.001), urea (P < 0.001), and IGF-I (P < 0.001); plasma levels of NEFA were lower (P < 0.001). During REAR, LactLO heifers had a greater growth rate than did LactHI heifers (P < 0.001), partially overcoming the lower gains during lactation. The differences in size measurements registered at weaning were also compensated, with the exception of LO–LO heifers. The IGF-I profile was highly correlated with animal performance traits and metabolic profiles, providing a useful indicator of growth, nutritional, and metabolic status at key points in development. By contrast, the function of leptin as an indicator of growth and reproductive development of heifers was less clear. All treatments had similar weights at puberty onset (55.9% mature BW), although LactLO (P < 0.01) and the low rearing treatment (RearLO; P < 0.001) heifers were older than the others. The animals with greater glucose and IGF-I levels at weaning and greater cholesterol concentrations during REAR reached puberty earlier. The fertility rate (86%) was similar among treatments. The heifers in the high rearing treatment (RearHI) required more AI services to become pregnant and were older at conception (P < 0.05). The age of conception was positively correlated with glucose (r = 0.57, P < 0.01) and cholesterol (r = 0.68, P < 0.001) at 9 mo. Our results show that a 0.7 kg/d gain from birth allowed the first breeding at 15 mo, 6 mo earlier than usual for these conditions, without any negative effect on heifer reproductive performance.



INTRODUCTION

The development of heifers is a key component of a beef production enterprise because it is crucial to future dam productivity. In systems based on seasonal feeding, it is not uncommon that first calving occurs at 30 to 36 mo of age (Le Cozler et al., 2010). Particularly in Spain and according to official data from Ministerio de Agricultura Alimentación y Medio Ambiente (MAGRAMA; 2014), approximately 50% of heifers are older than 3 yr at the first calving. This delay is due to the belief of farmers that earlier calving impairs future growth, production, and reproductive performance (Stygar et al., 2014). Additionally, because of the extensification of beef cattle production systems (García-Martínez et al., 2009) and/or the small herd size, replacement heifers are often managed with the rest of the herd and do not receive specific care to ensure optimal rearing.

The cost of rearing replacements could be reduced if heifers calved at 2 yr, if heifers reaching puberty before 12 to 13 mo, and if heifers had their first breeding at approximately 15 mo of age (Wathes et al., 2014). Optimum nutritional management is required to ensure the success of this strategy, and specific replacement programs have yet to be developed. The lifetime productivity of a cow begins at the onset of puberty and depends on subsequent critical events such as age at first breeding and calving and fertility rate (Diskin and Kenny, 2014). These aspects could be influenced by growth rates both before and after weaning, which depend on nutritional management. Therefore, different patterns of feeding may influence the metabolic and endocrine profiles during lactation and rearing, which, consequently, may modify development and reproductive performance (Brickell et al., 2009b).

The objective of this experiment was to evaluate the effects of different feeding strategies during the lactation period (LACT; 0–6 mo) and the rearing period (REAR; 6–15 mo) on the patterns of growth, onset of puberty, fertility rate, and metabolic (glucose, NEFA, cholesterol, β-hydroxybutyrate, and urea) and endocrine status (IGF-I and leptin) of beef heifers bred at 15 mo.


MATERIALS AND METHODS

The Animal Ethics Committee of the Centro de Investigación y Tecnología Agroalimentaria (CITA) approved the experimental procedures, which were in compliance with the guidelines of the European Union (Directive No. 86/609/CEE, 1986) on the protection of animals used for experimental and other scientific purposes.

Animals, Management, and Diets

The study was conducted at the CITA-La Garcipollera Research Station in the mountain area of the central Pyrenees (northeastern Spain; 42°37′ N, 0°30′ W, 945 m above sea level, mean annual temperature 10.2 ± 0.2°C, and mean annual rainfall 1,059 ± 68 mm) and at the CITA-Montañana Research Station (41°43′ N, 0°48′ W, 225 m above sea level, mean annual temperature 15.2 ± 0.2°C, and mean annual rainfall 318 ± 63 mm).

Sixty-two Parda de Montaña (selected from old Brown Swiss for beef purposes) multiparous cows (7.6 ± 3.5 yr) calved in autumn at CITA-La Garcipollera, but only female calves and their dams (29 pairs), were used for this study. At calving, cow–calf pairs were randomly assigned to 1 of the 4 feed management strategies in a 2 × 2 factorial experiment. Two growth rates were targeted in LACT (0–6 mo: 1.0 kg/d target ADG [HI] and 0.7 kg/d target ADG [LO] treatments, respectively) and 2 in REAR (6–15 mo; HI and LO treatments). The experimental design of the study, the diets supplied, and the resulting 4 treatments (HI–HI, HI–LO, LO–HI, and LO–LO) are presented in Fig. 1. The treatments were randomly balanced according to dam calving BW (580 ± 65 kg) and BCS (2.6 ± 0.1; Lowman et al., 1976) and to calf birth date (October 12 ± 13 d) and birth weight (41 ± 3 kg).

Figure 1.
Figure 1.

Experimental design with the treatment diets and the target ADG for each period and strategy.

 

The cow–calf pairs remained indoors throughout lactation in a loose housing system with straw-bedded pens. The dams were group-fed daily with 12 kg per animal of a total mixed ration (56% forage and 44% grains, with byproducts and vitamin and mineral supplements; 861 g/kg DM, 13.0 MJ ME/kg DM, 85 g CP/kg DM, and 499 g NDF/kg DM) to meet maintenance requirements for energy and protein in a 580-kg beef cow producing 9 kg of energy-corrected milk (ECM; NRC, 2000). The calves were kept in straw-bedded cubicles adjacent to their dams and were allowed to suckle twice daily for 30 min at 0800 and 1600 h. All heifers had access to fresh bed straw to ensure an adequate rumen development. To achieve the desired growth rates, heifers in the high lactation treatment (LactHI) had free access to starter concentrate (Table 1).


View Full Table | Close Full ViewTable 1.

Ingredients and composition of concentrate and alfalfa hay provided to heifers during the lactation (0–6 mo) and rearing (6–15 mo) periods1

 
Concentrate
Item Lactation Rearing Alfalfa hay
Ingredient (as-fed basis), %
    Corn 30.00 44.00
    Soybean flour 16.50 4.60
    Barley 15.50 21.60
    Corn gluten 15.00
    Extruded cereal 15.00
    Wheat bran 15.00
    Rapeseed flour 5.00
    Milk byproducts 3.00
    Beet pulp 2.00 3.00
    Palm oil 1.30 2.90
    Calcium carbonate 1.00 1.20
    Vitamin–mineral premix2 0.20 2.00
    Sodium chloride 0.50 0.20
    Urea 0.50
Nutrient composition
    DM, g/kg 894 900 851
    ME, MJ/kg DM 15.1 15.2 9.2
    CP, g/kg DM 166 147 98
    NDF, g/kg DM 214 252 462
1Lactation concentrate was provided ad libitum to heifers in the high lactation treatment. Rearing concentrate was provided in amounts of 12 g/kg BW to the high rearing treatment and 6 g/kg BW to the low rearing treatment heifers. Alfalfa hay was provided ad libitum in the rearing period to all heifers.
2 Vitamin A, 7,000 IU/kg; Vitamin D3, 1,500 IU/kg; Copper (cupric sulfate pentahydrate), 2 mg/kg; Iodine (potassium iodide), 0.5 mg/kg; Cobalt (cobaltous carbonate monohydrate), 0.5 mg/kg; Zinc (zinc oxide), 40 mg/kg; Manganese (manganese oxide), 30 mg/kg; Selenium (sodium selenite), 0.2 mg/kg; Iron (ferrous carbonate), 5 mg/kg; Butylhydroxytoluene, 2 mg/kg.

Before reaching 3 mo of age, the calves were vaccinated against infectious bovine rhinotracheitis (Bovilis IBR Marker; MSD Animal Health, Salamanca, Spain) and Clostridium perfringens (Polibascol; Schering-Plough, Kenilworth, NJ). At 6 mo (175 ± 13 d), the calves were weaned and transported to the CITA-Montañana facilities, where REAR was conducted. The heifers were housed indoors in a loose housing system with straw-bedded pens with fresh and clean water supplied ad libitum. To achieve the targeted weight gains, heifers were group-fed alfalfa hay ad libitum and 12 (the high rearing treatment [RearHI]) or 6 g concentrate/kg BW (the low rearing treatment [RearLO]) throughout this period (Table 1).

At 15 mo, a 90-d breeding season began (Fig. 2). One month before breeding, the heifers were vaccinated against bovine viral diarrhea (Bovilis BVD; MSD Animal Health). All heifers were synchronized at 15 mo with an Ovsynch + progesterone releasing intravaginal device (PRID) program (Fig. 2) in which they simultaneously received 1.55 mg of progesterone in a PRID (CEVA, Barcelona, Spain) and a 10-μg injection of GnRH (Busol; INVESA, Barcelona, Spain) followed 10 d later by 25 mg of prostaglandin F (Enzaprost; CEVA). After 12 d, the PRID was removed, and 500 IU of pregnant mare serum gonadotrophin (Foligon; Intervet, Salamanca, Spain) was administered followed 48 h later by a second injection of GnRH (10 μg). Eight hours after the final GnRH injection, the heifers were randomly inseminated from 1 of 4 bulls by an expert technician.

Figure 2.
Figure 2.

Synchronization protocol used in beef heifers at 15 mo of age managed with different feeding treatments. PRID = progesterone releasing intravaginal device.

 

After the first AI, estrus detection was recorded twice daily (0700 and 1900 h) until the end of the breeding season. The heifers were inseminated approximately 12 h after estrus was detected. Return to estrus after each AI was considered a diagnostic indicator of nonpregnancy status. Pregnancy was confirmed by ultrasonography (Aloka SSD-500V equipped with a linear-array 7.5 MHz transducer; Aloka, Madrid, Spain) 31 d after the end of the breeding season.

The day of the first timed AI was used to determine the age and BW at first breeding, and the day of the effective AI was used to determine the age and BW at conception. The first-service fertility rate was determined as the number of pregnant heifers at the first AI divided by the total number of heifers. The number of AI necessary to become pregnant was calculated considering only heifers that were pregnant at the end of the breeding season. The fertility rate was determined as the number of pregnant heifers in the breeding season divided by the total number of heifers.

Measurements and Blood Sampling

The dams were milked monthly during lactation to determine the quantity and composition of daily milk intake by calves using the oxytocin and machine milking technique (Le Du et al., 1979). The milk fat and protein were analyzed with an infrared scan (Milkoscan 4000; Foss Electric Ltd., Hillerod, Denmark), and these data were used to calculate ECM yield (adjusted to 3.5% fat and 3.2% protein content), as described by Casasús et al. (2004).

The starter concentrate intake of LactHI heifers was recorded by group daily. The feed refusal was removed and weighed weekly. Throughout REAR, concentrate intake was recorded by group daily and adjusted monthly by average group weight. The intake of alfalfa hay was recorded by pen at weekly intervals. The actual daily intake along the experiment was calculated as feed provided minus feed refused. Feed samples were collected at weekly intervals and were pooled on a monthly basis for chemical analyses. The samples were dried at 60°C until a constant weight and mill ground (1-mm screen) and DM, ash, ether extract, and CP (N × 6.25) contents were determined according to the Association of Official Analytical Chemists (1990; Method 942.05, 920.39, 968.06). Analyses of NDF, ADF, and ADL were conducted according to the sequential procedure of van Soest et al. (1991). All values were corrected for ash-free content.

The heifers were weighed once a week throughout the 18 mo of the experiment before morning feeding, without prior deprivation of feed and water. The weight at key points (3, 6, 9, 12, and 15 mo and puberty onset, first breeding, and conception) was calculated as the average of 3 consecutive weights. The ADG during LACT, REAR, and the birth-to-puberty period were calculated with linear regression of weight against time. The ADG at 3-mo intervals from birth to 15 mo were used for further analysis.

Body development was studied using size measurements at the end of LACT and REAR. The height at withers (from the highest point of the shoulder blade to the ground), rump length (from the ischial tuberosity to the iliac tuberosity), and rump width (the maximum distance between iliac tuberosities) were recorded with a height stick. The heart girth (the body circumference immediately posterior to the front legs) was measured with a flexible tape.

The heifers were bled monthly throughout the experiment to determine both metabolites and hormones. The blood samples were collected before morning feeding from the jugular vein during LACT and from the coccygeal vein during REAR. Additionally, heifers were bled weekly during REAR to determine the onset of puberty based on plasma progesterone concentration. The samples to determine progesterone, β-hydroxybutyrate, IGF-I, and leptin concentrations were collected into 9-mL heparinized tubes (Vacuette España S.A., Madrid, Spain). The samples to determine plasma glucose, NEFA, cholesterol, and urea concentrations were collected into 9-mL tubes containing EDTA (Vacuette España S.A., Madrid, Spain). Blood samples were centrifuged at 1,500 × g for 20 min at 4°C immediately after collection, and the plasma was harvested and frozen at –20°C until analysis.

Assays

Plasma progesterone concentrations were measured using an ELISA kit (Ridgeway Science, Lydney, UK), according to the manufacturer’s instructions. The mean intra- and interassay CV were 8.0 and 10.4%, respectively. The sensitivity was 0.27 ng/mL. The onset of puberty occurred when progesterone levels were ≥1.0 ng/mL in at least 2 consecutive samples (normal estrus cycle, ≥14 d; Álvarez-Rodríguez et al., 2010a). The age at puberty was defined as the date of collection of the first blood sample that contained ≥1.0 ng/mL of plasma progesterone. To ensure the continuation of estrous cycles, blood samples analyzed after the attainment of puberty were confirmed by the observation of at least 1 subsequent estrous cycle of normal duration, based on progesterone concentration. The first day of the synchronization protocol was used as the date for onset of puberty for prepubertal heifers.

Plasma concentrations of glucose (glucose oxidase/peroxidase method), cholesterol (enzymatic colorimetric method), β-hydroxybutyrate (enzymatic colorimetric method), and urea (kinetic UV test) were determined with an automatic analyzer (GernonStar; RAL/TRANSASIA, Dabhel, India). The reagents for glucose, cholesterol, and urea analyses were provided by the analyzer manufacturer (RAL, Barcelona, Spain), and the reagents for β-hydroxybutyrate were supplied by Randox Laboratories Ltd. (Crumlin Co., Antrim, UK). The mean intra- and interassay CV for these metabolites were <5.4 and <5.8%, respectively. The sensitivity was 0.056, 0.026, 0.030, and 0.170 mmol/L for glucose, cholesterol, β-hydroxybutyrate, and urea, respectively. The plasma NEFA were analyzed with an enzymatic method using a commercial kit (Randox Laboratories Ltd.). Commercial reference plasma samples (bovine precision serum; Randox Laboratories Ltd.) were used to evaluate the accuracy of the analyses. The mean intra- and interassay CV were 5.1 and 7.4%, respectively. The sensitivity was 0.060 mmol/L.

Circulating IGF-I concentrations were quantified with a solid-phase enzyme-labeled chemiluminescent immunometric assay (Immulite; Siemens Medical Solutions Diagnostics Limited, Llanberis, Gwynedd, UK). The mean intra- and interassay CV were 3.1 and 12.0%, respectively. The sensitivity was 20 ng/mL.

Plasma leptin concentrations were determined by RIA with a multispecies commercial kit (Multispecies Leptin Ria kit; LINCO Research, St. Charles, MO). The mean intra- and interassay CV were 3.54 and 6.87%, respectively. The sensitivity averaged 1.30 ng/mL.

Statistical Analyses

All data were analyzed as a completely randomized design with the SAS statistical software package (SAS Inst. Inc., Cary, NC). The heifer was the experimental unit. Data for BW and metabolic (glucose, NEFA, cholesterol, β-hydroxybutyrate, and urea) and endocrine (IGF-I and leptin) profiles collected at 3-mo intervals (3, 6, 9, 12, and 15 mo) were analyzed using the SAS MIXED procedure for repeated measures. The covariance structure was selected on the basis of the lowest Akaike information criterion. Therefore, an unstructured covariance matrix was used for the analysis of repeated measures, which included feeding treatment at lactation and rearing phases, time, and their interaction as fixed effects and with heifer as the random effect in a univariate linear mixed model.

The ADG (during LACT, REAR, and the birth-to-puberty period and at 3-mo intervals from birth to 15 mo) and size measurements (height at withers, heart girth, and rump width and length at 6 and 15 mo of age) were tested with ANOVA using the GLM procedure. The feeding treatment during LACT and REAR and their interaction were fixed effects. Similar analyses were performed to analyze the age and weight at puberty, at the first AI, and at conception and number of AI necessary to become pregnant. The fertility rate was analyzed using the FREQ procedure of SAS (χ2 test). Pearson’s correlation coefficients between variables were calculated using the CORR procedure of SAS. Means were separated using the LSMEANS procedure of SAS. For all tests, the level of significance was P = 0.05.


RESULTS AND DISCUSSION

Growth Performance

The development of BW with time is shown in Fig. 3, and the ADG in each period is displayed in Table 2. During the lactation phase, LactHI heifers had greater ADG than the heifers in the low lactation treatment (LactLO; 1.063 vs. 0.672 kg/d, respectively; P < 0.001) and, consequently, were heavier at weaning (228 vs. 164 kg, respectively; P < 0.001). Being that the dam milk yield throughout lactation was similar in LactHI and LactLO feeding treatments (mean ECM yield: 7.66 vs. 7.81 kg/d, respectively; P > 0.10), the provision of concentrate ad libitum (mean intake: 1.26 DM kg/d) caused the differences in LactHI heifers. This result occurred both in the first half of lactation (0–3 mo; 0.892 vs. 0.711 kg/d in LactHI and LactLO heifers, respectively; P < 0.001) and, more intensively, in the second half (3–6 mo; 1.234 vs. 0.651 kg/d in LactHI and LactLO heifers, respectively; P < 0.001). The gains observed during the first 3 mo of age in the LactLO heifers were similar to those described in calves without supplements of the same breed under similar conditions by Álvarez-Rodríguez et al. (2009, 2010b). The larger difference in the later stage of lactation was most likely caused by the increased intake of concentrate from 0.20 kg/d in the first month to 3.45 kg/d in the sixth month, which provided greater intake of both energy and protein for LactHI heifers (Fig. 4). The increase in rate of concentrate intake was similar to that described by Blanco et al. (2008a) for suckling calves from birth to the fifth month of lactation under similar conditions.

Figure 3.
Figure 3.

Development of heifer weight throughout the experiment according to the feed management applied in the lactation (0–6 mo) and rearing (6–15 mo) periods. LO = 0.7 kg/d target ADG; HI = 1.0 kg/d target ADG.a a–dMeans at a given age with different superscripts differ significantly (P < 0. 05).

 

View Full Table | Close Full ViewTable 2.

Rate of weight gain (kg/d) of heifers from birth to first breeding according to the feed management applied in the lactation period (LACT) and the rearing period (REAR)

 
LACT (0–6 mo)
P-value
LO1
HI1
REAR (6–15 mo)
LACT REAR LACT × REAR
Item LO HI LO HI SEM
ADG LACT 0.643b 0.699b 1.046a 1.080a 0.03 <0.001 0.18 0.72
ADG REAR 0.744c 0.998a 0.593d 0.925b 0.05 <0.001 <0.001 0.10
ADG birth to puberty 0.680c 0.863b 0.833b 1.085a 0.02 <0.001 <0.001 0.14
a–dMeans within a row with different superscripts differ significantly (P < 0.05).
1LO = 0.7 kg/d target ADG; HI = 1.0 kg/d target ADG.
Figure 4.
Figure 4.

Estimated energy and protein intake by heifers with different nutrition treatments during the lactation (0–6 mo) and rearing (6–15 mo) periods. LO = 0.7 kg/d target ADG; HI = 1.0 kg/d target ADG.

 

As shown in Table 2, the gains during REAR were significantly influenced by feeding treatment during LACT (P < 0.001) and REAR (P < 0.001), with no significant interaction between them (P > 0.10). In the rearing phase, gains were influenced by previous performance during lactation, and LactLO heifers had a compensatory response that resulted in greater rate of gain than that of LactHI heifers (0.870 vs. 0.759 kg/d, respectively; P < 0.001), which partially corrected the lower gains in the previous phase. The compensatory growth was more intense in the first 2 trimesters of REAR (ADG at 6–9 mo: 0.649 vs. 0.767 kg/d in LactHI and LactLO heifers, respectively; P < 0.01; ADG at 9–12 mo: 0.899 vs. 1.002 kg/d in LactHI and LactLO heifers, respectively; P < 0.01), whereas in the last trimester, gains in both groups were similar (ADG at 12–15 mo: 0.849 vs. 0.891 kg/d in LactHI and LactLO heifers, respectively; P > 0.10). Because the average intake of concentrate (2.90 kg/d) and alfalfa hay (6.10 kg/d) was similar for the 2 treatments, the feed conversion efficiency might have been greater in the LactLO heifers that displayed compensatory growth (Hoch et al., 2005). Despite this greater rate of growth, compensation was not complete in the LactLO treatment, and the large differences in weight at weaning remained to some extent at 15 mo (455 vs. 414 kg in LactHI and LactLO heifers, respectively; P < 0.01; Fig. 3).

The gains in REAR were also influenced by feeding treatment in this phase, with greater gains in RearHI than RearLO heifers (0.960 vs. 0.668 kg/d, respectively; P < 0.001). This difference is expected to result from greater intake of energy and protein by RearHI heifers, except for the last third of REAR (Fig. 4).

The size measurements at 6 and 15 mo are shown in Table 3. The greater BW and growth rate of LactHI heifers at weaning resulted in larger size, and LactLO heifers showed compensatory growth in some of the parameters during the rearing.


View Full Table | Close Full ViewTable 3.

Size measures of heifers (cm) at 6 and 15 mo of age according to feed management applied in the lactation period (LACT) and the rearing period (REAR)

 
LACT (0–6 mo)
LO1
HI1
P-value
REAR (6–15 mo)
Item LO HI LO HI SEM LACT REAR LACT × REAR
Height at withers
    6 mo 98.0c 99.0b 103.9bc 104.6a 1.8 0.004 0.64 0.94
    15 mo 118.6b 122.8a 120.1ab 122.0ab 1.4 0.78 0.04 0.42
Heart girth
    6 mo 124.3b 127.9b 141.9a 143.8a 2.1 <0.001 0.24 0.78
    15 mo 168.0d 182.9b 173.3c 188.6a 1.7 0.002 <0.001 0.79
Rump width
    6 mo 29.7b 29.9b 32.9a 34.8a 0.8 <0.001 0.20 0.28
    15 mo 41.3b 46.5a 45.6a 45.4a 0.8 0.05 0.004 0.002
Rump length
    6 mo 32.5b 32.9b 36.1a 37.5a 1.0 <0.001 0.41 0.64
    15 mo 43.4b 47.4a 46.3a 48.0a 0.7 0.02 <0.001 0.14
a-cMeans within a row with different superscripts differ significantly (P < 0.05).
1LO = 0.7 kg/d target ADG; HI = 1.0 kg/d target ADG.

The height at withers in cattle is primarily a composite of the long bone measurement of the forelimb and is a good indicator of skeletal development. The height at withers at 6 mo was significantly affected by the lactation feeding treatment, and LactHI heifers were taller than LactLO heifers (104.2 vs. 98.5 cm, respectively; P < 0.01). This difference was compensated for during REAR (121.1 vs. 120.7 cm in LactHI and LactLO heifers at 15 mo, respectively; P > 0.10), although compensation was not complete for the LO–LO heifers, which remained smaller than their counterparts. The compensation in size was larger than that for BW, which confirmed the results of Swali et al. (2008), who reported that animals are less able to compensate for weight than for skeletal growth. Concomitantly, the relationship between height at withers and BW in our work was stronger at 6 mo (r = 0.81, P < 0.001) than at 15 mo (r = 0.46, P < 0.05). Therefore, our results show that height at withers is a better indicator of animal development and size than BW, consistently with previous works (Heinrichs et al., 1992; Le Cozler et al., 2010).

The heart girth provides an indirect measure of the development of the gastrointestinal tract and liver. In the current study, heart girth was influenced by feeding treatment in both LACT and REAR (P < 0.001). At 6 mo, LactHI heifers had greater heart girth than LactLO heifers (142.8 vs. 125.8 cm, respectively; P < 0.001), which was not fully compensated for after the rearing phase. Similarly, at the end of REAR, RearHI heifers showed greater heart girth than RearLO heifers (185.5 vs. 170.6 cm at 15 mo, respectively; P < 0.001). These results confirmed those reported by Abeni et al. (2012), who found differences in heart girth but not in height at withers after REAR. In the current work, strong and positive relationships between heart girth and weight both at 6 (r = 0.98, P < 0.001) and 15 mo were found (r = 0.98, P < 0.001), which confirmed that this measure provides an accurate indirect measure of BW. A similar relationship was found at weaning between heart girth and the immediately previous ADG (3–6 mo; r = 0.90, P < 0.001). However, at 15 mo of age, the relationship of this measure with the previous ADG (12–15 mo) was weaker (r = 0.58, P < 0.01) than at 6 mo.

The rump width and length provide an estimate of the internal pelvic area, which can influence the incidence and degree of calving difficulty in primiparous heifers. The rump width at weaning was affected by lactation treatment (33.8 vs. 29.8 cm in LactHI and LactLO heifers, respectively; P < 0.01). However, an interaction (P < 0.001) was found between feed treatments applied in LACT and REAR; at 15 mo of age, the rump width in HI–HI and HI–LO heifers did not differ, but those of LO–LO and LO–HI did (Table 3). Similarly, LactHI heifers had longer rumps at weaning (36.8 vs. 32.7 cm in LactHI and LactLO heifers, respectively; P < 0.001), and LO–LO heifers did not reach a similar rump length as their counterparts at 15 mo (Table 3).

All size measurements were positively correlated with each other at key points in time (6 and 15 mo). This relationship was stronger at weaning (r ≥ 0.69 among the different traits, P < 0.001) than at 15 mo (r ≥ 0.32, P < 0.05), perhaps because bone growth is maximal in the first year of life and ceases once the growth plates in the long bones and pelvic region have fused; therefore, compensation at a later date is not possible for poor early skeletal development (Wathes et al., 2014).

In summary, heifer BW at 15 mo was different among treatments because of the different ADG in both lactation and rearing feeding treatments. The LactLO heifers compensated for the lower weight gains in lactation during REAR and for body size as well, except for heifers that remained in a low feed treatment.

Reproductive Performance

The results for reproductive performance are presented in Table 4. All heifers were pubertal before the breeding season, except for 3 heifers from the LO–LO treatment. The heifers reached puberty at a similar BW (324 ± 35 kg), which was 55.9% of the expected mature BW, considering the mature BW described for this breed (580 kg; Casasús et al., 2002). The weight at puberty was similar to that described by Revilla et al. (1992) for Parda de Montaña heifers with ADG from birth to puberty similar to the LO-LO heifers herein. Moreover, these results confirm that puberty is reached at a critical BW (Schillo et al., 1992). This critical BW depends on the breed and is approximately 55% of mature BW for a wide range of breeds (Freetly et al., 2011), particularly for dual-purpose beef–dairy breeds (Larson, 2007; Diskin and Kenny, 2014), such as Parda de Montaña.


View Full Table | Close Full ViewTable 4.

Reproductive performance according to feed management applied in the lactation period (LACT) and the rearing period (REAR)

 
LACT (0–6 mo)
LO1
HI1
P-value
REAR (6–15 mo)
Item LO HI LO HI SEM LACT REAR LACT × REAR
Weight at puberty, kg 330.6 313.7 326.2 328.8 14.18 0.71 0.62 0.50
Age at puberty, mo 13.5a 10.2bc 11.3b 9.2c 0.52 0.005 <0.001 0.26
Percent MBW2 at puberty 57.0 54.1 56.2 56.3 0.02 0.75 0.56 0.53
Pubertal heifers3 4/7 8/8 7/7 7/7 0.08 0.06
Weight at first AI, kg 388.1d 464.5b 424.8c 513.1a 12.03 0.001 <0.001 0.62
Age at first AI, mo 15.8 15.6 15.7 15.9 0.15 0.67 0.93 0.26
Conception BW, kg 382.3d 486.2b 431.7c 530.2a 11.36 <0.001 <0.001 0.71
Conception age, mo 15.9b 16.7a 15.9b 16.4ab 0.25 0.55 0.02 0.64
Number of AI 1.20b 2.25a 1.33b 1.67a 0.30 0.49 0.04 0.27
Fertility at first AI 4/7 2/8 4/7 3/7 0.58 0.19
Fertility 5/7 8/8 6/7 6/7 0.94 0.25
a–dMeans within a row with different superscripts differ significantly (P < 0.05).
1LO = 0.7 kg/d target ADG; HI = 1.0 kg/d target ADG.
2MBW = mature BW.
3Pubertal heifers is the number of heifers pubertal at first day of the synchronization protocol.

The age at the onset of puberty was significantly affected by the feeding treatments applied in LACT (10.3 vs. 11.9 mo in LactHI and LactLO heifers, respectively; P < 0.01) and REAR (9.7 vs. 12.4 mo in RearHI and RearLO heifers, respectively; P < 0.001); therefore, faster growing heifers reached puberty earlier. The age at puberty showed a strong negative correlation with ADG of heifers from birth to the onset of puberty (r = –0.75, P < 0.001), as was also described by Patterson et al. (1992). Considering the different phases, the age of puberty was correlated with gains in LACT (r = –0.50, P < 0.01) but not after weaning (weaning to puberty; r = –0.30, P = 0.12). Other studies also reported that the age of puberty was affected by energy intake during lactation, whereas feeding treatments during REAR did not exert a major effect (Wiltbank et al., 1966; Gasser et al., 2006; Cardoso et al., 2014). The current study shows that feed management in the earlier juvenile period is critical and supports the idea that the timing at onset of puberty can be nutritionally programmed by promoting high weight gains during targeted periods of heifer development (Amstalden et al., 2014).

Two months before the breeding season, 90% of heifers were pubertal, thus achieving one of the main objectives of the replacement programs. In these programs, heifers should reach puberty 30 to 45 d before the breeding season (Gasser, 2013), because the fertility rate can be increased by up to 21% from the first to the third estrus (Byerley et al., 1987). In the current experiment, only 3 LO–LO heifers were not pubertal at the start of the breeding season, despite having optimal BW to reach puberty (>55% of mature BW).

As shown in Table 4, the weight at the first AI and at conception in all groups was affected by feeding treatment in LACT (P < 0.001) and REAR (P < 0.001). However, all treatments had weights at the first AI that were greater than 65% of the expected mature BW (381 kg), which complied with previous recommendations (Perry, 2012; Gasser, 2013). Because all heifers were inseminated at the same time, no differences were found in age at the first AI. However, the age at conception was influenced by the feeding treatment during rearing (P < 0.05), with RearHI heifers older than RearLO heifers (16.5 vs. 15.9 mo, respectively; P < 0.05), because they needed more AI services to become pregnant (1.96 vs. 1.27 AI in RearHI and RearLO heifers, respectively; P < 0.05). This result supports the findings by Brickell et al. (2009a) and Summers et al. (2014), who reported that the fastest growing heifers required more services per conception. Funston et al. (2012) also found that developing obese heifers increased the number of services required for conception by 7% compared with leaner animals. In our work, the inclusion of the PRID in the synchronization protocol most likely induced ovulation in the 3 heifers that were not pubertal, which became pregnant at the first AI.

In the current study, no differences were found in fertility rate at the first AI and over the entire breeding season, as has been described in many other works (Funston and Deutscher, 2004; Roberts et al., 2009; Eborn et al., 2013; Summers et al., 2014).

In summary, the onset of puberty was attained at similar BW but different ages depending on the growth pattern during the LACT and REAR, and the onset of puberty occurred in 90% of animals at least 2 mo before targeted breeding at 15 mo. The faster-growing heifers came into puberty earlier, but they required more AI services per conception. At the end of the breeding season, the pregnancy rate did not differ among treatments.

Metabolic Profiles

Circulating glucose, NEFA, cholesterol, β-hydroxybutyrate, and urea are indicators generally associated with ruminant energy metabolism, which were useful to characterize nutritional status of growing heifers in the current study. The profiles throughout the experiment are presented in Fig. 5.

Figure 5.
Figure 5.

Plasma concentrations of glucose, NEFA, cholesterol, β-hydroxybutyrate and urea in beef heifers with different nutrition treatments in the lactation (0–6 mo) and rearing (6–15 mo) periods. LO = 0.7 kg/d target ADG; HI = 1.0 kg/d target ADG. a–cMeans at a given age with different superscripts differ significantly (P < 0. 05).

 

The plasma glucose profile was affected by the lactation treatment (P < 0.001), with differences at weaning (6.42 vs. 4.75 mmol/L in LactHI and LactLO heifers, respectively; P < 0.001). These differences disappeared during REAR, and all treatments had similar glucose levels at 15 mo. The glucose concentration during LACT was greater than during the rearing phase (5.59 vs. 4.75 mmol/L in the LACT and REAR, respectively; P < 0.001), and the levels at the end of each period were greater than those described in other studies on dairy (Swali et al., 2008; Brickell et al., 2009b) and beef heifers (Cappellozza et al., 2014). The greater glucose levels of LactHI heifers at weaning were most likely caused by the intake of concentrate, which increased the propionate available from ruminal fermentation to be metabolized into glucose (Agle et al., 2010; Samadi et al., 2014). By contrast, the lower nutrient intake of LactLO heifers led to lower plasma glucose concentrations, as observed in other studies (Chelikani et al., 2004; Brickell et al., 2009b; Le Cozler et al., 2010).

In the current work, plasma glucose concentration at weaning was highly correlated to the previous ADG (3–6 mo; r = 0.77, P < 0.001), as described by other authors (Vizcarra et al., 1998; Cappellozza et al., 2014). The plasma glucose concentration was also significantly (P < 0.05) correlated with all skeletal measurements, as Swali et al. (2008) also observed, with correlation values (r) ranging from 0.46 (rump height) to 0.71 (heart girth). The strong relationship with heart girth confirmed the findings of Brickell et al. (2009b), who found that this parameter defines intake and digestive capacity and is thus related to metabolites reflecting intake, such as glucose and urea. This relationship for both ADG and size measurements was not evident at the end of REAR in the current work. The plasma glucose at weaning was negatively correlated with age at puberty (r = –0.50, P < 0.01), as Brickell et al. (2009a) also described, most likely because glucose is the primary source of energy for ovarian function and a major modulator of LH secretion (Bucholtz et al., 1996). In our study, the number of services per conception was positively correlated with the plasma glucose concentration at 9 mo of age (r = 0.57, P < 0.01). As glucose is an indicator of energy balance, this result is consistent with other studies reporting that more services are necessary in faster growing (Brickell et al., 2009a; Summers et al., 2014) and obese heifers (Funston et al., 2012).

The plasma NEFA concentrations were significantly affected by the treatment during lactation but opposite to the effect observed for plasma glucose (0.200 vs. 0.442 mmol/L in LactHI and LactLO heifers at weaning, respectively; P < 0.001). This opposite could be caused by the lower estimated energy intake by LactLO heifers during lactation (Fig. 4), because NEFA levels are inversely related to the level of nutrition (Chelikani et al., 2009). Moreover, NEFA are released into circulation as a result of fat mobilization and lipid catabolism, and therefore, the increased NEFA concentrations indicate a lower energy balance in LactLO heifers. This relation explains the negative relationship between ADG and NEFA at weaning (r = –0.59, P < 0.01), which was also described in other works (Bell, 1995; Yelich et al., 1995; Blanco et al., 2011). Concomitantly, a negative relationship between NEFA and glucose concentrations was found at weaning (r = –0.78, P < 0.001). The NEFA concentrations were also negatively correlated with height at withers (r = –0.53, P < 0.01) and heart girth (r = –0.56, P < 0.01) at 6 mo, which indicate that animals with greater energy balance were larger, but this relationship disappeared at 15 mo. No relationship between NEFA concentrations at weaning and the rump measurements was found, but at 15 mo of age, rump width (r = –0.52, P < 0.01) and rump length (r = –0.47, P < 0.05) were inversely correlated with NEFA levels, thus indicating that heifers with a lower energy balance were less developed at the end of REAR.

The plasma cholesterol concentration was affected significantly by time (P < 0.001), with the highest values at weaning (3.966 ± 0.192 mmol/L) and the lowest values at 12 mo of age (1.310 ± 0.103 mmol/L), and overall, greater concentrations were found during LACT than during REAR (3.487 vs. 1.993 mmol/L, respectively; P < 0.001). The observed range of this metabolite was slightly wider than that previously described in Parda de Montaña adult cows (Álvarez-Rodríguez and Sanz, 2009).

In contrast with the previous metabolites, feed management did not influence plasma cholesterol levels during lactation (P > 0.05). During REAR, significantly greater concentrations were found in RearHI than in RearLO heifers both at 9 (2.896 vs. 2.054 mmol/L, respectively; P < 0.001) and at 15 mo of age (2.440 vs. 1.952 mmol/L, respectively; P < 0.05). Throughout the experiment, plasma cholesterol and glucose concentrations were positively correlated (r = 0.61, P < 0.001) because cholesterol level depends on the glucose concentration (Ndlovu et al., 2007); both metabolites indicate a positive energy balance.

As the heifers reach sexual maturity, the ovaries become functional and increase progesterone production, with cholesterol uptake as the main source for the synthesis of steroid hormones (Yart et al., 2014). Therefore, the lower level of plasma cholesterol during REAR could be explained by the negative relationship with plasma progesterone, a relationship also described by Talavera et al. (1985). Moreover, a negative relationship between plasma cholesterol concentration and age at onset of puberty was found (r = –0.56, –0.50, and –0.49 at 9, 12, and 15 mo, respectively; P < 0.01). The cholesterol concentration decreased with the onset of puberty, but a minimum level might be necessary to reach puberty. Similar to plasma glucose, at 9 mo of age, cholesterol was positively correlated with number of services needed per conception (r = 0.68, P < 0.001).

Plasma β-hydroxybutyrate is a ketone body synthesized in the liver after adipose tissue catabolism and is commonly used to indicate a short-term negative energy balance (Ndlovu et al., 2007). In the current study, β-hydroxybutyrate was not influenced by management treatments, but it was significantly affected by time (P < 0.001) and increased from a low level at 3 mo of age until a plateau was reached at 12 mo (0.117 ± 0.012 and 0.261 ± 0.013 mmol/L, respectively). The high levels observed at 12 mo could be a response to the decrease in plasma glucose concentration at 12 mo (Lean et al., 1992).

The treatment during lactation had a major effect on urea concentrations (5.570 vs. 4.129 mmol/L in LactHI and LactLO calves at weaning, respectively; P < 0.001). This was explained by the greater protein intake of LactHI calves receiving the concentrate (Fig. 4), because circulating urea is positively correlated with dietary protein intake (Walsh et al., 2008; Kelly et al., 2010). In REAR, the only differences were found at 9 mo of age, when urea levels were greater in LO–LO heifers (5.999 ± 0.500 mmol/L; P < 0.05) than in the other heifers (4.356 ± 0.500 mmol/L), which might indicate a deficit of energy intake and an increase in breakdown of endogenous proteins for energy production (Chimonyo et al., 2002). The plasma urea concentration was also significantly influenced by time (P < 0.001) and increased throughout the experiment from 3.635 ± 0.150 mmol/L at 3 mo to 7.673 ± 0.403 mmol/L at 15 mo of age.

The plasma urea concentration at weaning was positively correlated with BW (r = 0.71, P < 0.001), previous ADG (3–6 mo; r = 0.76, P < 0.001), and glucose (r = 0.66, P < 0.001) and was negatively correlated with NEFA (r = –0.53, P < 0.01). These relationships suggest that LactHI heifers had a greater energy balance and more protein available to increase BW faster, as Hall et al. (1995) suggested, and would confirm the diagnostic value of urea as an indicator of energy and protein intake (Brickell et al., 2009b; Abeni et al., 2012). Similar to glucose, plasma urea concentrations at weaning had positive significant (P < 0.05) relationships with all size measurements, and the estimated correlation coefficients ranged from 0.43 (height at withers) to 0.72 (heart girth); the relationships were not observed at 15 mo.

In summary, plasma glucose, NEFA, and urea concentrations showed the greatest differences between treatments at weaning, when the estimated energy and protein intake were most markedly different according to the feed management. By contrast, plasma cholesterol levels differed more during REAR. Our results provide evidence that these metabolites are responsible for some of the underlying mechanisms regulating growth and reproductive development and are accurate indicators of the nutritional status of heifers.

Endocrine Profiles

The profiles of plasma IGF-I and leptin during the experiment are presented in Fig. 6. The concentrations of IGF-I were significantly different between feed treatments during lactation. The concentrations increased 2.7-fold from 3 to 6 mo of age in LactHI heifers (106.0 vs. 288.9 ng/mL, respectively; P < 0.001), concomitantly with the intake of concentrate, as Blanco et al. (2008b) described for similar conditions. In the LactLO heifers, the IGF-I concentration remained stable throughout lactation, most likely because milk intake at weaning was not sufficient to support potential growth rates for Parda de Montaña calves (Blanco et al., 2008b). Moreover, other studies showed that with feed restrictions, the age-related increase in IGF-I concentrations of calves was attenuated (Elsasser et al., 1989; Hayden et al., 1993; Blanco et al., 2009).

Figure 6.
Figure 6.

Plasma concentrations of IGF-I and leptin in beef heifers with different nutrition treatments in the lactation (0–6 mo) and rearing (6–15 mo) periods. LO = 0.7 kg/d target ADG; HI = 1.0 kg/d target ADG. a,bMeans at a given age with different superscripts differ significantly (P < 0. 05).

 

As shown in Fig. 6, IGF-I concentrations declined immediately after weaning in LactHI heifers, whereas they increased in LactLO heifers but then were similar among treatments thereafter. These profiles reflected the compensatory growth shown by heifers in the 6 to 9 mo period, which confirmed that IGF-I concentration is a good indicator of growth at particular points in time (Cabaraux et al., 2003; Blanco et al., 2009). In REAR, IGF-I concentrations were lower than those of feedlot cattle of similar age but fed high-concentrate diets (Blanco et al., 2010), which was reflected in lower ADG.

The concentration of IGF-I at weaning was positively correlated with BW (r = 0.78, P < 0.001), as Kerr et al. (1991) also described, and with previous ADG (3–6 mo; r = 0.80, P < 0.001), as reported also by Blanco et al. (2009). Simultaneously, the concentration of IGF-I was positively correlated with glucose (r = 0.78, P < 0.001) and urea (r = 0.63, P < 0.001) concentrations and was negatively correlated with NEFA (r = –0.57, P < 0.01) concentration, which reflected the response of IGF-I concentration to nutritional status (Cabaraux et al., 2003). The greater energy and protein intake by LactHI heifers at the end of LACT led them to synthesize more glucose and urea and to reach greater ADG, which was reflected in greater IGF-I levels. By contrast, LactLO heifers had a lower energy balance at weaning, greater NEFA concentrations, lower weight gains, and lower IGF-I levels. Concurrently, all size parameters were positively correlated with IGF-I at weaning (r ranged from 0.59 to 0.78, P < 0.001), as described in earlier works (Brickell et al., 2009b), which reinforced the key role of IGF-I in the control of body growth as a regulator of skeletal and muscle development in growing cattle (Yelich et al., 1995).

At 9 mo of age, IGF-I concentration was 36.7 ng/mL greater in RearHI heifers than in RearLO heifers (169.2 vs. 132.5 ng/mL, respectively), although the difference was not significant (P > 0.10). A negative relationship between IGF-I level at 9 mo and age at onset of puberty was found (r = –0.54, P < 0.01). Plasma IGF-I was described as a major metabolic mediator involved in the onset of puberty in heifers that could be delayed by low levels of IGF-I (Velazquez et al., 2008), whereas greater concentrations could trigger an earlier start of ovarian function (Yelich et al., 1995, 1996). Furthermore, IGF-I in the juvenile period was associated with subsequent cow longevity (Swali et al., 2008), and therefore, IGF-I has predictive value.

In the current work, the mean plasma concentration of IGF-I was affected by time throughout the experiment and increased as heifers became older (from 146.0 ± 12.3 ng/mL to 210.1 ± 11.9 ng/mL at 3 and 15 mo of age, respectively; P < 0.001), most likely because of an increment in nutrient intake, as suggested by Blanco et al. (2008b). Furthermore, IGF-I concentrations in the current study were greater than those described for the same breed in the postpartum period of primiparous and multiparous cows (71.8 and 54.7 ng/mL, respectively; Álvarez-Rodríguez et al., 2010a).

The circulating leptin was influenced only by the sample date (P < 0.01) and increased from the lactation to the rearing phase (2.04 vs. 2.48 ng/mL, respectively; P < 0.01). This age-related increment was due to the increase in deposition of fat (Geary et al., 2003), because leptin is a key metabolic signal synthesized by fat cells that communicates information about body energy reserves, nutritional state, and metabolic shifts to reproductive axis (Hausman et al., 2012). Unexpectedly, however, the concentration of leptin did not differ among treatments at any of the key points in time (Fig. 6).

Plasma leptin concentrations did not differ among treatments as puberty approached, and there was no evidence of a prepubertal increase. These results are in contrast with other studies that reported a linear prepubertal increase in plasma leptin concentrations in both beef (Garcia et al., 2002, 2003) and dairy (Díaz-Torga et al., 2001) heifers. Although leptin was proposed as a crucial hormone in determining the timing of puberty (Garcia et al., 2002, 2003), leptin might not be a critical trigger for puberty in rapidly growing heifers, as Lents et al. (2013) have suggested. However, a certain threshold of leptin levels appears important for puberty (Cooke et al., 2013), particularly in heifers with normal or restricted growth rates (Chelikani et al., 2009), to ensure sufficient nutritional reserves to support the transition to puberty.

In summary, plasma IGF-I concentrations differed between feeding strategies at weaning and were associated with a wider range of estimated energy and protein intakes. The IGF-I profile was highly correlated with animal performance traits and metabolic profiles and provided a good indicator of growth, nutritional, and metabolic status at given key points in heifer development. Although plasma leptin levels were age related, concentrations were similar in all treatments throughout the study.

In the current experiment, both lactation and rearing feeding treatments resulted in different growth patterns. As a result, the onset of puberty was attained at a similar BW (55.9% of mature weight) but at a different age, with faster-growing heifers reaching puberty earlier but requiring more AI services to conceive. However, the fertility rate did not differ among treatments at the end of the 90-d breeding season. The profiles of plasma glucose, NEFA, urea, and IGF-I were particularly different at weaning, when the ranges of energy and protein intake were larger, whereas cholesterol differed more among treatments in REAR, most likely because of its role as steroid hormone precursor. Therefore, these parameters were excellent indicators of growth, nutritional, and metabolic status at particular key points in time. By contrast, the function of leptin in growth and reproductive development of heifers was less clear. Our results demonstrated that even a 0.7 kg/d gain from birth until breeding allowed the first breeding to be 6 mo earlier than usual for these conditions, without any negative effect on heifer reproductive performance. However, additional research is necessary to determine the impacts of the different growth strategies on size at maturity, production, reproductive performance at first and subsequent calvings, and lifespan of early-bred heifers.

 

References

Footnotes


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