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. 2023 Oct 1;101:skad330. doi: 10.1093/jas/skad330

Effects of early weaning on the reproductive performance of suckled Nelore cows in the subsequent breeding season

Thiago Kan Nishimura 1, Amanda Guimarães da Silva 2, Gabriela Abitante 3, Carl Robertson Dahlen 4, Rodrigo Silva Goulart 5, Germán Darío Ramírez Zamudio 6, Saulo Luz Silva 7, Miguel Henrique de Almeida Santana 8, Arlindo Saran Netto 9, Paulo Roberto Leme 10, Guilherme Pugliesi 11,✉
PMCID: PMC10642726  PMID: 37777868

Abstract

This study aimed to evaluate the effects of early weaning (EW) on body composition, hormone concentrations and metabolites, and reproductive performance of Nelore cows in the subsequent breeding season (BS). Suckled cows that became pregnant by timed-AI (TAI) in the 2020-BS were exposed in 2021 to early weaning at 150 d (27 primiparous [PRI] and 74 multiparous [MUL]) or conventional weaning (CW) at 240 d postpartum (30 PRI and 77 MUL). Body weight (BW) and body condition score (BCS) were determined at 2020-BS, EW, CW, prepartum, and 2021-BS. Blood samples were collected at EW, CW, prepartum (54.75 ± 0.56 d prepartum), and 2021-TAI and assayed for insulin-like growth factor-1 (IGF-I), non-esterified fatty acid (NEFA), and β-hydroxybutyrate (BHB) concentrations. In 2021-BS, cows were exposed to a P4/E2-based protocol for TAI at day 0 (D0), and a second TAI was performed at D22 in females detected with luteolysis (D20) by Doppler ultrasound. The presence of corpus luteum (CL) on D10, estrous expression, and dominant follicle (DF) diameter, and blood perfusion (BP) on D2 and D0 were determined. Data were analyzed by ANOVA or logistic regression of SAS as a 2 × 2 factorial with main factors of parity (PRI or MUL) and weaning strategy (EW or CW). An interaction of parity and weaning strategy was not observed (P > 0.1), but the weight (kg) and BCS were greater (P < 0.05) in MUL cows at the five timepoints, and EW cows were heavier than CW at the moment of CW (541 vs. 493 kg; and 5.3 vs. 4.3), prepartum (551 vs. 506 kg; and 5.2 vs. 4.4) and 2021-BS (475 vs. 450 kg; and 4.5 vs. 3.7). Plasma urea concentration at 2021-BS was greater (P = 0.01) for PRI than for MUL. A parity-by-time interaction was observed (P ≤ 0.05) for concentrations of IGF-I, NEFA, and BHB. PRI cows had greater (P ≤ 0.05) concentrations of IGF-I at EW and greater (P ≤ 0.05) prepartum concentrations of NEFA and BHB than MUL cows. The proportion of cows with CL at D10 was not affected (P > 0.1) by weaning but was greater (P < 0.05) in MUL than in PRI cows (40.4 vs. 15.7%). The diameter of DF and proportion of BP on D0 were greater (P < 0.05) in EW cows than in CW cows. The pregnancy rate (P/AI, %) at the first TAI was greater (P < 0.05) in EW cows (60% vs. 45%), whereas no difference (P > 0.1) was observed at the second TAI. Cumulative P/AI (first and second TAIs) was greater (P < 0.05) in EW cows (81% vs. 63%). In conclusion, weaning at 150 d in Nelore cattle is a strategy to successfully recover the parous cow’s body condition and to improve pregnancy success in the next BS, regardless of the cow’s parity order.

Keywords: Beef cattle, body condition score, metabolic status, nutritional status, multiparous cows, primiparous cows

Early weaning improves the recovery of body condition score and metabolic status and benefits the reproductive performance of suckled Nelore cows in the subsequent breeding season.

Introduction

iIn beef production systems, several factors can affect the reproductive performance of suckled cows. One of the most important factors is the duration of postpartum anestrus, which can extend over 4 mo (Yavas and Walton, 2000). The anestrous period is normally longer in suckled Nelore (Bos indicus) cows than in Bos taurus cows (Abeygunawardena and Dematawewa, 2004) and is affected by body condition score (BCS), nutrition status, and presence of a suckling calf (Short et al., 1990; Abeygunawardena & Dematawewa, 2004; Baruselli et al., 2004). Beef herds in tropical conditions commonly use extensive management based on areas of pastures with limited forage quality and quantity during the dry period of the year. Therefore, nutrient availability in subtropical pastures likely does not meet the cow’s metabolic and energetic requirements, resulting in a prolonged period of postpartum anestrous (Samadi et al., 2013).

The time of weaning is an important factor related to postpartum anestrus. Providing a longer suckling period can benefit the calf growth but increases the energy requirements and may decrease the BCS and reproductive performance of the dam (Restle et al., 2001; Vaz et al., 2010; Wiseman et al., 2019). As a consequence of lactation, suckled cows have greater energy requirements, and most enter a period of negative energy balance (NEB) after parturition. In most Brazilian beef production systems, the herd is comprised of B. indicus breeds, and calves are commonly weaned at 8 mo of age. This provides a short time for the dam to recover body energy reserves before parturition and in the next breeding season (BS) and also coincides with a major energy demand to accommodate the exponential growth of a late-gestation fetus (Bauman and Bruce Currie, 1980). In addition, primiparous cows have a greater energy demand than multiparous because additional nutrients are required for continued body growth (NRC, 2016). Consequently, a more extended anestrous period and reduced reproductive efficiency are observed in primiparous cows (Sá Filho et al., 2009, 2013; Sales et al., 2016). Therefore, the association between low energy availability and high energy demand in primiparous cows managed in a system that used conventional weaning (CW; up to 8 mo) may reduce reproductive performance in the subsequent breeding season.

Nutritional strategies have been developed after parturition to overcome the NEB. Supplementation with energetic and protein feed during the periparturient period has been proven to benefit dams’ metabolic status and reproductive performance (Da Silva et al., 2017; Fellipe et al., 2020). However, these strategies are confounded by innate energy use priorities that partition a portion of the energy consumed towards milk production and maternal tissue recovery (Reynolds and Tyrrell, 2000). Alternatively, studies in B. taurus beef cattle have suggested that early weaning (EW) of suckling calves eliminates the nutrient demands of lactation, allowing body condition and fat reserves to recover before parturition (Arthington and Kalmbacher, 2003; Vaz et al., 2010; Wiseman et al., 2019). In timed artificial insemination (TAI) programs, the BCS at birth and at the time of breeding is positively associated with pregnancy rates (Meneghetti & Vasconcelos, 2008; Ayres et al., 2014). It is plausible, that early weaning could enhance fertility in the subsequent breeding season, especially in B. indicus beef cattle in pastures during the dry period of the year.

In the herein study, we aimed to compare the effect of two periods of weaning (150 d vs. 240 d) on the reproductive performance of the Nelore dams (primiparous and multiparous) in the subsequent breeding season. We hypothesized that early weaning at 150 d would increase the reproductive performance of Nelore cows in extensive grazing conditions compared with conventional weaning at 240 d.

Material and Methods

The experiment was approved by the ethics committee of the School of Animal Science and Food Engineering of the University of São Paulo (CEUA No.: 2884250620) and was conducted at the campus of Pirassununga—SP of the University of São Paulo.

Animals and experimental design

Cows that calved in 2019 and became pregnant to one of two TAI in 22 d using semen from three sires during the 2020 breeding season (2020-BS; November 2020 to January 2021) were used. A total of 57 suckling primiparous and 151 multiparous cows were randomized according to the sex of suckling calves, BCS, sire, and sex of the fetus to receive one of two weaning strategies: 1) early weaning at 150 d (average: 149 ± 2.0) of age (EW; n = 27 primiparous and 74 multiparous); or 2) conventional weaning at 240 d (average: 247 ± 2.4) of age (CW; n = 27 primiparous and 77 multiparous).

According to the calving date, cow–calf pairs were allocated into seven breeding groups, ranging from 40 to 50 pairs each. Each group arrangement was kept on Brachiaria ssp pastures with ad libitum access to water and a protein supplement containing 30.12% crude protein and 42.00% total digestible nutrient (1 g/kg of body weight [BW]/animal/d) during the dry season (April to September) or a protein supplement containing 26.12% crude protein and 50.50% total digestible nutrient (1g/kg of BW/animal/d) during the wet season (October to March). Beginning at 90 d of age, only calves had access to supplemental creep-feed (separate creep area (5 × 10m) and 2.5 linear meters of bunk space) targeting an average consumption of 5 g/kg of BW of the supplement providing daily (26.30% of crude protein and 80.70% of total digestible nutrients, on dry matter).

Weaning was done abruptly at each respective weaning time, involving the permanent separation of the calf from the dam (Enríquez et al., 2011). After weaning, cows were maintained in the same breeding groups until the subsequent calving and breeding seasons (2021).

In the 2021 breeding season (2021-BS), all suckled cows were submitted to two consecutive TAIs, between 30 and 60 d postpartum, and were exposed to a natural mating with a single bull per breeding group for at least 30 d after the second TAI ­(Figure 1). The length of pregnancy (conception at TAI to birth) and calves’ birth weight during 2021 birth season were recorded to evaluate a subsequent performance on the next birth season the calves’ birth moment related to the beginning of the 2022 birth season (day of the first calf born) was evaluated.

Figure 1.

Figure 1.

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Schematic of experimental design to evaluate the reproductive performance of Nelore cows exposed to early (150 d) or conventional (240 d) weaning strategies in the previous production cycle. Abbreviations: BCS, body condition score; BS, blood samples; RFT, rump fat thickness; US OV, ovary ultrasonography; PD, pregnancy diagnosis; TAI, timed artificial insemination.

Body condition score, body weight, and body composition

Measures of BCS (scale of 1 to 9, which 1 [emaciated] and 9 [obese]) (Wagner et al., 1988) and BW were determined at five-time points: at the beginning of the TAI protocol in the 2020 breeding season (2020-TAI), at 150 d when calves were removed from cows on early weaning treatment (EW), at 240 d when calves were removed from cows on the conventional weaning treatment (CW), 30 to 40 d before anticipated parturition (prepartum), and at the beginning of the first TAI protocol (day 10 = D10; D0 = first TAI) in 2021 breeding season (2021-TAI). Data for average daily gain (ADG) was calculated for the four intervals: Period 1: the interval from 2020-TAI to EW; Period 2: the interval from EW to CW; Period 3: the interval from CW to prepartum; Period 4: the interval from prepartum to 2021-TAI.

Rump fat thickness (RFT) was evaluated at EW (150 d), CW (240 d), and prepartum. Images were obtained by placing the transducer at the intersection of the gluteus media and biceps femoris muscles located between the hip and pin bones. The RFT was evaluated by a single operator with ultrasound equipment Aloka SSD 500 Micrus (Aloka Co. Ltd.), with a 3.5-MHz linear transducer and 172 mm length.

Pregnant shrunk body weight (SBWp), non-pregnant shrunk body weight (SBWnp), and pregnancy components (PREG) were calculated according to the models described by (Gionbelli et al., 2015; Lopes et al., 2020), where PREG = gravid uterus plus udder accretion during the pregnancy (GUdp) + weight of udder of a pregnant cow minus the udder weight of the cow in a non-pregnant condition (UDdp), being GUdp = increase of the gravid uterus during pregnancy, which corresponds to the difference between the weight of the gravid uterus and the weight of the uterus in the non-pregnant condition; and UDdp = increase in udder weight during pregnancy, which corresponds to the difference in weight of the udder of the pregnant cow and the estimated weight of the udder in the non-pregnant condition. The SBW corresponds to the estimated body mass of the cow free of digesta; SBW was initially calculated in the pregnant condition, where: SBWp = 0.8084 × BWp1.0303, where BWp = body weight of the pregnant cow. The SBW of a non-pregnant cow corresponds to the difference between the SBWp and the PREG (SBWnp = SBWp − PREG; Gionbelli et al., 2015; Lopes et al., 2020).

Blood samples

Blood (~10 mL) was collected at EW (150 d), CW (240 d), prepartum, and 2021-TAI by jugular venipuncture into evacuated tubes (BD Vacutainer, São Paulo, Brazil) containing sodic heparin as an anticoagulant. Tubes were placed ­immediately on ice until processing. Tubes were centrifuged at 2,800 × g for 15 min at 4°C, and two aliquots (1.5 mL) of plasma were frozen at −20 °C until analysis for non-esterified free fatty acids (NEFA), β-hydroxybutyrate (BHB), urea, and insulin-like growth factor-1 (IGF-I).

Concentrations of BHB and NEFA were performed using commercial kits (Randox Laboratory, Crumlin, UK) in an autoanalyzer biochemistry system (Cobas Mira, Roche Diagnostics, GmbH, Mannheim, Germany), by enzymatic colorimetric endpoint method, according to the guidelines provided by the manufacturer. Concentrations of plasma urea were measured by a colorimetric test using an automated analyzer (Mindray BC-2800 Vet, China) and a commercial kit (Labtest, Ref. 104-4). Concentrations of IGF-I were evaluated using a chemiluminescent assay obtained by Dimension EXL 200 Integrated Biochemistry system with an IMMULITE 1000 commercial IGF-I kit (Siemens Healthcare Diagnostics, Munich, Germany), and the intra-assay coefficient of variation and sensitivity were, respectively, 2.68% and 20 ng/mL.

Reproductive management

For the first TAI on the 2021-BS, all cows underwent an ovulation synchronization protocol (10 d of length; day of TAI = D0). On D10, cows received intravaginal progesterone (P4), releasing a device with 0.96 g P4 (Progestar, Biogénesis-Bagó Animal Ltda, Curitiba, Paraná, Brazil) and 2 mg estradiol benzoate (i.m., Bioestrogen, Biogénesis-Bagó Animal Ltda). Cows were examined by transrectal ultrasonography, and those with a corpus luteum (CL) in their ovary received 150 μg D-Cloprostenol (i.m., Croniben, Biogénesis-Bagó Animal Ltda). On D2, the P4 device was withdrawn, and cows received an administration of 150 μg D-Cloprostenol (i.m., Croniben, Biogénesis-Bagó Animal Ltda), 300 IU equine chorionic gonadotropin (i.m., Ecegon, Biogénesis-Bagó Animal Ltda), and 1 mg estradiol cypionate (i.m., Croni-Cip, Biogénesis-Bagó Animal Ltda). Cows were also painted with chalk marker halfway between the hip and tail head as an estrus detection aid. On D0 (48 h after P4 device withdrawal), cows were submitted to TAI by a single, experienced technician with thawed semen from one of three sires, which were equally disturbed among the experimental groups. The condition of the chalk on D0 was used as an indication of estrus, and cows with ≥50% of chalk removed were considered in estrus.

Twelve days after the first TAI (D12), cows were submitted to a resynchronization protocol, according to Pugliesi et al. (2019). On day 12 (D12), all cows received an intravaginal P4-releasing device with 0.96 g of P4 (Progestar) and 1 mg estradiol benzoate (i.m., Bioestrogen). On D20, an early diagnosis of non-pregnancy was performed by color-Doppler ultrasonography (Mindray Z5 Vet, Shenzhen, China) with a linear multi-frequency B-mode transducer (frequency 7.5 MHz; D 6.5; gain 71; FR 22; DR 120) and in Doppler mode (5.7 MHz; gain 72; WF 260; PRF 0.7 kHz). Cows with a functional CL (≥25% of blood perfusion [BP]) were considered potentially pregnant (Pugliesi et al., 2019) and had the intravaginal P4 device removed, and no further treatment was administered. For non-pregnant cows (having a CL with <25% BP), the resynchronization protocol was continued by P4 device removal and administration of 300 IU equine chorionic gonadotropin (i.m., Ecegon) and 1 mg estradiol cypionate (i.m., Croni-Cip). Also, on D20, non-pregnant cows were painted with chalk marker as previously described. On D22 (48 h after device withdrawal), cows were inseminated, and the conditions of the chalk were evaluated as previously described. The confirmatory diagnosis of pregnancy was conducted by transrectal ultrasound, between 30 and 40 d after the first and second TAIs, by visualization of an embryo with heartbeats. Pregnancy loss was considered as the number of pregnant cows in the confirmatory diagnosis that did not calve during the 2022 birth season.

Ultrasound scanning and endpoints

Ovarian structures were evaluated by a single operator by transrectal ultrasonography (Mindray Z5 Vet, Shenzhen, China) with a linear multi-frequency B-mode transducer (frequency 7.5 MHz; D 6.5; gain 71; FR 22; DR 120) and in Doppler mode (5.7 MHz, gain 72, WF 260; PRF 0.7 kHz). On D10, ovaries were evaluated as previously reported by Nishimura et al., (2018), and cows were characterized in three scores (1 to 3) according to the ovarian structures: score 1, presence of follicles < 8 mm; score 2, presence of follicles ≥ 8 mm; and score 3, presence of a CL. On D2 and D0, the diameter of the largest follicle was calculated by the average of the maximum length and width using the caliper function. On D0, BP was measured in the largest follicle with the color Doppler and assigned a percentage value according to the visualized proportion of the follicular wall with signals of BP (Siddiqui et al., 2009).

At the time of P4 device insertion for the resynchronization protocol (D12), cows were evaluated to detect the presence of a CL, indicating the effectiveness of the ovulation protocol. At the time of P4 device removal (D20), non-pregnant cows had the diameter of the largest follicle measured by the mean of the maximum length and width using the caliper function. On D22, the diameter of the largest follicle was measured for all cows submitted for a second AI.

The ovulation rate was calculated based on the proportion of inseminated cows with CL present on D12. The proportion of cows with an active CL on D20 was calculated based on the number of cows with a functional CL over the number of cows inseminated. Pregnancy per TAI (P/AI) from the first and second TAIs was calculated based on the number of animals with an embryo with heartbeats over the number of cows inseminated. The cumulative pregnancy rate was calculated based on the number of cows diagnosed as pregnant in the confirmatory diagnoses after the first and second TAIs over the total number of cows exposed to the TAI program. The potential embryonic loss (between D20 and D30 to D35) was considered as the number of cows without a viable embryo in the confirmatory pregnancy diagnosis (D30 to D35) over the number of cows with active CL on D20.

Statistical analyses

All statistical analyses were performed using SAS (version 9.2, SAS Institute Inc., Cary, NC USA). The experiment was conducted as a factorial 2 × 2 (dam’s parity [primiparous and multiparous] and weaning strategy [early and conventional weaning]). The continuous dependent variables (age, weight, body condition score, follicular size, follicular BP, metabolite concentrations, length of pregnancy, calves’ birth weight [2021 birth season], and calves’ birth moment [2022 birth season]) were evaluated for the normality of the residuals by the Shapiro–Wilk test and homogeneity of variance by Levene’s test. When the raw data did not follow a normal distribution, data were transformed into natural logarithms or ranked. Data were analyzed by ANOVA using PROC MIXED considering the effects of dam’s parity, weaning strategy, and their respective interaction. For the length of pregnancy, calves’ birth weight, and calves’ birth moment the sex of calve was also included in the model.

All the continuous data for BCS, body weight, RTF, and concentrations of metabolites were analyzed for the effects of dam’s parity, weaning strategy, time, and their respective interactions. The PROC MIXED procedure of SAS was used with a REPEATED statement to account for autocorrelation between sequential measurements. The LSD was used when comparisons between times were made within a treatment group or among more than two means.

The dependent variables (estrus, intensity of estrus, presence of CL on D12, pregnancy diagnosis on D20, ovulation before TAI, P/AI, pregnancy loss, and potential embryonic loss) were analyzed by the GLIMMIX procedure using a binomial distribution. For the presence of CL on D12, P/AI, potential embryonic loss, and the occurrence of estrus, the initial statistical model was composed of the fixed effects of dam’s parity, weaning strategy, sire, and their respective interactions. For the random effects, dam’s parity (primiparous and multiparous) and weaning strategy (early and conventional weaning) were considered. Therefore, the final models for CL on D12, P/AI, potential embryonic loss, and occurrence of estrus included only the effects of dam’s parity, weaning strategy, and dam’s parity by weaning strategy interaction. Results were expressed as mean ± SEM. Significant differences were declared at P ≤ 0.05, and a tendency was declared when P ≤ 0.1 and P > 0.05.

Results

Measures of performance, body condition, and maternal tissue adjustments

A significant triple interaction of weaning strategy, dam’s parity, and time was not detected for any endpoint evaluated. Cow’s body weight was impacted by dam’s parity-by-time interaction (P = 0.004) and weaning strategy by time interaction (P < 0.0001). The dam’s parity-by-time interaction revealed that multiparous cows had greater body weight at each evaluation time point and that the body weight of both parity classes increased from the 2020 breeding season until the prepartum time point and decreased from prepartum until the 2021 breeding season (Figure 2). The weaning strategy by time interaction indicated that EW and CW cows presented no difference at EW moment, but at the time of conventional weaning and continuing for the duration of the evaluation period EW cows were heavier than CW (Figure 2).

Figure 2.

Figure 2.

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Mean ± SEM of body weight and body condition score in primiparous and multiparous Nelore cows that were weaned at early (150 d of age) or at conventional (240 d of age) time points during the previous production cycle. Main effects of weaning strategy (W), dam’s parity (D), time (T), and interactions (W*T and D*T) that were significant or approached significance are shown. *Indicates difference (P < 0.05) in weight among times. a,b,c,d,e Within a group, means without a common letter differed (P < 0.05).

Cow’s body condition score was impacted by dam’s parity-by-time interaction (P < 0.001) and weaning strategy by time interaction (P < 0.0001). The dam’s parity-by-time interaction revealed that multiparous cows had greater BCS than primiparous cows at 2020-TAI, time of conventional weaning, prepartum, and 2021-TAI. (Figure 2). The weaning strategy by time interaction revealed that EW and CW cows presented no difference at EW moment, but had greater BCS than CW cows beginning at the time of conventional weaning, and this difference persisted for the duration of the evaluation period (Figure 2).

Cow’s pregnant and non-pregnant shrunk body weight and pregnant compounds were impacted by dam’s parity-by-time interaction and weaning strategy by time interaction (Figure 3). The dam’s parity-by-time interaction revealed that multiparous cows had greater pregnant shrunk body weight (±55.6 kg), non-pregnant body weight (±53.6 kg), and pregnant compounds (±2.1 kg) at each evaluation time point and that the body weight of both parity classes increased from the 2020 breeding season until the prepartum time point (Figure 3). The weaning strategy by time interaction indicated that EW cows had greater pregnant shrunk body weight (±23 kg), non-pregnant body weight (±21.5 kg), and pregnant compounds (±1.4 kg) than CW cows beginning at the time of conventional weaning, and continuing until prepartum (Figure 3).

Figure 3.

Figure 3.

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Mean ± SEM of pregnant shrunk body weight, non-pregnant shrunk body weight, and pregnant compounds in primiparous and multiparous Nelore cows that were weaned at early (150 d of age) or at conventional (240 d of age) time points during the previous production cycle. Main effects of weaning strategy (W), dam’s parity (D), time (T), and interactions (W*T and D*T) that were significant or approached significance are shown. *Indicates difference (P < 0.05) in weight among times. a,b,c,dWithin a group, means without a common letter differed (P < 0.05).

Cow’s ADG was impacted by parity-by-time interaction (P < 0.0001) and weaning strategy by time interaction (P < 0.0001). The dam’s parity-by-time interaction revealed that multiparous cows had greater ADG from 2020-TAI to 150 d and from 240 d to prepartum than primiparous cows (Figure 4). The weaning strategy by time interaction revealed that EW cows had greater ADG (0.529 ± 0.03 kg/d) than CW cows (0.067 ± 0.03 kg/d) during the interval from 150 to 240 d, but CW cows (–0.534 ± 0.03 kg/d) had greater ADG during the interval from prepartum until the 2021-TAI compared with early-weaned cows (–0.690 ± 0.04 kg/d) (Figure 4). For the overall ADG (from 2020-TAI to 2021-TAI), a weaning strategy by dam’s parity interaction or the main effect of dam’s parity was not detected, but a greater (P < 0.0001) ADG was observed in EW cows (0.174 ± 0.01 kg/d) than CW cows (0.121 ± 0.01 kg/d).

Figure 4.

Figure 4.

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Mean ± SEM average daily gain (ADG) in primiparous and multiparous Nelore cows that were weaned at early (150 d of age) or at conventional (240 d of age) time points during the previous production cycle. Main effects of weaning strategy (W), dam’s parity (D), time (T), and interactions (W*T and D*T) that were significant or approached significance are shown. Upper panel: Main effects of dam’s parity-by-time interaction (D*T). Different uppercase letters indicate difference between time and dam’s parity (P < 0.05) in ADG in primiparous cows. Different lowercase letters indicate difference between dam’s parity-by-time (P < 0.05) in ADG in multiparous cows. Bottom panel: Main effects of weaning strategy by time interaction (W*T). *Indicates difference (P < 0.05) in ADG among times in between dam’s parity (Upper panel), and between weaning strategy (Bottom panel).

Cow’s rump fat thickness was impacted by dam’s parity-by-time interaction (P < 0.004) and weaning strategy by time interaction (P < 0.0001). The dam’s parity-by-time interaction revealed that multiparous cows had greater RFT than primiparous cows at the time of conventional weaning and before parturition. The weaning strategy by time interaction revealed that the RFT at the time of early weaning did not differ but was greater in EW cows at the subsequent evaluation at 250 d and prepartum compared with CW cows (Figure 5). The calves’ birth weight during the 2021 birth season was affected by the dam’s parity by calf sex interaction (P = 0.02), and by calf sex (P < 0.0001). The dam’s parity by calf sex interaction revealed that female calves from multiparous cows (34.57 ± 0.47 kg) were heavier than calves from primiparous cows (32.55 ± 0.85 kg). The calf sex effect revealed that male calves were heavier (37.21 ± 0.47 kg) than female calves (24.03 ± 0.42 kg). The gestational period was affected only by calf sex (P = 0.0004); male calves had a longer gestational period (294.01 ± 0.55 d) than female calves (291.58 ± 0.47).

Figure 5.

Figure 5.

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Mean ± SEM rump fat thickness in primiparous and multiparous Nelore cows that were weaned at early (150 d of age) or at conventional (240 d of age) time points during the previous production cycle. The main effects of weaning strategy (W), dam’s parity (D), time (T), and interactions (W*T and D*T) that were significant or approached significance are shown. Main effects of weaning strategy by time interaction (W*T). *Indicates difference (P < 0.05) in RFT among times between weaning strategy. a,b,cWithin a group, means without a common letter differed (P < 0.05).

Concentrations of metabolites

A significant triple interaction of weaning strategy, dam’s parity, and time was not detected for any metabolite analyzed. An interaction of dam’s parity-by-time was detected for the NEFA and BHB concentrations (P = 0.002), ­revealing that primiparous cows had a greater concentration of NEFA at the prepartum blood collection than multiparous cows (Figure 6). The concentration of BHB was greater in multiparous cows at EW and CW but reduced at prepartum compared with primiparous cows (Figure 6). The weaning strategy did not affect the NEFA and BHB concentrations (P = 0.9).

Figure 6.

Figure 6.

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Mean ± SEM plasma NEFA, BHB, Urea, and IGF-I concentration in primiparous and multiparous Nelore cows that were weaned at early (150 d of age) or at conventional (240 d of age) time points during the previous production cycle. Main effects of weaning strategy (W), dam’s parity (D), time (T), and interactions (W*T and D*T) that were significant or approached significance are shown. *Indicates difference (P < 0.05) in weight among times. a,b,cWithin a group, means without a common letter differed (P < 0.05).

Concentrations of urea were affected by dam’s parity (P = 0.01) and time (P < 0.0001). Primiparous cows had greater concentrations of urea than multiparous cows (averaged: 13.5 ± 0.5 ng/mL vs. 12.4 ± 0.8 ng/mL; Figure 6). Concentrations of urea decreased from EW to CW, then increased at prepartum and followed by a decrease at postpartum (Figure 6). The weaning strategy did not affect the urea concentration (P = 0.9).

The concentration of IGF-I was affected by a dam’s parity-by-time interaction (P < 0.0001), with multiparous cows having reduced concentrations of IGF-I at the time of EW compared with primiparous cows (Figure 6). A main effect (P = 0.02) of the weaning strategy was observed, indicating a greater concentration of IGF-I in EW cows (136.6 ± 4.7 ng/mL) than in CW cows (111.5 ± 4.7 ng/mL) concentration over time. Although a treatment-by-time interaction only approached significance (P = 0.07), when each moment was evaluated separately, a difference between treatment groups was only observed at CW and postpartum moment (Figure 6).

Ovarian and estrous manifestation responses

The ovarian score and proportion of cows with CL on D10 were not affected by a weaning strategy by dam’s parity interaction (P ≥ 0.7) or by the main effect of the weaning strategy (P = 0.4; Table 1). However, multiparous cows had greater ovarian scores (P = 0.02) and a proportion of CL on D10 (P = 0.001) than primiparous cows.

Table 1.

Ovarian characteristics and estrus expression in primiparous and multiparous for Nelore cows that were weaned at early (150 d of age) or at conventional (240 d of age) time points during the previous production cycle.

Early Conventional Probability
Primiparous
(n = 27)		 Multiparous
(n = 74)		 Primiparous
(n = 30)		 Multiparous
(n = 77)		 Weaning strategy (W) Dam parity (D) W*D
Ovarian structures at D10 (1 to 3)a 2.1 ± 0.08 2.3 ± 0.06 2.1 ± 0.07 2.3 ± 0.06 0.4 0.02 0.7
Ovary score 3 on D10, % 18.5 41.8 13.3 38.9 0.5 0.001 0.7
Ovary score 1 on D10, % 3.7 2.7 3.3 7.7 0.5 0.7 0.4
Estrous expression at D0, % 94.1 75.6 78.9 65.9 0.13 0.07 0.4
Dominant follicle diameter at D2, mmb 12.2 ± 0.41 12.8 ± 0.29 12.0 ± 0.41 11.8 ± 0.29 0.13 0.66 0.29
Dominant follicle diameter at D0, mmb 14.1 ± 0.42 14.1 ± 0.30 13.3 ± 0.50 13.1 ± 0.30 0.04 0.83 0.76
Follicular blood perfusion at D0, %c 0.3 ± 0.02 0.3 ± 0.01 0.2 ± 0.03 0.2 ± 0.01 0.01 0.67 0.81
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P values that were significant are in bold.

aOvary structures were evaluated at D10 and classified in three scores 1 to 3. Score 1: presence of follicle <5 mm; score 2: the presence of follicle >8 mm; and score 3: the presence of CL.

bMeasured by taking the mean of the maximum length and width using the caliper function.

cFollicle blood perfusion of the dominant follicle at TAI moment.

The diameter of the largest follicle on D2 was not affected by the weaning strategy (P = 0.1), dam’s parity (P = 0.6), or weaning strategy by dam’s parity interaction (P = 0.2). The diameter of the largest follicle on D0 and the follicular wall BP was not affected by parity (P = 0.8), but EW cows had a larger dominant follicle (DF; P = 0.04) with greater BP (P = 0.01) than CW cows. The expression of estrus was not affected by the weaning strategy (P = 0.1); however, a greater proportion of primiparous cows tended (P = 0.07) to display estrus than multiparous cows (Table 1).

Pregnancy and birth responses

The P/AI at first TAI was not affected (P = 0.6) by the dam’s parity (primiparous, 54.3%, 31/57 vs. multiparous, 51.6%, 78/151), but EW cows (60.4%) had greater (P = 0.02) pregnancy rate than CW cows (44.8%; Figure 7). The P/AI at the second TAI was not affected (P = 0.4) by dam’s parity (multiparous; 43% vs. primiparous; 34%) or weaning strategy (P = 0.2). The cumulative P/AI (first and second TAIs) was not affected (P = 0.8) by dam’s parity (primiparous, 70%, 40/57 vs. multiparous, 72.8%, 110/151), but EW cows (81.1%) had greater (P = 0.001) cumulative pregnancy rate than CW cows (63.5%). Pregnancy by natural mating was affected only by the dam’s parity (P = 0.03), primiparous cows had a greater pregnancy rate than multiparous cows (35.71% vs. 16%). The overall rate of pregnancy loss between the pregnancy diagnosis and the 2022 birth season was 8.00% (12/150) and was not affected by the dam’s parity, weaning strategy, or interaction.

Figure 7.

Figure 7.

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Proportion (%) of pregnant Nelore cows after first TAI and second TAI, or cumulative pregnancy rate [1stTAI + 2ndTAI] in early and conventional groups. *Significant differences were declared at P ≤ 0.05 and a tendency was declared when P ≤ 0.1 and P > 0.05.

Considering the beginning of the 2022 birth season as the day the first calf was born, the day of the calves’ birth in the 2022 birth season was not affected by the dam’s parity or interaction of dam’s parity by weaning, but an effect of the weaning strategy (P = 0.03) was observed. Calves from EW (35.64 ± 3.50 d) cows were born 6.59 d earlier than calves from CW (42.23 ± 3.21 d) cows.

Discussion

Early weaning is a potential alternative that reduces energy requirements, alleviates NEB, and achieves maternal tissue gain in B. taurus cattle (Reynolds and Tyrrell, 2000; Wiseman et al., 2019). In the herein study, we aimed to compare for the first time the effects of two weaning strategies (150 vs. 240 d of age) on the body reserves and reproductive performance of the Nelore dam in the subsequent breeding season. We expected that early-weaned cows would improve their metabolic and nutritional status after weaning and during gestation, promoting a greater BCS at parturition and improving reproductive performance. The results reported herein indicate that the early weaning strategy can be used in Nelore cows to successfully improve body condition and reproductive performance in the next breeding season.

The first impact of early weaning was the increased BCS, body weight, ADG, and RFT during the 90 d in which cows were without calves. Therefore, the greater ADG from 150 to 240 d in early-weaned cows was a direct effect of the reduction in the dam’s metabolic requirements due to the cessation of lactation. It is noteworthy that this positive effect on body reserves was first observed at the time of the conventional weaning (240 d) and persisted until the next breeding season (2021-BS). In this regard, Neville and Station (1974) and Reynolds and Tyrrell (2000) demonstrated that the nutrients required for milk production correspond to 44% to 51% of beef dams’ energy demands between 4 and 10 wk of lactation in Hereford and Hereford × Angus cows, respectively. Previous studies in B. taurus cattle also reported increased BCS in suckled cows after the implementation of early weaning (Restle et al., 2001; Arthington and Kalmbacher, 2003; Schultz et al., 2005; Caldwell et al., 2011; Wiseman et al., 2019). Most importantly, the greater body weight, BCS, and RFT observed in early-weaned cows in the current study at the prepartum evaluation and the initiation of the subsequent breeding season could benefit ovarian activity and reproductive performance.

Another important effect on cow metabolism was that urea, NEFA, and BHB were greater from prepartum, then by a decrease until the subsequent breeding season, following the same results of body weight and BCS independent of the weaning strategy. The late gestational period is characterized by accelerated fetal growth as the fetus reaches ~60% of birth weight during the last two months of gestation (Bauman and Bruce Currie, 1980). During this period, the space occupied by the growing fetus decreases the rumen capacity. Late gestation also coincides with the dry period in tropical regions, where most pastoral systems limit the quantity and nutritive value of pastures providing a reduced ADG at the end of the prepartum period (Funston et al., 2010). The reduced ADG and rumen capacity culminate in an NEB at the prepartum, providing an increase in NEFA, BHB, and urea concentration observed in this study. Despite expecting an NEB after postpartum, in this study was observed that the concentrations of NEFA, BHB, and urea decreased from the prepartum collection to the 2021-TAI. This NEB effect was likely not so evident in Nelore cows because in this postpartum period, despite of lactation period, the fact occurs during the same period of rainy period in Brazil, which provides enhanced forage availability and nutritive value. This greater pasture availability supports the energy and metabolism cows’ necessity but apparently does not provide an NEB period for Nelore cows.

The influence of BCS in the return of postpartum cyclicity was demonstrated by several authors (Ayres et al., 2009; Sá Filho et al., 2010a; Nishimura et al., 2018). Interestingly, according to Ayres and coworkers (2014), cows with a greater BCS at parturition are associated with an increased probability of first-service conception rate and a reduced probability of pregnancy loss. In the study reported herein, early-weaned cows had an increased mobilization of body reserves as indicated by the greater loss of body weight (lower ADG) and BCS from prepartum to the beginning of the next breeding season. However, they were still heavier and had greater BCS than conventionally-weaned cows. Besides this, greater mobilization of body reserves did not affect the concentration of metabolites such as NEFA and BHB, demonstrating that early-weaned cows were in a better metabolic state during the subsequent breeding season than conventional-weaned cows. Additionally, the greater concentration of IGF-I in early-weaned cows supported this finding.

The return of postpartum ovarian activity can be affected by many factors such as nutrition condition, BCS, age, breed, and others. Also, nutrition and postpartum BCS are positively associated with early follicular development and resumption of ovulation after calving (Yavas and Walton, 2000). Thus, we anticipated that the beneficial effects of early weaning on body weight and reserves would consequently impact the return of ovarian cyclicity before the beginning of the subsequent breeding season. However, ovarian cyclicity was not affected by the time of weaning in the present study. The proportion of cows with CL present or in deep anestrous was similar between early and conventional-weaned cows.

Although the early weaning had no detectable impacts on the ovarian response at the initiation of the breeding season, it did result in improved ovarian response to the TAI program. The dominant follicle size and follicular BP at the time of the first TAI were greater in cows submitted to the early weaning. Therefore, the increased BCS, body weight, and RFT in early-weaned cows may have been related to a greater stimulus to follicle development during the TAI protocol. In this regard, BCS and RTF are positively associated with the circulating concentrations of IGF-I, glucose, and leptin (Hess et al., 2005), which are directly related to an earlier resumption of ovarian activity and better development and response of the growing follicle in a TAI protocol. Our results demonstrated that concentrations of IGF-I were ~33% greater at the time of breeding in cows exposed to early weaning during the previous production cycle compared to cows exposed to conventional weaning. Therefore, the larger DF in early-weaned cows could be a consequence of the greater stimulus of IGF-I on DF growth, as these concentrations of IGF-1 have a positive effect on follicular cell proliferation, growth, differentiation, and maturation (Lynch et al., 2010). In addition, a larger follicle and greater follicular BP at the time of TAI are correlated with an increase in pregnancy rates during TAI protocols (Siddiqui et al., 2009; Sá Filho et al., 2010a, 2013; Nishimura et al., 2018). Therefore, the early weaning strategy influenced many important characteristics related to reproductive performance, such as body weight, BCS, ADG, RFT, concentrations of IGF-1, and size and BP in the dominant follicle. Consequently, these factors support the improvement in pregnancy outcomes observed in early-weaned cows in the TAI program.

In the herein study, the hypothesis that early weaning would increase the reproduction performance of Nelore cows in extensive grazing conditions was fully supported. The beneficial effects of early weaning on body reserves and ovarian response to TAI are reflected in a 35% increase in pregnancy rates at first TAI (60.4% vs. 44.8%) and a 28% increase in pregnancy rate after two TAIs in 22 d of interval (81.1% vs. 63.5%). Other studies evaluating different times of weaning (90 to 130 d) also reported an improvement in pregnancy rates in B. indicus (Restle et al., 2001; De Oliveira et al., 2019), B. taurus (Wiseman et al., 2019) and crossbred (Arthington and Kalmbacher, 2003) cows exposed to early weaning strategies. The study reported herein included a larger number of animals compared with previous studies and demonstrated the benefits of early weaning as a potential strategy to improve reproductive performance in the subsequent breeding season in Nelore cows. This powerful positive impact on pregnancy outcomes has an important influence on beef cattle operations, as > 80% of the cows submitted to early weaning can become pregnant with two inseminations in a 22-d period at the beginning of the breeding season. According to Ojeda-Rojas et al. (2021), the use of reproductive TAI programs allows an increased proportion of conception in the first months of the breeding season, as obtained by high pregnancy rates after two TAIs in 22 to 24 d, which leads to a greater number of births and heavier calves at weaning. Therefore, the early weaning at 150 d would improve the number of calves born (~81.1% in this study become pregnant from the first and second TAI in a 22-d interval) early in the calving season (September to November in the southern hemisphere), which may positively impact the economic performance of B. indicus beef systems. One of the first consequences of early conception during the breeding season and that was confirmed in the herein study is the anticipation of the birth in the subsequent birth season, which will impact the weaning weight of calves and the age of replacement heifers at the beginning of the breeding season. However, additional research is needed to evaluate the effects of early weaning on other key facets of productivity in the beef production system, including a list of a few factors that are going to be reported in associated research from this present project.

The positive effects of early weaning on reproductive performance occurred regardless of cow parity, as interactive effects of the main factors of weaning strategy and parity were not observed in any characteristic evaluated. However, several variables, including BCS and some reproductive endpoints, were affected by dam’s parity. Body weight, BCS, and RFT were lesser in primiparous than multiparous cows in several time points evaluated. Most importantly, all these characteristics related to body reserves were reduced in primiparous cows during the prepartum period. This response was expected because primiparous beef cows are still growing and thus have a greater need for net energy of growth than multiparous cows (NRC, 2016). Regarding the characteristics related to reproductive performance, an improved ovarian score was observed in multiparous cows as a consequence of a greater proportion of animals bearing a CL at the beginning of the breeding season compared to primiparous cows. Although this impact on ovarian activity in the postpartum period, the pregnancy outcomes were not affected by dam’s parity. Nevertheless, the number of primiparous cows used in the present study limited a powerful analysis for the comparison of binomial data as P/AI. In this regard, previous studies (Sá Filho et al., 2010b, 2013; Sales et al., 2016) have reported that primiparous B. indicus beef cows have reduced reproductive performance compared to multiparous cows.

Conclusion

Early weaning at 150 d compared to 240 d can benefit multiparous and primiparous Nelore cows, providing enhanced recovery of the dam’s BCS and RFT before calving. Early weaning positively affects the dam’s metabolic and nutritional status, as early-weaned cows had greater BCS, weight, and circulating IGF-I concentrations at the beginning of the subsequent breeding season. The positive effects also impact the improvement of follicle growth and blood perfusion during a TAI program, resulting in greater pregnancy rates in early-weaned cows in the subsequent breeding season.

Acknowledgments

The authors would like to acknowledge the University of São Paulo, Campus Fernando Costa for providing the animals and animals facilities. Sincere appreciation is also expressed to the staff at the University of São Paulo and the students of the Department of Animal Reproduction from the School of Veterinary Medicine and Animal Science and the students of the Department of Animal Science of the School of Animal Science and Food Engineering. The authors also ­acknowledge FAPESP (2017/18937-0) for the financial support and CNPq for the scholarship provided to the first author, and also Biogenesis-Bagó Animal Ltda for providing estrous synchronization products for this study.

Glossary

Abbreviations

ADG

average daily gain

BCS

body condition score

BHB

β-hydroxybutyrate

BS

breeding season

BP

blood perfusion

CL

corpus luteum

CW

conventional weaning

DF

dominant follicle

E2

estradiol

EW

early weaning

IGF-I

insulin-like growth factor-1

MUL

multiparous

NEB

negative energy balance

NEFA

non-esterified fatty acid

P4

progesterone

PREG

pregnancy components

PRI

primiparous

RFT

rump fat thickness

SBWnp

non-pregnant shrunk body weight

SBWp

pregnant shrunk body weight

TAI

timed artificial insemination

Contributor Information

Thiago Kan Nishimura, University of São Paulo, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, Pirassununga, São Paulo, 13635-900, Brazil.

Amanda Guimarães da Silva, University of São Paulo, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, Pirassununga, São Paulo, 13635-900, Brazil.

Gabriela Abitante, University of São Paulo, Department of Animal Science, School of Animal Science and Food Engineering, Pirassununga, São Paulo, 13635-900, Brazil.

Carl Robertson Dahlen, North Dakota State University, Department of Animal Science, Center for Nutrition and Pregnancy, NDSU Department 7630, Fargo, ND 58108-6050, USA.

Rodrigo Silva Goulart, University of São Paulo, Department of Animal Science, School of Animal Science and Food Engineering, Pirassununga, São Paulo, 13635-900, Brazil.

Germán Darío Ramírez Zamudio, University of São Paulo, Department of Animal Science, School of Animal Science and Food Engineering, Pirassununga, São Paulo, 13635-900, Brazil.

Saulo Luz Silva, University of São Paulo, Department of Animal Science, School of Animal Science and Food Engineering, Pirassununga, São Paulo, 13635-900, Brazil.

Miguel Henrique de Almeida Santana, University of São Paulo, Department of Animal Science, School of Animal Science and Food Engineering, Pirassununga, São Paulo, 13635-900, Brazil.

Arlindo Saran Netto, University of São Paulo, Department of Animal Science, School of Animal Science and Food Engineering, Pirassununga, São Paulo, 13635-900, Brazil.

Paulo Roberto Leme, University of São Paulo, Department of Animal Science, School of Animal Science and Food Engineering, Pirassununga, São Paulo, 13635-900, Brazil.

Guilherme Pugliesi, University of São Paulo, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, Pirassununga, São Paulo, 13635-900, Brazil.

Conflict of Interest Statement

The authors declare no real or perceived conflicts of interest.

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