A review of the effect of nutrient and energy restriction during late gestation on beef cattle offspring growth and development

Abstract

Changes in the environment, including nutritional changes, can influence fetal and postnatal development of the offspring, which can result in differences in growth, metabolism, reproduction, and health later in life. In beef cattle research on energy and protein restriction during late gestation appears to be contradictory. Therefore, in this review, we will examine the nutrient requirements recommended for this period. We are summarizing contradictory data on effects on offspring performance with possible explanations of the reason for why the data seems contradictory. We will finish by discussing some areas that we consider important for further research to increase the knowledge on how maternal nutrition influences offspring development. In particular, suggestions are provided on the need for more accurately measuring nutrient and energy supply and use and the impact on subsequent epigenetic effects. This will improve understanding of nutritional effects during gestation on offspring performance.

Protein and energy restriction on late gestation on beef cows impact their offspring growth performance and carcass characteristics. This review describes the current knowledge in the area and future research based on gaps on the current literature.

Introduction

It is becoming more evident that changes in the environment, including nutritional changes, can influence fetal and postnatal development of the offspring, which can result in differences in growth, metabolism, reproduction, and health later in life (NASEM, 2016; Caton et al., 2019). Protein and energy restriction during late gestation seems to negatively affect some growth and carcass characteristics parameters; however, results are not consistent and it is unclear as to why. Therefore, the objective of this review is to summarize the current knowledge on the effect of protein and energy restriction during the last third of gestation to beef cows on growth performance of offspring, focusing principally on Bos taurus cows. We chose to focus on B. taurus breeds because it is thought that B. taurus and B. indicus breeds respond differently to changes in the environment and in energy and nutrient supply (Turner, 1980; O’Rourke et al., 1991), and therefore, nutrient effects on developmental outcomes could be different as well.

We will examine the nutrient requirements during this period as recommended by the NASEM (2016), highlighting some areas where we consider the current recommendations need to be reviewed. We are also summarizing contradictory data on effects on offspring performance with possible explanations of the reason why the data are contradictory. We will finish this review by discussing some areas that we consider important for further research to increase the knowledge on how maternal nutrition influences offspring development.

Nutrient Requirements During Late Gestation

To understand the effect of nutrient or energy restriction during gestation on offspring growth first, we need to evaluate the equations used to predict requirements. The NASEM (2016) indicates that the prioritization of nutrients is for 1) basal metabolism, 2) activity to gather food, 3) growth, 4) basic energy reserves, 5) maintenance of pregnancy, 6) lactation to support an existing offspring, 7) accumulation of additional energy reserves, 8) estrous cycles and initiation of pregnancy, and 9) accumulation of excess energy reserves. When gestating cows are undergoing feed restriction, priorities 6 to 9 above likely are not relevant. The first priorities are the primary components contributing to maintenance requirements. Therefore, this results in 3 primary categories for nutrient utilization: maintenance, growth (particularly in heifers), and maintenance of pregnancy. However, the proposed and accepted hierarchy of nutrient utilization should be re-evaluated as this may be an oversimplification of priorities for nutrient use. Also, the efficiency of use of dietary energy for maintenance and production function should be further studied (Galyean et al., 2016; NASEM, 2016). Because current prediction equations may underestimate the needs of the heifer, future prediction equations may wish to consider animal body condition score (BCS) and heifer BW at parturition as a percentage of the herd BW. Including these 2 parameters in future equations could allow researchers to contemplate the importance of conceptus free BW and BCS of the heifer. The last point that will be discussed is how some of this information in the current NASEM (2016) could be presented differently to avoid misinterpretations.

Many of the studies on nutrient or energy restriction during late gestation reported no difference in calf birth weight when the dam is supplemented (Tudor, 1972; Summers et al., 2015a; Maresca et al., 2018; Nickles et al., 2022a, 2022b); however, much of these data are contradictory. Ramirez et al. (2020) reported a decrease in calf birth weight due to a moderate (25%) or severe (50%) nutrient restriction. This decrease in calf birth weight was associated with a decrease in dam BW at calving. However, Nickels et al. (2022a, b) reported that cows and heifers with a decrease in BW and BCS resulted in no effects on calf birth weight. In the Nickels et al. (2022a, 2022b) experiments, cattle were fed to meet nutrient requirements based on BW and stage of pregnancy, but a group of cattle was exposed to other stressor conditions, such as mud, which subsequently increased the nutrient requirements. This supports the concept that the priorities for nutrient use do not always follow the suggested hierarchy discussed above.

Efficiency of nutrient use

When considering the efficiency of energy utilization, energy for maintenance is used more efficiently than the energy used for growth (Galyean et al., 2016; NASEM, 2016). It is assumed that the efficiency of energy use for fetal growth (and milk production) is similar to the efficiency of energy use for maintenance in heifers and cows. However, limited research (Ferrell et al., 1976) has been conducted to confirm that the efficiency of energy use for maintenance and gestation is indeed similar in both heifers and cows.

Prediction equations

The equations that predict energy requirements do not fully consider the effects of BCS. This may be more of a concern in heifers because of the extra BW gain expected in growing animals. The current NASEM (2016) equation considers BW but not BCS, so if we have two animals with the same BW, but one with a BCS of 3 and the other one with a BCS of 7, the requirement of energy using the current equations is similar. Although there are equations explaining the energy required per kg lost gained at a specific BCS (NASEM, 2016), we consider that these equations are not integrated with the equations for maintenance, growth, and gestation. To estimate gestational requirements of a heifer, we need to consider the current weight of the heifer, the weight of the mature cow, and the calf weight. A pregnant heifer increases in BW not only because of the growth of the heifer but also because of the growth of the fetus. For this reason, the conceptus free BW is applied in the equation (Ferrell et al., 1976; NASEM, 2016: equations 13–27). This concept is not well understood by many using the NASEM (2016) model, although BW at the beginning of the end of the feeding period are critical for accurately predicting requirements.

Conflicting Results on the Effect of Nutrient Restriction and Offspring Outcomes

Studies focusing on energy, protein, or an overall nutrient restriction in late gestation have inconsistent results. For example, there are studies presenting no differences in offspring growth or carcass characteristics (Funston et al., 2010; Bohnert et al., 2013; Shoup et al., 2015; Summers et al., 2015b; Wilson et al., 2015) with dam nutrient restriction on offspring outcomes, whereas other studies report treatment effects on growth or carcass characteristics (Corah et al. 1975; Stalker et al., 2007; Underwood et al., 2010; Summers et al., 2015b; Shoup et al., 2015; Maresca et al., 2018, 2019a, 2019b; Webb et al., 2019; Ramirez et al., 2020; Block et al., 2022). The discrepancy in the results may be because the experimental designs, basal dies, or level of restriction differ across studies, making it difficult to compare results across experiments. A summary of studies that examined the effects of nutrient or energy restriction on offspring performance is presented in Table 1. For example, Maresca et al. (2018, 2019a, 2019b) examined the effect of protein restriction and observed no treatment effects on weight or growth of steers, but a larger Longissimus muscle area, dressing percentage (Stalker et al., 2006; Maresca et al., 2019a, 2019b), sarcomere length, muscle fiber number, and lower shear force (Maresca et al., 2019b) were observed in the steers born from cows supplemented with protein. These experiments were using animals fed either diets that exceeded (12% crude protein [CP]) or did not meet (6% CP) dietary protein requirements. Because dietary supply either exceeded or was deficient in protein, it is difficult to compare to other studies such as the study of Webb et al. (2019). Webb et al. (2019) reported that the only effect observed was a mid- and late-gestation interaction effect on shear force in steers from cows that received a control (102% metabolizable [MP]) or restricted (80% MP) diet in midgestation and/or late gestation (using a Balaam’s crossover treatment design). Block et al. (2022) conducted an experiment with a similar design to Webb et al. (2019) and observed an increase in G:F and longissimus muscle area in steers from cows restricted in late gestation, implying that restriction can improve carcass characteristics which contradicts other studies. Webb et al. (2019) and Block et al. (2022) may have observed fewer differences because the differences in protein supply between treatments were not great enough to result in significant effects. The dietary treatments in the studies by Maresca et al. (2018, 2019a, 2019b) had a much greater difference in dietary protein (high protein was 121% of CP requirements and low protein was 64% of CP requirements; NRC, 2000). Therefore, it is possible that the differences (or lack of) observed are not just a matter of if restriction or supplementation occurred, but the magnitude of the difference in protein supply between treatments.

Table 1.

Summary of the effect of protein or energy restriction during late gestation on offspring growth and carcass characteristics¹

Study	Restriction	Amount of restriction	Basal diet	NDF of the basal diet2	Crude protein provided2	Energyprovided2,3	Differences in growth	Differences in carcass characteristics
Webb et al. (2019), Block et al. (2022)	Protein	102% CP requirements	Wheat straw, glycerin, dry supplement	~ 66.78%	MI	2.12 Mcal/d NE	No differences observed	Mid and late gestation interaction effect on WBSF (Webb et al., 2019) Restriction increased G:F and longissimus muscle area (Block et al., 2022)
		80% CP requirements			MI	2.10 Mcal/d NE
Maresca et al. (2018, 2019a, 2019b)	Protein	12% CP	Corn silage, sunflower pellet, urea, mineral premix	60.1	MI	2.36 Mcal/kg ME	High protein (HP) improved initial and final longissimus muscle area in the finishing phase (2019a) HP improved final longissimus muscle area in the rearing and finishing periods (2019b)	High protein improved dressing percentage (2019a) HP improved dressing percentage, muscle fiber number, and sarcomere length, and reduced 3-d and 14-d shear force (2019b)
		6% CP	Corn silage, mineral premix	63.2	MI	2.38 Mcal/kg ME
Stalker et al. (2007)	Protein	None 0.443 g CP/d	Dormant upland range	71-75%	MI MI	MI MI	CP supplementation improved weaning and finishing BW	CP supplementation increased HCW
Summer et al. (2015b) 4	RUP	None	Meadow hay	MI	631 g/d MP	11.4 Mcal/d NE	High MP improved initial feedlot BW	Supplement decreased empty body fat percentage, marbling score, 12th-rib fat thickness, and yield grade, and increased WBSF
		0.83 kg/d DDGS (high MP)			817 g/d MP	12.5 Mcal/d NE
		0.83 kg/d corn gluten feed (LO MP)			733 g/d MP	12.3 Mcal/d NE
LeMaster et al. (2017)	Protein	None	Tall fescue or fescue hay and 1.3 kg/head high-concentrate feed	MI	12 – 17 % CP	MI	Restriction reduced birth weight, supplementation had no effect on birth weight.	Not available
		Restricted			MI	MI
		0.45 kg SBM (3 d/wk)			MI	MI
Wilson et al. (2015)	DDGS	None	Tall fescue and red clover	59.6%	12.7% CP	MI	No change	No change
		2.1 kg/cow/d		57.4%	14.4% CP	MI
Shoup et al. (2015)	DDGS and soybean hulls	None	Tall fescue and red clover	MI	MI	MI	No change	HS increased percentage of steers grading average choice or above
		2.16 kg/cow/d			MI	MI
		8.61 kg/cow/d			MI	MI
Underwood et al. (2010)	Improved pasture	None	Grama-needlegrass-wheatgrass	MI	MI	MI	Improved steer weaning weight, finishing period ADG, and total body weight gain	Improved live weight at slaughter, 12th-rib fat thickness (and adjusted), HCW, and longissimus muscle WBSF
		Improved pasture	Wildrye-wheatgrass	MI	MI	MI
Ramirez et al. (2020)	Energy	50% NE requirements	Corn silage, urea, mineral mix	64.8	MI	MI	Linear decrease in birth weight Quadratic effect on finishing final BW, BW gain, and ADG	Quadratic effect on HCW, 12th-rib fat thickness, adipose diameter, and 3-d shear force
		75% NE requirements			MI	MI
		100% NE requirements			10.3% CP	2.46 MJ/kg ME

¹NDF, neutral detergent fiber; CP, crude protein; WBSF, Warner–Bratzler shear force; G:F, average daily gain:dry matter intake ratio; MP, metabolizable protein; RUP, rumen undegradable protein; BW, body weight; ADG, average daily gain; DDGS, dry distillers grain with solubles; NE, net energy; HCW, hot carcass weight.

²MI represent missing information regarding the energy or protein provided in the diet.

³Unites of energy can be NE_m or ME.

⁴Treatments with protein supplementation provide the same CP but they differ the MP.

The previously described studies were based on different levels of protein inclusion in the diet. However, there are many studies that examine how protein supplementation influences cows in grazing conditions, typically where the basal diet does not meet protein requirements. Unfortunately, feed intake is often not measured in these types of studies because of the difficulties in quantifying intake in grazing animals. However, protein supplementation of dams during late gestation seems to improve some aspects of carcass characteristics in the offspring compared with the feeding studies described above, but the specific carcass effects observed are not consistent between studies (Larson et al., 2009; Ramirez et al., 2020). LeMaster et al. (2017) reported linear trends in calf birth and weaning weight when cows grazed tall fescue to maintain or increase BCS (control), strip-grazed to reduce BCS by 1 to 1.5 BCS units (nutrient restricted), or strip-grazed and supplemented with protein (nutrient restricted with supplementation). Calves born from the protein-supplemented cows had numerically higher birth weights than the calves from the nutrient-restricted cows, but numerically lower birth weights than the calves from control cows, implying that protein restriction can alleviate some of the effects of nutrient restriction. Underwood et al. (2010) observed improved steer weaning weight, finishing period average daily gain (ADG), total body weight (BW) gain, live weight at slaughter, 12th-rib fat thickness, adjusted 12th-rib fact thickness, hot carcass weight, and Longissimus muscle area in steers born from cows on improved pasture compared with steers born from cows on native pasture. However, detailed information on dietary intake and protein quality of the pasture was not quantified, making it difficult to understand why Underwood et al. (2010) observed more differences than other studies. Shoup et al. (2015) reported improved meat quality grades in offspring when dried distillers grains with solubles (DDGS) or soybean hull were supplemented to cows grazing tall fescue, but no changes in growth. However, Summers et al. (2015b) observed greater empty body fat percentage, 12th-rib fat thickness, marbling score, and yield grade in steers from dams fed meadow hay (control) compared with steers born from cows supplemented with corn gluten feed, and steers from cows supplemented with DDGS cows were intermediate to, but not different from the steers born from the control or corn gluten supplemented cows. Wilson et al. (2015) reported no effect of DDGS supplementation to the dam on steer growth or carcass characteristics. The differences between studies may be because of differences in supplementation amount. Wilson et al. (2015) and Shoup et al. (2015) fed similar diets to cows, but in addition to the 2.1 kg DDGS/cow/d supplement treatment provided in both studies, Shoup et al. (2015) also had another treatment that provided almost four times the amount of DDGS as the first (8.3 kg DDGS/cow/d), and this treatment is the only one that resulted in differences in calf performance measures. Summers et al. (2015b) only supplemented 10% of the amount of DDGS (0.83 kg DDGS/cow/d), and because the cows in Summers et al. (2015b) from all treatments likely met NRC (2000) recommendations for MP, supplementation was probably not necessary. It is worth mentioning that for the basal diets of Wilson et al. (2015) and Shoup et al. (2015) the total nutrient/energy intake is not known, and it is difficult to evaluate if nutrient supply met suggested nutrient recommendations; also, the basal dietary protein concentration in the studies by Wilson et al. (2015) and Shoup et al. (2015) were above 11.9%, which likely meets the protein requirements of those cows. There are other studies on protein supplementation where the amount supplemented may not have been enough to maintain maternal BW and condition. For example, Funston et al. (2010) supplemented cows with approximately 124 g/d of CP to a basal diet with CP concentration of less than 6.8%. Therefore, it is possible that the lack of differences observed in Funston et al. (2010) might be because none of the diets met daily protein needs and differences in supply of protein between treatments were not great enough to result in differences in offspring performance.

In general, protein restriction often results in lesser effects on offspring outcomes than energy restriction. Ramirez et al. (2020) and Valiente et al. (2018) both observed a quadratic effect when energy or energy and protein, respectively, were restricted. The treatments were three levels of restriction: severe, moderate, or none (50%, 75%, or 100% NE; NRC, 2000) in the Ramirez et al. (2020) study and to provide 50% NE and 58% CP, 75% NE and 85% CP, or 100% NE and 116% CP NRC (2000) requirements in the Valiente et al. (2018) study. Calves from severely energy- and protein-restricted cows weighed less at calving than the other two treatments in both studies. In the study by Valiente et al. (2018), calves from severely restricted cows were similar in size to the control calves at weaning, whereas the moderately restricted calves had the lowest BW compared with the other two treatments. Ramirez et al. (2020) found no treatment differences in BW in calves at weaning, but severely restricted steers were the heaviest and had the greatest 12th-rib fat thickness and adipose cell diameter at slaughter and moderately restricted steers were the lightest and had the lowest 12th-rib fat thickness and adipose cell diameter at slaughter. In both cases, compensatory growth may have occurred in calves from severely restricted cows, but moderate restriction was probably not enough to trigger these effects. The physiological mechanisms mediating these differences in response to level of restriction are unknown and should be further explored.

Future Research

When performing studies that aim to determine the effects of nutrient and energy supply as related to requirements on cow and calf performance, there are several experimental design considerations that should be addressed. The common dietary treatment designs to test the effect of energy or nutrient supply on developmental outcomes consist of changing intake of the same mixed diet, changing feed ingredients to alter nutrient intake or availability, and supplementation of protein or energy feeds to cattle consuming or grazing forage for ad libitum intake. Although there is good justification for examining these different treatment scenarios, it is difficult to compare and integrate results between studies. Also, many of the studies to date that have aimed to evaluate different planes of nutrition during gestation have examined effects on fed or grazed cows, or heifers in group housing. Despite the useful information that such research has provided, it does not allow for accurate evaluation of the individual animal, which makes it hard to understand the degree of restriction of individual cows. Having the knowledge of each individual animal’s daily dry matter intake is important, so that more accurate nutrient and energy daily intakes can be determined. When combined with the BWs of the cows and heifers, this information allows for future meta-analyses to be completed to combine study outcomes and provide recommendations on nutrient requirements. Another consideration for nutritional studies with cows and heifers is the lack of information on total dry matter and specific nutrient intakes when they are housed on pasture. It is difficult to measure daily dry matter intake when cattle are housed extensively on pasture, but research measuring intake on pasture would help provide needed information to better understand the effects of nutrition and supplementation on cow and calf performance.

Finally, we propose that future experiments are needed that better characterize energy use, partitioning, and requirements throughout gestation. Although the predictions used to estimate nutrient and energy requirements of maintenance of the cow and fetal and conceptus growth are useful (NASEM, 2016), the currently used equations were developed using growing heifers with “old genetic” as the experimental model (Ferrell et al.,1976); further research is needed in both growing heifers and mature cows that represent current genetics of the beef herd in North America and abroad. Research is also needed to understand the underlying mechanisms responsible for programming of offspring through altered maternal nutrition. We propose that moving forward, researchers should take into consideration the need for more accurately measuring nutrient and energy supply and use and subsequent epigenetic effects in the fetus to allow for a better understanding of nutritional effects during gestation on offspring performance and to aid in future meta-analyses of studies in this research area.

Glossary

Abbreviations

ADG

average daily gain

BCS

body condition score

BW

body weight

CP

crude protein

DDGS

dried distillers grains with solubles

G:F

average daily gain:dry matter intake ratio

HCW

hot carcass weight

MP

metabolizable protein

NASEM

National Academy of Science, Engineering, and Medicine

NE

net energy

WBSF

Warner–Bratzler shear force

Conflict of Interest Statement

The authors have no conflicts of interest to declare.