RFI as Efficiency Metric for Pre-Weaning Dairy Calves: Comparison
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Please note this is a comparison between Version 2 by Sirius Huang and Version 1 by Camila Sousa da Silva.

Dairy cattle systems have targeted improvements in feed efficiency by selecting animals that can convert less feed into more products. Residual feed intake (RFI) has been the index of choice when selecting dairy cattle for feed efficiency. Nonetheless, RFI studies have focused on lactating cows, and the crucial importance of pre-weaning efficiency on farm profitability and cow productivity has been mostly neglected. Current results suggest great potential for selecting high-efficiency calves while in pre-weaning to accelerate the progress of genetic selection in dairy cattle.

  • efficiency testing
  • high efficiency
  • low efficiency
  • young cattle

1. Introduction

Feed expenses have accounted for 30 to 70% of the total costs of milk production over the past two decades [1]. Hence, improving feed utilization efficiency has always been of great interest in dairy farms and has gained even more attention with the pressing environmental concerns about the impact of livestock on greenhouse gas emissions [2].
Ruminants have been intensively selected for a combination of feed efficiency and milk production traits. Residual feed intake (RFI) has been included in genetic selection programs in some countries [3,4][3][4] as a measure of feed efficiency in dairy cattle production systems. RFI was originally proposed in 1963 [5] and can be defined as the difference between observed and predicted intake. The residual is generated by a multiple regression model where dry matter intake (DMI) is regressed on average daily gain (ADG) and BW0.75 [6]. Negative RFI values refer to the most efficient animals during the testing period and exhibit a lower feed intake than predicted for a given weight gain.
Most RFI studies in dairy cattle have focused on lactating cows. Because in lactation orchestrated adaptations prioritize a certain physiological state, estimates of RFI in lactating cows need to account for additional sources of variation aside from ADG and BW0.75, such as body maintenance, possible pregnancy, milk production, parity, and stage of lactation [7].
Some studies observed a repeatability of RFI from growing to lactating phase [8[8][9],9], indicating that RFI may be a lifetime trait. Thus, the determination of RFI in young calves may be simpler and cheaper and might accelerate genetic progress [10].

2. Relationship between RFI and Nutrient Metabolism in Pre-Weaning Dairy Calves

Albeit tissue catabolism and anabolism, activity, and thermoregulation play a significant role in feed efficiency divergence in cattle [22][11], feed efficiency divergence is generally attributed to differences in nutrient intake and digestion. The relationship between RFI and several variables related to feed intake and nutrient utilization in pre-weaning calves are discussed below and have been summarized in Table 1.
Table 1.
Effects of RFI divergence on feed efficiency, nutrient metabolism, and microbiome of pre-weaning calves.
Item Variable Low Efficiency High Efficiency Reference
Intake RFI (kg/d) 0.130 −0.140 ** [19][12]
    0.049 −0.052 ** [17][13]
    0.168 −0.173 ** [16][14]
Performance Average daily gain (kg/d) 0.98 0.98 [19][12]
    0.59 0.60 [17][13]
    0.57 0.56 [16][14]
Heat production Heat production (kcal/d per BW0.75) 172 148 ** [19][12]
    628 586 [17][13]
Gas exchanges O2 uptake (L/d) 787 668 ** [19][12]
    568 567 [17][13]
  CO2 production (L/d) 702 592 ** [19][12]
    525 534 [17][13]
Nutrient digestibility Dry matter (%) 85.8 89.2 * [17][13]
  Crude protein (%) 87.8 91.8 **  
  Ether extract (%) 93.1 96.4 **  
N metabolism N intake (g/d/BW0.75) 1.74 1.56 ** [17][13]
  Urine N (g/d/BW0.75) 0.46 0.54  
  Fecal N (g/d/BW0.75) 0.21 0.13 **  
  Retained N 0.97 0.99  
Fermentation profile pH 6.31 6.52 [18][15]
  Total VFAs (μmol/mL) 43.4 32.9  
  Acetate (% total VFAs) 0.67 0.75 **  
  Propionate (% total VFAs) 0.27 0.21 **  
Metabolomics Energy-generating metabolites - Upregulated [16][14]
i. Birth Amino acid metabolism - Upregulated  
  Odoribacter1 0.668 0.130 **  
  Prevotellaceae UCG-004 1 0.233 0.149 **  
  Ruminiclostridium 9 1 0.251 0.064 **  
ii. Pre-weaning period Fusobacterium2 0.167 0.230 **  
  Succinivibrio2 0.012 0.020 **  
  Bacteroides2 0.052 0.075 **  
  Vitamin B supply - Upregulated  
  Amino acid supply - Upregulated  
  BCAA 3 catabolism - Upregulated  
1 Pathogenic bacteria. 2 Carbohydrate-fermenting bacteria. 3 Branched-chain amino acids. * Significant at p ≤ 0.10. ** Significant at p ≤ 0.05.

2.1. Effects of RFI on Heat Increment and Gas Exchanges

Feed intake is mainly driven by maintenance requirements; hence, the amount of energy spent on feed digestion, or simply heat increment, is proportional to feed intake. Thus, heat increment increases as feed intake increases [22][11]. It has been estimated that heat increment can account for 75% of total energy intake [23][16]. Consequently, animals that can consume less feed but convert more gross energy into net energy are considered more efficient.
Traditionally, heat increment has been estimated through indirect calorimetry, which measures oxygen (O2) uptake and carbon dioxide (CO2) and methane (CH4) production by animals using open-circuit respiration chambers [24,25][17][18]. An alternative method, called “the face mask method”, has also been proposed [26][19]. In this method, energy expenditure is estimated based on gas exchanges but, unlike the chambers, measured using a face mask. Because O2 uptake is directly related to feed intake [27][20], it has been suggested that O2 uptake is lowest in efficient animals. Indeed, RFI was positively correlated with heat production (r = 0.48), O2 uptake (r = 0.48), CO2 production (r = 0.48), and heart rate (r = 0.40) in pre-weaning dairy calves [19][12]. In addition, high-efficiency calves spent 15.3% less energy as heat, exhibited a lower heart rate, consumed less O2, and produced less CO2 compared to high-RFI animals.
Data collected in that trial [19][12] were acquired using face masks. When gas exchanges were evaluated via respirometric chambers, no differences in O2 uptake or CO2 and heat production between low and high-efficiency calves were observed [17][13]. The discrepancy in these results may be related to the difference in feed intake between the low- and high-efficiency groups reported in the two studies: in the former, calves in the high-efficiency group consumed 320 g less milk + starter than low-efficiency calves, whereas the latter study reported that the difference in feed intake between the two groups was only 80 g and mainly driven by lower starter intake.
Notwithstanding statistical significance, this difference might not have been large enough to cause detectable changes in gas production and heat increment. Furthermore, data behavior acquired from 1049 dairy heifers housed in outdoor facilities and classified as low or high efficiency at 5–9 months of age have shown differences in feeding behavior over 24 h, with the most efficient animals eating less and having fewer meals during daylight (0600 to 2100 h), especially during the afternoon (1200 to 1800 h), but eating for a longer time during the night (0000–0600 h) than the least-efficient animals [28][21]. Nonetheless, behavior patterns might not reflect the regular calf behavior for animals placed inside respirometric chambers, and the potential effects of the chamber’s environment on feed intake and energy utilization cannot be ruled out [29][22].

2.2. Effects of RFI on Nutrient Digestibility

In pre-weaning dairy calves, it has been suggested that differences in feed utilization between RFI-divergent groups may be related to greater intestinal activity due to the large contribution of intestinal digestion [17][13]. In broad terms, nutrient digestibility is expected to be lower in the least efficient cattle because of the higher feed intake [30][23]. High-efficiency pre-weaning calves (RFI = −0.052 kg/day) had greater digestibility of crude protein and ether extract and tended to show a higher total dry matter and organic matter digestibility compared to low-efficiency (RFI = 0.049 kg/day) calves [17][13].
Small intestine mass (g) and relative small intestinal mass (g/kg BW) were positively correlated with dry matter intake and RFI in young cattle [31][24], and high efficiency was negatively correlated with crypt perimeter, crypt area, and nuclei number in duodenum cells [32][25]. Tissues of the splanchnic bed, which include the gastrointestinal tract, liver, spleen, pancreas, mesenteric fat depots, connective tissue, and blood vessels, comprise 15 to 20% of the total body mass in ruminants [33][26], and O2 uptake by the portal-drained viscera can reach 25% [34][27]. These observations suggest that efficient animals have a lower energy requirement for tissue maintenance as well as a greater ability to acquire nutrients per unit of small intestinal mass [31][24]. In fact, low efficiency was positively correlated (r = 0.50) with a greater gross energy intake in pre-weaning calves [17][13].

2.3. Effects of RFI on Nitrogen (N) Metabolism

The efficiency of N utilization in ruminants is typically low due to the several steps involved in peptide degradation in these animals [35][28]. The introduction of RFI in selection programs increased the interest in exploring how RFI divergence affects nitrogen metabolism [36][29]. However, studies revealing the potential effects of divergent RFI on N utilization in pre-weaning dairy calves are almost inexistent.
RFI was moderately and positively correlated with nitrogen intake (r = 0.50) and fecal losses (r = 0.60) in pre-weaning calves [17][13], supporting the observation of lowest CP digestibility by low-efficiency animals. Moreover, low-efficiency calves tended to present higher blood urea levels (21.4 mg/dL) than high-efficiency calves (18.4 mg/dL) [18][15]. Considering that urea is a product of protein degradation, this could be a result of protein catabolism [18][15] or lower N recycling in the least efficient animals, as suggested for lactating cows. Nonetheless, the lack of differences in urinary N and N retention between low- and high-efficiency calves indicates that more research is needed to elucidate the N metabolism in this rearing phase.
Recent results obtained with lactating cows show an association between RFI and milk protein efficiency, expressed as dietary protein captured in milk [37][30]. Cows classified as most efficient based on RFI utilize dietary N for milk protein and body N synthesis more efficiently [38][31]. Possible reasons for improved efficiency of N utilization in most efficient lactating cows may include greater N digestibility and N recycling to the gut [38][31], which has also been suggested for pre-weaning calves [17][13] and 90-day-old lambs [36][29].

2.4. Effects of RFI on Rumen Fermentation Profile

Changes in rumen fermentation products have been reported in pre-weaning calves classified as low or high efficiency [18][15] from 28 to 56 days of age; low-efficiency calves had lower molar concentrations of VFAs and propionate (% VFAs) and a greater proportion of acetate in rumen fluid compared to high-efficiency animals. However, these differences were not linked to RFI per se but rather to the higher intake of starter feed by low-efficiency calves, which may have increased the passage rate and altered the ratios of absorption and digestion. In addition, no differences in pH or ammonia concentration were found, suggesting similar fermentation conditions between RFI groups. Subsequent results [20][32] also reported no effects of RFI divergence on the fermentation profile of pre-weaning calves, and rumen fermentation variables were not correlated with RFI.
The lack of correlation between rumen fermentation parameters and RFI in the pre-weaning phase is probably related to insufficient rumen function in milk-fed animals, as neonatal calves have an underdeveloped rumen until close to weaning [16][14], and differences in rumen fermentation products have been reported for RFI-divergent animals in later life [39,40][33][34]. In fact, β-hydroxybutyrate levels have been pointed out as a potential marker for the identification of high-efficiency heifers post-weaning [40][34]. It is possible that gene expression in rumen epithelium [41][35] and epithelium-associated bacteria [42][36], rather than fermentation, might be involved in improved efficiency in pre-weaning calves, as it has been indicated for older cattle.

2.5. Effects of RFI on Hindgut Microbiome

In lactating cows, low and high efficiency of milk production has been correlated with variations in the abundances of certain rumen bacterial communities [43][37]. Because pre-weaning digestion is marked by substantial hindgut fermentation of undigested diet components, it has been suggested that the hindgut microbiome is implicated in RFI divergence between young calves. Indeed, Elolimy et al. [16][14] have demonstrated that RFI is associated with unique hindgut microbiome and metabolome profiles in neonatal Holstein heifer calves. Furthermore, they observed a maternal and pre-weaning nutrition effect of hindgut microbial communities and metabolome profile.
High-efficient calves had a lower abundance of pathogenic bacteria at birth, such as Odoribacter, Cyanobacteria, Ruminiclostridium 9, Prevotellaceae UCG-001, and Eubacterium nodatum, indicating superior hindgut functionally in these animals. In addition, high-efficient calves had a greater number of functional genes involved in VFA biosynthesis. The analysis of the hindgut metabolome also showed significant differences in the metabolic profile between low- and high-efficiency calves at birth. High-efficient calves had greater enrichment of key metabolites involved in energy-generating pathways, including the citric acid cycle, gluconeogenesis, and pyruvate metabolism, potentially enhancing the supply of energy to the calf and the ability to activate metabolic pathways for amino acid, vitamin, and fatty acid metabolism, which could benefit hindgut development and function [16][14]. On the contrary, high-efficient calves downregulated metabolites associated with the inhibition of several pathways, such as folate metabolism, amino sugar metabolism, sphingolipid metabolism, steroidogenesis, and bile acid biosynthesis.
Interestingly, microbiome communities shifted in response to RFI divergence during the pre-weaning period [16][14]. The results revealed an increased abundance of several carbohydrate-fermenting bacteria in high-efficiency calves, suggesting a greater capacity for utilizing complex carbohydrates reaching the hindgut and improved colonocyte growth and function through the production of VFAs [44][38].
The microbiome of low- and high-efficiency calves also exhibited distinct vitamin and amino acid metabolism [16][14]. Synthesis of vitamin B7, vitamin B6, and vitamin B9, as well as the amino acids arginine, proline, methionine, tyrosine, tryptophan, and phenylalanine, is upregulated in high-efficiency calves, suggesting a positive association between high efficiency and reduced oxidant status and a line of communication between hindgut and brain during the pre-weaning period. Catabolism of branched-chain amino acids (BCAA) was also upregulated in the high-efficient calves. Degradation of BCAA generates α-keto acids, known for promoting cellular growth through the activation of the mechanistic target of rapamycin (mTOR) signaling [45][39]. As with neonatal calves, steroid, and bile acid synthesis was downregulated in high-efficiency calves during pre-weaning.
A study investigating mucosa and digesta bacterial communities throughout the gastrointestinal tract (GIT) of pre-weaned calves [46][40] has identified that the prevalence of Prevotella, Bacteroides, Lactobacillus, and Faecalibacterium, which were among selected abundant bacteria, was significantly different among the GIT regions and between mucosa- and digesta-associated communities. The rumen contained the most diverse bacterial population, comprising 47 genera in total and 16 rumen-specific genera. Additionally, it has been acknowledged that bovine ruminal bacterial populations change from birth to adulthood [47][41]. It is possible that rumen bacterial communities and colonization are associated with RFI divergence among pre-weaning calves. Future studies exploring the connection between RFI and rumen bacterial diversity colonization could deepen our understanding of feed efficiency in early life and whether pre-weaning rumen bacterial diversity is linked to RFI during lactation.

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