Reducing GHG emissions through genetic improvement for feed efficiency: effects on economically important traits and enteric methane production

Abstract

Genetic selection for residual feed intake (RFI) is an indirect approach for reducing enteric methane (CH₄) emissions in beef and dairy cattle. RFI is moderately heritable (0.26 to 0.43), moderately repeatable across diets (0.33 to 0.67) and independent of body size and production, and when adjusted for off-test ultrasound backfat thickness (RFI_fat) is also independent of body fatness in growing animals. It is highly dependent on accurate measurement of individual animal feed intake. Within-animal repeatability of feed intake is moderate (0.29 to 0.49) with distinctive diurnal patterns associated with cattle type, diet and genotype, necessitating the recording of feed intake for at least 35 days. In addition, direct measurement of enteric CH₄ production will likely be more variable and expensive than measuring feed intake and if conducted should be expressed as CH₄ production (g/animal per day) adjusted for body size, growth, body composition and dry matter intake (DMI) or as residual CH₄ production. A further disadvantage of a direct CH₄ phenotype is that the relationships of enteric CH₄ production on other economically important traits are largely unknown. Selection for low RFI_fat (efficient, −RFI_fat) will result in cattle that consume less dry matter (DMI) and have an improved feed conversion ratio (FCR) compared with high RFI_fat cattle (inefficient; +RFI_fat). Few antagonistic effects have been reported for the relationships of RFI_fat on carcass and meat quality, fertility, cow lifetime productivity and adaptability to stress or extensive grazing conditions. Low RFI_fat cattle also produce 15% to 25% less enteric CH₄ than +RFI_fat cattle, since DMI is positively related to enteric methane (CH₄) production. In addition, lower DMI and feeding duration and frequency, and a different rumen bacterial profile that improves rumen fermentation in −RFI_fat cattle may favor a 1% to 2% improvement in dry matter and CP digestibility compared with +RFI_fat cattle. Rate of genetic change using this approach is expected to improve feed efficiency and reduce enteric CH₄ emissions from cattle by 0.75% to 1.0% per year at equal levels of body size, growth and body fatness compared with cattle not selected for RFI_fat.

Implications

Selection for residual feed intake (−RFI_fat; efficient) will result in cattle that consume less dry matter intake, have improved feed conversion ratio and reduced enteric CH₄ emissions at equal levels of production, body size and body fatness. Rate of genetic change, using multi-trait selection and a comprehensive record keeping system, is expected to be 0.75% to 1.0% per year compared with no selection for RFI_fat. There will be few, if any, antagonistic effects on growth, carcass quality, fertility and cow lifetime productivity. Direct selection for an enteric CH₄ phenotype must be viewed with caution since enteric methane has low to moderate repeatability (0.16 to 0.55) with distinctive diurnal patterns associated with cattle type, diet and genotype, necessitating whole day measurement for at least 35 days. Furthermore, the relationships of enteric CH₄ production with other economically important traits are largely unknown.

Introduction

Methane (CH₄) is the major greenhouse gas (GHG) emitted from ruminant production systems with CH₄ from enteric fermentation accounting for 12% to 17% of GHG emissions (Beauchemin et al., 2009). In North America, the cow herd is responsible for about 85% of GHG emissions, where 6 to 7 month old weaned calves are adjusted to a high grain diet over 1 to 1.5 months, fed for 6 months and then harvested at 14 to 16 months of age (Beauchemin et al., 2010; Basarab et al., 2012a). In a calf-to-beef system that couples backgrounding and finishing, more CH₄ is emitted from the forage-fed backgrounded phase than from the grain-based finishing phase and the cow herd is responsible for almost 70% of GHG emissions. The high proportion of CH₄ associated with the cow herd is because of the cow herd consuming a higher proportion of the feed in a calf-to-beef system, inherently low biological efficiency of the beef cow and the very high proportion of the cow herd's diet as conserved forage, pasture, range and crop residues rather than concentrates (Allen et al., 1992; Verge et al., 2008; Capper, 2011). The impact of roughage v. concentrate diets on increasing the CH₄ emissions in ruminant systems is well known (Johnson and Johnson, 1995; Beauchemin and McGinn, 2005; Beauchemin et al., 2008). Reducing daily CH₄ emissions by increasing cereal grain content in backgrounding and finishing diets and increasing the starch content of small grain and corn silages can be an effective mitigation method that fits logically into the feedlot system (Beauchemin and McGinn, 2005; Beauchemin et al., 2009).

Methane mitigation for the cow herd may be achieved by improving the digestibility of annual and perennial forages through grazing management, increasing legume composition and utilization of species containing secondary metabolites such as tannins or saponins that affect methanogenesis in the rumen (Beauchemin et al., 2008 and 2009). Use of high-sugar perennial ryegrass (Lolium multiflorum L.) cultivars and increasing alfalfa (Medicago sativa L.) and clover (Trifolium repens L.) sward content, where practical, can help improve forage digestibility, although increasing long-term legume content of swards can prove difficult (Dewhurst et al., 2009; Clark et al., 2011) . However, many tannin containing species showing potential are weak competitors with grasses and have a narrow climatic and geographic adaptation, necessitating a long-term plant breeding process (Abberton et al., 2007) to improve agronomic traits such as winter hardiness, seedling vigor and competitive capacity. Thus, widespread renovation of grasslands to incorporate tannin and saponin-containing species to reduce CH₄ production may not be practical.

Reducing cow herd CH₄ emission is a necessity for improving the carbon footprint of beef production which ranges from as low as 17 kg carbon dioxide equivalents (CO₂e)/kg carcass beef for feedlot finished beef in Canada (Verge et al., 2008; Beauchemin et al., 2010; Basarab et al., 2012a) to as high as 40 CO₂e/kg carcass beef for grass-finished beef in Brazil (Cederberg et al., 2011). Ultimately, the combined impacts of plant and livestock breeding for low CH₄ emission rates may result in substantial reductions of enteric CH₄. However, the most practical and rapid mitigation procedure may be to reduce the per cow CH₄ emission through animal breeding and genetic selection for feed efficiency as it is permanent and cumulative (Alford et al., 2006). It is also easier to improve efficiency within the cattle population as opposed to the riskier re-establishment or renovation of long-term grasslands, much of which exists on marginal and often arid lands. Furthermore, as the global population surpasses nine billion by 2050, improving feed efficiency becomes even more urgent to meet the increasing demand for feed grains for food and ethanol production (FAO, 2009). Moreover, feeding more grain to the cow herd is not a sustainable practice and feeding additives and supplements on pasture is not practical.

Thus, the purpose of this paper is to discuss genetic selection for feed efficiency, specifically RFI, as an indirect approach to reducing CH₄ emissions in ruminants. The impact of RFI on economically important traits will be discussed, as well as the impact of within- and between-animal variation in feed intake on CH₄ emissions.

Feed efficiency and RFI

Feed is the largest variable cost and an important determinant of profitability in beef production (ARD, 2005; Ramsey et al., 2005). In North America, 55% to 75% of the total costs of calf-to-beef production systems are associated with feed costs (NRC, 2000; ARD, 2005). The cattle herd (cows, bulls and breeding replacements) consumes 82% of the feed inputs in a calf-to-beef systems where animals are harvested at 11 to 14 months of age and 63% to 64% of the feed inputs in a calf-to-beef system where animals are harvested at 19 to 23 months of age (Basarab et al., 2012a). In Irish grass-based calf-to-weanling and calf-to-beef systems the cow herd consumes about 85% and 50% of the total feed inputs, respectively (McGee, 2009). About two-thirds of the feed energy is required for body maintenance (Ferrell and Jenkins, 1985; Montano-Bermudez et al., 1990), and considerable animal-to-animal variation, independent of body size and growth, exists in maintenance requirements of cattle (Herd and Bishop, 2000; Arthur et al., 2001a and 2001b; Basarab et al., 2003; Nkrumah et al., 2006; Crowley et al., 2010). Thus, improving feed efficiency through genetic selection holds significant opportunity for the beef industry. Traditionally, feed efficiency in beef cattle was defined as feed to gain ratio or FCR. However, genetic evaluation of ratio traits like FCR or methane yield (g CH₄/kg dry matter intake (DMI)) are problematic in that selection response is unpredictable, usually placing higher than expected emphasis on the trait with higher genetic variance (Gunsett, 1984; Kennedy et al., 1993; van der Werf, 2004). Further, the genetic correlation between the numerator (e.g. DMI) and denominator (e.g. average daily gain (ADG)) is positive (Koots et al., 1999; Berry, 2012), and therefore, selection for improved FCR has resulted in cattle that grow faster, have increased mature size, and increased maintenance and feed requirements (Bishop et al., 1991; Archer et al., 1999; Herd and Bishop, 2000; Crews, 2005; Kelly et al., 2010a and 2010b). As a result, efficiency measures that remove various known energy uses from feed intake, such as BW and production, are being used within breeding programs. RFI, also referred to as net feed efficiency, was first proposed by Koch et al. (1963) and was defined as the difference between an animal's actual feed intake and its expected feed requirement for maintenance of body size and production. Low RFI in growing animals represents individuals with lower feed intake at equal body size and growth, with lower maintenance energy requirements and thus greater efficiency. More recently, RFI values have been adjusted for body fatness (RFI_fat), thus attempting to render RFI independent of carcass fatness in slaughter cattle and later maturity or fattening in replacement heifers and bulls (Basarab et al., 2003, 2007 and 2011; Schenkel et al., 2004; Crews, 2005). Similarly, residual gain (RG) is adjusted for body size and DMI and represents animals with superior gain at equal levels of BW and DMI, and a trait that combines both RFI and RG, referred to as residual intake and gain (RFI–RG) represents efficient, fast growing animals that consume less feed (Crowley et al., 2010; Berry and Crowley, 2012). These latter two measures of feed efficiency should also be adjusted for body composition using final off-test ultrasound backfat thickness, marbling score and/or ribeye area. These measures of feed efficiency are heritable (h ² = 0.26 to 0.43) and either moderately (RFI v. RG, r _g = −0.46, r _p = −0.40) or highly (RG v. RFI–RG, r _g = −0.87, r _p = −0.85) correlated with each other (Crews, 2005; Crowley et al., 2010; Berry and Crowley, 2012). In lactating dairy cows, RFI is defined as the difference between an animal's actual feed intake and its expected feed requirement for BW, fat mobilization, as well as milk fat, protein and yield (Rius et al., 2012).

Feed intake, variation and repeatability

All direct measures of feed efficiency require accurate measurement of feed intake and energy uses such as BW, growth and body composition in young cattle (Arthur et al., 2001a and 2001b; Basarab et al., 2003, 2007 and 2011), and BW, fat mobilization and milk fat, protein and yield in lactating dairy cattle (Rius et al., 2012). Typically RFI is measured in young cattle (7 to 10 months of age; maximum age difference = 60 days) in feedlot pens fitted with feeding stations designed to automatically monitor individual animal feed intake (e.g. GrowSafe Systems Ltd, Airdrie, Alberta, Canada) following a 21 to 28 days adjustment to their test diet (Basarab et al., 2003 and 2011). The adjustment period is followed by a 76-day test period, which has been recommended as being adequate for the determination of feed intake and growth (Wang et al., 2006). Cattle are weighed before feeding on 2 consecutive days at the start and end of the test period and at ∼14- to 28-day intervals. They are also measured for ultrasound backfat thickness (mm), longissimus thoracis area (cm²) and marbling score at the start (optional) and end of the test period.

Many factors affect the DMI of cattle such as body size, growth, body composition, gender, age, season, ambient temperature, physiological status, previous nutrition and diet (NRC, 2000). Most of these factors are either equal between animals during a standardized feed intake test (e.g. gender, season, ambient temperature and physiological status) or are adjusted for, such as body size, body composition and growth. However, considerable within- and between-animal variation exists in DMI and measures of feed efficiency. The average daily feed intakes and coefficients of variation (CV) for 61 replacement heifers are presented in Figure 1 (J.A. Basarab, 2012; unpublished). The daily CV for feed intake ranged from 11% to 22% and are a reflection of the daily between-animal variation in feed intake. The between-animal repeatability as determined by the ratio-of variance method and conducted in 10-day intervals (e.g. 1 to 10, 1 to 20, 1 to 30 days) ranged from 0.325 to 0.358 for feeder heifers, 0.341 to 0.407 for feeder steers, 0.286 to 0.380 for replacement heifers, 0.374 to 0.449 for young bulls and 0.361 to 0.491 for cows (Table 1). These levels of repeatability are weak to moderate, meaning that an animal was unable to repeat its feed intake consistently over days as reflected by the deceasing repeatability estimates for the same group of cattle as the feeding interval increased (e.g. feeder steers, replacement heifers). Kelly et al. (2010b) reported a similar repeatability of 0.34 for DMI of feeder heifers weighing 418 kg (s.d. = 31.5 kg) fed a total mixed ration consisting of 70 : 30 concentrate and corn silage on a dry matter (DM) basis. Wang et al. (2006) reported that the phenotypic variances for DMI decreased rapidly from 7 to 35 days of feed intake data collection and then stabilized after 35 days, indicating that extending the duration of data collection beyond 35 days resulted in only small improvement in accuracy.

Figure 1 Daily feed intake (solid dots) and coefficient of variation (solid line) averaged for 61 beef heifers (8 to 12 months old) fed ad libitum a 78.2% barley silage and 21.8% barley grain diet (dry matter basis) over 108 days (Basarab, 2012, unpublished).

Table 1 Diet ingredient composition, length of feed intake tests and repeatability of feed intake by period for various beef cattle types (Basarab, 2012, unpublished)

DMI = dry matter intake; DM = dry matter.

¹Corn-based dried distillers grains and solubles.

²Feed intake period length was 1 to 84 days for feeder steers and heifers and 1 to 77 days for young bulls and mature cows.

The within-day pattern of feed intake for 61 replacement heifers fed ad libitum a high forage diet is illustrated in Figure 2. The animals were fed once daily at about 0930 h. The repeatability of hourly DMI (00:00:00 to 00:59:59 = 0:00 h, 01:00:00 to 01:59:59 = 1:00 h, …) across 9 days was low for hour 0:00 to 8:00 (r = 0.04 to 0.13), 10:00 to 18:00 (r = 0.02 to 0.16) and 19:00 to 23:00 (r = 0.09 to 0.28), and moderate for hour 09:00 (r = 0.42) indicating considerable within-day within animal variation in feed intake. Thus the within-day repeatability of feed intake is affected when the animal is offered or obtains its feed and varies by RFI phenotype. Collectively, these results suggest that since enteric CH₄ production is proportional to DMI (Grainger et al., 2007), within- and between-day enteric CH₄ emissions would be at least as variable as daily DMI and would require at least 35 continuous days of recording for a given diet and animal type (e.g. feeder steers on a finishing diet, replacement heifers on a growing diet).

Figure 2 Daily feed intake pattern of the 10 highest and 10 lowest heifers for residual feed intake (RFI_fat; 78.2% barley silage and 21.8% barley grain diet, ad libitum, dry matter basis; Basarab, 2012, unpublished).

Repeatability of RFI across diets

Because RFI is a relatively new trait, there are questions regarding its repeatability at different stages of an animal's life, on different diets and in different environments. Moderate-to-high positive phenotypic (r _p) and genetic (r _g) correlations, and repeatability (r) have been reported between RFI measured on a grower diet and then again on a finisher diet (r _g = 0.55, Crews et al., 2003; r _p = 0.67, Carstens and Tedeschi, 2006; r = 0.62, Kelly et al., 2010b), and between post-weaning RFI in heifers and when measured again later in life as mature cows (r _g = 0.98; Archer et al., 2002). Lower repeatability estimates (r _p = 0.33 to 0.42) have been reported by Durunna et al. (2011) when RFI was measured between two successive feed intake test periods varying in dietary energy content (low v. high energy) and ambient temperature. In their study, 51% to 58% of the animals re-ranked by 0.5 s.d. (0.295 kg DM/day) from the grower phase to the finisher phase which is similar to the 54% identified by Kelly et al. (2010b). This level of re-ranking for RFI, DMI and ADG occurred whether the diet changed from a grower to finisher diet or stayed the same from feeding period 1 to 2. Durunna et al. (2011) proposed that such re-ranking was because of 1. BW and feed intake measurement error, 2. animal variation in response to compensatory gain, 3. animal variation in efficiency with animal maturity and 4. animal variation in diet digestibility because of differences in feeding behavior, rate of passage and rumen microbial population. Preliminary data from the Lacombe Research Centre, Canada, also confirms the moderate to strong repeatability of RFI over different stages of the animal's life (Basarab, 2012; unpublished). Replacement heifers identified as −RFI_fat and +RFI_fat when they were 8 to 12 months of age and fed a 90% : 10% barley silage and barley grain diet (as fed; −0.373 v. 0.365 kg DM/day) were also −RFI_fat and +RFI_fat when measured again as 4 to 7 year old cows and fed a 70% : 30% grass hay and barley straw cube diet (as fed; −0.375 v. 0.459 kg DM/day). Thus, these results indicate that RFI, and presumably RG and RFI–RG, are consistent across different stages of an animal's life.

RFI and related traits

Growth, carcass traits, FCR and feed intake

There are numerous studies examining the relationships of RFI with growth and carcass traits in cattle (Arthur et al., 2001a and 2001b; Richardson et al., 2001; Herd et al., 2002; Basarab et al., 2003; Nkrumah et al., 2007; Crowley et al., 2010 and 2011) including a recent review by Hill and Ahola (2012). Briefly, RFI is not related to pre- and post-weaning growth, body size and slaughter weight in beef cattle and the phenotypic and genetic correlations are near zero. Carcass traits are also poorly correlated to RFI (Hill and Ahola, 2012), though some studies have reported a low-to-moderate correlation between RFI and carcass fatness (r _p = 0.25 for grade fat; r _p = −0.22 for lean meat yield; Nkrumah et al., 2004) and RFI and marbling (r _g = 0.17; Robinson et al., 2001). However, when RFI is adjusted for body fatness using ultrasound backfat thickness (RFI_fat), the correlations were near zero (Basarab et al., 2003 and 2007). Thus, selection for low RFI_fat breeding stock will have little to no effect on progeny growth, frame size, mature size or carcass characteristics.

RFI is moderately to highly correlated with feed intake (r _p = 0.47 to 0.72; r _g = 0.69 to 0.79; Arthur et al., 2001a and 2001b; Herd et al., 2002; Basarab et al., 2003; Nkrumah et al., 2007; Kelly et al., 2010b) and FCR (r _p = 0.46 to 0.70; r _g = 0.66 to 0.88; Arthur et al., 2001a and 2001b; Basarab et al., 2003; Kelly et al., 2010b). This implies that selection for −RFI_fat will decrease feed intake at equal levels of BW, growth and body fatness, and will improve feed-to-gain ratio in feeder cattle and growing replacement heifers. These results also imply that selection for −RFI_fat will decrease CH₄ emissions (g/animal per day) since CH₄ emissions are proportional to feed intake (Blaxter and Clapperton, 1965; Beauchemin and McGinn, 2006; IPCC, 2006). A comprehensive analysis of Australian and Canadian data spanning a wider range in enteric CH₄ emissions, diet quality, animal type (lactating dairy cows; growing beef steers) and CH₄ measurement technique (SF₆ in whole animal chambers; whole animal chambers) revealed strong positive, linear relationships between CH₄ emissions (g/day) and DMI (Australian, R ² = 0.45, P < 0.001; Canadian, R ² = 0.68, P < 0.001; Grainger et al., 2007; Figure 3). Generally, the higher the DMI the higher the daily enteric CH₄ emissions as more substrate is available for rumen fermentation and more hydrogen is available for methanogenesis (Pinares-Patinõ et al., 2003; Lovett et al., 2005; Beauchemin and McGinn, 2006; Grainger et al., 2007).

Figure 3 Relationship between CH₄ emission determined in chambers and dry matter intake (DMI) for Australian and Canadian data. Lines are through the origin and have slope estimates of 17.06 for the Australian data (r ² = 0.454, P < 0.0001) and 20.79 for the Canadian data (r ² = 0.677, P < 0.0001). Adapted from Grainger et al. (2007).

Since CH₄ production rates (g/day) are proportional to DMI, they are often standardized to g CH₄/kg DMI or expressed as a percentage of gross energy intake (GEI). Unfortunately, this has resulted in contradictory conclusions as CH₄ production expressed as g/kg DMI or as a percent of GEI are not related to DMI (r < 0.20, P > 0.20; Beauchemin and McGinn, 2006). In addition, when feed intake was expressed relative to maintenance, thus removing some variation because of daily feed intake, it was moderately and negatively associated with CH₄ expressed as percent of GEI (r = −0.30; P = 0.04). Thus, increasing the intake level to 2.5 times maintenance decreased CH₄ conversion by 19%, presumably because of reduced retention time in the rumen and lower acetate : propionate ratio (Beauchemin and McGinn, 2006). Lower acetate and greater propionate production directs hydrogen away from CH₄ production. Despite the strong positive relationship between daily CH₄ production and DMI, there are numerous within- and between-animal factors that are unrelated to DMI since 54% to 70% of the total variation in daily CH₄ production is associated with the animal despite being fed the same diet (Pinares-Patinõ et al., 2003).

Feeding behavior

The genetic components of feeding behavior are important in animal breeding since they have economic and animal welfare implications, contribute to animal-to-animal variation in energetic efficiency (Herd et al., 2004; Herd and Arthur, 2009; Kelly et al., 2010a), digestibility and enteric methane emissions (Johnson et al., 1994; Harper et al., 1999). Feeding behaviors such as feeding duration, frequency and rate are moderately repeatable (r = 0.37 to 0.62: Kelly et al., 2010b) and heritable (h ² = 0.28 to 0.38; Nkrumah et al., 2007). Furthermore, research from Australia (Robinson and Oddy, 2004), Canada (Basarab et al., 2007; Nkrumah et al., 2007; Montanholi et al., 2010; Durunna et al., 2011), Ireland (Kelly et al., 2010a) and the United States (Golden et al., 2008; Bingham et al., 2009) have reported mostly moderate to strong positive correlations (r = 0.08 to 0.62) of RFI and RFI_fat to feeding duration, frequency and eating rate. Several of these relationships are further illustrated in Figures 4 and 5 by the moderate correlation between RFI_fat and feeding event frequency in replacement heifers fed a growing diet (r _p = 0.16, P < 0.1) and cows fed straw : hay cubes (r _p = 0.57, P < 0.001) tested for feed efficiency at the Lacombe Research Centre, Canada (Basarab, 2012, unpublished). Collectively, these results show that –RFI_fat and +RFI_fat cattle have distinctive diurnal patterns of feeding behavior, with inefficient cattle having 14% to 22% more daily feeding events than efficient cattle (Nkrumah et al., 2007; Kelly et al., 2010a), thus expending 2% to 5% more energy in feeding activities (Herd et al., 2004; Basarab et al., 2011). There are also implications for the direct measurement of enteric CH₄ as CH₄ emissions from the rumen are closely associated with feeding patterns; higher after feeding than at ruminating or resting (Johnson et al., 1994). Thus, whole-day measurement repeated across many days (e.g. 35 days as recommended for DMI by Wang et al., 2006) are required to accurately reflect animal-to-animal differences in enteric CH₄ production.

Figure 4 Daily average feeding event frequency (FF) and feed intake (FI) for residual feed intake (+RFI_fat; n = 29) and −RFI_fat (n = 32) beef heifers fed ad libitum a 78.2% barley silage and 21.8% barley grain diet (dry matter (DM) basis) over 108 days. Means (s.d.) are as follows: +RFI_fat, FF = 116.3 events/day (33.2), black solid line; –RFI_fat, FF = 106.3 events/day (33.2), black dashed line; +RFI_fat, FI = 7.27 kg DM/day (1.34), red solid line; –RFI_fat, FI = 6.81 kg DM/day (1.25), blue dashed line (Basarab, 2012, unpublished).

Figure 5 Daily average feeding event frequency (FF) and feed intake (FI) for residual feed intake (+RFI_fat; n = 23) and –RFI_fat (n = 17) beef cows fed a hay-straw cube over 79 days (25% straw: 75% grass hay-alfalfa mix, dry matter (DM) basis). Means (s.d.) are as follows: +RFI_fat, FF = 105.3 events/day (21.0), black solid line; –RFI_fat, FF = 85.5 events/day (17.9), black dashed line; +RFI_fat, FI = 15.10 kg DM/day (1.55), red solid line; –RFI_fat, FI = 13.32 kg DM/day (2.42), blue dashed line. Ad libitum and about 85% restricted feeding occurred from days 1 to 30 and 31 to 79, respectively (Basarab, 2012, unpublished).

In a recent review on feed efficiency and animal robustness, Rauw (2012) hypothesized that because efficient animals have decreased feeding event duration and frequency, they are less able to adapt to changes in environment conditions. However, observation of beef cows reared under extensive Canadian winter conditions has shown that cows that produced –RFI calves actually had higher backfat thickness with no differences in lifetime productivity compared with their herd mates that produced +RFI calves (Basarab et al., 2007). In addition, –RFI_fat heifers calving for the first time had lower calf death within 30 days of birth than +RFI_fat heifers, suggesting that calves born to efficient cows have improved early life survival possibly because of lower maintenance requirements and more available nutrients for accumulation of body fat, better uterine environment (Basarab et al., 2007 and 2011) and possibly improved calf passive immunity status. Indeed, recent unpublished research from the Lacombe Research Centre confirm these findings in that –RFI_fat cows gained more body fat and BW than +RFI_fat cows when both groups swath grazed forages for the first time during Canadian winters where night time ambient temperatures dropped below −20°C and animals grazed through the snow from November to March. Previous to this, both –RFI and +RFI young cows had been wintered together in smaller holding areas and fed barley silage to meet their nutritional requirements. Thus, while efficient cattle have lower feeding event duration and frequency and lower feed intake this does not mean that –RFI_fat animals cannot compete or acquire forages during extensive grazing. Instead, it may imply that efficient animals are more adaptable and less susceptible to stress than +RFI_fat or inefficient animals.

Fertility and cow productivity

The relationships of RFI or RFI_fat on fertility and productivity in heifers and cows have recently been reviewed by Basarab et al. (2012b). Briefly, −RFI and +RFI cows and heifers were similar in culling, pregnancy, calving and weaning rate, calving pattern, calf birth weight, level of dystocia and kilogram of calf weaned per mating opportunity (Arthur et al., 2005; Basarab et al., 2007 and 2011), however, −RFI cows calved 5 to 6 days later in the year than +RFI cows suggesting a delay in the onset of first estrus that may have delayed conception during the first breeding season (Arthur et al., 2005; Basarab et al., 2007; Shaffer et al., 2011). When RFI was adjusted for body fatness (final off-test backfat thickness; RFI_fat) no differences were observed in percentage of −RFI_fat and +RFI_fat heifers reaching puberty by 10, 11, 12, 13, 14 or 15 months of age nor in the percentage of calves born by day 28 of the calving season (86.5 v. 92.0, P = 0.28; Basarab et al., 2011 and 2012b). Calving difficulty, age at first calving, calf birth weight, calf pre-weaning ADG, calf actual and 200-day weaning weight and heifer productivity, expressed as kg calf weaned per heifer exposed to breeding, were also similar between −RFI_fat and +RFI_fat heifers. Fertility of young bulls, as measured by scrotal circumference, breeding soundness evaluation, calves born per sire and semen characteristics, for the most part has been unrelated to RFI, though several weak associations (r _p = 0.13 to 0.21; P < 0.05) have been observed with sperm morphology and motility (Hafla et al., 2012; Wang et al., 2012). These observations may also reflect the need to adjust RFI for off-test ultrasound backfat thickness and feeding behaviors in an effort to prevent the selection for later maturing bulls.

Basarab et al. (2007 and 2011) also reported a lower calf death loss in −RFI_fat compared with +RFI_fat heifers and cows, and suggested that the improved early life survival of progeny from −RFI mothers may be because of their improved feed efficiency resulting from more available nutrients and a better uterine environment compared with +RFI mothers. In addition, mothers that produced −RFI progeny consistently had 2 to 3 mm more backfat thickness, on average, over the 12th and 13th ribs and lost less weight during early lactation (pre-calving to pre-breeding) than mothers that produced +RFI progeny, thus indicating that the lower maintenance requirement of −RFI heifers and cows results in the accumulation of body fat or the loss of less body fat and weight during stressful environmental periods.

RFI, methane production and digestibility

Reduction of CH₄ emissions from ruminants is important because it represents 2% to 12% loss of feed energy by cattle (Johnson et al., 1994; Johnson and Johnson, 1995) and is linked to global warming. There are numerous opportunities for nutritional and microbial manipulation to reduce CH₄ emissions in ruminants and these have been extensively reviewed by Beauchemin et al. (2008) and McAllister and Newbold (2008). Enteric CH₄ is produced during fermentation of feeds in both the reticulorumen and hindgut, with 95% to 98% excreted through the esophagus and lungs via brief 5 to 30 s eructations, burps and/or breaths and 2% to 5% via flatus (Johnson and Johnson, 1995; Grainger et al., 2007). This leads to large fluctuations within and between days, and from animal-to-animal in CH₄ production (Beauchemin and McGinn, 2005 and 2006; Jones et al., 2011; Pinares-Patinõ et al., 2011). Methane production has low-to-moderate heritability (h ² = 0.13 to 0.38; Crowley et al., 2010; de Haas et al., 2011; Pinares-Patinõ et al., 2011), low-to-moderate repeatability (r = 0.16 to 0.55; Robinson et al., 2010; Pinares-Patinõ et al., 2011) and is positively correlated to RFI (r _p = 0.35 to 0.44; Nkrumah et al., 2006; Hegarty et al., 2007), suggesting that it may be possible to breed for lower CH₄ production and/or yield (g CH₄/day; g CH₄/kg DMI) either by directly selecting for a lower CH₄ phenotype or indirectly by selecting for low RFI_fat. The latter approach will be the emphasis of the following discussion.

A review of the scientific literature revealed three basic hypotheses as to why −RFI or −RFI_fat animals have lower CH₄ production and/or yield (Ørskov et al., 1988; Nkrumah et al., 2006; Hegarty et al., 2007; Pinares-Patinõ et al., 2011; Waghorn and Hegarty, 2011; Rius et al., 2012; Gomes et al., 2013). The first hypothesis is primarily feed intake driven. Efficient animals have lower feed energy intake at equal levels of production, BW and fatness and lower CH₄ and manure production since CH₄ production is either 6.5% or 4% of GEI (<85% v. ≥85% concentrates in the diet) and manure production and N excretion is predicted based on DMI, and total digestible nutrient, CP and ash content of the diet (Herd et al., 2002; IPCC, 2006). This hypothesis assumed no effects of RFI phenotypes on digestibility or CH₄ yield (g/kg DMI; % of GEI). The second hypothesis is also feed intake driven but assumed that feed intake affects retention time of digesta in the rumen and rumen volume such that longer retention times and higher rumen volumes are associated with increased CH₄ production, likely because of increased digestion of structural carbohydrates and a greater supply of hydrogen for methanogens (Nkrumah et al., 2006; Hegarty et al., 2007; Gomes et al., 2013). Any small differences in DM or N digestibility (1 to 2 percentile points) are attributed to decreased metabolizability of the diet and increased heat increment of feeding at higher levels of feed intake above maintenance (Ferrell and Jenkins, 1985). The third hypothesis suggested that inherent differences in feeding behavior and activity as previously discussed, feed intake and ruminal retention time results in a host-mediated response in microbial communities (bacteria, archaea, ciliate protozoa and fungi) favoring improved DM and N digestibility (Russell and Gahr, 2000; Nkrumah et al., 2006). Higher ruminal fermentation rates favor a shift in acetate to propionate, thus decreasing the hydrogen available for methanogens.

Only a few studies have actually measured whole or near-whole day CH₄ production from cattle differing in RFI. Measurement techniques have included indirect calorimetry where CH₄ was measured continuously over 16 to 24-h periods (Nkrumah et al., 2006; Montanholi et al., 2011), SF6 as a tracer gas where CH₄ was measured in a series of 10-day measurement periods (Hegarty et al., 2007), respiration chambers over 48 hs (Waghorn and Hegarty, 2011) and open path Fourier Transform Infrared spectrophotometry over two 6-day periods (summer and winter, Western Australia; Jones et al., 2011). Diets varied from high grain fed to steers to low- and high-quality forage fed to cows. In three of these studies, −RFI steers consumed less feed and produced 24.6% to 27.5% less CH₄ than +RFI steers (Canadian, University of Alberta data, 97.5 v. 129.3 g CH₄/day, P = 0.04; Canadian, University of Guelph data, 493.4 v. 680.2 ml CH₄/min, P = 0.08; Australian data, 142 v. 190 g CH₄/day, P = 0.01). When expressed as % of GEI or per kg DMI, only the Canadian data reported lower methane yields for –RFI as compared with +RFI steers (3.19% v. 4.28% of GEI, P = 0.04). The cow results were more variable and ranged from no difference between RFI phenotypes in CH₄ production (Waghorn and Hegarty, 2011) to 23.1% less CH₄ produced for −RFI cows and their calves grazing high quality (81% digestibility) annual pasture during the winter (0.34 ± 0.017 v. 0.46 ± 0.023 g CH₄/kg live weight (LW)/day, P < 0.05; 13.1 ± 1.63 v. 14.0 ± 1.50 kg DM/500 kg LW/day, P>0.1; Jones et al., 2011). In this same study, RFI groups were similar in CH₄ production when the cows were pregnant and grazing poor quality (55% digestibility) annual pasture during the summer (0.26 ± 0.018 v. 0.26 ± 0.013 g CH₄/kg cow LW/day, P > 0.1; 10.2 ± 0.27 v. 10.7 ± 0.26 kg DM/500 kg LW/day; P > 0.1). The lack of differences in CH₄ emissions between the RFI phenotypes during the summer may be attributed to the low CP content (7.1%) of the poor quality forage as 8% to 9% CP is required to meet the nitrogen requirements for the rumen microbes (NRC, 2000), thus affecting DMI and digestibility. The lack of difference in DMI between –RFI and +RFI cows may also be because of the large error associated with the mass balance method used to assess forage intake.

Similarly, only a few studies have measured DM and/or N digestibility in cattle differing in RFI (Nkrumah et al., 2006; Cruz et al., 2010; Lawrence et al., 2011; Rius et al., 2012). In the study by Nkrumah et al. (2006), DM and CP digestibility tended to be greater for –RFI compared with +RFI steers, with medium RFI steers being intermediate (75.3% v. 73.4% v. 70.9% for DM digestibility, P = 0.10; 74.7% v. 73.5% v. 69.8% for CP digestibility, P = 0.09). In addition, RFI was positively associated with DMI, feeding event duration and bunk attendance, and feeding event duration was negatively related to DM (r = −0.55) and CP (r = −0.47) digestibility, indicating that lower feeding durations were associated with lower DMI and improved digestibility. These results are in agreement with Rius et al. (2012) where 16 ruminally cannulated (eight –RFI and eight +RFI) early lactating Holstein-Friesian heifers were fed ad libitum fresh vegetative ryegrass during an 8-day digestibility trial where total intake of nutrients and outputs of milk, feces and urine were determined. Efficient (−RFI) cows had greater apparent N digestibility (77.2% v. 75.5%, P = 0.02) and tended to have greater DM (78.5% v. 77.3%, P = 0.07) and organic matter (81.1% v. 80.1%, P = 0.08) digestibility than +RFI cows. Gomes et al. (2013), after a 5-day adaptation period, sampled feed and orts and collected total feces and urine throughout a 48-h period on 12 –RFI and 12 +RFI steers fed a finishing diet. Non-significant numeric differences between RFI phenotypes were observed in apparent DM digestibility (−RFI, 75.2%; +RFI, 72.3%; P = 0.18), nitrogen retention (−RFI, 60.0 g/day; +RFI, 53.2 g/day; P = 0.34) and nitrogen excretion (−RFI, 97.3 g/day; +RFI, 108.8 g/day; P = 0.31). Cruz et al. (2010) and Lawrence et al. (2011) used internal markers (lignin and acid-insoluble ash) and fecal grab samples to estimate digestibility reported no differences in N or DM digestibility between –RFI and +RFI cattle.

Thus, there is direct evidence indicating that –RFI cattle will produce less CH₄ (g CH₄/day) than +RFI cattle, primarily through lower feed intake at equal levels of production, BW and fatness. However, the evidence for greater feed efficiency in –RFI_fat cattle due, at least partially to an enhanced capacity to digest feeds is controversial as CH₄ yield (g CH₄/kg DMI or as % of GEI) between RFI phenotypes were inconsistent among studies. The relationship between RFI and DM and N digestibility is also unclear, though it is known that higher DMI will increase CH₄ production, but shorter rumen retention time associated with higher DMI will lower digestibility by 1 to 4 percentage points depending on the level of feed intake above maintenance, lower CH₄ yield (g/kg DMI) and increase heat increment of feeding (Ferrell and Jenkins, 1985; NRC, 2000; Waghorn and Hegarty, 2011). Thus, the small differences in digestibility between –RFI and +RFI cattle observed in the above mentioned studies are more likely because of differences in feed intake rather than because of any real differences in ability to digest feed.

RFI, rumen microbiota and methane emissions

This section examines the third hypothesis which implies that inherent differences between RFI phenotypes in feed intake and feeding behaviors results in host-mediated alterations in microbial profiles and fermentation patterns. Indeed, the rumen bacterial profiles and not the total numbers of bacterial cells of −RFI steers are different than those in +RFI cattle when fed growing (Hernandez-Sanabria et al., 2010) and finishing diets (Guan et al., 2008; Hernandez-Sanabria et al., 2010). A recent study by Irish researchers further confirmed segregation of rumen microbial profiles in forage-fed beef heifers with different RFI values (Carberry et al., 2012). In this study, abundance of some Prevotella species was higher (P < 0.0001) in +RFI animals. Further, some Prevotella sp. have been associated with increased butyrate production, poorer FCR and a lower straight-chain to branched-chain volatile fatty acids (VFA) ratio (Hernandez-Sanabria et al., 2010). Conversely, other Prevotella species were higher in −RFI animals (Ghoshal et al., 2012). The Prevotella genus predominates (up to 60% of total population) in the rumen under many dietary conditions (Stevenson and Weimer, 2007) and plays a role in degradation and utilization of starch (Cotta, 1992) and proteins (Wallace et al., 1993). Therefore, it is not surprising that some species belonging to this genus are associated with better fermentation profiles and feed efficiency. In addition, some bacterial species such as Clostridium sp. are associated with lower straight-chain to branched-chain VFAs and improved FCR (Hernandez-Sanabria et al., 2010). Branched-chain VFAs are derived from branched-chain amino acids (e.g. leucine, valine and isoleucine) and the ratio of straight-chain to branched-chain VFA is an indicator of amino acid fermentation (Hernandez-Sanabria et al., 2010). Thus, Clostridium sp. can ferment amino acid and peptide to produce ammonia (Eschenlauer et al., 2002), suggesting that the increased amino acid metabolism plays an important role in feed efficiency. Furthermore, some novel ruminal species have been observed to be associated with specific fermentation functions. Pelotomaculum thermopropionicum, for example, is an anaerobic propionate-oxidizing bacterium (Imachi et al., 2002) that has been associated with low propionate and improved FCR (Hernandez-Sanabria et al., 2010). Propionate, one of the major VFA in the rumen, is the major gluconeogenic precursor whose concentration is dependent on digestible energy intake (Stewart et al., 1997).

Recent high throughput sequencing studies have revealed that the rumen has greater than 700 bacterial species (Brulc et al., 2009), suggesting that there is limited value in studying the rumen microbial community at the taxonomy level and emphasizing the need to examine enzymes involved in carbohydrate and amino acid metabolism. Use of a metagenomic approach has revealed variation in ruminal microbial enzymes between –RFI and +RFI animals (Ghoshal et al., 2012). The activity of enzymes involved in benzoate metabolism was higher in the rumen of +RFI steers while enzymes involved in carbazol degradation were higher in −RFI steers. The 4-carboxymuconolactone decarboxylase enzyme plays a role in benzoate degradation which leads to overproduction of CO₂ ultimately leading to increased production of CH₄ in +RFI steers. Further, carbazol degradation may lead to a decreased production of CO₂ which lowers the substrate necessary for CH₄ emission.

The methanogenic process plays a role in regulating the overall fermentation in the rumen by removing H₂ that benefits the donors by providing an electron sink for reducing equivalents to minimize the partial pressure of H₂ in the rumen (Wolin et al., 1997; Russell, 2002). Methanogens are found in a symbiotic relationship with ruminal bacteria (Wolin et al., 1997) and protozoa (Lange et al., 2005). Only a few species of methanogens have been successfully isolated from the rumen and identified because of their stringent requirements for growth. Recent studies using molecular-based approaches have reported that the differences in methanogenic profiles, not the total population of methanogens may be associated with feed efficiency of cattle (Zhou et al., 2009 and 2010). The methanogenic community in +RFI cattle has been observed to be more diverse than that in –RFI cattle, and the differences at genus, species, strain and genotype levels were associated with feed efficiency when fed low energy diets. Several researchers have examined the relationship between methanogenic populations and variation in feed efficiency. The observed proportion of Methanosphaera stadtmanae and Methanobrevibacter sp. AbM4 in the rumen were higher in +RFI compared with −RFI cattle (Zhou et al., 2009). M. stadtmanae utilizes methanol for CH₄ synthesis (Miller and Wollin, 1985), and M. sp. AbM4 is closely related to Methanobrevibacter smithii, a species that utilizes acetate for CH₄ production (Zhou et al., 2009). These results suggest increases in populations that shift more organic substrates to CH₄ biosynthesis pathways, which may contribute to low feed efficiency. In addition, the association between methanogen profiles and RFI was affected when the animals were switched from low to high-energy diets (Zhou et al., 2010). These results suggest that the diversity of the methanogenic community affects CH₄ emissions and feed efficiency in cattle. However, CH₄ was not measured in the above studies, and trials to link the methanogenic profiles with the CH₄ emissions are necessary to verify and elucidate the roles of methanogen in the animals with different feed efficiency. Furthermore, the interaction between methanogens and bacteria, as well as protozoa is largely unknown.

Breeding for low RFI and reduced CH₄ emissions

Actual selection for RFI has been conducted at the Trangie Agricultural Research Centre, NSW, Australia, with a direct yearly response because of selection of −0.125 kg DM/day compared with no selection for RFI (Arthur et al., 2001c). However, given that multi-trait breeding goals will be pursued by the industry, Alford et al. (2006) assumed an annual rate of response in RFI of −0.08 kg DM/day (0.8%/year) in a 25-year simulation assessing the impact on enteric CH₄ abatement for the Australian beef industry. Cumulative CH₄ reduction over 25 years was 568 100 t which was equivalent to an annual reduction of 568 100 t CO₂e/year or $8.5 million/year in carbon credits assuming a global warming potential of 25 for CH₄ and a value of $15/t for CO₂e. This study did not account for reduced manure CH₄ and N₂0, cropping N₂O and energy CO₂ because of reduced feed requirements resulting from lower RFI. The HOLOS whole-farm model (Little et al., 2008) which does account for enteric CH₄, manure CH₄ and N₂0, cropping N₂O and energy CO₂ was used to predict the reduction in total GHG emissions that would occur after 25 years of selection for −RFI compared with a baseline 120-cow herd ( four breeding bulls) not selected for RFI. Animal and cropping data from Beauchemin et al. (2010), percentage RFI reduction (% of base year) for different age cohorts in a commercial herd over 25 years from Alford et al. (2006), and updated global warming potentials of 25 for CH₄ and 298 for N₂O were used for this HOLOS simulation. After 25 years of selection for −RFI, the efficient 120-cow beef herd had lower GHG emissions by 101 t CO₂e per year or 0.844 t CO₂e per cow per year compared with the average 120-cow herd. In addition, the feed nitrogen use efficiency and carbon footprint of the efficient herd were improved by 17% to 22% and 14%, respectively, compared with the cow herd not selected for RFI (19.82 v. 23.06 kg CO₂e/kg carcass beef) and the total farm area decreased by 13% because we use less farm grown resources to produce an equivalent amount of animal product. These estimates of GHG reduction are conservative as improved DM digestibility in –RFI cattle and improved accuracy and rate of genetic change resulting from genomic enhanced breeding values were not considered.

There is on-going debate as to the best methods to use when selecting for improved RFI. The merit of including RFI in the breeding goal over and above just feed intake exists to a different extent depending on the breeding tools available to a particular group of producers. For example, where a multiple trait selection index is used, including RFI as a goal trait may hold little or no advantage to using the components (feed intake, ADG, metabolic LW and back fat) as goal traits along with proper weightings. However, RFI may be a ‘cleaner’ trait than feed intake to include as it is essentially feed intake corrected for different energy uses at the time of measurement. Similarly, since RFI is effectively a selection index, a feed efficiency sub-index can be derived using restricted selection index methodology (Eisen, 1977). Ultimately, including either feed intake or RFI in a breeding goal is mathematically equivalent given that all parameters are known without error (Van der Werf, 2004).

In a situation where only expected progeny difference (EPD) are generated for different traits, and selection pressure for each trait is determined by the producer, selecting for multiple traits simultaneously as well as attempting to select for feed efficiency without a direct measure may be a lot to ask. Selecting for reduced feed intake alone may be equivalent as producers would inherently select for increased weaning weight but the notion of selecting for reduced feed intake (if selection pressure was left to the producer) may seem improper especially when there is a ‘feed for fertility’ mantra in existence. In this instance, deriving EPD for RFI is useful. In a third situation, where no genetic evaluation is available to the producer, RFI can be used to rank animals for feed efficiency within population. It should also be taken into consideration when proposing RFI, RIG or residual intake and gain to producers as a selection criterion that it is a difficult concept to grasp (Wulfhorst et al., 2010) and this may lower industry acceptance of residual feed efficiency measures. It is positive to note that RFI is favorably genetically correlated or not correlated with the majority of other production and carcass quality traits as previously discussed and selection for RFI will reduce GHG emissions in ruminants.

Conclusion

Selection for feed efficiency through residual or its component traits (DMI, BW, ADG and backfat) in a multi-trait selection index will result in slow incremental improvement to feed efficiency and methane intensity, with few antagonistic effects on traits of economic importance.