The Role of Productivity inImproving the EnvironmentalSustainability of RuminantProduction SystemsJudith L. Capper1 and Dale E. Bauman2

1Department of Animal Sciences, Washington State University, Pullman, Washington99164; email: capper@wsu.edu2Department of Animal Science, Cornell University, Ithaca, New York 14853; email:deb6@cornell.edu

Annu. Rev. Anim. Biosci. 2013. 1:469–489

First published online as a Review in Advance onDecember 13, 2012

TheAnnual Review of Animal Biosciences is onlineat animal.annualreviews.org

This article’s doi:10.1146/annurev-animal-031412-103727

Copyright © 2013 by Annual Reviews.All rights reserved

Keywords

greenhouse gas emissions, dilution of maintenance, carbon footprint,animal source foods, dairy, beef

Abstract

The global livestock industry is charged with providing sufficientanimal source foods to supply the global population while improvingthe environmental sustainability of animal production. Improved pro-ductivity within dairy and beef systems has demonstrably reduced re-source use and greenhouse gas emissions per unit of food over the pastcentury through the dilution of maintenance effect. Further environ-mental mitigation effects have been gained through the current useof technologies and practices that enhance milk yield or growth inruminants; however, the social acceptability of continued intensifica-tion and use of productivity-enhancing technologies is subject to de-bate. As the environmental impact of food production continues tobe a significant issue for all stakeholders within the field, further re-search is needed to ensure that comparisons among foods are madebased on both environmental impact and nutritive value to truly as-sess the sustainability of ruminant products.

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INTRODUCTION

The global agricultural industry faces a challenge in providing enough safe, affordable, andabundant food to supply the growing population. According to theWorld Food Summit, “Foodsecurity exists when all people, at all times, have physical and economic access to sufficient, safe,and nutritious food to meet their dietary needs and food preferences for an active and healthylife” (1). According to estimates from the Food and Agricultural Organization (FAO) of theUnited Nations, the global population will reach 9.5 billion people by the year 2050, and foodproduction will need to increase by 70% to provide worldwide food security (2). Food demandfor livestock products will not rise in a linear fashion—demand is expected to double in sub-Saharan Africa, South Asia, and other developing regions, which also will see the greatest risein population numbers, with relatively little change in developed countries (3). Dwindlingsupplies of nonrenewable resources (e.g., fossil fuels, minerals) exacerbate this challenge, whichis complicated further by the burden that an increased population places upon renewableresources such as land and water. Available cropland per person is predicted to decline by 25%between 2010 and 2050 (4); thus, there is a clear need to improve yields per unit area of land aswell as total food production. However, a desire to improve agricultural sustainability runs intandem with the need to produce greater amounts of food per unit area, and these two needsoften are considered to conflict.

The Brundtland Report provides what is arguably the most widely used definition of sus-tainable development, which is that it “meets the needs of the present without compromising theability of future generations to meet their own needs” (5, p. 5). This can be further dissected intothree components: environmental stewardship, economic viability, and social responsibility (6).For a system or industry to be sustainable, all three components must balance—if one factor ismisaligned, the system cannot achieve long-term sustainability. Animal welfare considerations onmodern dairy farms serve as an example of this balance; optimal animal care represents theproducer’s social responsibility and is linked intrinsically to system productivity. If the animal’swell-being and health are compromised, milk production and the efficiency of resource usedeclines, which thereby has adverse effects on both the economic viability and environmentalstewardship of the dairy operation.

The environmental impact of food production has focused, to date, on greenhouse gas(GHG) emissions, also referred to as the carbon footprint. A complete analysis, however, alsowould need to consider water use as well as land- and air-quality aspects. There is no doubt thatGHG emissions are of vital importance, especially in light of food stakeholder concerns relatingto climate change, but it should be remembered that water use is likely to be the major limitingfactor, and thus a critical environmental metric in the near future. Nevertheless, the sciencerelating to GHG emissions is more developed at present than estimates of water or otherresources per unit of food; therefore, GHG emissions can be used as a proxy for environmentalimpact. Global GHG emissions from all agriculture were estimated by Bellarby et al. (7) toaccount for between 17% and 32% of all human-induced emissions, and the EnvironmentalProtection Agency (EPA) (8) estimated that agriculture contributes approximately 6% of thetotal US carbon footprint, with animal agriculture accounting for half of the agriculturalcomponent. A recent report by the FAO (9) concluded that animal agriculture was reportedto account for 18% of GHG emissions, and these conclusions have been adopted eagerly byactivist groups as evidence for the benefits of a vegetarian or vegan lifestyle (10, 11).

The methodology and results of the FAO report have been discussed at length (12, 13).Pitesky et al. (12) credited the FAO report with sound recommendations as to the importanceof improving productivity and efficiency to reduce future GHG emissions, but they documented

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discrepancies inmethodology between analyses of animal agriculture and other sources of GHGemissions that led to the marked overestimation of the global contribution made by animalagriculture. Nonetheless, Pelletier & Tyedmers (14) suggest that animal agriculture accountedfor 14% of global GHG emissions in the year 2000, and given that a subsequent FAO reportcalculated that global dairy production contributes 4% to global anthropogenicGHG emissions(15), it is clear that animal agriculture makes a significant contribution. Given current concernover this issue, and assuming that consumer demand for ruminant animal proteins will remainhigh, this paper discusses the options available for improving the environmental sustainability ofruminant production.

EVALUATING THE ENVIRONMENTAL SUSTAINABILITY OF RUMINANTPRODUCTION

Choosing an Environmental Sustainability Metric

Ruminant production systems are inherently variable across regions and climates, with consid-erable diversity conferred by management systems and production practices. For example, themajority of beef production systems in the United States are characterized by an industry com-prising seed stock producers, cow-calf operators, backgrounders, and feedlots, with a small quantityof calf inputs from the dairy industry and considerable technological inputs. By contrast, Euro-pean beef production systems tend to employ less-intensive finishing systems, with a greater re-liance on crossbred calves from the dairy industry. To attempt to determine the environmentalimpact of any one of themyriad individual subsystems that comprise beef production in theUnitedStates or Europe would render interregional comparisons meaningless. Yet all of these industriesexist to supply animal protein for human consumption, with associated by-products includinghides, fertilizers, and pharmaceuticals. Whole-system analyses therefore have evolved to encom-pass all relevant resource inputs and waste outputs within the defined boundaries of a productionsystem and thus facilitate comparisons between regions and production systems.

Early environmental analyses used limiting resource availability as the denominator, for ex-ample using carbon emissions per unit of land to compare the environmental impact of conven-tional versusorganic dairyproduction (16). However, such denominators again lead to difficultiesin regional comparisons and do not consider externalities—it is not obvious whether a unit of landused for dairy production in the Netherlands has food production potential equivalent to that ofa unit of land in theMidwesternUnited States or arid regions of Australia. The accepted functionalunit for environmental comparisons among ruminant systems therefore has become the unit offood (kg, t); for ruminant production this translates to mass of milk for dairy or meat for beef andlamb. Given the wide variation in milk composition, as discussed by Bertrand& Barnett (17), thishas been further refined to units of fat and protein-corrected (or energy-corrected) milk whenassessing dairy production’s environmental impact. This corrects for production-system variation,but it still may lead to confusion when consumers concerned about the environmental impact oftheir food choices choose foods based on carbon emissions without due regard for differences innutrient composition.

The Relationship Between Ruminant Productivity and Environmental Impact

Resource use and GHG emissions decline with increased productivity and feed efficiency—ruminant production systems tend to have a greater environmental impact than the verticallyintegrated, monogastric production systems. Nonetheless, the US dairy and beef industries have

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made significant productivity gains over the past century in tandem with increasing intensifica-tion of ruminant production systems. The US dairy industry is considered to have originated withthe importation of European cattle to the Jamestown settlement in 1611, and the earliest recordedUSmilk production data relate to a Jersey cow that produced 232 kg ofmilk in a 350-day lactationin 1854 (18). Annual averagemilk yield per cowhas increased from1,890 kg in 1924,whenUSDAdairy production record keeping began, to 9,682 kg in 2011 (19), and the current record-holdingcow (named Ever-Green-View My 1326) produced over 32,800 kg.

The introduction of genetic selection tools and the potential to produce a large number ofhigh–genetic merit offspring via artificial insemination have allowed dairy producers to makeinformed decisions as to selection criteria when breeding replacement cattle. The greatestprogress since the early 1980s has been made in yield traits, with genetic improvement ac-counting for approximately 55% of phenotypic gains (20). However, a negative trade-off alsohas occurred between milk yield and fertility, with a 6% decline in pregnancy rate since 1980(equivalent to a 24-d increase in calving interval), of which approximately one-third can beattributed to genetics. VandeHaar& St-Pierre (21) noted that, although improved genetics haveplayed a significant role in these productivity gains, advances in nutrition and managementpractices have been essential to allow dairy cattle to reach their genetic potential for milk yield.Over the past century, theUS dairy industry has shifted from extensive production systems basedentirely on forage to intensive systemswith diets still founded on forage but formulatedwith feedcomponents to optimize rumen fermentation and meet the dairy cow’s nutrient requirements.This has allowed the use of a variety of feeds, including by-products from the human food andfiber industry,which has resulted in a totalmixed ration approach that improves the efficiency ofrumen fermentation and digestibility, more adequately meets the cow’s nutrient requirements,and allows for greater performance (21, 22). In combination with improved knowledge of dairycattle health and welfare, modern management practices have demonstrably improved pro-ductivity within the dairy industry.

Productivity advances also have occurred within the US beef industry, with a regressed an-nual increase in beef yield per animal of 2.09 kg between 1930 (average yield 239 kg/animal) and2010 (average yield 350 kg/animal) (19). The US beef industry has followed similar trends inimproving productivity to those of the dairy industry; however, owing to regional and climaticvariation within cow-calf and backgrounder operations, and to the nutritional, labor, andeconomic limitations imposed by forage-based diets within these systems, the greatest rate ofprogress in terms of growth rates, technology adoption, and feed efficiency has beenmadewithinfinishing operations (23). Until the 1950s, themajority of beef consumed in theUnited Stateswasproduced in pasture-based systems; however, the advent of finishing diets formulated to meetcattle requirements and containing a significant proportion of corn and by-product feeds, withconsequent improvements in growth rate, intramuscular fat, and grading score, encouragedproducers to move toward a more intensive system (24).

The Dilution of Maintenance Concept

Every animal requires a certain amount of nutrients on a daily basis to support vital functions,health, and minimum activities (the maintenance requirement) plus an additional nutrient re-quirement to support production, i.e., growth, pregnancy, or lactation. The maintenance re-quirement is dependent principally upon bodyweight and thus does not change as a function ofproduction (25). As this daily nutrient requirement is applicable to every animal, the maintenancerequirement of the livestock population therefore may be considered as a fixed cost of animalproduction. When applied to the livestock industry, improving productivity of an individual

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animal such that a greater quantity of milk, meat, or eggs is produced in a set period of time, thetotal maintenance cost per unit of food produced is reduced. Thus, the dilution of maintenanceconcept is central to improvements in economic viability and environmental sustainability. Thelatter is especially noteworthy because maintenance represents a cost in terms of both resourceuse (including feed, land, water, and fossil fuels) and waste output (e.g., manure and GHG). Anexample of the dilution of maintenance concept is illustrated in Figure 1, in which nutrientrequirements are compared for cows at two different levels of production. In 1944, when milkyield averaged 7 kg/d, maintenance represented 69% of the metabolizable energy requirement.In contrast, the maintenance requirement was diluted out over more units of production andrepresented 37% of metabolizable energy for cows averaging 29 kg/d milk in 2007. Improvingproductivity consequently reduces resource use and waste output per unit of dairy. This rel-atively simple mechanism has been the foundation for improvements in the environmentalsustainability of the US ruminant livestock industries over the past century (26–28).

RUMINANT LIVESTOCK’S ENVIRONMENTAL IMPACT: THE USPERSPECTIVE

Dilution of Maintenance and the Environmental Sustainability of US DairyProduction

Within dairy production, improving milk yield per cow is the most widely understood pro-ductivity measure. The environmental impact of increased milk yield may be exemplified bycomparing resource use and GHG emissions from US dairy production in 1944 and 2007, asdescribed by Capper et al. (26). In 1944, the average US dairy farm had six cows fed a primarilypasture-based diet with occasional corn or soy supplementation. Neither antibiotics nor arti-ficial hormones were available for animal use, and animal manures provided fertilizer. Incontrast to highly mechanized modern dairy systems, 1944 farms averaged only 1.2 tractors—

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The impact of increasing daily milk yield on the proportion of daily energy used for maintenance versuslactation indairy cows from1944comparedwith2007—thedilutionofmaintenance effect.Data adapted fromCapper et al. (26). Abbreviations: ME, metabolizable energy; MJ, megajoules.

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the majority of agronomical operations were achieved through draft horse work. This historicalsystem, with a national herd comprising 54% small breeds (Jersey, Guernsey, Ayrshire) and46% large breeds (Holstein, Brown Swiss) and an average milk yield of 2,074 kg/year, issubstantially different from modern dairying. As a result of the previously discussed gains innutrition, genetics, and management, the average dairy cow produced 9,193 kg milk/year in2007 and the national herd contained more than 90%Holstein cattle. As described previously,increasing milk yield per cow between 1944 and 2007 diluted out the maintenance cost andreduced the energy required per kg of milk from 15.3 MJ to 7.1 MJ (Figure 1). As milk yieldincreased, fewer lactating cows were required to produce a set amount of milk, and the numberof associated support animals (dry cows, replacement heifers, bulls) in the population decreased;thus, the total population maintenance requirement was reduced. The 2007 dairy industrytherefore produced 84.2 billion kg ofmilkwith a national herd containing only 9.2million dairycattle (and 89.0 billion kg of milk from the same number of cattle in 2011) compared with 53.0billion kg of milk from 25.6 million head in 1944. In combination with advances in cropproductivity over this time period, feed use per unit of milk was reduced by 77%, land use by90%, water use by 65%, and manure production by 76% (Figure 2). The carbon footprintof a kg of milk in 2007 was 63% lower than that in 1944 (1.35 kg CO2-eq compared to 3.66 kgCO2-eq), and the total dairy industry carbon footprint (with the boundary of the farm gate) wasreduced by 41%, despite the substantial increase in total milk production (26).

Mature cow bodyweight has increased concurrently with productivity gains over the pastcentury; thus, although the environmental impact of a unit of milk has been reduced, daily re-source use and GHG emissions per animal have increased. This may lead to future legislativecomplications if environmental assessments are based upon the number of livestock units peroperation without consideration of productivity. Although the previous historical exampledemonstrates the environmental advantages of reducing the number of animals required to

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Resource use and waste outputs from modern US dairy production systems typical of the year 2007,compared with historical US dairying (characteristic of the year 1944). Data adapted from Capper et al. (26).Abbreviations: GHG, greenhouse gas.

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produce a set quantity of milk, the population maintenance requirement is determined by thecombination of animal numbers and animal bodyweight. In a comparison of the environmentalimpact of cheese production from Jersey and Holstein milk, Capper & Cady (29) demonstratedthat land use, water use, andGHG emissions were reduced by 32%, 11%, and 20% respectivelythrough the use of Jersey cattle. In this instance, the environmental gains were conferred by acombination of factors, primarily an increase in milk fat and protein content combined withdecreases in bodyweight and milk yield for Jersey cattle. Nonetheless, when breed-specific traitswere examined in isolation, the difference in bodyweight between Jersey (454 kg) and Holstein(680 kg) cattle led to a 74% reduction in population bodymass despite a 9% increase in the totalnumber of cattle required to produce an equivalent amount of cheese. Capper & Cady (29)found that bodyweight was the most influential factor affecting environmental impact, withmilk composition (and thus cheese yield per unit of milk) andmilk yield following closely behindbut with little effect of age at first calving, culling rate, or calving interval. These results wereechoed by Bell et al. (30), who reported that changing energy-corrected milk (ECM) yield byone standard deviation conferred a 14.1% decrease in the carbon footprint per unit of ECMcompared with feed efficiency, calving interval, or culling rate (6.0%, 0.40%, and 0.14%decreases, respectively).

Improving management practices that have a positive effect on dairy cow productivity,for example reducing calf mortality, improving heifer growth, or decreasing the incidence ofmastitis, also will reduce the environmental impact of dairy production. Garnsworthy (31)reported thatmethane emissions could be reduced by up to 24%by improving fertility within theUK dairy herd and thus reducing the number of heifers required to maintain milk production.Sexed semen also has been suggested as a mechanism to improve productivity by ensuring thatheifers are born to superior animals, which thus improves the potential genetic merit andproductivity of the herd (32). Nonetheless, if Y-sorted semen were not equally available, thispotentially would affect the efficiency of beef production if a greater number of dairy heifercalves were diverted into beef production. Further research is required on the comparative andinteractive effects of herd productivity metrics to identify the management practices that havethe greatest impact on environmental metrics within systems.

Between-system comparisons of US dairy production’s resource use and GHG emissionsagain demonstrate the importance of improved productivity. A recent study from the OrganicCenter (33) concluded that organic dairy production had considerable environmental advantagesover conventional systems but made the assumption that productivity was equivalent in bothsystems. Consumers appear to consider that organic production systems have a lesser environ-mental impact than their conventional counterparts (34), but the majority of studies comparingyields in organic and conventional production reveal that yields are substantially lower in organicsystems both in theUnited States (35–37) andoverseas (16, 38). Thenutrient costs formaintenancein an organic system are approximately 20% greater owing to increased nutrients required tosupport the physical act of grazing (25), and milk yield averages 20% less across studies (39).When the increased nutrient use for maintenance and milk-yield reductions are included in theanalysis, the increase in GHG emissions per unit of milk conferred by organic production isapproximately 13% (39).

Dilution of Maintenance and the Environmental Sustainability of US BeefProduction

In contrast to dairy production, in which lactation length has a relatively narrow range (generally∼300–420 days) and thus the primary dilution ofmaintenance effect is conferred during lactation,

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both beef yield and growth rate have a significant effect upon the environmental impact of beefproduction. If we compare productivity gains made in conventional beef production systemsbetween 1977 and 2007, average slaughter weight increased over this time period from 274 kgto 351 kg, thus reducing the number of slaughter animals and the size of the national herdrequired to meet beef meat demand (27). Average growth rate was increased from 0.71 kg/d to1.16 kg/d between 1977 and 2007, which reduced both the proportion of total energy useapportioned tomaintenance from 53% (1977) to 45% (2007; Figure 3) and the average numberof days required to reach slaughter weight from 609 to 485. As shown in Figure 4, the reductionin total maintenance requirements conferred by the combination of the reduced beef populationand the lesser number of days for animals to reach slaughter weight reduced feed use by 19%,land use by 33%, water use by 12%, fossil fuel use by 9%, and the carbon footprint per kg ofbeef by 16% (27).

Yield gains within the US beef industry have been significant over the past century, but anec-dotal evidence from the processing and retail industry suggests that slaughterweights have reacheda plateau. Consumer demand for portion sizes greater than those conferred by the current averageslaughter weight of 582 kg (40) is unlikely to increase, and the current processing infrastructureis ill-equipped to deal with larger carcass sizes without considerable reorganization. This isunfortunate, because the negative correlation between beef yield and population size required tomaintain beef production means that yield gains have a substantial effect on total environmentalimpact, particularly as the supporting population (i.e., cow-calf herd) contributes the greatestproportion of GHG emissions per unit of beef (41) and is less susceptible to dietary modificationof enteric methane emissions than cattle in other sectors owing to their forage-based diets (42).Within an efficient cow-calf system, calves should be weaned at approximately half the dam’smature weight, but given the nutritional limitations of pasture-based diets, this is difficult to

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The impact of the increasing growth rate of beef cattle on the proportion of daily energy used formaintenance versus growth in 1977 compared with 2007—the dilution of maintenance effect. Data adaptedfrom Capper (27). Abbreviations: ME, metabolizable energy; MJ, megajoules.

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achieve when mature cows approach or exceed 635 kg bodyweight. Although Notter et al. (43)reported some advantages of increased mature weight upon cow-calf system efficiency, if calfgrowth rates andweaningweights can bemaintained from cattle with amatureweight of less than580 kg, environmental sustainability will be improved. Furthermore, according toUSDepartmentof Agriculture data (44), only 89.1% of cattle produce a live calf each year in US systems; if thiswere increased substantially, the consequent reduction in population size required to support beefproduction would be expected to have a considerable effect upon beef’s environmental impact.

Conventional production systems contribute approximately 97% of total US domestic beefsupply and are characterized by forage-based cow-calf and backgrounder operations followedby an intensive finishing period on corn-based diets (45). Given the reliance of these systems onfossil fuel and fertilizer inputs for feed production and transportation, they may appear to havean intrinsically greater environmental impact than pasture-based systems. Indeed, Sithyphoneet al. (46) conclude that increased GHG emissions per animal confer an environmental dis-advantage for corn-finished beef cattle compared with their hay-fed compatriots in Japanesesystems. However, as discussed previously, assessing environmental impact on a per-head basisfails to account for the productivity of the system; in this instance, the slaughter weight of corn-fed cattle was almost double that of hay-fed cattle, which would have a considerable effect uponGHG emissions per unit of beef.

Both Capper (45) and Pelletier et al. (41) reported that GHG emissions per unit of beef meatwere greater in pasture-finished systems than in feedlot systems. Pelletier et al. (41) cite GHGemissions of 19.2 kg CO2-eq/kg liveweight for pasture-finished beef compared with 16.2 kg CO2-eq/kg liveweight for yearling-fed beef, whereas Capper (45) reports 26.8 kgCO2-eq/kg hot carcassweight beef for pasture-finished beef and 16.0 kg CO2-eq/kg hot carcass weight beef for feedlotbeef. In both studies, the increased GHG emissions associated with pasture-finished beef werea direct consequence of slower growth rates and lower slaughterweights. Pelletier et al. (41) furthershowed that calf-fed beef, i.e., a system in which calves bypass the backgrounder stage and enter

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Comparative resource use and waste outputs per unit of beef produced in US systems characteristic of 1977compared with 2007. Data adapted from Capper (27). Abbreviations: GHG, greenhouse gas.

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the feedlot directly as weaned calves, had the lowest GHG emissions (14.8 CO2-eq/kg liveweightbeef) as a consequence of an increased growth rate and thus fewer days to reach slaughter weightcompared with yearling-fed cattle. Although pasture-based beef production systems predomi-nated in the first half of the twentieth century within the United States, the increased land requiredto supply sufficient beef meat for the current domestic and international market would renderwhole-scale conversion of the US beef production system to pasture-fed production practicallyimpossible. However, if conversion did occur and annual beef production was maintained at 11.8billion kg (40), the increase in carbon emissions would be equal to adding 25.2 million cars to theroad on an annual basis (45).

Pasture-based beef finishing systems have the potential to reduce net GHG emissions throughcarbon sequestration. Pasture does not, however, sequester carbon indefinitely, nor does se-questration occur at a constant rate (47, 48). Over time, soil carbon concentrations reach anequilibrium beyond which no further sequestration occurs unless land is subjected to significantmanagement change (47,48). The present body of literature indicates that the degree to whichcarbon may be sequestered by crop- or pastureland is infinitely variable among systems and isdependent on amultitude of factors including land-use change, tillage, organic matter input, soiltype, and crop or pasture species (49, 50). Reliable data on carbon sequestration under a rangeof environmental conditions and global regions are notably lacking from environmental lit-erature, and this is one area where future research would pay dividends in bridging the currentknowledge gap.

The reliance of both conventional and pasture-based US beef systems upon pasture- andforage-based diets for animals within the cow-calf and backgrounder systems means that anypotential mitigating effect of carbon sequestration could be attributed only to differences in thefinishing period. Pelletier et al. (41) calculated that sequestration at a rate of 0.4 tons C/ha/yearwould reduce the GHG emissions from pasture-based beef production to 11.2 kg CO2-eq/kgliveweight. However, when differences in dressing percentage and thus beef yield per animalbetween pasture-finished and feedlot beef are considered, this would underestimate GHGemissions per unit of beef produced. Owing to greater GHG emissions from pasture-finishedbeef cattle in the study by Capper (45), sequestrationwould need to exceed 1.3 tons C/ha/year toproduce pasture-finished beef with GHG emissions similar to feedlot beef. Either estimate isa lofty target, given that Bruce et al. (51) suggest that the potential for carbon sequestration inwell-managed pastureland is 200 kg/ha, whereas Conant et al. (52) estimate the potential forsequestration at 540 kg/ha. Furthermore, complete comparisons of environmental effects needto be based on an equivalent production of meat and account for the increased requirement forland and feed, the greater supporting herd population (cows, calves, heifers, and bulls) conferredby slower growth rates and reduced slaughter weights in the pasture-finished system, and thepropensity for pasture-based diets to increase ruminal methanogenesis and thus enteric GHGemissions (53, 54). However, this is still complicated by the fact that approximately 24%of beefproduction results from dairy systems in the United States (either through the provision of cullcows or dairy calves raised for beef), thus a whole-system large ruminant analysis may berequired to properly assess the environmental impact of beef and dairy production in future.

RUMINANT LIVESTOCK’S ENVIRONMENTAL IMPACT: THE GLOBALPERSPECTIVE

Worldwide, ruminant livestock make a significant contribution to sustainability through pro-vision of nutrition via animal-source foods in combination with fertilizer, draft power, socialstanding, and economic income (3, 55, 56). Animal system productivity within developing regions

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generally is diminished owing to a combination of factors including inadequate nutrition (asa consequence of both feed quality and quantity and lack of nutritionally balanced diets), lackof access to genetic selection techniques, and increased incidence of livestock disease (3). Withreference to animal health, developed nations have seen a reduction in the burden placed by animaldisease as a result of improved veterinary services and vaccine availability and the implementationof preventative medicine programs (57), although concern is rising with regard to the emergenceand spread of new diseases such as avian influenza H5N1 and the Schmallenberg virus (58).Nonetheless, relatively little progress has been made in the developing world save for the erad-ication of rinderpest (59). The World Organization for Animal Health estimates that worldwide,more than 20%of animal protein is lost as a result of disease (60); thus, significant potential existsto reduce the environmental impact of global livestock production through improving health.

Global livestock production has increased substantially over the past 50 years—beef pro-duction has doubled, poultry meat production has increased almost tenfold, and both dairy andegg yields have increased by approximately 30% (61). Major international dairy regions (in-cluding the United States, Canada, New Zealand, and Europe) all have improved milk yield percow since the 1960s, the rate of improvement varying from 129 kg/year and 117 kg/year for theUnited States and Canada, respectively, to 77 kg/year and 24 kg/year for Europe and NewZealand (61, 62). A portion of the variation in the rate of improvement may be related to geneticselection priorities, for example the need for smaller-framed, lower-yielding cattle in antipodeansystems compared with the trend for increasing yields in the United States and Canada (63).Nevertheless, the environmental effects of regional productivity variation are exemplified by theresults of a recent FAO (15) report that modeled GHG emissions from dairy production usinglife-cycle analysis. As intensity of production declines and the average milk yield shifts fromapproximately 9,000 kg/cow for North America to ∼250 kg/cow for sub-Saharan Africa, thecarbon footprint increases from 1.3 kg CO2-eq/kg milk to 7.6 kg CO2-eq/kg milk (Figure 5). Ifenvironmental sustainability were the only consideration, the FAO data could provoke theconclusion that all regions should adopt North American– and Western European–style

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Average annual milk yield and carbon footprint per unit of energy-corrected milk across global regions. Dataadapted from Food Agric. Organ. (15).

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production systems, or that dairying should be focused in these areas and discouraged in less-productive regions such as sub-Saharan Africa and South Asia. However, the significant social(both status and nutritional) and economic value of dairying in less-developed regions must notbe underestimated. The challenge for global dairy production is to improve productivity andoptimize sustainability within each region rather than prescribe one-size-fits-all productionsystems or management practices.

At present, no comprehensive analyses have compared the environmental impact of beefproduction across global regions. A literature scan reveals a range of GHG emissions attributedto beef production from9.90 kgCO2-eq/kg carcass weight for intensive production in Australia(64) to 44.0 kg CO2-eq/kg carcass weight for Brazilian production with land-use change anddeforestation taken into account (65). Biologically, the dilution of maintenance concept wouldsuggest that improving productivity through intensification (as discussed previously withreference to US systems) should reduce environmental impact on a global basis, but a pasture-based Australian system (64) is cited as having GHG emissions per unit of beef considerablylower than those exhibited by a range of intensive systems (41, 45, 66–69). In this instance,a considerable amount of the variation in GHG emissions may simply be attributed to dif-ferences in methodology and system boundaries. For example, Ogino et al. (67) examined theenvironmental impact of the finishing system alone; Pelletier et al. (41) assumed that identicalcow-calf systems were used to supply calves to both calf-fed, yearling-fed, and pasture-basedfinishing systems; and Capper (45) included the effect of production-enhancing technology inthe analysis. As discussed by Bertrand & Barnett (70) with reference to dairy production, adefinitive methodology for comparing the environmental impacts of beef production systemswill be required in future.

FUTURE ON-FARM STRATEGIES TO ENHANCE SUSTAINABILITY OFRUMINANT PRODUCTION

Future gains in environmental sustainability can be achieved only through continuous im-provement within all sectors of ruminant production, with specific emphasis placed on im-proving productivity. Identifying the best management practices that can be applied throughoutthe national and global industries, without bias toward specific systems, will be key in en-couraging producers tomaximize efficiency and thus reduce environmental impact and improveeconomic viability. The use of production-enhancing technologies (PET) provides a clear op-portunity to improve environmental sustainability. Examples include technologies that alternutrient partitioning toward milk production (lactating animals) or lean muscle accretion(during growth), improve feed quality, enhance rumen fermentation and diet digestibility, in-crease reproductive performance, improve herd health programs, and promote animal welfare(28, 39). However, a dichotomy often exists between consumers’ desire for environmentallysustainable foods (71) and a mistrust of technology use within food production (3).

Recombinant bovine somatotropin (rbST) provides an example of PET use within dairyproduction. This technology alters nutrient partitioning, which results in an increase in dailymilk yield of an average of 4.5 kg per cow (39, 72). This increase affects environmental sus-tainability through the dilution of maintenance concept, the net effect being that rbST usereduces the amount of land required to produce a unit ofmilk by 9.2%,water use by 10.4%, andthe carbon footprint by 9.1% (39). On an industry basis, rbST supplementation of 1 millioncows would therefore reduce the dairy industry’s carbon footprint by the annual equivalent ofremoving ∼400,000 cars from the road. The mitigating effect of rbST use on environmentalimpact has also been noted by other investigators (72–77), including Johnson et al. (78), who

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suggested that large-scale use of rbST would reduce methane emissions by approximately 9%.Nonetheless, the political and social acceptability of rbST use within dairy production hasbeen a contentious issue in several countries (79–81).

As discussed previously, opportunities to improve beef system productivity through greaterslaughter weights are limited; however, considerable potential exists to further improve effi-ciency through improving growth rate, which thereby improves environmental sustainability(27, 45, 82). Technologies such as hormone implants, ionophores, and beta-agonists may beused effectively to improve growth rate, but these may be perceived as undesirable by theconsumer owing to concerns relating to animal welfare (83, 84), human health (85), or envi-ronmental impact (86). Nonetheless, perceived concerns may not follow through into consumerpurchasing behavior. Lusk et al. (87) demonstrated no difference in consumer valuation of beeffrom hormone-treated or nontreated animals in the United States, Germany, and the UnitedKingdom; however, such concerns are cited often by processors and retailers as rationales forprohibiting PET use within the supply chain. Capper &Hayes (88) demonstrated that, throughan increase in production costs, the global competitiveness of US beef would be reduced bywhole-scale PET removal, which would increase resource use on an annual basis and cumu-latively increase global GHG emissions through a deficit in US beef production being com-pensated for by increased production in less-efficient regions.

Technological approaches to directly reduce GHG emissions from ruminants include the in-clusionof tannins in the diet to reduce the release ofN2O frommanure (89), nitrification inhibitorsto reduceN losses from pastureland (90), and use of various approaches to reduce rumenmethaneproduction (91). Within the latter category, methane is of particular interest because, dependingon diet, ruminants lose 2–12% of digestible energy intake as methane (54). On a global basis,this represents ∼28% of methane production (92). Methane is a normal product of ruminalfermentation, representing a pathway for the disposal of metabolic hydrogen produced duringmicrobial metabolism. Therefore, strategies to reduce ruminal methane production center onreducing the population ofmicrobes involved inmethanogenesis or providing alternative sinks formetabolic hydrogen. These approaches include use of high-grain diets, addition of lipid sup-plements, chemical antimicrobials (e.g., bromoethanesulfonic acid), ionophores (e.g., monensin),and immunization against rumen methanogens (91–94). Most of the technologies for entericmethane abatement have shown somewhat inconsistent results. Althoughmethaneproduction canbe mitigated for short periods, the dynamic nature of the rumen ecology allows for adaptation asthe microbial population reverts to the initial fermentation pattern (93). Furthermore, mitigationstrategies often affect more than just methanogenesis such that rumen fermentation rates, di-gestibility, and intake are reduced, which thereby adversely affects animal performance (94, 95).Further scientific advances are inevitable within this field, but at present, productivity advancesappear to confer a greater environmental (and economic) gain than specific technologies thattarget GHG emissions.

COMPARISON OF ANIMAL SOURCE FOODSWITH PLANT SOURCE FOODS

Human diet quality is assessed by the extent to which it provides the entire complement ofhigh-quality protein, energy, minerals, trace metals, and vitamins necessary to meet humanrequirements. Consuming a high-quality diet is important for everyone, but children, preg-nant and lactating women, and the elderly are most vulnerable to nutritional inadequacies.The value of dairy products and beef meat (referred to as animal source foods) in meeting thefood security and nutritional needs of the global population is well recognized (96–98), andthey are included in dietary recommendations to promote human health and well-being by

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governments and public health organizations around the world. Dairy products and meat arenutrient-dense foods that represent the predominant, most affordable source for many es-sential dietary nutrients (99–102). Multidisciplinary studies in developing countries haveestablished that schoolchildren consuming diets with little or no animal source foods have aninadequate intake of essential micronutrients that results in negative health outcomes in-cluding poor growth, suboptimal cognitive performance, neuromuscular deficits, psychiatricdisorders, and mortality (96, 97). Meta-analyses of prospective cohort studies with diseaseevents and death as the outcomes also provide convincing evidence that consumption of milkand dairy products is associated with survival benefits in long-term health maintenance andwith the prevention of chronic diseases including diabetes, cardiovascular disease, and manytypes of cancer (103–105).

The environmental sustainability of animal agriculture systems is currently under scrutinyby both impartial scientific associations (9) and agenda-driven activist groups (11, 106). Theconsensus opinion is that animal agriculture uses a significant amount of resources and makesa significant contribution to global carbon emissions (9, 14). The majority of food-related GHGemissions are generated during farming; thus, there has been interest in using whole-systemapproaches to compare the environmental impact of animal source foods in comparison withplant source foods. The purpose of food consumption is to supply nutrients within a balanceddiet that sustains development, health, and well-being throughout the life cycle. Unfortunately,comparisons of the environmental sustainability among foods have not used a metric that isfunctional from an environmental perspective while recognizing the nutrient value of differentfoods. For example, studies comparing animal and plant food sources on the basis of GHGemissions per unit of mass or food energy (107–111) uniformly concluded that producing plantsource foods, such as cereal grains, rather than animal source foods minimized the carbonfootprint. Similar conclusions were reached by investigators evaluating GHG emissions per unitof selected macronutrients (e.g., protein) who concluded that the environmental impact of foodproduction could be mitigated by replacing dairy products and meat with plant source foods(109, 112–115). However, the latter comparisons did not recognize that animal source proteinshave a high digestibility and a near-ideal balance of essential amino acids, whereas plant proteinshave a lower bioavailability and are typically deficient in one or more essential amino acids (97,116). Given that food sources also differ in their composition of other essential macro- andmicronutrients, it is critical that these also be considered in comparisons of the environmentalsustainability of alternative food choices.

Nutrient density index, also referred to as nutrient profiling, is a system that allows com-parison of foods based on their full nutrient content (117, 118). Smedman et al. (119) were thefirst to use a nutrient density index in comparisons of the environmental sustainability of differentfood sources. They compared the provision of required nutrients (nutrient density,ND) in relationto GHG emissions (climate index, CI) for a variety of beverages, expressed as an index of the twometrics. As shown in Figure 6, milk had a substantially more favorable NDCI index than otherbeverages, including orange juice, soy drink, and oat drink. Animal source foods not only supplyhigh-quality and readily digested protein and energy but are also a compact and efficient source ofreadily availablemicronutrients. Clearly future considerations of the environmental sustainabilityof food sources needs to utilize an approach similar to that of Smedman et al. (119) so that theevaluations include a functional metric that is relevant from both a nutritional and an envi-ronmental perspective.

The suggestion that animal agriculture should be abolished and that the global populationcould subsist upon a vegetarian or vegan diet (11, 112, 120) is somewhat myopic. Most com-parisons are based on substituting plant source foods for animal source foods on the basis of mass

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or energy (calories), and these results are extrapolated to estimates of impact on GHG emissions.For example, the Environmental Working Group (11) ignored nutritional needs and publisheda report suggesting that whole-scale adoption of a vegetarian or vegan diet by the US populationwould reduce national GHG emissions by 4.5% annually, but the US EPA (8) allocates only 3.1%of total GHG to animal agriculture (including all food animals and equines). Less-extremereductions in consumption of animal source foods often are proposed as a solution to reducinganthropogenic carbon emissions, although Millward & Garnett (121) note that this poses sig-nificant nutritional challenges and would result in increased fortification of foods to provideessential nutrients. Nonetheless, the so-called Meatless Mondays campaign was invigorated byWeber&Matthews (111), who considered only the calories available from differing food choicesand concluded that changing from redmeat and dairy to fish, chicken, or vegetable sources for oneday per week’s worth of calories would mitigate GHG to a greater extent than buying all locallysourced food. However, a simple calculation based on US EPA data for the contribution of redmeat and dairy to national GHG emissions (3.05% in total) demonstrates that if that the entire USpopulation removed these food sources from their diet for one day perweek, it would reduceGHGemissions by a maximum of 0.44%, without accounting for adequacy of meeting nutritionalrequirements or the increased production of alternative food sources. Any attempt to reduceanthropogenic GHG emissions is laudable; however, it appears that far greater mitigation may beachieved through changes in other societal and industrial activities than simply by reducingmeatconsumption.

Finally, the use of by-products from human feed and fiber production as animal feedsmust beconsidered as part of any evaluation of the environmental sustainability of animal source foods(Table 1). Activist groups often cite ruminant production systems as being particularly in-efficient, as the grains fed to livestock could instead be used to fulfill human energy requirements.However, these claims are based on the assumption that all livestock feeds are human edible,whereas Wilkinson (122) demonstrates that a considerable proportion of livestock feeds are

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Comparative nutrient density/climate change indices for a range of beverages.Data fromSmedman et al. (119).

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human inedible; thus, the ratio of human-edible energy or protein inputs into animal productionsystems compared with human-edible energy or protein output in animal source foods is morefavorable than the traditional measures of feed efficiency would suggest. Furthermore, datafrom the USDA’s Economic Research Service (123) indicate that only 8% of US grazed land issufficiently productive to be classified as cropland pasture and therefore cannot be used forhuman food production aside from conversion into animal source foods via grazing. As noted byKock & Algeo (23) with reference to beef production, the entire ruminant industry must utilizeits competitive advantage of forage crops and by-product feeds in an arena where competitionbetween human food and livestock feed is ever increasing.

CONCLUSIONS AND FUTURE DIRECTIONS

The importance of productivity gains as mechanisms to improve the environmental sustain-ability of ruminant production systems is without question. Advances in genetics, nutrition,management, preventative medicine, and animal welfare have improved milk yields in dairycattle and both slaughter weights and growth rates in beef animals, which has led to reductionsin resource use and GHG emissions per unit of animal source foods. Animal source foods area principal source of essential nutrients, and continuous improvement in all sectors of dairy andbeef production will be of crucial importance in future food production systems to meet the dualchallenge of producing sufficient animal source foods to supply the growing population whilereducing environmental impact. Current research has focused on principal productivitymetrics,i.e., milk or meat yields, over time, but a considerable knowledge gap exists as to the contri-butionmade by other on-farm practices and herd dynamics, e.g., the specific effects of improvedhealth, reproduction, or animal bodyweight upon environmental impact. These knowledge gapsmust be filled for producers to make future management decisions based on economic viabilityand environmental sustainability. All stakeholders within food production need to gain agreater awareness of the multifaceted nature of sustainability to make informed production-system and dietary choices in future. This will involve assessing food products through a com-bination of environmental, nutritional, and economic metrics and will offer conventionallivestock producers the opportunity to reclaim the concept of sustainable food production,which is perceived currently as applying only to niche production systems.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

Table 1 By-products from human food and fiber production commonly usedin ruminant diets within US production systems

Almond hulls Dust

Apple pomace Distiller’s grains (dry or wet)

Bakery products Feather meal

Blood meal Peanut meal

Citrus pulp Potatoes and other vegetables

Corn gluten Soybean meal

Cottonseed meal Wheat pasture and straw

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Annual Review of

Animal Biosciences

Volume 1, 2013 Contents

After 65 Years, Research Is Still FunWilliam Hansel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

Cross Talk Between Animal and Human Influenza VirusesMakoto Ozawa and Yoshihiro Kawaoka . . . . . . . . . . . . . . . . . . . . . . . . . 21

Porcine Circovirus Type 2 (PCV2): Pathogenesis and Interaction withthe Immune SystemXiang-Jin Meng . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43

Evolution of B Cell ImmunityDavid Parra, Fumio Takizawa, and J. Oriol Sunyer . . . . . . . . . . . . . . . . . . 65

Comparative Biology of gd T Cell Function in Humans, Mice,and Domestic AnimalsJeff Holderness, Jodi F. Hedges, Andrew Ramstead,and Mark A. Jutila . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99

Genetics of Pigmentation in Dogs and CatsChristopher B. Kaelin and Gregory S. Barsh . . . . . . . . . . . . . . . . . . . . . . 125

Cats: A Gold Mine for OphthalmologyKristina Narfström, Koren Holland Deckman,and Marilyn Menotti-Raymond . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157

Comparative Aspects of Mammary Gland Development andHomeostasisAnthony V. Capuco and Steven E. Ellis . . . . . . . . . . . . . . . . . . . . . . . . . . 179

Genetically Engineered Pig Models for Human DiseasesRandall S. Prather, Monique Lorson, Jason W. Ross,Jeffrey J. Whyte, and Eric Walters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203

Accelerating Improvement of Livestock with Genomic SelectionTheo Meuwissen, Ben Hayes, and Mike Goddard . . . . . . . . . . . . . . . . . . 221

vi

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Integrated Genomic Approaches to Enhance Genetic Resistancein ChickensHans H. Cheng, Pete Kaiser, and Susan J. Lamont . . . . . . . . . . . . . . . . . . 239

Conservation Genomics of Threatened Animal SpeciesCynthia C. Steiner, Andrea S. Putnam, Paquita E.A. Hoeck,and Oliver A. Ryder . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261

Phytase, A New Life for an “Old” EnzymeXin Gen Lei, Jeremy D. Weaver, Edward Mullaney, Abul H. Ullah,and Michael J. Azain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 283

Effects of Heat Stress on Post-Absorptive Metabolism and EnergeticsLance H. Baumgard and Robert P. Rhoads Jr. . . . . . . . . . . . . . . . . . . . . 311

Epigenetics: Setting Up Lifetime Production of Cows by ManagingNutritionR.N. Funston and A.F. Summers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 339

Systems Physiology in Dairy Cattle: Nutritional Genomicsand BeyondJuan J. Loor, Massimo Bionaz, and James K. Drackley . . . . . . . . . . . . . . 365

In Vivo and In Vitro Environmental Effects on MammalianOocyte QualityRebecca L. Krisher . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393

The Equine Endometrial Cup Reaction: A Fetomaternal Signalof SignificanceD.F. Antczak, Amanda M. de Mestre, Sandra Wilsher,and W.R. Allen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419

The Evolution of Epitheliochorial PlacentationAnthony M. Carter and Allen C. Enders . . . . . . . . . . . . . . . . . . . . . . . . . 443

The Role of Productivity in Improving the Environmental Sustainabilityof Ruminant Production SystemsJudith L. Capper and Dale E. Bauman . . . . . . . . . . . . . . . . . . . . . . . . . . 469

Making Slaughterhouses More Humane for Cattle, Pigs, and SheepTemple Grandin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 491

Contents vii

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AnnuAl Reviewsit’s about time. Your time. it’s time well spent.

AnnuAl Reviews | Connect with Our expertsTel: 800.523.8635 (us/can) | Tel: 650.493.4400 | Fax: 650.424.0910 | Email: service@annualreviews.org

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Annual Review of Statistics and Its ApplicationVolume 1 • Online January 2014 • http://statistics.annualreviews.org

Editor: Stephen E. Fienberg, Carnegie Mellon UniversityAssociate Editors: Nancy Reid, University of Toronto

Stephen M. Stigler, University of ChicagoThe Annual Review of Statistics and Its Application aims to inform statisticians and quantitative methodologists, as well as all scientists and users of statistics about major methodological advances and the computational tools that allow for their implementation. It will include developments in the field of statistics, including theoretical statistical underpinnings of new methodology, as well as developments in specific application domains such as biostatistics and bioinformatics, economics, machine learning, psychology, sociology, and aspects of the physical sciences.

Complimentary online access to the first volume will be available until January 2015. table of contents:•What Is Statistics? Stephen E. Fienberg•A Systematic Statistical Approach to Evaluating Evidence

from Observational Studies, David Madigan, Paul E. Stang, Jesse A. Berlin, Martijn Schuemie, J. Marc Overhage, Marc A. Suchard, Bill Dumouchel, Abraham G. Hartzema, Patrick B. Ryan

•The Role of Statistics in the Discovery of a Higgs Boson, David A. van Dyk

•Brain Imaging Analysis, F. DuBois Bowman•Statistics and Climate, Peter Guttorp•Climate Simulators and Climate Projections,

Jonathan Rougier, Michael Goldstein•Probabilistic Forecasting, Tilmann Gneiting,

Matthias Katzfuss•Bayesian Computational Tools, Christian P. Robert•Bayesian Computation Via Markov Chain Monte Carlo,

Radu V. Craiu, Jeffrey S. Rosenthal•Build, Compute, Critique, Repeat: Data Analysis with Latent

Variable Models, David M. Blei•Structured Regularizers for High-Dimensional Problems:

Statistical and Computational Issues, Martin J. Wainwright

•High-Dimensional Statistics with a View Toward Applications in Biology, Peter Bühlmann, Markus Kalisch, Lukas Meier

•Next-Generation Statistical Genetics: Modeling, Penalization, and Optimization in High-Dimensional Data, Kenneth Lange, Jeanette C. Papp, Janet S. Sinsheimer, Eric M. Sobel

•Breaking Bad: Two Decades of Life-Course Data Analysis in Criminology, Developmental Psychology, and Beyond, Elena A. Erosheva, Ross L. Matsueda, Donatello Telesca

•Event History Analysis, Niels Keiding•StatisticalEvaluationofForensicDNAProfileEvidence,

Christopher D. Steele, David J. Balding•Using League Table Rankings in Public Policy Formation:

Statistical Issues, Harvey Goldstein•Statistical Ecology, Ruth King•Estimating the Number of Species in Microbial Diversity

Studies, John Bunge, Amy Willis, Fiona Walsh•Dynamic Treatment Regimes, Bibhas Chakraborty,

Susan A. Murphy•Statistics and Related Topics in Single-Molecule Biophysics,

Hong Qian, S.C. Kou•Statistics and Quantitative Risk Management for Banking

and Insurance, Paul Embrechts, Marius Hofert

Access this and all other Annual Reviews journals via your institution at www.annualreviews.org.

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