The Nexus of Environmental Quality and Livestock Welfare

arav2Mitloehner ARI 27 August 2013 22:37

The Nexus of EnvironmentalQuality and LivestockWelfareSara E. Place1 and Frank M. Mitloehner2,�

1Department of Animal Science, Oklahoma State University, Stillwater, Oklahoma74078; email: [email protected] of Animal Science, University of California, Davis, California 95616;email: [email protected]

Annu. Rev. Anim. Biosci. 2014. 2:1.1–1.15

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

This article’s doi:10.1146/annurev-animal-022513-114242

Copyright © 2014 by Annual Reviews.All rights reserved

�Corresponding author: Address: 2251Meyer Hall,One Shields Avenue, Davis, CA 95616

Keywords

climate change, air quality, water quality, stress, animal well-being

Abstract

In recent years, the livestock production industry has been receivingpressure to assess and improve production practices in two seeminglyunrelated areas: environmental quality and animal welfare. In this ar-ticle, we argue that the nexus of these two areas of study should bea priority for future research and that the integration of these disci-plines in research, extension, and education efforts has the potentialto improve the sustainability of production livestock agriculture.

1.1

Review in Advance first posted online on September 6, 2013. (Changes may still occur before final publication online and in print.)

Changes may still occur before final publication online and in print

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mailto:[email protected]

mailto:[email protected]

animal.annualreviews.org

INTRODUCTION

In the coming decades, responsibly meeting growing demand for animal products (e.g., meat andmilk) will present a serious challenge. The specific definition of responsible animal productionwilllikely vary by region and culture; however, any future definition of responsible animal proteinproduction can be expected to include considerations of environmental stewardship and animalwelfare.

By 2050, the world population is expected to reach over 9 billion people, and, combined withincreasing incomes in developing nations leading to higher per capita consumption of animalproducts, global dairy and meat consumption are expected to increase by 74% and 58%, re-spectively (1). The increased demand for animal products in developing nations has already led toan increase in livestockpopulations in these nations; however, this is likely anunsustainableway tomeet future demand owing to negative environmental impacts (2). To meet growing demand,between2000and2011,China increased its pig populationby32million (a 7% increase),whereasBrazil increased its cattle population by 42.9 million head (a 25% increase) over the same timeperiod (3). Cultural differenceswill partially determine the extent of the per capita increase and thetype of animal protein that will be the most popular (4), as well as the complicated issue of what isaccepted as proper welfare or well-being for farm animals used in food and fiber production.

In the United States andWestern European nations, both livestock’s impact on environmentalquality and the welfare of livestock have moved to the forefront of public concern and have led tochanges in public policy. However, these issues often are approached separately without ac-knowledgment or understanding that they are intertwined. In the following article, we brieflydiscuss the major issues facing the livestock industries in both of these areas, and we put forwardthe case thatmore interdisciplinary research is needed to ascertain the critical relationship betweenenvironmental quality and animal welfare and to better inform public policy and improve thesustainability of livestock production.

LIVESTOCK ENVIRONMENTAL QUALITY SCIENCE

Environmental quality concerns surrounding livestock production can be broken down in severalways, but for the purpose of this review, we discuss the air emissions that result from livestock andtheir waste as well as soil- and water-quality issues (Table 1). Interest in greenhouse gas (GHG)emissions from livestock agriculture has been growing in the past two decades, with increasingawareness of the consequences of anthropogenic climate change and a desire to find strategies tomitigate GHG emissions. Other air pollutants from livestock agriculture have come under par-ticular scrutiny in regions that suffer frompoor air quality, such asCalifornia’s San JoaquinValley,which has led to governmental emissions regulations for livestock operations as well as seriousefforts by researchers to characterize emission sources. Issues of water quality were the first area offocus, leading to regulationof concentrated animal feedingoperations (CAFOs) byUSgovernmentagencies under the Clean Water Act, but concerns have expanded into the impacts of CAFOs onhuman health (e.g., impacts of air-pollutant emissions on human respiratory health) (5). Thefollowing sections act as aprimer for themajor sources from livestock agriculture for each categoryof concern.

Air Emissions

Air emissions from livestock production can be categorized broadly into GHG emissions [e.g.,methane (CH4) and nitrous oxide (N2O)] and all other air-pollutant emissions [e.g., ammonia(NH3)]. GHG emissions are often standardized to 100-year carbon dioxide equivalents (CO2e)

1.2 Place � Mitloehner



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because different GHGs have different global warming potentials, or abilities to trap heat in theatmosphere, given their dissimilar radiative forcings (i.e., the change they impose on the Earth’sradiation balance) and lifetimes in the atmosphere (6). For the 2007 International Panel onClimateChange report (7), the 100-year CO2e of CH4 and N2O were 25 and 298, respectively, meaningthat the potential for these gases to trap infrared radiation is 25 and 298 times that of CO2 overa 100-year timescale.

CO2 from animal respiration is generally not considered a net source of GHG emissions fromlivestock production, as it is assumed that the carbon sequestered via photosynthesis by the plantsthe livestock are consuming is equal to the respiratory carbon the animals release (4). Emissions ofCO2 from the burning of fossil fuels associated with livestock production (e.g., CO2 emissionsfrom equipment used to harvest crops and transportation vehicles) is generally considereda source; however, life-cycle assessments often find these emissions to be a small proportionof totalCO2e emissions per unit of production (e.g., per kg of energy-corrected milk) from livestockagriculture when considering the entire supply chain (8).

CH4 emissions from livestock agriculture generally result either from enteric fermentation inthe digestive tracts of ruminants (e.g., cattle, sheep, and goats) or from manure of all livestockspecies stored under anaerobic conditions, which account for 23% and 9% of US CH4 emissions,respectively (9). In both instances, obligate anaerobic microorganisms known as methanogenicarchaea are directly responsible for CH4 emissions. In ruminants, CO2 and hydrogen (H2) gasresult as by-products of bacterial fermentation of the animal’s feed, and these are the primarysubstrates used by methanogenic archaea for energy production in those organisms’ electrontransport chains during methanogenesis (CH4 production) (10). The removal of H2 via themethanogenic pathway plays an important role in the rumen because as the partial pressure of H2

increases, the rate of rumen fermentation is slowed, limiting the animal’s ability to extract nutritivevalue from its diet (11). Total CH4 emissions per animal per daywill depend largely on the forage-to-concentrate ratio of the diet, the level of feed intake, the degree of fat inclusion in the diet, thedigestibility of the carbohydrates in the diet, and the presence of any feed additives that may alterthe microbial populations of the rumen (e.g., monensin) (12). Enteric CH4 emission-abatementstrategies that attempt to directly reduce emissions per animal have been reviewed extensively

Table 1 Major categories of environmental quality concerns from livestock agriculture

Item Source(s) from livestock production Area of concern

Carbon dioxide (CO2) Fossil fuel combustion, respiration Climate change

Methane (CH4) Enteric fermentation, anaerobically stored manure Climate change

Nitrous oxide (N2O) Manure-amended soil Climate change

Ammonia (NH3) Manure Air quality, eutrophication, odor

Volatile organic compounds Fermented feeds, fresh manure Tropospheric ozone formation

Particulate matter Dry-lot housing for livestock, formation from ammonia Air quality

Nitrate (NO3�) Manure-amended soil Eutrophication

Phosphorus runoff Manure-amended soil Eutrophication

Salts Manure-amended soil Soil quality

Bacteria Manure-amended soil Soil and water quality

Antimicrobials Manure-amended soil Soil and water quality

1.3www.annualreviews.org � Environment and Livestock



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elsewhere (13–15). In anaerobically storedmanure, the fermentation of organicmatter also resultsin the formation of CO2 andH2, which can be used for methanogenesis, and the total yield of CH4

from stored manure depends primarily on the pH, temperature, absence or presence of oxygen,substrate availability, and presence of any inhibiting compounds (16).

N2O emissions related to livestock agriculture are typically associated with emission from soilthat has been fertilized with manure or solid manure storage systems (16). Denitrification is theprimary microbial metabolic pathway that can result in N2O emissions, as nitrate (NO3

�) isreduced to dinitrogen (N2) gas under anaerobic conditions; however, N2O emissions can alsoresult from the nitrification pathway as ammonium (NH4

þ) is oxidized to NO3� (17).

Air-quality issues from livestock agriculture primarily result from manure and fermentedfeedstuffs; however, air pollutants also result from fossil fuel combustion in farm equipment[e.g., oxides of nitrogen (NOx) released from diesel fuel combustion in tractors]. The primaryair pollutant that results frommanure isNH3, and livestock are estimated to be the single largestsource of NH3 emissions in the United States, producing 71.3% of annual emissions (18). NH3

results from the mixing of urine and feces (together, manure), with the urea in urine hydro-lyzed by the enzyme urease found in livestock feces. The rate of hydrolysis of urea is deter-mined by the degree of mixing of the urine and feces, as well as the presence of any ureaseinhibitors. Volatilization of NH4

þ in the liquid phase to NH3 gas is dependent on pH, tem-perature, andwind speed; therefore,NH3 emissions froman animal feeding facility can be highlyvariable and dependent on season, manure management practices, and the level of protein in thediet (19).

Particulate matter (PM) emissions can occur from livestock facilities through the locomotionof the animals on dry lots, the exhaust of animal-housing ventilation systems, or the movementof farm equipment on site or indirectly through the formation of secondary aerosol particles thatform in part from NH3 emissions from the livestock manure (20, 21). Both visibility and humanhealth can be negatively impacted by PM emissions (22, 23). Volatile organic compounds (VOC)result primarily from the fermented feeds fed to livestock (24), though someminor emissions resultfrom the fresh manure of livestock as well (25). Photochemical ozone (O3) production is driven inpart by VOC, as VOC can lead to oxidation of NO to NO2 (together known as NOx), and in thepresence of sunlight, O3 production can result (26). Not all VOC have the same potential to drivethe formation ofO3 (27), andmany of theVOC that are emitted in large quantities from fermentedfeeds (e.g., acetic acid) have low ozone-formation potentials relative to other anthropogenicsources (24). Nonetheless, in regions such as California’s San Joaquin Valley, where sunlight,NOx, and fermented feeds for cattle are abundant, VOC from livestock production can bea significant source of air pollution (24).

Water and Soil Quality

Soil- and water-quality issues surrounding livestock are generally related to manure-amendedagricultural land and runoff from livestock facilities. However, with nitrogen there is overlapbetween gaseous NH3 emissions and water quality, because NH3 in the atmosphere can be de-posited either dry (particles) or wet (precipitation) near the originating livestock facility and cancontribute to nitrogen pollution in waterways not adjacent to the facility (28). Nitrates andphosphorus are typically the nutrient pollutants of concern regarding water quality. Nitrates canresult from manure NH4

þ undergoing nitrification processes to NO3� in manure-amended soil.

Once in the form of NO3�, the nitrogen can easily be lost from the soil structure via leaching into

groundwater, which is a concern for the health of animals and humans, depending on thegroundwater source for drinking water (29). Phosphorus is much less likely to be lost through




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leaching, as it is closely associated with soil particles; therefore, as a source from livestock ag-riculture it is typically lost through soil erosion and in runoff from agricultural fields applied withmanure (30). Both nitrogen and phosphorus contribute to the eutrophication of water bodies andwaterways (e.g., the Chesapeake Bay and Gulf of Mexico).

Similarly, soil quality is influenced by the availability of nitrogen and phosphorus, as these areessential nutrients for plant growth, but also by other constituents, such as salts (31), bacterialcontent (32), and antibiotics (33). A complete review of all of these soil-quality considerations is,like the other categories of environmental impact, beyond the scope of this review; however, thereare reviews that can be consulted for further information regarding the impacts of livestockagriculture on soil quality (34�36).

ANIMAL WELFARE SCIENCE

History and Definition

The welfare of domesticated animals is a relatively new discipline and one created out of ethicalconcerns, which sets it apart from many other disciplines in animal science, such as nutrition,physiology,or reproduction(37). Public concern in theUnited States over thewelfare orwell-beingof farm animals in the early twentieth century was primarily instigated by fears regarding foodsafety sparked by Upton Sinclair’s novel The Jungle (38), which contributed to the passage of thePure Food and Drug Act (1906) and created the antecedent of the Food and Drug Administration(39). As US livestock operations have continued to increase in size since World War II, publicinterest in the welfare of animals on larger farming operations has grown. Many in the generalpublic now have a negative perception of modern livestock farming (40), driven in part by books,such as Ruth Harrison’s Animal Machines, which coined the term “factory farming” (41), andAnimal Factories by Jim Mason & Peter Singer (42), as well as several recent, well-publicizedincidences of inhumane treatment of animals on farms and in slaughterhouses (43�45). Addi-tionally, because fewer than 2% of Americans are involved in production agriculture today (46),the sight of production practices considered routine to farm workers and operators can be viewedas shocking and interpreted as not beneficial to the animals’ welfare to many unfamiliar withlivestock production (47). It is in this complicated environment that animal welfare science hasevolved and undergone several definitional debates, while researchers have grappled with howbest to address the concerns of the public and livestock producers objectively (for more in-formation, see sidebar, Five Freedoms).

In defining andmeasuring animal welfare, the value systems of individuals and cultures impactboth the research questions asked by scientists and what is considered ethical, acceptable treat-ment of animals; thus, researchers may rigorously design and execute experiments, but valuejudgments will influence the interpretation of what the results mean for the animal’s welfare (37,48). Fraser et al. (49) produced a robust concept of animal welfare [though scientists currently usemany competing definitions (50)], defining it as a balance between biological function, naturalliving, and the affective state of the animal. Fraser et al. (49) argued that scientists need toconsider all three ethical concerns, because considering only one at a time would give an in-complete picture of an animal’s welfare and would limit the science’s ability to address thepublic’s concerns. For example, some (51) have argued physiological measures should be theonly indicator of animal welfare; however, such a narrow definition would ignore the ethicalconcerns that certain animal housing systems inhibit animals’ natural behaviors, which havedriven public initiatives likeCalifornia’s Proposition 2 (Prevention of FarmAnimalCrueltyAct).To further explain the more multifaceted definition of animal welfare, the following sections




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briefly outline the three major criteria of animal welfare and the indicators used by animalwelfare scientists to assess each component.

Biological Function

The biological-function aspect of welfare is concerned with the health of the animal and theanimal’s productivity. For livestock producers, a highly productive animal (e.g., a cow producinghigh yields ofmilk) is often viewed to be in a good state ofwelfare. Conversely, animals that are notas high performing are considered to be in a poor state of welfare. With regard to the effects ofdisease and stressors on an animal’s performance, there is merit with this definition. Disease canimpact an animal’s growth (52), reproductive function (53), and milk yield (54). However, ifproductivity is defined solely through economicmeans, themost productive systemof housing andmanaging livestock may not ensure a good state of welfare. Increasing stocking rates withina housing systemmay increase the livestock’s economic productivity for the producer butmay alsonegatively impact the other areas of an animal’s welfare by causing social stress (37, 55). Anotherexample would be isolated housing systems for neonatal dairy calves for the purpose of diseaseprevention; whereas the limited contact with other calves may decrease the spread of pathogens,the social isolation may negatively impact other aspects of the animal’s welfare (56).

Affective State

The affective state of the animal can be defined simply as how the animal feels, which encompassesboth physical and psychological aspects. The feelings an animal experiences may be negative (e.g.,pain or suffering) or positive (e.g., joy and contentment) in nature (57), with farm animals able toexperience a continuumof emotions (58).When assessing the affective state of an animal, scientistsuse a variety of methods, which include trying to understand the cognitive state of the animal (57),physiologic or immunologicalmeasures (59, 60), andbehavior (54).Although there is currently nouniversal methodology to assess the animal’s affective state, there is much agreement that because

FIVE FREEDOMS

In Great Britain, concerns regarding farm animal welfare were heightened in the 1960s following the publication ofAnimalMachinesbyRuthHarrison (41),which led to an investigative report, called theBrambell Report, released inDecember 1965. This report contained the origins of what has become known as the Five Freedoms and has beenadopted by the FarmAnimalWelfare Council (FAWC) in the United Kingdom (90) and theWorldOrganization forAnimal Health (OIE), among others (91). These five guidelines have been the focal point of many European farmanimal welfare regulatory frameworks and are as follows:

1. Freedom from Hunger and Thirst—by providing ready access to fresh water and a diet to maintain fullhealth and vigor.

2. Freedom from Discomfort—by providing an appropriate environment, including shelter and a comfort-able resting area.

3. Freedom from Pain, Injury, or Disease—by ensuring prevention or rapid diagnosis and treatment.4. Freedom toExpressNormalBehavior—byproviding sufficient space, proper facilities, and companyof the

animal’s own kind.5. Freedom from Fear and Distress—by ensuring conditions and treatment that avoid mental suffering (90).




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livestock are sentient beings, concern about their affective state is the principal reason we(i.e., humans) care about their welfare when compared with that of other organisms (e.g., plantsand insects) (50).

Natural Living

The natural behaviors or natural living aspects of animal welfare are a challenge to define andexplain, because livestock are domesticated animals; therefore, which behaviors or living con-ditions are natural versus unnatural can be unclear. However, the naturalness of how animals areraised andmanaged is important to a growing number of consumers inwestern nations (61) and isa driving force behind many of the recent US legislative efforts to impact animal welfare (43).Alternative housing systems for livestock that are perceived as more closely mimicking nature areoften put forward by those advocating for improved animal welfare. However, such systems canoften impact the other ethical areas ofwelfare.One such example is outdoor sow-housing systems.These systems allow sows to express their behaviors in a way more similar to their wild ancestors;however, there is also an increased incidence of piglet mortality in these systems when comparedwith conventional housing systems that use farrowing crates (62). Another example is access topasture for dairy cattle. Legrand et al. (63) found that when given the choice between pasture andfree-stall barn housing, dairy cows spent more time on the pasture at night and more time in thebarn during the daylight hours, particularly in warmer temperatures. Presumably, the lack ofshade on the pasture during the warmer days was not as desirable for the cows as the shaded free-stall barn (63). As these examples demonstrate, finding the balance between allowing domesti-cated animals to live more naturally, their biological function, and their affective state can bedifficult to discern.

NEXUS OF LIVESTOCK ENVIRONMENTAL QUALITY AND ANIMALWELFARE

At its essence, agriculture is about transforming rawmaterials and natural resources into food andfiber products of higher value to humans. During this transformation, losses occur and pollutantscan be created, as outlined previously. When considering the mitigation of livestock production’simpacts on environmental quality, it is important to use appropriate metrics to quantify thoseimpacts. In the context that agricultural food production is necessary for civilization and that weface certain near-term growth in global demand for animal agriculture products, measuringenvironmental impacts of livestock on a per-animal-per-day basis would be inappropriate. Sucha strategywould lead to conclusions that cattle that produced fewer enteric CH4 emissions per daywould be more environmentally benign without consideration of the human nutritional valuegenerated by those cattle per day or per lifetime (i.e., kg of energy- and protein-corrected milk perday or kg of beef produced per cow). A more appropriate metric would be environmental impactper unit of production (e.g., all air, water, and soil impacts per kg of pork), which has been thestrategy used in more recent analyses of environmental impacts of animal products by bothuniversity researchers and industry-commissioned analysts (8, 64). Additionally, using a per-animal-per-day approach to measure environmental impacts misses the opportunities to makeefficiency improvements over the animal’s entire lifetime that may be observed only on a per-unit-of-output basis but are masked when considering impacts per animal per day. As Figure 1demonstrates with an example of a dairy cow’s life cycle, although the animal may be producingpotential environmental pollutants every day of its life (e.g., NH3 and CH4 emissions), the totalenvironmental impacts must be weighed against the total human nutritional value produced asa result of the animal’s life.When the dairy cow’smilk production can bemaximized relative to the




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times in the animal’s life when she is not producing milk (i.e., the unproductive proportion of thecow’s life), her environmental impact per unit of production can be minimized. Therefore, theproportion of an animal’s life spent being productive must be considered when quantifying ormitigating environmental impacts. This concept can be extended beyond just one animal’s life tothe total population of animals on an individual livestock operation or within a region. Improvingthe production efficiency of livestock has been discussed previously as way to mitigate envi-ronmental impacts (13). Historical analyses of the US beef and dairy industries (65, 6) haverevealed that improvements in animal management have been an important factor in loweringenvironmental impacts per unit of production and have greatly reduced the total number ofanimals required to meet demand.

When measuring environmental impacts and pollution-mitigation opportunities per unit ofoutput, the nexus of animalwelfare issues and environmental quality emerges (Figure 2). In certainareas of environmental quality, such as manure management and feed management (e.g., silagemanagement that impacts VOC emissions), there is little direct overlapwith animal welfare issues.Similarly, some painful procedures that clearly influence animal welfare by impacting the animal’saffective state (e.g., dehorning and tail docking) can have varying degrees of impact on the animal’sproduction efficiency and, consequently, fall into the nexus area to varying degrees. Therefore, insomebut not all cases, improved animalwelfare can translate intomore efficient conversion of feednutrients into growth, milk, and conceptus and a longer productive life for the animal. Furtherexplanation and specific nexus examples are given in the following sections.

Nexus Examples

Heat stress. Heat stress occurs when an animal’s capacity to maintain its body temperaturerequires energy expenditure above maintenance requirements, which can impact the other pro-ductive functions of the animal (67). St-Pierre et al. (68) estimated that heat stress costs the USlivestock and poultry industries $1.7–2.4 billion annually. The economic impacts are primarilydriven by decreased productivity of livestock in the form of decreasedmilk yields and growth. Theimpacts of heat stress are not only losses of milk production and growth but also negative impactson the reproductive success of animals, which can have negative impacts far after the time of theinitial heat stress (69). Furthermore, as Baumgard & Rhoads (70) reviewed, milk-productionlosses in dairy cattle during heat stress cannot be solely attributed to decreases in feed intake by the

Unproductive life

Productive life

Milk yield Milk yieldMilk yield

Birth Death Meat

Total lifetime human nutritional value

Total impacts on environmental quality

Figure 1

A representation of the life cycle of a dairy cow. Blue shaded areas are products of human nutritional value. The number of lactations,the calving-to-conception interval, the proportion of the cow’s life spent in the unproductive state, and the amount of milk pro-duced per lactation will all impact the metric of measuring environmental impact.




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heat-stressed animals. In an elegant experiment, Rhoads et al. (71) pair-fed dairy cows housed inenvironmentally controlled chambers that either were thermoneutral or induced heat stress toinvestigate the impacts of heat stress beyond reduced feed intake. They found that the heat-stresseddairy cows had significantly altered postabsorptive metabolisms that made them less efficient atconverting feed nutrients and body reserves into milk production (71). The implication of thisdifference in efficiency is that the non-heat-stressed dairy cattle would likely have a lower en-vironmental impact per unit of energy- and protein-corrected milk when compared with the heat-stressed cattle. When considering the decreased reproductive performance of cattle undergoingheat stress, the implication is that a larger supporting herd of dairy cattle likely would be requiredto produce the same amount of milk. The same principles would apply to meat animals, such asbeef cattle and swine.

Heat-stress-abatement techniques vary in their effectiveness by the climate of the region (67).Provision of shade has been shown to improve the feed efficiency of growing beef cattle and toreduce antagonist behaviors (72, 73). Additionally, Mitlöhner et al. (72) found that there wasa greater incidence of dark cutters for unshaded cattle compared with shaded cattle, which isanother indicator of reduced welfare, is an economic cost to livestock producers, and reducescarcass quality and yield (74). Thus, heat-stress abatement can improve not only an animal’swelfare but also the efficiency of converting feed nutrients that have low human nutritional valueinto higher-value human food and fiber products (e.g., beef and leather). Although animalsprovided shade tend to eatmore than unshaded cattle (and presumably excretemore nutrients intothe environment per day), the improvement in the gain-to-feed ratio and higher final carcassweights should result in lower negative environmental-quality impacts per kg of beef; however, tothe authors’ present knowledge, such an analysis of the potential of heat-stress mitigation to alterthe environmental impact of beef or any other livestock commodity has yet to be undertaken.

Handling, management, and facilities. Animal handling, management, and facility design aregreatly linked to welfare inmanyways and have often been the focus of legislative efforts in recent

Animal welfareEnvironmental quality(impacts per unit of production)

Nexus

• Environmental enrichment

• Painful procedures

• Feed management

• Manure management

• Heat stress

• Lameness

• Genetics

• Transport

• Nutrition

Figure 2

The nexus of issues that impact both environmental quality and animal welfare. Items within interceptrepresent issues that are impactful to both areas of concern. Areas removed from the intersect are impactfulin either environmental quality or animal welfare, but not both.




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years. Animal handling and the temperament and personality of the stockperson have been shownto be significantly associated with dairy cow welfare and milk production (75–77). Proper han-dling and facility design are critical factors in determining the welfare of all livestock species, atthe farm when carrying out routine management practices, during transportation, and atslaughter (78).

Lameness in dairy and beef cattle provides a strong example of the potential to improvewelfarein concert with environmental impact per unit of production and is an issue with multifacetedcauses, including facility design and nutrition (56, 79). Lameness impacts the dairy cow’s milkyield and reproductive success and the length of her productive life (80, 81). These effects on theanimal’s life cycle influence the environmental quality impacts per unit of energy- and protein-corrected milk by reducing the total milk yield the cow will produce in her lifetime relative to hertotal nutrient excretion (i.e., feces, urine, and enteric CH4). Additionally, these impacts havenegative economic implications for the dairy farmer. Unfortunately, rates of lameness in the dairyindustry can be quite high. In a recent survey study, von Keyserlingk et al. (82) conducted lo-comotion scoring of dairy cattle on farms in British Columbia (42 farms), California (39 farms),and the northeastern United States (40 farms). Mean rates of clinical lameness [a score of �3 ona 1–5 scale where 1 ¼ sound and 5 ¼ severely lame (83)] were found to be 27.9% in BritishColumbian, 30.8% in Californian, and 54.8% in northeastern US dairies (82). The issue oflameness in dairy cattle is not confined to North America. Barker et al. (84) used a four-pointlocomotion scale to evaluate lameness (0¼ sound, 3¼ severely lame) and found a mean lamenessrate (a score of�2) of 36.8% across 205 dairy farms in England andWales. For both studies, andothers that have conducted on-farm assessments of dairy cattle lameness, the range in lamenessincidence across dairies can be wide-ranging, implicating management and the environment thecattle are housed in as major determining factors.

Furthermore, lameness is not solely an issue for the dairy and beef industries. Lameness in sowsis one the major reasons for culling; a 2007 study of the US swine industry found that 15.2% ofbreeding-age females were culled owing to lameness (85). Anil et al. (86) found that sow longevityon a farm is significantly influenced by the incidence of lameness; thus, as with dairy cattle andother livestock species, lameness is not only an animal welfare concern but an issue that influencesthe proportion of an animal’s life it spends being productive, which can influence environmentalimpacts per unit of production.

In the United States, farm animal welfare is not regulated by the federal government until theanimal is transported and reaches a slaughter facility. The Humane Slaughter Act was first passedin 1958 and was updated to its current status in 1978. Today it is the primary piece of US legis-lation enforcedby theUSDepartment ofAgriculture’s Food Safety and Inspection Service (FSIS) atUS livestock slaughterhouses (poultry are excluded) (87). Cattle handling and transport prior toslaughter can have a significant impact on the carcass yields of animals being slaughtered.Mortality losses during transportation not only are a great concern for animal welfare but alsorepresent a great waste of the inputs used to grow the animal for its entire life, because mortalitiesduring transportation will not contribute any human nutritional value. Welfare concerns thatintersect with environmental quality for transportation prior to slaughter go beyond simplymortalities and include increased incidences of bruising and dark cutters on carcasses (88).

Additionally, transportation of animals at stages of their life before slaughter (e.g., trans-portation of weaned pigs and beef cattle) can be a major welfare concern and is associated withincreased risk of respiratory disease (60), which decreases the efficiency of growth and likelyincreases environmental impacts per unit of production (52). The degree to which transportationnegatively impacts an animal’swelfare is greatly influenced by the duration of the trip, the stockingdensity on the transport vehicle, and any stressful events that the animal has experienced prior to




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transport (e.g., cattle that are weaned via being transported from their originating cow-calfoperation rather than being backgrounded prior to transport) (60, 89). Although the precedingexamples are by no means an exhaustive list, they do demonstrate how animal handling, man-agement, and facility issues can influence both livestock welfare and environmental impacts perunit of production.

CONCLUSIONS

Research of the nexus between environmental quality and animal welfare is greatly lacking, andthe dissemination of knowledge gained from such research would be valuable to those directlyinvolved in livestock production, policymakers, and a general public that is increasingly interestedin the origins of their food. Research of the specific nexus areas outlined above, aswell as areas notexplicitlymentioned (i.e., genetics), could advance science’s ability to find sustainable solutions tomeeting growing global demand for animal products. Improving animal welfare has potential toimprove the production efficiency of the livestock industries and allow demand to be met withfewer animals. Disseminating the science of the nexus between these two issues, which havehitherto been largely approached separately, could enhance public policy discussions and bringmore nuanced, valuable discussions of what future sustainable and responsible livestock pro-duction should entail into the public forum.

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.

ACKNOWLEDGMENTS

The authors would like to thankMichelle Calvo-Lorenzo andMegan Rolf for helpful discussionsduring the writing of this manuscript.

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The Nexus of Environmental Quality and Livestock Welfare