Number 61 Issue Paper July 2018 Impact of Free-range Poultry Production Systems on Animal Health, Human Health, Productivity, Environment, Food Safety, and Animal Welfare Issues

Since animals were first domesticated, there have been major changes in both the animals and their care. The remarkable changes in poultry production efficiency have been well documented. (Shutterstock photo fromAlexius Sutandio.)

there is a distinct lack of usable defini- what is known about poultry egg and Abstract tions and knowledge, as well as a great meat production with specific atten- As farmers in the United States try to deal of confounding research related to tion to available research on free-range develop new poultry operations, there this field. The popularity and beliefs production systems. Stressors related to are two main possibilities. The first is to associated with what some consider a alternatively housed and managed birds, work within the existing vertically inte- return to old systems are very strong as well as the known advantages and grated systems. The second is to develop and have not dissipated. The consumer disadvantages for farmers, are reviewed. independent, smaller operations. Those has worked to fuel this movement to- Food quality and food safety in regard to that choose the second option look ward free-range, organic, or even simply poultry meat and eggs are often under- toward alternative production systems, what some consider natural poultry stood by farmers and consumers as one such as free-range poultry production. production. and the same. Clarification of food qual- As such, these individuals often find that This publication serves to review ity and food safety with regard to poultry CAST Issue Paper 61 Task Force Members

Authors Brigid McCrea, Alabama Cooperative Research Unit, Mississippi State, Extension System, Auburn University, Mississippi Jacqueline P. Jacob, Cochair, Depart- Alabama Hongwei Xin, College of Agriculture ment of Animal and Food Sciences, Daniel P. Shaw, Veterinary Diagnos- and Life Sciences, Iowa State Univer- University of Kentucky, Lexington tic Laboratory, University of Missouri, sity, Ames Anthony J. Pescatore, Cochair, Columbia Department of Animal and Food CAST Liaison Sciences, University of Kentucky, Reviewers Lexington Michael Hulet, Department of Animal Annie Donoghue, USDA–ARS, Univer- Science, Pennsylvania State Univer- Kenneth E. Anderson, Prestage sity of Arkansas, Fayetteville sity, University Park Department of Poultry Science, North Carolina State University, Raleigh Joseph Purswell, USDA–ARS Poultry

production systems will be discussed. cy was improved to 1.63 (Thiruvenkaden, may be provided either continuously The role of farming systems in disease Prabakaran and Panneerselvam 2011). or during specified daylight hours. The control is included in this discussion. Despite the ever-increasing separation outdoor area does not require a specified Attention to the environmental system, between farming and the general public, amount of space per bird nor specified soil contamination, and manure burdens today’s consumers are increasingly inter- environmental enrichments (e.g., grass, placed on the land by free-range poultry ested in where their food comes from and shelters, and dust baths), although the is also considered. This consolidation of how the food is produced. With regard birds are able to move about freely and information is aimed at helping further to animal food products, animal welfare, perform natural behaviors. “Free range” the discussion of free-range poultry as food quality, and sustainability have be- is a similar term in that it refers to a it pertains to larger farming systems and come key issues because consumers are system in which poultry have outdoor the future of this growing field of niche increasingly concerned with the depic- access, but in the case of free-range market poultry production. tions of commercial poultry production production, a shelter or a secured outdoor issued by agenda-driven groups online. space (i.e., run) may or may not be As a result of consumers’ changing provided. As with outdoor access, the Introduction perception of animal production systems, outdoor area does not have a specified The domestication of animals for there has been an increased interest in amount of space per bird nor speci- food production has played an important free-range1 poultry production. Although fied environmental enrichments. Birds role in the development of agriculture presently a small portion of the poultry are permitted to move about freely and as a whole (Mourão et al. 2006). Since industry in the United States, there is exhibit natural behaviors. There are no animals were first domesticated, there growing pressure by some consumers stipulations with regard to maximum have been major changes in both the to transition from conventionally raised flock size or type of bird raised. animals and their care. The remarkable poultry to free-range poultry production The terms “pastured” or “pasture changes in poultry production efficiency with improved animal welfare, improved raised” are also sometimes used. There have been well documented (Havenstein, product quality, and decreased environ- are distinct differences between free- Ferket, and Qureshi 2003). In the last mental impact cited as justification. range and pasture-related terms. Whereas few decades, the number of eggs a hen Any discussion on the impact of free- poultry flocks are kept outdoors in both can lay each year has doubled and the range poultry must begin with a definition cases, pasture must be provided in the amount of feed required to produce these of what “free-range production” actually latter. Pasture is defined as a tract of land eggs has been cut in half (Anderson et means. Free range and outdoor access covered with grasses, legumes, brassicas, al. 2013), resulting in decreased cost to are two terms that are often confused. or other forages suitable for grazing by consumers. Similar improvements have In the United States, there are no legal livestock. In the case of pasture poultry, occurred in poultry meat production. In definitions for either term. With regard the pasture is maintained specifically for 1923, chickens were raised to 16 weeks to poultry production, the term “outdoor ingestion by poultry, for the rotation of of age and only weighed 1 kilogram (kg) access” typically refers to production poultry after another livestock species, or (2.2 pounds [lb]). The feed efficiency of systems that allow flocks to leave a sta- for use in a mixed crop-livestock program weight of feed to weight of body weight tionary housing structure. Outdoor access with harvest of a forage crop. The flock gain was 4.7. By 2001, chickens were may be maintained in housing structures raised to 6 weeks of age and had a live 1 Italicized terms (except genus/species names and that are either mobile or stationary. Bot- weight of 2.6 kg (5.73 lb). Feed efficien- published material titles) are defined in the Glossary. tomless, moveable pens have become

2 COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY popular in the United States. The birds or lots used for outdoor access, must be at least 4 m per 100 m2 (12 ft per 100 ft2) are kept in the pens, which are moved on certified organic. Organic poultry produc- surface of the house. The feed used in a regular basis, giving the birds access ers may provide temporary confinement the fattening stage must contain at least to fresh pasture. If allowed to run free, or shelter in specific instances. There 70% cereal grains. For “traditional free- natural shade or man-made shelters may are no current space requirements in the range” production systems, the stocking be incorporated into the pasture system American organic standards for poultry. densities are slightly lower but the total to protect the birds from extreme weather In January 2017 new space requirements usable area of the poultry houses at any conditions. were proposed, but they were officially single production site may not exceed In the United States, “free range” is withdrawn in May 2018. The rule would 1,600 m2 (~17,250 ft2). There are limita- often mistakenly interchangeably used have given specific space requirements tions on flock size, and the birds must with “natural,” “free roaming,” “cage for both meat- and egg-producing chick- be of a strain recognized as being slow free,” and at times “organic.” “Cage free” ens based on age and housing system. growing. To be considered slow growing, or “free roaming” are terms typically The European Union (EU) has more they must have a body weight gain of used in reference to egg production and specific definitions for the term free- less than 50 grams (1.76 ounces) per day. are simply defined as a housing system range poultry (CEC 1991) than does the The amount of open-air access is also in which poultry are not maintained in United States. For table egg production, increased. For “free-range total freedom” cages. Outdoor access is not a require- there are four general categories: organic, production systems, the criteria set for ment, and environmental enrichments free range, barn, and cage (CEC 2002). traditional free range are the same except may or may not be provided. Birds are The regulations include specific condi- that the birds must have continuous day- permitted to move about freely within the tions that must be met in order for a flock time access to open-air runs of unlimited confines of a poultry house, however, and to be considered free range. Poultry must area. exhibit natural behaviors. The U.S. De- have continuous daytime access to open- In both Europe and the United States, partment of Agriculture (USDA) defines air runs, except in the case of tempo- the number of farms with free-range “natural” as a product with no artificial rary restrictions imposed by veterinary or organic poultry production is small. ingredients or added colors and mini- authorities, as in the instance of an avian France is an exception in that a large mally processed. “Minimal processing” influenza (AI) outbreak. The open-air number of farms are involved in alterna- means that the product was processed in runs must be mainly covered with vegeta- tive chicken meat production. This would a manner that does not fundamentally tion and not used for other purposes ex- include the Label Rouge chicken meat alter the product. The label must include cept for orchards, woodland, or livestock production system. Label Rouge, which a statement explaining the meaning of grazing. The EU regulations provide is French for “red label,” is a sign of the term natural (such as “no artificial specific housing and outdoor area density quality assurance in France as defined by ingredients”; “minimally processed”). regulations. There must be a minimum Law No. 2006-11. Label Rouge certifies According to the USDA definition, “natu- of 4 square meters (m2) (~45 square feet that a product has a specific set of char- ral” poultry may be kept in free-range, [ft2]) of outdoor access per hen. The open acteristics. In the case of chicken meat, a organic, pasture, cage-free, or caged sys- areas cannot extend beyond a radius of certain breed is required and grown to at tems. The term “natural” is different from 150 m (~500 ft) from the nearest pop- least 81 days of age. The chickens must “naturally raised.” “Naturally raised” hole of the building, although an exten- be allowed access to free range, and the refers to live animal production prac- sion of up to 350 m (~1,150 ft) is allowed carcasses are air chilled. No statistics tices and previously fell under a USDA provided that a sufficient number of are available on the number of alterna- Agricultural Marketing Services (AMS) shelters and drinking troughs are evenly tive meat chickens (i.e., organic and/ voluntary marketing claim standard for distributed throughout the whole open-air or free range) in Europe and the United which USDA provided third party verifi- run, with at least four shelters per hectare States. Estimated market share of alterna- cation. In 2016 AMS withdrew “naturally (~1.6/acre). tive chicken meat production in Europe raised,” as well as “grass fed” labeling For poultry meat production, the EU is only 5–10% (van Horne and Bondt standards, noting that it does not have the Council Regulations state that there are 2013). It is probably much lower in the ability to define the standards for these three forms of free-range poultry includ- United States, which has a larger conven- terms. ing “free range,” “traditional free range,” tional chicken meat production system. In order to be sold as certified organic, and “free range total freedom” (CEC There is no official reporting system for the National Organic Program Final Rule 2008). In a “free-range” system, the free-range poultry production in the Unit- Section §205.236 requires that poultry or stocking rate in the house and the age of ed States. According to the USDA–AMS edible poultry products be from poultry slaughter are similar to those for barn- June 4, 2018, cage-free shell egg report that have been under continuous organic reared poultry. The birds must have had (USDA–AMS 2018), there were almost management beginning no later than the continuous outdoor access to open-air 54 million cage-free egg layers in the second day of life. All agricultural com- runs for at least half of their lifetime. United States during the month of May ponents of the feed ration must be 100% In addition, the open-air runs must be 2018. This represents 14% of all the table organic. All poultry must have access to mainly covered by vegetation. The total egg layers in the country (USDA–NASS the outdoors. Fields, including pastures amount of pop-hole length should equal 2018). This would include both confined

COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY 3 and free-range production systems. Of a free-range laying hen farm) resulted in is physical health. It is uniformly agreed the cage-free hens, almost 16 million the culling of 30 million chickens and 87 that injury, disease, and deformities result were certified organic, which would have human cases. Productivity of free-range in poor animal health and welfare. A access to the outdoors. This would repre- poultry will also be discussed. For ex- whole host of factors can affect disease sent only 0.3% of the total hen inventory ample, the production cycle is longer for incidence, and the production system for May. Organic, however, is only a free-range poultry meat production com- used will impact many of these. Accord- portion of the free-range hen production pared to conventional indoor systems. As ing to the Danish Poultry Council, 17.1% in the United States. There currently is no a result, feed consumption and manure of the hens died in the production period database specific for only free-range table production per bird can be expected to be in organic systems, which includes out- egg producers in the United States. higher in the free-range systems. This, in door access, while 5.4% and 12.1% died Consumers, egg producers, state leg- turn, can have a major impact on the en- in cage and deep litter systems, respec- islatures, and consumer advocate groups, vironmental burden related to free-range tively (Eigaard et al. 2003). Research has along with the animal rights organiza- production. shown, however, that laying hens that tions, are taking on and claiming a vested used outdoor areas had lower plumage interest in how eggs are produced. Egg damage and a lower incidence of footpad producers have always worked to provide Animal Welfare dermatitis (Rodriguez-Aurrekoetxea and products to meet consumer demands. The assessment of animal welfare Estevez 2016). In comparison, hens that In Europe, however, these production for poultry flocks reared under differ- walked long distances indoors showed a system changes have been driven by ent production systems is complicated higher incidence of footpad dermatitis. environmental and consumer advocate and, at times, controversial. There are Yilmaz Dikmen and colleagues (2016) groups, which culminated in the 2012 considerable differences regarding what also reported reduced foot lesions in free- ban on the use of conventional cages in constitutes acceptable animal welfare, range systems compared to conventional egg production (European Commission how welfare status should be measured, or enriched cages. 1999). In the United States, California and the interpretation of research results. Modern strains of egg layers can fre- voters passed Proposition 2 (2008) which The comparison between different hous- quently suffer from structural bone loss defined the housing conditions for laying ing systems is complicated because of as a result of the large calcium demand hens starting in 2015 (California Health the fact that management, nutrition, and with the high levels of egg production. and Safety Code 2009). In the 2016 elec- breed vary among the different housing Regmi and colleagues (2016) examined tion, Massachusetts voters passed similar systems used. In addition, behavioral the bones of hens at the end of their lay- legislation for changes in housing condi- changes as birds adapt to a management ing cycle, comparing different strains and tions by 2025. These laws and legislative system can mask any welfare concerns. housing systems. They concluded that actions have been promulgated and As a result, while the presence of a range and cage-free housing may have passed with little understanding of the specific behavior may effectively identify benefits on bone integrity compared to implications on animal well-being and poor welfare, its absence is not evidence conventional cages, but the improvement the safety of the products they produce of good welfare. is not enough to prevent fractures or keel (Anderson 2009). Comparisons of poultry production bone deformities. While many perceive improved animal systems also must examine the effects If animal welfare encompasses more welfare with free-range production sys- of flock size in addition to the housing than simply animal health, as it does for tems, the use of outdoor access has some system used. Chickens naturally live in most consumers, the problem becomes inherent risks related to food safety, ani- small groups and establish a pecking or- how to assess the “psychological health” mal health, biosecurity, productivity, and der within their group. This is presumed of nonhuman animals. This issue has environmental impact. This report will to involve serial aggressive interactions. been debated for more than 20 years, and detail the animal welfare, food safety, The individual birds remember the result the only consensus is that no single mea- animal health, biosecurity, productivity, of these interactions and the hierarchy sure of animal welfare is adequate. Al- and environmental impact of free-range becomes established. In larger flocks, this though it is accepted that several different poultry. There is an ongoing debate as system breaks down because the hens are measurements are necessary, there is no to whether or not poultry products from only able to identify a limited number of consensus regarding which combination free-range production systems are more individuals. In such cases, the hens adapt of measures should be used. Individual likely to be contaminated with major by becoming less aggressive and chang- measures that include physiological, bio- foodborne bacteria such as Salmonella ing their social system to one in which chemical, and behavioral factors can be and/or Campylobacter than those from dominance is determined through direct used, but they may result in contradictory conventional, indoor production systems. assessment of “status signaling,” which conclusions. Avian influenza is a global threat to pub- can include comb size and postural clues, The effect of stress on physiologi- lic health and can cause large economic rather than the remembered individual cal measures, including heart rate, body losses to commercial poultry industries. assessment used in a small group pecking temperature, respiratory rate, increases The 2003 outbreak in the Netherlands order (D’Eath and Keeling 2003). in adrenal secretion and corticosteroids, (potentially introduced by wild fowl to The basic measure of animal welfare and depression of immune function, has

4 COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY been widely studied in poultry (Puvadol- ing a feed restriction stress. This would to behavioral and physiological changes pirod and Thaxton 2000). Stressors in indicate that the response of a flock to a that help the animal to cope with the chickens result in increased circulating stress may be related to genetics (Zim- stimulus. Traditionally, this has been as- concentrations of corticosterone (Scanes merman and Koene 1998). For one strain sessed by the duration of tonic immobil- 2016). Corticosterone influences the of laying hens there was an increase in ity reaction and H/L ratio. Long durations heterophil:lymphocyte (H/L) ratios, and the level of alarm calls as an indicator of of tonic immobility are believed to be such shifts can be used as markers of frustration due to the lack of a reward in a indicative of high levels of fearfulness. stress. Yilmaz Dikmen and colleagues situation that previously was consistently Increases in avian basophils and hetero- (2016) reported that H/L ratios were rewarding. Alternatively, for a different phils have been associated with stress. highest in birds in conventional cages strain more gakel-calls and increased Interestingly, results from studies suggest compared to enriched cages and free locomotor activity were some common that frequent movement between indoor range. The use of such parameters, how- indicators of frustration. and outdoor areas was associated with ever, has had conflicting results, with the Some researchers have divided animal indicators of fearfulness (Mahboub, levels obtained varying as a function of welfare factors into two groups—aver- Müller, and von Boreel 2004). Whereas how the birds were handled. In addition, sion and deprivation. Aversion would increased time outside of the house was obtaining these measurements itself can refer to stress resulting from conditions associated with decreased feather pecking be stressful and at the same time not that an animal is motivated to avoid. De- (Bestman and Wagenaar 2003; Mahboub, practical at the production level. privation refers to a condition in which an Müller, and von Boreel 2004), it was Since physiological responses are animal is unable to complete a behavior it also associated with an increase in other difficult to precisely measure under field is motivated to do. This may result from stress indicators. In contrast, Hartcher conditions, animal welfare research has a physical restraint or the lack of suitable and colleagues (2016) studied tonic im- focused primarily on behavioral respons- stimuli. A fundamental question raised mobility to assess the welfare of laying es. Yet, there are inherent difficulties with here is how are an animal’s “needs” de- hens on range. They used radio frequency interpreting such data. Interpretation of termined? Two test types have been used identification (RFID) to identify the top behavioral data when evaluating different in the past. In preference tests, animals 15 and bottom 15 hens for range use as housing conditions is complicated. Ani- are offered choices between alternatives determined by the time spent on range mals can become acclimatized or adapted to see which one they prefer. In operant over a 13-day period. Hens that spent the to their environment. There may be ge- conditioning, the animal is trained to most time outside displayed a decrease in netic differences between the strains used make some response to gain access to or fearfulness. Similarly, hens that spent less in the housing conditions. Behavior may to avoid certain consequences. This can time outside had higher tonic immobil- also be dependent on external stimuli, be pecking a key or pressing a lever. Such ity durations, indicating higher levels of such as antipredator behavior, that may methods have been used to determine fearfulness. not be present in both systems. animal responses to different flooring A computer model was developed to In order to determine what constitutes types, different cage sizes, different tem- assess the welfare of laying hens housed normal behavior of chickens, time bud- peratures and light levels, and many other in different production systems (De Mol gets were developed for semi-wild jungle factors (Dawkins 1988). et al. 2006). The European model used 25 fowl kept in a zoo (Dawkins 1989). Dur- Laboratory tests measuring the choice attributes, each with two or more levels, ing the active part of the day, jungle fowl and preference of an animal for differ- defining the characteristics of a produc- spent 60% of their time ground pecking ent “wants,” such as floor types, perches, tion system. Each attribute was given a and 34% ground scratching. Although nest boxes, dust bathing, etc., may or may weighted factor based on the available the chickens were fed regularly, they not be applicable at the farm level. It is scientific knowledge of the effects of the still spent most of their time on foraging important to watch the animals in situ. attribute levels on the welfare aspects. behaviors. Housing systems in which For example, in some free-range broiler Based on the model, the factors of feed- chickens are not able to forage would, systems many chickens do not leave the ing level, space per hen, perches, water therefore, prevent them from perform- house and, if they do, do not venture availability, and nests were the most ing what can be perceived as a natural far from the house. One could conclude important attributes. The attribute of free behavior. that chickens do not want to go outside. range was of minor importance. In regard Vocalizations have been suggested as It could be, however, that the outdoor to the welfare assessments, however, a measure of animal welfare, with the area is not providing the ranging habitat the computer model concluded that cage major challenge being how to interpret that suits their natural behavioral needs. systems scored the lowest, barn and avi- the meaning of a noise emitted during a Research has shown that chickens are ary systems intermediate, and European specific circumstance. Approximately 30 attracted to trees and are more likely to organic systems scored the highest. distinct vocalizations from both young venture outside a house if there are trees A different protocol was developed for and adult chickens have been detected or shrubs in the outdoor run (Dawkins et assessing the welfare of laying hens in (Wennrich 1981). A comparison of two al. 2003; Fanatico et al. 2016). free-range production systems, examin- lines of laying hens noted distinct differ- Fear is defined as an emotional state ing both physical and emotional ele- ences in the vocalization of the hens dur- that arises from negative stimulus leading ments (Whay et al. 2007). This protocol

COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY 5 was then used to investigate the effects bushes, or artificial roofs can decrease included restricting group size, keeping of different approaches to housing and aerial predation (Berg 2001). Weeks, cockerels with the hens, rotating runs, management on the welfare of the hens. Lambton and Williams (2016) also re- and providing well-dispersed covers. Measures of the hens’ attitude included ported high variability in mortality asso- Additional recommendations included arousal, noise, flight distance, and ciated with free-range egg laying flocks. appropriate pullet rearing and breed- response to a novel object. Measures Cumulative mortality at 60–80 weeks of ing strategies. The limited amount of of activity included feather pecking, age averaged 10% but ranged from 0 to research involved in resolving problems aggression, and use of range. Physical 69.3%. More research and training are encountered in free-range systems makes welfare was measured by mortality, body needed to improve production in com- it difficult to make a final judgment on condition, and egg quality. In the study, mercial free-range systems. the welfare aspects of outdoor access there were five visits to each of 25 egg When comparing conventional cages, compared to completely indoor facilities production units. Estimated losses, which furnished cages, noncage (floor) systems, (Knierim 2006). included deaths and culls, ranged from and outdoor systems, the main conclusion Although there have been several 1.8% to 21.5%, with a median value of was that no single housing system can be studies comparing the welfare status of 6.95%. The distribution of the mortality identified as being ideal for hen welfare laying hens in different management numbers was skewed by a small number (Lay et al. 2011; Widowski et al. 2016). systems, there are only a few looking at of farms with heavy losses. As a result, Each system has its own merits and chal- meat poultry, with very few focusing on the median value provides a more repre- lenges. Cage systems, which limit hen turkeys. Dawkins and colleagues (2003) sentative indicator. No facility features movement, can result in problems with studied the factors that affect range use were identified as having a significant osteoporosis. On the other hand, floor of commercial free-range broilers in effect on mortality, but the absence of systems can result in more bone frac- England. They reported that few broilers perches altered hens’ attitude, activity, tures (Regmi et al. 2016). Although more range in winter, but, even in summer, the and performance, suggesting that the space allows the hens to perform a wider maximum number of chickens observed welfare of hens was decreased when they repertoire of behaviors, it also includes an outside during daylight hours at any one were housed on plastic floors without increase in detrimental behaviors such as time was less than 15% of the flock. perches. feather pecking, cannibalism, and piling. Taylor and colleagues (2017a) tracked More recent research has indicated a Production systems in which hens are ex- the ranging behavior of 300 individual possible link between stress and eggshell posed to litter and/or soil provide greater broilers from each of four flocks in two irregularities (Alm et al. 2016). Nest de- risk for disease and parasites. Thus, seasons on a commercial farm in Austra- privation in laying hens has been shown although the perception may be that lia. They found that there was consider- to increase fecal levels of corticosterone animal welfare is increased in free-range able variation between flocks. Chickens metabolite as well as corticosterone production systems, this may not be the that never accessed the range varied concentrations in yolk. These levels case with all operations. More research from 13% to 67% of the tagged individu- were found to be positively correlated is required to determine what constitutes als. Those using the range infrequently with increased incidences of eggshell good animal welfare, how welfare should ranged from 15% to 44% and accounted irregularities. This would suggest that the be measured, and which production sys- for less than 15% of all the range visits. incidence of eggshell irregularities may tem best meets these welfare needs. High-ranging chickens varied from only be a noninvasive welfare indicator. When compared with barn systems 3% to 9% and accounted for 33% to 50% In a Danish study, the outdoor area use for laying hens, providing an outdoor of all range visits. As expected in this of 18 egg production flocks ranging in run can lead to higher space allowances, Australian study, daily frequency and size from 1,200 to 5,000 hens was evalu- an increase in the number and types of duration of range use was greater for ated. Hegelund, Sørensen, and Herman- behavioral and physiological stimula- summer flocks (Taylor et al. 2017b). sen (2006) found that the outdoor area tions, and the freedom to move between Behavioral observations are already use ranged from 7% to 38% of the flock, different environments with changes in used in the clinical assessment of animal with an overall mean of 18%. The major- climatic conditions and bird preferences health for meat poultry, as in the case ity of the hens that did go outside stayed (Knierim 2006). Based on these criteria, of gait scores to assess the leg health of close to the hen house. Mortality ranged one can assume that there is an increase broiler chickens. Such assessments do not from 9% to 62%, with high mortality in animal welfare. Knierim (2006) noted, identify the underlying problem, but gait partly due to outbreaks of Pasteurella however, that outdoor runs are also as- scores give a convenient on-farm assess- multocida. In some flocks, predation and sociated with increased risk factors that ment of leg health. Škrbić and colleagues piling were important causes of mortality. have the potential to adversely affect hen (2014) compared the performance of As would be expected, keeping poultry welfare. This included increased contact Redbro broilers raised to 81 days of age outdoors exposes them to predators. In with infectious agents, greater difficulties in either a confinement or a free-range many cases, ground predators can be maintaining hygienic standards, increased system and reported that those broilers controlled with an electric fence, but pre- possibilities of unbalanced diets, and in- reared in the free-range system had a dation by birds of prey is more difficult creased threat of predation. Management decrease in the number of chickens with to control. Providing natural shelters, like factors recommended to limit these risks footpad dermatitis as well as a decrease

6 COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY in the frequency of associated lesions. In portable houses that are able to deal with Meat contrast, Castellini and colleagues (2012) weather fluctuations, especially in areas As with the egg, the popular literature reported higher incidences of severe foot with high summer temperatures. describing the effect of pasture on per- and breast lesions in organic systems formance, carcass composition, and meat than in conventional indoor produc- quality has been contradictory. The qual- tion. Both systems used the same strain Food Quality ity of chicken breast meat produced in the of fast-growing chickens, leading the The popular literature addressing the United Kingdom (UK) from conventional authors to conclude that the fast-growing effect of free-range production systems and free-range systems was compared by chicken strains are not well suited to the on food quality is contradictory and can Brown and colleagues (2008). The breast organic system and their welfare is worse be confusing to consumers, with different fillets from the chickens raised in the in organic systems than in conventional sides of the debate selectively referencing conventional system were rated as being indoor. Foot and breast lesions were not studies supporting their side. Many dif- more tender and juicy, but no signifi- noted in the slower-growing chickens in ferent factors need to be considered when cant differences in chicken flavor were the organic-plus system. comparing food quality between produc- detected. Givens and colleagues (2011) Knierem and colleagues (2007) used tion systems. found no evidence that meat from free- the latency-to-lie test to evaluate leg range chickens had a fatty acid profile problems in broilers raised in organic or Eggs that would be classified as healthier than conventional systems. The shorter the Many consumers perceive eggs that of intensively reared birds. Free- time to lay down, the more likely they are from hens kept in free-range production range breast and leg meat contained sig- to have leg problems. The latency-to-lie systems as being nutritionally superior nificantly less polyunsaturated fatty acids test showed less leg problems for those to those produced from hens in cages. (both omega-6 and omega-3) and higher raised in organic conditions. The changes What the hens eat is more important omega-6/omega-3 ratios. Dal Bosco and are most likely due to differences in the than whether or not they go outside. The colleagues (2016), however, showed that genetics of the broilers reared in the two type of feed and pasture composition grazing improved the nutritional value production systems. They found no dif- are important considerations in addition of meat by increasing the omega-3s and ference in tonic immobility (the longer to the management of the pasture itself decreasing the omega-6/omega-3 ratios. the time, the more fearful the birds), (Horsted, Hammershøj, and Allesen- Meat from the outdoor chickens also had breast condition, and foot pad condition Holm 2010). Anderson (2011) reported higher levels of antioxidants. This was between the two systems. Durali and that eggs from “range-reared” hens had mainly due to the higher levels of tocoph- colleagues (2014) used RFID to evaluate more total fat, including higher levels of erols and tocotrienols. Despite the higher the level of range of specific broilers in a unsaturated fats such as omega-3 fatty oxidant protection in the drumstick, the commercial free-range flock. They found acids. Karsten and colleagues (2010) thiobarbituric acid reactive substances that level of range use had no effect on reported that, compared with eggs from (TBARS) were higher. The authors latency-to-lie time. caged hens, eggs from “pastured” hens hypothesized this is because of the higher As with laying hens, providing meat contained twice as much vitamin E and kinetic activity of the chickens and the birds with outdoor access leads to in- long-chain omega-3 fatty acids, two-and- higher percentage of polyunsaturated creased space allowances, an increase in a-half times as much total omega-3 fatty fatty acids. They recommended strategies the variation of behavioral and physi- acids, and half the ratio of omega-6 to to decrease activity in the last days of ological stimulations, and the ability to omega-3 fatty acids. As with Anderson rearing. move between different environments. (2011), Karsten and colleagues (2010) re- Castellini, Mugnai, and Dal Bosco Research shows, however, that the use of ported no differences in vitamin A levels. (2002) reported that organic chickens had outdoor access is limited with meat birds; There was no effect of range production carcasses with higher breast and drum- therefore, evaluation of the impact of the system on cholesterol levels. Mugnai and stick percentages and lower levels of range use on the welfare of meat birds is colleagues (2014) also reported signifi- abdominal fat. The muscles had lower pH difficult. cant decreases in omega-6 and higher and water holding capacity. The organic The use of moveable, bottomless pens omega-3 fatty acids. Eggs from hens on a chicken meat also had higher cook- on pasture may provide outdoor access grass-clover pasture and fed a traditional ing loss, lightness values, shear values, while limiting some of the negative layer diet had less favorable scores in iron, polyunsaturated fatty acids of the aspects of free-range production, such as several sensory quality attributes com- omega-3 series, and higher TBARS. The predation and exposure to wild birds. Ad- pared to hens in an indoor system. Based sensory quality of the breast muscle from ditional research is needed in the animal on the omega-3 content, the research organic chickens was reported to be bet- welfare status of birds reared in this type would support the belief that eggs from ter. The reasons for the conflicting results of production system. In one study, using hens on pasture were nutritionally supe- are unclear but would most likely be re- fast-growing meat chickens kept in hoop- rior to eggs from hens in cages, although lated to the quality of the forage material houses in the summer (Moyle et al. 2014) taste may be adversely affected. This is in the outdoor areas. had to be terminated early because of related to their diet and not whether or Stadig and colleagues (2016) com- extreme heat. It is important to develop not the hens were outside. pared slow-growing broilers raised

COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY 7 indoors or with outdoor access to 70 days the omega-6 and omega-3 precursors’ lin- of Campylobacter jejuni (Sulonen et al. of age. The outdoor access was either on oleic acid and alpha-linolenic acid (ALA) 2007). grassland with artificial structures or on in breast meat. In spring, the levels of an area being used in short-term rota- eicosapentaenoic acid (EPA) in the breast Eggs tion coppice with willow trees providing meat were higher, suggesting a greater In European table egg production, shelter. Those chickens with the willow conversion of ALA into EPA in these three areas of concern have been defined trees used the range more and ranged fur- chickens. Ponte and colleagues (2008), by the Codex Alimentarius Commission ther than those with artificial structures. however, showed that broilers on pasture (2001). These include microbiologi- Although those chickens raised indoors consumed less than 5% of the daily in- cal (pathogens), chemical, and physical were larger at harvest, there were no take of dry matter (DM) from pasture. contamination. The management systems statistically significant differences in feed Outdoor access was shown to have and facilities used to house laying hens consumption or feed efficiency. Breast no effect on growth performance of a can exert powerful influences on the fillets of chickens with free-range access slow-growing breed, but the appearance sources, transmission, and persistence of were darker and yellower than those and meat quality of the chickens was pathogens such as Salmonella enteritidis raised indoors. There were no differences improved. In addition, giving outdoor ac- within flocks (Carrique-Mas et al. 2009). in fat, protein, moisture, or ash content, cess beginning at 36 days of age appeared Diverse and sometimes contradictory but chickens on range had higher levels to be more beneficial than providing results have emerged from prior research of unsaturated fatty acids. A taste panel outdoor access beginning at 71 days of comparing the effects of the various found no differences in taste, color, ap- age (Chen et al. 2013). housing systems on the prevalence of pearance, or aroma of the meat. The taste Although research directly comparing Salmonella infection and environmental panel found the breast meat from those the attributes of pasture-fed to conven- contamination. Poultry with access to chickens with the willow trees, and thus tional chicken meat has indicated some outdoor areas are vulnerable to patho- the most range use, to be more tender and nutritionally significant differences, the gen introduction from external sources, less fibrous compared to the chickens on differences are very much diet specific which can be a particularly significant grassland with artificial shelters and those and may not be carried through to the Salmonella risk factor (Mollenhorst et al. chickens raised indoors. In addition, the market place. In a survey of organic, 2005). In contrast, Van Hoorebeke, Van meat from the chickens with the willow free-range, and conventionally produced Immerseel, De Vylder, and colleagues trees was juicer than that of the indoor chicken purchased in the market place, (2010) reported that the housing system chickens. Overall, free-range access there were no differences in the protein had no significant effect on the inci- negatively affected slaughter weight, content, fatty acid composition, and dence of Salmonella in laying hens. It is but positively affected meat taste or sensory properties between free-range important to note, however, that all flocks composition. and conventionally produced chicken sampled had been vaccinated against A meta-analysis of the literature noted (Husak, Sebranek, and Bregendahl 2008). Salmonella with an attenuated vaccine. such inconsistencies among research Surprisingly, the thigh meat of chicken The use of vaccinations, therefore, could reports (Sales 2014) and concluded that marketed as organic was higher in protein eliminate the differences between the two the consumer preference for meat from than conventional and free-range chicken, systems as far as Salmonella contamina- free-range poultry is not justified by the as well as lower in saturated and higher tion is concerned. research. Instead, it would be preferred to in monounsaturated fatty acids. The Hens in free-range systems were re- identify factors that do positively affect diets and production environment of the ported to have a higher ratio of dirty eggs meat quality. Breed, slaughter age, and products purchased, however, could not (Yilmaz Dikmen et al. 2016). Cage-free feeding strategy all have major impacts be confirmed. Thus, it is possible that the housing systems were reported to be as- on the sensory profile of chicken meat chicken in this study marketed as free sociated with higher levels of Enterobac- (Horsted, Allesen-Holm, and Hermansen range may not have had access to pasture, teriaceae bacteria (Salmonella is among 2010). whereas that of the organic chicken did. this family of bacteria) on egg shells Pasture composition can have a major (Jones and Anderson 2013), more fre- effect on meat quality. Dehydrated pas- quent Salmonella isolation from environ- tures (which included Italian rye grass Food Safety mental samples, and a greater likelihood [Lolium multiform] and balansa clover Food safety is another factor in the of horizontal transmission of Salmonella [Trifolium michelianum] harvested in production system debate. For poul- infection within flocks (De Vylder et al. the flowering state) in the diet of broiler try meat production, Salmonella and 2011; Hannah et al. 2011; Watanabe et chickens significantly decreased ratios of Campylobacter are the main pathogens al. 2012). In other studies, cage-based saturated to polyunsaturated fatty acids of concern. The most significant public housing systems were associated with a (Mourão et al. 2008). In addition, legu- health risk is transmission of Salmonella higher probability of Salmonella infec- minous pasture intake has been shown to to humans via eggs. A Finnish study, tion in flocks, especially in the presence decrease the ratio of omega-6 to omega-3 however, showed that organic laying of large populations of rodents (Huneau- fatty acids in breast meat. Ponte and flocks that have access to the outdoors are Salaün et al. 2009; Snow et al. 2010; Van colleagues (2008) observed decreases of commonly colonized by diverse strains Hoorebeke, Van Immerseel, Schulz, et al.

8 COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY 2010). A third group of studies identi- and other pests; cleaning and sanitation; that poultry are omnivores, free-range fied no significant differences between and mixing of hen ages. Namata and hens will ingest these compounds and ac- cage-based and cage-free flocks in either colleagues (2008) identified additional cumulate them in both their body fat and Salmonella fecal shedding or environ- factors such as the rearing environment, eggs (Holt et al. 2011). An unsuspecting mental contamination (Jones, Anderson, ventilation, or vaccination programs. source of chemical contamination may and Guard 2012; Siemon, Bahnson, The chemical contaminants related to be in pressure-treated lumber for fencing and Gebreyes 2007). These conflicting food safety include dioxins, polychlori- and building construction, particularly observations appear to be due to the influ- nated biphenyls, pesticides, and heavy in older construction. The chemicals ence of rodents and insects that remain in metals (Holt et al. 2011). The dangers used in treating these materials to resist the facility after cleaning and disinfect- associated with these compounds are well insects and rot could find their way into ing. The high-incident rate reported in documented and represent a significant the paddocks and soils contributing to the some cage systems may be related to the food safety concern. They tend to accu- chemical contamination of the laying hen rodent population becoming infected and mulate through the food chain and are not or meat birds on those paddocks (Marc- reinfecting hens by fecal contamination readily cleared by the body but stored in zew et al. 1989). of feed. fat tissue. Dioxin compounds, which are As the number of urban egg produc- Other management factors could have very stable and persistent in the environ- tion flocks continues to grow across the impacts including vaccination, improper ment and in animal tissues, have been United States, a new food safety concern cleaning, or sanitation. The elevated lev- found associated with eggs from free- has arisen—lead. Spliethoff and col- els of contamination come into play when range flocks (Chang et al. 1989; Harnly et leagues (2014) measured lead concentra- eggs that are not laid in the nest boxes, al. 2000). A study in California conducted tion in eggs from New York City com- such as floor eggs or eggs laid on the near a former paper mill found hens on munity gardens, and lead was detected paddock, are collected, washed, and sold. soil produced eggs with polychlorinated between 10 and 167 parts per billion Mallet and colleagues (2006) showed that dibenzodioxin (PCDD) and polychlori- (ppb). In contrast, lead from store-bought eggs laid in the dust bath and other areas nated dibenzofuran (PCDF) levels 100 eggs were less than 7 to 13 ppb. Rural of the cage-free system had higher total times higher than eggs from conven- areas, however, are not immune to lead bacteria and enterococci than eggs laid tional cage hens. A study in Europe also contamination. Lead has been found in in the nest. The contamination rates for found higher PCDD and PCDF levels eggs from chicken raised in rural areas these floor eggs may be logarithmically in eggs from free-range hens (Schoeters of Belgium (Waegeneers, Hoenig, et al. higher than eggs laid in the nest, and the and Hoogenboom 2006). These authors 2009; Waegeneers, Steur, et al. 2009). times the eggs were exposed to the fecal observed similar contamination in eggs Lead contamination in eggs was less than contamination are not known. De Reu produced near urban areas as well as 2 to 477 ppb. Lead egg contamination and colleagues (2005) indicated that eggs from eggs in rural areas where PCDD was significantly associated with soil lead from hens housed in aviaries had higher levels would have been considered low. levels that were found to range from 12 total aerobic bacteria than either conven- Another aspect of PCDD levels in to 174 parts per million. In a lead-transfer tional or enriched cage systems. There eggs is related to the use and access a model, the authors concluded that soil was no appreciable difference in aerobic flock has to the outdoor range. Kijlstra, lead levels accounted for up to 92% of bacteria between the conventional and the Traag, and Hoogenboom (2007) found the lead in the eggs (Waegeneers, Steur, enriched cage systems. In later studies that the smaller the flock size, the higher et al. 2009). (Singh, Cheng, and Silversides 2009), the PCDD levels in the eggs they pro- Another point of concern that has eggs from conventional caged hens were duced, and the larger flocks had lower received almost no attention is the use of found to have lower levels of E. coli. and levels. This appears to be related to compounds treating free-range poultry other coliforms when compared to nest the fact that small flocks are out on the for external and internal parasites. These and floor eggs from hens in free-range paddocks during the daylight and larger antiparasitic compounds could be either systems. De Reu and colleagues (2006), flocks have a greater propensity to remain absorbed or ingested, pass through the however, reported that eggs from alterna- indoors, thereby limiting the PCDD hen’s system, and end up in the produc- tive systems, including free range, had intake. tion environment. Eggs from the com- lower gram-negative bacteria. Pesticides and heavy metals can mercial operations using these appear Based on these studies, the main fac- also contaminate the environment and to have higher concentrations due to tors that put poultry flocks at risk for mi- contaminate eggs from free-range flocks the increased use of these chemicals to crobiological contamination include the at levels that reflect the soil’s contamina- control the insect populations (Hamscher season of the year (Jones, Anderson, and tion. Vieira, Torres, and Malm (2001) et al. 2003). Intestinal worms are be- Musgrove 2011); the size and strain of reported that dichlorodiphenyltrichloro- coming a greater issue as poultry move the flock (Muir and Aggrey 2003), with ethane (DDT) levels in eggs produced on from cages to litter floors to outdoor larger flocks having a higher incidence free-range farms were 1,000 times greater paddocks. To control these organisms, a rate; housing system, such as outdoor than the levels in commercially produced variety of compounds is used (Ssenyonga access or cage free and management eggs. Given the persistence of pesticides 1982; Young and Dawe 2008), most of (De Rue et al. 2009); control of rodents and heavy metals in the environment, and which require withdrawal periods but,

COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY 9 nonetheless, would be recycled in the birds were not the source of the C. jejuni successful poultry production. Studies cage-free or free-range environment. contamination. This was confirmed by have shown increased mortality in free- In 2017, eggs tainted with Fipronil Colles, Dingle, and colleagues (2008), range production systems compared to were discovered in eggs produced in who examined wild geese and found conventional cages (Eigaard et al. 2003; Belgium and the Netherlands and found that they carry Campylobacter, but there Sossidou et al. 2011; Wongrak et al. in several European countries. Fipronil is was limited mixing of Campylobacter 2014). Diseases are caused by bacterial, commonly used by veterinarians to treat populations among geese, starlings, and viral, and parasitic agents. Diseases, at fleas and ticks on cats and dogs. It is not free-range chicken populations. They the worst, kill, or, at the least, rob a flock allowed for any animal entering the food concluded that geese are not likely to be of optimal productivity. Many infections chain. Around 180 Dutch farms were sources of human cases of C. jejuni. that do not kill the host rob it of vitality temporarily shut down, and a criminal Interestingly, Young and colleagues by impaired appetite, decreasing efficien- investigation was launched. Two men (2009) indicated that although organic cy of nutrient absorption, or disrupting were arrested for the illegal use of Fipro- broiler chickens had higher levels of the function of other essential systems nil at poultry farms to treat red mites, Campylobacter at slaughter, there were such as the respiratory tract or excretory which can be a problem in cage-free egg no differences between organic and con- and immune systems. production systems. ventional in the prevalence of Campylo- It is unclear how the housing situation bacter at the retail level. Bacteria isolated affects the immune system of poultry. Meat from conventional poultry had a higher Antibody production has been shown Many consumers believe that free- incidence of resistance to antimicrobials, to be significantly higher in caged hens range organic poultry meat is safer than but some of the resistant strains were also (Arbona, Anderson, and Hoffman 2011). that of conventional poultry. This is not identified in a number of organic produc- Caged hens also had the greatest ratio of necessarily true, because Näther and col- tion systems as well. heterophil to lymphocytes, which is an leagues (2009) reported that the preva- Regardless of the research conclu- indication of stress. Comparing immune lence of Campylobacter was significantly sions concerning relative food safety of response of laying hens kept in battery higher in flocks from free-range and or- chickens from different systems, consum- cages, on the floor with litter and perches, ganic farms in Germany when compared ers should not assume that all free-range or in a free-range housing environment, to conventionally raised broilers. This or organic chicken are free of Salmonella research has shown that the antibody re- was confirmed by several researchers in and Campylobacter. Bailey and Cosby sponse is higher in battery cages and on- other areas of Europe (Bokkers and de (2005) surveyed the microbiological the-floor housing (van Loon et al. 2004). Boer 2009; Esteban et al. 2008) and the status of chicken from different lots from In addition, the titers remained higher in United States (Van Loo, Alali, and Ricke four different free-range chicken produc- battery cages. The T-cell response, how- 2012). Outdoor production systems result ers and reported that 64% of the lots and ever, was higher in free-ranging hens. In in longer rearing times because of either 31% of the carcasses were positive for contrast, Rehman and colleagues (2017) the breed or the environment, thereby Salmonella. For the “all-natural” chick- reported that vaccinated hens in semi- increasing the risk of contamination. ens sampled, 37% of the lots and 25% of intensive and free-range egg production With outdoor access, broilers and turkeys the chickens tested positive. The sampled systems had higher antibody titer against will be more prone to exposure to stress lots from organic chicken all tested Newcastle disease (ND) and infectious from environmental conditions, wild positive for Salmonella, with 60% of the bronchitis viruses. birds, and animals, as well as insects and individual carcasses testing positive. Alali There are several reports indicating rodents (Lubin, Samish, and Mishoutch- and colleagues (2010), however, showed that the incidence of helminth infections enko 2003; Lund 2006). Van Loo, Alali, that within a North Carolina poultry com- (Ascaridia galli, Heterakis gallinarum, and Ricke (2012) cautioned that compar- pany, the prevalence of fecal Salmonella and Capillaria spp.) is higher when ing the results between studies is difficult contamination was lower in certified poultry have outdoor access as compared because of differences in geographic organic chickens and the prevalence of to the incidence of such infections when locations, seasons, and detection and antimicrobial-resistant Salmonella was raised in conventional housing (Permin isolation methods. higher in conventionally raised chickens et al. 1999). Kaufmann and colleagues The source of Campylobacter jejuni than in those certified organic. A major (2011) evaluated the intestinal parasite contamination in poultry flocks has yet source of contamination in the conven- load of hens raised on organic free- to be definitively determined. A yearlong tional chickens may have been the feed. range farms where outdoor access is study by Colles, Jones, and colleagues Contamination of feed samples from or- required. They reported that 99.6% of (2008) examined Campylobacter jejuni ganic and conventional farms were 5.0% hens examined had nematode or cestode shedding in flocks of free-range chickens and 38.8%, respectively. infestation. The probable reason for this as well as wild birds in the area. Although is, with outside access, poultry will ingest both populations were shown to shed insects and other invertebrates, such as oultry ealth C. jejuni, there was a high degree of P H earthworms, that serve as intermediate genetic difference between the chickens Flock Health hosts for several digestive tract parasites. and wild birds, suggesting that the wild Optimal health management is key to In low numbers, roundworms (Ascaridia

10 COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY sp.) appear to have little deleterious effect has been shown to decrease nematodes tion on the causes of mortality carried on the vitality of the host, but they can in- per gram of dry soil. In Europe, the EU out at a Danish farm with organic layers crease carcass condemnation or decrease Waste Management Strategy has resulted demonstrated establishment and spread of egg production. in increased low-cost composted recycled fowl cholera and that losses in free-range Insects, such as flies and darkling vegetable waste. Composting eradicates chickens can reach as high as 91% (Stok- beetles, serve as intermediate hosts for nematodes from the vegetable material holm et al. 2010). Although not all stud- tapeworms that complete part of their and lessens the ability of nematodes, and ies demonstrate fowl cholera problems in life cycle in the insect. In caged chicken some bacteria, to repopulate the material. free-range poultry (Fossum et al. 2009), egg layers, tapeworms can occur if flies Such composted material can act as a the findings of Stokholm and colleagues are numerous. Flies can become infected good soil medium, and good forage mate- (2010) demonstrate the potential. A nega- in one location and fly to another. The rial can be established. tive interaction between roundworms and flies are then able to get into the feed- Coccidiosis is caused by infection the bacterium that causes fowl cholera ers and be consumed by the chickens. In with a single-celled protozoal parasite has been reported, leading the authors free-range systems, poultry are expected in the genus Eimeria. The organisms are to suggest that free-range chickens are to forage and ingest insects that poten- host specific. Every class of poultry and at a higher risk of being subjected to tially harbor an intermediate form of the livestock has at least one species that outbreaks of fowl cholera when they are tapeworm. Once the insect intermediate affects them. It is common in animals infected with roundworms. host is ingested, the tapeworm is released raised on solid surfaces, whether on dirt and matures in the intestine of the poultry or concrete. Every commercial livestock Disease Spread host and begins producing eggs. In low enterprise has some type of control There is concern that free-range numbers, the tapeworm appears to have a program for this parasite. Coccidiosis is poultry may serve as reservoirs of disease minor deleterious effect on the vitality of most devastating in young animals, but it exposure to conventional production the host or on the production of eggs. In can occur in older animals that have not systems. Avian influenza and exotic New- heavy infestations, they may occasionally been previously exposed. Chickens, in castle disease (END) are the two most se- migrate out of the digestive tract through particular, are susceptible to coccidiosis rious diseases of concern. This is not only the cloaca and into the oviduct where at any age. Lampkin (1997) identified because of the high mortality they cause, they may become incorporated into an coccidiosis as the major health issue with but also because of the economic impact egg. This is extremely undesirable for organic chicken meat production as well that may result due to trading restrictions the consumer. The incidence of tape- as pullet rearing. The problem was found and embargoes placed on infected areas. worms in free-range poultry can be high to be less serious for layers because adult Many countries, including the United (Kaufmann et al. 2011). The cecal worm chickens can rely more on natural im- States, enforce strict control measures in (Heterakis gallinae), which is a nematode munity. Fisker (1998), however, indicated the event of outbreaks of either of these parasite carried by the earthworm (trans- that there is little evidence to suggest that two diseases. port host), carries the protozoal parasite coccidiosis is a major problem in organic Concerns are based on the contact Histomonas meleagridis, the cause of chicken meat production in Denmark, with wild birds and other animals com- blackhead disease (histomoniasis), which despite the ban on the prophylactic use of mon in free-range poultry. Free-range can be deadly to turkeys. Blackhead is anticoccidials. flocks are at a similar or higher level of now becoming a problem in cage-free, Fowl cholera is caused by infection risk as the conventionally reared flocks free-range, and organic flocks of laying with Pasteurella multocida, which may because of the lack of solid barriers to re- hens. Broiler breeder flocks are suscep- be present in most species of wild birds. liably keep out wild birds and mammals. tible to blackhead as well. Transmission of Pasteurella multocida Even though intensive rearing provides Rotational grazing of the paddock area from wild birds to domestic poultry has much more control of exposure oppor- was not found to have an effect on the been demonstrated (Sossidou et al. 2011). tunities, having a source of infection in worm burden (Ascaridia galli, Heterakis It is associated with high death losses in the neighborhood with free-range flocks gallinarum, Capillaria spp.) of free-range poultry, especially turkeys. It can be eas- increases the potential of an infectious laying hens (Maurer et al. 2013). There is ily carried on fomites and spreads through agent entering a closed house by some some research, however, that shows that water. The disease is prevented by strict means. As a result of minimal clinical there may be genetic differences in the biosecurity methods, and live and killed signs while shedding the virus in the susceptibility to Ascaridia galli infec- vaccines are available. The vaccines do early stages of the infection, it is theoreti- tions (Permin and Ranvig 2001), which not completely prevent infection, but cally possible that infected free-range may provide a tool for geneticists when they greatly lessen the severity of the flocks could be a source of infection and selecting breeders for free-range poultry disease. Comparing the genetic makeup contamination for other poultry in the production in the future. of fowl cholera strains isolated from area. The type of soil media in the free- Danish free-ranging flocks and those of There are several categories of in- range system can affect the level of isolated waterfowl showed that they were fectious agents, and the possibilities nematodes present (Sossidou et al. 2008). closely related (Christensen, Dietz, and of transmission from a reservoir vary Composting recycled vegetable waste Bisgaard 1998). A longitudinal investiga- considerably among them. The role of

COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY 11 passerine and terrestrial wild birds in the the Midwest outbreak occurring during enza (Kuiken et al. 2003). Chicken to spread of AI may be minimal (Forrest, the winter when those birds would have human transmission of avian influenza Kim, and Webster 2010), however, given been confined indoors because of the cold has been reported in Asia and the Nether- that there is no evidence to indicate that outside temperatures and thus be less lands. To date, human to human transmis- they are a natural reservoir of the virus vulnerable to exposure. It is important to sion has been very limited. (Slusher et al. 2014). To properly under- note that many of the hobby-type produc- There are three forms of the ND: len- stand the risks associated with wild birds, ers are less likely to seek a diagnosis togenic (mild), mesogenic (medium clini- a better knowledge of the interaction if they have dead birds because their cal signs), and velogenic (severe disease, between wild birds and poultry is needed, financial livelihood was not dependent also known as END). Both live and killed as well as of the possible transmission on the flock and they do not always have vaccines for commercially reared chicken of influenza virus between these two affordable access to an avian veterinar- and turkeys are available. Flocks infected populations. Passerine birds could enter ian or diagnostic lab. It is interesting to with the velogenic strains (END) are the barns and infect poultry directly or note, however, that the first introduction eradicated when detected. Wild birds can contaminate surfaces near poultry barns. of the virus into egg-producing chickens transmit the disease to free-range flocks. This contamination can be transported by occurred in a backyard flock. In 1992, for example, it was documented farm workers, equipment, rodents, and The AI outbreak in British Columbia that cormorants in North Dakota trans- insect pests to the poultry (Burns et al. occurred in the winter months when mitted ND virus to a free-ranging turkey 2012). waterfowl are at their highest numbers flock (Heckert et al. 1996). In addition, Burns and colleagues (2012) docu- near poultry farms. Free-ranging flocks END was confirmed in a backyard flock mented wild bird activity on poultry in close proximity to water reservoirs, in the state of California in October 2002. farms in two major poultry-producing therefore, would be more likely to have Within six months, the disease had spread regions of Canada. Of the nearly 300 interaction between wild waterfowl and to backyard flocks in Nevada, Arizona, wild birds known to inhabit these areas, the poultry flock. The Swiss national and Texas. In California, the virus was approximately 20% were observed in the monitoring of AI in wild waterfowl and eventually transmitted to commercial vicinity of commercial poultry farms. free-range poultry farms documented the poultry. As a result, 3.5 million birds These included the American robin, barn introduction of AI in Switzerland by wild were destroyed to eradicate the disease. swallow, common grackle, dark-eyed waterfowl in mid-February 2006. As per In May 2018, END was again detected in junco, European starling, horned lark, the surveillance reports, however, the backyard flocks in California. All the ini- northwestern crow, rock dove, and song virus was not detected in the free-range tial flocks were exhibition chickens. It is sparrow. There is very little information poultry flocks at the same time period not yet clear how the flocks were infected published on the presence of the AI virus (Dalessi, Hoop, and Engels 2007). and how the disease spread. in these species. Burns and colleagues Based on surveillance data, there is a Mycoplasma is another disease- (2012) also identified conditions that re- significantly higher risk of introducing causing organism of concern in com- sulted in large flocks of birds near poultry AI on farms with Anseriformes species mercial poultry flocks, especially those farms. These included flooded pastures (duck, geese, and game birds) compared with outdoor access. The National and harvested corn fields. Freemark and to those housing Galliformes poultry Poultry Improvement Plan (NPIP) has Kirk (2001) reported that the practices types (broilers, layer chickens, and tur- a control program for testing and elimi- of noncrop habitat, more permanent crop keys) (Gonzales 2012). Outdoor chicken nation of breeder flocks infected with cover, and less intensive management egg production as well as duck (breeders Mycoplasma gallisepticum (MG). Many on organically managed cropland lead to and meat) and turkey farms were shown of the commercial egg production flocks, increased diversity of bird populations. to have a significantly higher risk of in- however, are infected. Flock infec- This may be critical to maintain avian troduction of AI compared with indoor tions cost producers in condemnation at diversity, but for those mixed-farming egg production farms. This may be due slaughter of meat birds and in loss of egg operations, it brings more birds in closer to their higher risk of exposure to an production in egg-producing flocks (up to proximity to the poultry houses. AI-contaminated environment and/or 12 eggs lost per hen out of the 250 eggs In 2014 there was an outbreak of AI contact with wild waterfowl. Their longer expected by 60 weeks of age [Moham- in British Columbia, Canada. In 2015, it production cycle would also affect the med, Carpenter, and Yamamoto 1987]). spread to California and then the Mid- length of exposure. In a study in the There are live and killed vaccines avail- west. According to an epidemiological Netherlands, outdoor layer, turkey, duck- able to help control or mitigate the effects analysis, the incidences occurred on the breeder, and meat-duck farms had an 11, of MG infections. Vaccines, however, Pacific and Mississippi flyways, and -mi 8, 24, and 13 times higher rate of intro- do not eliminate the infection. Chickens, gratory fowl are believed to have played duction of AI than indoor layer farms, especially the white leghorn, are more a role in the outbreak (USDA–APHIS– respectively (Gonzales et al. 2012). resistant to the effects of infection than VS 2015). It should be noted, however, The 2003 AI outbreak in the Nether- turkeys and can serve as a source of that no free-range commercial poultry lands resulted in 87 human cases. There infection for them. There have been anec- flocks were reported to be infected in is a continuing threat of a new influenza dotal reports of outbreaks in turkey flocks the 2015 outbreak. This may be due to pandemic developing from avian influ- associated with hauling spent laying hens

12 COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY past a turkey farm (Mohammed, Carpen- ner. Sustainability, however, is hard to phosphorus (available for plant update) ter, and Yamamoto 1987). The organism, define. Producers are under intensive in free-range egg layer operations in therefore, can be spread from one farm to pressure to minimize the impact of their Australia were concentrated within 6 m another. Many backyard flocks have birds production on the environment or carbon (6.56 yards) of the poultry house. that are not sourced from NPIP-certified footprint. Putnam and colleagues (2017) Lee, Wen, and Chang (2010) reported flocks, and outbreaks of MG have been completed a retrospective analysis of that nutrient loading in free-range poultry reported. the U.S. poultry industry from 1965 to operations in Taiwan can lead to envi- Infectious laryngotracheitis (ILT) is 2010. They found that climate change, ronmental problems from leaching and a disease that primarily affects chick- acidification, and eutrophication impacts runoff. Similar findings were reported ens, but it can also infect pheasants and associated with chicken meat production by Kratz, Rogasik, and Schnug (2004) peafowl. Chickens must be in fairly close decreased by 36%, 29%, and 25% per for chicken meat production and by contact for transmission among them. 1,000 kg (2,204.62 lb) of meat produced, Haneklaus, Schnug, and Berk (2000) for The virus, however, can survive for short respectively. There were also reductions turkey meat production, both in Germany. periods of time to be transported on fo- in resources required. Fossil energy use Jones and colleagues (2007), however, mites and clothing if conditions are cool decreased by 39%, water depletion by did not detect changes in groundwater and moist. If a chicken survives the infec- 58%, and agricultural land occupation nitrate and phosphate concentrations as- tion, it is a carrier for life and can shed by 72% per 1,000 kg (2,204.62 lb) of sociated with the expansion of free-range the virus at irregular intervals. An infec- chicken meat produced. poultry production in the UK. The rela- tion of ILT is more readily spread from The environmental impact of poultry tive environmental risks from excessive acutely infected birds than from contact production depends on several factors, nutrient loading of range area will be site with latently infected birds (Swayne et and waste disposal is a primary concern. specific and will depend on a number al. 2013). The likelihood of airborne If properly managed, the manure and of environmental factors, especially soil spread is not well documented. The virus litter produced is a valuable resource. The type. can be carried short distances, however, large amount of waste generated, howev- Some free-range systems use bottom- on a variety of fomites that have been er, may exceed the local demand, making less, moveable shelters in which the ma- contaminated by contact with materi- poultry waste a potential problem instead nure is deposited directly to the range and als from infected birds (Swayne et al. of a valuable resource. It is possible to the shelters moved regularly. Although 2013). It frequently appears in backyard turn manure from a cost and negative these represent a small proportion of the chickens after exposure at various exposi- environmental impact to a money-making commercial flocks, they do provide a tions when they contact sick or latently enterprise. This requires proper handling means to evenly distribute the manure infected birds. of the manure and development of a in the range area, minimizing nutrient It is not common for nematodes to be distribution plan that does not overload a buildup. present in caged laying hens. Confined specific area. Animals, feed, manure, and hous- poultry on solid flooring, especially if the There has been very little research ing accessories contribute to potential litter is reused, often have roundworms. looking at manure deposition in free- sources of the environmental footprint. It is unlikely that free-range poultry range poultry facilities. Larsen and col- The impact of poultry production on the would serve as a reservoir and source of leagues (2017) used RFID to look at ecological systems may result from direct infestation for confined poultry because range use on two commercial free-range release of airborne constituents into the of the separation of the caged birds from egg laying farms in Australia. They iden- atmosphere, direct runoff to water bod- their fecal material. Some nematodes are tified three areas of the range based on ies, leaching to groundwater, or indirect carried by invertebrates. Their presence the distance from the shelter. They in- deposition of airborne constituents into in confinement poultry would indicate cluded the veranda (0–2.4 m [0–2.62 water bodies. The different commercial a breach in biosecurity in the area of yards]), close range (2.4–11.4 m [2.62– poultry production facilities vary signifi- pest control rather than some means of 12.47 yards]), and far range (>11.4 m cantly in terms of housing and manure exposure to an infested free-range flock. [12.47 yards]). They found that most hens handling practices. Different housing With regard to cestodes, insect intermedi- used the range every day (68.6% for one options vary in the ability to regulate ate hosts may be readily available to both flock and 82.2% for the second). Hens environmental conditions that will, in free-range and confined poultry. Infested typically only spent 14% of their time on turn, affect resource utilization efficiency. free-range flocks would not be consid- range (Larsen et al. 2017), which would There is very little research comparing ered a reservoir for conventionally reared imply that most of the manure would be the efficiency of free-range production commercial poultry. deposited in the poultry house. The hens to more confined systems. Livestock spent half their outdoor time in the veran- production is believed to have a major da area adjacent to the shelter. This would impact on the environment, and consum- Environmental Impact be the area of heaviest manure build up, ers are looking to include more environ- The main aim of sustainable animal possibly leading to nutrient runoff. mentally friendly products in their diet. production is to produce a high-value Wiedemann and colleagues (2018) Comparative assessments of free-range animal protein in a sustainable man- showed that soil nitrate and colwell- and conventional production systems,

COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY 13 however, can be difficult. There are amount of feed consumed per hen. It indoor and the organic systems; however, often differences in strains used and feed was largely these general differences that the organic-plus system used a different formulations, in addition to the differ- affected the environmental impacts of slower-growing strain. The total cost of ences in production systems. Bokkers and the systems. The different systems also feed per production unit was 20% higher de Boer (2009) compared conventional used different diets, resulting in different for the organic system compared to the chicken meat production raising a fast- environmental burdens per unit of feed. conventional system. The final weight, growing strain with organic chicken meat Overall, the results showed that the cage feed conversion, and mortality rates were production raising a slow-growing strain, system had the lowest eutrophication and better for the conventional indoor system, both on the same farm in the Netherlands, acidification potentials, as well as lowest but the conventional system was found and reported that the organic system with primary energy use and global warming to have the highest impact on climate outdoor access had higher emissions of potential (GWP). Comparing the cage change and environmental loading. greenhouse gases (GHGs), higher use of and free-range systems, the hens in cages The results of Castellini and col- fossil fuels, and increased land use. produced more eggs, consumed less feed, leagues (2012) was similar to the results Not all forms of energy have the same had lower mortality, less land use, and reported by Boggia, Paolotti, and Castel- “quality.” Solar emergy measures solar decreased feed spillage. lini (2010). They also used the LCA (equivalent) energy. Emergy evaluation Leinonen and colleagues (2012b) also method to compare conventional indoor, is a tool for evaluating environmental used the LCA method, from cradle to organic, and organic-plus chicken meat impact of animal production systems. It farm gate, to compare the environmental production systems in Italy, cradle to is expressed as solar emjoules. Castellini burden of conventional indoor, free- farm gate. The systems differed in final and colleagues (2006) used this approach range, and organic chicken meat produc- market weight, strain used, grow-out to compare conventional and organic tion in the UK. Different strains were time, and feed composition, making di- chicken meat production for the period used in each system, with the organic sys- rect comparison of indoor and free-range covering cradle to gate. The conven- tem having a slower-growing strain. They production systems difficult. In their tional system with a fast-growing strain also had different feed formulations. study, feed for the conventional system of chickens reared in a well-controlled Surprising, the authors reported that the accounted for 78.8% of the overall envi- environment and using veterinary treat- number of chickens required to produce ronmental impact for the conventional in- ments (coccidiostats and antibiotics) out- 1,000 kg (2,204.62 lb) of edible carcass door system. The main contribution was performed the slower-growing strain of was highest for the conventional indoor from the soybeans and corn. Feed pro- chickens in the organic system with out- system. This, however, was due to a low- duction in the organic system represented door access. In both systems the poultry er finishing weight in the indoor system. 87.3% of the total environmental impact, feed represented 50% of the emergy flow. Mortality, however, was higher and the whereas it was 87.8% in the organic-plus Although the performance was lower for length of the grow-out period longer in system. The organic-plus system had the the organic system, the environmental the free-range and organic systems. As a highest land use. The overall results of impacts were also lower. result, feed consumption per chicken was the study showed that the organic system There are different methods for assess- higher in these two systems. The GWP had a better environmental performance ing the environmental impact of poul- was highest for the type of feed used in than the other two systems. try production systems. One is GHGs. the conventional indoor system, primar- As indicated previously, mortal- Greenhouse gas emissions, however, are ily resulting from the use of imported ity rates tend to be higher in free-range only part of the environmental impact. soybean meal and palm oil. Comparing production systems compared to con- Ammonia and particle emissions are also the conventional indoor and free-range ventional indoor systems (Eigaard et al. released from poultry houses. In addi- systems, the conventional system had 2003; Sossidou et al. 2011; and Wongrak tion, energy is used directly for feeding, higher primary energy use, slightly higher et al. 2014). Weeks, Lambton, and Wil- heating, lighting, and ventilation. The GWP, higher eutrophication potential, liams (2016) completed a mega-analysis life cycle assessment (LCA) method higher acidification potential, but similar of ten studies in the UK and reported considers the environmental burdens pesticide and land use. Organic systems, that, whereas cumulative mortality for and resource use over a specific period however, had the highest primary energy free-range layer flocks averaged 7.89%, of the production cycle. Leinonen and use, eutrophication potential, and land it ranged from 0 to 69.3%. High levels of colleagues (2012a) used the LCA method use. mortality decreased the sustainability of from cradle to farm gate to compare the Castellini and colleagues (2012) used egg production. They investigated how environmental burden of egg produc- a multicriteria approach to compare the changes in cumulative mortality affect tion in four production systems in the sustainability of conventional indoor, or- the environmental burden of flocks. The UK: conventional cage systems, barn ganic, and organic-plus (required a slow- general effect of increased cumulative systems (cage free), free range, and growing strain and increased outdoor mortality was to increase all environmen- organic. The number of hens needed to access) chicken meat production systems tal impacts, including GHG emissions, produce 1,000 kg (2,204.62 lb) of eggs in Italy. They looked at economic, social, eutrophication potential, acidification was highest for the organic produc- environmental, and quality factors. Simi- potential, pesticide use, abiotic resource, tion system, which also had the highest lar strains were used in the conventional and land occupation. If the higher

14 COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY mortality could be decreased to levels kept in floor pens were reported to have poultry meat, Salmonella and Campylo- associated with caged production, GHG decreased egg production rates (Karcher bacter are the main pathogens of con- emissions could be lessened by 25%. The et al. 2015). Moving from intensive cern, whereas the most significant public results show the potential scale for the (cage) to extensive production systems health risk for eggs is the transmission effect of very poor management, housing, requires significant increases in labor of Salmonella, specificallySalmonella or biosecurity. time commitments—a 45% increase enteritidis. The research on the bacterial On a global scale, livestock occupy in man-hours from cage to cage free, a loads of poultry meat from conventional about 70% of all the agricultural land and 279% increase in man-hours from cage and free-range systems has been conflict- 26% of the ice-free land surface (Stein- to free range, and a 161% increase in ing. Comparing results between systems feld et al. 2006). With the still-growing man-hours from cage free to range (An- is difficult because of differences in geo- global population and per capita incomes, derson 2014). There are no peer-reviewed graphic location, seasons, and detection the amount of food required will be studies looking at the man-hours for and isolation methods. considerably higher in years to come. To moveable pens, but presumably they will Regardless of the research conclu- meet this demand, we will need to have be the highest. It will vary depending on sions regarding the relative food safety of better feed efficiency in animal food pro- the size and type of moveable pens used. chickens, consumers should not assume duction, decreased food wastage, and di- Based on labor inputs, free-range produc- that all free-range chickens are free etary changes in favor of vegetable food tion is less efficient than caged systems. of Salmonella and/or Campylobacter. and less-demanding meat (Wirsenius, The same can be said for conventional Azar, and Berndes 2010). The switch to production systems. Proper handling of free-range poultry production systems is Conclusions poultry meat from any production system counter to this with decreased production Management is key to optimizing is essential and should not be overlooked performance, decreased feed efficiency, animal welfare in any production system. based on the production system used. The and increased land use (Golden, Arbona, Although many perceive free-range poul- microbial load on eggshells in both cage and Anderson 2012). try production systems to be more animal and free-range nests is comparable from As previously indicated, the environ- welfare friendly, the research comparing well-managed facilities. The difference mental impacts associated with chicken the different production systems is incon- comes from eggs that are laid outside of meat production arise primarily from clusive and often contradictory. Providing the nest on the floor and the range pad- feed consumption. Diet formulation and an outdoor run can lead to higher space dock, which both have microbial popula- feed ingredient choice should be consid- allowances, an increase in the number tions that even washing cannot decrease ered to mitigate these impacts. Tallen- and types of behavioral and physiological to a safe level. The food safety of eggs tire, Mackenzie, and Kyriazakis (2017) stimulations, and the freedom to move from the range must also include chemi- looked at different diet formulations for between different environments with cal safety because dioxins, pesticides, production systems in the UK and the changes in climatic conditions and bird and lead can be issues with free-range United States and found that using a preferences. Based on these criteria, one production in some locations. multicriteria approach to diet formula- can assume that there is an increase in There is very little documented tion, where environmental impact as well animal welfare. It is important to note, research with regard to the disease risks as economic impacts are considered, will however, that there are also increased associated with free-range as compared be the basis for improving the sustain- risk factors that can adversely affect bird with conventional poultry production ability of chicken meat production. The welfare. These include increased contact systems. It is documented that free-range two regions were considered separately with infectious agents, greater difficulties poultry have more exposure to certain since legislation, trade agreements, and maintaining hygienic standards, increased external and internal parasites because climatic conditions result in different feed possibilities of unbalanced diets, and of access to invertebrates and wild birds. ingredients being used in the two areas. increased threat of predation. Although free-range poultry may be more The GWP for the UK system is much The main conclusion that can be made vulnerable to certain diseases, there is no higher than that of the U.S. system. This with regard to the nutritional composi- indication that the presence of free-range is primarily due to the importation of the tion of poultry products is that it is more poultry poses a risk to conventional soybean meal from South America where reflective of what the bird eats rather poultry. deforestation is common. In the United than the type of production system used. The research results regarding the States, however, 100% of the soybeans Outdoor access itself does not alter the environmental impact of different pro- used in conventional poultry production nutritional content of the products. It does duction systems vary considerably and are grown domestically. In both regions appear, however, that the nutrient content are often conflicting. The main issues af- it was not possible to minimize the effect of poultry meat and eggs can be enhanced fecting environmental impact are manure on one category without impacting at with access to pastures, with the effect management and feed formulation. Free- least one other. Formulating for decreased depending on the type and quality of the range poultry production requires more environmental impact, for example, pasture provided. land at a time when there is high demand results in higher feed costs. Food safety is an important consid- for agricultural land. When compared with caged hens, hens eration with any production system. For There is considerable variation in

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COUNCIL FOR AGRICULTURAL SCIENCE AND TECHNOLOGY 19 Widowski, T. M., P. H. Hemsworth, J. L. Barnett, Syst 103:621–638. potentially zoonotic bacteria and bacterial and J.-L. Rault. 2016. Laying hen welfare I. Wongrak, K., G. Daş, E. Moors, B. Sohnrey, and J. resistance to antimicrobials in organic and Social environment and space. World Poultry M. Gauly. 2014. Establishment of gastro- conventional poultry, swine, and beef produc- Sci J 72:1–10. intestinal helminth infections in free-range tion: A systematic review and meta-analysis. Wiedemann, S., C. Pratt, N. Bliefield, D. G. Mayer, chickens: A longitudinal on farm study. Berl Epidemiol Infect 137:1217–1232. M. R. Redding, and E. McGahan. 2018. Münch Tierarztl 127:314–321. Young, S. and J. Dawe. 2008. Treatment of Intesti- Establishing soil nutrient distribution zones Yilmaz Dikmen, B., A. İpek, Ü. Şahan, M. Petek, nal Worms in Broiler Breeders. Arbor Acres across free-range egg farms to guide practical and A. Sözcii. 2016. Egg production and wel- Service Bulletin, 0708-AVNAA-018, July. nutrient management strategies. Agr Ecosyst fare of laying hens kept in different housing Zimmerman, P. H. and P. Koene. 1998. The effect Environ 257:20–29. systems (conventional, enriched cage, and free of frustrative nonreward on vocalisations and Wirsenius, S., C. Azar, and G. Berndes. 2010. How range). Poultry Sci 95:1564–1572. behaviour in the laying hen, Gallus gallus much land is needed for global food produc- Young, I., A. Rajic, B. J. Wilhelm, L. Waddell, S. domesticus. Behav Process 44:73–79. tion under scenarios of dietary changes and Parker, and S. A. McEwen. 2009. Comparison livestock productivity increases in 2030? Agr of the prevalence of bacterial enteropathogens,

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The mission of the Council for Agricultural Science and Technology (CAST): CAST, through its network of experts, assembles, interprets, interprets, and com- municates credible, balanced, science-based information to policymakers, the media, the private sector, and the public. The vision of CAST is a world where de- cision making related to agriculture and natural resources is based on credible information developed through reason, science, and consensus building. CAST is a nonprofit organization composed of scientific societies and many individual, student, company, nonprofit, and associate society members. CAST's Board is composed of representatives of the scientific societies, commercial companies, nonprofit or trade organizations, and a Board of Directors. CAST was established in 1972 as a result of a meeting sponsored in 1970 by the National Academy of Sciences, National Research Council. ISSN 1070-0021

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Citation: Council for Agricultural Science and Technology (CAST). 2018. Impact of Free-range Poultry Production Systems on Animal Health, Human Health, Productivity, Environment, Food Safety, and Animal Welfare Issues. Issue Paper 61. CAST, Ames, Iowa.

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