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Selection method and early-life history affect behavioural development, feather pecking and cannibalism in laying hens: A review
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Applied Animal Behaviour Science 110 (2008) 217–228 www.elsevier.com/locate/applanim
Review
Selection method and early-life history affect behavioural development, feather pecking and cannibalism in laying hens: A review T. Bas Rodenburg *, Hans Komen, Esther D. Ellen, Koen A. Uitdehaag, Johan A.M. van Arendonk Animal Breeding and Genomics Centre, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands Accepted 14 September 2007 Available online 30 October 2007
Abstract The aim of this review is to discuss the effects of selection method and early-life history on the behavioural development of laying hens. Especially in larger groups, laying hens often develop damaging behaviours, such as feather pecking and cannibalism, leading to impaired animal welfare. We hypothesise that the propensity to develop feather pecking and cannibalism is affected by a bird’s genetic background and by its early-life history. The genetic background can be influenced by genetic selection. Laying hens are traditionally selected on individual performance, which may lead to co-selection of feather pecking and cannibalism. For hens kept in small groups, it has recently been demonstrated that a novel group selection method, focusing on group performance, can help to reduce cannibalism. However, the biological background behind the success of group selection is unknown. It is also not known whether these results from small groups can be translated to larger groups of laying hens. Regarding early-life history, laying, brooding and rearing conditions have been shown to have major effects on behavioural development and on feather pecking and cannibalism. The presence of a hen during rearing has been shown to improve foraging- and social behaviour, to decrease feather pecking and to decrease fearfulness in chicks. Applying group selection and rearing laying hens in a more natural environment may be key factors in solving the problems caused by feather pecking and cannibalism, especially if the promising results of group selection from small groups in experimental settings can be translated to large-group housing systems. # 2007 Elsevier B.V. All rights reserved. Keywords: Laying hens; Genetic selection; Rearing conditions; Feather pecking
* Corresponding author. Tel.: +31 317 483 936; fax: +31 317 483 929. E-mail address: [email protected] (T.B. Rodenburg). 0168-1591/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2007.09.009
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Contents 1. 2. 3. 4. 5.
Introduction . . . . . . . . . . . . . . . Feather pecking and cannibalism . Genetic background . . . . . . . . . . Early-life history . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . References . . . . . . . . . . . . . . . .
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1. Introduction Especially in large groups, laying hens often develop damaging behaviours, such as feather pecking and cannibalism, leading to impaired animal welfare. Feather pecking is a multifactorial problem affected by the genetic background of the birds, their early-life history and by environmental factors. Despite a considerable research effort aiming to solve the problem of feather pecking, it is still a major welfare problem in commercial laying hen husbandry. The aim of this review is to discuss the effect of selection method and early-life history on the behavioural development of laying hens. It is hypothesised that the propensity to develop feather pecking and cannibalism is affected by a bird’s genetic background and by its early-life history. Future research should aim at integrating promising research approaches regarding the combined effect of genetic background, early-life history and environmental factors on the development of feather pecking to come to a solution for the problem.
2. Feather pecking and cannibalism Feather pecking is the pecking at- or pulling out of feathers of other birds. Feather pecking varies in severity from gentle- to severe feather pecking (Savory, 1995). Gentle feather pecking can be explorative (Riedstra and Groothuis, 2002) or stereotyped gentle feather pecking. Both forms of gentle feather pecking seem to be separate forms of pecking behaviour and do not seem to develop into severe feather pecking (Rodenburg et al., 2004b; Newberry et al., 2007). Severe feather pecking may lead to denuded areas. If pecking continues in these areas, it develops into cannibalism. A victim of cannibalism is wounded and eventually killed. Vent pecking is a separate form of cannibalistic pecking that can also be observed in well-feathered birds (Savory, 1995). Feather pecking should not be confused with aggressive pecking, which is used to maintain the dominance hierarchy (Savory, 1995), although social rank may influence feather pecking behaviour (Wennrich, 1975). Feather pecking seems to derive from a ground pecking motivation and not from an aggressive motivation. That feather pecking, cannibalism and aggression are not the same, for instance, can be seen in an experiment by Cloutier and Newberry (2002). They found that mixing unfamiliar hens led to an increase in aggression, but had no effect on feather damage or cannibalism. There is an ongoing debate regarding the causes of feather pecking. Feather pecking is thought to be a form of redirected behaviour, developing either from ground pecking (Blokhuis, 1986) or pecking during dustbathing (Vestergaard and Lisborg, 1993). Access to sand, straw or grain during rearing has been shown to reduce feather pecking later in life, probably because this
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stimulates ground pecking and dustbathing early in life (Blokhuis and Haar, 1992; NorgaardNielsen et al., 1993; Vestergaard et al., 1993). Blokhuis and Arkes (1984) showed that groups of birds housed on slatted floors showed more feather pecking than groups housed on litter. Moreover, when groups kept on litter were transferred to pens with slatted floors, feather pecking also developed in these groups. Vestergaard and Lisborg (1993) showed that chicks that were trained to dustbathe on feathers instead of sand during the first days of life, continued to dustbathe on- and peck at feathers in tests at an age of 5 weeks. Huber-Eicher and Wechsler (1997), however, showed that provision of sand did not prevent feather pecking up to 7 weeks of age, whereas the provision of straw led to a reduction of feather pecking in the same period. Furthermore, feather pecking on group level was inversely related with foraging activity, but not with dustbathing activity in their study. Recently, Newberry et al. (2007) performed a detailed study on the relationships between pecking behaviours over age on an individual level. They found a positive relationship between foraging behaviour at young age (3–15 weeks of age) and severe feather pecking behaviour at adult age (17–37 weeks of age). Furthermore, observations on the same birds when adult revealed a positive correlation of 0.41 between foraging and severe feather pecking (Bilcı´k and Keeling, 2000). This correlation does not support the theory that feather pecking is redirected behaviour, but indicates that birds that are more active and show high levels of foraging and seeking behaviour are more likely to develop severe feather pecking. These results are not necessarily in contradiction with the results found by Blokhuis and Arkes (1984) and by Huber-Eicher and Wechsler (1997). Between groups, it still holds true that groups housed in pens without litter will show more feather pecking than groups housed in pens with litter. Within a group, however, it does not seem true that severe feather pecking substitutes for foraging behaviour (at the level of the individual bird). In studies of feather pecking behaviour, not only the feather pecker but also the receiver of feather pecking has been studied. It does not seem the case that some birds are genetically predisposed to become victims of feather pecking, as the heritability estimate for receiving feather pecking is generally not significantly different from zero (Kjaer and Sørensen, 1997; Rodenburg et al., 2003). Keeling et al. (2004), however, showed that the heritable trait feather pigmentation can have a marked influence on the risk of an individual to become a victim of feather pecking, with pigmented birds being more vulnerable to feather pecking than white birds. No relationship was found between feather pigmentation and propensity to peck feathers, which accounts for the fact that feather pecking is still a major problem in white feathered birds. The authors argue that pigmented birds may be more attractive to peck at, because the white litter particles show a sharper contrast when deposited on their plumage compared with white birds. Similarly, McAdie and Keeling (2000) showed that birds with feathers that were already damaged or ruffled were more attractive to peck at than birds with intact feathers. The behaviour of the receiver of feather pecking may also play a role. Recently, Riber and Forkman (2007) found that inactive birds were more at risk to be targeted by feather peckers than active birds. When comparing feather peckers and victims in a frustration test, Rodenburg et al. (2005) found that feather peckers showed higher levels of aggressive, dominance-related pecking than victims. Victims of feather pecking are not likely to be the dominant birds in a group, as the dominant birds would react aggressively to birds pecking at their feathers. Indeed, Wennrich (1975) showed that the majority of feather pecking was directed at low-ranking individuals. In conclusion, feather pecking is a multi-factorial problem affected by the genetic background of the birds (Bessei, 1984; Kjaer and Sørensen, 1997; Rodenburg et al., 2003), their early-life history (Roden and Wechsler, 1998; Riber et al., 2007), and by environmental factors, such as availability of floor substrate (Blokhuis, 1986), nutrition (van Krimpen et al., 2005),
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adequate lighting (Kjaer and Vestergaard, 1999), and group size and stocking density (Nicol et al., 1999; Bilcı´k and Keeling, 2000; Rodenburg and Koene, 2007). To come to a solution for the problem of feather pecking and cannibalism, an integrated approach is needed that takes all three important factors (genetic background, early-life history and environmental factors) into account. 3. Genetic background Line differences in plumage condition and in feather pecking behaviour suggest a genetic background (Hughes and Duncan, 1972; Ambrosen and Petersen, 1997; Wahlstrom et al., 2001; Kjaer and Sørensen, 2002; Hocking et al., 2004; Uitdehaag et al., 2007). Uitdehaag et al. (2007) compared six pure lines from a Rhode Island Red origin (brown egg layers) and six pure lines from a White Leghorn origin (white egg layers) and found a consistent difference in feather damage between the two origins. White Leghorn lines had more feather damage than Rhode Island Red lines. These line differences can be used to breed laying hens with a reduced propensity to develop feather pecking and cannibalism. It would be useful to further study the causation of feather pecking in these different lines, and study whether birds that are active and show high levels of foraging at young age develop more feather pecking as adults (as found by Newberry et al., 2007). Apart from selection between lines, selection within lines can be used to improve existing lines by genetic selection using genetic variation within lines. Direct selection against feather pecking or mortality due to cannibalism within lines has been shown to be feasible, using either individual selection (Kjaer and Sørensen, 1997; Kjaer et al., 2001) or group selection (Craig and Muir, 1993; Muir, 1996). Kjaer and Sørensen (1997) used individual selection to select for and against feather pecking. This divergent selection led to a marked difference in feather pecking behaviour between the high (HFP) and the low feather pecking (LFP) lines. Commercial breeders generally use selection on individual performance to select their breeding stock. A negative aspect of selection on individual performance is that it can lead to coselection of undesired behavioural traits, such as feather pecking and cannibalism, because these traits are not expressed in individually housed birds. An alternative to individual selection is group selection, which tries to avoid selecting for undesirable behaviour by accounting for the effect of an animal on its group members and vice versa. Muir (1996) used group selection within sire family groups to select on group survival in small groups of laying hens. Using this method, mortality was successfully reduced from 68% in generation 2 to 9% in generation 6. A drawback of this method is that information on the performance of individual birds cannot be measured. From the field of evolutionary genetics, alternative statistical models are available that allow the construction of novel group selection methods (Muir and Schinckel, 2002; Bijma et al., 2007a,b; Ellen et al., 2007). The method developed by Bijma et al. (2007a,b) can be used to estimate a bird’s genetic propensity for pecking and for being pecked in groups of laying hens randomly placed together and this information can then be included in the selection program. Ellen et al. (2007) used a selection program, where selection of individually housed birds was based on the performance of their relatives kept in family groups. Using this method, vital information from individually housed birds, such as feed intake and egg production, can be combined with the information on the propensity to develop damaging behaviour in grouphoused birds. They used this method to select for and against mortality in laying hens and found a marked difference between the birds selected for high and low mortality after only one generation of selection.
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Although the success of group selection methods in reducing mortality in laying hens is clear (Muir, 1996; Ellen et al., 2007), very little is known about the biology behind it. Cheng and Muir (2005) studied the physiological response to group selection on mortality and found major differences in the regulation of the adrenal system and in immunity between their low and high mortality populations. They suggested that these differences may reflect that birds from the low mortality population have better abilities to cope with novel environments and to have a greater resistance to stressors than birds from the high mortality population. When these populations were subjected to immunological stress, using an LPS-challenge, birds from the low mortality population had acute, transient behavioural and physical changes with less negative effects on body weight gain, organ development, and core temperature compared with birds from the high mortality population (Cheng et al., 2004). Similarly, in the high (HFP) and low (LFP) feather pecking lines created by Kjaer and Sørensen (1997), Buitenhuis et al. (2006) found that birds from the HFP line had a stronger response to an immunological challenge and a smaller number of white blood cells after the challenge compared with the LFP line. Cheng et al. (2001b) also compared the high and low mortality populations under social stress, by housing birds together with unknown individuals from a cannibalistic line in a two-bird cage. It was found that birds from the low mortality population had a longer attack latency and showed less feather pecking behaviour than birds from the high mortality population. Furthermore, birds from the high mortality population showed a stronger corticosterone response and an increased adrenal gland weight in response to social stress compared with birds from the low mortality population, indicating that the change in social environment was physiologically more stressful for birds from the high mortality population (Cheng and Muir, 2004). Cheng et al. (2001a) found that birds selected for low mortality had lower serotonin and catecholamine levels than birds selected for high mortality and tended to have higher basal corticosterone levels. Similar results were found in a comparison of high (HFP) and low (LFP) feather pecking lines of laying hens (Korte et al., 1997; Van Hierden et al., 2002b). These lines were commercial selection lines that showed a consistent difference in feather pecking (Rodenburg and Koene, 2003). In these HFP and LFP lines, major differences in behaviour were found as well. HFP birds showed higher levels of gentle and severe feather pecking than LFP birds, but also showed differences in targeting of pecking behaviour: HFP birds seemed to be more animal-directed (preening, feather pecking), whereas LFP birds seemed to be more environment-directed (foraging, feeding, object pecking) (Van Hierden et al., 2002a; Rodenburg and Koene, 2003). Furthermore, HFP and LFP birds responded very differently when they were tested repeatedly in an individual test, isolated from their group members: HFP birds showed a sharp increase in number of vocalisations over time, whereas LFP birds showed a decrease (Rodenburg and Koene, 2003). This indicated that HFP and LFP birds had different ways of coping with the test situation. In a cross-population of these lines, birds that were more fearful at 5 weeks of age were more likely to develop feather pecking as adults (Rodenburg et al., 2004a). Craig and Muir (1996) also studied behavioural differences between the group selected birds and random-bred controls. They found no differences in fearfulness between both populations. Group selection is a promising method to reduce mortality due to feather pecking and cannibalism (Muir, 1996; Ellen et al., 2007), but presents some ethical challenges. Using a black box approach, we could end up with an animal that is not responsive to its environment, similar to the example of the blind hens described by Ali and Cheng (1985). They compared blind and sighted hens and found that blind hens had a better performance and were less affected by factors such as group size and stocking density. On the other hand, these blind hens were unable to interact with each other or to display all their natural behaviours. Although the results presented
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by Cheng et al. (2001b, 2004) and Cheng and Muir (2004, 2005) do not indicate that selection against mortality leads to birds that are less responsive to their environment, the effects of group selection on behavioural development should be studied further. An intriguing question is whether group selection against mortality leads to birds that are more social, less fearful and have a decreased propensity to develop feather pecking and cannibalism, without losing their responsiveness to the environment. Until now, the experiments on the effect of selection method have been done using small groups of laying hens. Research is needed to study whether these results can be translated to large groups of laying hens. The results presented by Bijma et al. (2007a,b) indicate that group selection against mortality may be more efficient in groups of 12 birds than in groups of four birds. It is unknown whether birds that show no feather pecking and cannibalism in groups of four or 12 birds will also show no damaging behaviour when housed in larger groups. This is especially important because of the ban of traditional cages in the European Union from 2012, which will result in more laying hens being kept in larger groups. 4. Early-life history Both the conditions under which the eggs were laid, the brooding period and the early-life history of the chicks (0–7 weeks of age) can have profound effects on the behavioural development of the chicks. Janczak et al. (2007) showed that chicks from mothers that were stressed during egg laying were more fearful and less competitive than chicks from control mothers, although these chicks were reared without their mother. Similar results were found if eggs were treated with the stress hormone corticosterone (Freire et al., 2006; Janczak et al., 2006), indicating that the level of stress hormones in the egg influences the behaviour of the chicks. Furthermore, Nordgreen et al. (2006) found that exposure to corticosterone also affects filial imprinting of the chick on its mother and hence may affect social behaviour of chicks. Treatment of the eggs with testosterone, on the other hand, boosts the development of the chicks and makes the chicks more aggressive and competitive (Schwabl, 1996; Gil, 2003; Eising et al., 2006). In nature, maternal testosterone increases in each subsequently laid egg in a clutch, presumably to correct for reduced growth caused by later hatching (Schwabl, 1993). Furthermore, it has been found that the testosterone concentration is dependent on the social status of the mother, as Mu¨ller et al. (2002) found in laying hens. They found that dominant females allocated more testosterone to male eggs than to female eggs, whereas subdominant females increased the testosterone concentration of female eggs. The authors suggested that differential deposition of testosterone might provide a mechanism for adaptive maternal investment. Similarly, the increased deposition of corticosterone in the eggs of mothers that reproduce in a stressful environment may be an advantage (being smaller and more flighty) for the chicks, preparing them for a potentially difficult life in the same environment (Hayward and Wingfield, 2004). Testosterone has been found to have an effect on feather pecking and cannibalism. Hughes (1973) found that the amount of feather pecking and cannibalism could be reduced by administering testosterone to pullets. Testosterone has been shown to boost aggressive-, sexualand learning behaviour in the domestic chick (Andrew et al., 1981; Clifton and Andrew, 1983). Hence, testosterone may also affect learning of pecking behaviour and substrate preferences. Regarding corticosterone, also a direct relationship with feather pecking has been found. Ellethey et al. (2001) found that feeding young laying hens corticosterone led to reduced growth, increased flightiness and increased feather pecking.
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Regarding the brooding period, it has been found that prenatal light exposure during brooding affects development of the chicks. Riedstra and Groothuis (2004) found that chicks that had been exposed to light for 2 h on day 19 showed higher levels of gentle feather pecking than darkbrooded chicks. They suggested that gentle feather pecking is social exploration (Riedstra and Groothuis, 2002) and that exploration is a laterized function in the domestic chick (Deng and Rogers, 2002). This laterization of functions in the brain can be stimulated by light exposure late in the embryonic development. After hatching, using a light or a dark brooder has major effects on the behavioural development of the chicks (Johnsen and Kristensen, 2001; Jensen et al., 2006b). Johnsen and Kristensen (2001) found that birds kept under dark brooders showed lower levels of severe feather pecking than birds kept under light brooders (heating lamps), but that there were no differences in feather damage and mortality. Jensen et al. (2006b), however, found major, positive effects of dark brooding on prevention of feather pecking, feather damage and mortality. The authors argued that the development of feather pecking was impeded because inactive chicks could rest in darkness, separated from the active chicks, hence avoiding being pecked. Maternal deprivation can have serious consequences. In rats, Mirescu et al. (2004) showed that maternal deprivation led to a reduced ability to respond to stress later in life. Another study (Gardner et al., 2005) reports that maternal deprivation in rats can result in changes in coping strategy: maternally deprived rats developed a reactive strategy and control rats a proactive strategy. In domestic chicks, the presence of a hen during the rearing period has been shown to increase foraging activity of the chicks (Roden and Wechsler, 1998; Riber et al., 2007). Riber et al. (2007) found that brooded chicks performed more ground pecking than non-brooded chicks, especially during the first week of life. Interestingly, the foster hens performed about four times as much ground pecking as their chicks in this first week, presumably to stimulate their ground pecking behaviour. Based on the hypothesis presented by Newberry et al. (2007), the birds that show high levels of foraging when young are more likely to develop feather pecking as adults, it may be expected that brooded chicks would develop more feather pecking than non-brooded chicks. Riber et al. (2007), however, found lower mortality levels due to feather pecking and cannibalism in brooded chicks than in nonbrooded chicks, showing that this is not the case. It could be that the hen is guiding the chicks to peck at more rewarding substrates, such as food or litter. Hence, the active ground-peckers, who are at risk of developing feather pecking, may be less likely to do so when they are reared with a hen. Wauters et al. (2002) studied the influence of the presence of a mother hen on the food preferences of the chicks. They provided the hens with a choice between three different foods. Each hen had a clear preference and showed this preference by pecking the preferred food and uttering food calls. From the brooded chicks, 93% showed a preference and this preference was strongly correlated to its mother’s choice with correlations ranging from 0.66 to 0.80. From the non-brooded chicks, only 64% showed a preference and non-brooded chicks showed much less feeding activities. Perre´ et al. (2002) found that brooded chicks were less fearful and had a higher social motivation later in life than non-brooded chicks. Interestingly, it has been found that chicks that are fearful at young age have an increased propensity to develop feather pecking behaviour as adults (Rodenburg et al., 2004a). Similarly, chicks from a high feather pecking line had a lower social motivation at young age, when tested in an open-field (Jones et al., 1995). Jensen et al. (2006a) also found that brooded chicks were more synchronised in their behaviour than non-brooded chicks and they suggested that synchronisation may also
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help to reduce severe feather pecking, as feather pecking is frequently directed at inactive chicks. Chicks reared with a hen are guided by the hen by vocalisations and visual displays, such as pecking movements. Woodcock et al. (2004) studied the effects of hen vocalisations on feeding behaviour of broiler chicks, and found that chicks that received hen vocalisations during the first 9 days of life grew faster during this period than control chicks. Chicks that received hen vocalisations also spent more time in the vicinity of the speaker that produced the vocalisations than control chicks. Kent (1987) showed that chicks can discriminate between familiar and unfamiliar hens by means of the hen’s cluck vocalisations. This discrimination is better when hens are presented than when recorded hen vocalisations are presented. Apart from vocalisations, the hen uses her own pecking behaviour to guide her chicks and to teach them to peck at edible items. Nicol and Pope (1996) showed that hens are sensitive to errors made by the chicks: when chicks pecked at coloured food items that were unpalatable to the hen, hens increased ground and food pecking and scratching behaviour, presumably to encourage the chicks to continue searching. Clearly, the presence of a hen has major effects on the behavioural development of the chicks. However, poultry species are about the only domesticated animals in which mother and offspring are completely separated in practice. Eggs are brooded in artificial brooders and chicks are reared in large, single-age groups without mother hens present. There are reasons for this separation of mother and offspring. Mixing of age groups is generally avoided in poultry husbandry to avoid transmission of infections from one population to the other. Mixing age groups would also reduce the efficiency level of the industry. Research shows, however, that rearing chicks with a mother hen may be a very rewarding method to reduce behavioural problems in laying hens. For future research, it would be interesting to study whether presenting chicks with key stimuli, imitated from the stimuli presented by the mother, can have a similar, positive impact on the behavioural development of the chicks. Furthermore, it may be a challenge both for research and industry, to develop new systems that include rearing chicks with foster mothers, without endangering animal health or efficiency. 5. Conclusion The aim of this review was to discuss the effects of selection method and early-life history on the behavioural development of laying hens. The literature showed that novel selection methods can help to reduce mortality in laying hens, but little is known about the effect of these methods on behavioural development of the birds. Research is needed to study what type of animal we are selecting for. Regarding early-life history, literature showed that laying- and brooding conditions and the presence of a hen during rearing have profound effects on behavioural development and on reduction of feather pecking and cannibalism. Until now, the experiments on the effect of selection method and of early-life history have been done using small groups of laying hens. It should be studied whether these results can be translated to larger groups of laying hens. Applying group selection and rearing laying hens in a more natural environment may be key factors in solving the problems caused by feather pecking and cannibalism, especially if the promising results from small groups in experimental settings can be translated to large-group housing systems. Future research should aim at integrating promising research approaches regarding the effect of genetic background, earlylife history and environmental factors on the development of feather pecking to come to a solution for the problem.
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Acknowledgements The authors would like to thank Hendrix Genetics for participating in this study. This research is supported by the Dutch Technology Foundation STW, Applied Science Division of NWO and the Technology Program of the Ministry of Economic Affairs.
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Applied Animal Behaviour Science 110 (2008) 217–228 www.elsevier.com/locate/applanim
Review
Selection method and early-life history affect behavioural development, feather pecking and cannibalism in laying hens: A review T. Bas Rodenburg *, Hans Komen, Esther D. Ellen, Koen A. Uitdehaag, Johan A.M. van Arendonk Animal Breeding and Genomics Centre, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands Accepted 14 September 2007 Available online 30 October 2007
Abstract The aim of this review is to discuss the effects of selection method and early-life history on the behavioural development of laying hens. Especially in larger groups, laying hens often develop damaging behaviours, such as feather pecking and cannibalism, leading to impaired animal welfare. We hypothesise that the propensity to develop feather pecking and cannibalism is affected by a bird’s genetic background and by its early-life history. The genetic background can be influenced by genetic selection. Laying hens are traditionally selected on individual performance, which may lead to co-selection of feather pecking and cannibalism. For hens kept in small groups, it has recently been demonstrated that a novel group selection method, focusing on group performance, can help to reduce cannibalism. However, the biological background behind the success of group selection is unknown. It is also not known whether these results from small groups can be translated to larger groups of laying hens. Regarding early-life history, laying, brooding and rearing conditions have been shown to have major effects on behavioural development and on feather pecking and cannibalism. The presence of a hen during rearing has been shown to improve foraging- and social behaviour, to decrease feather pecking and to decrease fearfulness in chicks. Applying group selection and rearing laying hens in a more natural environment may be key factors in solving the problems caused by feather pecking and cannibalism, especially if the promising results of group selection from small groups in experimental settings can be translated to large-group housing systems. # 2007 Elsevier B.V. All rights reserved. Keywords: Laying hens; Genetic selection; Rearing conditions; Feather pecking
* Corresponding author. Tel.: +31 317 483 936; fax: +31 317 483 929. E-mail address: [email protected] (T.B. Rodenburg). 0168-1591/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2007.09.009
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Contents 1. 2. 3. 4. 5.
Introduction . . . . . . . . . . . . . . . Feather pecking and cannibalism . Genetic background . . . . . . . . . . Early-life history . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . References . . . . . . . . . . . . . . . .
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1. Introduction Especially in large groups, laying hens often develop damaging behaviours, such as feather pecking and cannibalism, leading to impaired animal welfare. Feather pecking is a multifactorial problem affected by the genetic background of the birds, their early-life history and by environmental factors. Despite a considerable research effort aiming to solve the problem of feather pecking, it is still a major welfare problem in commercial laying hen husbandry. The aim of this review is to discuss the effect of selection method and early-life history on the behavioural development of laying hens. It is hypothesised that the propensity to develop feather pecking and cannibalism is affected by a bird’s genetic background and by its early-life history. Future research should aim at integrating promising research approaches regarding the combined effect of genetic background, early-life history and environmental factors on the development of feather pecking to come to a solution for the problem.
2. Feather pecking and cannibalism Feather pecking is the pecking at- or pulling out of feathers of other birds. Feather pecking varies in severity from gentle- to severe feather pecking (Savory, 1995). Gentle feather pecking can be explorative (Riedstra and Groothuis, 2002) or stereotyped gentle feather pecking. Both forms of gentle feather pecking seem to be separate forms of pecking behaviour and do not seem to develop into severe feather pecking (Rodenburg et al., 2004b; Newberry et al., 2007). Severe feather pecking may lead to denuded areas. If pecking continues in these areas, it develops into cannibalism. A victim of cannibalism is wounded and eventually killed. Vent pecking is a separate form of cannibalistic pecking that can also be observed in well-feathered birds (Savory, 1995). Feather pecking should not be confused with aggressive pecking, which is used to maintain the dominance hierarchy (Savory, 1995), although social rank may influence feather pecking behaviour (Wennrich, 1975). Feather pecking seems to derive from a ground pecking motivation and not from an aggressive motivation. That feather pecking, cannibalism and aggression are not the same, for instance, can be seen in an experiment by Cloutier and Newberry (2002). They found that mixing unfamiliar hens led to an increase in aggression, but had no effect on feather damage or cannibalism. There is an ongoing debate regarding the causes of feather pecking. Feather pecking is thought to be a form of redirected behaviour, developing either from ground pecking (Blokhuis, 1986) or pecking during dustbathing (Vestergaard and Lisborg, 1993). Access to sand, straw or grain during rearing has been shown to reduce feather pecking later in life, probably because this
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stimulates ground pecking and dustbathing early in life (Blokhuis and Haar, 1992; NorgaardNielsen et al., 1993; Vestergaard et al., 1993). Blokhuis and Arkes (1984) showed that groups of birds housed on slatted floors showed more feather pecking than groups housed on litter. Moreover, when groups kept on litter were transferred to pens with slatted floors, feather pecking also developed in these groups. Vestergaard and Lisborg (1993) showed that chicks that were trained to dustbathe on feathers instead of sand during the first days of life, continued to dustbathe on- and peck at feathers in tests at an age of 5 weeks. Huber-Eicher and Wechsler (1997), however, showed that provision of sand did not prevent feather pecking up to 7 weeks of age, whereas the provision of straw led to a reduction of feather pecking in the same period. Furthermore, feather pecking on group level was inversely related with foraging activity, but not with dustbathing activity in their study. Recently, Newberry et al. (2007) performed a detailed study on the relationships between pecking behaviours over age on an individual level. They found a positive relationship between foraging behaviour at young age (3–15 weeks of age) and severe feather pecking behaviour at adult age (17–37 weeks of age). Furthermore, observations on the same birds when adult revealed a positive correlation of 0.41 between foraging and severe feather pecking (Bilcı´k and Keeling, 2000). This correlation does not support the theory that feather pecking is redirected behaviour, but indicates that birds that are more active and show high levels of foraging and seeking behaviour are more likely to develop severe feather pecking. These results are not necessarily in contradiction with the results found by Blokhuis and Arkes (1984) and by Huber-Eicher and Wechsler (1997). Between groups, it still holds true that groups housed in pens without litter will show more feather pecking than groups housed in pens with litter. Within a group, however, it does not seem true that severe feather pecking substitutes for foraging behaviour (at the level of the individual bird). In studies of feather pecking behaviour, not only the feather pecker but also the receiver of feather pecking has been studied. It does not seem the case that some birds are genetically predisposed to become victims of feather pecking, as the heritability estimate for receiving feather pecking is generally not significantly different from zero (Kjaer and Sørensen, 1997; Rodenburg et al., 2003). Keeling et al. (2004), however, showed that the heritable trait feather pigmentation can have a marked influence on the risk of an individual to become a victim of feather pecking, with pigmented birds being more vulnerable to feather pecking than white birds. No relationship was found between feather pigmentation and propensity to peck feathers, which accounts for the fact that feather pecking is still a major problem in white feathered birds. The authors argue that pigmented birds may be more attractive to peck at, because the white litter particles show a sharper contrast when deposited on their plumage compared with white birds. Similarly, McAdie and Keeling (2000) showed that birds with feathers that were already damaged or ruffled were more attractive to peck at than birds with intact feathers. The behaviour of the receiver of feather pecking may also play a role. Recently, Riber and Forkman (2007) found that inactive birds were more at risk to be targeted by feather peckers than active birds. When comparing feather peckers and victims in a frustration test, Rodenburg et al. (2005) found that feather peckers showed higher levels of aggressive, dominance-related pecking than victims. Victims of feather pecking are not likely to be the dominant birds in a group, as the dominant birds would react aggressively to birds pecking at their feathers. Indeed, Wennrich (1975) showed that the majority of feather pecking was directed at low-ranking individuals. In conclusion, feather pecking is a multi-factorial problem affected by the genetic background of the birds (Bessei, 1984; Kjaer and Sørensen, 1997; Rodenburg et al., 2003), their early-life history (Roden and Wechsler, 1998; Riber et al., 2007), and by environmental factors, such as availability of floor substrate (Blokhuis, 1986), nutrition (van Krimpen et al., 2005),
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adequate lighting (Kjaer and Vestergaard, 1999), and group size and stocking density (Nicol et al., 1999; Bilcı´k and Keeling, 2000; Rodenburg and Koene, 2007). To come to a solution for the problem of feather pecking and cannibalism, an integrated approach is needed that takes all three important factors (genetic background, early-life history and environmental factors) into account. 3. Genetic background Line differences in plumage condition and in feather pecking behaviour suggest a genetic background (Hughes and Duncan, 1972; Ambrosen and Petersen, 1997; Wahlstrom et al., 2001; Kjaer and Sørensen, 2002; Hocking et al., 2004; Uitdehaag et al., 2007). Uitdehaag et al. (2007) compared six pure lines from a Rhode Island Red origin (brown egg layers) and six pure lines from a White Leghorn origin (white egg layers) and found a consistent difference in feather damage between the two origins. White Leghorn lines had more feather damage than Rhode Island Red lines. These line differences can be used to breed laying hens with a reduced propensity to develop feather pecking and cannibalism. It would be useful to further study the causation of feather pecking in these different lines, and study whether birds that are active and show high levels of foraging at young age develop more feather pecking as adults (as found by Newberry et al., 2007). Apart from selection between lines, selection within lines can be used to improve existing lines by genetic selection using genetic variation within lines. Direct selection against feather pecking or mortality due to cannibalism within lines has been shown to be feasible, using either individual selection (Kjaer and Sørensen, 1997; Kjaer et al., 2001) or group selection (Craig and Muir, 1993; Muir, 1996). Kjaer and Sørensen (1997) used individual selection to select for and against feather pecking. This divergent selection led to a marked difference in feather pecking behaviour between the high (HFP) and the low feather pecking (LFP) lines. Commercial breeders generally use selection on individual performance to select their breeding stock. A negative aspect of selection on individual performance is that it can lead to coselection of undesired behavioural traits, such as feather pecking and cannibalism, because these traits are not expressed in individually housed birds. An alternative to individual selection is group selection, which tries to avoid selecting for undesirable behaviour by accounting for the effect of an animal on its group members and vice versa. Muir (1996) used group selection within sire family groups to select on group survival in small groups of laying hens. Using this method, mortality was successfully reduced from 68% in generation 2 to 9% in generation 6. A drawback of this method is that information on the performance of individual birds cannot be measured. From the field of evolutionary genetics, alternative statistical models are available that allow the construction of novel group selection methods (Muir and Schinckel, 2002; Bijma et al., 2007a,b; Ellen et al., 2007). The method developed by Bijma et al. (2007a,b) can be used to estimate a bird’s genetic propensity for pecking and for being pecked in groups of laying hens randomly placed together and this information can then be included in the selection program. Ellen et al. (2007) used a selection program, where selection of individually housed birds was based on the performance of their relatives kept in family groups. Using this method, vital information from individually housed birds, such as feed intake and egg production, can be combined with the information on the propensity to develop damaging behaviour in grouphoused birds. They used this method to select for and against mortality in laying hens and found a marked difference between the birds selected for high and low mortality after only one generation of selection.
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Although the success of group selection methods in reducing mortality in laying hens is clear (Muir, 1996; Ellen et al., 2007), very little is known about the biology behind it. Cheng and Muir (2005) studied the physiological response to group selection on mortality and found major differences in the regulation of the adrenal system and in immunity between their low and high mortality populations. They suggested that these differences may reflect that birds from the low mortality population have better abilities to cope with novel environments and to have a greater resistance to stressors than birds from the high mortality population. When these populations were subjected to immunological stress, using an LPS-challenge, birds from the low mortality population had acute, transient behavioural and physical changes with less negative effects on body weight gain, organ development, and core temperature compared with birds from the high mortality population (Cheng et al., 2004). Similarly, in the high (HFP) and low (LFP) feather pecking lines created by Kjaer and Sørensen (1997), Buitenhuis et al. (2006) found that birds from the HFP line had a stronger response to an immunological challenge and a smaller number of white blood cells after the challenge compared with the LFP line. Cheng et al. (2001b) also compared the high and low mortality populations under social stress, by housing birds together with unknown individuals from a cannibalistic line in a two-bird cage. It was found that birds from the low mortality population had a longer attack latency and showed less feather pecking behaviour than birds from the high mortality population. Furthermore, birds from the high mortality population showed a stronger corticosterone response and an increased adrenal gland weight in response to social stress compared with birds from the low mortality population, indicating that the change in social environment was physiologically more stressful for birds from the high mortality population (Cheng and Muir, 2004). Cheng et al. (2001a) found that birds selected for low mortality had lower serotonin and catecholamine levels than birds selected for high mortality and tended to have higher basal corticosterone levels. Similar results were found in a comparison of high (HFP) and low (LFP) feather pecking lines of laying hens (Korte et al., 1997; Van Hierden et al., 2002b). These lines were commercial selection lines that showed a consistent difference in feather pecking (Rodenburg and Koene, 2003). In these HFP and LFP lines, major differences in behaviour were found as well. HFP birds showed higher levels of gentle and severe feather pecking than LFP birds, but also showed differences in targeting of pecking behaviour: HFP birds seemed to be more animal-directed (preening, feather pecking), whereas LFP birds seemed to be more environment-directed (foraging, feeding, object pecking) (Van Hierden et al., 2002a; Rodenburg and Koene, 2003). Furthermore, HFP and LFP birds responded very differently when they were tested repeatedly in an individual test, isolated from their group members: HFP birds showed a sharp increase in number of vocalisations over time, whereas LFP birds showed a decrease (Rodenburg and Koene, 2003). This indicated that HFP and LFP birds had different ways of coping with the test situation. In a cross-population of these lines, birds that were more fearful at 5 weeks of age were more likely to develop feather pecking as adults (Rodenburg et al., 2004a). Craig and Muir (1996) also studied behavioural differences between the group selected birds and random-bred controls. They found no differences in fearfulness between both populations. Group selection is a promising method to reduce mortality due to feather pecking and cannibalism (Muir, 1996; Ellen et al., 2007), but presents some ethical challenges. Using a black box approach, we could end up with an animal that is not responsive to its environment, similar to the example of the blind hens described by Ali and Cheng (1985). They compared blind and sighted hens and found that blind hens had a better performance and were less affected by factors such as group size and stocking density. On the other hand, these blind hens were unable to interact with each other or to display all their natural behaviours. Although the results presented
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by Cheng et al. (2001b, 2004) and Cheng and Muir (2004, 2005) do not indicate that selection against mortality leads to birds that are less responsive to their environment, the effects of group selection on behavioural development should be studied further. An intriguing question is whether group selection against mortality leads to birds that are more social, less fearful and have a decreased propensity to develop feather pecking and cannibalism, without losing their responsiveness to the environment. Until now, the experiments on the effect of selection method have been done using small groups of laying hens. Research is needed to study whether these results can be translated to large groups of laying hens. The results presented by Bijma et al. (2007a,b) indicate that group selection against mortality may be more efficient in groups of 12 birds than in groups of four birds. It is unknown whether birds that show no feather pecking and cannibalism in groups of four or 12 birds will also show no damaging behaviour when housed in larger groups. This is especially important because of the ban of traditional cages in the European Union from 2012, which will result in more laying hens being kept in larger groups. 4. Early-life history Both the conditions under which the eggs were laid, the brooding period and the early-life history of the chicks (0–7 weeks of age) can have profound effects on the behavioural development of the chicks. Janczak et al. (2007) showed that chicks from mothers that were stressed during egg laying were more fearful and less competitive than chicks from control mothers, although these chicks were reared without their mother. Similar results were found if eggs were treated with the stress hormone corticosterone (Freire et al., 2006; Janczak et al., 2006), indicating that the level of stress hormones in the egg influences the behaviour of the chicks. Furthermore, Nordgreen et al. (2006) found that exposure to corticosterone also affects filial imprinting of the chick on its mother and hence may affect social behaviour of chicks. Treatment of the eggs with testosterone, on the other hand, boosts the development of the chicks and makes the chicks more aggressive and competitive (Schwabl, 1996; Gil, 2003; Eising et al., 2006). In nature, maternal testosterone increases in each subsequently laid egg in a clutch, presumably to correct for reduced growth caused by later hatching (Schwabl, 1993). Furthermore, it has been found that the testosterone concentration is dependent on the social status of the mother, as Mu¨ller et al. (2002) found in laying hens. They found that dominant females allocated more testosterone to male eggs than to female eggs, whereas subdominant females increased the testosterone concentration of female eggs. The authors suggested that differential deposition of testosterone might provide a mechanism for adaptive maternal investment. Similarly, the increased deposition of corticosterone in the eggs of mothers that reproduce in a stressful environment may be an advantage (being smaller and more flighty) for the chicks, preparing them for a potentially difficult life in the same environment (Hayward and Wingfield, 2004). Testosterone has been found to have an effect on feather pecking and cannibalism. Hughes (1973) found that the amount of feather pecking and cannibalism could be reduced by administering testosterone to pullets. Testosterone has been shown to boost aggressive-, sexualand learning behaviour in the domestic chick (Andrew et al., 1981; Clifton and Andrew, 1983). Hence, testosterone may also affect learning of pecking behaviour and substrate preferences. Regarding corticosterone, also a direct relationship with feather pecking has been found. Ellethey et al. (2001) found that feeding young laying hens corticosterone led to reduced growth, increased flightiness and increased feather pecking.
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Regarding the brooding period, it has been found that prenatal light exposure during brooding affects development of the chicks. Riedstra and Groothuis (2004) found that chicks that had been exposed to light for 2 h on day 19 showed higher levels of gentle feather pecking than darkbrooded chicks. They suggested that gentle feather pecking is social exploration (Riedstra and Groothuis, 2002) and that exploration is a laterized function in the domestic chick (Deng and Rogers, 2002). This laterization of functions in the brain can be stimulated by light exposure late in the embryonic development. After hatching, using a light or a dark brooder has major effects on the behavioural development of the chicks (Johnsen and Kristensen, 2001; Jensen et al., 2006b). Johnsen and Kristensen (2001) found that birds kept under dark brooders showed lower levels of severe feather pecking than birds kept under light brooders (heating lamps), but that there were no differences in feather damage and mortality. Jensen et al. (2006b), however, found major, positive effects of dark brooding on prevention of feather pecking, feather damage and mortality. The authors argued that the development of feather pecking was impeded because inactive chicks could rest in darkness, separated from the active chicks, hence avoiding being pecked. Maternal deprivation can have serious consequences. In rats, Mirescu et al. (2004) showed that maternal deprivation led to a reduced ability to respond to stress later in life. Another study (Gardner et al., 2005) reports that maternal deprivation in rats can result in changes in coping strategy: maternally deprived rats developed a reactive strategy and control rats a proactive strategy. In domestic chicks, the presence of a hen during the rearing period has been shown to increase foraging activity of the chicks (Roden and Wechsler, 1998; Riber et al., 2007). Riber et al. (2007) found that brooded chicks performed more ground pecking than non-brooded chicks, especially during the first week of life. Interestingly, the foster hens performed about four times as much ground pecking as their chicks in this first week, presumably to stimulate their ground pecking behaviour. Based on the hypothesis presented by Newberry et al. (2007), the birds that show high levels of foraging when young are more likely to develop feather pecking as adults, it may be expected that brooded chicks would develop more feather pecking than non-brooded chicks. Riber et al. (2007), however, found lower mortality levels due to feather pecking and cannibalism in brooded chicks than in nonbrooded chicks, showing that this is not the case. It could be that the hen is guiding the chicks to peck at more rewarding substrates, such as food or litter. Hence, the active ground-peckers, who are at risk of developing feather pecking, may be less likely to do so when they are reared with a hen. Wauters et al. (2002) studied the influence of the presence of a mother hen on the food preferences of the chicks. They provided the hens with a choice between three different foods. Each hen had a clear preference and showed this preference by pecking the preferred food and uttering food calls. From the brooded chicks, 93% showed a preference and this preference was strongly correlated to its mother’s choice with correlations ranging from 0.66 to 0.80. From the non-brooded chicks, only 64% showed a preference and non-brooded chicks showed much less feeding activities. Perre´ et al. (2002) found that brooded chicks were less fearful and had a higher social motivation later in life than non-brooded chicks. Interestingly, it has been found that chicks that are fearful at young age have an increased propensity to develop feather pecking behaviour as adults (Rodenburg et al., 2004a). Similarly, chicks from a high feather pecking line had a lower social motivation at young age, when tested in an open-field (Jones et al., 1995). Jensen et al. (2006a) also found that brooded chicks were more synchronised in their behaviour than non-brooded chicks and they suggested that synchronisation may also
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help to reduce severe feather pecking, as feather pecking is frequently directed at inactive chicks. Chicks reared with a hen are guided by the hen by vocalisations and visual displays, such as pecking movements. Woodcock et al. (2004) studied the effects of hen vocalisations on feeding behaviour of broiler chicks, and found that chicks that received hen vocalisations during the first 9 days of life grew faster during this period than control chicks. Chicks that received hen vocalisations also spent more time in the vicinity of the speaker that produced the vocalisations than control chicks. Kent (1987) showed that chicks can discriminate between familiar and unfamiliar hens by means of the hen’s cluck vocalisations. This discrimination is better when hens are presented than when recorded hen vocalisations are presented. Apart from vocalisations, the hen uses her own pecking behaviour to guide her chicks and to teach them to peck at edible items. Nicol and Pope (1996) showed that hens are sensitive to errors made by the chicks: when chicks pecked at coloured food items that were unpalatable to the hen, hens increased ground and food pecking and scratching behaviour, presumably to encourage the chicks to continue searching. Clearly, the presence of a hen has major effects on the behavioural development of the chicks. However, poultry species are about the only domesticated animals in which mother and offspring are completely separated in practice. Eggs are brooded in artificial brooders and chicks are reared in large, single-age groups without mother hens present. There are reasons for this separation of mother and offspring. Mixing of age groups is generally avoided in poultry husbandry to avoid transmission of infections from one population to the other. Mixing age groups would also reduce the efficiency level of the industry. Research shows, however, that rearing chicks with a mother hen may be a very rewarding method to reduce behavioural problems in laying hens. For future research, it would be interesting to study whether presenting chicks with key stimuli, imitated from the stimuli presented by the mother, can have a similar, positive impact on the behavioural development of the chicks. Furthermore, it may be a challenge both for research and industry, to develop new systems that include rearing chicks with foster mothers, without endangering animal health or efficiency. 5. Conclusion The aim of this review was to discuss the effects of selection method and early-life history on the behavioural development of laying hens. The literature showed that novel selection methods can help to reduce mortality in laying hens, but little is known about the effect of these methods on behavioural development of the birds. Research is needed to study what type of animal we are selecting for. Regarding early-life history, literature showed that laying- and brooding conditions and the presence of a hen during rearing have profound effects on behavioural development and on reduction of feather pecking and cannibalism. Until now, the experiments on the effect of selection method and of early-life history have been done using small groups of laying hens. It should be studied whether these results can be translated to larger groups of laying hens. Applying group selection and rearing laying hens in a more natural environment may be key factors in solving the problems caused by feather pecking and cannibalism, especially if the promising results from small groups in experimental settings can be translated to large-group housing systems. Future research should aim at integrating promising research approaches regarding the effect of genetic background, earlylife history and environmental factors on the development of feather pecking to come to a solution for the problem.
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Acknowledgements The authors would like to thank Hendrix Genetics for participating in this study. This research is supported by the Dutch Technology Foundation STW, Applied Science Division of NWO and the Technology Program of the Ministry of Economic Affairs.
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