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Review of the social and environmental factors affecting the behavior and
welfare of Turkeys (Meleagris gallopavo)

Article in Poultry Science · June 2013

DOI: 10.3382/ps.2012-02943 · Source: PubMed

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 Review

Review of the social and environmental factors affecting the behavior

and welfare of turkeys (Meleagris gallopavo)

J. Marchewka,* T. T. N. Watanabe,† V. Ferrante,† and I. Estevez*‡1

*Neiker-Tecnalia, ArkauteAgrifood Campus, Animal Production, PO Box 46, E-01080 Vitoria-Gasteiz, Spain;
†Department of Veterinary Pathology Hygiene and Public Health, University of Milan, Via Celoria 10,
Milan 20133, Italy; and ‡Ikerbasque, Basque Foundation for Research, 48011 Bilbao, Spain

ABSTRACT In modern rearing systems, turkey pro- turkeys as influenced by the physical and social en-
ducers often face economic losses due to increased ag- vironment that may be relevant to advances toward
gression, feather pecking, cannibalism, leg disorders, or turkey production systems that take welfare into con-
injuries among birds, which are also significant welfare sideration. We addressed the effects that factors such
issues. The main underlying causes appear to relate as density, group size, space availability, maturation,
to rapid growth, flock size, density, poor environmen- lightning, feeding, and transport may have over param-
tal complexity, or lighting, which may be deficient in eters that may be relevant to ensure welfare of turkeys.
providing the birds with an adequate physical or so- Available scientific studies were based in experimental
cial environment. To date, there is little information environments and identified individual factors corre-
regarding the effect of these factors on turkey welfare. sponding to particular welfare problems. Most of the
This knowledge is, however, essential to ensure the wel- studies aimed at finding optimal levels of rearing con-
fare of turkeys and to improve their quality of life, but ditions that allow avoiding or decreasing most severe
may also be beneficial to industry, allowing better bird welfare issues. This paper discusses the importance of
performance, improved carcass quality, and reduced these factors for development of production environ-
mortality and condemnations. This paper reviews the ments that would be better suited from a welfare and
available scientific literature related to the behavior of economic point of view.
Key words: turkey behavior, welfare, production, social behavior, density/group size
2013 Poultry Science 92:1467–1473
http://dx.doi.org/10.3382/ps.2012-02943

INTRODUCTION turkeys, but also because this information is needed to

reduce losses due to poor bird performance.
Turkey production is considered small compared with A recent study showed that 60% of female and 33.8%
broiler production; however, this industry has achieved of male 16-wk-old turkeys in commercial German facili-
a relevant increase since 1980, escalating from 122 mil- ties showed some degree of footpad lesions (Krautwald-
lion to 226 million turkeys produced in 2006 within the Junghanns et al., 2011). Lupo et al. (2010) indicated
European Union countries (Food and Agriculture Orga- that in the French turkey industry the average con-
nization, 2012), whereas the value of turkeys produced demnation rate was 1.8%, whereas condemnation rate
in the United States during 2010 was $4.37 billion (US for broilers was lower and reached 0.87% (Lupo et al.,
Poultry and Egg Association, 2013). Despite the grow- 2008). These are only some examples of relevant animal
ing relevance of turkeys, the scientific literature regard- welfare issues that also have important implications for
ing the welfare of intensively reared turkeys is scarce the economic return of turkey production. Knowledge
compared with other poultry species. There is a major of the main factors affecting the welfare of turkeys and
need for more insight into the factors influencing turkey the means to minimize this impact can not only im-
welfare, not only due to public demands to ensure a prove their quality of life, but may also be beneficial to
sustainable production system that foments manage- industry by achieving better bird performance, improv-
ment practices that take in consideration the welfare of ing carcass quality, and reducing mortality and con-
demnations.
Unfortunately, there is a lack of studies conducted
©2013 Poultry Science Association Inc. under commercial settings, on the effects of the social
Received November 27, 2012.
Accepted February 17, 2013. and physical environment over the behavior, welfare,
1 Corresponding author: [email protected] and performance of commercial turkeys. Most of these

1467
1468 Marchewka et al.

studies have been conducted under particular experi- Turkeys, as birds with a highly competitive social
mental situations (Martrenchar, 1999); therefore, the system (Buchholz, 1997), are prone to behaviors lead-
application of results to commercial practice is difficult. ing to the establishment of a social hierarchy. The hi-
In this paper, we review the available scientific litera- erarchy in groups of wild turkeys is based on close kin
ture regarding fundamental factors affecting behavior relationships between relatives, where external males
and welfare of turkeys; this literature is relevant to con- are rejected from the group after moderately aggres-
sider the establishment of science-based management sive fights, and where the closed units are created for
practices and to ensure animal welfare. life (Balph et al., 1980; Healy, 1992). The effects of
group size, group composition, and space availability
MAIN FACTORS AFFECTING on the behavior of turkeys have been mainly investi-
gated by Buchwalder and Huber-Eicher (2003, 2004,
THE BEHAVIOR AND WELFARE
2005a). They indicated that insufficient space may lead
OF TURKEYS to increased risk for broken wings due to hitting the
pen walls or other birds during aggressive encounters
Density and Group Size
caused by unfamiliarity of newly introduced group
Maintenance of high bird densities per unit of space members (Buchwalder and Huber-Eicher, 2004). The
is a common practice in intensive turkey production incidence of this problem in commercial farms is, so
systems. Although literature for turkeys is scarce, the far, unknown, but probably would be more likely to oc-
abundant references on the effects of density in broilers cur in small enclosures rather than in large commercial
(for a review, see Estevez, 2007) shows the important facilities.
behavioral and performance changes that may occur Small groups of familiar toms seem to be able to dis-
when increasing density, especially when environmental tinguish nongroup members toward whom they display
control is not matched to maintain the demands of the aggressive interactions, but the frequency of interac-
increased number of animals (Dawkins et al., 2004). tions appears to be modulated by enclosure size (Bu-
This situation may lead to more or less severe perfor- chwalder and Huber-Eicher, 2004). More pecks toward
mance and welfare problems. newly introduce unfamiliar toms were observed in small
Density and group size are factors which effects are (2 × 3 m) compared with large pens (6 × 13 m). Buch-
often confounded, together with space availability, be- walder and Huber-Eicher (2004) explained these results
cause only 2 parameters can be controlled simultane- in terms of a minimum critical distance requirement
ously. Therefore, individual effects of each contribut- between opponents, which would be essential to avoid
ing factor are difficult to differentiate. Although it is chances of aggressive interactions. Therefore, the newly
possible to minimize the confusion to a certain extent introduced bird would have been able to keep a larger
by using specific experimental designs (i.e., Leone and distance in large pens, resulting in fewer aggressive en-
Estévez, 2008), it is not always a practical approach, counters. These results differed somewhat from other
especially in applied research, in which the size of the scientific evidences that suggest that aggressive interac-
commercial housing is fixed. Keeping in mind those is- tions, at least in broilers, occur at a higher frequency in
sues, in the current review we treat the effects of group open areas rather than in more crowded regions of the
size and density, as well as the space availability, as enclosure (Pettit-Riley and Estevez, 2001).
were described in the original study. Nevertheless, in another study Buchwalder and Hu-
The influence of density on the behavior and health ber-Eicher (2003), found that the response toward non-
of turkey poults was investigated by Martrenchar et al. familiar conspecifics mainly depended on the size of
(1999), who reduced space allowance from 24 to 15 dm2 the group in which the foreigner was introduced. The
and from 16 to 10 dm2 for males and females, respec- smaller the group (minimum of 6 up to 30 birds), the
tively, until wk 12, and from 40 to 25 dm2 afterward in more intense the aggressive reaction was, with more
case of males. The authors observed gait deterioration fights being initiated and more aggressive pecks being
at higher density, suggesting stocking density as one delivered. These results seem to be in accordance with
of the potential causal factors. They also showed that other poultry studies, without aggression-enhancing in-
stocking density had less influence on behaviors such troductions of foreign individuals to the group, where
as standing, walking, feeding, drinking, preening, and a reduction in the frequency of aggressive interactions
pecking at the environment, or at another bird. How- with increased group size was also reported (Estevez et
ever, similar to the findings for other density studies al., 1997, 2002, 2003).
conducted in broilers (Estévez, 1994; Cornetto et al., Unfamiliarity between several thousand birds of a
2002; Ventura et al., 2012), they found that increased commercial flock is a common situation in modern tur-
density lead to a significant increment in the frequency key rearing systems due to the group becoming too
of disturbances among resting poults (Martrenchar et large to allow any form of hierarchical system. In this
al., 1999). This behavior is considered a factor closely situation, it is inefficient to even attempt to establish a
linked with carcass quality in meat poultry (Cornetto hierarchy. It has been speculated that the cost in terms
et al., 2002). of energy necessary for hierarchy formation in large
 REVIEW 1469
groups of poultry would outweigh the benefits (Estevez available space. However, detailed studies of space use
et al., 1997). Furthermore, the probability of finding in broilers demonstrated that space use related more to
the same individuals over time to get the advantages the size of the enclosure, utilizing a greater amount of
of dominance will be small (Pagel and Dawkins, 1997). space when available, rather than to flock size or den-
Other social strategies, such as a tolerant social system sity (Leone and Estévez, 2008). This might also be the
based on scramble competition, have been proposed to case for turkeys.
explain the social dynamics in large groups of domestic
fowl (Estevez et al., 1997), and they may apply also to Aging and Maturation
turkeys.
Feather pecking is, together with aggressive encoun- Changes in time budgets and behavioral repertoire
ters, an important welfare and management concern are common in growing animals. Poultry is no excep-
in large poultry flocks. They are commonly considered tion. Similar to broilers (Newberry and Hall, 1990; Bi-
to be linked to large groups, as found for laying hens zeray et al., 2000; Pettit-Riley and Estevez, 2001; Este-
(Bilčík and Keeling, 2000). No study has looked over vez et al., 2003), a general decline in activity with age
the effects of group size over feather pecking in turkeys, has been observed in commercial turkeys (Hocking et
but in an experimental study Busayi et al. (2006) com- al., 1999; Martrenchar et al., 1999; Busayi et al., 2006)
pared feather pecking rates of a commercial male line together with a general reduction of oral activities such
selected for growth and breast yield with a traditional as feeding, foraging, drinking, preening, and pecking at
Nebraska Spot turkey coming from small experimen- the pen walls and fixtures (Hocking et al., 1999; Busayi
tal flocks. A higher frequency of pecks and pulls oc- et al., 2006). Parallel results were obtained by Sherwin
curred in males (32%) compared with females (15%) and Kellend (1998), who found a similar decline from
of the commercial line, but were not observed in the 4 to 22 wk of age in sleeping, environment pecking,
traditional one. However, differences in time budgets wing flapping, and running in turkeys maintained in
across sexes were small. Some differences were also ob- small groups and low density, whereas the time engaged
served with regard to age, where males showed stronger in feeding, standing, sitting, strutting, and preening
feather pecks and pulls at 3 wk of age, whereas females varied through the study. At 18 wk, birds spent 30%
showed the highest frequency at 9 wk. of their time strutting, which may be considered as
a threatening behavior but also as courtship toward
Space Availability and Spatial Distribution humans as found in other bird species (Bubier et al.,
1998). Main differences in the behavior of turkeys com-
Spatial distribution, also referred to as space use pat- pared with other poultry species were related to the
terns, is defined as the localization of birds within the absence of dust bathing or ground scratching, which
living area in relation to their group mates and resource are commonly observed in broilers or laying hens (Sher-
distribution. Spatial patterns can be very important win and Kelland, 1998). Running and frolicking were
in terms of bird management as, for example, it was observed, but injurious pecking was rarely noticed and
observed that overcrowding of broilers around the walls feather pecking or cannibalism were not registered at
of the enclosure caused increased disturbances during all during development, even though the animals were
the resting period (Cornetto et al., 2002; Ventura et not beak trimmed, and the light intensities were higher
al., 2012), which may increase the risk of scratches and than the ones of commercial facilities.
downgrading. Although the literature on spatial distri- Similar results were obtained by Hughes and Grigor
bution in turkeys is practically inexistent, one study on (1996) studying time budgets of beak-trimmed turkey
nocturnal turkey behavior reported that sleeping areas poults up to 12 wk, kept in small groups of 10 to 11
were mainly located around enclosure walls (Sherwin birds. Percentage of sitting/sleeping behavior increased
and Kelland, 1998). Therefore, it is expected that tur- over time, whereas standing/walking behavior primar-
keys’ space use would be driven by similar factors as ily declined, and rose at the end of the study. Beak-
those in broilers. related behaviors (feeding, drinking, preening, environ-
In relation to inter-individual distances, Buchwalder mental and bird pecking) rose to the peak of 45% in
and Huber-Eicher (2004) observed that the distance be- wk 2 and then declined gradually to around 28% by
tween the birds was larger across nongroup members the end of the study. The general decline in activity
than within group members. However, this distance with age have been found even when the effects of high
was not the maximum distance that the pen allowed, stocking density and group size were minimized, and
and 50 cm seemed to be sufficient space between the sufficient space was provided to the birds (Sherwin and
unfamiliar individual and the other birds of the group. Kelland, 1998). Reduction in activity also reflected on
This was interpreted as an attempt to integrate in the the distances covered: 27.5 m/30 min at 7 wk to 11.9 at
group, while keeping a safe distance to avoid aggres- 12 wk (Buchwalder and Huber-Eicher, 2005b).
sive reactions from encounters (Buchwalder and Huber- Turkeys are known to increase the incidence of feath-
Eicher, 2004). Under commercial conditions, restricted er pecking and cannibalism with age, and this may have
space availability may inhibit birds to fully use the practical implications. In a comparative study of tra-
1470 Marchewka et al.

ditional and commercial strains of turkeys from 3 to 9 (Lewis et al., 2000), or it may relate to the composi-
wk of age, the frequency of feather pulls was found to tion and proportion of red light that they contain (10%
increase with age in both strains, and a higher occur- for fluorescent compared with 70% for incandescent;
rence of gentle pecks was found in the traditional line, Moinard et al., 2001). Other types of lighting types are
but in no case had effects on mortalities (Busayi et al., known to have powerful effect over the behavior of tur-
2006). However, damaging pecking in turkeys can occur keys. Studies by Gill and Leighton (1984) found birds
as early as the first or second week of age (Moinard et maintained in low intensity blue light were more docile
al., 2001). and less active. Sexual behavior in these pens was at
a minimum, and social interactions were rare. In con-
Photoperiod and Lighting trast, birds exposed to high intensity intermittent white
light were hyperactive and showed extreme flightiness
Lighting has profound effects on the physiology and during handling.
behavior of poultry (Manser, 1996). In modern poultry Another aspect that should be considered in turkey
production, photoperiod and light intensity are strictly management is that turkeys are known for having po-
controlled to promote growth and to avoid excessive tential for vision in the UV-A spectral range, and it is
feather pecking and cannibalism. Interestingly, even possible that plumage may contain visual information
under artificial low light intensity, time budgets seem detectable only under in UV-A wave bands (Hart et al.,
to follow a photoperiod rhythm, with higher propor- 1999). In fact, results from Hart et al. (1999) and Moi-
tion of resting, and low standing and walking occurring nard and Sherwin (1999) suggest that turkeys preferred
during midday (Busayi et al., 2006). At night, turkeys a UV-A-enriched environment to one illuminated by
appear to be mostly inactive, although they may stand fluorescent light alone. In modern housing, the use of
up 2 to 12 times during the dark period, usually turn- fluorescent or incandescent lamps that emit low levels
ing around slowly and lying down again (Sherwin and of the UV-A spectrum may limit the natural commu-
Kelland, 1998). nication conveyed by the plumage of turkeys. In fact,
Although low lighting intensity (1/10 lx) is used to Hart et al. (1999) suggested that provision of supple-
reduce the risk of undesirable behaviors such as feather mentary UV light may reduce the incidence of visually
pecking and cannibalism, it can also inhibit walking, mediated, aberrant behaviors.
foraging, exploration, and social behaviors (Hughes and Besides light intensity and type, the lighting pro-
Grigor, 1996; Barber et al., 2004). In general, turkeys gram has been proven to have a significant effect on
prefer bright environments, as Sherwin and Kelland the behavior of turkeys and may be used to improve
(1998) demonstrated that turkeys avoided chambers bird management. For example, Classen et al. (1994)
with less than 1 lx light intensity compared with 5, 10, demonstrated that turkey male poults of a heavy strain
or 25 lx. But additional studies indicated that turkeys reared to 188 d of age in 6L:18D at 7 d increasing to
may prefer different light intensities to perform differ- 20L:4D by 63 d, or starting with 6L:18D and increas-
ent activities. In this line Barber et al. (2004) demon- ing to 10L:14D from 84 to 112 d, showed a superior
strated that in an experimental situation where birds walking ability and sat less often compared with birds
were given continuous access to 4 rooms with different maintained at constant 24L:0D. Lewis et al. (1998) in-
light treatments (below 1, 6, 20, and 200 lx), at wk 2 vestigated the influence of 4 different photoperiods (8,
birds spent most of time in the brightest environment, 12, 16, or 23 h) with light intensities of 1 or 10 lx on the
whereas at 6 wk the authors observed partition of be- behavior of male turkeys. Light intensity did not influ-
haviors between the 2 light environments. Resting and ence feeding behavior, but injurious pecking took place
perching were only observed in the environment below at a higher frequency for the 12-h photoperiod, 10-lx
1 lx, whereas the rest of the behaviors were performed combinations. On the other hand, Sherwin et al. (1999)
in the 2 brightest environments. Although environmen- carried out an experiment in which the control group
tal enrichment through variation in light intensities was reared under conditions approximating to commer-
may be interesting to improve health and welfare of cial and compared with 2 intermittent lighting patterns
turkeys, this has never been tested under commercial regimens: 12L/24 h and eight 2-h scotoperiods/24 h,
conditions. From a management point of view, it should finding that even though some patterns of intermit-
be considered that a sudden and temporary increase in tent lightning were effective in reducing the frequency
light intensity, for bird inspection for example, may lead of injurious pecking behavior, they compromised other
to fear reaction among birds (Appleby et al., 1992). welfare indicators, such as musculoskeletal function and
Regarding the type of lighting, some studies have the occurrence of blindness (Sherwin et al., 1999).
shown that the use of fluorescent, compared with in-
candescent, lighting reduced the incidence of injuries in Feeding
tails and wings, whereas incidence of tail and wing inju-
ries was positively correlated with the intensity (5, 10, The number of studies dedicated to the effects of diet
36, or 70 lx) of fluorescent lights (Moinard et al., 2001). composition, the form in which is presented, and how
Potential benefits from the use of fluorescent light are its availability may influence behavioral patterns and
that turkeys may perceive it as lower light intensity welfare in turkeys is very limited. Turkey poults at 6 to
 REVIEW 1471
12 wk fed with pellets spent less time feeding compared mals, and the human factor (Mitchell and Kettlewell,
with their behavior at the younger age of 1 to 5 wk, 1998; Prescott et al., 2000; Petracci et al., 2006).
when fed with crumbs (Hughes and Grigor, 1996). On For turkeys, there seem to be some benefits of au-
the contrary, Hale and Schein (1962) found that 12-wk- tomatic, compared with manual, crating in terms of
old pellet-fed birds spent more time feeding; less time reduction of body damage and heart rate (Prescott et
drinking, preening, and resting; and had higher engage- al., 2000). Even though the birds were herded into the
ment in other behaviors compared with mash-fed ones. module using an automatic loading system, the manual
The main differences between these results may relate handling proved to be more stressful than the auto-
to genetic factors due to 30-yr difference between them, matic conveyance. The human participation during the
the age of the birds, and how the feed was presented. manual crating procedure was the factor with the most
Nutritional enrichment in the form of whole wheat influence on turkeys’ stress indicators.
provided in separate feeders, replacing 10% of wheat Recently, Wichman et al. (2010) described the ef-
from their regular diet, has been used with the objec- fect of crate height (45, 50, or 90 cm) during 6 h con-
tive of increasing the time dedicated to feeding and finement on the behavior of turkeys. Whereas turkeys
decreasing time availability for injurious pecking (Mi- could not stand in the lowest crates, they stood 35
rabito et al., 2003). A positive effect of the intervention and 43% of the total time in the 50- and 90-cm-height
was detected during the first 2 wk. However, from 9 wk crates, respectively. More stepping, turning, and preen-
onward, increased feeding frequency was only detected ing were performed in 50- and 90-cm crates, whereas in
during the evening, and in general, the provision of the 40-cm crates more rising attempts were observed.
whole meal had little effect on feeding behavior, and no The conclusion of this study was that 40-cm crates de-
effects on the turkeys’ pecking behavior. creased the possibility of birds moving and changing
Feed restriction is a commonly used management postures. However, a potential danger that should be
practice in the breeder turkey industry to control male considered is that bigger crates can lead to further car-
BW for optimal semen production and to manage risk cass damages due to scratches made by the nails among
of heat stress or musculoskeletal lesions. However, food crated birds.
deprivation can have a negative impact on the welfare
of turkeys, which may manifest through changes in DISCUSSION
their behavior patterns. Hocking et al. (1999) compared
the behavior of ad libitum and feed restricted commer- Scientific studies on the effects of the characteristics
cial Large White turkey male line from 8 to 28 wk. of the physical and social environment of turkeys’ be-
Ad libitum fed birds mainly showed standing, walking, havior and their implications from a welfare standpoint
and preening behavior (44 to 77% of the time budget), are still scarce. In general, studies have demonstrated
whereas feed-restricted birds showed high frequencies that turkeys may show large behavioral adjustments as
of oral activities such as pecking on pen walls and fur- a response to inadequate environmental conditions. For
nishings (20 to 59% of the time budget depending on example, studies focused on the effects of density, group
the week). It was emphasized by the authors that first size, or both have shown that high densities led to gait
signs of the increased oral activity and reduction of sit- deterioration and decreased activity, insufficient space
ting was observed already 2 wk after restriction began. availability related to a higher frequency of injuries, es-
pecially wing breakages, as well as increased aggression
Transport levels, whereas large group size led to feather pecking
occurrences (Sherwin and Kelland, 1998; Martrenchar
Catching and transport of live turkeys, as for other et al., 1999; Buchwalder and Huber-Eicher, 2003, 2004,
poultry, may be one of the most stressful events in the 2005a; Busayi et al., 2006). Similar to other poultry, a
bird’s lifetime if not done properly. Pretransportation general decline in activity was found with increasing
procedures such as inadequate catching and crating age (Hughes and Grigor, 1996; Sherwin and Kelland,
have a major negative impact on birds’ welfare, vary- 1998; Hocking et al., 1999; Martrenchar et al., 1999;
ing from mild stress to death before arriving at the Busayi et al., 2006), with first signs of decreased lo-
slaughterhouse. Therefore, the way in which these pro- comotion becoming apparent generally from 4 wk of
cedures are conducted can have a dramatic impact on age onward (Sherwin and Kelland, 1998), whereas the
carcass quality and economic profit. Most of the avail- injurious pecking may occur already after wk 3 of life
able studies in turkeys describe the direct effects of the (Busayi et al., 2006).
procedures on animal welfare in form of deaths on ar- Feed presentation has also the potential to alter tur-
rival (DOA; Wichman et al., 2010). A large-scale study key activity; the provision of feed in pellets compared
conducted by Petracci et al. (2006) in Italy showed an with crumbles has been associated with longer feeding
average DOA of 0.38% up to 0.52% during the summer. bouts (Hughes and Grigor, 1996), which could be ben-
Causing factors are suspected to be similar to broil- eficial to divert the birds from other undesirable ac-
ers: thermal stress, acceleration, vibration, motion, im- tivities such as feather pecking. However, these results
pacts, fasting, withdrawal of water, social disruption are in opposition to the increased feeding time when
and noise, incorrect transport of sick or injured ani- provided with crumble feed in turkey studies conducted
1472 Marchewka et al.

30 yr ago (Hale and Schein, 1962). Also, the addition Jong et al., 2012). This uncertainty could be reduced
of fodder enrichments in the form of whole wheat was by further studies, expert opinions and their judgments,
found to increase eating time; however, it did not influ- and obviously by studies conducted under commercial
ence birds from 6 wk onward (Mirabito et al., 2003). scenarios. The use of mathematical models for complex
Similar to broiler breeders, in turkeys feed restriction analysis may also be relevant to find the optimal bal-
increased oral activity paralleled with increments in ance between flock productivity and welfare (Estevez,
standing, walking, and preening behavior (Hocking 2007).
et al., 1999), which is typically interpreted as a sign
of hunger and frustration (Bokkers and Koene, 2004). REFERENCES
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most detrimental procedures for welfare, with the po- space on aggressive behaviour in male turkeys (Meleagris gal-
lopavo). Appl. Anim. Behav. Sci. 89:207–214.
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