Applied Animal Behaviour Science 100 (2006) 117–128
www.elsevier.com/locate/applanim
How important is natural behaviour
in animal farming systems?§
Marek Špinka *
Ethology Group, Research Institute of Animal Production,
CZ-104 01 Prague-Uhřı́něves, Czech Republic
Available online 2 May 2006
Abstract
It is often assumed and demanded that for a good welfare, farm animals should be given ‘‘the freedom to
express their natural behaviour’’. This demand is problematic for at least two reasons. First, natural
behaviour is difficult to delineate because of its variability and flexibility. Second, some behavioural patterns
that are clearly natural are in fact detrimental to animal welfare. These include emergency behaviours such
as flight reactions that bring the animal into a state of stress without achieving the goal for which the
behaviour had evolved; and damaging behaviours such as rank-related or illness-related aggression during
which animals inflict injuries or deprive their penmates of resources. Nevertheless, when these reservations
are taken into account, opening possibilities for natural behaviour may be useful as guidance for improving
the existing husbandry systems. Specifically, providing the farm environment with the key features towards
which the behaviour was originally adapted brings three classes of benefits. First, it is often more efficient to
allow animals to satisfy their own needs and achieve their goals than to address these needs and goals
through technical means. Second, a large class of natural behaviours is associated with positive affective
experience, and thus their performance directly enhances animal welfare. Third, the performance of natural
behaviour in its richness and complexity often brings long-term benefits for the animal, such as improved
proficiency in coping with social and physical challenges. Thus, while the freedom to perform the whole
repertoire of natural behaviour is not per se crucial for farm animal welfare, the opportunity to perform
natural behaviour may be an effective way improve their welfare in practice immediately, and a promising
basis for the design of husbandry systems for the future.
# 2006 Elsevier B.V. All rights reserved.
Keywords: Welfare; Natural behaviour; Housing; Motivation; Emotions
§
This paper is part of the special issue entitled Sentience in Animals, Guest Edited by Dr. John Webster.
* Tel.: +420 267 009 596; fax: +420 267 710 779.
E-mail address: spinka@vuzv.cz.
0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2006.04.006
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1. Technical foreword—definitions
In order for me to be able to build up arguments consistently, and for the reader to understand
them, it is necessary to start with a working definition of three key concepts.
In this paper, I will use the word(s) (animal) welfare as a label for how well an animal is doing
in a farming system. By ‘‘doing well’’, I mean primarily how the animal is feeling (Duncan,
1996). However, the term welfare in my usage also includes how well the animal is functioning
biologically as an organism, i.e., how well it is maintaining itself. The reason is that biological
malfunctioning (ill health, injury, physiological failures to cope and pathological behaviour)
ultimately almost always results in negative feelings of the animal like pain, nausea,
psychologically perceived distress, tiredness, etc. On the other hand, the ‘‘wholeness’’ or
‘‘naturalness’’ of the animal’s state will not feature as a concept of welfare in this paper.
Performance of natural behaviour often opens the possibility for good biological functioning and
positive affective states, but this is not always the case. The main purpose of this paper is to
clarify the relationship between natural behaviour and welfare, and positioning of ‘‘naturalness’’
within the concept of welfare, would just complicate the argumentation.
The second term in need of clarification is the word ‘‘natural’’. By natural behaviour, I mean
those behavioural elements and their sequences that are adaptive, i.e., that have evolved either
during the evolution of the species or during its domestication ‘‘in order’’ to increase the fitness
(see definition below) of the behaving animal. This means that behaviour which is natural in one
situation or towards one object may be non-natural in other situation or towards another object.
Thus, massaging the teats of a lactating sow is a natural behaviour for a suckling piglet, but
directing this behaviour towards the bellies of its littermates (the behaviour called ‘‘bellynosing’’) is not natural.
Natural behaviour is never fully hard-wired; it always includes an element of plasticity.
Sometimes, the propensity to learn is even the core of the natural behaviour pattern. It is natural
for young chicks to peck at small objects and to follow intently what the mother hen is pecking at.
Through this trial and error, and the socially facilitated learning, they acquire the knowledge
about the edibility of different kinds of food.
Third, the term ‘‘fitness’’ is used here as evolutionary biologists understand it, i.e., as the
capacity of the individual to survive and spread its genes through producing offspring or
supporting relatives. Thus, fitness in this paper does not denote healthiness or ability to produce
or capacity to withstand challenges, although these properties may contribute to the fitness.
Fitness in this sense is neither identical with nor a part of the welfare of the animal. For example,
a red deer stag A that succeeds to impregnate 10 hinds through fiercely fighting with his rivals but
then is constantly harassed and dies slowly and painfully from a sustained debilitating injury has
a higher fitness, but lower welfare than stag B that avoids conflicts and sires just five progenies
during his 10-year long healthy life.
2. The odd freedom
Somewhat similarly to Tinbergen’s Four Whys in ethology, the Five Freedoms developed by
the British Farm Animal Welfare Council (Webster, 1994) have become a paradigm for
organizing thoughts in animal welfare science. Among the five freedoms, four are freedoms from.
It is relatively straightforward how to strive for their achievement. When an animal is well fed
and watered, its nutritional needs are met, and so the ‘‘freedom from hunger, thirst and
malnutrition’’ is provided. Similarly, the next three freedoms (from discomfort; from pain, injury
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and disease; from fear and distress) could be secured when adequate environment including a
good resting place is provided; when painful procedures, risk of injury and occurrence of disease
are kept at a minimum; when situations and conditions inducing fear or hindering effective
coping are avoided.
The fifth freedom is of a different kind: the freedom to express normal behaviour. This
freedom is less clearly delimited and more controversial than the other four freedoms for two
reasons. First, in contrast with the other four, it does not demand that specific undesirable
physiological, health or psychological states are prevented; it rather requires a kind of general
liberty for all kinds of behaviour of the animal. Thus, the boundaries of this freedom are loose and
open to reinterpretation. Second, the yardstick for this liberty is ‘‘the normal’’ or, in some
versions of this principle, ‘‘the natural’’ form of the behaviour. However, is it straightforward
what behaviour is normal (or natural) and which is not?
3. The complexity of natural behaviour
Natural behaviour does not exist in a form of one standard gauge. Some simple behavioural
patterns are quite uniform across time and across individuals, such as ritualized signal
movements (e.g., the play bow in canids; Bekoff, 1977). However, most behavioural elements are
rather variable in form, duration, and intensity (even those that may seem rather uniform for the
humans, e.g., barking in dogs; Yin and McCowan, 2004) and they occur at widely different rates
and sequential combinations. Based on genetic predispositions, they are guided by interplay
between internal motivational states of the animal and the time dynamic of the stimuli from the
environment (Jensen and Toates, 1993).
Nest building by sows provides a good example of this general point. Prepartum building of a
nest from available vegetation or similar material is a natural behavioural pattern in prefarrowing sows. Nest building starts about 15 h before the start of parturition (Damm et al.,
2003b), probably triggered by the rise in prostagladin F2a (Burne et al., 2001b). The behaviour
can be roughly divided into two phases, namely the initial rooting phase, serving for the
excavation of a hollow, and the second arranging phase, during which nesting material is gathered
and arranged around the hollow. The duration and intensity of the nest building varies widely
according to internal factors (e.g., sow experience; Thodberg et al., 2002) and external stimuli
like availability of building material (Damm et al., 2000), space (Damm et al., 2002) and
environmental temperature (Burne et al., 2001a). Jensen (1993) suggested that the termination of
the second arranging phase may be under control of external stimuli. It is possible that if the sow
perceives the nest as already adequate, taking into account the current environmental conditions,
the location of the nest and available material (Arey, 1997), it will stop the nest building. Indeed,
Jensen (1989) and Mayer et al. (2002) found that the nests of free-ranging domestic and wild boar
sows were less elaborate when located in cover from trees or canopy that provided a better
thermal environment and possible better security. Damm et al. (2000) demonstrated that a higher
quality of the nest (due to inclusion of tree branches in it) induced an earlier termination of nest
building activity, and Kurz and Marchington (1972) reported that in a hot climate, the nest may
consist only of a bedded hollow. If what motivates sows to perform nest-building is the mismatch
between the goal of a comfortable secure nest and the current state of the real nest, one would
expect that the provision of a readymade nest in the form of soft, insulated and slightly hollow
lying surface in a semi-hidden place would substantially reduce at least the second phase of the
nest building in indoor housing systems (Baxter, 1983). On the other hand, if part of
the motivation is a direct drive to execute nest building behaviour independently of the state
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of the environment (as it seems to be the case in nest building in laying hens; Hughes et al., 1989),
then the pre-parturient sow’s motivation will not be entirely quenched by the provision of a prefabricated comfortable and secure bed. Both these models focus on the duration of nest building
and what stops it (Hughes and Duncan, 1988). Newer studies indicate that what matters is not
only the quantity but also the quality of nest building. Damm et al. (2003a) showed that nest
building was less varied, more fragmented by postural changes and accompanied by higher heart
rate and more frequent oral/nasal stereotypies in crate-housed sows than in sows in enriched pens.
These results indicate that nest building may be internally driven yet its form may be sensitive to
the feedback from the environment. Given this complexity in the motivation of nest building, the
current knowledge is insufficient to decide unequivocally whether nest building ‘‘in its natural
form’’ is or is not allowed for in different husbandry systems.
The complexity of the natural behavioural patterns could be illustrated on yet another class of
examples, namely calves’ behavioural reactions to their separation from the mother. Beef calves,
when suddenly separated from their mothers at the age of 2–6 months, produce a lot of
vocalizations and show other signs of distress. However, when calves of the same age are first
prevented from suckling while still in contact with the dam (e.g., through nose plates that do not
allow to grasp the teat or through a net covering the udder), and physically separated a few days
later, almost no vocalizations or other behavioural signs of distress occur (Haley et al., 2005).
Since this two-stage method mimics the key feature of the natural weaning process, namely the
presence of a stage when the calf still wants to suck milk but is prevented to do so by the mother, it
is probable that both the strong and the very weak reaction of the calf to the separation from the
mother are natural behaviours: if the mother disappears suddenly and the calf has been sucking
until now, a strong reaction is appropriate since the mother is a very valuable source of milk. If
weaning has been already fully accomplished, the mother is no longer provides the milk, the
benefit from her vicinity for the calf drops to a fraction of the pre-weaning level, and it is thus
adaptive not to invest much into attempts to reverse her loss. This example shows that the natural
behaviour depends not only on the current internal motivation and the immediate state of the
environment, but may also be quite different depending on how the behavioural interaction of the
animal with the environment develops over time. A similar situation occurs in very early
separation of dairy calves from their mothers. If the separation is accomplished during the first
day, the behavioural (and physiological) reactions of the calf are much weaker than after a
separation at 4, 7 or 14 days (Lidfors, 1996; Flower and Weary, 2001; Stěhulová et al., 2004). The
weak reaction to mutual separation early after birth is once more a natural behaviour, since cattle
are a ‘hiding’ species so it is natural for the newborn calf to see for only a couple of hours per day.
It may also be that newborn calves assess whether mother is taking care of them by their satiation
level, whereas older calves actually monitor the presence of the mother in their vicinity. Even the
reaction of older calves to separation from mother is much dependent on the circumstances.
When other lactating cows are available, the orphaned calf quickly redirects its efforts from
attempts to reunite with the mother into endeavours to get milk from another source. If it is
successful (e.g., through ‘‘stealing’’ milk between the hind legs of the stepmother), its behaviour
in terms of activity, vocalizations and playing is unaffected by the removal or returns back to preseparation levels within 1 or 2 days (Špinka and Illmann, 1991, 1992). Thomas et al. (2001)
showed that just feeding the calf with enough milk more frequently attenuates the reaction to a
fraction of its usual level, thus proving that the post-separation reaction is mainly, although not
exclusively, about the loss of regular milk supply. Overall, these results demonstrate that it is
natural for a calf to suckle milk up to the age for at least 7 months (Reinhardt and Reinhardt,
1981; Reinhardt et al., 1986; Veissier et al., 1990); it is natural for it to strive for reunion with the
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mother when she disappears suddenly; but it is also natural for it not to seek the mother strongly
when she disappears after it has been already weaned or when it has other reliable source of milk.
Beside the fact that ‘‘natural’’ behavioural pattern ‘‘naturally’’ vary enormously in quantity,
there is another even more radical source of variation in natural behaviour: the existence of
behavioural strategies. The term behavioural strategies denotes the fact that different individual
animals (or one individual on different occasions) can and do achieve one and the same goal
through several behavioural routes.
For example, young piglets get their nutrition through sucking milk from their mother. When
several lactating sows are housed together in one area, individual piglets also take milk from alien
sows in a certain proportion of cases. This behaviour, usually labelled cross-sucking or allosucking, is not a case of abnormal or mistaken behaviour. It does occur in free-roaming domestic
sows (Newberry and Wood-Gush, 1985) as well as in free-living wild boar groups (Mauget,
1981). In the case of group-housed lactating domestic sows, there are in fact three sucking
strategies among the piglets (Maletı́nská and Špinka, 2001; Illmann et al., 2005). The faithful
piglets suckle exclusively on their own mother; the opportunistic allosucklers have the own
mother as the main source of milk but occasionally suckle at other sows and finally permanent
allosucklers are piglets that had switched completely to another lactating sows at some point
during the suckling period of life. In a stable group of lactating sows and their litters, all three
strategies are represented and more than one third of all sucklings may occur between a piglet and
a non-biological mother. Yet, in spite of this high level of allosuckling, none of the piglets seem to
suffer from lack of milk intake. In fact, the three strategies seem to be equally successful
(Maletı́nská and Špinka, 2001).
In sum, animals are usually very flexible and often have several alternative strategies available in
their natural behaviour. Therefore, if animals of the same species perform a behavioural pattern
differently (or do not perform it at all in one environment (e.g., a more artificial one) than in another
(a more ‘‘natural’’ one), it does not necessary mean that they are behaving ‘‘unnaturally’’.
4. Is the performance of natural behaviour always good for animal welfare?
The performance of natural behaviour does not necessarily make a positive contribution to the
welfare of farm animals At least two classes of naturally occurring behaviours actually decrease
the welfare of animals.
The first class includes patterns that I will label as ‘‘Emergency behaviours’’, i.e., behavioural
reactions to situations that the animal perceives as immediate and serious threats to its fitness. For
instance, fowl kept in large groups have little experience with humans and a person entering the
stable may cause a sudden increase in panic-like anti-predatory behaviour (Mills and Faure,
1990). A second example relates to sows of modern breeds, whose appetite has been strongly
increased through artificial selection for high food intake. While they are pregnant, their ration is
reduced to 60% of their ad libitum intake (Lawrence et al., 1988). Although this ration is
perfectly adequate for their body maintenance and the pregnancy, the sows perceive it as a threat
of starvation. Consequently, they engage in intensive foraging attempts and if these are not
attenuated through the provision of fibrous material such as straw (Whittaker et al., 1998) they
may develop repetitive abnormal behaviours like bar biting and sham chewing (Lawrence and
Terlouw, 1993). Emergency behaviours are thus behaviours that cost a lot in terms of fitness but
were adaptive in the natural environment of the ancestors because the high cost was outweighed
by the prevention of an even higher fitness loss. However, in terms of welfare in the current
husbandry situations, these behaviours do not bring any benefits to the animals, while their
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welfare cost are high, both in terms of biological functioning and health (e.g., risk of injury;
Knierim and Gocke, 2003) and in the subjective experience, as their performance is usually
accompanied by aversive motivational affective states (Fraser and Duncan, 1998). The
discrepancy between the naturalness and the welfare-compromising effect of emergency
behaviours stems from the fact that natural selection was maximizing fitness, and not welfare,
and these two parameters do not go hand in hand. Although emergency behaviours are perfectly
natural responses to the outstanding situation, it would be a non-sense to argue that farm animals
must be provided with the opportunity to perform these behaviours. On the contrary, the welfare
of the animals requires that situations that are perceived as fitness-threatening by the animals
should be avoided in captivity.
The second class of natural behaviours that may compromise the welfare of the population are
those that contribute to the fitness (and welfare status) of the actor, while, at the same time,
compromise the welfare of another animal or animals. These are the damaging behaviours. The
ancestors of our domestic animals were selected to behave in such a way that would enhance their
own fitness and, in proportion to the degree of relatedness, the fitness of their relatives. When a
limited resource such as space, food or mating partners are at stake, the natural adaptive
behaviour is to push rivals out of the competition. Thus, pigs naturally live in small groups
(Graves, 1984). They therefore perceive the intrusion (and non-retreat) of alien conspecifics as a
threat to their resources and vigorously attack these ‘‘intruders’’ (Rushen and Pajor, 1987). When
mutually unacquainted pigs or groups of pigs are mixed, aggression results. Young suckling
piglets, too, fight fiercely for the possession of teats (de Passillé and Rushen, 1989). Newborn
piglets are in fact equipped with effective weapons (sharp incisor teeth) that can inflict painful
injuries. In large litters, the weakest ones (Fraser and Thompson, 1991) suffer from this
competition in terms of milk intake and weight gain. Social animals such as pig also can behave
aggressively towards lame or injured animals, possibly as a prevention against infectious
diseases. Sometimes, not allowing these damaging behaviours through making the situation
unnatural may be better for the welfare of the animals. For instance, keeping weaned and growing
pigs in large groups reduces substantially the aggression level among the pigs (Turner and
Edwards, 2004; Andersen et al., 2004).
As with emergency behaviours, it would not be in the line of welfare-improving policy to
guarantee the animals the freedom to perform such damaging behaviours, even though they are
undoubtedly a part of their natural behaviour repertoire. The discrepancy between naturalness
and welfare arises here because natural selection was maximizing individual fitness, while
welfare-caring people are concerned with welfare of all animals in the group equally.
5. What use natural behaviour in farm animal welfare?
Is the concept of natural behaviour of any use in farm animal welfare after all? Clearly natural
behaviour can differ in accordance with rather subtle factors and hence it is a vague guide at best
of what we should strive for in farming systems. Moreover some behavioural patterns that clearly
match our concept of natural behaviour are obviously detrimental to the welfare of the animals.
Should we therefore exclude the concept of natural behaviour from animal welfare science and
from the search for practical strategies to improve animal welfare? Would not it be better to
restrict ourselves to the first four freedoms?
In my view, the answer is no. There are important areas of concern in animal welfare that are
not covered by the first four freedoms. I identify three examples of the importance of natural
behaviour to good welfare:
M. Špinka / Applied Animal Behaviour Science 100 (2006) 117–128
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(1) Allowing animals to behave freely in an environment with key natural features may be the
most effective and prudent way of achieving the goals of the farmer.
(2) Natural behaviour involves patterns that are associated with positive affective states.
(3) Natural behaviour may bring long-term benefits to the animals that are difficult to achieve
otherwise or even just to foresee.
6. Allowing for behavioural needs
It has been long noted that animals do possess needs with regard to their behaviour. Thus,
prevention of performance of certain behavioural patterns may cause distress or even
suffering. To take an obvious example, if feeding is prevented, the animal’s welfare is reduced
because of increasing hunger, and may be reduced even further if the individual sees
neighbouring animals feeding (Desiré et al., 2002). Although a narrow definition of
‘‘behavioural needs’’ as internally driven behaviours has been proposed (Hughes and Duncan,
1988; Duncan, 2005), it seems to be more useful not to split the behavioural repertoire of a
species into a catalogue of ‘‘needs’’ and ‘‘non-needs’’. The alternative broader approach
proposed by Jensen and Toates (1993) maintains that to what extent certain behaviour is a need
at the moment depends on the combination of species-specific motivational structure and the
current environmental conditions. The ‘‘needyness’’ of the behaviour is a complex of
obtaining a goal and performing the (usually feedback-sensitive) species-specific behaviour
on the route to the goal (Jensen and Toates, 1993) and can be evaluated by considering what
will happen if the behaviour was prevented. Non-executing of the behaviour may have
negative consequences, and the frustration from the non-performance itself may be one of
them. Considering all these consequences is a more inclusive approach to behavioural
‘‘needs’’ than that focused solely on the contrast between internally and externally driven
behaviours.
For instance, suckling maternal milk is a need for young piglets because if this behaviour is
prevented (e.g., through early weaning), piglets suffer from (at least temporary) undernutrition
(Pajor et al., 2002). These problems can be at least partially prevented if piglets are provided by a
very specific diet. Coping with the switch from suckling milk to eating solid food can be further
ameliorated if piglets are given the opportunity and indeed encouraged to take in solid food
already before weaning. In very young piglets (certainly before the age of 3 weeks; Worobec
et al., 1999), the need to suckle milk has also the component of performing the behaviour leading
to milk intake, because piglets weaned at that age perform the behaviour called ‘‘belly-nosing’’
which is most probably a re-oriented teat-massaging behaviour.
Although it is theoretically possible to secure the goals associated with a specific behaviour
by adjustments of the environment without involvement of the behaviour (e.g., through
specific diets for the piglets) and thus reduces the needyness of certain behaviours, it is in most
cases more efficient to allow for the natural behaviour. The flexibility of natural behaviour is
not an argument against using the concept of natural behaviour in our efforts to improve farm
animal welfare—it is, in fact, one of its main advantages. The flexibility of the route towards
achieving a goal is in most natural motivational systems secured through a number of feedback
mechanisms and choice points. If we allow for natural behaviour, the animals will, in many
cases, use this opportunity flexibly to achieve their goals and thus satisfy their needs. For
instance, the goals of thermoregulation at high and low temperatures and the goal of keeping
body clean from faeces can be all achieved by the pigs through their own behaviour if they are
housed in group pens that contain both a dry bedded area, an unbedded part with cool flooring
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and enough room so that the animals can designate their own dunging areas (Wechsler and
Bachmann, 1998).
7. Promoting positive behaviours
Besides behaviours that serve some immediate goal, the behavioural repertoire of farm animal
species also contains patterns that may be seen as ‘‘luxuries’’, since nothing serious immediately
happens if they are not performed. The examples of such behaviours are play exploration (WoodGush and Vestergaard, 1991), or, to take a more specific example, copious use of a rotating brush
as a scratching post by loose housed cattle. The fact that non-performance of these behaviours
does not pose an immediate threat to fitness is also reflected in their low motivational priority. If
any behavioural need appears, they are immediately interrupted, and may not reappear until long
after the behaviours satisfying needs have ceased. Fraser and Duncan (1998) characterized these
behaviours as being incited by ‘‘opportunity’’, i.e., by a situation when the cost of performing
them is especially low. The important aspect for our discussion is that these behaviours are
associated with positive affective states (e.g., Widowski and Duncan, 2000, for dust-bathing;
Špinka et al., 2001, for play). The reason why negative affective states are linked with needdriven behaviours and the positive ones with opportunity-driven behaviours is the above
mentioned motivational priority: animals will first attempt to remove the source of negative
feelings, and only thereafter strive for positive experience. Obviously, allowing or even
encouraging the animals to perform behavioural patterns associated with positive emotions
undoubtedly improves their welfare.
8. Supporting behaviours with long-term benefits
Allowing for natural behaviours, besides being an effective way of satisfying needs and
promoting affectively positive behaviours, may also contribute to farm animal welfare through
bringing long-term benefits. Common sense wisdom suggests that rearing conditions that
allow or even stimulate the richness of natural behaviour would lead to harmonious
development of the various skills in the animals, especially the social ones. Substantial
scientific evidence has accumulated in support of this claim. For instance, suckling piglets
reared in environments that allow the sow to leave her litters and/or provide the opportunity of
piglets from different litters to mingle together at early age are less affected by the stressful
weaning procedure (Weary et al., 2002; see Section 9.1 for more details). Calves that have
spent several days rather than just the first few hours with their cow mother are more stressed
in the hours immediately following the separation, but when tested 3–6 weeks later for social
competence, display higher level of socially positive behaviours (Stěhulová et al., 2004;
Flower and Weary, 2001). Laying hens exposed to perches at 4 weeks of age later use them at
least twice as much as birds with no experience with perches before week 8 (Appleby and
Duncan, 1989).
The performance of one type of natural behaviour can also positively affect other, seemingly
unrelated behavioural patterns. For instance, caged mink farmed for fur value an access to a water
pool very highly (Mason et al., 2001). The pool allows swimming, diving, head-dipping and
exploration around water, but also increases substantially the amount of playing in the main cage,
away from the water.
Since natural selection probably shaped in the animals a choice between ‘‘keeping low
profile’’ when conditions are unfavourable and expanding activity if life is good, it is probable
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that many instances of long-term or behaviourally remote positive consequences of behaving
naturally will be found.
9. Allowing for natural behaviour improves welfare—examples from practice
9.1. Natural social environment for suckling piglets
Suckling piglets of the ancestor of the domestic pig, the wild boar (Sus scrofa) naturally live in
a complex social environment. Beside the mother who suckles them until the natural weaning at
17 weeks (Jensen and Recén, 1989), there are usually other lactating sows in the group and other
litters of similarly aged suckling piglets (Graves, 1984). The most widely used commercial
intensive housing system allow the piglets just contact with the mother, and that only for a limited
period of 3–5 weeks and in a restricted way, since the sow herself is confined to a small crate.
A more nature-like alternative is a system that has been designed and tested by the teams of Ed
Pajor and Dan Weary in Canada. In its full version, it is ‘‘sow-controlled’’, i.e., it allows the sow
to leave the piglets over a roller barrier (that the piglets cannot cross) into a space where she can
socialize with other sows; and it also allows several litters of piglets to mingle a common area. In
production terms, this alternative housing brings results comparable to the confinement systems
(Weary et al., 2002), and yet it provides welfare advantages for both the sows and the piglets.
First, the sows can regulate the amount time of time that they want to spend away from piglets and
thus reduce the demand by the litter for a too-frequent nursing. Second, they can interact socially
with each other and since the majority of interactions in stable groups of sows are positive, this is
beneficial for their welfare. Third, although the piglets tend to grow a bit slower during the
suckling period in this housing than in the restrictive one, this is fully compensated through their
substantially better growth during the period after weaning, especially during the very first postweaning days. Because for piglets the weaning is a major stress associated with health and
behavioural problems (diarrhoea, fighting and belly-nosing), the obviously better coping of litters
from the alternative housing system enhances their welfare substantially. Other systems for
farrowing and lactating sows that are based on the performance of natural behaviour have been
developed and successfully put in practice in Scandinavia and in the United States (Lidfors et al.,
2005).
9.2. Driving pigs in slaughterhouses
Allowing animals to behave in a natural way can be effective and welfare-promoting also in
more specific, down-to-earth situations. For instance, farm animals such as pigs need often to be
brought somewhere on foot. There are two extreme options available: either to drive them by
brute force, or to incite them to walk there by themselves. This problem is very acute on pig
slaughterplants. Pigs must be moved fast and in a constant pace in order to achieve good
economic results. Forcing the movement through shouting, hitting and electric proding of
individual pigs in narrow aisles that guide the movement is possible. However, it needs a high
input of very unpleasant labour, and the pigs are extremely stressed through this procedure. The
alternative option is to use the natural tendency of groups of pigs to move gradually into an open
space. Using slowly moving barriers that open new space in front of the animals and gradually
close the space behind, groups of pigs can be moved much more peacefully towards the stunning
point. If this system is connected with a well-functioning group stunning procedure using carbon
dioxide, the pre-slaughter stress of pigs can be decreased.
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10. Conclusion
Farm animals do not need ‘‘natural behaviour’’ per se for good welfare. However, providing
the opportunity for natural behaviour is often a very effective way to satisfy the needs and/or
goals of the animals, to provide them with emotionally positive experience, and to stimulate their
behavioural development in such a way that it brings long-term benefits. Therefore, natural
behaviour of the species in question should be considered both when new housing systems are
being developed (Lidfors et al., 2005) but also when solutions to particular problems in existing
systems are being sought.
Acknowledgements
The preparation of this paper was supported by the grant IAA6307402 from the Grant Agency
of the Czech Academy of Science and the grant MZE 0002701402 from the Czech Ministry of
Agriculture. I am most grateful to the CIWF Fund for inviting me to write the paper. Bo Algers
provided me with the information on alternative way of driving pigs in slaughterhouses.
References
Andersen, I.L., Naevdal, E., Bakken, M., Boe, K.E., 2004. Aggression and group size in domesticated pigs, Sus scrofa:
‘‘when the winner takes it all and the loser is standing small’’. Anim. Behav. 68, 965–975.
Appleby, M.C., Duncan, I.J.H., 1989. Development of perching in hens. Biol. Behav. 14, 157–168.
Arey, D.S., 1997. Behavioral observations of peri-parturient sows and the development of alternative farrowing
accommodation—a review. Anim. Welf. 6, 217–229.
Baxter, M.R., 1983. Ethology in environmental-design for animal production. Appl. Anim. Ethol. 9, 207–220.
Bekoff, M., 1977. Social communication in canids: evidence for the evolution of a stereotyped mammalian display.
Science 197, 1097–1099.
Burne, T.H.J., Murfitt, P.J.E., Gilbert, C.L., 2001a. Influence of environmental temperature on pgf(2 alpha)-induced nest
building in female pigs. Appl. Anim. Behav. Sci. 71, 293–304.
Burne, T.H.J., Murfitt, P.J.E., Johnston, A.N.B., 2001b. Pgf(2 Alpha)-induced nest building and choice behaviour in
female domestic pigs. Appl. Anim. Behav. Sci. 73, 267–279.
Damm, B.I., Bildsoe, M., Gilbert, C., Ladewig, J., Vestergaard, K.S., 2002. the effects of confinement on periparturient
behaviour and circulating prolactin, prostaglandin f-2 alpha and oxytocin in gilts with access to a variety of nest
materials. Appl. Anim. Behav. Sci. 76, 135–156.
Damm, B.I., Lisborg, L., Vestergaard, K.S., Vanicek, J., 2003a. Nest-building, behavioural disturbances and heart rate in
farrowing sows kept in crates and Schmid pens. Livest. Prod. Sci. 80, 175–187.
Damm, B.I., Pedersen, L.J., Marchant-Forde, J.N., Gilbert, C.L., 2003b. Does feed-back from a nest affect periparturient
behaviour, heart rate and circulatory cortisol and oxytocin in gilts? Appl. Anim. Behav. Sci. 83, 55–76.
Damm, B.I., Vestergaard, K.S., Schroder-Petersen, D.L., Ladewig, J., 2000. The effects of branches on prepartum nest
building in gilts with access to straw. Appl. Anim. Behav. Sci. 69, 113–124.
de Passillé, A.M.B., Rushen, J., 1989. Suckling and teat disputes by neonatal piglets. Appl. Anim. Behav. Sci. 22, 23–38.
Desiré, L., Boissy, A., Veissier, I., 2002. Emotions in farm animals: a new approach to animal welfare in applied ethology.
Behav. Process. 60, 165–180.
Duncan, I.J.H., 1996. Animal welfare defined in terms of feelings. Acta Agric. Scand. Sect. A-Anim. Sci. 29–35.
Duncan, I.J.H., 2005. Behavioral needs, stereotypies and animal welfare. SCAW Newslett. 27, 9–14.
Flower, F.C., Weary, D.M., 2001. Effects of early separation on the dairy cow and calf. 2. Separation at 1 day and 2 weeks
after birth. Appl. Anim. Behav. Sci. 70, 275–284.
Fraser, D., Duncan, I.J.H., 1998. ‘‘Pleasures’’, ‘‘pains’’ and animal welfare: toward a natural history of affect. Anim. Welf.
7, 383–396.
Fraser, D., Thompson, B.K., 1991. Armed sibling rivalry among suckling piglets. Behav. Ecol. Sociobiol. 29, 9–15.
Graves, H.B., 1984. Behavior and ecology of wild and feral swine (Sus scrofa). J. Anim. Sci. 58, 482–492.
M. Špinka / Applied Animal Behaviour Science 100 (2006) 117–128
127
Haley, D.B., Bailey, D.W., Stookey, J., 2005. The effects of weaning beef calves in two stages on their behaviour and
growth rate. J. Anim. Sci. 83, 2205–2214.
Hughes, B.O., Duncan, I.J.H., 1988. The notion of ethological ‘need’, models of motivation and animal welfare. Anim.
Behav. 36, 1696–1707.
Hughes, B.O., Duncan, I.J.H., Brown, M.F., 1989. The performance of nest building by domestic hens: is it more
important than the construction of a nest? Anim. Behav. 37, 210–214.
Illmann, G., Pokorná, Z., Špinka, M., 2005. Nursing synchronization and milk ejection failure as maternal strategies to
reduce allosuckling in pair-housed sows (Sus scrofa domestica). Ethology 111, 652–668.
Jensen, P., 1989. Nest site choice and nest building of free-ranging domestic pigs due to farrow. Appl. Anim. Behav. Sci.
22, 13–21.
Jensen, P., 1993. Nest building in domestic sows—the role of external stimuli. Anim. Behav. 45, 351–358.
Jensen, P., Recén, B., 1989. When to wean—observations from free-ranging domestic pigs. Appl. Anim. Behav. Sci. 23,
49–60.
Jensen, P., Toates, F.M., 1993. Who needs’ behavioural needs’—motivational aspects of the needs of animals. Appl.
Anim. Behav. Sci. 37, 161–181.
Knierim, U., Gocke, A., 2003. Effect of catching broilers by hand or machine on rates of injuries and dead-on-arrivals.
Anim. Welf. 12, 63–73.
Kurz, J.C., Marchington, R.L., 1972. Radiotelemetry studies of feral hogs in South Carolina. J. Wildl. Manage. 36, 1240–
1248.
Lawrence, A.B., Appleby, M.C., MacLeod, H.A., 1988. Measuring hunger in the pig using operant conditioning: the effect
of food restriction. Anim. Prod. 47, 131–138.
Lawrence, A.B., Terlouw, E.M.C., 1993. A review of behavioral factors involved in the development and continued
performance of stereotypic behaviors in pigs. J. Anim. Sci. 71, 2815–2825.
Lidfors, L., Berg, C., Algers, B., 2005. Integration of natural behavior in housing systems. Ambio 34, 325–330.
Lidfors, L.M., 1996. Behavioural effects of separating the dairy calf immediately or 4 days post-partum. Appl. Anim.
Behav. Sci. 49, 269–283.
Maletı́nská, J., Špinka, M., 2001. Cross-suckling and nursing synchronisation in group housed lactating sows. Appl.
Anim. Behav. Sci. 75, 17–32.
Mason, G.J., Cooper, J., Clarebrough, C., 2001. Frustrations of fur-farmed mink. Nature 410, 35–36.
Mauget, R., 1981. Behavioural and reproductive strategies in wild forms of Sus scrofa (European wild boar and feral pigs).
In: Sybesma, W. (Ed.), The Welfare of Pigs. Martinus Nijhoff, The Hague, pp. 3–13.
Mayer, J.J., Martin, F.D., Brisbin, I.L., 2002. Characteristics of wild pig farrowing nests and beds in the upper coastal plain
of South Carolina. Appl. Anim. Behav. Sci. 78, 1–17.
Mills, A.D., Faure, J.M., 1990. Panic and hysteria in domestic fowl: a review. In: Zayan, R., Dantzer, R. (Eds.), Social
Stress in Domestic Animals. Kluwer Academic Press, Dordrecht, pp. 248–272.
Newberry, R.C., Wood-Gush, G.M., 1985. The suckling behaviour of domestic pigs in a semi-natural environment.
Behaviour 95, 11–25.
Pajor, E.A., Weary, D.M., Caceres, C., Fraser, D., Kramer, D.L., 2002. Alternative housing for sows and litters. Part 3.
Effects of piglet diet quality and sow-controlled housing on performance and behaviour. Appl. Anim. Behav. Sci. 76,
267–277.
Reinhardt, C., Reinhardt, A., Reinhardt, V., 1986. Social behaviors and reproductive performance in semi-wild Scottish
Highland cattle. Appl. Anim. Behav. Sci. 15, 125–136.
Reinhardt, V., Reinhardt, A., 1981. Natural sucking performance and age of weaning in zebu cattle (Bos indicus). J. Agric.
Sci. 96, 309–312.
Rushen, J., Pajor, E., 1987. Offence and defence in fights between young pigs (Sus scrofa). Aggress. Behav. 13, 329–346.
Špinka, M., Illmann, G., 1991. Development of group-housed dairy calves behaviour and the effect of separation of the
mother 5 days post partum. In: Abstracts of the 25th International Congress of the Society of Veterinary Ethology,
Edinburgh, July 3–6, p. 93.
Špinka, M., Illmann, G., 1992. Suckling behaviour of young dairy calves with their own and alien mothers. Appl. Anim.
Behav. Sci. 33, 165–173.
Špinka, M., Newberry, R.C., Bekoff, M., 2001. Mammalian play: training for the unexpected. Q. Rev. Biol. 76, 1–28.
Stěhulová, I., Lidfors, L., Špinka, M., 2004. Response of dairy calves to the early separation from their mothers: effect of
calves’ age and visual/auditory contact. In: Hänninen, L., Valros, A. (Eds.), Proceedings of the 38th International
Congress of the ISAE, Helsinki, Finland, ISAE, p. 157.
Thodberg, K., Jensen, K.H., Herskin, M.S., 2002. Nest building and farrowing in sows: relation to the reaction pattern
during stress farrowing environment and experience. Appl. Anim. Behav. Sci. 77, 21–42.
128
M. Špinka / Applied Animal Behaviour Science 100 (2006) 117–128
Thomas, T.J., Weary, D.M., Appleby, M.C., 2001. Newborn and 5-week-old calves vocalize in response to milk
deprivation. Appl. Anim. Behav. Sci. 74, 165–173.
Turner, S.P., Edwards, S.A., 2004. Housing immature domestic pigs in large social groups: implications for social
organisation in a hierarchical society. Appl. Anim. Behav. Sci. 87, 239–253.
Veissier, I., Lamy, D., Le Neindre, P., 1990. Social behaviour in domestic beef cattle when yearling calves are left with the
cows for the next calving. Appl. Anim. Behav. Sci. 27, 193–200.
Weary, D.M., Pajor, E.A., Bonenfant, M., Fraser, D., Kramer, D.L., 2002. Alternative housing for sows and litters. Part 4.
Effects of sow-controlled housing combined with a communal piglet area on pre- and post-weaning behaviour and
performance. Appl. Anim. Behav. Sci. 76, 279–290.
Webster, J., 1994. Animal Welfare. A Cool Eye Towards Eden. Blackwell Science, Oxford.
Wechsler, B., Bachmann, I., 1998. A sequential analysis of eliminative behaviour in domestic pigs. Appl. Anim. Behav.
Sci. 56, 29–36.
Whittaker, X., Spoolder, H.A.M., Edwards, S.A., Lawrence, A.B., Corning, S., 1998. The influence of dietary fibre and the
provision of straw on the development of stereotypic behaviour in food restricted pregnant sows. Appl. Anim. Behav.
Sci. 61, 89–102.
Widowski, T.M., Duncan, I.J.H., 2000. Working for a dustbath: are hens increasing pleasure rather than reducing
suffering. Appl. Anim. Behav. Sci. 68, 39–53.
Wood-Gush, D.G.M., Vestergaard, K., 1991. The seeking of novelty and its relation to play. Anim. Behav. 42, 599–606.
Worobec, E.K., Duncan, I.J.H., Widowski, T.M., 1999. The effects of weaning at 7, 14 and 28 days on piglet behaviour.
Appl. Anim. Behav. Sci. 62, 173–182.
Yin, S., McCowan, B., 2004. Barking in domestic dogs: context specificity and individual identification. Anim. Behav. 68,
343–355.