Volume 164, March 2015, Pages 12–28
Filial attachment in sheep: Similarities and differences between ewe-lamb and human-lamb relationships ☆
Highlights
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- Lambs do search specifically the proximity of their mother or human caregiver.
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- Attachment to humans develop more easily in lambs reared without mothers.
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- Lambs show emotional responses in the presence or the absence of their partner.
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- Infant attachment relies on positive interactions that includes feeding and touch.
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- Attachment develops more rapidly if positive interactions take place soon after birth.
Abstract
Animals
develop relationships with intra- and interspecific partners, including
humans. In some cases this can lead to strong emotional bonds
indicating the existence of attachment. The sheep is well known to
develop various forms of social attachment (mothers towards young, lambs
towards siblings). The relationship they can develop with humans is
much less understood. In this review, based on the attachment theory
framework developed in human infants, we outline features and mechanisms
that participate in the development and the expression of affiliative
behaviours that lambs can develop with their mother or a human.
Behavioural tests comparing responses towards a presumed attachment
figure with those directed towards unfamiliar or familiar conspecifics
demonstrate that lambs do search specifically the proximity of their
mother or human caregiver. Differential emotional responses in the
presence (calmness) or the absence of the partner (agitation) are also
expressed. However, a relationship with a human takes place more easily
when lambs are reared without their primary attachment figure, the
mother. Human-lamb attachment is then facilitated by positive social
contacts (gentling, hand-feeding) provided by a specific caregiver. In
the case of attachment with the mother, suckling is the main reward.
Although the existence of a sensitive period is still unclear, in both
cases attachment develops more rapidly if positive interactions take
place immediately after birth. Three neurochemical systems have profound
impact on the expression of filial attachment in sheep: the gut peptide
cholecystokinin, endogenous opioids, and oxytocin, all known to play a
key role in prosocial behaviours in mammals. In addition, positive
nutritive or non-nutritive interactions activate specific brain regions
that are involved in the expression of social and emotional behaviours.
In conclusion, lambs do develop intra- and interspecific attachment but
not in a concomitant manner as the presence of the mother strongly
reduces their motivation to interact with a human. Nonetheless, under
artificial rearing conditions the human becomes a salient attachment
figure.
Keywords
- Attachment;
- Affiliation;
- Lamb;
- Mother;
- Human;
- Suckling;
- Gentling;
- Stroking;
- Distress;
- Comfort;
- Sensitive period;
- Oxytocin;
- Emotion;
- Cognition
1. Introduction
Social
behaviour is believed to exist because it is beneficial to those who
engage in it, which means that these individuals are better off than
they would be on their own. In mammals, social behaviour serves many
purposes and is exhibited in a wide variety of forms (Alcock, 2009).
Even the so-called solitary species, which as adults interact socially
only to mate, have a close behavioural interaction with their mothers
when they are young (Eisenberg, 1983).
Many mammals are more successful at finding food when they search as a
group; this is especially true if food resources are clumped together in
only certain places. Ungulates clearly gain protection from predators
by living in social groups, since nearly all of them are vulnerable, at
least when young (Veissier et al., 1998).
Sociality thus provides several modes of defence not available to
solitary individuals and members of a social group are probably better
able to detect predators by depending on mutual vigilance.
The
stability of the group relies on individual recognition that may even
lead to some kind of affiliation between related or unrelated
individuals (Rault, 2012).
In some cases a strong bonding process may take place between two or
more individuals. Social bonds are a subset of affiliative or positive
behaviours, which are most simply characterised by approach rather than
avoidance or withdrawal. The best described examples of social bonds
include parent-offspring relationships in ruminants and primates (Broad et al., 2006, Maestripieri, 2001, Nowak et al., 2011a and Poindron et al., 2007) and adult heterosexual relationships in monogamous species (Wang and Aragona, 2004 and Young and Wang, 2004).
Such social bonds are associated with reproduction and social stability
and are most readily interpreted in the context of their evolutionary
and adaptive functions (Gubernick, 1981).
Mammals
do not interact exclusively in an intra-specific context and a great
complexity in relationships between various populations is found in
nature. Those existing between members of different species are termed
interspecific relationships and some may be beneficial (mutualism: Boucher and Douglas, 1985 and Farine et al., 2012). Interspecific relationships are rather common in mammals (Stensland et al., 2003).
They fall into two main categories: spontaneous and usually temporary
associations, or induced and often long-lasting ones. The first category
is seen in wild species, one of the most famous examples being found in
species sharing the African savannah. An obvious advantage is a more
efficient anti-predator strategy since some species may benefit from
early detection of predators by identifying alert signals emitted by
other species (Fichtel, 2004, Kitchen et al., 2010 and Magrath et al., 2009). In parallel, predators can also form temporary interspecific hunting association and this increases their hunting success (Minta et al., 1992).
In the second category, induced and long-lasting interspecific
relationships are usually found amongst domesticated and farmed animals.
By mixing species varying in fear behaviour, some may benefit from the
protection of others that can be aggressive towards predators. Such
characteristic has been used to protect vulnerable small ruminants by
inducing mixed bonds between herds of cattle and flocks of sheep in
order to reduce attacks on the latter by coyotes in North America (Anderson et al., 1992 and Hulet et al., 1987), or by raising dogs with sheep to guard them against wolves in Europe (Rigg, 2001).
In the web of induced interspecific relationships, the most common and
probably best known association is the one that involves animals and
humans: it can be intense, vital and lifelong in some species (pets) or
casual and temporary in others (farm species). Yet, our scientific
knowledge of the mechanisms leading to the establishment and maintenance
of these diverse interspecific relationships, and their nature, is far
more limited than in the case of intraspecific relationships. Surprising
this is even true for the case of the animal-human relationship.
Although
animals are widely employed in human societies, it is only recently
that the scientific community have acknowledged the relationship that
frequently, perhaps inevitably, develops between “them” and “us”.
Indeed, an increasing body of evidence suggests that it results in
profound behavioural and physiological changes in the animal subject in
both laboratory and field settings (Hemsworth and Boivin, 2011, Konok et al., 2011 and Odendaal and Meintjes, 2003; Scott, 1992; Waiblinger et al., 2006 and Waiblinger, 2009).
Such effects are not confined to obvious cases involving primates and
dogs, but appear in less expected species like farm animals. The
relationship between humans and farm animals has been shown to have
strong impacts on their welfare, ease of handling, and productivity.
Farm animals that receive additional gentle human contact are less
fearful of humans than those that receive minimal contact (Hemsworth and Boivin, 2011, Waiblinger et al., 2006 and Waiblinger, 2009).
They are also less agitated during loading and transport, during
veterinary procedures, and spend more time near their stockperson. Thus,
the affinity for the stockperson appears as a good indicator of
positive animal-human relationships. While our understanding of the
human aspects that influence these interactions in livestock production
has improved considerably over the last decade or so, we still know very
little about the way humans are perceived by animals or included in
their social network.
Can
they bond to us in the same way they bond to each other? We attempt to
answer this question in the present review by taking the sheep as a
model. Under farming conditions sheep interact both with conspecifics
and humans, interactions with humans being more frequent under intensive
livestock production systems or in more traditional pastoral
shepherding. Amongst farm animals, it is the subject that has been
studied the most extensively in the field of affiliative behaviours both
for interspecific and intraspecific relations, especially at a young
age when individuals develop strong bonds (Nowak, 2006, Nowak and Boivin, 2002 and Nowak et al., 2011a). As the mechanisms of attachment to the mother have been well described from a behavioural and physiological point of view (Nowak et al., 2007),
it will be used as a base to investigate whether the interactions that
lambs have with humans may fall into the category of attachment
behaviours. In a first step, we summarize the general attributes of the
concept of attachment and the criteria used to measure it that have been
developed from research on humans and extrapolated to sheep. Then, we
illustrate this point by drawing together the behavioural, physiological
and neurobiological mechanisms involved in the development and/or the
expression of intra- and inter-specific bonding in the lamb. Finally,
this paper also considers some of the main weaknesses in our
understanding of the two processes in an effort to assist in directing
future research.
2. Attachment theory
The theoretical background of our work is John Bowlby's theory of attachment (Bowlby, 1958 and Bowlby, 1969) to which Mary Ainsworth's finding has contributed (Ainsworth, 1979 and Ainsworth and Bell, 1970).
Within this theory, attachment is seen as an affectional bond between
an individual (the infant) and a specific figure, usually an adult
caregiver, binding them together in space and enduring over time. Such
bonds are not present at birth but develop during the first year of
life. Early sensory recognition of the mother, which has been well
documented even in neonates (Porter, 1991),
does not necessarily reflect attachment to the mother. In the first 6
months, the infant's behaviour is generally indiscriminant towards
adults even though the primary figures receive more enthusiastic
responses (Bowlby, 1969)
The true attachment phase is seen between 8 months and 2 years when
infants become more discriminating and protest when separated from
particular people.
Between a
child and a caregiver these bonds are based on the child's need for
safety, security and protection. It is an emotional tie to a special
person (the primary attachment figure) characterised by a tendency to
seek and maintain contact especially during periods of stress. The
attachment theory proposes that children attach to caregivers
“instinctively”, the biological aim being survival and the psychological
aim, security. Infants form attachments to any caregiver who is
socially sensitive and responsive with them. This means that the quality
of the social engagement is more influential than the amount of time
spent (Ainsworth, 1979).
Although the biological mother is usually the principal attachment
figure, the role can be taken by anyone who consistently behaves in a
caregiving way over a period of time. In attachment theory this means a
set of behaviours that involves engaging in lively social interaction
with the infant and responding readily to signals and approaches.
Fathers or any other individuals are equally likely to become attachment
figures if they provide most of the child care and related social
interaction. However, these figures are arranged hierarchically, with
the principal attachment figure at the top. If the figure is unavailable
or unresponsive, in particular in a novel environment, separation
distress occurs. This is what Ainsworth and Bell (1970)
clearly showed in the “strange situation” paradigm where physical
separation from the mother causes immediate agitation, crying and
despair. Infants cannot be calmed down by people other than the
attachment figure.
If
infants perceive their attachment figure as a source of security and
support, they are more likely in his/her presence to develop confidence
towards new items or other individuals and expect positive consequences
from them. This important aspect of the attachment theory has been
conceptualised as the development of an “internal working model” shaping
the infant's ability to adapt to the present but also the future
relational world (Cassidy, 2008).
This process is based simultaneously on the care-seeking drive from the
infant and the caregiver's sensitivity to respond. Fearful or stressful
events can contribute to reinforce the relationship if the two partners
react correctly to each other in a contiguous manner. Conversely,
children from abusive relationships with their caregiver will generalise
negative expectations into other relationships. In the absence of
appropriate responses from the attachment figure (e.g. depressive
mother), the care-seeking individual is likely to develop an ambivalent,
avoidant, or disorganized attachment relationship.
