1 s2.0 S0168159116302088 Main

You might also like

Download as pdf or txt
Download as pdf or txt
You are on page 1of 9

Applied Animal Behaviour Science 183 (2016) 1–9

Contents lists available at ScienceDirect

Applied Animal Behaviour Science


journal homepage: www.elsevier.com/locate/applanim

Measuring dog-owner relationships: Crossing boundaries between


animal behaviour and human psychology
Therese Rehn ∗ , Linda J. Keeling
Swedish University of Agricultural Sciences, Department of Animal Environment and Health, P.O. Box 7068, SE-750 07 Uppsala, Sweden

a r t i c l e i n f o a b s t r a c t

Article history: Previous research suggests that dogs (Canis familiaris) form attachment bonds to their owners and that
Received 4 February 2016 the strengths of the attachment can vary. However, it does not seem reasonable to believe that all dogs
Received in revised form 8 July 2016 share the same attachment style, considering their differences in genetic background, their previous
Accepted 19 July 2016
experiences and the many different caregiving strategies that are known to exist among humans. Rather,
Available online 28 July 2016
the level of security felt by dogs towards their owner probably varies, as seen in children towards their
parent. The aim of this review is to highlight the strengths and weaknesses of current approaches of
Keywords:
investigating the dog-human relationship in order to contribute to this rapidly developing field. The main
Attachment
Reunion focus is related to trying to increase our understanding about the dog’s experience of the relationship.
Strange situation procedure Current knowledge about the dog-human relationship is reviewed and discussed. Concepts from human
Animal welfare psychology are used to clarify some of the terms that are also used in anthrozoology, thereby giving
Caregiving stronger theoretical support to our suggestions of how to adapt and apply methods to further develop
Human-animal interaction assessments of dog-owner relationships. We highlight potential factors that deserve more attention in
future studies to improve our understanding of the dog-human relationship, and we suggest a more
coordinated approach, with a unified terminology, to develop an overarching framework. Suggestions
for the future to achieve this include focusing on attachment styles at the individual dog level, rather than
talking about the ‘average’ dog. Furthermore, a dyadic approach is suggested, where both the attributes of
the dog (its attachment style) and the owner (its caregiving strategy) are incorporated when assessing the
relationship. One way to do this is to focus on the balance between the dog’s separation distress and how
effective the owner’s caregiving strategy is in calming the dog when reunited. The consequence, from an
applied point of view, is owners becoming more aware of what type of attachment style their dog has
and what caregiving strategy they have. Knowing this may contribute to identifying sources of conflict in
past or present relationships, so helping owners form more successful and positive relationships in the
future. It may also contribute to better matching when rehoming shelter dogs.
© 2016 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Relationships, affectional bonds and attachment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .2
2.1. Attachment and caregiving . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.2. Attachment styles and caregiving strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3. Methods to study the dog-human relationship: what have we learnt? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.1. Owner questionnaires . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.2. Behavioural assessments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.3. Combined questionnaire and behavioural studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.4. Physiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

∗ Corresponding author.
E-mail address: Therese.Rehn@slu.se (T. Rehn).

http://dx.doi.org/10.1016/j.applanim.2016.07.003
0168-1591/© 2016 Elsevier B.V. All rights reserved.
2 T. Rehn, L.J. Keeling / Applied Animal Behaviour Science 183 (2016) 1–9

4. Towards measuring different relationship styles in dog-human dyads . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5


4.1. Changing the focus in attachment evaluations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4.2. Reunion situations per se . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.3. Measures of the owner . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.4. Factors that may affect attachment development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

1. Introduction identified. Furthermore, we give suggestions for which factors may


contribute to the development of different attachment styles in
Many people report that they are as emotionally involved with dogs, hence deserving more attention in future studies of the dog-
their dog (Canis familiaris) as they are with their family or friends human relationship. We will 1) describe the terms associated with
(Archer, 1997; Barker and Barker, 1988; Voith, 1985) and the dog- relationship quality, as defined in the human literature, 2) survey
owner relationship has been suggested to resemble that between the available anthrozoology literature to compare and evaluate cur-
a child and its parents (Topál et al., 1998; Serpell, 2004). Experi- rent experimental methods to measure the relationship between
ences from relationships, especially early in life, are important for dogs and humans. Lastly, we will 3) propose where the focus should
an animal’s social development and its ability to cope with its sur- lie in future assessments of dog-owner relationships.
roundings (e.g. Foyer et al., 2014; Gazzano et al., 2008a; Sachser
et al., 2013 for a review). 2. Relationships, affectional bonds and attachment
A relationship, that is to say the bond the owner has to the dog
and vice versa, is a multi-faceted and complex phenomenon. This A relationship is generally referred to as an association between
review aims to combine relevant factors related to bonding, both two individuals over time (Hinde, 1976a). Even long-term, ‘stable’
from the dog’s perspective as well as the owner’s. relationships are dynamic in the sense that they are constantly
In the past, efforts have been made to answer whether or not affected by the regular interactions that occur between the involved
the bonds dogs have to human caretakers constitute an attach- individuals (Hinde, 1976b). In other words, and perhaps not very
ment or not. Research has shown that dogs do express attachment surprisingly, the quality of a relationship is highly dependent on the
behaviour towards their owners, as tested in the Strange Situ- direct effects of day-to-day interactions as well as on the indirect
ation Procedure (SSP) (e.g. Mariti et al., 2013; Palestrini et al., effects of external factors contributing to the individual’s physio-
2005; Palmer and Custance, 2008). However, in current anthrozo- logical or psychological state.
ology literature, the difference between attachment behaviour and Relationships may result from or lead to an affectional bond,
attachment bond seems unclear. While the former can be expressed defined as “a relatively long-lasting tie in which the partner is
to many people or objects and in a variety of contexts, the latter is important as a unique individual and is interchangeable with none
a developed strategy directed only to a few individuals (Bowlby, other” (Ainsworth, 1989). Unfortunately, the term ‘bond’ is some-
1958). One section of this review compares the similarities and dif- times equated with a ‘relationship’ within anthrozoology literature.
ferences in how terms from human psychology are used in anthro- In contrast to a relationship, which is dyadic, a bond refers to the
zoology. For example, we question the use of the terms ‘stronger’ characteristic of an individual, i.e. it describes one individual’s bond
or ‘weaker’ when referring to an attachment (e.g. Marinelli et al., to another individual (Ainsworth, 1989). This way, it is possible to
2007; Mariti et al., 2013; Rehn et al., 2014a). These are rarely (if claim that an owner is affectionately bonded to his/her dog, with-
ever) used in human psychology, where the focus is on the style of out having to account for whether or not the dog is bonded to the
the attachment, not the strength of it. Moreover, so far the majority owner.
of studies have summarised data from individual dogs and focused
on responses at the group level, to for example, provide evidence of
2.1. Attachment and caregiving
an existing attachment bond or to compare responses between dif-
ferent types of dogs, rather than taking into consideration variation
Attachment is defined as an affectional bond with the added
at the individual level. This averaging across dogs may mask dif-
experience of security and comfort obtained from the relation-
ferent strategies between different dog-owner dyads.Worthwhile
ship (Ainsworth, 1989). It is applied to many long-lasting bonds in
underlining here is the exception in the initial work of Topál et al.
humans, such as those experienced by an infant to its mother, that
(1998), who categorised dogs into different ‘types’ based on their
of a person to his/her romantic partner or to close friends (Crowell
behaviour in the SSP, i.e. the anxiety, acceptance and attachment
et al., 2008; Hazan and Shaver, 1987). Attachment has also been
factors (see also e.g. Fallani et al., 2006; Marinelli et al., 2007). In
applied to dog-human relationships, although sometimes without
human psychology literature, three organised attachment styles
accurate consideration of the specific criteria that must be met for
are well defined in infants. These are all functional in that they
it to be labeled an attachment (see Kobak, 2009). Bowlby (1969)
act to successfully regulate emotions in situations with the attach-
developed attachment theory based on fundamental principles in
ment figure (e.g. the parent). The development of these different
ethology, evolutionary biology and cognitive science. He formu-
strategies is mainly influenced by the caregiving behaviour of the
lated the operational criteria of attachment to include the concepts
attachment figure. Hence, we propose a dyadic approach when
proximity maintenance, safe haven and secure base.
investigating the relationship between dogs and their owners, tak-
While the background to the attachment system is well accepted
ing into consideration attributes of both the dog and the owner.
as it deals with the individual’s own survival chances, the back-
In this review, we propose that the next step in anthrozoology
ground to caregiving behaviour seems to be somewhat more
research is to use all the potential information within attachment
debated (Bell and Richard, 2000). The evolutionary background to
theory, to reveal whether or not different types of relationship styles
caregiving behaviour is related to the benefits of parental invest-
exist among different dog-owner dyads and how they might be
ment (e.g. Trivers, 1972), and it is motivated by activation of neural
T. Rehn, L.J. Keeling / Applied Animal Behaviour Science 183 (2016) 1–9 3

subcortical circuits in the brain during affiliative social interac- of adult attachment; secure-autonomous, dismissing, preoccupied
tion (Panksepp et al., 1994). These circuits are referred to as the and unresolved/disorganised (Table 1). If a person’s adult attach-
nurturant ‘care circuits’ and involve the release of oxytocin, pro- ment style or general caregiving behaviour is reflecting how that
lactin, vasopressin and endogenous opioids such as endorphins person is taking care of or interacting with their dog is yet to be
(Panksepp, 1998), which makes the experience of caregiving in studied, but it is tempting to assume this may be the case.
itself rewarding. This way, the caregiver bonds to the child, driven
by a behavioural system which promotes care and protection of 3. Methods to study the dog-human relationship: what
offspring. In the dog-owner relationship, the owner is taking the have we learnt?
role of the caregiver and is presumably bonded to the dog, and the
dog is considered the attached individual. The increasing amount of work on the dog-human relationship
in recent anthrozoology literature reflects that dogs are taking a
2.2. Attachment styles and caregiving strategies more important role in Western modern society. Below this work
is summarised and discussed, focusing on the methodology used.
In contrast to anthrozoology, terms such as ‘higher’ or ‘stronger’
attachment are rarely used in human psychology. Instead, attach- 3.1. Owner questionnaires
ment is described as a behavioural strategy used by a child to
maximise its survival chances. Ainsworth et al. (1978) defined three Most research on dog-human relationships has been carried out
different styles of attachment among children; secure, avoidant and using questionnaires in order to assess the owner’s way of interact-
ambivalent attachment. Some years later, the disorganised attach- ing with the dog or his/her feelings about the dog (e.g. Dwyer et al.,
ment style was described (Main and Solomon, 1986) (Table 1). 2006; Johnson et al., 1992; Shore et al., 2006; Templer et al., 1981).
These different styles describe the relational expectations, emo- Authors have investigated the effects of owner characteristics, such
tions and behaviours that result from a particular history of as their behaviour, attitudes or personality on the incidence of dog
interactions with attachment figures (Bowlby, 1958; Hazan and behavioural problems, but findings are still somewhat inconclu-
Shaver, 1987). Most probably all but the disorganised attachment sive. For example, while Jagoe and Serpell (1996) and Kobelt et al.
style are adaptive from an evolutionary perspective since they are (2003) found that the higher the level of previous dog experience
developed by the child as a functional strategy to fit the parent’s the owner had, the lower the risk of the dog developing owner-
behaviour (Main, 1990). This is why a child can show a different directed aggression and fear related behaviour problems, Line and
attachment style to the mother and to the father. Attachment styles Voith (1986) found no such correlations. Furthermore, Voith et al.
are therefore partly genetically determined and partly learnt by the (1992) did not find any effects on the level of behaviour problems
child and presumably dogs can also learn to adapt their style of expressed by the dog and owner ‘spoiling’ behaviour (e.g. letting the
attachment to the behaviour of their caregiver, i.e. their owner. dog sleep in the owner’s bed), but Jagoe and Serpell (1996) found
The Ainsworth’s Strange Situation Procedure (ASSP) was devel- that dogs who were allowed to sleep in the owner’s bed did show
oped to categorise the attachment style of infants less than two more aggression and separation anxiety.
years of age (Ainsworth and Bell, 1970). The test aims to activate Well-designed questionnaires can give valuable information
the attachment behavioural system by putting the attached indi- from a large sample size over a wide geographic area at a low cost.
vidual in a stressful situation. By looking at the balance between However, questionnaires are subjective as they are based on the
two motivational systems, protection from threat (seek protection human respondent’s perception of the situation, rather than solid
and comfort from the attachment figure) and the urge to explore observational data. Another possible problem with questionnaires
the surroundings (ability to move away from the attachment figure is that respondents may represent a biased group of dog owners,
once comfort is gained), different attachment styles are described based on the simple fact that they agree to participate.
(Bowlby, 1969). An individual who fails to receive unconditioned
support and care from its attachment figure develops alternative 3.2. Behavioural assessments
ways to cope with the situation. This may be observed, for exam-
ple, as an absence of distress at separation and avoidance of the As mentioned above, the ASSP was first adapted by Topál et al.
attachment figure upon reunion, as in the insecure avoidant attach- (1998) to explore the dog-human relationship hypothesizing a
ment style (Table 1). This strategy is mainly driven by attempts similarity with the child-parent relationship. A large number of
to minimise the activation of the attachment system (Main and studies, using the SSP with dogs, have been performed since then.
Solomon, 1986). Modified versions of the ASSP, usually referred to Due to slight differences in the methodology of data collection
as the Strange Situation Procedure (SSP) or the Strange Situation and analyses, direct comparisons between these studies are not
Test (SST), have been used to explore the dog-human relationship, straightforward, but generally marked differences between the
which will be discussed in more detail in section 3. dog’s behaviour in the presence of the owner and the stranger indi-
An infant’s attachment style is specific to its caregiver, but cate that dogs discriminate between their owner and the stranger
attachment styles can be transferred to new relationships later and that they show attachment behaviour towards their owners
in life. This is often referred to as an adult attachment style and (e.g. Mariti et al., 2013; Mongillo et al., 2013; Topál et al., 1998).
describes a general state of mind with respect to overall attach- These differences in behaviour are most prominent in proximity-
ment history and is not necessarily directed towards a particular seeking and reunion behaviour (e.g. Fallani et al., 2007; Kerepesi
individual (Main, 2000). The adult attachment style is proposed et al., 2014; Prato-Previde et al., 2003; Rehn et al., 2013).
to influence a number of human social behaviours, among others An important methodological difference between human ASSP
parental care and caregiving (Main, 2000; Mikulincer and Shaver, studies and dog SSP studies is related to the sampling techniques
2007), and could thus have a significant effect on the caregiving used when coding the material. When analysing the ASSP, qualita-
strategy directed towards the dog. Depending on the measure- tive observer ratings are performed while quantitative behavioural
ment used, the terminology to categorise adult attachment styles coding is used for the SSP. Although the latter may be more stan-
may vary. In order to avoid too much confusion in this review, dardised, it may also hide features relevant to studying dynamic
we have chosen to restrict ourselves to the terminology used in aspects of attachment. Qualitative observer rating has, to our
adult attachment interviews (AAI’s) (Mikulincer and Shaver, 2007; knowledge, only recently been applied to dogs (Schöberl et al.,
Bartholomew and Shaver, 1998). The AAI includes four categories 2015).
4 T. Rehn, L.J. Keeling / Applied Animal Behaviour Science 183 (2016) 1–9

Table 1
An overview of behavioural characteristics of different attachment styles in humans.

Child Parent

Behaviour in the Ainsworth’s Behaviour in reunion studies of 6 yr-olds Response to the Adult Typical caregiving style
Strange Situation Procedure Attachment Interview

Secure Protests departure of AFa , seeks Calm and friendly Secure- Values relationships Sensitive and
proximity and is comforted greeting, including a autonomous and is objective and responsive to the
upon reunion, returning to fluent conversation coherent. child’s signals and
exploration or play activities. with AF. needs.
Greeting behaviour is active,
open and positive. Attention to
threat vs. e.g. play is flexible.
Insecure avoidant Shows little/no distress on Subtle avoidance when Dismissive Avoids discussing Little/no response to
departure, little/no visible reunited with AF (gaze negative attachment distressed child.
response to return, and body directed related events or Discourages crying,
ignors/turns away but does not away), restricted admits such events encourages
resist interaction altogether. conversation. while undermining independence.
Shifts attention away from their potential negative
AF/threat. effects on self.
Insecure Distressed during separation Exaggerated Preoccupied Confused about Inconsistent between
ambivalent/ with ambivalence, anger, expression of affection, self/others. Unclear comfort giving and
resistant reluctance towards AF upon and often inconsistent descriptions of early neglect.
reunion. May return to play in between moving away relationships.
shorter bouts. Seeks contact and seeking physical
but resists angrily when it is contact. Conversation
achieved or shows exaggerated seems focused on
proximity-seeking and clinging feelings and the
behaviour. Attention relationship as such.
only/mainly to AF.
Disorganized No clear behavioural pattern, Role-inverting and Unresolved/ Lapses in reasoning, Frightening behaviour,
may show stereotypies on controlling, dysfluent disorganised focuses conversation intrusiveness,
return (e.g. freezing or conversation. on loss or abuse. withdrawal or abusive
rocking), without approaching behaviour towards
AF. Lack of coherent strategy child.
shown by contradictory
behaviour (e.g. approaching
with the back turned). Unable
to focus attention on either AF
or the environment.
a
AF = Attachment Figure.

Studies using the SSP, suggest that dogs quite readily show alone with the device. Gácsi et al. (2013) showed that the pres-
attachment behaviour towards humans, probably due to our long ence of the owner during the approach of a threatening stranger
history together (Topál et al., 2005). Gácsi et al. (2001) showed that had ameliorative effects on heart rate (HR) compared to dogs being
dogs subjected to minimal (10 min per day for three days) addi- exposed to the stranger alone, indicating a calming effect of the
tional human handling expressed attachment behaviour towards owner which may be related to the safe haven feature of attachment
the handler during the SSP. Moreover, attachment behaviour is theory.
expressed more towards a complete stranger compared to another
dog in the household (Mariti et al., 2014). Yet the strategy of acquir- 3.3. Combined questionnaire and behavioural studies
ing comfort from the owner, i.e. the dynamic patterns between
episodes on an individual level is rarely discussed. Sometimes the Studies have examined correlations between the owner’s
focus has been on whether dogs managed in different ways (work- reported emotional closeness, their interactions with the dog and
ing vs. pet dogs) are ‘more’ or ‘less’ attached to the owner (e.g. Mariti the dog’s behaviour. The view that if a person perceives a strong
et al., 2013). While attachment behaviour can be expressed in many bond to their dog, this would be reflected in the dog’s behaviour
situations towards a variety of subjects, attachment bonds are only during the SSP was not supported by the results in Rehn et al.
developed towards a few specific individuals (Bowlby, 1958). It is (2014a). The few correlations found were linked to how the owner
knowledge about the style of attachment bond and so the strategy interacted with the dog on a daily basis, but no associations were
used to gain comfort from an attachment figure, which we believe found between the dog’s behaviour and the level of the owner’s per-
is worthy investigating in the future so taking a next step forward ceived emotional closeness to the dog. This result was in accordance
in this field. with that of Mariti et al. (2011), showing that dogs expressed the
Other approaches to study the dog-human relationship based on most intense attachment behaviour towards the family member
behavioural observations have been initiated. For example, Wedl who reported being the one who took the dog on walks.
et al. (2010) investigated the level of social attraction shown by the One might expect that the level of emotional closeness reported
dog to its owner in a novel environment. Among other things, they by an owner would be related to how much the owner actually
found that dogs belonging to owners who believed it was important interacts with the dog, but findings report the opposite. Kotrschal
to spend time with their dog, spent more time close to the owner. et al. (2009) found that the more social support the dog was per-
Horn et al. (2013) presented dogs with a manipulative task in differ- ceived as being to the owner, the less time the owner spent together
ent conditions as an alternative way to study the secure base aspect with the dog on a daily basis. Furthermore, these dog-owner
of attachment theory. Comparisons of the time engaged in trying to dyads took longer to complete a task together, which is perhaps
solve the task showed that dogs manipulated it for longer when the explained by a less synchronised interaction pattern between them.
owner was present (passive) in the room than when the dog was In the light of this, it is interesting to note that much research on
T. Rehn, L.J. Keeling / Applied Animal Behaviour Science 183 (2016) 1–9 5

the dog-human relationship relies on attitudinal or ‘attachment’ Cortisol has been used extensively to measure the effect of
questionnaires (e.g. Johnson et al., 1992; Templer et al., 1981). Find- environmental challenges in dogs (e.g. Haverbeke et al., 2008;
ings from such studies do suggest that a dog can provide social Hydbring-Sandberg et al., 2004; Steiss et al., 2007). Cortisol lev-
support for humans with limited social networks, as these owners els decrease when the owner administers calm, tactile stimulation
reported stronger affectional bonds to their dogs (Johnson et al., (Handlin et al., 2012), but even the presence of a passive human
1992). But the aspects related to how emotionally involved the has ameliorative effects on cortisol levels when dogs are exposed
owner is probably have limited influence on the dog’s perception to a stressful environment (e.g. Shiverdecker et al., 2013; Tuber
of the relationship as the two factors, emotional closeness and level et al., 1996). Basal cortisol levels in securely attached children tend
of shared activities, seem to counteract each other. to be lower than those of insecurely attached individuals (Gunnar,
Siniscalchi et al. (2013) found that an owner’s attachment profile 1998), possibly related to the greater predictability in such relation-
towards other people, which may be related to his/her caregiving ships (Creel, 2001). Recently, Schöberl et al. (2015), found that dogs
strategy, was associated with the dogs’ behaviour during the SSP. characterised as securely attached to their owners showed lower
Owners scored as ‘confident’ (resembling the secure-autonomous cortisol reactivity in the SSP compared to insecurely attached dogs.
adult attachment style, Table 1) had dogs showing a behavioural Comparable therefore to what has been found for oxytocin, attach-
response similar to that of securely attached children. Dogs belong- ment style seem to contribute to differences in cortisol levels (or
ing to ‘not-confident’ owners (resembling a mix of the dismissing, vice versa).
preoccupied and unresolved adult attachment styles, Table 1) did Attachment style in humans seems also to influence cardiac
not seem to use their owner as a secure base to the same extent activity. Sroufe and Waters (1977) found that securely attached
and there were fewer differences in their behaviour towards the infants return to baseline HR after exposure to a stressor quicker
owner and the stranger. Konok et al. (2015) showed that owners than do insecurely attached individuals. While HR reveals some-
scoring high on attachment avoidance on the Adult Attachment thing about the absolute difference in activity of the sympathetic
Scale were more likely to own a dog suffering from separation- and parasympathetic autonomic nervous system, heart rate vari-
related disorders. Hence, it seems that questionnaires or interviews ability (HRV) gives a more detailed picture of their continuous
used to determine adult attachment styles can serve as instruments interplay (e.g. Appelhans and Luecken, 2006). Because emotion reg-
to measure owner caregiving strategies and so contribute towards ulation is dependent on adjustments of physiological arousal on a
assessing dog-human relationships. momentary basis (Gross, 1998), HRV is suggested to be a more sub-
tle indicator of an individual’s mental arousal than is HR (Von Borell
3.4. Physiology et al., 2007). For example, Gácsi et al. (2013) found that separation
from the owner did not increase HR but affected HRV.
Several neuropeptides are highly conserved throughout evo- To conclude this section on methods to study the dog-human
lution, probably due to their importance for social behaviour relationship, it is important to emphasise that it is not only the
(e.g. Insel and Young, 2001; Panksepp, 2009). Oxytocin is sug- choice of method that is crucial (e.g. questionnaire, behavioural or
gested to promote affiliative behaviour and facilitate bonding physiological approaches), but also what is measured (i.e. aspects of
between mother and young, as well as between partners (Carter, the relationship, the affectional bond or the attachment behaviour).
1998; Carter et al., 1992; Keverne and Kendrick, 1994; Witt If, for example, the aim is to investigate the quality of a relationship
et al., 1992). Also, it inhibits the development of opioid toler- then the frequency and type of interactions and how these are syn-
ance (Kovachs et al., 1987), which is important in order to sustain chronised between the individuals in that relationship need to be
the pleasant experience of close social interaction, further pro- measured (Hinde, 1976b). This is further discussed in the context
moting bonding (Panksepp, 1998). Interestingly, mothers with a of dog-human relationships in the next section.
secure-autonomous attachment style have higher levels of periph-
eral oxytocin during interaction with their child, compared to more
insecure mothers (Strathearn et al., 2009). 4. Towards measuring different relationship styles in
Increased levels of plasma oxytocin have been observed in dog-human dyads
humans during positive and calm interaction with their dog (Miller
et al., 2009), and the effect seems to be mutual (Handlin et al., 2011; Below we emphasise the possible benefits of investigating dyads
Odendaal and Meintjes, 2003). The effect in humans is stronger during separation and reunion events as well as specific measures
when the person is interacting with their own dog compared to from the dog’s view of the relationship (attachment style) and from
an unfamiliar dog, indicating the importance of the relationship the owners view (caregiving strategy).
on oxytocin release (Odendaal, 2000). This is further supported by
the findings of Handlin et al. (2012), suggesting that the higher fre-
quency of close contact with the dog (e.g. kissing it on a daily basis), 4.1. Changing the focus in attachment evaluations
the higher the oxytocin release in both humans and dogs. Even the
mere reappearance of a person can elicit oxytocin release in dogs, It is important to remember that the central element of attach-
and if dogs are physically affirmed at reunion elevated levels of oxy- ment theory is the balance between proximity-seeking behaviour
tocin remain for a longer duration (Rehn et al., 2014b). Nagasawa towards the attachment figure (initial response to the stressor) and
et al. (2015) found that when dogs, but not hand-raised wolves, the propensity to move away from the attachment figure to explore
looked at their owner oxytocin levels increased in the human. a potential threat (delayed response to the stressor) (Bowlby, 1958).
Moreover, they observed an increased frequency of gazing at the Hence, to further develop the potential in future SSP studies, we
owner after administrating the dogs with oxytocin intra-nasally; suggest that focus should be on variations in individual behavioural
leading them to suggest that an ‘interspecies oxytocin-mediated patterns throughout the test, rather than trying to explain general
positive loop’ may have played an important role during domesti- attachment behaviour based on comparisons of the dogs’ behaviour
cation. It has also been suggested that variation caused by genetic in episodes where the owners are present vs. absent. We suggest
polymorphisms in the oxytocin receptor gene may be related to that focusing more on the strategies developed to gain comfort
proximity-seeking to the owner in dogs (Kis et al., 2014), as the from the caregiver (i.e. the attachment bond) would be a fruitful
same receptor gene has previously been shown to be related to line of research in order to increase our understanding about the
secure/insecure infant attachment styles (Chen et al., 2011). dog-owner relationship.
6 T. Rehn, L.J. Keeling / Applied Animal Behaviour Science 183 (2016) 1–9

It may also be more suitable to develop reliable observer rat- developed within human psychology. Moreover, observations of
ing scales to score responses during the SSP (Schöberl et al., 2015) the owner’s behaviour during reunion and how well they are syn-
than quantitative recording methods, but this remains to be inves- chronised with the dog’s behaviour may reveal characteristics of
tigated. We further propose that individual attachment styles may their caregiving strategy. For example, it is already known that dogs’
become more apparent when the dog is presented with another greeting behaviour is influenced by how the person initiates contact
type of challenging stressor, in order to control for some of the dif- at reunion (Rehn et al., 2014b).
ferences in early experience of a particular situation. Examples of Since an individual’s adult attachment style influences overall
such stressors are the approach of a threatening stranger (Gácsi caregiving behaviour, investigation of the dog owner’s adult attach-
et al., 2013) or a sudden visual/acoustic surprise in a novel envi- ment style (assessed through interviews or questionnaires) and its
ronment. An additional stressor has been introduced previously possible correlation with their dog’s attachment style deserves fur-
during the SSP in the form of a puppet (e.g. Fallani et al., 2006) ther attention in the future, e.g. see recent work by Konok et al.
and could easily be standardised. During stressor applications, (2015) and Siniscalchi et al. (2013). One could also hypothesise that
we suggest to include observations of the dog’s gaze alternations while the caregiving strategy of a parent towards their child may
(stressor/owner) as it is known that more securely attached chil- be to promote eventual independence, it may be different towards
dren have a greater attention flexibility when challenged with their dog. That is, even if attachment theory may serve as a base
a stressor (gaze shifts between stressor and attachment figure) for future studies of the dog-owner relationship, it should not be
(Main, 2000). assumed that the owner necessarily treats their dog as they would
their child or that owners use the same caregiving strategy to all
4.2. Reunion situations per se dogs in the household.

In order to understand the balance between separation distress 4.4. Factors that may affect attachment development
and the calming effect of a returning attachment figure and so iden-
tify individual attachment styles in dogs, separation and reunion It may be that different breeds are predisposed to different styles
events, in their own right, deserve more attention in future stud- of attachment as a result of intensive selective breeding. It is tempt-
ies. Methods using separation and particularly reunion behaviour ing to speculate that such biases may be seen between different
outside of the SSP seem to provide stable measures of different types of working dogs, where some breeds are supposed to perform
attachment styles in older children (Cassidy, 1988; Goldberg, 1991). their tasks with minimal guidance from a handler, while others
Behaviour at reunion reflects individuals’ previous experiences of work in close contact constantly attentive to their handlers’ signals.
each other as well as expressing their intentions for future interac- No such differences in the SSP have been confirmed (Mariti et al.,
tions. Behaviour during separation and reunion can therefore give 2013) even if working dogs are often associated with characteristics
us a ‘snap-shot’ of their relationship. During reunion within SSP such as sociability, courage and self-confidence (e.g. Koda, 2001;
studies, approach latency and the frequencies of initiating physical Svartberg, 2006). Perhaps the differences lies in the distribution of
contact are expressed differently by the dog according to the famil- different attachment styles between breeds.
iarity of the human (e.g. Rehn et al., 2013; Topál et al., 1998), as are The interaction between the genetic background and the envi-
the frequencies of tail wagging, lip licking, body shaking and vocal- ronment is another challenge to be further explored. Udell et al.
izing (Rehn, 2013). Variation with which these greeting behaviours (2014) compared breeds selected for exaggeration (Border collie)
are expressed in different situations outside the SSP may be use- and inhibition (Anatoalian shepherd) of predation behaviour in a
ful in assessing the quality or type of relationship, and such tests socio-cognitive challenge, the human pointing task. They found
are easy to standardise. In future, studies of separation and reunion that Border collies outperformed the Anatoalian shepherds when
behaviour (outside or within the SSP) should include the owner’s naïve to the task, but after some additional training the shepherds
behaviour around departure and return, and also how the inter- reached the same success rate, suggesting that explicit experience
actions between the dog and the owner are ‘synchronised’ when can be used to overcome breed-specific predispositions. Whether
reunited as this could reflect the owner’s caregiving strategy. or not breed biases in attachment style exist, the influence of early
experience and the owner’s behaviour is crucial for the social devel-
4.3. Measures of the owner opment of the dog (e.g. Gazzano et al., 2008b). Just recently, it was
found that the level of maternal care experienced by the pup is pos-
As has already been stated, the attachment style that an infant itively correlated to the level of engagement in social activities with
develops is dependent on the attachment figure’s caregiving strat- people (Foyer et al., 2016), perhaps indicating its relevance also to
egy (Ainsworth, 1989; Main, 2000). The infant’s behaviour and attachment development. Also, more fearful dogs are reported to
expressions are not related to the parent’s behaviour initially, have experienced lower quality of maternal care during puppyhood
but they gradually become tailored to the parent’s willingness to (Tiira and Lohi, 2016). Cultural differences in caregiving behaviour
respond (Bowlby, 1969). These variations in caregiving behaviour in humans are suggested to influence the distribution of attachment
are likely to be present also among dog owners and dogs can be styles in different countries (e.g. Dilworth-Anderson et al., 2002;
expected to adapt their behaviour accordingly, so leading to the You and Malley-Morrison, 2000). However, to our knowledge, pos-
formation of different attachment styles. sible effects of maternal care during puppyhood, age of weaning or
A potential process by which mutual understanding or misun- possible cultural differences in caregiving on the development of
derstandings in behaviour may lead to different attachment styles attachment bonds in dogs to humans have not yet been explored.
is illustrated in Fig. 1. This framework links together the different Age is another interesting factor which deserves further investi-
scenarios during dog-owner interactions and their possible effects gation in relation to attachment to people. Are dogs (like humans)
on relationship quality. Variations in owner caregiving behaviour, more ‘flexible’ (adaptive) when they are younger and if so, is there
as defined in human psychology, have not yet been implemented a ‘cut-off’ point with respect to developing their basic attachment
in anthrozoology research. An owner’s caregiving strategy may be style? Dogs are most adaptable to their social environment during
measured by using questionnaires directly related to their inter- their sensitive period for socialization, 3–16 weeks of age (Scott
actions with the dog, e.g. the human-dog interaction subscale and Fuller, 1965), but we do not know if this is the crucial time
of the Monash Dog Owner Relationship Scale (MDORS; Dwyer for them to develop an attachment style, although it is tempting
et al., 2006) or by modifying caregiving questionnaires/interviews to assume that this may be the case. On the one hand, it has been
T. Rehn, L.J. Keeling / Applied Animal Behaviour Science 183 (2016) 1–9 7

Fig. 1. An illustration of different scenarios during dog-owner interactions and their possible effects on the relationship. The light-grey circle in the top represents an
organized interaction pattern between a dog and its owner. The dog expresses attachment behaviours in a stressful situation, followed by a response by the owner. This
response is successful if it has a calming effect on the dog, including an increased feeling of security and comfort. The light-grey circle may illustrate a variety of different
behavioural patterns used by the dog (attachment styles) and the owner (caregiving strategies), but they are all functional in that they meet the expectations of the dog and
the owner. The dark-grey circle in the bottom of the figure illustrates a situation where the owner and dog do not understand (or are ignorant to) each other’s communicative
attempts (i.e. the owner’s behavioural response is not successful in calming the dog). In this case, the dog may adapt its behaviour, trying alternative ways in order to reach
a functional response from the owner. In a worst case scenario, the interactions between the dog and the owner continue to mismatch, with an increased risk for conflict in
the relationship or the dog may be unable to cope and develops abnormal behaviour.

shown that dogs acquired when older than 6 months of age are at their primary caregiver at around 6–7 months of age (Bowlby, 1969;
an increased risk of relinquishment (Patronek et al., 1996), which Ainsworth, 1973). But that different attachment styles can be devel-
supports this assumption. It is however unclear if such dogs are oped does not necessarily mean that they can change easily once
more prone to have already developed behavioural problems and developed. For example, a dog may have developed its attachment
this was the reason for re-homing the dog in the first place. On style with a previous owner, but if this style is no longer adap-
the other hand, Valsecchi et al. (2010) suggested that attachment tive together with a new owner (Fig. 1), this may have implications
is not ‘full-fledged’ until the dog reaches the age of around three for its welfare. A previously low tendency for aggressiveness or
years. However, in their study with guide dogs for the blind, it was fearfulness may increase in unsuccessful relationships and such
not possible to disentangle the dogs’ physical and psychological behavioural problems are one of the most common reasons to why
development vs. its relationship to the ‘owner’, since the dogs were people relinquish dogs to shelters (e.g. Miller et al., 1996; Salman
tested in the SSP together with the puppy walker (at 11 months of et al., 1998). Accounting for the individual’s attachment style and
age), the trainer (at 16 months) and finally with the blind owner the person’s caregiving strategy around rehoming of dogs may be
(at 36 months). In another study, focusing only on the effect of age beneficial for both the dog and the new owner.
on attachment behaviour, the overall behaviour pattern during the
SSP was the same between a group of adult (<7 years old) and aged
4.5. Conclusions
(≥7 years old) dogs (Mongillo et al., 2013). But they did find that the
aged dogs sought more physical contact with their owners at the
In this concluding section, we give recommendations for how to
beginning of the SSP, and showed less proximity-seeking behaviour
better merge the approaches used in human psychology and animal
when the owner was absent. Whether dogs change the details of
behaviour when measuring dog-owner relationships.
their comfort-seeking strategies with age or if these differences
may be explained by genuine changes in attachment styles are yet
to be explored. 1) The dog-owner relationship is multi-faceted and challenging
In humans, the development of attachment behaviour begins to explore. Attachment theory will continue to be a promising
around the age of 2–6 month and infants usually show all of the framework to base future work upon, however it is important
behaviours that define attachment selectively directed towards that terms used when referring to attachment in anthrozoology
research are clearly defined.
8 T. Rehn, L.J. Keeling / Applied Animal Behaviour Science 183 (2016) 1–9

2) Attachment theory has been used successfully before to study Bowlby, J., 1958. The nature of the child’s tie to his mother. Int. J. Psychoanal. 39,
the dog-owner relationship, but here we suggest broadening 350–373.
Bowlby, J., 1969. Attachment and Loss, Vol. 1 Attachment. Basic Books, New York.
from the narrow focus on the secure aspect of attachment and Carter, C., Williams, J., Witt, D., Insel, T., 1992. Oxytocin and social bonding. Ann. N.
allowing for the possibility that other attachment styles by the Y. Acad. Sci. 652, 204–211.
dog may be equally functional in a good dog-owner relationship. Carter, C.S., 1998. Neuroendocrine perspectives on social attachment and love.
Psychoneuroendocrinology 23, 779–818.
3) The owner’s overall caregiving strategy should be evaluated Cassidy, J., 1988. Child-mother attachment and the self in six-year-olds. Child Dev.
and considered in order to understand the relationship. This is 59, 121–134.
important as dogs probably adapt their behaviour to their pri- Chen, F.S., Barth, M.E., Johnson, S.L., Gotlib, I.H., Johnson, S.C., 2011. Oxytocin
receptor (OXTR) polymorphisms and attachment in human infants. Front.
mary caregiver’s behaviour. Investigations could even include
Psychol. 2 (art 200), 1–6, http://dx.doi.org/10.3389/fpsyg.2011.00200.
aspects such as the owner’s previous experience of human Creel, S., 2001. Social dominance and stress hormones. Trends Ecol. Evol. 16,
relationships, since this seems to be a predictor of a person’s 491–497.
Crowell, J.A., Frayley, R.C., Shaver, P.R., 2008. Measurement of individual
caregiving behaviour.
differences in adolescent and adult attachment. In: Cassidy, J., Shaver, P.R.
4) The majority of previous studies assessing the dog-human (Eds.), Handbook of Attachment: Theory, Research and Clinical Applications.
relationship have focused on one of the individuals in the rela- Guilford Press, New York/London, pp. 599–634.
tionship (dog or owner), which tells only one side of the story. In Dilworth-Anderson, P., Canty Williams, I., Gibson, B.E., 2002. Issues of race,
ethnicity, and culture in caregiving research: a 20-year review (1980–2000).
the future it is recommended to combine studies of owners and Gerontologist 42, 237–272.
their dogs (a dyadic approach) to better understand the factors Dwyer, F., Bennett, P.C., Coleman, G.J., 2006. Development of the monash dog
contributing to more or less successful relationships. owner relationship scale (MDORS). Anthrozoös 19, 243–256.
Fallani, G., Prato-Previde, E., Valsecchi, P., 2006. Do disrupted early attachments
5) Behavioural evaluations of the dog and owner should preferably affect teh relationship between guide dogs and blind owners? Appl. Anim.
be made in combination with physiological measures. Based on Behav. Sci. 100, 241–257.
the current literature, the most promising physiological mea- Fallani, G., Prato-Previde, E., Valsecchi, P., 2007. Behavioral and physiological
responses of guide dogs to a situation of emotional distress. Physiol. Behav. 90,
sures related to bonding and social interactions are oxytocin and 648–655.
HRV. Foyer, P., Bjällerhag, N., Wilsson, E., Jensen, P., 2014. Behaviour and experiences of
6) Findings suggest that a focus on separation and reunion situ- dogs during the first year of life predict the outcome in a later temperament
test. Appl. Anim. Behav. Sci. 155, 93–100.
ations between dogs and their owners would be a promising
Foyer, P., Wilsson, E., Jensen, P., 2016. Levels of maternal care affect adult offspring
future line of research to better classify ‘relationship styles’, that temperament. Sci. Rep. 6, 19253, http://dx.doi.org/10.1038/srep19253.
take into account the attributes of the dog (attachment style) and Gácsi, M., Topál, J., Miklósi, Á., Dóka, A., Csányi, V., 2001. Attachment behavior of
adult dogs (Canis familiaris) living at rescue centers: forming new bonds. J.
the owner (caregiving strategy).
Comp. Psychol. 4, 423–431.
7) The consequences of classifying relationship styles from an Gácsi, M., Maros, K., Sernkvist, S., Faragó, T., Miklósi, Á., 2013. Human analogue safe
applied point of view are for owners to become more aware of haven effects of the owner: behavioural and heart rate responses to stressful
what type of attachment style their dog has and what caregiving social stimuli in dogs. PLoS One 8 (3), e58475.
Gazzano, A., Mariti, C., Notari, L., Sighieri, C., McBride, E.A., 2008a. Effects of early
strategy they have. Knowing this may contribute to identifying gentling and early environment on emotional development of puppies. Appl.
what might be a source of conflict in past or present relation- Anim. Behav. Sci. 110, 304–394.
ships, and help owners to form a more successful and positive Gazzano, A., Mariti, C., Alvares, S., Cozzi, A., Tognetti, R., Sighieri, C., 2008b. The
prevention of undesirable behaviors in dogs: effectiveness of veterinary
relationship. behaviorists’ advice given to puppy owners. J. Vet. Behav. 3, 125–133.
Goldberg, S., 1991. Recent developments in attachment theory and research. Can. J.
Psychiatry 36, 393–400.
Conflict of interest Gross, J.J., 1998. The emerging field of emotion regulation: an integrative review.
Rev. Gen. Psychol. 2, 271–299.
None. Gunnar, M.R., 1998. Quality of early care and buffering of potential neuroendocrine
stress reactions: potential effects on the developing human brain. Prevent.
Med. 27, 208–211.
Acknowledgements Handlin, L., Hydbring-Sandberg, E., Nilsson, A., Ejdeback, M., Jansson, A.,
Uvnäs-Moberg, K., 2011. Short-term interaction between dogs and their
owners: effects on oxytocin cortisol, insulin and heart rate—an exploratory
We would like to thank the Swedish Research Council for study. Anthrozoös 24, 301–315.
Environment, Agricultural Sciences and Spatial Planning (FOR- Handlin, L., Nilsson, A., Ejdeback, M., Hydbring-Sandberg, E., Uvnäs-Moberg, K.,
2012. Associations between the psychological characteristics of the
MAS, 221-2013-329) for financing this work. The work was carried
human-dog relationship and oxytocin and cortisol levels. Anthrozoös 25,
out within the Centre of Excellence in Animal Welfare Science, a 215–228.
Swedish collaborative research environment. Haverbeke, A., Diederich, C., Depiereux, E., Giffroy, J.M., 2008. Cortisol and
behavioral responses of working dogs to environmental challenges. Physiol.
Behav. 93, 59–67.
References Hazan, C., Shaver, P.R., 1987. Romantic love conceptualized as an attachment
process. J. Personal. Soc. Psychol. 52, 511–524.
Ainsworth, M.D.S., Bell, S.M., 1970. Attachment, exploration and separation: Hinde, R.A., 1976a. On describing relationships. J. Child Psychol. Psychiatry 17,
illustrated by the behavior of one-year-olds in a strange situation. Child Dev. 1–19.
41, 49–67. Hinde, R.A., 1976b. Relationships and social structure. Man New Ser. 11, 1–17.
Ainsworth, M.D.S., Blehar, M.C., Waters, E., Wall, S., 1978. Patterns of Attachment: Horn, L., Huber, L., Range, F., 2013. The importance of the secure base effect for
A Psychological Study of the Strange Situation. Lawrence Erlbaum Associates, domesticated dogs −evidence from a manipulative problem-solving task. PLoS
Hillsdale, New Jersey. One 8 (5), e65296.
Ainsworth, M.D.S., 1973. The development of infant-mother attachment. In: Hydbring-Sandberg, E., von Walter, L.W., Höglund, K., Svartberg, K., Swenson, L.,
Cardwell, B., Ricciuti, H. (Eds.), Review of Child Development Research. Forkman, B., 2004. Physiological fear responses to fear provocation in dogs. J.
University of Chicago Press, Chicago, pp. 1–94. Endocrinol. 180, 439–448.
Ainsworth, M.D.S., 1989. Attachment beyond infancy. Am. Psychol. 44, 709–716. Insel, T.R., Young, L.J., 2001. The neurobiology of attachment. Nat. Rev. Neurosci. 2,
Appelhans, B.M., Luecken, L.J., 2006. Heart rate variability as an index of regulated 129–136.
emotional responding. Rev. Gen. Psychol. 10, 229–240. Jagoe, A., Serpell, J., 1996. Owner characteristics and interactions and the
Archer, J., 1997. Why do people love their pets? Evol. Hum. Behav. 18, 237–259. prevalence of canine behaviour problems. Appl. Anim. Behav. Sci. 47, 31–42.
Barker, S.B., Barker, R.T., 1988. The human-canine bond: closer than family ties? J. Johnson, T.P., Garrity, T.F., Stallones, L., 1992. Psychometric evaluation of the
Mental Health Counselling 10, 46–56. lexington attachment to pets scale (LAPS). Anthrozoös 5, 160–175.
Bartholomew, K., Shaver, P.R., 1998. Methods of assessing adult attachment: do Kerepesi, A., Dóka, A., Miklósi, Á., 2014. Dogs and their human companions: the
they converge? In: Simpson, J.A., Rholes, W.S. (Eds.), Attachment Theory and effect of familiarity on dog-human interactions. Behav. Process. 110, 27–36.
Close Relationships. The Guilford Press, New York, pp. 25–45. Keverne, B., Kendrick, K.M., 1994. Maternal behaviour in sheep and its
Bell, D.C., Richard, A.J., 2000. The forgotten element in attachment. Psychol. Inquiry neuroendocrine regulation. Acta Paediatr. 83, 47–56.
11, 69–83.
T. Rehn, L.J. Keeling / Applied Animal Behaviour Science 183 (2016) 1–9 9

Kis, A., Bence, M., Lakatos, G., Pergel, E., Turcsán, B., Pluijmakers, J., Vas, J., Elek, Z., Rehn, T., Lindholm, U., Keeling, L., Forkman, B., 2014a. I like my dog, does my dog
Brúder, I., Földi, L., Sasvári-Székely, M., Miklósi, Á., Rónai, Z., Kubinyi, E., 2014. like me? Appl. Anim. Behav. Sci. 150, 65–73.
Oxytocin receptor gene polymorphisms are associated with human directed Rehn, T., Handlin, L., Uvnäs-Moberg, K., Keeling, L.J., 2014b. Dogs’ endocrine and
social behaviour in dogs (Canis familiaris). PLoS One 9 (1), e83993. behavioural responses at reunion are affected by how the human initiates
Kobak, R., 2009. Defining and measuring of attachment bonds: comment on contact. Physiol. Behav. 124, 45–53.
Kurdek (2009). J. Fam. Psychol. 23, 447–449. Rehn, T., 2013. Best of friends? Investigating the dog-human relationship Doctoral
Kobelt, A.J., Hemsworth, P.H., Barnett, J.L., Coleman, G.J., 2003. A survey of dog thesis no 2013 67. Swedish University of Agricultural Sciences, SLU
ownership in suburban Australia—conditions and behaviour problems. Appl. Service/Repro, Uppsala.
Anim. Behav. Sci. 82, 137–148. Sachser, N., Kaiser, S., Hennessy, M.B., 2013. Behavioural profiles are shaped by
Koda, N., 2001. Development of play behavior between potential guide dogs for the social experience: when, how and why. Philos. Trans. R. Soc. B 368, 20120344,
blind and human raisers. Behav. Process. 53, 41–46. http://dx.doi.org/10.10198/rstb.2012.0344.
Konok, V., Kosztolányi, A., Rainer, W., Mutschler, B., Halsband, U., Miklósi, Á., 2015. Salman, M.D., New, J.G., Scarlett, J.M., Kass, P.H., Ruch-Gaillie, R., Hetts, S., 1998.
Influence of owners’ attachment style and personality on their dogs’ (Canis Human and animal factors related to the relinquishment of dogs and cats in 12
familiaris) separation-related disorder. PLoS One 10 (2), e0118375. selected animal shelters in the United States. J. Appl. Anim. Welfare Sci. 1,
Kotrschal, K., Schöberl, I., Bauer, B., Thibeaut, A., Wedl, M., 2009. Dyadic 207–226.
relationships and operational performance of male and female owners and Schöberl, I., Beetz, A., Solomon, J., Gee, N., Kotrschal, K., 2015. Social factors
their male dogs. Behav. Process. 81, 383–391. influencing cortisol modulation in dogs during a strange situation procedure. J.
Kovachs, G.L., Sarnyai, A., Izbek, F., Szabo, G., Telegdy, G., Barth, T., Jost, K., 1987. Vet. Behav. 11, 77–85.
The effect of oxytocin-related peptides on acute morphine tolerance: opposite Scott, J.P., Fuller, J.L., 1965. Genetics and the Social Behavior of the Dog. University
action by oxytocin and its receptor antagonist. J. Pharmacol. Exp. Ther. 241, of Chicago Press, Chicago.
569–574. Serpell, J.A., 2004. Factors influencing human attitudes to animals and their
Line, S., Voith, V.L., 1986. Dominance aggression of dogs towards people: behavior welfare. Anim. Welfare 13, 145–151.
profile and response to treatment. Appl. Anim. Behav. Sci. 16, 77–83. Shiverdecker, M.D., Schiml, P.A., Hennessy, M.B., 2013. Human interaction
M. Main, J. Solomon, Discovery of a nonsecure disoriented attachment pattern moderates plasma cortisol and behavioral responses of dogs to shelter
(1986). housing. Physiol. Behav. 109, 75–79.
Main, M., 1990. Cross-cultural studies of attachment organizations: recent studies, Shore, E.R., Riley, M.L., Douglas, D.K., 2006. Pet owner behaviours and attachment
changing methodologies and concept of conditional strategies. Hum. Dev. 33, to yard versus house dogs. Anthrozoös 19, 325–334.
48–61. Siniscalchi, M., Stipo, C., Quaranta, A., 2013. Like owner, like dog: correlation
Main, M., 2000. The organized categories of infant, child, and adult attachment: between the owner’s attachment profile and the owner-dog bond. PLoS One 8
flexible vs: inflexible attention under attachment-related stress. J. Am. (10), e78455.
Psychoanal. Assoc. 48, 1055–1095. Sroufe, L.A., Waters, E., 1977. Heart rate as a convergent measure in clinical and
Marinelli, L., Adamelli, S., Normando, S., Bono, G., 2007. Quality of life of the pet developmental research. Merrill-Palmer Q. 23, 3–27.
dog: influence of owner and dog’s characteristics. Appl. Anim. Behav. Sci. 108, Steiss, J.E., Schaffer, C., Ahmad, H.A., Voith, V.L., 2007. Evaluation of plasma cortisol
143–156. levels and behavior in dogs wearing bark control collars. Appl. Anim. Behav.
Mariti, C., Carlone, B., Borgognini-Tarli, S., Prescuittini, S., Pierantoni, L., Gazzano, Sci. 106, 96–106.
A., 2011. Considering the dog as part of the system: studying the attachment Strathearn, L., Fonagy, P., Amico, J., Montague, P.R., 2009. Adult attachment
bond of dogs toward all members of the fostering family. J. Vet. Behav. 6, predicts maternal brain and oxytocin response to infant cues.
90–91. Neuropsychopharmacol 34, 2655–2666.
Mariti, C., Ricci, E., Carlone, B., Moore, J.L., Sighieri, C., Gazzano, A., 2013. Dog Svartberg, K., 2006. Breed-typical behavior in dogs−historical remnants or recent
attachment to man: a comparison between pet and working dogs. J. Vet. constructs? Appl. Anim.Behav. Sci. 96, 293–313.
Behav. 8, 135–145. Templer, D.I., Salter, C.A., Dickey, S., Baldwin, R., Veleber, D.M., 1981. The
Mariti, C., Carlone, B., Ricci, E., Sighieri, C., Gazzano, A., 2014. Intraspecific construction of a pet attitude scale. Psychol. Rec. 31, 343–348.
attachment in adult domestic dogs (Canis familiaris): preliminary results. Appl. Tiira, K., Lohi, H., 2016. Early life experiences and exercise associate with canine
Anim. Behav. Sci. 152, 64–72. anxieties. PLoS One 10 (11), e0141907, http://dx.doi.org/10.1371/journal.pone.
Mikulincer, M., Shaver, P.R., 2007. Attachment in Adulthood: Structure, Dynamics, 0141907.
and Change. The Guilford Press, New York, pp. 81–115 (324–345). Topál, J., Miklósi, Á., Csányi, V., Dóka, A., 1998. Attachment behavior in dogs (Canis
Miller, D.D., Staats, S.R., Partlo, C., Rada, K., 1996. Factors associated with the familiaris): A new application of the Ainsworth’s (1969) strange situation test.
decision to surrender a pet to an animal shelter. J. Am. Vet. Med. Assoc. 209, J. Comp. Psychol. 112, 219–229.
738–742. Topál, J., Gácsi, M., Miklósi, Á., Virányi, Z., Kubinyi, E., Csányi, V., 2005. Attachment
Miller, S.C., Kennedy, C., Devoe, D., Hickey, M., Nelson, T., Kogan, L., 2009. An to humans: a comparative study on hand-reared wolves and differently
examination of changes in oxytocin levels in men and women before and after socialized dog puppies. Anim. Behav. 70, 1367–1375.
interaction with a bonded dog. Anthrozoös 22, 31–42. Trivers, R.L., 1972. Parental investment and sexual selection. In: Cambell, B. (Ed.),
Mongillo, P., Pitteri, E., Carnier, P., Gabai, G., Adamelli, S., Marinelli, L., 2013. Does Sexual Selection and the Descent of Man. Aldine, Chicago.
the attachment system towards owners change in aged dogs? Physiol. Behav. Tuber, D.S., Sanders, S., Hennessy, M.B., Miller, J.A., 1996. Behavioral and
120, 64–69. glucocorticoid responses of adult domestic dogs (Canis familiaris) to
Nagasawa, M., Mitsui, S., En, S., Ohtani, N., Ohta, M., Sakuma, Y., Onaka, T., Mogi, K., companionship and social separation. J. Comp. Psychol. 110, 103–108.
Kikusui, T., 2015. Oxytocin-gaze positive loop and the coevolution of Udell, M.A.R., Ewald, M., Dorey, N.R., Wynne, C.D.L., 2014. Exploring breed
human-dog bonds. Science 348, 333–336. differences in dogs (Canis familiaris): does exaggeration or inhibition of
Odendaal, J.S.J., Meintjes, R.A., 2003. Neurophysiological correlates of affiliative predatory response predict performance on human-guided tasks? Anim.
behaviour between humans and dogs. Vet. J. 165, 296–301. Behav. 89, 99–105.
Odendaal, J.S.J., 2000. Animal-assisted therapy—magic or medicine? J. Valsecchi, P., Prato-Previde, E., Accorsi, P.E., Fallani, G., 2010. Development of the
Psychosomatic Res. 49, 275–280. attachment bond in guide dogs. Appl. Anim. Behav. Sci. 123, 43–50.
Palestrini, C., Prato-Previde, E., Spiezio, C., Verga, M., 2005. Heart rate and Voith, V.L., Wright, J.C., Danneman, P.J., 1992. Is there a relationship between
behavioural responses of dogs in the Ainsworth’s Strange Situation Procedure. canine behavior problems and spoiling activities, anthropomorphism, and
Appl. Anim. Behav. Sci. 94, 75–88. obedience training? Appl. Anim. Behav. Sci. 34, 263–272.
Palmer, R., Custance, D., 2008. A counterbalanced version of Ainsworth’s Strange Voith, V.L., 1985. Attachment of people to companion animals. Vet. Clin. N. Am.
Situation Procedure reveals secure-base effects in dog-human relationships. Small Anim. Pract. 15, 289–295.
Appl. Anim. Behav. Sci. 109, 306–319. Von Borell, E., Langbein, J., Despres, G., Hansen, S., Leterrier, C., Marchant-Forde, J.,
Panksepp, J., Nelson, E., Siviy, S., 1994. Brain opioids and mother-infant social Marchant-Forde, R., Minero, M., Mohr, E., Prunier, A., Valence, D., Veissier, I.,
motivation. Acta Paediatric Suppl. 397, 40–46. 2007. Heart rate variability as a measure of autonomic regulation of cardiac
Panksepp, J., 1998. Affective Neuroscience: The Foundations of Human and Animal activity for assessing stress and welfare in farm animals—a review. Physiol.
Emotions. Oxford University Press, New York. Behav. 92, 293–316.
Panksepp, J., 2009. Primary process affects and brain oxytocin. Biol. Psychiatry 65, Wedl, M., Schröberl, I., Bauer, B., Day, J., Kotrschal, K., 2010. Relational factors
725–727. affecting dog social attraction to human partners. Interact. Stud. 11, 482–503.
Patronek, G.J., Glickman, L.T., Beck, A.M., McCabe, G.P., Ecker, C., 1996. Risk factors Witt, D.M., Winslow, J.T., Insel, T.R., 1992. Enhanced social interactions in rats
for relinquishment of dogs to an animal shelter. J. Am. Vet. Med. Assoc. 209, following chronic, centrally infused oxytocin. Pharmacol. Biochem. Behav. 43,
572–581. 855–861.
Prato-Previde, E., Custance, D.M., Spiezio, C., Sabatini, F., 2003. Is the dog-human You, S.H., Malley-Morrison, K., 2000. Young adult attachment styles and intimate
relationship an attachment bond? An observational study using Ainsworth’s relationships with close friends: a cross-cultural study of Koreans and
strange situation. Behaviour 140, 225–254. Caucasian Americans. J. Cross-Cult. Psychol. 31, 528–534.
Rehn, T., McGowan, R.T.S., Keeling, L.J., 2013. Evaluating the Strange Situation
Procedure (SSP) to assess the bond between dogs and humans. PLoS One 8 (2),
e56938.

You might also like