2. 120
which attract the mother so that she finds and approaches
her young (Bowlby, 1958; Harlow and Harlow, 1965).
A condition related to attachment behaviors, known as
separation anxiety, has been described in human beings and
in dogs. Dogs affected by separation anxiety suffer from
anxiety episodes, and even short absences of their owners
can result in urination, defecation, vocalizations, and object
destruction (Manteca, 1996; Overall, 1997; Pageat et al.,
1999). This is one of the most common behavior problems
reported in pet dogs (Voith and Ganster, 1993; King et al.,
1999). This also seems to be true for dogs in Mexico
(Edwards et al., 2002; Heiblum et al., 2005).
Given the fact that, until recently, little attention had
been paid to the extent to which domestic cats are social, the
issues of attachment and separation anxiety remain relatively unexplored in this species. It is known that cats are
social animals and the extent to which this characteristic is
seen depends on the resources available in the environment
(Fogle, 1995; Crowell-Davis et al., 1997). There is now
some evidence that cats may also suffer from separation
anxiety (Schwartz, 2001, 2002). It has become more important to understand feline social behavior problems associated with separation anxiety since pet cat populations in
several countries are increasing. For instance, the estimated
cat population in the United States ranges from 23 to 61
million, with a population of 1 cat per 3.2 family units
(Beaver, 2003). Since there is little information regarding
attachment behaviors in cats, it is very likely that, similarly
to what happens in dogs, there are large numbers of separation anxiety cases that are not properly diagnosed. Given
the importance of generating more information that could be
useful to better understand separation anxiety in cats, this
study was carried out to experimentally identify attachment
behaviors. These attachment behaviors could be used as a
basis for future studies of the incidence of separation anxiety in domestic cats.
Materials and methods
Location and subjects
This study was carried out in the Department of Ethology
and Wildlife of the Faculty of Veterinary Medicine, Universidad Nacional Autónoma de México (UNAM) in Mexico City. A 3 meter by 2 meter room containing 2 chairs,
one for the owner and another for the stranger, was used as
an observation room. There were 2 cat toys in this room:
one was a commercial toy (a jumping ladybug) fixed to the
floor opposite the door, and the other consisted of a string
attached to a ball meant for the subjects to play with the cat.
A one-way mirror located on the upper left side of the room
was used for observations.
The cat owners were recruited by placing advertisements
in veterinary clinics, in the Cat Show of the Asociación
Gatófila Mexicana (Mexican Cat Fanciers’ Association),
and the Asociación Mexicana de Gatos (Mexican Cat As-
Journal of Veterinary Behavior, Vol 2, No 4, July/August 2007
Table 1
List of behaviors measured
Individual Behaviors
● Locomotion/Exploration: Searching and active
investigation of new situations in absence of an urgent
necessity, including movement from one place to another
(Immelmann and Beer, 1989). Activity can be directed to
objects or people present. Olfactory or oral inspection was
considered exploration as well.
● Vigilance: State of alertness, of being prepared to
perceive events that could pose a danger to the animal
itself or its companion (Immelmann and Beer, 1989). This
state was referred to if the cat was standing, sitting or
lying down and making ear movements. Body posture and
looking in a specific direction were considered as a part of
this state.
● Inactivity: Standing, sitting or lying down without making
any movements.
● Approaching a door: This behavior included approximating
the door, touching it, lying down or staying still in the
vicinity of the door.
Interactive behaviors
● Physical contact with owner.
● Physical contact with stranger.
● Marking: rubbing face or body against an object or
person.
● Vocalizations.
● Play: Hunt-like postures which could be directed to people
or toys.
sociation). The cats included in the study were between 1
and 7 years of age; this age range was chosen to mirror that
of the only other study reporting on aspects of attachment
(Schwartz, 2002).
Three pilot situations were used with different cats to
obtain the list of behaviors to be measured (Table 1). A total
of 28 owner-cat pairs were recruited for the study, which
included cats of different body types ranging from 1 to 7
years of age, without taking into account their sex or reproductive status. These owner-cat pairs were subjected to the
Ainsworth’s Adapted Strange Situation Test.
For data analysis, cats were divided by sex and reproductive status, and into 3 recognized body types (Paragon
and Vaissaire, 2000): muscular, cobby or Persian-type, and
oriental or Siamese-type (Table 2). In this study, all cobbies
were Persians, all Orientals were Siamese, and the muscular
type included Domestic Europeans and one Maine Coon.
Behavioral event frequencies and duration of states of individual behaviors (i.e., exploration/locomotion, alertness,
and inactivity) (Table 3) were recorded and measured by
means of focal sampling.
Experimental design
The Ainsworth Strange Situation Test (Ainsworth et al.,
1978) was adapted for use in cats. The procedure began with
a 30-second introductory event, and consisted of 7 experimental events of 3 minutes each, for a total duration of 21
3. Edwards et al
Table 2
Attachment in cats
121
Number of animals belonging to the three different body types, sex and reproductive condition
Body Type
Number of Individuals (%)
Sex
Intact (%)
Neutered (%)
Cobby
(all were Persians)
Oriental
(all were Siamese)
Muscular
(Domestic European and one Maine Coon)
21.4
M
F
M
F
M
F
33.3
16.7
33.3
16.7
0
6.3
50
0
16.7
33.3
62.5
31.3
21.4
57.1
N ϭ 28; M ϭ Male; F ϭ Female.
minutes. Instructions were given to both owner and stranger
regarding the sequence and duration of the aforementioned
events, as in Topál’s (1998) and Parthasarathy’s (2000)
tests. The stranger was always the same individual.
The owners were not informed of the real purpose of the
study; they were told instead that the purpose of the study
was to determine the cat’s behavior in a strange situation.
The observation room, toys, and chairs were cleaned
with water and soap and then with an enzymatic odor
neutralizer (Four Paws, Hauppauge, NY) before and after
each experimental situation. The observation of cats always
took place on different days. Never were 2 cats observed on
the same day.
Event 2 (3 minutes): Stranger, Owner, and Cat. A
stranger comes in, takes a seat, and after 30 seconds she
starts a conversation with the owner. At the 2-minute mark,
the stranger attempts to play with the cat, and the owner
leaves without interrupting, distracting, or saying goodbye.
Play can occur by touching the cat or using a toy, only if the
cat allows it.
Event 3 (3 minutes): Stranger and Cat. This is the first
separation episode. The stranger’s behavior is focused on
the cat. During the first minute, the stranger tries to attract
the cat’s attention and to get it to move away from the door
through playing. If the cat is not ready to play, the stranger
tries to attract its attention by means of petting. At the 2
minute mark, the stranger stops playing, but contact is
allowed as long as the cat seeks it.
Event 4 (3 minutes): Owner and Cat. This is the first
reunion episode. The owner approaches the closed door
from the outside and calls the cat. Then the owner opens the
door and waits for the cat to respond. The owner rewards the
cat by petting it. In the meantime, the stranger leaves. After
2 minutes, the owner leaves as well.
Event 5 (3 minutes): Cat alone. This is the second separation episode.
Adapted ainsworth test
Introductory Event (30 seconds approximately): the observer introduces the owner and the cat to the experimental
room and leaves them there.
Event 1 (3 minutes): Owner and Cat. The owner does not
interact with the cat while the cat explores. At 1.5 minutes,
a signal (a knock on the door) is given to the owner to
stimulate play.
Table 3 List of behaviors observed during the different phases of the experiment: cat with owner, cat alone and cat with
stranger; means and standard deviation
Behavior
Locomotion/exploration (%)
Alertness (events/min)
Inactivity (%)
Proportion of time in physical contact (%)
Vocalizations (events/min)
Remaining near the door (%)
Approximating the door (events/min)
Physical contact frequency (events/min)
Physical contact latency (seg)
Following the owner (events/min)
Marking (events/min)
Play (events/min)
Owner
19
1.67
9
32
0.66
3
0.30
1.83
22.48
0.40
0.41
0.07
Alone
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
a
11
1.42a
18a
19a
1.53a
4a
0.41a
1.31a
18.71a
0.49
0.88a
0.17
07
3.75
27
*
5.38
10
1.62
*
*
*
0.02
*
Stranger
Ϯ8
Ϯ 3.99b
Ϯ 30b
b
Ϯ 7.03b
Ϯ 17b
Ϯ 3.76b
Ϯ 0.09b
13
1.80
23
04
1.00
22
0.83
0.54
52.84
*
0.14
*
*No data obtained
a
Different letters on the same line indicate a difference in the means (PϽ0.05) Friedman (ANOVA) and Wilcoxon.
b
Different letters on the same line indicate a difference in the means (PϽ0.05) Friedman (ANOVA) and Wilcoxon.
c
Different letters on the same line indicate a difference in the means (PϽ0.05) Friedman (ANOVA) and Wilcoxon.
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
Ϯ
(P)
c
14
1.04c
28c
45b
2.36a
59b
1.50c
0.09b
1.19b
Ϯ 0.44c
0.001
0.05
0.05
0.001
0.001
0.05
0.001
0.001
0.001
0.001
0.001
0.001
4. 122
Event 6 (3 minutes): Cat and stranger. This is a follow-up
of the second separation episode. During the first minute,
the stranger tries to attract the cat’s attention through play to
get it away from the door. If the cat is not ready to play, the
stranger tries to get its attention through petting. At the
2-minute mark, the stranger stops playing, but contact is
allowed if the cat seeks it.
Event 7 (3 minutes): Owner and Cat. This is the second
reunion episode. The stranger’s behavior is focused on the
cat. The owner opens the door and pauses for a moment
before rewarding the cat, giving it an opportunity to respond
spontaneously. The owner does not initiate contact with the
cat, but allows contact if the cat seeks it.
Procedure for obtaining data
Focal sampling was employed to obtain information on
the sequence of behaviors, on the frequency of behavioral
events, and on the proportion of time spent on each behavioral state (Martin and Bateson, 1986). Data was recorded
using “Registro Conductual Computarizado” (Computerized Behavioral Registry) software (Torres et al., 1992).
Episodes/events were used to assess attachment. Attachment to owners was assessed using events 4 and 7. To
obtain the corresponding information about the behavior of
the cat with the owner (episodes 4 and 7), with the stranger
(6), and when alone (5), the study evaluated 6 minutes of
observation with the owner, 3 minutes with the stranger, and
3 minutes alone, for a total analysis of 12 minutes per cat.
Each session was evaluated using several behavioral
categories, which were divided into interactive and individual behaviors (Table 1).
Statistical analysis
Nonparametric statistical tests were used to analyze the
data obtained in this study. Friedman’s test was used to
compare behavioral categories between episodes when cats
were with their owner, alone, and with a stranger. Wilcoxon’s test was used to compare behavioral categories
between 2 episodes (owner-stranger, owner-alone, and
stranger-alone). Different behavioral categories between the
3 body-type groups were compared using the Kruskal-Wallis test. The Mann-Whitney test was used to compare unrelated groups such as gender.
Results
Behavior comparisons for individuals during the
experimental episodes
Significant differences were found when comparing cats’
behavioral states when they were with their owners, when
alone, and when they were with a stranger. When looking at
Journal of Veterinary Behavior, Vol 2, No 4, July/August 2007
the proportion of time spent in different behavioral states, it
was revealed that cats spent more time in locomotion/exploration while in the company of their owner than while alone or
with the stranger (Friedman, F ϭ 13.55, P Յ 0.001; Table 3).
In addition, the proportion of inactivity time differed between
episodes. Cats were inactive longer when left alone than when
with the stranger or with their owners (Friedman, F ϭ 6.14, P
Ͻ 0.05; Table 3). Furthermore, when comparing the proportion of time spent interacting with a person between the 2
episodes in which a person was in the room with the cat, it was
seen that cats spent a significantly longer time in contact with
their owners than with the stranger (Table 3, 0.32 Ϯ 0.19
events/minute and 0.04 Ϯ 0.45 events/minute, Wilcoxon, z ϭ
2.02, P Ͻ 0.001).
Some statistical differences were also found when comparing the frequency of behavioral events between episodes.
The frequency of vigilant events was different between
episodes, as cats showed 5.00 Ϯ 4.26 events/minute, 11.25
Ϯ 11.95 events/minute, and 5.40 Ϯ 3.10 events/minute
when with their owner, alone, and with the stranger, respectively (Friedman, F ϭ 7.44, P Ͻ 0.05). In addition, cats
vocalized more when left alone than when they were with a
person in the room, either their owner or the stranger (Friedman, F ϭ 23.4, p Ͻ 0.001; Table 3). Facial marking events
were also different between episodes, being greater when
cats were with their owners than when alone or with a
stranger (Friedman, F ϭ 23.14, P Ͻ 0.001; Table 3).
When doing paired comparisons between episodes, an
additional difference was found in the proportion of time
spent near the door, which was much greater when the cats
were with a stranger (0.22Ϯ0.59) than when with their
owners (0.03 Ϯ 0.04) (Wilcoxon, z ϭ 2.06, P Ͻ 0.05).
Cats showed play behaviors only when they were with
their owners (0.21 Ϯ 0.52 events/minute, Wilcoxon, z ϭ
4.5, P Ͻ 0.001).
Behavior comparisons between groups of
different body type, sex, and reproductive status
(intact or neutered animals)
Some differences were found when doing behavior comparison between body types. The proportion of time spent in
locomotion/exploration was higher in the “cobby” type
group of cats than in the “oriental” and “muscular” types.
The time spent in locomotion for the 3 groups when the cat
was alone were: cobby 0.14 Ϯ 0.10 seconds; oriental 0.08 Ϯ
0.12 seconds, and muscular 0.06 Ϯ 0.05 seconds (KruskalWallis, H ϭ 6.34, N ϭ 3, P Ͻ 0.04). It was also seen that
the frequency of vocalization was greater in the oriental
type than in the other 2 groups (cobby, 3.28 Ϯ 0.10 events/
minute; oriental 11.55 Ϯ 0.12 events/minute, and muscle
2.55 Ϯ 0.05 events/minute; Kruskall-Wallis, H ϭ 6.01, N ϭ
3, p Ͻ 0.04). No significant differences were found in
reproductive condition or sex comparisons.
5. Edwards et al
Attachment in cats
Discussion
Outstanding differences were obtained in the proportion of
time spent in locomotion/exploration in the owner-alonestranger episodes. Cats spent more time in locomotion/
exploration when with the owner than when alone or with
the stranger. Locomotion in the presence of the owner is an
attachment indicator. Locomotive behavior is used by human infants to approach their favorite figure in following
this figure when it leaves, greeting it on its return, or simply
seeking to be near it (Bowlby, 1969).
Exploration and play also indicate that the cat has formed
an attachment, because it uses its owner as a safe base from
which to explore, just as it happens in human beings (Ainsworth, 1978) and primates, where the mother or primary
caretaker provides a “safe base” (Harlow and Harlow, 1965)
from which the infant learns to explore his world and
acquires security and stability in his relationships with others; similar ideas have been expressed regarding dogs
(Scott, 1962; Borchelt and Voith, 1982; Voith and Borchelt,
1985; McGrave, 1991). The results obtained in this study
are compatible with the ones found by Topál (1998) and
Parthasarathy (2000), where dogs tended to play more and
spend more time exploring in the presence of the owner,
compared to when they were in the presence of a stranger.
This pattern could explain the difference in behaviors when
in the presence of the owner in comparison to when the cat
is alone or with a stranger, as cats tend to become immobile
when stressed (Carlstead et al., 1992).
The amount of inactive time was lower when the cat was
with the owner and higher when the cat was alone or with
a stranger. With regard to locomotion/exploration, this finding reinforces that inactivity is compatible with states of
anxiety. Hemsworth and Barnett’s study (2000) associated
this behavior with high levels of cortisol. Such behaviors
may be considered a state of “freezing.”
Freezing is one way in which fear and anxiety are expressed in cats and dogs (Overall, 1997). Topál et al. (1998)
found no differences with dogs in passive behavior when
the presence of owner and stranger were compared. It has
been said that there is a decrease in exploration and an
increase in hiding which correlates with physiological measurements of stress in studies on large felines in captivity
(Konrad and Bagshaw, 1970; Carlstead et al., 1992; Carlstead et al., 1993a; Carlstead et al., 1993b). Behavioral
studies in domestic cats have revealed a reduction in general
activity (such as walking or running), exploration behavior
(smelling or rubbing), and grooming, which are correlated
with high levels of serum cortisol (Rochiltz et al., 1995).
Other studies on domestic and nondomestic felines indicate
that hiding and low levels of activity are indicators of stress
(McCune, 1992; Kessler and Turner, 1997). In human beings and other animals, an increase in the need to sleep can
be a sign of biological or physiological stress (Rampin et al.,
1991; Rushen, 2000). Other studies in domestic and nondomestic cats mention that behavioral apathy, hiding, and
low levels of activity are stress indicators (McCune, 1992;
123
Kessler and Turner, 1997; Kessler and Turner, 1999). Observation of zoo animals has also revealed a relationship
between sleeping and hiding (inactivity) with a higher level
of cortisol in feces (Wielebnowski et al., 2002). These
findings suggest that when compared to dogs, it is less likely
that cats suffering from separation anxiety will be destructive or exhibit inappropriate elimination behavior. It is well
known that cats are easily stressed; changing an object or
moving furniture in the house can trigger an anxiety response in cats. The cats’ response to this situation was
previously interpreted as territorial, rather than as a social
response (Konrad and Bagshaw, 1970).
In this adaptation of the Strange Situation Test, it was
anticipated that cats would be in a state of stress given the
simple fact that they were taken to a strange place. This
reaction is true even for dogs, which showed increased
sympathetic activity in the hypothalamic–adrenal axis when
introduced to a new environment (Beerda et al., 1997).
Accordingly, it was hypothesized that if the cats’ responses
were a result of a change in territory and not attachment
related, they would not move at all, except to hide in a
corner; but if they used their owners as a safe base, then
their behaviors would support the attachment theory, and if
they sought any person to find security, then their behaviors
would be associated with seeking refuge.
In the Ainsworth Strange Situation Test (Ainsworth, et
al., 1978) vocalization (crying) is considered an attachment
indicator. In this study, vocalizations (meows) were registered which could be equivalent to human youngsters crying. There is evidence within psychobiological literature
which indicates that stress responses associated to attachment are mediated in the brain by the opioid system (Panksepp et al., 1997). Pharmacological research with primates
shows that an opioid antagonist such as naloxone produces
an increase in the rate of separation-related vocalizations,
whereas an opioid agonist such as morphine produces a
decrease in such vocalizations (Wiener et al., 1997). There
are other studies conducted in guinea pigs which show that
offspring vocalize during separation from the mother (Arch
et al., 2000). These studies indicate that cat vocalizations
increase during isolation owing to the stress of being alone,
just as human youngsters cry when in the same situation. It
was also observed that cats vocalized more while with the
owner compared to when with the stranger. These vocalizations could be related to a certain type of calling behavior
rather than related to stress.
Clark (1992) and Case (2003) mention that facial and
body marking are friendly behaviors that make the cat feel
more comfortable with the owner. However, the opposite
could also be true: that the cat is already comfortable and
exhibits these behaviors as a consequence of that emotional
state. Either way, marking can be considered a special
means of communication, in which the cat deposits facial
pheromones that help him differentiate between familiar
and unfamiliar objects or persons and serves as a mood
stabilizer as well, and where the main goal is to mark the
6. 124
person as part of the group (Pageat and Gaultier, 2003). This
study found that owners were marked more often than
strangers because they were recognized by their cats. In this
case, the marking of strangers by cats could have occurred
because in this adaptation of the Ainsworth Strange Situation Test, cats got to spend a few minutes with the stranger
in the company of their owners before they were left alone
with her, and the cats might have begun getting acquainted
with the stranger during that time.
Regarding the proportion of time spent near the door,
cats spent more time near the door while in the presence of
the stranger compared to when they were with the owner.
This finding is consistent with studies by Topal (1998) and
ˇ
Parthasarathy (2000), in which dogs spent more time near
the door when the owner was away.
In the Ainsworth Strange Situation Test (1978), the infant response when the mother comes in and goes out is
considered an attachment indicator. Such responses include
following the mother when she leaves and greeting her
when she comes back in, reaching for her, bending over her,
smiling, vocalizing, and laughing. In this study, the owner
takes the mother’s place. The cats followed the owner, made
physical contact, and jumped onto the owner’s lap when the
owner was seated.
Body type, sex and reproductive condition
comparisons
In comparisons of behavioral categories between different body types, the cobby group spent more time in locomotion compared to other body types, an interesting discovery because literature reports that Persian cats belonging
to the cobby group are most indifferent to the environment
and not very active in comparison to the oriental and muscular types, which are more active (Schneck and Caravan,
1991; Clark, 1992; Case, 2003). On the other hand, results
of a study by Schwartz (2002) indicate that Persian cats are
more likely to suffer from separation anxiety. There is
another interesting finding regarding a significant difference
in the vocalization frequency between body types. Oriental
cats vocalize more in comparison to other groups. These
findings correspond with other studies saying that oriental
breeds, particularly Siamese cats, are more vocal than others
(Schneck and Caravan, 1991; Case, 2003). Unlike these
results, the ones obtained in the study by Topal (1998)
showed that there was no significant difference between dog
breeds.
When behavior categories were compared between neutered versus intact cats, there were no significant differences. There was no difference found in the attachment
bond, therefore it can be deduced that reproductive hormones have nothing to do with the creation of the attachment bond between cat and owner.
The data gathered through this study demonstrate that the
cats’ behaviors in this experiment meet the criteria enumerated for attachment to owners. These results indicate that
Journal of Veterinary Behavior, Vol 2, No 4, July/August 2007
cats exhibit attachment behaviors to their owners and thus
should be able to experience separation anxiety. These results, along with results of previous studies regarding stressful situations in felines (Carlstead et al, 1993a; Carlstead et
al, 1993b; Kessler, 1997; Rushen, 2000; Pageat, 2003),
indicate that cats are more likely to show a reduction in
general activity, with increased hiding or sleeping as the
major signs of stress or anxiety.
These findings indicate that in cases of separation anxiety in cats, the main signs may not be as easy to observe and
the cat remains undiagnosed (Bowlby, 1973; Monaghan and
Wood-Gush, 1990; Martin and Bateson, 1991; Voith, 1991;
Edney, 1993; Blunt and Goodnow, 1997; Hart and Eckstein,
1997; Kalin et al., 1997; Turner et al., 1998; King et al.,
2000; Heiblum et al., 2005).
Acknowledgments
The authors wish to thank:
●
●
●
●
Purina Pro Plan - Mexico.
Melissa Castillo Vázquez (Translation),
Valeria Aguilar Sánchez (Translation),
All the cats and their owners that participated in this
study.
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