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Behavioural disorders are a major reason for euthanasia and sheltering of pet dogs. The prevention and treatment of behavioural disorders requires a better understanding of the underlying causes. Early life experiences, such as maternal care, attachment and socialisation, have long lasting and serious consequences for the behavioural and physiological development of an individual. The complex interplay between these factors is likely to have consequences for the future dog-owner bond and the vulnerability to develop behavioural disorders. Here, we summarise the current literature on the interactions between maternal care, attachment formation, and the sensitive socialisation period and their potential consequences on adult dog behaviour. Based on the findings we highlight gaps in knowledge and provide suggestions for future research which are necessary to formulate recommendations for pet dog breeding and socialisation.
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Behaviour (2018) DOI:10.1163/1568539X-00003486
The importance of early life experiences for the
development of behavioural disorders in domestic dogs
Lisa Dietz a,,Anne-Marie K. Arnold b,Vivian C. Goerlich-Jansson band
Claudia M. Vinke b
aDepartment of Pathobiology, Faculty of Veterinary Medicine, Utrecht University,
Utrecht, The Netherlands
bDepartment of Animals in Science & Society, Faculty of Veterinary Medicine,
Utrecht University, Utrecht, The Netherlands
*Corresponding author’s e-mail address:
Received 12 January 2018; initial decision 19 February 2018; revised 19 March 2018;
accepted 20 March 2018
Behavioural disorders are a major reason for euthanasia and sheltering of pet dogs. The prevention
and treatment of behavioural disorders requires a better understanding of the underlying causes.
Early life experiences, such as maternal care, attachment and socialisation, have long lasting and
serious consequences for the behavioural and physiological development of an individual. The
complex interplay between these factors is likely to have consequences for the future dog-owner
bond and the vulnerability to develop behavioural disorders. Here, we summarise the current
literature on the interactions between maternal care, attachment formation, and the sensitive so-
cialisation period and their potential consequences on adult dog behaviour. Based on the findings
we highlight gaps in knowledge and provide suggestions for future research which are necessary
to formulate recommendations for pet dog breeding and socialisation.
maternal care, attachment, socialisation, behavioural development, behavioural disorders,
dog breeding, HPA, adolescence.
1. Introduction
Aggression, anxiety and separation related behavioural disorders are com-
monly seen in pet dogs worldwide, with a high impact for the owner and
©Authors, 2018 DOI 10.1163/1568539X-00003486
This is an open access article distributed under the terms of the prevailing CC-BY-NC license at the time of publication.
2Behaviour (2018) DOI:10.1163/1568539X-00003486
society (Voith, 2009). In the United States, Canada, Australia and Fin-
land, about 70% of the dogs referred to a behavioural clinic are diagnosed
with behavioural disorders related to aggression, while separation related
behavioural disorders are seen in 9–19% of dogs and anxiety in 14–21%
(Denenberg et al., 2005; Bamberger & Houpt, 2006; Tiira et al., 2016).
These behavioural disorders have been demonstrated to be the main cause
for sheltering in 11–34% of sheltered dogs and the main reason for 10–16%
of euthanasia requests (Lambert et al., 2015). Note that we distinguish ‘prob-
lem behaviour’ (normal behaviour for the dog yet unwanted behaviour for the
owner) and behavioural disorders (pathological behaviours excessive in fre-
quency, duration and/or intensity and/or applied in the wrong context). These
terms are used interchangeably in the literature, but here we focus on patho-
logical behaviour, which substantially decreases an individual’s capacity to
cope with its environment.
In The Netherlands, and probably in other western European countries
as well, the demand for dog pups largely exceeds the capacity of national
breeders to produce litters (Four Paws, 2013). About 150000 new pups are
obtained by owners in the Netherlands each year, of which only 40% are
bred by Dutch breeders (Feiten en Cijfers, HAS Hogeschool & Faculteit
Diergeneeskunde, 2015). This high demand has led to the establishment of
both legal and illegal networks that import pups to western European coun-
tries, with low regard for adequate vaccinations, weaning age or socialisation
programs (Van Uhm, 2010; Four Paws, 2013). Puppies sold through these
networks are often bred in large puppy mills, where they stay in small cages
and are weaned and transported at an early age (Van Uhm, 2010). During
this age period social and non-social stimulation is essential for a normal
behavioural development, enabling a young pup to adapt to a new environ-
ment and the regular challenges within, as will be discussed in this review.
This stimulation, however, is difficult to realise in puppy mills and trading
networks due to their magnitude and prevailing housing and transport condi-
A recent review on the behaviour of dogs originating from commercial
breeders, puppy farms and pet stores, highlights the increased incidence
of behavioural disorders such as fear and aggression towards other dogs
and humans in commercially bred dogs (McMillan, 2017). One study cat-
egorised breeders as “responsible” or “irresponsible” based on the outcome
of 11 questions (e.g., number of available litters, age of pup at purchase, was
L. Dietz et al. / Behaviour (2018) 3
mother dog seen interacting with her pups) and found that the prevalence
of aggression and separation related behavioural disorders is higher in dogs
obtained from irresponsible breeders (Gray et al., 2016). The increased inci-
dence of behavioural disorders in commercially bred dogs may be caused by
a lack of appropriate stimulation during early life (Jagoe, 1994 in Serpell &
Jagoe, 1995). Thus, in addition to other major factors influencing behaviour,
such as genetics (Houpt, 2007) and responsible ownership (Jagoe & Serpell,
1996), the early life experiences of the pup play a major role in its further
behavioural development (Wilsson, 2016). While research on domestic dogs
is scarce, studies on primates and rodents corroborate the importance of the
early life phase in shaping the individual phenotype (Harlow et al., 1971;
Sanchez et al., 2001). Especially negative experiences or insufficient stimu-
lation, as well as minimal maternal care and attachment, have been shown
to increase the chance for the development of behavioural disorders. This re-
view focusses on the domestic dog, while literature on other mammal species
is incorporated as well, to highlight research areas potentially of interest.
In most mammal species, the attachment bond between infants and their
mother is established before and during the so called sensitive period for
socialisation in early postnatal life (Bowlby, 1958, 1982; Ainsworth, 1978;
Carter, 1998). During this crucial period, interactions with the social environ-
ment shape the neuronal and behavioural profiles of an individual (Weaver,
2009; Roth & David Sweatt, 2011; Sachser et al., 2013). Although the central
nervous system retains some level of plasticity in adult life, its capacity for
adjustments based on experiences is substantially greater during the sensitive
period for socialisation (Knudsen, 2004).
Scott & Fuller (1965) were the first to investigate the early sensitive period
for socialisation in dogs. Since then this topic has attracted much attention,
but experimental research is scarce partly due to ethical considerations which
arose as soon as the impact and consequences of social deprivation for the
experimental animals involved became clear. The majority of the existing
literature on the importance of early life experiences in domestic dogs de-
scribes the human-dog relationship and compares human-dog attachment
with human-infant attachment. The mother-pup bond and its interactions
with the subsequent socialisation period, as well as its influence on the de-
velopment of behaviour, has not been studied in much detail so far (but
see Previde et al., 2009 and Mariti et al., 2014). In addition, studies on
behavioural patterns of human-dog attachment bonds in connection to the
4Behaviour (2018) DOI:10.1163/1568539X-00003486
quality and/or quantity of mother dog-pup attachment are lacking. Especially
the formation of the attachment bond of a pup with its mother during the sen-
sitive period, in which future socio-emotional behaviour is shaped, should
comprehensively receive more attention to gain better insight into the de-
velopment of (abnormal) behaviour in dogs. This review aims at elucidating
the complex interplay between the formation of the mother-pup attachment
bond and early socialisation, as well as their importance for the develop-
ment of behaviour and behavioural disorders, and the consequences for the
human-dog bond. To stimulate future research we also highlight deficits in
the current knowledge on these topics. Finally, the results of this review may
provide critical arguments to help policy makers take further steps against
commercial dog trade and puppy mills and to better inform future dog own-
2. The first step: mother–pup relationship
In dogs, primarily the female cares for the young (Pal, 2005). In the fol-
lowing section, we will review evidence suggesting that dog pups develop
a specific attachment style towards their mother, based on the quality and
quantity of maternal care. We discuss parallels with attachment theory in the
human literature and point out the gaps in knowledge on attachment forma-
tion in dogs. Finally, we review the physiological mechanisms involved in
maternal care and attachment and the role of the mother-pup relationship in
the development of behaviour, as well as the risk for potential behavioural
2.1. Maternal care
During the first two weeks of a dog pup’s life (i.e., the neonatal period; Scott
& Marston, 1950), its senses are not fully developed yet. Like most altricial
species, a new born dog pup is blind and deaf, and cognition and motor skills
are poor due to the immaturity of the brain (Fox, 1971a). In this virtually
isolated state, pups are highly dependent on their mother for nourishment,
warmth, and elimination, the latter of which is stimulated through anogenital
licking by the mother (Rheingold, 1963; Wilsson, 2016). From three weeks
of age pups signal distress upon brief separation from the mother in the form
of whining and yelping, which decreases in intensity with age (Elliot & Scott,
1961). This initial phase of distress upon maternal separation is also seen
L. Dietz et al. / Behaviour (2018) 5
in monkeys and humans (Kaufman & Rosenblum, 1967), and is followed
by a phase of despair and depression if separation is prolonged. Prolonged
or permanent maternal separation at an early age has potentially detrimental
consequences in dogs; disease and mortality related to separation stress occur
more often in pups weaned at six weeks of age compared to pups weaned at
twelve weeks (Slabbert & Rasa, 1993). In addition, early permanent maternal
separation, a common occurrence in commercial breeding, may play a role
in the development of behavioural disorders, as will be discussed further in
this review.
In the rodent literature, the quality and amount of maternal care is typi-
cally quantified by measuring the time females spend licking/grooming their
pups and arched back nursing (Liu et al., 1997). Maternal care in dogs
predominantly comprises physical contact with the pups, licking the pups
(including anogenital licking) and nursing, all of which occur frequently
during the first weeks of a pup’s life but then gradually decrease over time
(Rheingold, 1963; Overall, 2013). Recently, different nursing postures have
been described in dogs: vertical nursing (female standing or sitting), lateral
nursing (female lying on side) and ventral nursing (female lying on her stom-
ach) (Bray et al., 2017a). Since the accessibility of the teats vary per nursing
posture, it is conceivable that different styles between females may differen-
tially affect their pups, as has been suggested by another recent study with
guide dogs of the same author: the nursing style of the mother dog appeared
to influence the success rate of guide dog training in the pups, with ventral
nursing being associated with failure and vertical nursing with success (Bray
et al., 2017b). Ventral nursing requires less effort than vertical nursing, as
it is easier for the pups to stay attached to the mother’s nipple. The authors
suggested that pups from mothers with a primarily ventral nursing style ex-
perience too few challenges in their early days and this deprives them of the
opportunity to acquire a certain degree of independence, leading to an in-
creased incidence of anxiety-related behaviours with a lower success rate in
guide dog training as a consequence.
In rodents, the extent of maternal caregiving may vary among individuals,
with profound consequences for the offspring’s behavioural and physiolog-
ical development. Suboptimal levels of maternal care in these species may
lead to heightened stress responsiveness (Meaney et al., 1994; Champagne et
al., 2003; Czerwinski et al., 2016) and decreased cognitive function (Liu et
al., 2000). Also in dog pups the quality and quantity of maternal care shows
6Behaviour (2018) DOI:10.1163/1568539X-00003486
considerable variation among females (Rheingold, 1963; Czerwinski et al.,
2014; Bray et al., 2017a), and appears to affect the behavioural development
of dog pups (Foyer et al., 2016; Guardini et al., 2016; Bray et al., 2017b). In
German Shepherds, mother-pup interactions such as physical contact, nurs-
ing, licking and sniffing or poking the pup with the nose were recorded. Pups
that received a higher amount of maternal care scored higher in engagement
with humans and inanimate objects at 18 months of age (Foyer et al., 2016).
These findings are corroborated by several studies; a questionnaire-based
study asked dog owners to grade the quality of maternal care, specified as
spending time with and taking care of the pups, on a scale of 1 to 7. Lower
scores, indicating an estimated poor quality of maternal care by the owner,
were associated with more fearful behaviour in the adult dog (Tiira & Lohi,
2015). Likewise, a longer daily duration of maternal care (i.e. physical con-
tact, licking, ano-genital licking and nursing) during the first three weeks
postpartum was associated with more exploratory behaviour and less signs
of stress, such as increased locomotion and vocalisations during isolation, in
eight week old puppies (Guardini et al., 2016). Finally, pups separated from
the mother at 30 to 40 days of age, that consequently receive a lower amount
of maternal care compared to pups separated at 60 days of age, were more
likely to develop a variety of behavioural problems as an adult, including
fearfulness on walks, noise reactivity and excessive barking (Pierantoni et
al., 2011).
Collectively, the described literature indicates that, also in dogs, elements
of maternal care, such as nursing style and amount of nursing and licking,
are an important predictor for the development of adult behaviour.
2.2. Mother–infant attachment
An attachment bond is an affectional bond seen in many mammal species,
that is characterised by proximity seeking behaviour, a feeling of security
in the presence of the attachment figure, and distress upon separation from
this figure (Gubernick, 1981). The primary caregiver, usually the mother,
responds to the infant’s behaviour by providing care, comfort and protection
(Bowlby, 1958), thereby increasing the infant’s chances of survival.
In most mammals, the attachment bond with the primary caregiver is
formed during the postnatal period (Carter, 1998). The process of attachment
formation is likely an evolutionary adaptive and conserved process; young
animals are born with a predisposed repertoire of species-specific attachment
L. Dietz et al. / Behaviour (2018) 7
behaviours that promote proximity to their caregiver (Ainsworth, 1978). The
young often show a preference for a particular attachment figure above others
or above strangers, seek and maintain proximity to that figure, and may
show an acute stress response to brief separation from the attachment figure
(Bowlby, 1973). Even in the absence of food supply, young animals have
a strong preference to stay near their mother (Lorenz, 1935; Bowlby, 1958,
1982; Harlow & Zimmerman, 1959; Harlow & Harlow, 1965), which shows
the importance of the bond once it has been established. The attachment
bond with the mother reduces fear and the mother thus functions as a secure
base, which encourages the young to explore its environment (Gubernick,
1981). Most research on the attachment bond has been done in humans.
The developmental process of attachment in many non-human mammals,
including dogs, may be similar to the process described in human children,
but research is lacking.
To study attachment in human children, a well-known and frequently
used tool is the Strange Situation Test (SST), designed by Mary Ainsworth
(1978) and based on her joint work with John Bowlby (Bretherton, 1992). In
the SST procedure, the infant’s behaviour is recorded during eight different
episodes in an unfamiliar setting (Ainsworth, 1978). During these episodes
the behavioural responses upon separation and reunion with the attachment
figure are recorded and compared to behaviour exhibited in the presence of
a stranger. Based on the SST, four different attachment styles are described
for human infants: secure, anxious-ambivalent, avoidant and disorganised
(Ainsworth, 1978, Table 1). Attachment styles appear to be influenced by
temperament in humans, where proneness to distress is associated with in-
secure attachment styles (Goldsmith & Alansky; 1987). Notably, attachment
is not a one-way process, and the development of a particular attachment
style also depends on the nurturing behaviour of the mother, i.e., mater-
nal care (Ainsworth, 1978). A secure attachment style is associated with a
higher sensitivity and responsiveness of the mother to the infant’s attach-
ment behaviours, whereas an insecure attachment style is associated with
lower sensitivity and responsiveness (Ainsworth, 1978; Grossmann et al.,
1985; Table 1). Modified versions of the SST have been successfully per-
formed in dogs, however, mainly to investigate the human–dog attachment
bond (Topál et al., 1998; Gácsi et al., 2001; Palestrini et al., 2005; Schöberl et
al., 2016). Intriguingly, these studies describe similar behaviours of the dog
towards the human attachment figure as are seen in the human child: dogs
8Behaviour (2018) DOI:10.1163/1568539X-00003486
Table 1.
Overview of the relationship between maternal caregiving and attachment style in human
infants and adults, and similarities with attachment styles described in human–dog relation-
Maternal caregiving in humans1,2 Attachment styles and behaviours as described in
humans2,3 and dogs4,5,6
Sensitive, responsive1,2 Secure2,4 Proximity to caregiver2,4,5,6
Distress during separation2,5,6
Low interest in strangers2,5,6
Insensitive, unresponsive1,2 Anxious-ambivalent2High distress during
or ambivalent4separation2,4
Difficult to comfort upon
Seek constant reassurance
and proximity2
Avoidant2,4 No separation distress2
Ignore caregiver2,4
Similar towards stranger2
Disorganised3,4 Disoriented behaviours3
Approach-avoidance conflict
on reunion4
Note that the influence of maternal care on attachment styles in dogs has not yet been
1Grossmann et al. (1985).
2Ainsworth (1978).
3Main & Solomon (1990).
4Schöberl et al. (2016).
5Palestrini et al. (2005).
6Topál et al. (1998).
show distress upon separation from the owner, which cannot be alleviated by
the presence of a stranger, and show proximity seeking behaviour upon re-
union with the owner. In the study by Topál et al. (1998) 51 owner–dog pairs
underwent an SST and behaviour of the dog in the presence of their owner
or a stranger were recorded. Dogs exhibited significantly more play, physical
contact and exploratory behaviour in the presence of their owner. In separa-
tion episodes where only the stranger was present, the dogs spent more time
L. Dietz et al. / Behaviour (2018) 9
near the door of the test room compared to episodes with the owner present.
Contact seeking behaviour was seen more during reunion with the owner
compared to the stranger entering the room. Cluster analysis revealed dif-
ferences in attachment levels among the dogs, but specific attachment styles
were not distinguished. In another study 17 adult dogs underwent an SST
and showed higher activity levels and more play behaviour in the presence
of the owner compared to a stranger, and spent most of their time oriented
at the door of the test room upon separation from the owner (Palestrini et
al., 2005). Yet another study has described similar attachment styles in dogs
as have been found in humans, based on approaching behaviour, play, ex-
ploration and physical contact seen during separation and reunion with the
owner during a SST (Solomon et al., 2014 in Schöberl et al., 2016; Table 1).
Only two studies so far have investigated the intraspecific attachment bond
between adult dogs (Mariti et al., 2014) and mother-pup attachment bond
(Previde et al., 2009). At the age of 45–55 days, dog pups of different breeds
were either introduced to a novel environment or a stranger, or briefly sep-
arated from their mother. The pups showed a behavioural repertoire similar
to that described in human children: seeking proximity to the mother, dis-
tress upon separation, and a secure base effect in the presence of the mother
(Previde et al., 2009). These findings suggest parallels in the development
and nature of attachment bonds in social animals, but more studies on the
intraspecific attachment bond in dogs are needed in order to substantiate this
As described, attachment is not a one-way process. Since humans and
dogs are both altricial species in which maternal caregiving plays a vital role,
it is conceivable that, as in humans, attachment styles in dogs also develop
under the influence of the quality and quantity of maternal care. However,
information on the influence of maternal caregiving on attachment styles in
dogs is lacking, while this aspect may also affect the dog-human attach-
ment formation and, thus, urgently requires further investigation. Also the
potential role of temperament on attachment styles in dogs, as is seen in hu-
mans, has yet to be elucidated. Subsequently, mother-pup attachment bonds
could be compared to human–dog attachment bonds to validate extrapola-
tions based on research on human mother–child attachment. This approach
may provide insight in the development of attachment-related behavioural
problems in the domestic dog.
10 Behaviour (2018) DOI:10.1163/1568539X-00003486
2.3. Physiological mechanisms underlying maternal care and the
attachment bond
The common patterns found in attachment and behaviour between humans
and dogs may partly be explained by corresponding subcortical neural
and neurochemical mechanisms underlying parenting behaviour and care
(Rilling & Young, 2014). For example, the neuropeptide oxytocin plays an
important role in promoting maternal caregiving and the formation of an
attachment bond between mother and infant (Nelson & Panksepp, 1998;
Rilling & Young, 2014; Bos, 2016). In humans, parents with high levels
of oxytocin show more affection toward their children, facilitating a secure
attachment style of the infant to the parent (Rilling & Young 2014). Recent
research shows that oxytocin may play an important role in the dog-human
bonding as well (Beetz et al., 2012; Handlin et al., 2012; Romero et al.,
2014; Nagasawa et al., 2015) and interactions between dogs and humans can
result in increased levels of oxytocin in both species (Beetz et al., 2012). The
role of oxytocin in the formation and maintenance of the attachment bond
between the mother and her offspring specifically in dogs remains unclear.
During sensitive windows in early life neural structures mature (Knudsen,
2004), while environmental and social factors can profoundly affect this pro-
cess (Sachser et al., 2013; Blakemore & Mills, 2014; Brydges, 2016). Inter-
estingly, in new born rats, a stress hypo-responsive period (SHRP) has been
described (Sapolsky & Meaney, 1986), during which adrenocorticotropic
hormone (ACTH) and glucocorticoid (GC) release in response to a stres-
sor is strongly attenuated and modulated under the influence of maternal
care (Rincón-Cortés & Sullivan, 2014). The SHRP coincides with the de-
velopment of the nervous system, which is highly plastic and susceptible to
external influences during the perinatal period. Given the potential negative
impact of high levels of GC, the SHRP is thought to protect the developing
brain (Sapolsky & Meaney, 1986; Rincón-Cortés & Sullivan, 2014). Some
evidence for the presence of an SHRP was also found in dogs: brief maternal
separation did not elicit a physiological stress response in pups of three or
four weeks of age, but urinary cortisol did increase after maternal separation
at five and six weeks of age, suggesting the SHRP lasts until four weeks of
age in dogs (Nagasawa et al., 2014).
As described above, the variation in quantity and quality of maternal care
between female dogs has important implications for the subsequent devel-
opment of the pup (Foyer et al., 2016; Bray et al., 2017b), however, the
L. Dietz et al. / Behaviour (2018) 11
physiological mechanisms behind this relation have not yet been elucidated
in this species. In rodents, maternal care influences stress responsivity in
the young animal also beyond the SHRP, by programming the development
of the hypothalamic-pituitary-adrenal (HPA) axis (Champagne et al., 2003;
Rincón-Cortés & Sullivan, 2014), leading to heightened or reduced sensitiv-
ity to stressors later in life (e.g., Liu et al., 1997; Caldji et al., 1998; Capitanio
et al., 2005; Champagne & Curley, 2005; Champagne et al., 2008; Sachser et
al., 2013). High levels of maternal care in the form of licking/grooming and
arched back nursing lead to lower stress responsiveness in adulthood, both
physiologically and behaviourally (Liu et al., 1997). Conversely, offspring
that received low maternal care show increased and prolonged ACTH and
GC release after a stressful stimulus as an adult (Champagne et al., 2003;
Lupien et al., 2009; Meaney et al., 2013). Prolonged elevations of GC, espe-
cially during maturation, may lead to a dysregulation of the HPA axis, and
impaired neural development and cognitive function (De Kloet et al., 2005;
Lupien et al., 2009; Rincón-Cortés & Sullivan, 2014; Brydges, 2016). In-
deed, in rats the physiological changes produced by low levels of maternal
care are accompanied by more fearful behaviour in novel situations as an
adult (Caldji et al., 1998).
In short, maternal care influences the offspring’s neuroendocrine and be-
havioural responses to stress, with effects lasting into adulthood (Rincón-
Cortés & Sullivan, 2014). Low levels of maternal care lead to increased HPA
axis activity, which may impair neural development and results in height-
ened stress responsivity in the adult animal and a higher risk of disease on
the long term (De Kloet et al., 2005). It is conceivable that similar physio-
logical mechanisms occur in dogs, and the potential cognitive and emotional
deficits caused by poor quality of maternal care could pose a high risk for
the development of behavioural disorders, such as fearfulness, in this species
(Tiira & Lohi, 2015). However, solid research on this topic in dogs is neces-
sary in order to firmly draw these conclusions.
3. Socialisation
Following the neonatal period and transitional period, where the mother-pup
bond is of utmost importance, the first socialisation period begins. In this sec-
tion, we discuss the different phases of the sensitive period for socialisation
and its components, such as experiences with social and non-social stimuli,
12 Behaviour (2018) DOI:10.1163/1568539X-00003486
and play behaviour. Appropriate stimulation during the sensitive period for
socialisation results in a sociable dog with good adaptive capacity, that can
build relationships with humans and conspecifics and is able to cope with
novelty (Case, 2005). Inadequate and insufficient experiences on the other
hand increase the risk of developing behavioural problems later in life. We
also discuss the role of the mother dog during this sensitive period.
3.1. Early socialisation (3.5 to 12 weeks)
During the neonatal period, the pups’ senses are not yet fully developed,
making the young highly dependent on their mother. In the third week of life
(i.e., the transitional period), the eyes and ears of the pup gradually open,
they begin to walk and explore, and by the end of the third week pups are no
longer dependent on their mother for elimination (Scott, 1958). This devel-
opmental stage marks the beginning of the early socialisation period, which
is defined by both physiological and behavioural changes. A commonly ac-
cepted time frame for the early socialisation period in dogs is from 3.5 to
approximately 12 weeks of age (Scott & Marston, 1950; Scott & Fuller,
1965; Table 2). However, defining the exact timing of this sensitive period
in dogs is difficult due to breed-specific variation (Scott & Fuller, 1965). For
example, Morrow et al. (2015) found that Cavalier King Charles spaniel pups
had a significantly delayed onset of the early socialisation period compared
to Yorkshire terrier pups and German shepherd pups. Therefore, not the tim-
ing but the processes acting during attachment and socialisation should be
the main point of focus.
During the early socialisation period, a pup learns through experience to
associate social and non-social stimuli with positive or negative emotions.
These experiences allow the pup to build adaptive capacity in order to cope
with and adapt to new situations. To avoid fear responses in the dog’s future
it is recommended to expose a pup during the early socialisation period
to any social or non-social stimuli (e.g. objects, sounds, textures, locations
and situations) that will likely be part of their adult environment (Battaglia,
2009; Howell et al., 2015). A retrospective study found that dogs raised
in domestic environments (i.e., dogs that spent their sensitive period for
socialisation at the stimulus-rich breeder’s home) were less likely to develop
fear and aggression towards unfamiliar people compared to dogs raised in
non-domestic environments (Appleby et al., 2002). In a questionnaire study
with companion dogs, more socialisation experiences between eight and
L. Dietz et al. / Behaviour (2018) 13
Table 2.
Overview of the timing of the sensitive periods and developmental transitions during early life in dogs (Scott & Marston, 1950; Scott, 1958;
Scott & Fuller, 1965).
(0–2 weeks)
(2–3 weeks)
Early socialisation Late
(12 weeks–
6 months)
(6 months–
1 year)
3–5 weeks 5–8 weeks 8–12 weeks
Vision and
Opening of
eyes and ears
Brain maturation
and myelination
Brain maturation
and myelination
Sexual maturation Sexual maturity
Poor locomotory
Sensitive to
novelty in
Sensitive to
novelty in
Adult EEG
Reinforcement of
SHRP Weaning
Immature brain Immature brain Exploratory
Peak sensitivity
to human contact
Care seeking
Care seeking
Increasing fear of
Increasing fear
of novelty
Play with mother Play with mother
Play with
Play with
Play with
SHRP =stress hypo-responsive period.
14 Behaviour (2018) DOI:10.1163/1568539X-00003486
twelve weeks of age were associated with lower fearfulness in adult dogs
(Tiira & Lohi, 2015). Thus, sufficient exposure to relevant stimuli during the
early socialisation period appears to be associated with lower fearfulness and
aggression in dogs.
Socialisation periods or similar sensitive periods are seen in many mam-
mal and bird species, including rodents and humans (Scott, 1962). In wolves
it is suggested that a sensitive period for interspecific socialisation to humans
is also present, but it is much shorter than in dogs, ending around three weeks
of age (Klinghammer & Goodmann, 1987). It is thought that the more flex-
ible sensitive period in dogs is a result of domestication, as it allows dogs
more time to form strong social bonds with humans during this developmen-
tal period (Udell et al., 2010).
Although animals keep learning about their environment throughout their
life, they are substantially more sensitive to environmental stimuli during the
sensitive period for socialisation (Knudsen, 2004). This increased sensitivity
to environmental stimuli is caused by underlying physiological changes. In
the first two weeks of a pup’s life the central nervous system is still immature.
Brain activity during awake and sleeping states cannot be distinguished using
electroencephalography (EEG; Fox, 1971a) and auditory or visual stimuli do
not evoke reactions in the pup (Scott, 1958). As the pup’s visual and audi-
tory senses start developing from three weeks of age and motor skills are
rapidly improving (Pal, 2008), the nervous system also develops at a rapid
pace. Between three and five weeks of age, the somatomotor, visual and
auditory cortex show increased dendrite length and number, and myelina-
tion (Fox, 1971a). Changes in the EEG responsiveness now become evident
and at eight weeks of age, the EEG of pups shows adult-like patterns (Fox,
1971a). These physiological changes are accompanied by an increase in ap-
proaching and exploratory behaviour, and altogether indicate an increased
sensitivity of the pup to both social and non-social stimuli (Scott & Fuller,
1965; Fox & Stelzner, 1966; Battaglia, 2009). At the beginning of the early
socialisation period the central nervous system has reached a level of matu-
rity that allows conditioning and associative learning (Scott, 1958), and as the
pup interacts with its environment and learns about relevant stimuli, the con-
nections between neural synapses become stronger and neural circuits more
stable (Coppinger & Coppinger, 2001; Knudsen, 2004). Between three and
five weeks of age, a drop in heart rate can be detected in pups, followed by an
increase in heart rate that peaks at 7–8 weeks (Scott & Fuller, 1965; Lindsay,
L. Dietz et al. / Behaviour (2018) 15
2013). Simultaneous with this increase in sympathetic activity, the matura-
tion of the central nervous system, and the ending of the SHRP, pups show
another change in behaviour. From 5 weeks of age (with some notable breed
differences in onset; Morrow et al., 2015), dogs gradually become more fear-
ful of novel unfamiliar stimuli (Freedman et al., 1961; Woolpy & Ginsburg,
1967), recovery after a fear response becomes increasingly delayed (Scott
& Fuller, 1965), and desensitisation to a new stimulus will take increasingly
more time and effort. This neophobia increases until it inhibits exploration
tendencies by the end of the early socialisation period, around 12 weeks of
age (Table 2). In order to avoid fear responses to stimuli and consequent neg-
ative associations or trauma during this time, the exposure and intensity of
stimuli should be tightly controlled and increased gradually (Overall, 2013;
Rooney et al., 2016). Exposure of pups to various stimuli on video images as
early as three to five weeks of age has been shown to reduce fear responses
at 7–8 weeks of age (Pluijmakers et al., 2010). Gradual exposure results in
a moderately challenging environment for the pup, which has been shown to
promote resilience (Macrì & Würbel, 2006). Resilient dogs are better able to
cope with new challenges in the future.
3.1.1. Intraspecific socialisation and play
The sensory and cognitive development at three weeks of age allows for
the formation of social relationships (Scott & Marston, 1950; Scott, 1962).
The primary social relationships are formed with the mother and littermates.
Through these relationships the pup learns to identify itself with its own
species, a process termed filial imprinting (Bolhuis 1991; Dehasse, 1994).
The process of imprinting has first been comprehensively described in geese
by Konrad Lorenz (1935). It is seen in many bird and mammal species, and
is defined as “the acquisition of a preference for a familiar object” (McCabe,
2013). During a sensitive time period a young animal acquires a preference
for the mother or caregiver, as this is, from a functional perspective of sur-
viving, the most relevant ‘object’ in their environment.
In humans, the primary social relationships are also formed during the
early socialisation period, with one major difference compared to dogs. In
dogs, the neonatal period is followed by a transitional period in which the
pup rapidly matures, and consequently a pup enters the early socialisation
period in a relatively physically mature state. Since the pups are not fully
dependent on their mother at this time, the mother dog frequently leaves the
nest for brief periods of time, and as a consequence the strongest primary
16 Behaviour (2018) DOI:10.1163/1568539X-00003486
social relationships in dogs are formed with the littermates (Scott, 1963).
This promotes the characteristic pack forming in most canids. By contrast,
in humans the neonatal period is directly followed by a sensitive period
for socialisation, thus before the transitional period of maturation. Conse-
quently, the human infant is highly dependent on its caregiver — usually
the mother — during the early socialisation period, and the strongest social
relationship is formed with this person (Scott, 1963).
Fox & Stelzner (1967) demonstrated the importance of social contact
with conspecifics during the early socialisation period for the appropriate
social development in dogs. Seventeen pups were reared under three different
conditions: hand-reared from birth to 3.5 weeks of age and then isolated
until 12 weeks (II-group), reared by the mother and then isolated from 3.5
to 12 weeks (CI-group), or reared by the mother and isolated from 8 to 12
weeks (CCI-group). At 12 weeks these pups underwent a series of behaviour
tests. Pups of the II-group showed the largest deficits in social development,
whereas the pups of the CCI-group behaved as expected of a dog, with no
apparent deficits. Pups of the CI-group showed a mixture of the behaviours,
with some showing deficits in social behaviour and others appearing normal.
The variation within this group could possibly be explained by individual
differences between pups and/or small group size (Scott & Fuller, 1965).
The results, however, not only emphasise the importance of social contact
during the early socialisation period, but also provide evidence for the role
of the mother dog in social development. When pups are between 5 and 7
weeks of age the mother gradually starts to wean her pups by walking away,
growling, baring her teeth, or biting softly (Rheingold, 1963; Wilsson, 1984),
introducing the pups to dominant and submissive social interactions. Also
through other social interactions apart from weaning, the mother dog will
discipline her pups, providing them with important information on social
behaviour (Case, 2005). Therefore, for a proper social development it is
crucial for pups to stay with their mother at least until natural weaning has
occurred, which is usually when the pups are around 7–9 weeks old (Wilsson,
1984; Case, 2005), but may differ among breeds.
Around the time pups acquire their social behavioural repertoire through
interactions with their mother, interactions with littermates also contribute to
the social, cognitive and physiological development of the pups. Intraspecific
communication is largely established during play-fights among littermates,
in which the pups alternately bite each other and learn to associate specific
L. Dietz et al. / Behaviour (2018) 17
vocalisations with pain (Dehasse, 1994; Case, 2005). Through these play-
fights, pups learn how to interpret and display signals, such as agonistic,
dominant, submissive and appeasement behaviours, as has been observed in
a group of free-ranging dogs (Pal, 2008). In addition, the play-fights help im-
prove the pups’ motor skills. In a study on a group of free-ranging domestic
dogs, play behaviour was first seen when pups were three weeks of age and
the occurrence of play behaviour gradually declined after eight to nine weeks
of age (Pal, 2008). Although the function of play in dogs is still a point of
discussion, the most supported theory indeed involves motor skill and social
development (Sommerville et al., 2017).
In rats, the inability to perform play behaviours during a sensitive pe-
riod in early life has been shown to reduce social activity (Hol et al., 1999).
Rats housed in isolation at four weeks of age, deprived of the opportunity
to play, displayed decreased social activity in adulthood. Similarly, the pro-
vision of specific play enrichments in 6–7-week-old dog pups elicited more
play opportunities, resulting in less fear and anxiety at the age of 1.5 years
compared to a control group with less opportunities for play in the period of
6 to 7 weeks (van Eijk et al., 2006, unpublished).
Restriction of contact with conspecifics as a pup during the eight weeks
following their first experience in public has been shown to be strongly asso-
ciated with the occurrence of aggressive behaviour (i.e., growling, snapping,
biting, or lunging at an unfamiliar dog) between one and three years of age
(Wormald et al., 2016). Surprisingly, in the same study, commencing pub-
lic social exposure at eight weeks of age was associated with higher odds
of aggressive behaviour as an adult compared to starting public exposure at
18 weeks. A potential explanation may be that pups starting social expo-
sure at eight weeks of age had a higher chance to have negative or traumatic
experiences (intense exposure causing a fear response). Therefore, social in-
teractions with unfamiliar conspecifics in the early weeks of life may better
be restricted to a safe and controlled domestic environment.
3.1.2. Interspecific socialisation
As pups form social relationships with their littermates (i.e., intraspecific
bond) they also become receptive to contact and social relationships with
humans (i.e., interspecific bond) (Scott, 1958). The importance of early hu-
man contact for the successful formation of dog-human bonds later in life
has been illustrated by Freedman et al. (1961). Freedman and colleagues di-
vided 34 Cocker spaniel and Beagle pups into groups which were socialised
18 Behaviour (2018) DOI:10.1163/1568539X-00003486
to humans at different ages (2, 3, 5, 7, or 9 weeks) or were not socialised at
all (control). At 15 weeks of age all dogs were subjected to three behaviour
tests and their performance in the tests was documented. In the handling
test, the attraction of a pup to the handler was scored. Pups socialised at 2
weeks and control pups scored significantly lower than pups socialised at 5,
7, or 9 weeks. The leash-control test was designed to test resistance to train-
ing walking on a leash. Again the pups socialised to humans at 5, 7 and 9
weeks scored significantly higher than the other groups. In the reactivity test
behavioural and physiological (heart rate, depth of respiration and muscle
tension) responses to aversive stimuli were scored. Pups socialised to humans
at 7 weeks scored significantly better than the controls. Overall, this group
performed best in all three tests, whereas the control group scored lowest in
all tests. Additionally, the control pups were extremely fearful and avoidant
towards humans. Despite the small number of pups per group, which renders
the results susceptible to the influence of individual differences, this study
suggests that pups should be exposed and introduced to humans at an early
age, during the sensitive early socialisation period (Battaglia, 2009), and ide-
ally between five and eight weeks of age (Scott, 1963; Overall, 2013).
In summary, similar to the perinatal period, the experiences gained dur-
ing the early socialisation period are likely to have long-term effects on a
behavioural and physiological level, and contribute to the dog’s (social) be-
haviour as an adult (Scott, 1962).
3.2. Late socialisation (12 weeks to 6 months)
The early or first socialisation period is followed by the late or second social-
isation phase (Table 2), also called juvenile period in the literature. The late
socialisation phase extends to approximately six months of age, when sex-
ual maturity is reached (Scott, 1958; Case, 2005; Wilsson, 2016). Although
considered less sensitive than the early socialisation period, the importance
of the juvenile and succeeding adolescence period for further behavioural
development has recently been discussed in rodents (Sachser et al., 2011;
Brydges, 2016). Juveniles require extensive stimulation during these phases
to reinforce their socialised state. This has been demonstrated by a study
with a group of future guide dogs (Pfaffenberger & Scott, 1959), which were
socialised to humans at the end of the early socialisation period, between 8
and 12 weeks. When the pups reached the age of 12 weeks, roughly half of
them were quickly rehomed while the other half remained in the kennels with
L. Dietz et al. / Behaviour (2018) 19
conspecifics for 2–11 weeks. The dogs that remained in the kennels received
no further reinforcement of socialisation to humans and the results of the
study showed that these dogs were more likely to fail as guide dogs, largely
due to fear and nervous behaviour. Also, a study on wolves emphasises the
complementary function of experiences during the early and late socialisa-
tion phase. Young wolves that were socialised to humans until three months
of age, but received no further reinforcement until 6 months of age, became
fearful of humans and the positive effects achieved during early socialisation
seemed to have disappeared. Wolf cubs that were reared and reinforced with
human contact until 6 months of age, thus during both the early and late so-
cialisation period, remained fearless of humans even without reinforcement
during a subsequent period of over a year (Woolpy & Ginsburg, 1967). In
line with these findings, dogs exposed to busy urban environments during
the late socialisation period (between three and six months of age) are less
likely to develop behavioural disorders in the form of avoidance behaviour
and aggression towards unfamiliar people later in life (Appleby et al., 2002).
These studies demonstrate the importance of the juvenile and adolescent pe-
riod, as the behavioural profile of an individual as it was shaped early in life
may be confirmed or adjusted during these periods, depending on the degree
to which the current environment matches the rearing environment (Sachser
et al., 2013; Groothuis & Taborsky, 2015).
4. Synthesis: plasticity and interactions
The reviewed literature so far confirms that the behaviour of an adult dog
is determined to a large extent by the quality of maternal care, its attach-
ment style to its mother, and the variety of both social and non-social stimuli
provided during the early and late socialisation period. Insufficient or inad-
equate stimulation during these periods may increase the risk of developing
behavioural disorders as an adult. Although the sensitive periods and mother-
pup relationship have been presented separately in this review, they interact
with each other in a complex manner, and in addition, these interactions are
also influenced by genetic variation (Scott & Fuller, 1965). Given the com-
plex interplay of genes and environment, the question can be raised: how
reversible or irreversible are the consequences of early life experiences?
The central nervous system remains plastic in adult life, keeping the ca-
pacity to modify neural connections based on the interactions with its en-
vironment (Kolb et al., 2008), although this capacity for adjustments is sub-
20 Behaviour (2018) DOI:10.1163/1568539X-00003486
stantially smaller than during the sensitive period for socialisation (Knudsen,
2004). Some studies suggest that behaviour can be altered by experiences
even later in life. For example, in rats that underwent early maternal separa-
tion, the increased neuroendocrine and behavioural stress responsivity could
be attenuated by social enrichment after weaning, although the physiologi-
cal changes in the hypothalamus caused by the early separation could not be
reversed (Francis et al., 2002). In monkeys, social contact after 7 months of
age in previously socially deprived animals appeared to have positive effects.
Mothers that had had some social contact with conspecifics during their de-
velopment, albeit late in development, appeared more likely to acquire an
adequate maternal care style compared to mothers that had been completely
socially deprived as an infant (Harlow et al., 1966). However, due to small
sample sizes and large individual variation these results remain suggestive.
Whereas some evidence exists for plasticity in behavioural development
in rodents (Champagne & Curley, 2005), literature on this matter in dogs
remains scarce and is largely anecdotal and based on small sample sizes. In
their influential book Genetics and the Social Behavior of the Dog,Scott
& Fuller (1965) anecdotally describe the case of one mixed breed dog that
was raised by humans, isolated from other dogs, and was introduced to
her littermates for the first time at the age of nine weeks. Initially the dog
appeared fearful, but the littermates showed “playful aggressiveness” and
the dog reacted to this. A few days later the effects of poor socialisation in
the first weeks of life were no longer apparent. Although the most sensitive
window for filial imprinting had passed in this nine week old pup, the early
socialisation period extends to twelve weeks, and it has even been suggested
that sensitive periods may be prolonged under suboptimal circumstances
lacking stimulation (Knudsen, 2004). Scott & Fuller (1965) further describe
a group of Beagles that were kept in complete isolation from birth until 16
weeks of age, and thereafter were introduced to unfamiliar conspecifics for
the first time. The isolated individuals were repeatedly attacked by the other
dogs and seemed unable to develop social relationships. When researchers
held play sessions with the isolated dogs, mimicking play-fights, they did
manage to elicit play behaviour and after a few days the isolated dogs would
respond to the researchers as properly socialised individuals would (Fuller,
1961; in Scott & Fuller, 1965). Besides the possibility of some plasticity in
the social behaviour, this study also underlines the importance of play during
the sensitive period for socialisation.
L. Dietz et al. / Behaviour (2018) 21
Figure 1. Graphical model of factors contributing to an adult dogs’ behavioural profile.
In the previous sections we have emphasised the importance of both the
early and late socialisation period for a proper behavioural development in
dogs. It is clear that interactions between the early and late socialisation pe-
riod influence the behaviour of these dogs. A poor start in life may be partly
compensated by enrichment and proper stimulation later in life, whereas an
optimal early environment may be counteracted by later poor experiences.
Unfortunately, we cannot derive from the few available anecdotal examples
whether counteracting effects of experiences in the late socialisation phase
persist throughout adult life. Here, we assume that the adult behavioural pro-
file — including the vulnerability to develop behavioural disorders — is the
cumulative sum of experiences during the sensitive periods of early devel-
opment (Battaglia, 2009; Figure 1). Nevertheless, behavioural profiles may
22 Behaviour (2018) DOI:10.1163/1568539X-00003486
remain flexible to a certain degree even into adulthood, thus behavioural dis-
orders may remain treatable and/or reversible given appropriate training and
5. Implications
In this review we have summarised and analysed the existing literature on
mother-pup attachment and maternal care, early and late socialisation, inter-
actions between these essential components in the early development, and
their influence on the development of behaviour and behavioural disorders
in domestic dogs. In the following, we list some applied implications of
this scientific knowledge for dog breeders and other relevant parties. As we
identified major gaps in knowledge on this topic in dogs, we also suggest
opportunities for future research.
As discussed in this review, there is now a growing body of evidence that
negative or traumatic experiences and/or lack of stimuli in the early develop-
ment of dog pups may have negative long-term consequences on health and
behaviour (Table 3). Pups weaned at six weeks of age show higher morbid-
ity and mortality rates than pups weaned at twelve weeks (Slabbert & Rasa,
1993), and removal from the litter prior to eight weeks of age may cause
severe distress (Serpell & Jagoe, 1995) and heighten the risk of behavioural
disorders (Pierantoni et al., 2011). Rehoming pups at a later age, however,
may also facilitate the development of behavioural disorders. According to a
recent survey study, pups that were rehomed between 13 and 16 weeks of age
showed a higher prevalence of growling, snapping and avoidance behaviour
towards unfamiliar humans after one year of age, compared to pups rehomed
between six and eight weeks of age (Jokinen et al., 2017). Therefore, the
ideal moment to rehome dog pups may be a balance between biological
needs such as a sufficient period of maternal care, and appropriate sociali-
sation to the future environment. It should be noted that pups spend a large
part of the sensitive period for socialisation at their breeder, who therefore
has the prominent responsibility in the early socialisation process. Breeders
should be strongly advised to provide their pups with a sufficient stimulating
and variable environment, including social interactions with other dogs and
humans, while taking care not to overstimulate the pups (Battaglia, 2009;
Howell et al., 2015). A survey study with 48 Belgian dog breeders showed
that environmental enrichment with non-social stimuli was provided by only
L. Dietz et al. / Behaviour (2018) 23
Table 3.
Overview of reviewed literature in dogs that provides evidence for the influence of mater-
nal care and the early and late socialisation period on the development of behaviour and
behavioural disorders.
Early and late socialisation
Appleby et al. (2002) A stimulus-rich environment during the early and late
socialisation period is associated with a lower risk of
developing aggression towards strangers
Gazzano et al. (2008) Expert advice on raising a pup reduces the risk of
developing behavioural disorders
Gray et al. (2016) Pups from irresponsible breeders have a higher risk of
developing aggression
Wormald et al. (2016) Restriction of contact with conspecifics is associated
with aggressive behaviour as an adult
Starting public social exposure at 8 weeks is associated
with higher odds of aggressive behaviour as an adult
compared to starting public exposure at 18 weeks
Jokinen et al. (2017) Rehoming pups at 13 to 16 weeks of age is associated
with a higher prevalence of aggressive behaviour than
McMillan (2017) Pups from commercial breeders show more aggression
towards dogs and humans
Fear and anxiety
Maternal care
Pierantoni et al. (2011) Weaning at 30 to 40 days has a higher risk of
developing fearful behaviour than weaning at 60 days
Tiira & Lohi (2015) Poor maternal care quality is associated with more
fearful behaviour in the adult dog
Bray et al. (2017b) A ventral nursing style with easy nipple access is
associated with more anxiety
Early socialisation
Freedman et al. (1961) Isolation from humans until 14 weeks of age leads to
more fearfulness and avoidance towards humans
Appleby et al. (2002) A stimulus-rich environment during the early
socialisation period is associated with a lower risk of
developing fear towards strangers
Van Eijk et al. (2006)
Play enrichment in 6–7-week-old pups results in less
fear and anxiety as an adult
Pluijmakers et al. (2010) Exposure to various stimuli on video images reduces
fear responses in seven to 8-week-old pups
24 Behaviour (2018) DOI:10.1163/1568539X-00003486
Table 3.
Tiira & Lohi (2015) More socialisation experiences between 8 and 12
weeks of age reduces the risk of developing fear
McMillan (2017) Pups from commercial breeders show more aggression
towards dogs and humans
Late socialisation
Pfaffenberger & Scott (1959) Lack of reinforcement of socialisation to humans after
the early socialisation period increases the risk of
developing fear and nervous behaviour
Woolpy & Ginburg (1967) In wolves, lack of reinforcement of socialisation to
humans after 12 weeks of age leads to the development
of fear towards humans
Separation related behaviour
Early socialisation
Gray et al. (2016) Pups from irresponsible breeders have a higher risk of
developing separation related behavioural problems
Vaterlaws-Whiteside &
Hartmann (2017)
A socialisation program tailored to the pup’s
behavioural and physiological development of a pup
reduces the risk of separation related behaviour
a small percentage of the investigated breeders (De Meester et al., 2005).
Breeders with less than ten litters appeared to stimulate their pups with inan-
imate stimuli more than breeders with more than ten litters, although this
was still insufficient. In particular exposure to a large variety of unfamiliar
locations was seldom provided and is recommended by the authors. A sur-
vey with dog owners revealed that almost one-third of dog pups in the United
States and Canada are insufficiently exposed to other dogs and humans dur-
ing the sensitive period for socialisation (Cutler et al., 2017). Recently, a
socialisation program was developed tailored to the behavioural and phys-
iological development of a pup during the first six weeks of its life. The
program led to reduced separation related behaviour and general anxiety in
dogs at the age of eight months, and is therefore recommended for pet dog
breeders (Vaterlaws-Whiteside & Hartmann, 2017).
In The Netherlands, breeders are obligated by law to socialise dogs to
humans and conspecifics during the sensitive period for socialisation (Article
3.22, Wet Dieren, Besluit houders van dieren). However, imported dogs are
not protected by Dutch law, but by the law of their country of origin. The
largest puppy trade network in western Europe imports pups from Hungary
L. Dietz et al. / Behaviour (2018) 25
and Slovakia (Van Uhm, 2010; Four Paws, 2013). In the Act of Animal
Protection in Hungary no guidelines regarding dog breeding or socialisation
are mentioned (Zoltán, 2011) and Slovakia has no specific law protecting
dog rights (Global Animal Law Project). Alarmingly, the pup’s essential
behavioural needs and requirements during the socialisation period are often
not taken into consideration in puppy farms (Van Uhm, 2010; Four Paws,
Apart from breeders, veterinarians have an important responsibility in
ensuring the appropriate care of breeding dogs (Voith, 2009), as they are
usually the first to examine the mother and her just born pups (Howell et al.,
2015). Pups raised by owners who received expert advice, e.g., from veteri-
nary behaviourists, are less likely to develop behavioural disorders later in
life (Gazzano et al., 2008). Expert advice on dog behaviour and behavioural
development therefore appears to be effective in reducing the prevalence of
behavioural disorders in the pet dog population, and should be given to own-
ers in a pro-active manner. Ideally, this advice is based on sound scientific
findings, however, alarmingly little has been scientifically investigated re-
garding the early social development of dogs and the mother-pup attachment
bond in particular. Lacking in-depth knowledge on dog attachment formation
hampers the development of socialisation protocols and adequate advice to
breeders and potential dog owners, with serious consequences for the wel-
fare of dogs. Experts in this field univocally agree that more research on this
topic is needed, given its relevance for animal welfare and society. There-
fore, we have highlighted gaps in knowledge and proposed future research
avenues to further investigate what shapes a dog pup during its early life and
how to ensure good adaptive capacity and the fulfilment of essential needs.
The authors would like to thank the Koninklijke Hondenbescherming for
their funding and flexibility, and ir. Ineke van Herwijnen, dr. Bart Houx, dr.
Matthijs Schilder and the three reviewers for their comments on this review.
Ainsworth, M.D.S. (1978). Patterns of attachment: a psychological study of the strange situ-
ation. — Lawrence Erlbaum Associates, Hillsdale, NJ.
26 Behaviour (2018) DOI:10.1163/1568539X-00003486
Appleby, D.L., Bradshaw, J.W.S. & Casey, R.A. (2002). Relationship between aggressive and
avoidance behaviour by dogs and their experience in the first six months of life. — Vet.
Rec. 150: 434-438.
Bamberger, M. & Houpt, K.A. (2006). Signalment factors, comorbidity, and trends in behav-
ior diagnoses in dogs: 1,644 cases (1991–2001). — J. Am. Vet. Med. Ass. 229: 1591-1601.
Battaglia, C.L. (2009). Periods of early development and the effects of stimulation and social
experiences in the canine. — J. Vet. Behav. Clin. Appl. Res. 4: 203-210.
Beetz, A., Uvnäs-Moberg, K., Julius, H. & Kotrschal, K. (2012). Psychosocial and psy-
chophysiological effects of human-animal interactions: the possible role of oxytocin. —
Front. Psychol. 3: 234.
Blakemore, S.J. & Mills, K.L. (2014). Is adolescence a sensitive period for sociocultural
processing? — Annu. Rev. Psychol. 65: 187-207.
Bolhuis, J.J. (1991). Mechanisms of avian imprinting: a review. — Biol. Rev. 66: 303-345.
Bos, P.A. (2016). The endocrinology of human caregiving and its intergenerational transmis-
sion. — Dev. Psychopathol.: 1-29.
Bowlby, J. (1958). The nature of the child’s tie to his mother. — Int. J. Psycho-anal. 39: 350.
Bowlby, J. (1973). Attachment and loss, Vol. 2: separation: anxiety and anger. — Basic
Books, New York, NY.
Bowlby, J. (1982). Attachment and loss: retrospect and prospect. — Am. J. Orthopsychol. 52:
Bray, E.E., Sammel, M.D., Cheney, D.L., Serpell, J.A. & Seyfarth, R.M. (2017a). Character-
izing early maternal style in a population of guide dogs. — Front. Psychol. 8: 175.
Bray, E.E., Sammel, M.D., Cheney, D.L., Serpell, J.A. & Seyfarth, R.M. (2017b). Effects of
maternal investment, temperament, and cognition on guide dog success. — Proc. Natl.
Acad. Sci. USA 114: 9128-9133.
Bretherton, I. (1992). The origins of attachment theory: John Bowlby and Mary Ainsworth. —
Dev. Psychol. 28: 759.
Brydges, N.M. (2016). Pre-pubertal stress and brain development in rodents. — Curr. Opin.
Behav. Sci. 7: 8-14.
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P.M. & Meaney, M.J. (1998).
Maternal care during infancy regulates the development of neural systems mediating the
expression of fearfulness in the rat. — Proc. Natl. Acad. Sci. USA 95: 5335-5340.
Capitanio, J.P., Mendoza, S.P., Mason, W.A. & Maninger, N. (2005). Rearing environment
and hypothalamic-pituitary-adrenal regulation in young rhesus monkeys (Macaca mu-
latta). — Dev. Psychobiol. 46: 318-330.
Carter, C.S. (1998). Neuroendocrine perspectives on social attachment and love. — Psy-
choneuroendocrinology 23: 779-818.
Case, L.P. (2005). The dog: its behavior, nutrition and health, 2nd edn. — Blackwell, Oxford.
Champagne, F.A., Francis, D.D., Mar, A. & Meaney, M.J. (2003). Variations in maternal care
in the rat as a mediating influence for the effects of environment on development. — Phys.
Behav. 79: 359-371.
Champagne, F.A. & Curley, J.P. (2005). How social experiences influence the brain. — Curr.
Opin. Neurobiol. 15: 704-709.
L. Dietz et al. / Behaviour (2018) 27
Champagne, D.L., Bagot, R.C., van Hasselt, F., Ramakers, G., Meaney, M.J., De Kloet, E.R.,
Joëls, M. & Krugers, H. (2008). Maternal care and hippocampal plasticity: evidence for
experience-dependent structural plasticity, altered synaptic functioning, and differential
responsiveness to glucocorticoids and stress. — J. Neurosci. 28: 6037-6045.
Coppinger, R. & Coppinger, L. (2001). Dogs: a startling new understanding of canine origin,
behavior & evolution. — Simon and Schuster, New York, NY.
Cutler, J.H., Coe, J.B. & Niel, L. (2017). Puppy socialization practices of a sample of dog
owners from across Canada and the United States. — J. Am. Vet. Med. Ass. 251: 1415-
Czerwinski, V.H., Hynd, P.I., Smith, B.P. & Hazel, S.J. (2014). Maternal care differs between
litters of labradors: a pilot study. — J. Vet. Behav. Clin. Appl. Res. 9: e16-e17.
Czerwinski, V.H., Smith, B.P., Hynd, P.I. & Hazel, S.J. (2016). The influence of maternal
care on stress-related behaviors in domestic dogs: what can we learn from the rodent
literature? — J. Vet. Behav. Clin. Appl. Res. 14: 52-59.
De Kloet, E.R., Joëls, M. & Holsboer, F. (2005). Stress and the brain: from adaptation to
disease. — Nature Rev. Neurosci. 6: 463-475.
De Meester, R., Moons, C., van Bree, H. & Coopman, F. (2005). Critical evaluation of the
environment in Belgian dog breeding kennels during the puppies’ socialization period. —
Vlaams Diergeneesk. Tijdschr. 74: 364-374.
Dehasse, J. (1994). Sensory, emotional and social development of the young dog. — Bull.
Vet. Clin. Ethol. 2: 6-29.
Denenberg, S., Landsberg, G.M., Horwitz, D. & Seksel, K. (2005). A comparison of cases
referred to behaviorists in three different countries. — In: Current issues and research in
veterinary behavioral medicine, proceedings 5th IVBM. Purdue University Press, West
Lafayette, IN, p. 56-62.
Elliot, O. & Scott, J.P. (1961). The development of emotional distress reactions to separation,
in puppies. — J. Gen. Psychol. 99: 3-22.
Francis, D.D., Diorio, J., Plotsky, P.M. & Meaney, M.J. (2002). Environmental enrichment
reverses the effects of maternal separation on stress reactivity. — J. Neurosci. 22: 7840-
Freedman, D.G., King, J.A. & Elliot, O. (1961). Critical period in the social development of
dogs. — Science 133: 1016-1017.
FOUR PAWS International (2013). Puppy trade in Europe: research on the impact of ille-
gal businesses on the market, on consumers, on the one-health concept and on animal
welfare. Available online at http://www.vier-
Trade_in_Europe/REPORT_EUROPEAN_PUPPY_TRADE.pdf (accessed 22 February
Foyer, P., Wilsson, E. & Jensen, P. (2016). Levels of maternal care in dogs affect adult
offspring temperament. — Sci. Rep. 6: 19253.
Fox, M.W. (1971a). Integrative development of brain and behavior in the dog. — University
of Chicago Press, Chicago, IL, USA.
Fox, M.W. (1971b). Behaviour of wolves dogs and related canids. — Dogwise Publishing,
Wenatchee, WA.
28 Behaviour (2018) DOI:10.1163/1568539X-00003486
Fox, M.W. & Stelzner, D. (1966). Behavioural effects of differential early experience in the
dog. — Anim. Behav. 14: 273-281.
Fox, M.W. & Stelzner, D. (1967). The effects of early experience on the development of inter
and intraspecies social relationships in the dog. — Anim. Behav. 15: 377-386.
Fuller, J.L. (1961). Effects of experimental deprivation upon behavior in animals. — In: Proc.
3rd world cong. psychiatry. Montreal, p. 223-227.
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. Comp. Psychol.
115: 423.
Gazzano, A., Mariti, C., Alvares, S., Cozzi, A., Tognetti, R. & Sighieri, C. (2008). The pre-
vention of undesirable behaviors in dogs: effectiveness of veterinary behaviorists’ advice
given to puppy owners. — J. Vet. Behav. Clin. Appl. Res. 3: 125-133.
Global Animal Law Project. Available online at
national/slovakia/ (accessed 22 February 2018).
Goldsmith, H.H. & Alansky, J.A. (1987). Maternal and infant temperamental predictors of
attachment: a meta-analytic review. — J. Consult. Clin. Psychol. 55: 805.
Gray, R., Douglas, C., Butler, S. & Serpell, J. (2016). Do puppies from “puppy farms”
show more temperament and behavioural problems than if acquired from other sources
- using CBARQ to assess. — Presented at British Society of Animal Science “Annual
Conference”, Chester, UK.
Groothuis, T.G. & Taborsky, B. (2015). Introducing biological realism into the study of
developmental plasticity in behaviour. — Front. Zool. 12: S6.
Grossmann, K., Grossmann, K.E., Spangler, G., Suess, G. & Unzner, L. (1985). Maternal
sensitivity and newborns’ orientation responses as related to quality of attachment in
northern Germany. — Monogr. Soc. Res. Child Dev. 50: 233-256.
Guardini, G., Mariti, C., Bowen, J., Fatjó, J., Ruzzante, S., Martorell, A., Sighieri, C. &
Gazzano, A. (2016). Influence of morning maternal care on the behavioural responses
of 8-week-old beagle puppies to new environmental and social stimuli. — Appl. Anim.
Behav. Sci. 181: 137-144.
Gubernick, D.J. (1981). Parent and infant attachment in mammals. — In: Parental care in
mammals (Gubernick, D. & Klopfer, P., eds). Plenum, New York, NY, p. 243-305.
Handlin, L., Nilsson, A., Ejdebäck, M., Hydbring-Sandberg, E. & Uvnäs-Moberg, K. (2012).
Associations between the psychological characteristics of the human–dog relationship and
oxytocin and cortisol levels. — Anthrozoös 25: 215-228.
Harlow, H.F. & Harlow, M.K. (1965). The affectional systems. — In: Behavior of nonhuman
primates: modern research trends 2: 287-334.
Harlow, H.F. & Zimmermann, R.R. (1959). Affectional response in the infant monkey. —
Science 130: 421-432.
Harlow, H.F., Harlow, M.K., Dodsworth, R.O. & Arling, G.L. (1966). Maternal behavior of
rhesus monkeys deprived of mothering and peer associations in infancy. — Proc. Am.
Phil. Soc. 110: 58-66.
L. Dietz et al. / Behaviour (2018) 29
Harlow, H.F., Harlow, M.K. & Suomi, S.J. (1971). From thought to therapy. Lessons from a
primate laboratory. How investigation of the learning capability of rhesus monkeys has led
to the study of their behavioral abnormalities and rehabilitation. — Am. Sci. 59: 538-549.
HAS Hogeschool, Den Bosch & Faculteit Diergeneeskunde, Utrecht (2015). Feiten en cijfers
van de gezelschapsdierensector. Available online at (accessed
22 February 2018).
Hol, T., Van den Berg, C.L., Van Ree, J.M. & Spruijt, B.M. (1999). Isolation during the play
period in infancy decreases adult social interactions in rats. — Behav. Brain Res. 100:
Houpt, K.A. (2007). Genetics of canine behavior. — Acta Vet. Brno 76: 431-444.
Howell, T.J., King, T. & Bennett, P.C. (2015). Puppy parties and beyond: the role of early age
socialization practices on adult dog behavior. — Vet. Med. Res. Rep.: 6.
Jagoe, A. & Serpell, J. (1996). Owner characteristics and interactions and the prevalence of
canine behaviour problems. — Appl. Anim. Behav. Sci. 47: 31-42.
Jokinen, O., Appleby, D., Sandbacka-Saxén, S., Appleby, T. & Valros, A. (2017). Homing age
influences the prevalence of aggressive and avoidance-related behaviour in adult dogs. —
Appl. Anim. Behav. Sci. 195: 87-92.
Kaufman, C.I. & Rosenblum, L.A. (1967). The reaction to separation in infant monkeys:
anaclitic depression and conservation-withdrawal. — Psychosomat. Med. 29: 648-675.
Klinghammer, E. & Goodmann, P.A. (1987). Socialization and management of wolves in
captivity. — In: Man and wolf: advances, issues, and problems in captive wolf research
(Frank, H., ed.). Kluwer, Dordrecht, p. 31-61.
Knudsen, E.I. (2004). Sensitive periods in the development of the brain and behavior. —
J. Cogn. Neurosci. 16: 1412-1425.
Kolb, B., Gibb, R., Stuss, D., Winocur, G. & Robertson, I. (2008). Principles of neuroplas-
ticity and behaviour. — In: Cognitive neurorehabilitation, second edition: evidence and
application (Stuss, D., Winocur, G. & Robertson, I., eds). Cambridge University Press,
Cambridge, p. 6-21.
Lambert, K., Coe, J., Niel, L., Dewey, C. & Sargeant, J.M. (2015). A systematic review and
meta-analysis of the proportion of dogs surrendered for dog-related and owner-related
reasons. — Prev. Vet. Med. 118: 148-160.
Lindsay, S.R. (2013). Handbook of applied dog behavior and training, adaptation and learn-
ing. — Wiley, New York, NY.
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pear-
son, D., Plotsky, P.M. & Meaney, M.J. (1997). Maternal care, hippocampal glucocorticoid
receptors, and hypothalamic-pituitary-adrenal responses to stress. — Science 277: 1659-
Liu, D., Diorio, J., Day, J.C., Francis, D.D. & Meaney, M.J. (2000). Maternal care, hippocam-
pal synaptogenesis and cognitive development in rats. — Nature Neurosci. 3: 799-806.
Lorenz, K. (1935). Der Kumpan in der Umwelt des Vogels. — J. Ornithol. 83: 289-413.
Lupien, S.J., McEwen, B.S., Gunnar, M.R. & Heim, C. (2009). Effects of stress throughout
the lifespan on the brain, behaviour and cognition. — Nature Rev. Neurosci. 10: 434-445.
30 Behaviour (2018) DOI:10.1163/1568539X-00003486
Macrì, S. & Würbel, H. (2006). Developmental plasticity of HPA and fear responses in rats:
a critical review of the maternal mediation hypothesis. — Horm. Behav. 50: 667-680.
Main, M. & Solomon, J. (1990). Procedures for identifying infants as disorganised/disori-
ented during the Ainsworth Strange Situation. — In: Attachment in the preschool years:
theory, research, and intervention 1: 121-160.
Mariti, C., Carlone, B., Ricci, E., Sighieri, C. & Gazzano, A. (2014). Intraspecific attachment
in adult domestic dogs (Canis familiaris): preliminary results. — Appl. Anim. Behav. Sci.
152: 64-72.
McCabe, B.J. (2013). Imprinting. — Wiley Interdisc. Rev.: Cogn. Sci. 4: 375-390.
McMillan, F.D. (2017). Behavioral and psychological outcomes for dogs sold as puppies
through pet stores and/or born in commercial breeding establishments: current knowledge
and putative causes. — J. Vet. Behav. Clin. Appl. Res. 19: 14-26.
Meaney, M.J., Tannenbaum, B., Francis, D., Bhatnagar, S., Shanks, N., Viau, V., O’Donnell,
D. & Plotsky, P.M. (1994). Early environmental programming hypothalamic-pituitary-
adrenal responses to stress. — Semin. Neurosci. 6: 247-259.
Meaney, M.J., Aitken, D.H., Bodnoff, S.R., Iny, L.J., Tatarewicz, J.E. & Sapolsky, R.M.
(2013). Reprinted article: early postnatal handling alters glucocorticoid receptor concen-
trations in selected brain regions. — Behav. Neurosci. 125: 637-641.
Morrow, M., Ottobre, J., Ottobre, A., Neville, P., St-Pierre, N., Dreschel, N. & Pate, J.L.
(2015). Breed-dependent differences in the onset of fear-related avoidance behavior in
puppies. — J. Vet. Behav. Clin. Appl. Res. 10: 286-294.
Nagasawa, M., Shibata, Y., Yonezawa, A., Morita, T., Kanai, M., Mogi, K. & Kikusui, T.
(2014). The behavioral and endocrinological development of stress response in dogs. —
Dev. Psychobiol. 56: 726-733.
Nagasawa, M., Mitsui, S., En, S., Ohtani, N., Ohta, M., Sakuma, Y., Onaka, T., Mogi, K.
& Kikusui, T. (2015). Oxytocin-gaze positive loop and the coevolution of human-dog
bonds. — Science 348: 333-336.
Nelson, E.E. & Panksepp, J. (1998). Brain substrates of infant–mother attachment: contribu-
tions of opioids, oxytocin, and norepinephrine. — Neurosci. Biobehav. Rev. 22: 437-452.
Overall, K. (2013). Manual of clinical behavioral medicine for dogs and cats. — Elsevier
Health Sciences, Amsterdam.
Pal, S.K. (2005). Parental care in free-ranging dogs, Canis familiaris. — Appl. Anim. Behav.
Sci. 90: 31-47.
Pal, S.K. (2008). Maturation and development of social behaviour during early ontogeny in
free-ranging dog puppies in West Bengal, India. — Appl. Anim. Behav. Sci. 111: 95-107.
Palestrini, C., Previde, E.P., Spiezio, C. & Verga, M. (2005). Heart rate and behavioural
responses of dogs in the Ainsworth’s Strange Situation: a pilot study. — Appl. Anim.
Behav. Sci. 94: 75-88.
Pfaffenberger, C.J. & Scott, J.P. (1959). The relationship between delayed socialization and
trainability in guide dogs. — J. Gen. Psychol. 95: 145-155.
Pierantoni, L., Albertini, M. & Pirrone, F. (2011). Prevalence of owner-reported behaviours
in dogs separated from the litter at two different ages. — Vet. Rec. 169: 468.
L. Dietz et al. / Behaviour (2018) 31
Pluijmakers, J.J., Appleby, D.L.& Bradshaw, J.W. (2010). Exposure to video images between
3 and 5 weeks of age decreases neophobia in domestic dogs. — Appl. Anim. Behav. Sci.
126: 51-58.
Previde, E.P., Ghirardelli, G., Marshall-Pescini, S. & Valsecchi, P. (2009). Intraspecific at-
tachment in domestic puppies (Canis familiaris).—J.Vet.Behav.Clin.Appl.Res.4:
Rheingold, H.L. (1963). Maternal behavior in the dog. — In: Maternal behavior in mammals
(Rheingold, H.L., ed.). Wiley, New York, NY, p. 169-202.
Rilling, J.K. & Young, L.J. (2014). The biology of mammalian parenting and its effect on
offspring social development. — Science 345: 771-776.
Rincón-Cortés, M. & Sullivan, R.M. (2014). Early life trauma and attachment: immediate and
enduring effects on neurobehavioral and stress axis development. — Front. Endocrinol. 5:
Romero, T., Nagasawa, M., Mogi, K., Hasegawa, T. & Kikusui, T. (2014). Oxytocin promotes
social bonding in dogs. — Proc. Natl. Acad. Sci. USA 111: 9085-9090.
Rooney, N.J., Clark, C.C. & Casey, R.A. (2016). Minimizing fear and anxiety in working
dogs: a review. — J. Vet. Behav. Clin. Appl. Res. 16: 53-64.
Roth, T.L. & David Sweatt, J. (2011). Annual research review: epigenetic mechanisms and
environmental shaping of the brain during sensitive periods of development. — J. Child
Psychol. Psychiatr. 52: 398-408.
Sachser, N., Hennessy, M.B. & Kaiser, S. (2011). Adaptive modulation of behavioural profiles
by social stress during early phases of life and adolescence. — Neurosci. Biobehav. Rev.
35: 1518-1533.
Sachser, N., Kaiser, S. & Hennessy, M.B. (2013). Behavioural profiles are shaped by social
experience: when, how and why. — Phil. Trans. Roy. Soc. Lond. B: Biol. Sci. 368:
Sanchez, M.M., Ladd, C.O. & Plotsky, P.M. (2001). Early adverse experience as a develop-
mental risk factor for later psychopathology: evidence from rodent and primate models. —
Dev. Psychopathol. 13: 419-449.
Sapolsky, R.M. & Meaney, M.J. (1986). Maturation of the adrenocortical stress response:
neuroendocrine control mechanisms and the stress hyporesponsive period. — Brain Res.
Rev. 11: 65-76.
Schöberl, I., Beetz, A., Solomon, J., Wedl, M., Gee, N. & Kotrschal, K. (2016). Social factors
influencing cortisol modulation in dogs during a strange situation procedure. — J. Vet.
Behav. Clin. Appl. Res. 11: 77-85.
Scott, J.P. (1958). Critical periods in the development of social behavior in puppies. —
Psychosom. Med. 20: 42-54.
Scott, J.P. (1962). Critical periods in behavioral development. — Science 138: 949-958.
Scott, J.P. (1963). The process of primary socialization in canine and human infants. —
Monogr. Soc. Res. Child Dev. 28: 1-47.
Scott, J.P. & Fuller, J.L. (1965). Genetics and the social behavior of the dog. — University of
Chicago Press, Chicago, IL.
32 Behaviour (2018) DOI:10.1163/1568539X-00003486
Scott, J.P. & Marston, M.V. (1950). Critical periods affecting the development of normal
and mal-adjustive social behavior of puppies. — Pedagogic. Semin. J. Gen. Psychol. 77:
Serpell, J. & Jagoe, J.A. (1995). Early experience and the development of behaviour. — In:
The domestic dog: its evolution, behaviour and interactions with people (Serpell, J., ed.).
Cambridge University Press, Cambridge, p. 79-102.
Slabbert, J.M. & Rasa, O.A. (1993). The effect of early separation from the mother on pups
in bonding to humans and pup health. — J. S. Afr. Vet. Ass. 64: 4-8.
Solomon, J., Beetz, A., Schoeberl, I., McCune, S. & Kortrschal, K. (2014). Attachment
classification in pet dogs: application of Ainsworth’s Strange Situation and classifica-
tion procedures to dogs and their human caregivers. — Presented at Int. Soc. Antrozool.
(ISAZ) Annual Meeting, Vienna, Austria, July 17-21, 2014.
Tiira, K. & Lohi, H. (2015). Early life experiences and exercise associate with canine anxi-
eties. — PLoS ONE 10: e0141907.
Topál, J., Miklósi, Á., Csányi, V. & Dóka, A. (1998). Attachment behavior in dogs (Canis
familiaris): a new application of Ainsworth’s (1969) Strange Situation test. — J. Comp.
Psychol. 112: 219.
Udell, M.A., Dorey, N.R. & Wynne, C.D. (2010). What did domestication do to dogs? A new
account of dogs’ sensitivity to human actions. — Biol. Rev. 85: 327-345.
Van Uhm, D.P. (2010). De puppydossiers: een koppeling tussen theorie en praktijk. Available
online at
%20Puppydossiers.pdf (accessed 24 February 2018).
Vaterlaws-Whiteside, H. & Hartmann, A. (2017). Improving puppy behavior using a new
standardized socialization program. — Appl. Anim. Behav. Sci. 197: 55-61.
Voith, V.L. (2009). The impact of companion animal problems on society and the role of
veterinarians. — Vet. Clin. N. Am. Small Anim. Pract. 39: 327-345.
Weaver, I.C. (2009). Shaping adult phenotypes through early life environments. — Birth Def.
Res. C: Embryo Today: Rev. 87: 314-326.
Wilsson, E. (1984). The social interaction between mother and offspring during weaning
in German shepherd dogs: individual differences between mothers and their effects on
offspring. — Appl. Anim. Behav. Sci. 13: 101-112.
Wilsson, E. (2016). Nature and nurture—how different conditions affect the behavior of
dogs. — J. Vet. Behav. Clin. Appl. Res. 16: 45-52.
Woolpy, J.H. & Ginsburg, B.E. (1967). Wolf socialization: a study of temperament in a wild
social species. — Am. Zool. 7: 357-363.
Wormald, D., Lawrence, A.J., Carter, G. & Fisher, A.D. (2016). Analysis of correlations
between early social exposure and reported aggression in the dog. — J. Vet. Behav. Clin.
Appl. Res. 15: 31-36.
Zoltán, T.J. (2011). The regulation of animal protection in Hungary. — Dny práva 2011–Days
of Law 2011: 190. Available online at
2011/files/prispevky/03%20ZVIRE/Toth_Zoltan.pdf (accessed 22 February 2018).
... The domestic dog has been used for decades as experimental models in studies of neuroscience, cognition, evolutionary genetics, and diseases such as neurological and psychiatric disorders (Adams et al., 2000;Wang et al., 2013;Bunford et al., 2017;Liu et al., 2018;Cao et al., 2021). In particular, dogs are considered effective models for studying social behaviors and mental disorders caused by adverse early life experiences (Berns and Cook, 2016;Ogata, 2016;Bunford et al., 2017;Dietz et al., 2018). ...
... First, 3-7 weeks of age of dogs is a critical period for socialization with human beings (Freedman et al., 1961;Scott, 1963). Dog pups separated from the mother at 30 to 40 days during the critical period were more likely to develop a variety of behavioral problems, including fearfulness, noise sensitivity, and excessive barking at later ages (Sargisson, 2014;Dietz et al., 2018). Thus, when dogs experienced SI starting at 2 months of age, their social development was mostly completed. ...
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Social isolation (SI) exerts diverse adverse effects on brain structure and function in humans. To gain an insight into the mechanisms underlying these effects, we conducted a systematic analysis of multiple brain regions from socially isolated and group-housed dogs, whose brain and behavior are similar to humans. Our transcriptomic analysis revealed reduced expression of myelin-related genes specifically in the white matter of prefrontal cortex (PFC) after SI during the juvenile stage. Despite these gene expression changes, myelin fiber organization in PFC remained unchanged. Surprisingly, we observed more mature oligodendrocytes and thicker myelin bundles in the somatosensory parietal cortex in socially isolated dogs, which may be linked to an increased expression of ADORA2A, a gene known to promote oligodendrocyte maturation. Additionally, we found a reduced expression of blood-brain barrier (BBB) structural components Aquaporin-4, Occludin, and Claudin1 in both PFC and parietal cortices, indicating BBB disruption after SI. In agreement with BBB disruption, myelin-related sphingolipids were increased in cerebrospinal fluid in the socially isolated group. These unexpected findings show that SI induces distinct alterations in oligodendrocyte development and shared disruption in BBB integrity in different cortices, demonstrating the value of dogs as a complementary animal model to uncover molecular mechanisms underlying SI-induced brain dysfunction.
... Caregiver adversity studies have not been restricted to NHPs. Experimental studies in domestic dogs and domestic pigs demonstrated that maternal separation and/or early weaning resulted in abnormal later life immune function and stress responsivity, and more physical health and social behavior problems later in life (Gimsa et al., 2022;Pohl et al., 2017;Buttner et al., 2023;Fox and Stelzner, 1966;Dietz et al., 2018;Bruckmann et al., 2020). In contrast, one study in wolves (Canis lupus) found that pups reared without their mothers in a variety of ways displayed species-typical behaviors when assessed during adolescence (Mac Donald and Ginsburg, 1981). ...
Social nonhuman animals are powerful models for studying underlying factors related to lifelong health outcomes following early life adversities (ELAs). ELAs can be linked to lifelong health outcomes depending on the species, system, sensitive developmental periods, and biological pathways. This review focuses on the literature surrounding ELAs and lifelong health outcomes in large, social, relatively long-lived nonhuman mammals including nonhuman primates, canids, hyenas, elephants, ungulates, and cetaceans. These mammals, like humans but unlike the most-studied rodent models, have longer life histories, complex social structures, larger brains, and comparable stress and reproductive physiology. Collectively, these features make them compelling models for comparative aging research. We review studies of caregiver, social, and ecological ELAs, often in tandem, in these mammals. We consider experimental and observational studies and what each has contributed to our knowledge of health across the lifespan. We demonstrate the continued and expanded need for comparative research to inform about the social determinants of health and aging in both humans and nonhuman animals.
... Broom and Leaver [19] state that the increased complexity of the early-life environment improves the individual's behavioural flexibility and ability to respond suitably in novel situations. This is supported by research in a range of species (e.g., calves: [52], dogs: [53], humans: [54], quail: [5]). The animal welfare and productivity implications of promoting behavioural plasticity in dairy cattle may include an improved ability to adapt to the milking herd and novelty of the milking environment and equipment, including robotic milking systems and pasture-based systems, which may also improve adaptability to rotational grazing. ...
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This study aimed to determine the effects of early-life physical and social enrichment on the ability of dairy heifers to integrate into a herd of mature cows. Fifty heifer calves were reared from the ages of 2–13 weeks in one of three treatments: (1) Hand-reared and group-housed in sheds (CC); (2) Hand-reared and group-housed at pasture (−S); or (3) Hand-reared and group-housed at pasture, with 3 non-familial dry cows per group (+S). At 23 months of age, these heifers were introduced in groups to small herds of cows (Cows) at pasture. Social interactions were recorded continuously for two 1-h periods. Feeding, ruminating and resting behaviours of all animals and walking, standing and lying behaviours of 36 heifers only (+S = 14, −S = 13, CC = 9) were recorded for 48 h after mixing. Heifers that were managed as calves according to the CC treatment delivered less agonistic behaviour to other heifers after mixing than those reared in the +S or −S treatments (p = 0.002 and p = 0.041, respectively). On Day 2, +S heifers and cows spent the lowest proportion of time feeding (p = 0.961), with −S heifers spending significantly more time feeding than cows (p = 0.046), while CC heifers spent more time feeding than both +S heifers and cows (p = 0.027 and p < 0.002, respectively). Increasing the complexity of the early-life environment, particularly socially, may aid heifers in integrating into groups of multiparous cows later in life and shape their lifelong social experiences with same-age conspecifics.
... Dogs who have lived in adverse and impoverished conditions can offer further insight into the role of the environment in developing attachment bonds with humans, particularly how exposure to chronic stress and a lack of socialization with humans alter the stress response. Early experimental studies established that dogs that experienced confinement, stress, and social deprivation during critical phases of development displayed behavioral abnormalities as adults, particularly fear and timidity (e.g., Beerda et al., 2000;Fox & Stelzner, 1966;Scott & Fuller, 1965; for reviews, see Dietz et al., 2018;Serpell & Jagoe, 1995). More recently, research has shown that dogs obtained from adverse or impoverished conditions, such as large commercial breeding operations that provide substandard care (often referred to as puppy mills; McMillan et al., 2011), pet stores (McMillan et al., 2013, and hoarding situations (individuals who keep large number of animals in their home under unsanitary conditions; McMillan et al., 2016) also display increased levels of social and nonsocial fear, among many other behavioral differences (for a review see McMillan, 2017). ...
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Although owners can act as stress buffers for their dogs, whether dogs with poor early life histories with humans will respond similarly is unknown. We tested 45 dogs, 23 of which were rescued from adverse conditions, in a social paradigm in which a threatening stranger confronted them with either their owner or an unfamiliar human present. Salivary cortisol levels were assessed at three points, and the dogs' behavior and owners' responses to questionnaires were evaluated. Dogs from adverse backgrounds engaged in greater contact and exhibited more relaxed behaviors and social referencing when their owners were present. Dogs from the comparison group explored more when accompanied by their owners. Dogs from adverse backgrounds experienced greater decreases in cortisol levels from the first to third samples relative to dogs in the comparison group. Dogs from adverse backgrounds were also more likely to respond fearfully to a threatening stranger. Their owners rated them as having higher levels of stranger-directed fear, nonsocial fear, separation-related problems, attention seeking, and lower levels of chasing and trainability. These findings from this study suggest that early adverse environments may have lasting effects on dogs' social behavior.
... Pearson Chi-square values are indicated for significant differences in pairwise comparisons between the two time frames, per factor (P<0.05, df = 1). merits further studying as aggression in dogs has a hereditary component [26,29], next to the crucial role of for instance the mother dog-offspring bond, socialisation and general early-life experiences [27,28,34,35] as well as the experience of being involved in a biting incidents as a dog, which was seen to associate with dogs becoming 'biting dogs' in the future [8]. The finding of relatively high prevalence of the factors of roaming and care task transfer may also indicate a mismatch between care demands and capacities. ...
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To examine the dog ownership factors characteristic to a population of dogs confiscated after a human and/ or animal-directed biting incident, we compared bite risk assessment reports of 159 confiscated dogs in the time frame 2008, 2009, 2010 (tf1) and of 215 confiscated dogs in the time frame 2020, 2021, 2022 (until mid-May; tf2). The reports were compiled by the same institute in a standardized format. We studied frequencies and chi-square pairwise comparisons (P<0.05) for 30 identified ownership factors. Overall (tf1 and tf2), 1,308 ownership factors were mentioned in the reports and reports mentioning ≥5 factors were twice as frequent in tf2 (38%) than tf1 (16%). Our data suggest that nine factors may in particular serve as a warning signal for biting incidents, as these factors were most frequently (≥15%) prevalent in the total of reported cases: having a multiple dog household, a dog reportedly roaming a neighbourhood without an owner, a dog's care tasks being transferred, a short leash and muzzle obligation served to the owner for a dog, an isolated and/ or confined keeping of a dog, a dog owner's (suspected) substance abuse, a dog owner's (suspected) animal abuse, a dog owner aggressing at confiscation of the dog and a dog owner being reported on for antisocial behaviours such as intimidation. Particularly, a dog owner's aggressive or antisocial behaviours and previous obligations to muzzle and short leash a dog (in our dataset often inappropriately adhered to by owners), may indicate that a proportion of owners of confiscated dogs, may not always be willing and/ or capable to guarantee societal safety. The results show that identification of dog ownership factors, might be useful for establishing biting incident policies and further studies should be done on preventive measures and controls.
... Finally, this study had some limitations, primarily because it was carried out in a working CBE. Each dog's previous experiences (e.g., the amount and type of socialisation they had during early life) could have influenced their behavioural response in the testing arena (Dietz et al., 2018). A previous study found that both periparturient and early maternal behaviour differed between CBE dams that were born and reared within that particular CBE and mothers brought in after 6 months of age. ...
Background: Separation-related behavior problems (SRPs) are among the most common canine behavior problems, attributed to fear, anxiety, over-attachment, and lack of appropriate stimulation. The aim of the study was to find the underlying cause of SRPs and create an intervention to eliminate the stressor, taking into consideration the Indian context. Materials and Methods: The study was conducted spanning over 100 pets and pet parents residing in Mumbai, India. Other stakeholder groups included were veterinarians, canine behaviorists, breeders, and boarding houses. An online survey, empathy interviews, and a camera study gave a holistic understanding of the ecosystem. The proposed solution was tested with 15 pets and pet parents through moderated user testing sessions. Results: It was found that 40% of pet dogs were brought home to pacify the demand of one’s child or loneliness, corresponding with the population of dogs that displayed SRPs. About 71% pet parents fed into the illegal breeding market, highlighting the lack of awareness about animal welfare. The study indicates that the underlying cause of SRPs is anthropomorphism of dogs and their exploitation for commercial benefit. Thus, pet parents need to change this anthropomorphic perception to remedy the ailment. The proposed solution, PawPal, helps pet parents orient their pets to the human world. The two-part solution includes wearables for the dog that capture its emotional state and an app enabling pet parents to reinforce positive behaviors in the pet. PawPal acts as a bridge to the communication gap and tackles the illegal breeding ecosystem. The solution was well received by stakeholders and field experts. Conclusion: PawPal addresses the root cause of SRPs, thereby successfully remedying the ailment. Pet parents will be able to make mindful decisions concerning their pets, thus elevating the quality of life of dogs.KeywordSeparation-related behavior disordersPet careAnimal welfareDog socializationBehavioral developmentCanine care
Remote testing has been exploited in software development for several years. Until recently, virtual support in the design of physical tools and appliances has received much less attention. The years of pandemic travel restriction have created a completely novel set of requirements for usability testing, whereby the physical interaction between the experimenter and the end user has been no longer possible. In this frame, the host of new communication platforms that became available provided means for innovative protocols of remote synchronous interaction. Here, we successfully apply them for the testing of medical devices in the user-centered design development. The proposed protocol is validated along the development of a medical applicator tool, the SYMPLX, designed for the use in the operating room by cardiologists and cardiothoracic surgeons (the end users). The applicator is aimed at facilitating the combination of a protective pouch made of biosynthesized cellulose, the Hylomate, and a target pacemaker or defibrillator upon their implantation in cardiovascular patients. The testing with end user rendered a number of videos featuring a reproduced model of the operating room, where the clinical procedure was performed with the use of SYMPLX. The ensuing analysis extracted four quantitative descriptors of the performance, with sufficient reliability and reproducibility to evaluate design improvements, as well as user-related variability and learning process. Altogether, we describe and validate a new flexible and cost-effective protocol that can support the remote design of medical devices and has the potential to be optimized for other physical tools.KeywordsRemote usability test setupRemote usability testingRemote operating tableUser-centered design developmentUser-centered industrial design approachMedical product design developmentMedical designSurgical applicator
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Personality in pets and other domesticated animals is important for their well-being and it can also influence human-animal relationships. Genetic and environmental factors influencing unwanted behavior in dogs are somewhat well known, but the factors influencing dog personality remain understudied. Here we examined environmental and demographic factors associated with seven broad personality traits in a survey of over 11,000 dogs. We utilized linear models and extensive model validation to examine the factors that have the most significant influences on personality and calculated effect sizes to assess the importance of these variables. Breed and age had the strongest associations with dog personality traits. Some environmental factors, especially puppyhood socialization, were also associated with personality. All factors had small effect sizes, highlighting that a lot of variation in personality remains unexplained. Our results indicate that personality traits are complex and strikingly similar in dogs, humans, and other nonhuman animals.
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Studies identifying the underlying determinants of adult dog behavior and highlighting successful methods of early intervention are essential to reduce and ultimately prevent problem behaviors developing. The aim of this research was to create and assess the impact of a new nest socialization program. The new program was designed to: 1) provide a highly effective socialization experience, 2) be quick and easy to complete and 3) utilize low cost materials. The program was created by combining existing nest stimulation theories with young puppy developmental stages. As such the introduction and intensity of each socialization stimulus was tailored to mirror puppy physiological and behavioral development from birth to six weeks of age. The new socialization program was evaluated using six litters raised under standardized conditions. The impact of the program was measured using a practical puppy behavioral assessment at six weeks of age and an eight-month dog handler behavioral questionnaire.Results showed a significant positive effect of the new socialization program on puppy behavioral development, which persisted throughout the first year of life. Puppies that received the program had more favorable scores in a six-week practical assessment (P ≪ 0.01) and an eight-month dog handler questionnaire for separation-related behavior (P ≪ 0.01), distraction (P ≪ 0.01), general anxiety (P = 0.02) and body sensitivity (P = 0.03). This is the first socialization program tailored to the developmental stage of puppies from birth to six weeks of age to demonstrate measurable, long-term effects on individual dog behavioral traits. Results will be of interest to working and assistance dog organizations, animal shelters and pet dog breeders.
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Significance A successful guide dog must navigate a complex world, avoid distractions, and respond adaptively to unpredictable events. What leads to success? We followed 98 puppies from birth to adulthood. Puppies were enrolled in a training program where only ∼70% achieved success as guide dogs. More intense mothering early in life was associated with program failure. In addition, mothers whose nursing style required greater effort by puppies produced more successful offspring. Among young adult dogs, poor problem-solving abilities, perseveration, and apparently greater anxiety when confronted with a novel object were also associated with program failure. Results mirror the results from rodents and humans, reaffirming the enduring effects on adult behavior of maternal style and individual differences in temperament and cognition.
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In both humans and non-humans, differences in maternal style during the first few weeks of life can be reliably characterized, and these differences affect offspring's temperament and cognition in later life. Drawing on the breeding population of dogs at The Seeing Eye, a guide dog school in Morristown, New Jersey, we conducted videotaped focal follows on 21 mothers and their litters (n = 138 puppies) over the first 3 weeks of the puppies' lives in an effort to characterize maternal style. We found that a mother's attitude and actions toward her offspring varied naturally between individuals, and that these variations could be summarized by a single principal component, which we described as Maternal behavior. This component was stable across weeks, associated with breed, litter size, and parity, but not redundant with these attributes. Furthermore, this component was significantly associated with an independent experimental measure of maternal behavior, and with maternal stress as measured by salivary cortisol. In summary, Maternal behavior captured a significant proportion of the variation in maternal style; was stable over time; and had both discriminant and predictive validity.
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A review of seven published studies and one anecdotal report involving dogs born in high-volume commercial breeding establishments (CBE) and sold to the consumer directly via the Internet or indirectly through retail pet stores revealed an increased incidence of behavioral and emotional problems that cause distress in adulthood compared with dogs from other sources, especially breeders. The most consistent finding among studies is an increase in aggression, which is most commonly directed toward the dog’s owners and family members but also to unfamiliar people, and other dogs. Increased fear was also identified in response to unfamiliar people, children, other dogs, nonsocial stimuli, and when taken on walks. Undesirable behaviors related to separation and/or attention-seeking and a heightened sensitivity to touch have been reported.
OBJECTIVE To identify actions taken by owners to socialize puppies < 20 weeks of age, to determine factors affecting attendance of structured puppy classes, and to examine associations between class attendance and owner response to various undesirable puppy behaviors. DESIGN Cross-sectional study. SAMPLE 296 puppy owners (each with 1 puppy). PROCEDURES Participants completed a survey at enrollment (to gather data regarding owner demographics and puppy characteristics) and again when puppies were 20 weeks of age (to gather information on socialization practices and owner responses to misbehavior and signs of fear in their puppy). Responses were compared between owners that did (attendees) and did not (nonattendees) report attending puppy classes. RESULTS 145 (49.0%) respondents reported attending puppy classes. Class structure differed greatly among respondents. Attendees exposed their puppies to a greater number of people and other dogs than nonattendees as well as to various noises and situations. Puppies of attendees were less likely than puppies of nonattendees to have signs of fear in response to noises such as thunder and vacuum cleaners as well as to crates. Fewer attendees reported use of punishment-based discipline techniques than did nonattendees. Almost one-third of puppies received only minimal exposure to people and dogs outside the home during the survey period. CONCLUSIONS AND CLINICAL RELEVANCE A notable number of puppies < 20 weeks of age in this study received few early socialization opportunities, which could lead to behavior problems and subsequent relinquishment. Opportunities exist for veterinarians to serve an important role in educating puppy owners about the importance of early puppy socialization and positive reward training.
Homing puppies before 8 weeks has been associated with lower instance of avoidance and types of aggression in adult dogs. The current study aimed to further assess the impact of homing age on these behaviours in adult dogs. Finnish dogs provide an interesting population for this further study, as based on the clinical experience of the co-authors, puppies in Finland are predominantly reared in domestic maternal environments before first homing, which was not the case in the countries where previous studies have been performed. Online questionnaire-based data on frequencies of problematic behaviours (n = 3689) were analysed using Chi-Square, comparing adult dogs homed at 6-7 weeks (6-7), 8 weeks (8), 9-12 weeks (9-12) and 13-16 weeks (13-16). 31% were 6-7, 41% 8, 23% 9-12, 5% 13-16. If an overall association was observed, pairwise comparisons between homing age groups were conducted. All of the dogs included in the study came from domestic maternal environments, where the puppies were kept in the breeders' living quarters. Homing age was associated with avoiding, growling and snapping at unfamiliar people when away from the home environment (p = 0.004, p = 0.02 and p = 0.008, respectively); avoiding, barking at, growling at and snapping at unfamiliar people visiting the home (p = 0.02, p = 0.02, p = 0.04 and p = 0.03, respectively) and barking at unfamiliar dogs when away from the home environment (p = 0.001). With one exception, dogs homed later than 8 weeks, namely during weeks 9-12 and 13-16, had higher than expected prevalence of avoidance and aggressive behaviour than dogs homed at other ages. The exception being that for the measure, barking at unfamiliar dogs away from the home environment, there were higher than expected values in dogs homed at 8 and 13-16 weeks and lower in dogs homed at 6-7 and 9-12weeks. This research supports the view that homing age is associated with instances of avoidance behaviour and some types of aggression in adult dogs.
Temperament tests for working dogs can provide substantial information about a particular dog's behavioral phenotype. When a larger proportion of the population is tested, the test results can also provide information about the effects of different environmental conditions on the phenotype because if the population is large, the social and physical environments to which the dogs are exposed differ. This means that we need to include in our evaluations the perspective that uses information about the environment in relation to the individual dog's level of development. There is substantial evidence that basic temperament traits in dogs are moderately heritable. There is also evidence that postweaning conditions have a huge effect on development, and this effect is often not assayed. Selective breeding for desired traits in combination with optimal environmental conditions, adapted to the individual dog's level of maturation, is a key point when producing outstanding working dogs.