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Behaviour (2018) DOI:10.1163/1568539X-00003486 brill.com/beh
Review
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: l.dietz@uu.nl
Received 12 January 2018; initial decision 19 February 2018; revised 19 March 2018;
accepted 20 March 2018
Abstract
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.
Keywords
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-
tions.
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-
ers.
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
disorders.
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-
ships.
Maternal caregiving in humans1,2 Attachment styles and behaviours as described in
humans2,3 and dogs4,5,6
Secure
Sensitive, responsive1,2 Secure2,4 Proximity to caregiver2,4,5,6
Distress during separation2,5,6
Low interest in strangers2,5,6
Insecure
Insensitive, unresponsive1,2 Anxious-ambivalent2High distress during
or ambivalent4separation2,4
Difficult to comfort upon
reunion2,4
Seek constant reassurance
and proximity2
Avoidant2,4 No separation distress2
Ignore caregiver2,4
Similar towards stranger2
Disorganised3,4 Disoriented behaviours3
Confused3
Approach-avoidance conflict
on reunion4
Note that the influence of maternal care on attachment styles in dogs has not yet been
studied.
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
assumption.
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).
Neonatal
(0–2 weeks)
Transitional
(2–3 weeks)
Early socialisation Late
socialisation
(12 weeks–
6 months)
Adolescence
(6 months–
1 year)
3–5 weeks 5–8 weeks 8–12 weeks
Vision and
hearing
underdeveloped
Opening of
eyes and ears
Brain maturation
and myelination
Brain maturation
and myelination
Myelinated
nerves
Sexual maturation Sexual maturity
Poor locomotory
skills
Increased
locomotor
activity
Sensitive to
novelty in
environment
Sensitive to
novelty in
environment
Adult EEG
waves
Reinforcement of
socialisation
SHRP Weaning
Immature brain Immature brain Exploratory
behaviour
Peak sensitivity
to human contact
Care seeking
behaviour
Care seeking
behaviour
Increasing fear of
novelty
Increasing fear
of novelty
Decreasing
exploration
Decreasing
exploration
Play with mother Play with mother
Play with
littermates
Play with
littermates
Play with
littermates
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
interventions.
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.
Aggression
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
rehomingat6to8weeksofage
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)
(unpublished)
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.
(Continued.)
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,
2013).
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.
Acknowledgements
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.
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