Maternal behaviour in domestic dogs

Abstract

Mammalian parental care, in most of the cases, is given by the female, who provides food, warmth, and protection. In domestic dogs, maternal behaviour shown by the dam mainly consists of contact, nursing, grooming/licking, play, punishment, thermoregulation, and motion. Peer-reviewed literature published between 1952 and 2018 was retrieved from CAB Abstracts, PubMed, ISI Web of Knowledge, Scopus and book chapters. Keywords for this search included the following terms: behaviour, bonding, altricial, precocial, offspring, maternal , whelping, nursing, domestic dogs, female dog, aggression, puppies, anogenital licking. In this review, we reported and discussed scientific information about maternal behaviour in domestic bitches, comparing altricial vs precocial species; the importance of the bonding, grooming/licking and nursing, and their impacts on puppies' behaviour; altered maternal behaviours such as aggression, cannibalism, rejection, and also the relation between hormones and maternal care behaviours. We concluded that the level of interactions between the dam and the puppies influences the physiological, cognitive and behavioural development of the litter, and the main hormones in the bitch for inducing maternal care behaviours are estradiol, oxytocin, prolactin and progesterone.

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International Journal of Veterinary Science and Medicine
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Maternal behaviour in domestic dogs
Karina Lezama-García, Chiara Mariti, Daniel Mota-Rojas, Julio Martínez-
Burnes, Hugo Barrios-García & Angelo Gazzano
To cite this article: Karina Lezama-García, Chiara Mariti, Daniel Mota-Rojas, Julio Martínez-
Burnes, Hugo Barrios-García & Angelo Gazzano (2019) Maternal behaviour in domestic dogs,
International Journal of Veterinary Science and Medicine, 7:1, 20-30
To link to this article: https://doi.org/10.1080/23144599.2019.1641899
© 2019 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group.
Published online: 21 Jul 2019.
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Maternal behaviour in domestic dogs
Karina Lezama-García
a
, Chiara Mariti
b
, Daniel Mota-Rojas
a
, Julio Martínez-Burnes
c
,
Hugo Barrios-García
c
and Angelo Gazzano
b
a
Neurophysiology, Behavior and Assessment of Welfare in Domestic Animals, Department of Animal Production and Agriculture,
Universidad Autónoma Metropolitana (UAM), Mexico City, Mexico;
b
Department of Veterinary Sciences, University of Pisa, Pisa, Italy;
c
Graduate and Research Department, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Tamaulipas, Victoria,
Mexico
ABSTRACT
Mammalian parental care, in most of the cases, is given by the female, who provides food,
warmth, and protection. In domestic dogs, maternal behaviour shown by the dam mainly
consists of contact, nursing, grooming/licking, play, punishment, thermoregulation, and
motion. Peer-reviewed literature published between 1952 and 2018 was retrieved from CAB
Abstracts, PubMed, ISI Web of Knowledge, Scopus and book chapters. Keywords for this
search included the following terms: behaviour, bonding, altricial, precocial, offspring, mater-
nal, whelping, nursing, domestic dogs, female dog, aggression, puppies, anogenital licking. In
this review, we reported and discussed scientific information about maternal behaviour in
domestic bitches, comparing altricial vs precocial species; the importance of the bonding,
grooming/licking and nursing, and their impacts on puppies’behaviour; altered maternal
behaviours such as aggression, cannibalism, rejection, and also the relation between hor-
mones and maternal care behaviours. We concluded that the level of interactions between
the dam and the puppies influences the physiological, cognitive and behavioural develop-
ment of the litter, and the main hormones in the bitch for inducing maternal care behaviours
are estradiol, oxytocin, prolactin and progesterone.
ARTICLE HISTORY
Received 7 February 2019
Revised 28 June 2019
Accepted 2 July 2019
KEYWORDS
Maternal care; dog
behaviour; whelping;
nursing; puppy welfare
1. Introduction
Mammalian parental care in dogs is mainly performed
by the dam, who provides food, warmth [1,2], shelter
and protection from predators and conspecifics [3,4],
helping to the offspring´s survival and their mental and
physical well-being [5,6]. It has been documented that
maternal care has an impact on individuals’develop-
ment in many species, including rodents, pigs, non-
human primates, humans and recently in adult dogs
[7–9]. The quantity of the relationship between the dam
and the offspring interpose on physiological, cognitive
and behavioural offspring’s development [10]. The
maternal behaviour detected on bitches towards the
litter includes contact, nursing, licking (mainly anogen-
ital licking, that allows newborn puppies to urinate and
defecate in a duly manner), play, punishment, thermo-
regulation and motion [11,12].
Maternal behaviour, delivery and nursing synchro-
nisation assure that the dam responds to offspring’s
needs in time. A variety of studies in newborn mam-
mals prove that maternal behaviour directly impacts
on the neonatal survival [13–15] since mortality rates
between birth and weaning are related to maternal
and neonatal behaviour [16–21].
Dogs are altricial animals and, for that reason, the
establishment of dam-offspring bonds can take days
or even weeks to develop. Nevertheless, nest building,
licking, nursing and puppy’s rearing is present in
most of the cases. In comparison with wild canine
species, domestic dogs are considered to have
a reduced disposition for maternal behaviour [22],
and therefore, human intervention is sometimes
required to increase puppies’survival [12].
This review aims at discussing and comparing pro-
vided data by scientific papers about domestic dogs
maternal behaviour. Throughout this paper, we will
address several issues such as differences in maternal
behaviour between both altricial and precocial species,
maternal skills, licking and dam-offspring bond signifi-
cance and its impact on long-term puppies’behaviour,
abnormal maternal behaviour, and the relationship
between maternal behaviour and bitches’hormonal
levels. In this way, current findings allow readers to
get a comparison between the results of different
authors’studies, and also to have a conclusion about
the last published data on bitch maternal behaviour.
2. Maternal behaviour in altricial vs precocial
species
Natal viability is associated with foetal maturity, envir-
onmental conditions, and maternal care [23]. Usually,
CONTACT Daniel Mota-Rojas dmota100@yahoo.com.mx Universidad Autónoma Metropolitana, Xochimilco. Calzada del Hueso 1100, Col. Villa
Quietud, Del. Coyoacán, Mexico City CP 04960, Mexico
INTERNATIONAL JOURNAL OF VETERINARY SCIENCE AND MEDICINE
2019, VOL. 7, NO. 1, 20–30
https://doi.org/10.1080/23144599.2019.1641899
© 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits
unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

altricialand precocial terms areusedto indicate an early
for late stage of development at birth in mammals and
birds. The altricial-precocial scale describes the degree
of behavioural and morphological maturation of the
offspring at birth or hatching [24]. In precocial species,
offspring require minimal parental care and are rela-
tively mature, able to move and can feed themselves
(precocial birds) or forage independently from the start
while still being nursed (precocial mammals). In con-
trast, altricial canids, rodents, felids are initially incap-
able of moving around on their own and require
extensive parental care, like brooding or food access
[25]. In altricial species, such as the dog, offspring are
unable to care for themselves at birth, are usually born
deaf and blind, and have limited movement [12,26].
The ability of the newborn to survive and to grow
within the born environment depends on the vital
organs’maturation level at birth. Organs of placental
altricial neonates are capable of maintaining its vital
functions and the short-term metabolic changes
[27,28]. However, in some species, neonates need
a dam to hatch them or to feed them [25]. Altricial
species dams (as rodents, canines, and felines) built
a nest where they give birth to their offspring, which
are not fully developed and have limited sensorial and
motion skills [4,29]. Maternal behaviour largely differs
across species. For instance, once the rodent dam has
gathered its offspring within the nest, it spends most of
the time in a nursing position, grooming them and
eliminating faeces and urine [30]. In rabbits, maternal
behaviour is different: dam only suckles rabbits once or
twice a day, for periods no longer than 10 minutes each
[31]. Primate dams instead carry offspring most of the
time and hold it with its strong hands [32]. Dogs are born
blind and deaf, which limits newborn care [26]; for that
reason, puppies’physical and social development is
mainly determined by the interaction with the dam
[33]. During the fifth week postpartum, offspring fre-
quently gets out of the nest, and weaning starts [34].
In precocial species (most of the ungulates), off-
spring requires less parental care, as soon after birth
they can move and can graze between breast-feedings
[25]. Precocial placental newborns show an organs’
advanced development state to keep vital functions,
thermoregulation, and a highly energetic perfor-
mance [27]. Immediately after birth, dam licks off-
spring until they are free of amniotic fluid and
placental remains [35]. Precocial species deliver
small litters, with fully developed offspring, capable
of following the dam immediately after birth. Within
these species, dams develop discriminatory maternal
care that allows only its offspring to suck and avoid
other animals to do so [4,18].
The bitch nurses the puppies intensively during
the first days, and hardly leaves the nest. If the pup-
pies roam around, the dam will lick them to return
them to the nest. From birth to three or four weeks
old, the dam needs to stimulate urination and defeca-
tion (through anogenital licking), and she will eat any
waste, feed the puppies, and provide a heat source to
maintain them at stable body temperature [36,37].
All the reviewed data agree that maternal beha-
viour shows meaningful differences between precocial
and altricial species, which is less intense in precocial
species than in altricial ones. For a more comprehen-
sive review on altricial and precocial social complex-
ity, see Scheiber et al. [25].
3. Maternal behaviour and hormonal
influence
In all mammal species, the period surrounding the
birth is characterised by an increase of plasma estra-
diol, prolactin, and cortisol levels, and by the activa-
tion of the oxytocinergic system at the time of
delivery [4].
The factors causing the onset of typical maternal
behaviours are still subject to debate and widely stu-
died in rodents [38–41]. In rodents, the existence of
an attraction-acceptance neural circuit, that would
inhibit the activity of another defensive antisocial
neural circuit, has been hypothesised [38].
The hormonal constellation present at the end of
pregnancy allows a rapid display of maternal beha-
viour and acceptance of newborns, activating the
attraction-acceptance circuit [42].
Female primiparous rats immediately demonstrate
maternal behaviour, while virgin female rats when
exposed for the first time to newborns, show avoid-
ance lasting for 3–4 days [43].
On one hand, in pregnant rats, the increase in the
blood concentration of oestrogens and prolactin
would activate the medial preoptic area (MPOA) of
the hypothalamus, making it capable of responding to
stimuli from newborns, inhibiting the antisocial
defensive circuit and activating the attraction-
acceptance circuit (the mesolimbic dopamine system,
MDS), resulting in prosocial maternal responses [44].
On the other hand, recent studies support the
hypothesis that, in rats, unfamiliar olfactory stimuli
from pups activate the neural circuit responsible for
pup avoidance in virgins, composed by the olfactory
bulb, medial amygdala, anterior hypothalamic
nucleus and periaqueductal gray [43].
According to Numan et al. [43], MPOA neurons,
primed by prolactin and estrogen, becomeresponsive to
pup stimuli and activate neurons of the ventral tegmen-
tal area of the midbrain, where MDS has its origin, and
release dopamine in the nucleus accumbens, located in
the subcortical cerebral hemispheres. Dopamine causes
a reduction in the response of the nucleus accumbens to
stimuli originating from the defensive antisocial neural
circuit. The nucleus accumbens would also be inhibited
in its regulatory activity of the ventral pallidum,
INTERNATIONAL JOURNAL OF VETERINARY SCIENCE AND MEDICINE 21

a motivational control region. The ventral pallidum
could, therefore, become active and allow the appear-
ance of maternal behaviour.
It is generally accepted that dams identify their off-
spring by olfaction and this seems related to oxytocin
release [9,18,20]. Oxytocin, a neuropeptide with the
dual action of hormone and neurotransmitter, is
another molecule largely involved in triggering mater-
nal behaviour. Oxytocin enhances maternal interest in
young dogs by reducing anxiety and stimulating mater-
nal care [42]. The posterior pituitary gland is the site of
oxytocin release after neurologic stimulation [45,46].
There are two recognised stimuli to induce oxytocin
release. The first is Ferguson´s reflex, that consists of the
pressure of the head of a puppy into the cervix during
parturition [45,47,48]: the cervicovaginal stimulation
during labour and the secretion of prolactin, along
with the presence of estradiol and progesterone, release
oxytocin by producing reactions in the maternal brain
[47](Figure 1). The second stimulus is the suckling
stimuli of the mammary glands by the puppies [45].
Oxytocin is produced by the neurons of the para-
ventricular nucleus of the hypothalamus, which projects
to many regions of the brain, including the MPOA. The
action of oxytocin would be that of potentiating the
stimulating activity of MPOA on MDS [44].
In rats, the long-term persistence of maternal beha-
viour, also known as “maternal memory,”is also
maintained by oxytocin and dopamine action in the
nucleus accumbens shell [49]. Oxytocin is also respon-
sible for the synchronised uterine contractions during
parturition and the further dilation of the cervix. In
contrast, progesterone maintains pregnancy by promot-
ing the secretion of intrauterine glands to sustenance the
fertilised eggs, stimulates the expansion of the mammary
glands, and induces maternal behaviour. Further, the
decrease of progesterone and a subsequent rise in pro-
lactin cause the common maternal behaviours seen in
dogs, including nesting [45,50](Figure 1).
After birth, puppies are exposed to particular
pheromones secreted by the sebaceous glands located
in mother intermammary sulcus, the area in between
her breast where puppies detect them upon nursing.
Because these pheromones provide calm, comfort
and a sense of well-being to the puppies, they are
called Dog Appeasing Pheromones (DAP) [46,51,52].
Another factor related to the duration of the eleva-
tion of some hormones is the parity number by which
the bitch is passing; that is, it can be different in primi-
parous and multiparous. In a study performed by Seki
et al. [53] the initial increase of progesterone levels was
of shorter duration in primiparous bitches [4].
According to the above, we can conclude that the
levels of oxytocin, prolactin, and progesterone are
closely related to maternal behaviour. Oxytocin med-
iates several forms of affiliative behaviours, including
Figure 1. The behavioural repertoire of the bitch at birth. In order to trigger labour, there must be a decrease in the
progesterone, followed by the increase of the prostaglandin F
2
, which creates an increase in the oxytocin sensitivity in the
bitch’s uterus. At this moment, the dog begins with the construction of the nest or to move away to some dark place. Likewise,
it increases the prolactin, and the release of oxytocin from the neurohypophysis, and with signs of fainting, vomiting,
inappetence, trembling, and uterine contractions start. Here it is when the dilation phase begins. Subsequently, the expulsion
phase and the Ferguson reflex are activated, with more release of oxytocin; uterine contractions emerge, and the fetus places
itself, either anteriorly or posteriorly in the birth canal. The bitch starts to lick her vulva and to break the amnion, she cuts and
tears the umbilical cord, and subsequently, there is the placental expulsion, the bitch eats the placenta, and because of the
relaxin, prolactin, and oxytocin stimulus, the lactation starts.
22 K. LEZAMA-GARCÍA ET AL.

parental care, and grooming [54–56] the formation of
a pair-bond, as well as the establishment of the rela-
tionship between dams and offspring [57].
A study using potent prolactin inhibitors, mostly
dopamine agonists confirmed the role of prolactin as
luteotropic hormone from day 30 of pregnancy and
beyond and that it is crucial for the preparation,
initiation and sustaining lactation, as well as for the
activation of maternal and sexual behaviour [58].
Prolactin seems to be involved in ensuring maternal
behaviour, including the preparation for delivery and
the care of the litter, although it is not yet clear how it
shares these effects with oxytocin [59].
During the birthing process, the bitch licks the
placenta and start eating the foetal membranes, the
remains of the placenta and also tears the umbilical
cord [36,45,60–62], reducing the contamination of
the nest and avoiding predators [36](Figure 2(a,b)).
Cleaning the newborn, and consuming the amniotic
fluid and placenta, are common behaviours within
mammals [63], except the big aquatic mammals
(cetacean) or semi-aquatic (pinniped); likewise, the
dams produce vocalisations to keep close the off-
spring and drive away from the predators [4].
In most bitches and queens, a typical maternal
behaviour is that they wait until the whole litter is
born to feed them. It is generally accepted that dams
identify their offspring by olfaction, and this seems
related to oxytocin release [45,60].
The first contact of puppies and kittens with the
mother’s tit is by the sense of smell and by trials
and errors. The dam uses its paws to push the
newborns towards the nipples and allow them to
nurse. Also, the puppies and kittens press the
mammary gland to stimulate the descent of the
milk [45]. (Figure 3(a,b,c)).
After feeding the offspring, the dam stimulates in
them urination and defecation through anogenital
licking.
Figure 2. (a) The bitch breaks the amnion and devours the
fetal membranes, initially from the puppy’s head so it can
breathe quickly, and then cleans the rest of the body, licking
it and in the same way stimulating the offspring (Photo MVZ
David Rivera). (b) The bitch tears the umbilical cord keeps
licking and cleaning the puppy, and when the dam throws
the placenta, she starts eating it to avoid the nest contam-
ination and thus not attract predators. Placentophagy favours
the uterine involution and milk production.
Figure 3. Maternal behaviour at parturition. (a) The bitch,
provides warmth and protection to the puppy and stays with
it most of the time. It only leaves the nest to feed, urinate
and defecate. The rest of the time it is taking care of the
offspring at least during the first three weeks of the puppy’s
life. (b) The bitch pushes out the puppy with the snout to
mammary glands to facilitate its nursing. By doing so, it takes
advantage of licking the offspring’s genitals to stimulate the
puppy to urinate and defecate. In this picture, we can
observe the offspring’s umbilical cord, which will detach
approximately on the third day of birth. (c) Since the puppy
fails to move around by itself, bitch helps it by gently grab-
bing the neck with the muzzle to move it from place to place.
INTERNATIONAL JOURNAL OF VETERINARY SCIENCE AND MEDICINE 23

Those mentioned above continue when the puppies
and kittens start moving and until three weeks of age.
During the first week after parturition, the dam
rarely leaves alone the offspring, only to eat, urinate
and defecate. Maternal care can differ depending on
the experience of the mother: maternal care (specifically
licking the anogenital area, lactation and staying in
contact with the puppies) during the first three weeks
is markedly higher in primiparous than in multiparous
mothers [64]. Later (the 4
th
week after delivery) the dam
becomes evasive, rejecting the offspring to suckle as
their teeth start to erupt, and leave the litter for
extended periods [45,60]. In primiparous dams,
a higher licking of the anogenital area, nursing and
contact with the puppies from day 1 to 21 was found,
which led to a more significant amount of maternal care
in the third week compared to multiparous mothers.
3.1. Milk production from the hormonal point of
view
The study of the biological mechanisms that influence
on regulates pregnancy, delivery, and lactation, is very
important to understand maternal responses. Maternal
behaviours usually arise immediately after birth, where
the female quickly shows great interest in the newborn.
However, the most essential and natural maternal beha-
viour in mammals is lactation (Figure 5(a,b)), which
occurs right after birth and ensures that newborns grow
up healthy and strong [4].
The hormones prolactin and oxytocin play an essen-
tial role during lactation. Prolactin promotes milk pro-
duction and incites normal maternal behaviour.
Prolactin release is stimulated during pregnancy, and
its blood levels rise suddenly at parturition, while other
hormone concentrations abruptly decrease [45].
Oxytocin stimulates descent of milk into the mammary
glands, and its blood levels are high during nursing.
A correlation between the quantity of oxytocin secreted
with the efficiency of milk production is described in
some species [50].
4. Offspring grooming
Maternal licking in rats is associated with changes in
offspring behaviour, such as maternal and anxiety-like
behaviour [65]. It also affects receptors of glucocorti-
coid [66], oxytocin, vasopressin [67] and estrogen [68].
Published studies in animal models remark the
relevance of the extent of nursing, anogenital and
body licking, and the close body contact of the dam
with the offspring. These behaviours may further
influence the emotionally [69] and stress response
and social skills of the neonates [68,70,71].
Moreover, Champagne et al. [68]describethatindi-
vidual pups within a litter receive the same amount
of licking and grooming.
For all the above, it is unquestionable that licking
is one of the leading maternal behaviours that may
further affect the puppies’behaviours and the inter-
actions in their environments.
5. Bonding between dam-offspring and
maternal care
For parents, recognising their offspring help to prevent
misdirected parental care, limits energy losses, and
ensures reproductive success. On the other hand: for
young animals, recognition of parents is also essential
to their survival, since, in most species, parents feed only
their newborns. There is evidence that parent-offspring
recognition is crucial for colonial species, though the
degree of recognition seems to vary among different
species depending to some degree on environmental
constraints [4,72]. For the offspringofallmammalspe-
cies, their mothers are the essential social contact during
the first months of life as they facilitate acquiring infor-
mation about physical and social environments [73].
Besides providing genetic material, parents also play
afundamentalroleintheoffspring development [33].
The quality and quantity of the relationships between the
dam and the offspring take part in the puppies’physio-
logical, cognitive and behavioural development
[10,70,74].Thematernalbehaviourtowardstheoffspring
during the early stages plays an essential role in their
development, just as the following character and beha-
viour. For example, maternal behaviour alters the
hypothalamic-pituitary-adrenal axis or stress responsive-
ness pathways of the neonate, and these changes persist
throughout adult life [12]. In two studies conducted by
Guardini et al. [10,75], it has been found an association
between the amount of maternal care provided by the
mother to each puppy and their behaviour at two months
of age, suggesting that the extent of maternal care that
puppies receive during the neonatal period influences
their coping strategies at two months of age. However,
the patterns of behavioural responses widely differed
according to the environment in which puppies were
raised, so that authors suggested that maternal care con-
tributes to the adaptation of puppies to their environ-
ment, especially to the social relationship with humans
[75]. Besides, a high level of maternal care in dogs influ-
ences physical and social engagement, aggression, and
lower levels of anxiety and fear [8,10,76].
In the same way, in a study accomplished by Foyer
et al. [8], they taped 22 German shepherd litters during
the first three weeks postpartum, to evaluate maternal
care variations and their effects on behaviour and tem-
perament in puppies around one and a half years of age.
They observed that the maternal care level varied
between different bitches, during the first three weeks
after birth, and this affected the social and physical
engagements, as well as aggression, in the offspring
when they became adults. Foyer at al [8]. also found
24 K. LEZAMA-GARCÍA ET AL.

that the amount and quality of maternal care would vary
during the suckling period and that better maternal care
would lead to less reactive, more confident and explora-
tive puppies.
The maternal care and the early postnatal environ-
ment may also have marked effects on subsequent
stress-related behaviours. Tiira and Lohi [76]described
the correlation between maternal care in puppies and
the later development of anxiety. They collected data
from a family dog population (n = 3264) to evaluate the
association between environmental factors and fearful-
ness, noise sensitivity, and separation anxiety. The study
revealed that fearful dogs had had significantly fewer
socialisation experiences and lower quality of maternal
care during puppyhood. Noise sensitivity and separa-
tion anxiety was associated with a lower level of daily
exercise. Authors suggest that dogs share many of the
same environmental factors that contribute to anxiety
in other species, such as humans and rodents.
Nonetheless, there are limited studies about mater-
nal care as a predisposing factor for anxiety, because it is
a relatively new concept in dogs, but described in other
altricial species [12]. Also, the environment may affect
puppies’behaviours once they are adults. A study con-
ducted by Appleby et al. [77], described higher aggres-
sion rangesin adult dogs when they were puppies raised
in non-domestic maternal environments, compared to
those raised in domestic maternal conditions.
A study conducted by Bray et al. [78], follow 98
puppies from birth to adulthood, who were allocated
to be guide dogs and they observed a link between high
levels of maternal behaviour and a higher probability
of program failure. Also, that the dams who require
a higher effort from puppies to accomplish nursing are
more likely to have successful offspring to be guide
dogs; on the other hand, dams whose lactation
requires less effort from puppies are more likely to
have offspring who will not perform as guide dogs.
The same study describes in the temperament tests
that there is an association between maternal beha-
viours and the young adult behaviour, on the same
way that Foyer et al. [8] and Guardini et al. [10].
However, unlike them, Bray et al. [78] found that the
extreme maternal care is directly linked to adverse
anxiety behaviours in dogs when they are young
adults, as well as poor problem resolution and the
decrease of latency at the first barking period.
Another study conducted by Bray et al. [79], mon-
itored maternal interactions in twenty-one litters
from three different breeds. The study revealed that
a mother’s attitude and actions toward her offspring
varied naturally between individuals and that these
variations could be summarised by a single principal
component, which they described as Maternal
Behaviour. This element was stable across weeks,
associated with the breed, litter size, and parity, but
not redundant with these attributes.
6. Abnormal maternal behaviours;
aggression, cannibalism, reject, pseudocyesis
Studies have identified different causes for abnormal
maternal behaviour, such as high prepartum and
postpartum stress levels [80–83], hereditary predis-
position [84], low serotonin levels [85], and low oxy-
tocin levels [86].
6.1. Aggression
Maternal aggression is usually temporal, and it will
decrease just as puppies grow up [87]. The aggression
is towards whoever approaches the nest, to the pup-
pies or the objects the bitch perceives as puppies
during the false gestation [88].
In bitches, aggression may exacerbate by vocalisa-
tion of puppies. However, the aggressiveness may be
associated with pain, for example, in cases of mastitis
[45]. There is a critical role for oxytocin in the onset
between the dam and offspring bonding, associated
with low stress and fear [89,90], and on the increasing
maternal aggression toward threats [91].
The bitches with maternal aggressiveness monitor
the nest, the puppies, or when a person or an animal
is near. The puppies represent a precious resource for
the bitch, in which it has already invested much energy
required for a satisfactory pregnancy. The hormonal
changes associated with lactation can alter the dam
evaluation or perception of the range of resources, and
involve protection even in ordinary objects, with an
apparent disproportional ferocity. Fears may follow
attacks or bites in some cases [88]. The lactating bitches
may become aggressive towards humans or even
canines. This behaviour may cause difficulties when
trying to control the puppies progress and to secure
adequate socialisation. The aggression may be acceler-
ated because of environment troubles, especially in
anxious or immature bitches, within an unstable social
environment [36], and it decreases after a few days or
weeks, when the puppies grow up and become less
dependent on the dam and, therefore, their defence
needs are reduced [88].
6.2. Cannibalism
Maternal cannibalism is also called cronyism [45], and
it is a condition where a dam consumes her offspring
after killing them [92,93]. It is abnormal maternal beha-
viour unless it is a strategy to reduce litter size, balance
the sex ratio of the offspring, eliminate the offspring that
has come out defective [80,94]orwhenthereisapoor
significant environmental condition [95]. The dam can
accidentally kill and devour a puppy during the process
of cutting the umbilical cord (Figure 4)[36]. Although
some biological factors, such as low levels of oxytocin
and blood lipids are related to a failure in maternal
INTERNATIONAL JOURNAL OF VETERINARY SCIENCE AND MEDICINE 25

behaviour in different animals, this had not been inves-
tigated in detail. Kockaya et al. [93] measured these
substances in the serum of 15 adult Kangal bitches,
who had a cannibalism background, compared with
15 samples of bitches from the same breed, who had
no maternal cannibalism background. The results
revealed significantly lower levels of these substances
in bitches with a maternal aggressiveness background.
The oxytocin levels of 3.58 + 0.43 ng/ml and cholesterol
at 125.50 + 8.6 mg/dL in dogs with cannibalism, com-
pared with oxytocin of 9.68 + 1.58 ng/ml and choles-
terol at 159.18 + 13.85 mg/dL in bitches with normal
postpartum behaviour. Thus, they concluded that oxy-
tocin is an essential neuroendocrine factor in bitches, to
develop normal maternal behaviour.
Bitches rarely direct severe aggression towards
their puppies and are more likely to manifest such
behaviours with their first litter. However, there are
some cases in which bitches have caused severe inju-
ries and are considered a hereditary trait [96]. Causes
of cannibalism include pain (usually associated with
mastitis) and eclampsia, a large litter, stress, and
overcrowding [45].
6.3. Rejection of the offspring
Rejection of the offspring or maternal negligence, it is
uncommon, but some bitches may fail to attend their
puppies regarding warm, nutrition and urine and
faeces elimination [97]. Primiparous dams are more
prone to rejection. Also, in anxious dams who leave
the nest frequently, those with premature litters (less
than 57 days of gestation), litters born through a cae-
sarean section or where there are many discomforts
in the environment [36]. Breeding practices can also
alter the behaviour of the bitch towards her litter,
such as removing the pups from the nest areas and
holding them for a short period [98].
Rejection behaviour of the offspring is described in
bitches under some conditions, including when one
or two puppies are repeatedly moved from the nest or
hidden, then the dam perceives that something is
wrong with that puppy. Also, bitches routinely reject
pups that are cold or are not moving. However, if the
entire litter is rejected, it suggests that something is
wrong with the dam and medical assistance is neces-
sary to identify clinical signs of morbidities as masti-
tis, metritis, and eclampsia, or stressing factors
(overcrowding, large litters). Some primiparous
bitches are poor mothers, especially if they are ner-
vous or anxious. However, many of these dams tend
to be good mothers with subsequent litters [45].
6.4. Pseudocyesis
Pseudocyesis (also called false pregnancy) is a common
condition where the non-pregnant bitch goes through
Figure 4. Sometimes due to inexperience (primiparous) or
nervousness, the bitch pulls too much the umbilical cord of
the newborn when trying to tear it and this may cause
injuries in the puppy (such as evisceration) or inclusive can-
nibalism (Photo MVZ Gibran Olivera Rodríguez).
Figure 5. (a) The bitch acquires a lateral decubitus position to
nurse the offspring; they look for the closest nipple and begin
to suck hard. (Photo MVZ Esp. Juan Jose Santiago Garcia). (b)
The puppy indistinctly selects a nipple and begins to suck
and make massage movements that stimulate the mammary
gland to release milk (Photo MVZ Esp. Juan José Santiago
García).
26 K. LEZAMA-GARCÍA ET AL.

the same hormonal changes as the pregnant one. It can
depend on both serum prolactin levels and the sensitivity
of tissues to this hormone [36]. Pseudocyesis can be
underdiagnosed in bitches and may be the cause of
some cases of behavioural problems, including aggres-
sion [99]. At the end of dioestrus, when progesterone
concentrations fall, and prolactin concentrations rise, the
female dog exhibits mammary development, produces
milk and may show behavioural changes as if she is
whelped such as nesting and mothering of inanimate
objects and some bitches may become aggressive [45].
Apart from typical maternal behaviours such as care,
grooming, vomiting, the dam may show the enlargement
of the mammary glands, as well as restlessness and con-
struction behaviour nest, similar to the pregnant bitches
that have delivered –before,anxiety,agitation,lethargy,
aggression and pain [36,88,99–101]. Roth et al. [99]
developed a survey applied to 2000 veterinarians, to
know the frequency of cases of pseudocyesis in dogs
and the signs observed. The results revealed that 96% of
the respondents reported having observed cases of pseu-
docyesis with changes in maternal behavioural (the most
common was that the bitches adopted objects as if they
were puppies). Pseudocyesis was reported in 49% in
sterilised bitches, and the most common physical sign
was the enlargement of the mammary gland and milk
production (89%). Besides, 97% of veterinarians reported
cases of aggression associated with pseudocyesis.
7. Conclusion
Dogs are altricial species that depend entirely on the
dam to survive, obtaining warm, food, movement, pro-
tection from predators and stimulation through ano-
genital licking to eliminate waste. The main difference
in maternal behaviour between altricial and precocial
species is that, in the first, the dam-breeding link takes
from one day until weeks to be established, while in the
precocial, this bond is generated even in hours. For
delivery and maternal behaviour to take place, a set of
factors must happen both in the foetus and in the bitch,
thus activating the series of hormones involved, such as
oestradiol, cortisol, progesterone, prolactin, oxytocin,
and relaxin. The normal maternal behaviours include
the creation of the nest, contact, nursing, licking, play,
punishment and within abnormal maternal behaviours
authors describe aggression, pseudocyesis, cannibalism,
and abandonment of the offspring. Abnormal maternal
behaviour in the bitch is related to low levels of some
hormones, mainly oxytocin. All the authors revised
agree on the relationship between maternal care of
breeding and the development of desirable or undesir-
able behaviours in puppies when they are adults. With
more maternal care, the puppy becomes more depen-
dent, anxious and has a harder time adapting to its
environment. However, to date, few studies describe
maternal behaviour in domestic dogs, so it is necessary
to continue researching this topic.
Disclosure statement
No potential conflict of interest was reported by the
authors.
ORCID
Karina Lezama-García http://orcid.org/0000-0003-0084-
8135
Chiara Mariti http://orcid.org/0000-0001-7127-4680
Daniel Mota-Rojas http://orcid.org/0000-0003-0562-
0367
Julio Martínez-Burnes http://orcid.org/0000-0002-8681-
4261
Hugo Barrios-García http://orcid.org/0000-0001-7590-
319X
Angelo Gazzano http://orcid.org/0000-0001-9649-2027
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