Maternal behavior in bitches

Introduction

Studying mammalian maternal behavior gives an idea of the necessary interactions between a mother and her offspring and the level of dependence between the two, and the behaviors will vary between precocial and altricial species. In the bitch, good maternal behavior is important for two major reasons. Firstly, since puppies are born helpless, deaf and blind, and have limited movement (i.e., an altricial species), they are totally dependent on an external source to survive. For domestic dogs, in comparison to free-roaming dogs and some wild canids, parental care is performed mainly by the dam, so puppy survival is directly affected by the quality of the mothering abilities (assuming no human intervention). Secondly, the mother’s behavior can affect future development of her offspring; although recent studies are not conclusive, maternal quality seems to directly impact a puppy’s cognitive development and performance 1,2,3.

Canine maternal behavior has been studied for many decades 4,5,6, and it is agreed that such behavior is a response to the needs of the neonates. The main aspects involve direct contact (for thermoregulation of the puppies), oral interaction (by licking), and nursing, playing with and disciplining the puppies. However, the impact of maternal care in the cognitive development of dogs is a recent concept, with various studies (1,2,3,7,8) attempting to understand and predict how early interactions between a dam and her puppies can affect the latter’s cognitive abilities, how long-lasting these effects are, and how great the impact is on the future performance and behavior of adult dogs. Consequently, poor maternal care could be the origin for later unwanted behaviors. This review will focus on the common aspects of maternal behavior around parturition and during the first weeks of life, and will discuss how maternal care may influence a dog’s cognitive abilities and temperament.

Impending parturition

Behavior changes in the pregnant dam can appear one or two days before the due date 9, but the signs may or may not be obvious, depending on whether the bitch is primiparous or multiparous. In most cases she will be restless and have a reduced appetite 12-24 hours before whelping. Nesting and digging behavior is more variable and depends on both individual and environmental factors, and the level of human contact 10. No correlation has been established between the intensity of preparation for whelping and the quality of maternal behavior. Other signs also described include inattention, drowsiness, aggression, anxiety, unpredictability, irritation, and an increased tendency to seek attention from the owner, although some bitches may prefer seclusion. As parturition approaches, the bitch will spend more time in the whelping area. A decrease in body temperature may cause shivering 9, and could explain other behavioral changes, but the use of this parameter as an indicator for parturition is still debatable. A drop of around 1.0 °C has been used to indicate impending parturition 11, but vaginal temperature loggers have shown that this drop does not have a predictive value for the onset of whelping 12.

Parturition

Normal parturition (eutocia) is a combination of physiological, endocrinological and behavioral changes that culminate in delivery of the puppies. Whelping progresses in three stages with a distinct exhibition of behaviors. The first stage is the onset of subclinical uterine contractions, along with vaginal relaxation and cervical dilation, but with no indication of abdominal contractions. Some females will show no evident signs at this stage, but if seen, they mimic those described for impending parturition, such as rearranging the bedding material in an attempt to build a nest. The duration of this stage might be affected by parity of the bitch, and can be up to 36 hours in a nervous primiparous female 9, but usually lasts for 6-12 hours. The second stage is the active birthing process, and is characterized by strong and coordinated abdominal contractions, followed by vocalization of the bitch and release of fetal fluids. Once the cervix is fully dilated, the presence of the first puppy at the cervix initiates the Ferguson reflex and triggers oxytocin release, with contraction of the abdominal muscles that result in delivery.

Once the puppy is born, the bitch must break the amniotic sac (if it did not rupture during birth) (Figure 1); puppies that remain within the fetal membranes can die in a matter of minutes if not freed quickly. The bitch should also tear the umbilical cord and vigorously lick the newborn puppy 9, which is important both to stimulate respiration and to dry the puppy, and is essential to establish maternal bonding. Inexperience (in the primiparous bitch) and high levels of anxiety during parturition can disturb maternal behavior and lead to increased puppy mortality. The whole process will repeat until all puppies are born, and the bitch will interrupt the grooming of a newborn as contractions resume for the delivery of another puppy. In fact, a bitch may focus entirely on the whelping process, and may appear insensitive to the crying of the puppies 4, neglecting the litter until stage two is completed 5. In general, the first puppy will be born within 1-2 hours of the second stage commencing, although this can be up to 4 hours, and the overall duration of stage two varies depending on the size of the litter, but can last for up to 12 hours, and may possibly be delayed or arrested by any stress or disturbance 4,5.

The third stage is the expulsion of the fetal membranes, which may occur after each puppy or after two or three puppies have been born. If permitted, the bitch will eat the placentas, which in carnivores is important for several reasons; for hygiene, as a source of energy for the dam 4 and (possibly) to decrease the attraction of predators.

Maternal behavior in the early postpartum period

Once whelping is complete, the bitch should display a set of behaviors that will allow the survival, growth and development of the puppies 13. Studies of maternal behavior tend to focus on easy-to-measure aspects, such as oro-nasal interactions (licking or poking the puppies), time spent with the litter (both in close contact and within the whelping area), and the duration and position of the bitch during nursing. Although maternal behavior is important until weaning, the neonatal and transition periods are emphasized here; this is when the puppies are most dependent on the dam, and these stages are crucial for how the mother’s character and maternal abilities can affect the puppies’ development. The neonatal period (defined as days 1-16) is the adaptation to extra-uterine life, whilst the transition period starts when the puppies open their eyes, and is characterized by the development of hearing capacity and neurological skills 10. At the end of this period a puppy’s senses will be fully functional, and its levels of dependence start to decrease as its exploratory behavior increases.

Oro-nasal interaction

The first interaction of the bitch towards the newborn puppy is grooming 4,6,9. As discussed above, this is crucial not only to the puppy’s survival but is fundamental to trigger the maternal connection. Licking is thought to initiate a puppy’s urination and defecation in the first three weeks of life 6,9,14, and is also used by the dam to waken the puppies when she is ready to nurse them and to direct them towards the mammary glands. The dam will continue to lick the puppies at least until weaning, although this declines over time, and by around 21 days of age puppies are self-sufficient for toileting.

It is possible that the frequency and/or the time spent grooming the puppies can impact the cognitive behavior of dogs. Even though licking activity has been used to rank maternal behavior 1,2,3,7 no direct correlation has been established, although research in rodents has shown that offspring which are frequently licked by their mother are better adapted to stress and have enhanced signaling of genes associated with learning and memory.

Contact time

Another important maternal behavior is to stay in close contact with the puppies, and a new mother will be reluctant to vacate the whelping area (Figure 2) until at least around three days postpartum 5,6,8,14, after which she will gradually resume her daily activities, leaving the puppies more often. She can be extremely protective at this point, especially against strangers 4. The close contact between dam and young puppies is very important to prevent hypothermia; since neonates have poor thermoregulation, it is crucial that they have a source of heat (from the dam and/or the environment) to keep them warm. Hypothermia in a newborn can suppress certain body functions, including digestion and breathing. There is a physiological drop in the body temperature of a puppy immediately after birth 15 before it gradually increases to 35-37°C, the normal range for newborn puppies at day 7. The dependence on external warmth decreases over time, but a heat source that allows puppies to maintain a stable body temperature appears to be important up until the 4^th week of life 16. 

Nurturing activity

For mammals, nurturing basically relies on the nursing behavior of the dam. Nursing and suckling are connected activities, whereby the dam performs the nursing and the puppy responds by suckling. This activity is essential for the survival of the offspring, providing both nourishment and (in the first 24 hours after birth) transfer of colostral antibodies. It is one manifestation of maternal care controlled both by hormonal status and by the central nervous system 17. Nursing can be initiated before parturition is finished, but feeding the puppies is not a priority for the bitch until whelping is completed 4. During the first few days after parturition the bitch will nurse her puppies almost constantly 8,14. For the first 21 days postpartum, the bitch will lie down and lick the puppies to motivate nursing; this interaction is greatest at night-time 14. Once fully mobile, the puppies will initiate the suckling behavior 8,14, and the duration and frequency of nursing will gradually decrease. The bitch’s preferred position for nursing will also change with time; a sitting position has been more commonly observed during the day (Figure 3), whilst a recumbent position is frequently seen at nighttime (Figure 4) 14. This appears to influence a puppy’s development, although again more research is needed. Studies in guide dogs showed that puppies from bitches that nursed more often lying down were less likely to be selected for training than those where the dam nursed primarily in a sitting or standing position 2.

The puppy regulates the frequency and duration of suckling, although an individual puppy’s preference for a certain teat has not been identified. Once fed, the puppies will simply release the teats, but as long as they are attached a bitch will rarely leave the nest, at least in the early postpartum period. After around day 13, the bitch will start to actively interrupt the suckling activity 17.

Timeline of maternal behavior

As the puppies develop, the frequency and intensity of the maternal behavior declines 3,4,11. The time spent in licking activity decreases as the puppies develop 6,17, as does the degree of contact – as there is less reliance on the mother for warmth, the bitch spends more time away from the puppies 14. The duration and frequency of nursing will also decrease gradually 1,14, and as the puppies become stronger and suckle more efficiently, the bitch will leave them more often.

A wet diet should be introduced at around 3-4 weeks of age to habituate the litter to solid food and to complement their diet, since the dam’s milk production will start to reduce. The puppies are also capable of leaving the nest by this point, but although nursing may not be necessary from a nutrition standpoint, the puppies will continue to suckle, probably for emotional gratification 18.

Neonate behavior toward the dam

During the neonatal period, a puppy’s activities are predominantly suckling and sleeping. After birth, puppies seek a warm place, search for a mammary gland (olfactory cues seem to drive the attraction) and try to suckle as soon as possible. Newborn activity is minimal in the first two weeks of life, with puppies remaining close to the mother and each other (or an external heat source), presumably to maintain body temperature; as noted above, the interaction with the dam is normally initiated by the latter 14.

At the time the puppies open their eyes and their movements become more coordinated, the interaction between the dam and the littermates become more dynamic 6,8,14. They begin to actively search for the dam 6, patterns of nursing are more variable 14 and they show increased interaction with different players (the dam, littermate, toys and humans). Whining and/or crying is an indication of distress (e.g., cold, hunger) and normally urges the dam to respond to the puppies’ needs. Breeders will use the noise levels to rate a dam’s level of serenity (Figure 5) 8, so if a litter is crying regularly, it could be an indication of poor maternal behavior – for example, the bitch is not staying with the puppies enough, and/or the time spent nursing and licking them is insufficient. 

Factors shaping maternal behavior

Maternal behavior can be defined in two phases. A critical or sensitive phase, associated with important hormonal changes during parturition, followed by a maintenance phase, with a more psycho-sensory component that lasts until weaning 19. Although little information is available as to what elicits maternal behavior in dogs and how it differs amongst individuals, there are various possible factors involved.

Hormonal factors and stress

Various hormones are responsible for parturition in the bitch and they are probably also involved with maternal behavior, although how each hormone regulates this is poorly understood. The hormonal cascade will involve a drop in progesterone that initiates parturition, and an increase in the secretion of estrogens, oxytocin, relaxin, prolactin, prostaglandins and the down- and up-regulation of receptors. In particular, how prolactin and oxytocin regulate maternal behavior is still unclear. Oxytocin contributes to uterine contractions and seems to be important for maternal characteristics, with its influence well documented in other species, and low levels of the hormone have been associated with cannibalism in one canine study 20. Oxytocin levels in the saliva are not a predictive factor of maternal quality in the bitch 21, but intranasal oxytocin seems to help expression of maternal behavior after caesarean section 22. However, no controlled studies have been conducted to establish the effects of the hormone and a timeframe for when it is effective. Prolactin, as well as being responsible for promoting lactation, probably also contributes to maternal behavior, although it is not clear how it acts. The progesterone drop seems to play a role as well, since it explains the behavioral changes seen in pseudopregnancy.

Parturition and the establishment of maternity can be perceived as a stress situation. Overstressed bitches seem to struggle more to adjust to motherhood and the changes it requires. Dog-appeasing pheromones can reduce the stress and can positively modulate maternal care; their use has been shown to increase the wiliness of the bitch to stay with the puppies for longer, along with a better overall mother-offspring relationship 8.

Vaginocervical stimulation and amniotic fluid

Vaginocervical stimulation seems to be important for maternal behavior, since bitches that undergo a caesarean section without initiating parturition may have problems in displaying appropriate interactions with their puppies, although how important this stimulation is has yet to be proven (Figure 6).

Amniotic fluids also seem to play a fundamental role in directing a dam to accept her puppies 4,23. A bitch will refuse a puppy removed at birth and washed, but if the newborn is covered in amniotic fluid, she will then accept it again 23, so using amniotic fluid before presenting a litter to a bitch after caesarean section may improve maternal recognition.

Parity and litter size

The effect of parity on behavior seems to be relatively unimportant, as no major differences have been observed when comparing primiparous and multiparous bitches 1,4. The parturition experience improves a bitch’s recognition of the needs of the newborn, and reduces apprehension from the physiological changes around parturition 1. Multiparous bitches tend to show consistent maternal care, whereas primiparous improve in their maternal behavior over time 7. A study of dog breeders reported primiparous bitches to be over-represented with maternal behavioral problems 24, so it is important to monitor the process of parturition, in particular for nervous primiparous bitches, since the dam‘s inexperience can lead to her failing to display correct maternal traits and even exhibit abnormal behavior such as cannibalism. Dams with small litter sizes have more contact with individual puppies and tend to rank better for mothering attributes 1.

Genetics and breed

Genetics may have an important role in maternal behavior, but it is poorly understood, and selecting for good maternal care is not a priority for many breeders. Human interference could negatively impact how the dam interacts with her puppies, but avoiding breeding from offspring of a dam with poor maternal behavior may be advisable. Although there are anecdotal reports on how mothering qualities can vary between breeds, this has not been investigated in depth, and in one study no specific breed was singled out as being particularly problematic with maternal behavior 24. However, Golden Retrievers seemed to be better than German Shepherds in a study evaluating maternal behavior and success of puppy selection as guide dogs 2.

Inappropriate maternal behavior

The quality of maternal care may already be apparent during parturition. An inexperienced dam may not know what needs to be done to break the amniotic sac and tear the umbilical cord, increasing the chance of problems. Moreover, bitches that show little interest in licking their puppies may also have poor maternal behavior throughout the postpartum period. A bitch will normally choose a calm and safe environment to deliver her puppies, so if she feels threatened, she may become aggressive. Violence toward the puppies is rare and in general is towards strangers and other animals in the household. Even a very docile female can show signs of aggression if she perceives a situation to be a threat to her puppies. If aggressive behavior toward the puppies is observed, it is usually in the first days postpartum, typically in primiparous bitches, and may even lead to maternal cannibalism. Potential causes are excess stress, overcrowding and malnutrition, and low levels of oxytocin and blood lipids have been reported in the Kangal breed with a history of maternal cannibalism 20. Alternatively, in the author’s experience, a nervous primiparous bitch, when severing the umbilical cord, can unintentionally kill and eat her puppies. Lack of milk production (agalactia) can be also observed, typically in primiparous individuals, bitches that have undergone premature caesarean section, or have systemic illness, but no correlative studies have been done between agalactia and poor maternal behavior.

Maternal effects on cognitive development

Studies in rats confirm that the quality and quantity of interactions with the mother in the early postpartum period can influence the physiological, cognitive and behavioral development of the offspring. However, it is unclear if this can be extrapolated to a bitch and her puppies, and if so to what degree. The canine neonatal and transitional periods are characterized by rapid neurological development, and various studies looking at the impact of maternal behavior on an animal’s development are contradictory 1,2,3, with the results to date apparently depending on the dog’s breed and/or its prime functional aspect. So for military German Shepherd puppies, a high maternal score had a positive impact in the cognitive features required to perform their job 1, but when selecting guide dogs, puppies from mothers that showed greater levels of maternal behavior displayed characteristics that decreased their chances of selection. For example, they were more likely to have higher activity levels when left alone, they had a short latency period before vocalizing when presented with a novel object, and they showed low performance and perseverance in problem-solving tasks 2. In addition, the results of testing young puppies (aged two months) to handle stress situations were also paradoxical; higher maternal care improved the ability of puppies in a laboratory environment 25 but had a negative effect in puppies raised in a home environment 3.

There is no doubt that early interaction between the dam and the puppies can affect their cognitive ability. However, there are various unknowns; when is the crucial window during the postpartum period, what is the long-term effect on the performance and behavior of the dogs, and is it possible to compensate at a later stage for poor maternal behavior – and if so, how effectively? The socialization period, which starts around 3 weeks of age and ends at approximately 12-14 weeks, may be of greater importance, since puppies are more mature at this stage, and therefore more susceptible to both positive and negative effects of interactions with the dam, their littermates, other dogs and humans. Due to the many factors involved, the effects of early life experiences require further study and observation to better understand their impact on a dog’s development.

Conclusion

Many aspects of maternal behavior in the dog need still further consideration, but the veterinarian should be aware of certain factors that can, in particular, greatly influence the peripartum period. Perhaps most importantly, factors linked to the individual bitch and how they relate to her maternal behavior should be quantified. Anxious primiparous bitches, and any dog that has had a caesarean section, require closer attention in the first days of postpartum, and poor maternal behavior should be addressed as soon as possible in an attempt to avoid any long-lasting negative effects on the puppy and minimize unwanted behaviors later in life.