How to Raise Resilient Puppies – An Ontogeny Perspective

How to Raise Resilient Puppies – An Ontogeny Perspective

In the last 10-15 years, the emerging field of behavioural epigenetics has revolutionised our understanding of the ways in which genes and experience – nature and nurture – interact during development to produce effects on one’s early experience. It is now known, for example, that a wide variety of environmental factors, including maternal behaviour, physical and emotional stress, and exposure to toxins, drugs and hormones – especially during the early part of life – can modify the expression of the genes that regulate the central nervous system without altering the DNA sequence. This essentially means that, while the genome still provides the design blueprint for the developing brain and nervous system, it is an adjustable blueprint that can respond dynamically to information and experience coming from the environment, and thereby alter the course of behavioural development in adaptive ways.[1] Furthermore, at least some of these changes in gene expression appear to be heritable in the sense that they can be propagated, either through germ cells or via the quality of parental behaviour, to affect later generations.[2]

It is important to stress that these changes in gene expression occur more readily at certain stages of brain development. The early growth and development of the brain is punctuated by periods of increased plasticity during which it is more susceptible to remodelling and reorganisation in response to environmental triggers.[3] These episodes of sensitivity tend to occur in similar sequence across mammal species, but the time scales involved may differ considerably from one species to another.[4] It is therefore important to specify the key stages of development that are characteristic of the canin familiaris and its nearest relatives.

According to the findings of the Bar Harbor studies and subsequent research by Champagne, Heim & Binder and Joffe, the early development of the dog can be divided into a series of six natural stages or periods:

1. the pre-natal period,
2. the neo-natal period,
3. the transition period,
4. the socialisation period,
5. the juvenile period and
6. the pubertal period.

The pre-natal period has been largely ignored as a developmental stage in the ontogenesis of canid behaviour and temperament. Nevertheless, numerous studies of rodents and both human and non-human primates indicate that transplacental maternal influences can exert significant long-term effects on the subsequent behaviour of the offspring. Subjecting female rats to stressful experiences during pregnancy activates the maternal hypothalamic-pituitary-adrenal (HPA) axis, resulting in the release of glucocorticoid (stress) hormones. Offspring exposed to sufficiently high levels of these maternal hormones in utero display enhanced stress sensitivity when tested later in life. Similar effects have yet to be investigated in dogs but female cubs a related canid, the blue fox, whose mothers were subjected to stressful handling during the last third of pregnancy, were found to display higher behavioural reactivity in novel test situations at 35 days post-partum than those of unhandled females.[5]

During the neo-natal period the puppy is still comparatively helpless and dependent on the mother, and adapted to the life of suckling and care-soliciting. At this age, from birth till approximately two weeks, the puppies are sensitive to tactile stimuli and certain tastes and odour, but their motor abilities are limited, and neither their eyes nor ears are open or functional. Due to the immature state of their neurosensory systems, it was originally assumed that canine neonates were largely incapable of associative learning. Subsequently, it has been shown that neonatal puppies can learn simple associations and only within the limits of their own rather specialised sensory and behavioural capacities.[6] Both Fox and Zimen reported that wolves hand-reared from birth or six days of age are more reliable and friendlier towards humans than those hand-reared from 15 days or later. The mechanism for this effect is most likely some form of olfactory imprinting during the neonatal period.

Episodes of early life stress (ELS) can also have marked long-term effects on the behavioural and physical development of mammalian neonates, including puppies. In rodents, intense or prolonged stress, such as two or more hours of separation from their mother, seems to intensify neonatal sensitivity to stressful or anxiety-provoking situations later in life. In contrast, mild to moderate stressors such as brief periods of separation from the mother and litter, or daily handling, appear to have a positive impact on the stress resilience as well as producing accelerated maturation of the nervous system, more rapid hair growth and weight gain, enhanced development of motor and problem-solving skills, and earlier opening of the eyes.[7]

Some canine studies have found similar effects. For example, puppies exposed to varied stimulation from birth to five weeks of age were found to be more confident, exploratory and socially dominant when tested later in strange situations than unstimulated controls, and puppies handled gently on a daily basis from three to 21 days after birth were calmer, more exploratory, and gave fewer distress calls in eight weeks old puppy isolation tests than littermates who were not handled.[8]

To account for these effects of ELS, recent research indicates that the effects of these mild-moderate stressors are probably mediated through the changes they induce in maternal behaviour when the pups are returned to the nest. Variation in maternal behaviour toward offspring during the neonatal period is now known to have profound and lasting effects on the development of their physiological and behavioural responses to stress.

These effects appear to be mediated by four key hormones – corticotrophin releasing hormone, arginine vasopressin, oxytocin and prolactin – all of which contribute in different ways to change the developing brain’s responsiveness to stress hormones.[9] Female dogs whose pups are subjected to experimental stressors tend to lick and groom them more than the mothers of unstressed pups, and this extra attention suppresses the puppies’ HPA responsiveness. Conversely, stressed mothers tend to engage in reduced levels of licking and grooming of their offspring which respond to this by developing higher reactivity to stress and a lower propensity to engage in parental behaviour as adults, thereby perpetuating the stress-sensitive phenotype across generations.[10]

The transition period is marked by a period of metamorphosis during which behaviours associated with the neonatal existence disappear and are replaced by those more typical of later puppyhood and adult life. The whole process takes about a week, beginning with the opening of the eyes at around 13 to 16 days and ending at approximately 18-20 days with the opening of the ear canals and the first appearance of the auditory “startle” response to sudden loud noises. There is also a sudden increase in visual cortex activity during this period all the way to maturation at six to eight weeks of age. Puppies also exhibit a number of changes in behaviour during this transitional phase. They show an ability to crawl forward and backward and begin to stand and walk, albeit clumsily. They start to eliminate outside the nest and anogenital licking by the mother is no longer required to stimulate elimination. Puppies begin showing an interest in solid food at this time. They also start to engage in social play with littermates and display social signals such as growling and tail wagging. Patterns of distress vocalisation also change. Whereas neonatal puppies yelp primarily in response to cold or hunger, a three-week old puppy will also yelp if it finds itself outside the nest in an unfamiliar environment, even if it is otherwise warm and well-fed.[11] In terms of learning and the effects of early experience, the transition period resembles a continuation of the neonatal period. Puppies’ performances on both classical and operant conditioning tasks show a steady improvement at this age, although rates of learning and the stability of the conditioned response do not reach adult levels until four to five weeks.[12]

The socialisation period in puppies was first described as a “critical period” for the formation of primary social relationships or social attachments.[13] Current evidence, however, suggested that the boundaries of this period is not always as rigid as originally conceived, and that behaviour or preferences acquired during this period can often be modified or reversed at later stages, albeit with varying degrees of difficulty. Authorities in this field now favour the term “sensitive period” when responses or preferences are acquired more readily than at other times.[14]

Primary socialisation in puppies has been found to be largely independent of associated reinforcers or punishers, although emotionally arousing stimuli, both wanted and aversive, seem to accelerate the process.[15] In the case of the domestic dog, this period enables puppies to form non-conspecific attachments for humans or other animals encountered socially. For example, puppies can recognise their littermates at four to five weeks of age and cross-fostered puppies raised throughout the socialisation period – three to 16 weeks of age – with only kitten littermates tend to avoid interacting with strange puppies when first exposed to them. This contrasts with their kitten foster littermates who will interact playfully with strange puppies on first encounter. Such experiments demonstrate that the character of the socialisation experience not only determines the young animal’s choice of future social partners but also to some extent, defines the species to which it belongs.

The ease with which most domestic dog puppies are able to establish non-conspecific social attachments is a product of selection under domestication. In contrast to wolves, domestic dog puppies readily form such attachments if they have some human exposure before seven to eight weeks of age and their socialisation window seems to remain open until around 12-14 weeks or even longer in some individuals.[16] This difference was due primarily to delayed maturation of the HPA axis in dogs resulting in retarded onset of the normal fearful/avoidant response to unfamiliar individuals and situations. Confirming this theory, Morrow et al detected significant breed differences in the age of onset of fearful/avoidant responses in puppies, as well as correlated difference in stress responses as measured by salivary cortisol.[17] Recent studies in dogs indicate that genetic polymorphism in the oxytocin receptor gene (OXTR) may account for the differences in prosocial tendencies between dogs and wolves.[18] This meant that the reduction in fear/avoidance and enhanced prosocial tendencies are outcomes of selection for extreme socialiseablity early in the domestication of selected dog breeds.[19]

During the sensitive period for socialisation, puppies may also form attachments for particular places, a phenomenon known as localisation. This process is not significantly different from the puppies’ ability to form non-conspecific attachments – the outcome is that puppies become attached to both the living and non-living parts of its environment at this age.[20] Puppies’ cognitive abilities develop rapidly during this period. Puppies at three to five weeks of age can learn to recognise novel objects they have viewed previously only on video and will subsequently exhibit less fear of the actual objects when tested at seven to eight weeks old.

In a definitive study conducted by Freedman et al (1961), the upper and lower boundaries of the socialisation period was determined to be “2.5 to 9-13 weeks of age approximates a critical (sensitive) period for socialisation”.[21] Eight litters of beagle puppies were tested in laboratory conditions until 14 weeks of age, during which time each pup received one week of moderately intensive human testing and handling before being returned to the litter. Some pups received this week of human socialisation at two weeks, others at three, five, seven or nine weeks of age. Five “control” pups remained unsocialised until 14 weeks of age. At 14 weeks, all the pups were tested for their responses to a “passive” human handler, to being walked on a leash, and to being strapped into a physiology harness and subjected to various arousing or unpleasant stimuli. Those socialised at seven weeks obtained the most favourable scores in terms of their reactions to being tested in harness. Control pups remained uniformly fearful and intractable even after many weeks of careful handling and petting.

Scott and Fuller (1965), through behavioural observations of naïve puppies to human handlers at different ages have confirmed Freedman et al’s findings. Although initially fearful in the presence of an “active” human handler, young puppies show a rapid increase in their tendency to approach and make social contact with an unfamiliar person between ages of three to five weeks. This tendency decreases thereafter. Conversely, puppies at three to five weeks show little or no fear of a “passive” handler but they become increasingly wary or fearful of strange individuals or situations beyond this age. Scott and Fuller concluded that primary socialisation period ran from about the third to twelfth week after birth with a peak sensitivity between six and eight weeks of age. During this period of peak sensitivity, the puppies’ motivation to approach and make contact with a  stranger outweighs its natural wariness.

Fox and Stelzner (1966) identified a period at around eight weeks old when puppies are hypersensitive to distressing psychological or physical stimuli. Their heart rates and rates of distress vocalisation in strange situations also tend to show developmental peaks during this six-to-eight-week period. Naturalistic observations of free-roaming dog litters have revealed that puppies also exhibit a peak in social play at around seven to eight weeks of age which would suggest that heightened sensitivity displayed by pups at this age may be related to the rapid acquisition of social skills.

The result of the Bar Harbor studies and related investigations by Guide Dogs for the Blind, USA, gave rise to various practical recommendations regarding the husbandry and training of domestic dogs.[22] Two basic rules for producing well-balanced and well-adjusted dogs were proposed.

• Ideal time to produce a close social relationship between a young dog and its human owner is between six to eight weeks of age, and
• Puppies should be introduced, at least in a preliminary way, to the circumstances and conditions they are likely to encounter as adults, preferably by eight weeks and certainly no later than 12 weeks.

The proposed rules should not be taken to mean that puppies are to be removed from the litter to bond with their eventual human owner. Studies on puppy morbidity and mortality showed that early-age removal from the litter and their mothers produced exceptionally high morbidity and mortality.[23] What the rules meant therefore, was the prudent selection of dog breeders whose practices (a) allow the eventual human owner to start meeting the puppy as early as six weeks old, (b) expose the puppies to the eventual and prevalent environmental conditions before handing over the puppy to its owner after 12 weeks of age, and (c) continue to influence the human owner’s practices in socialising the puppy to its environment including other species beyond 12 weeks to at least 12 months of age. These rules can rarely be achieved by commercial breeders who supplies pet shops, whose objective is unambiguously the rapid sale of adorable puppies given the high inventory cost. Perhaps uninformed and inflexible, Singapore’s authorities have tightened rules on dog breeding recently, effectively criminalising home-breeding and giving commercial breeders the free rein to continue producing problematic puppies in the cramped and chaotic Sungai Tengah area.

The juvenile and pubertal periods runs from approximately 12 weeks to two years old, depending on breed and size of the dog. This period of the young dog’s life is probably the least studied in terms of its effects on adult behaviour, despite the fact that gonadal hormones are known to modulate adolescent brain plasticity.[24] Anecdotal evidence certain suggests that experience during the pre-adolescent and adolescent periods can exert long-term effects on behaviour.[25] There is a neophobia period between seven to nine months of age where the young dog may form lasting aversion to certain humans and/or circumstances through single-event learning, especially if the event is drastic and sudden. Recent studies of working dogs have found associations between the dogs’ experiences during this period and long-term changes in adult behaviour.[26] Poor handling by novice baiters for instance could result in irreversible aversion to biting. That said, the silver lining is that environmental enrichment during puberty was found to completely erase the negative effects of early life stress on the HPA axis.[27]