Dog Sense (25 page)

In this
juvenile period
, which is generally assumed to extend from the onset of the fear reaction until puberty at about one year of age, the young dog's character is still very malleable. The experiences it has during this time can have a profound effect on its personality for the rest of its life. In fact, there is some evidence that the month or so immediately after the socialization period, between twelve and sixteen weeks of age, is almost as important to the development of the dog's adult personality as the socialization period itself, but surprisingly little research has been done on the effects of the environment on a dog's behavior at this age. For example, few studies have examined the benefits of “puppy parties,” which, as noted in
Chapter 4
, are structured socialization sessions for juvenile puppies (see box titled “
Puppy Parties
”). Among those that have, researchers found only weak effects on, for example, obedience, even though regular socialization sessions for puppies are widely believed to be an essential part of dog ownership.

In contrast to the sensitive period, there is no evidence for anything special about the processes whereby puppies in the juvenile period adjust their behavior to their surroundings; the normal processes of learning are quite adequate to account for this. It's simply that as the dog gets older and more set in its ways, its capacity to deal with change gradually diminishes.

The learning that takes place during the juvenile period is often loosely referred to as “socialization,” but this term really ought to be reserved for what happens during the sensitive period. What seems to happen in the juvenile period is that the young dog, now vaccinated and able to go out and encounter the world, learns more about what the world is like, how to deal with it, and what strategies work best when coping with the unexpected. The former can be likened to an inventory of things that the dog recognizes and has a suitable reaction for; the latter, to a toolkit of default responses when the usual rules-of-thumb don't work. For example, research has shown that hearing fireworks during either the socialization period or the first few weeks of the juvenile period protects puppies against becoming fearful of loud bangs. Puppies that don't hear loud noises until later on are more likely to develop noise phobias. Thus, in general, dogs that fail to develop both knowledge and coping skills become especially vulnerable to developing
rather nonspecific anxieties and will tend to adopt strategies based on avoidance, or even aggression, when they are confronted with something unfamiliar that they feel they can't deal with.

“Problem” dogs—dogs whose owners have actively sought help for their pets due to behavioral issues—reveal a great deal about the importance of early-life experience. A decade ago I did an analysis of clinical records, looking for factors that might predispose dogs to show fearful aggression or avoidance.
⁹
Specifically, I was looking for dogs that had been bred in kennels and never brought into the house, and then gone to homes where they had been largely kept away from people other than their owners: Due to their restricted early experience, such dogs should find it much harder to cope with novel experiences than the average dog. None of the dogs was “wild”; they had all received some contact
with people during their “sensitive period,” or it would have been very unlikely that they'd ever have become pets.

In certain ways, these dogs functioned normally. They were no more likely than the average dog to be aggressive toward their owners, with whom they'd had every opportunity to develop a normal relationship. Nor were the dogs bred in kennels predisposed to become aggressive toward other dogs; after all, they'd had a typical amount of exposure to their own species. But they were different in one crucial way: They were often aggressive toward people they didn't know, or tried to avoid them when they met. I found an anticipated exception in the small number of dogs that had left the kennels where they had been born at seven weeks of age rather than the usual eight weeks and then happened to have gone into a busy urban family environment. Puppies taken out of kennels at a young enough age seemed able to compensate for their restricted early experience.

The great majority of these dogs had been homed at eight weeks, which is standard because it is when the puppies can be fully weaned. However, this age is also right in the middle of the “sensitive period” for socialization, so it has been suggested that a sudden change of environment at eight weeks may be particularly stressful for the puppy. There have been few other studies of this kind that could test this idea, and none in which the age at homing has been varied systematically. We therefore cannot yet be sure what is the optimum age for building up dogs' experience of the world—although we do know that, to be most effective, it should start before seven weeks and should go on for several months after that. There is also some evidence that taking puppies out of their litters before eight weeks of age predisposes them to become fearful of other dogs, so ideally the whole litter should be kept together until eight weeks, while at the same time beginning to introduce them to a wide variety of humans.

The process that leads to the bond between dog and owner is therefore set in motion when the puppy is about three weeks old. The behavioral strategies established during the sensitive period channel the puppy's behavior and set the ground rules for the subsequent formation of close relationships with individual human beings. Puppies that are given only very limited experience of the man-made world are likely to fail to adapt to
that world when they meet it. Specifically, although they should be able to form well-balanced relationships with their owners, they may react fearfully toward other people, due to their impoverished experience of the human race in all its diversity. Their default strategy for dealing with anything unknown may be to try to flee from it, rather than adopting the cautious curiosity that is the default strategy of the well-balanced dog.

All of this presupposes that a dog's formative experience begins at three weeks of age. However, the dog has already existed for twelve weeks before this—nine as a fetus and three as an apparently helpless puppy. When the original research into the dog's sensitive period was conducted fifty or sixty years ago, it was thought that fetuses and helpless newborn animals were incapable of learning very much and would grow along a predetermined path unless some catastrophe occurred. Reinforcing this idea was the anthropocentric view that newborn puppies, being blind and deaf, were incapable of learning much about their environment. Their sense of smell was largely forgotten about, although we now know that puppies can learn to distinguish between odors even before they are born as well as during the first three weeks following their birth. In short, this research largely overlooked the possibility that the twelve weeks following conception may be a time when reactions to the world are influenced by outside events.

Although dogs have not been studied with regard to external influences during the time from conception to birth, scientists believe that this period may be particularly critical to the development of behavior. We now know, from studies of other species, including our own, that the environment experienced by the mother can have profound effects on the character of her offspring. Research on rats, mice, monkeys, and humans has shown that the development of the fetal brain can be powerfully influenced by the mother's experiences during her pregnancy. There is no reason to suppose that the same does not apply to dogs. Most of the research on brain development in the fetus has focused on severe stress experienced by the mother. In our own species, it is now well established that maternal stress can be linked to a whole range of mental disorders in children, including chronic anxiety, attention deficit hyperactivity disorder (ADHD), and inadequate social behavior. Longer-term problems
can result, including poor intellectual and language skills, lack of emotional control, and even schizophrenia. Studies of rats have shown that these problems almost certainly stem from the effects of stress hormones produced by the mother that cross over the placenta into the fetus itself. There, they change the way that the brain is developing, resulting after birth in reduced activity of some neurohormones (e.g., dopamine and serotonin) and a hyperactive stress-response system. Although the details vary slightly depending upon the stage of pregnancy during which the stress occurs, the young animal can then exhibit impaired learning, poor play skills, and a weakened ability to cope with challenges.

Luckily, these deficits appear to be reversible if the infant receives additional maternal care after birth,
¹⁰
but they can also be made worse if the young animal is taken away from its mother prematurely or if her maternal skills are deficient. Surprisingly little attention has been paid to this phenomenon in domesticated animals, despite the potential lessons to be learned about how best to look after them. One study has shown, however, that domestic sows kept in unstable social groups not only become stressed, but their female offspring are, in turn, more than usually aggressive toward their own piglets, implying a profound and long-lasting effect on the development of their brains.
¹¹

Are these effects all pathologies, or do some of them actually prepare the young animal to cope with a changing world? Because much of this research has been done in an effort to substantiate factors affecting mental illness in humans, less thought has gone into trying to understand why evolution has allowed stress experienced by the mother to affect her offspring so profoundly. Indeed, the general assumption has been that these are pathologies beyond the reach of natural selection. Nevertheless, research on guinea pigs (and birds) suggests that it may sometimes be helpful for offspring to be pre-programmed in this way. Female guinea pigs that give birth in overcrowded social groups tend to produce female pups that behave more aggressively than normal. Their male offspring, on the other hand, become “infantilized”—for example, continuing to play-fight at an age when their normal counterparts are competing with other males for real. These changes may actually prepare the young guinea pigs for the environment in which they will live: In order to find food and space to breed in a crowd, females need to be
pushy whereas young males need to keep their natural competitive nature in check until they are big and strong enough to win against the most experienced males.

Thus it's quite possible that some of the changes in the brain wrought by maternal stress are, at least to some extent, adaptive—in the sense that they prepare the offspring for an uncertain world. However, this is more likely to be the case with wild animals than with domestic animals such as dogs; any response to stress that evolved in the wild ancestor, the wolf, is unlikely to still be adaptive in the man-made environment of today.

All these findings strongly suggest that dog breeders should place great emphasis on the psychological well-being of their breeding bitches. They should neither induce the stress of separation by isolating them for long periods nor allow the bitches to be intimidated by other dogs. Some of the deficits that I found in dogs born in nondomestic environments were quite possibly due as much to stress induced in their mother as to impoverished experience during the first eight weeks of their lives. (The owners who brought the dogs in for treatment were simply unable to give us this kind of detailed information about the environment in which their dogs had been born.) Purchasers of puppies, too, would do well to examine the conditions under which the breeder keeps her bitches as well as the environment experienced by the puppies themselves. Of course, owners also have a duty to ensure that their new puppy gets the right kind of experiences during its first few months, but however good these are, there is a risk that they may not be sufficient to completely reverse the consequences of having had a chronically stressed mother or an impoverished environment during its first eight weeks.

Overall, it's clear that a puppy's experiences, from soon after conception to when it is roughly four months old, play a crucial role in affecting its character. A dog that gets the wrong start in life can grow up to be overly fearful or anxious. This is not absolutely inevitable, as nature has built in a capacity, up to a point, to compensate for setbacks early on and return development to a balanced trajectory. Nevertheless, there is much we still don't know about why some dogs develop behavioral problems and others don't.