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Authors: John Bradshaw

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Thus dogs have to learn about species that are not their own, including humans. But do they also have to learn how to be dogs? In the 1961 experiment described at the beginning of the chapter, all of the puppies developed normal dog-to-dog social behavior because they were brought up by their mother—the normal circumstance for a wild animal, or indeed a feral dog. It was their dog-to-human social behavior that depended on their being exposed to people at between three and nine or ten weeks of age. They were still dogs, despite the fact that the ability of some of them to interact with our species had been compromised.

The extent to which dogs learn how to be dogs can be tested only if they never meet another dog from the minute they are born. In a series of experiments conducted in the 1960s, researchers demonstrated that puppies hand-raised from less than eight weeks old, and kept away from other dogs from then on, tended to be aggressive toward other dogs, presumably because they had forgotten, or had never learned, how to interact with members of their own species.
6
However, this was not a surprising result: Hand- or machine-raised animals of many species
show all kinds of abnormalities due to their restricted early experience (e.g., they have very restricted opportunities for play, which affects the development of their brains as well as their physical coordination).

A few years later a remarkably simple yet elegant study avoided these abnormalities, giving puppies as normal an upbringing as possible short of actually leaving them in their own litter.
7
Rather than raising puppies in isolation again, the scientists reasoned that a small enough dog could have a relatively normal life if brought up with a litter of kittens—normal, of course, apart from what they were testing, which was the opportunity to interact with others of its own species. The researchers worked with four litters of Chihuahuas. From each litter, two puppies were chosen to be raised in the normal fashion by their biological mothers. Another puppy from each litter, however, was instead introduced into a litter of kittens, beginning when the puppies were three and a half weeks old, at the beginning of the “sensitive period.” From then on until they were sixteen weeks old (i.e., after the “sensitive period” had ended), each puppy had only kittens as playmates. The stoical mother cats apparently adopted them without any fuss.
8

Chihuahua puppy fostered by a cat

Cat-raised puppy shying away from dog-raised puppies

When the behaviors of the two types of puppies were compared at sixteen weeks of age, the differences were remarkable. Each pup was presented with a mirror. This was a very exciting experience for the pups that had been raised by their own mother; they barked over and over again at their reflections, jumped up at the mirror, and pawed, scratched, and dug around it, presumably to get at the puppy they thought was on the other side. The cat-raised pups either ignored their reflections or acted as if they were something alien, gingerly approaching with their tails tucked between their legs. Presumably they had no mental image of what a dog looked like, having not seen one since their eyes began to work fully. When the two litters met, one dog-raised, the other cat-raised, the cat-raised puppies huddled together with the kittens and seemed not to know how to play with the dog-raised pups. If they interacted at all, they behaved just as they had done when presented with their reflection: keeping silent and tucking their tails away.

This is conclusive evidence that puppies do indeed have to learn how to be dogs—they are born with a basic repertoire of responses but need experience of other dogs before these can be properly expressed. However, the experiment also showed that even at sixteen weeks, when the window for socialization to people is about to close, dogs can rapidly adjust to living with their own species. After the initial experiments at sixteen weeks, all the puppies were put together. Within two weeks the cat-raised pups were playing like dogs; they were also reacting to their reflections as if they were other dogs.

This finding suggests that the “sensitive period” during which puppies learn how to socialize with other dogs is actually
longer
than the “sensitive period” for socialization to humans. However, since such research has never, as far as I know, been repeated or extended, a number of alternative explanations present themselves. For instance, it is possible that Chihuahuas develop their social preferences more gradually than the spaniels and beagles used in the earlier experiments. It's usually assumed that dogs have a single sensitive period during which they simultaneously learn about the other species they meet, but this possibility has never been examined scientifically; hence we do not know whether different types of dog have sensitive periods of different duration. We can be sure, however, that socialization to dogs and people is still far from complete at eight weeks of age, the time when most puppies are transferred to their pet homes.

It is remarkable, given how unformed a puppy's personality is at eight weeks old, that breeders rely so heavily on puppy behavior as a way of predicting the grown-up dog's eventual character. “Puppy tests” carried out at seven or eight weeks of age, before the puppy leaves its breeder, are still widely believed to have this predictive potential. Yet this is the precise age at which the puppy's behavior is at its most malleable. Numerous scientific studies have failed to find any validity in “puppy testing” as a predictor of future character. Most such tests also set out to predict characteristics that are probably erroneous, such as a direct correspondence between aggression and “dominance.” The only personality trait that seems to be resistant to change after seven weeks is extreme (genetically based) fearfulness, which is very rare; such a trait is so effective at inhibiting learning about new situations that it is virtually self-perpetuating.
Puppy tests may, however, be useful to prospective owners by indicating deficiencies in the breeder's socialization of the puppies that they will need to address. For example, the tests could reveal whether a puppy is fearful of men or children due to lack of exposure—though breeders are hardly likely to promote them for this purpose!

The sensitive period in today's wolves is much shorter than it is in dogs, indicating a fundamental change that must have arisen prior to or early on in domestication. Wolf cubs usually stay in the den with their mother until they are about three weeks old and only then emerge to meet the other members of the pack. Within a few days, they start to become fearful of all new animals that they meet; this “fear reaction” is what marks the end of their sensitive period. At this age, dogs are just
starting
their sensitive period, which will continue for another ten weeks or so. This extension of the socialization “window” must be a consequence of domestication. It's possible that the wolves that selected themselves for domestication had a longer socialization period than do the wild wolves that survive today, smoothing the initial transition from wolf to proto-dog, but it's also likely that the proto-dogs with longer socialization periods were more able to thrive in human environments. Thus, over a period of time, progressively longer and longer socialization periods were selected for, becoming fixed when no significant further advantage could be gained.

Today's wild wolves can become attached to people, but they are far more restricted than dogs in the number of attachments they can form. Wolves, like dogs, probably learn a “family odor” while they are in the den and are thus able to bond with the rest of the pack once they emerge into the daylight and can learn what the others look and sound like. If they are extensively handled by people during this period, they can become friendly toward them, but they usually restrict this behavior to the people who did the handling rather than generalizing to all similar people, as dogs seem to do. They also usually prefer wolf company to human company, however well acquainted with people they are. Thus imprinting in wolves is more similar to imprinting in birds than to socialization in dogs.

Nevertheless, what we see now in dogs must presumably have evolved from imprinting in wolves. The key changes are therefore likely to have been (a) the delay of the beginning of the “fear reaction” and (b) the
extension of learning about the characteristics of close “family” (whether biological or not) to other similar individuals. It is quite possible that these differences between dogs and modern wolves were already present in their common ancestor, making domestication easier; as I've already emphasized, we can only guess at what the behavior of this common ancestor was like. Presumably, domestication would have been very difficult if this ancestor had been as resistant to socialization as modern wolves are, so it is tempting to speculate that the onset of the fear reaction may have been somewhat later in (some) wolves then, as compared to wolves today.

The first three to four months of life are arguably the most important time in a dog's life. Born with a powerful urge to learn about the world around them, dogs adjust during this period to whatever type of environment they find themselves born into, from the back streets of a village in the Punjab to a New York high-rise. As with most animals, their default reaction to the unknown is fear. But for dogs, unlike most other animals, that fearful reaction is easily nullified by the right kind of experience. To be readily acquired, this experience has to be presented in a way that does not in itself instill fear. Puppies brought up in a chaotic, unpredictable environment can fail to assimilate the information with which they are being bombarded and develop into generally anxious dogs. Too much stimulation can be as damaging as too little. But everyday experience tells us that the majority of puppies do get roughly the right degree of experience, simply by being brought up in normal human households—precisely the environment that dogs have evolved to live within.

The sensitive period is when dogs
begin
to learn about people, not when that learning
ends
. Rather, as the sensitive period ends, a second phase begins. In the first phase, the “socialization period,” the puppy learned who it can trust; but once it is about twelve weeks old, it will start avoiding animals or types of people, even objects, that it has never met before. Individual relationships with other dogs also begin to appear at eleven to twelve weeks of age (see the box titled “
Brothers and Sisters
”). For many weeks after the socialization period is over, the young dog will greedily continue to gather information about its companions and the physical environment they live in, guided by the “friend or possible foe” categories established during the socialization period.

Brothers and Sisters

M
ost puppies are separated from their littermates when they're about eight weeks old, the typical age at which they go to their new homes. The evidence suggests that, even at eight weeks, they have only just begun to recognize one another as individuals (hence “dominance hierarchies” are even more unlikely than in groups of adults) and their “personalities” are not yet fully formed. Two students of mine tested these ideas by following the development of puppies in two litters, one of French bulldogs and one of border collies. They took siblings out of their litter two at a time and let them play together with a tug toy for one minute. They also observed the whole litter playing together, noting which puppies seemed to “win” when they were play-fighting. At six weeks, who “won,” whether in the pairs or the whole litter, changed from day to day, and each puppy seemed to begin each interaction afresh, as if it had no memory of which other puppy it was competing with. At this stage, puppies can tell their littermates apart from other puppies by their characteristic “litter odor,” but they may not be able to tell their brothers and sisters apart from each other. At eight weeks, who “won” had begun to settle into a pattern, and the puppies showed signs of investigating each other before and during the competitions, presumably trying to establish which puppy it was that they were playing with. However, even then there was no indication of anything resembling a “dominance hierarchy” within the litter. A puppy that had just “won” possession of a toy and was then put back into the litter was as likely as not to “lose” in a play-fight, even with the puppy it had just been paired with. At this age, puppies' personalities are still being formed, and they seem to be using their playing to try out all the personas available to them—giving in, holding back but then pouncing, trying to push every other puppy out of the way in quick succession, and so on. All this goes on under the watchful eye of their mother, and no one gets seriously hurt; indeed, it's at this stage that, by listening to feedback from the squeals of their “victims” (human as well as canine), puppies begin to learn to inhibit their bites.

It wasn't until the litters were about eleven weeks old that their relationships became consistent, with the smaller, less active puppies tending to give way to their heavier, more active littermates. Even then, there was no indication that the puppies had any concept of their “status” in the litter; rather, they were simply beginning to use their memories of previous encounters with their littermates to help them decide how best to interact with them.

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