As a result of such exchanges, there is a growing consensus that the dog’s supposed drive to “dominate” is, in fact, just a convenient myth for those who wish to continue physically punishing dogs—indeed, one that has been demolished by studies of both wolves and dogs. The wolf’s natural social behavior is now known to be based on harmonious family loyalties, not on an overwhelming and incessant desire to take control. Could such a desire for control conceivably have been induced in dogs during the process of domestication? It seems much more likely that precisely the opposite must have happened, since dogs that showed a tendency to control their human hosts would have been selected against, deliberately or accidentally. Yet despite all the accumulating evidence, old habits are proving remarkably slow to die, in terms of both training and the perception of dog as wolf.25 Thankfully, there are now some signs that the tide is beginning to turn; for example, some rapport seems to be developing between the old-school and reward-based trainers; Cesar Millan has even asked Dr. Ian Dunbar to contribute to his book Cesar’s Rules.26 The hope is that dogs will soon be universally portrayed as the utterly domesticated animals that they are, not as superficially cute animals disguising the demons that lurk within.
CHAPTER 5
How Puppies Become Pets
Dogs are not born friendly to humans. No, that’s not a misprint. Dogs are born to become friendly toward people, but this happens only if they meet friendly people while they’re still tiny puppies. Scientists have known this for half a century, but the implications are still not universally applied or even widely appreciated. Today, many puppies are still raised for the pet market under impoverished conditions—conditions that predispose them to a life blighted by fear and anxiety, causing behavior that will not endear them to their owners or indeed anyone else they come across. Yet all this is entirely preventable.
Domestication has not adapted dogs to human environments; it has merely given them the means to adapt. Exposure to both people and man-made environments must occur in a gentle and gradual way to enable them to learn how to cope. This process starts in about the fourth week of their life and goes on for several months. If the exposure is either deficient or defective, the dog will develop deep-seated fears or anxieties that can be very difficult to eradicate later. Although some details of precisely how this happens have not yet been scientifically explored, the overall process of this “socialization” is well charted, and it is a tragedy that so many puppies do not receive enough experience of everyday life to allow them to cope adequately with their life among humans.
In 1961, a short paper appeared in Science that completely revolutionized our thinking about the bond between man and dog.1 In order to study when puppies are most sensitive to exposure to people, researchers raised five litters of cocker spaniels and three litters of beagles in fields surrounded by a high fence, so that they never saw people—food and water were provided through holes in the fence. Then every other week from the time the puppies were two weeks old until they were two months old, a few of them were taken out to live indoors for a week’s “holiday,” receiving one and a half hours of intensive contact with people each day. At the end of their week’s socialization, they were put back in the field with their mother and littermates.
The timing of the “holiday” was absolutely crucial to how the puppies reacted to being handled. At two weeks old, they were too immature and sleepy to interact much, but the puppies taken out at three weeks were instantly attracted to the person looking after them. They would paw and mouth the researcher and play with the hem of his labcoat. Five-week-old puppies were wary for a few minutes but soon started boisterously playing with the person. Seven-week-old puppies needed two days of coaxing before they could be persuaded to play, and nine-week-old puppies took even longer, becoming friendly as late as the second half of their week’s holiday.
The timing of their first introduction to human contact was absolutely crucial to how the puppies reacted to people later on. All of the puppies in the experiment were taken out of the field when they were fourteen weeks old and at that point began to live with people like normal dogs. The five puppies that had spent all of their lives in the field never learned to trust people, even after months of intensive handling. The six that had been taken on “holiday” when they were only two weeks old and were then returned to the field for eleven weeks fared better: Though initially quite wary of people, they became somewhat friendly after a couple more weeks of gentle attention. All the other puppies were instantly friendly—remarkable, given that some had last seen a human over half their lifetime ago. The six that had not seen a person for ten weeks were initially difficult to leash-train, but training the others was straightforward.
Overall, the results indicated that puppies need some (but not very much) contact with people if they are to react in a friendly way toward them. There also seems to be an optimum age for this contact to be effective. Two weeks old appears to be too early. Twelve weeks old is definitely too late; by this age the puppies observed in the study had become fearful of anything they had never been exposed to when they were younger. This implies a window of opportunity between about three weeks and ten or eleven weeks of age—what the scientists referred to as their “critical period.”
The idea of a “critical period” derives from a 1930s study by Nobel Prize–winning biologist Konrad Lorenz. Suspecting that some animals have to learn their mother’s identity, rather than knowing it instinctively, Lorenz hand-raised a clutch of goslings. His prediction proved to be correct: Having never seen their mother, they adopted him as their “parent,” following him around like a pack of faithful hounds and paying no attention to their biological mother.
What Lorenz had discovered was the process now known as filial imprinting, whereby young animals learn the characteristics of their parents. 2 Geese will imprint onto the first moving object of about the right size that they encounter between approximately twelve and sixteen hours after hatching. In the wild, this is so likely to be the mother goose that the chances of anything going wrong are remote. It’s essential to their survival that goslings know what their mother looks like; otherwise, they could easily stray away from the nest and perish. But why do they need to learn this? Wouldn’t it be more sensible if they hatched with the mother’s image already burned into their brains? Biologists have no definitive answer to such questions, but perhaps learning is simply easier; three-dimensional images are probably difficult to encode in DNA. In fact, studies show that young birds are born with some built-in guidelines for what to look out for—something that moves, makes bird-type noises, and has a head and neck. (But not much more than this: For example, if prevented from seeing their mother, domestic chicks will readily imprint onto a stuffed ferret.)
Lorenz originally conceptualized his “critical period” as a rigid timetable of events. In the gosling example this enables a young bird that is mobile within a few short hours of hatching, and unlikely to survive for long on its own, to quickly latch onto its mother. It’s now known that there is more flexibility in this type of learning than was first thought: Subsequent research has shown, for instance, that a gosling hatched in an incubator and kept away from its mother until it is thirty-six hours old can nonetheless bond to her immediately. Thus the timetable isn’t quite as rigid as Lorenz originally thought it was, and for this reason these windows of opportunity for learning are nowadays usually referred to as “sensitive periods.” They seem to be modifiable according to circumstances, rather than coming to an abrupt end when a clock in the brain says they should. Nevertheless, it is true that eventually, after a few days, imprinting cannot be reactivated. The young bird’s brain does not wait indefinitely for the mother bird to show up; that door does eventually close as the baby’s brain matures.
Once the young bird has finished learning, persuading it to change its attachment to its mother is almost impossible. It will usually flee from other animals—a very sensible thing to do, considering that some might want
to catch and eat it. The blocking that prevents the young bird from accidentally forgetting its mother and latching onto something else is called “competitive exclusion”: Once a complete picture of the mother has built up, the imprinting process terminates automatically, preventing the bird from accidentally attaching itself to another goose if its mother is temporarily absent.
This “sensitive period” concept explains the behavior of many young animals. For example, it can explain why hand-raised rhesus monkeys, taken from their own mothers soon after birth, prefer to be with their surrogate “mother” rather than with real monkeys, even when the surrogate is only a cloth-covered, unresponsive dummy.
Dogs do this too: They imprint onto their mothers, and vice versa, and they do this using their number-one sense: olfaction. In one set of experiments,3 researchers collected scents from two-year-old dogs by placing cloths in their beds for three consecutive nights. The dogs had all been separated from their mothers since they were twelve weeks old or even younger. Nonetheless, when their mothers were presented with a selection of these cloths, they were much more interested in their offspring’s scent than in the scent of unrelated but otherwise similar dogs. Likewise, the young dogs’ behavior showed that they recognized their mothers’ scents. A second experiment done at the same time showed that two-year-old dogs were able to recognize their littermates by odor alone, but only if they were currently living with another member of the same litter. This suggests the existence of a “family odor” that reminded each dog of the brother or sister it was currently living with, even though the odor was coming from a dog living in a completely different household. Similar tests given to four- to five-week-old puppies showed that, even at that young age, they had already learned their litter odor. Unexpected abilities such as these serve to remind us that we still have a great deal to learn about how much information dogs get from odors, even those that are completely imperceptible to us.
However, the “competitive exclusion” principle doesn’t seem to apply to imprinting in the domestic dog. Puppies “imprint” not only onto their own mothers and littermates but also onto people. (Strictly speaking, this phenomenon is slightly different from true imprinting in that it does not seem to be restricted to one individual person, even at the start.) In fact, puppies can also “imprint” onto other animals that they have friendly encounters with during their sensitive period, such as cats. One of the beauties of the capacity for multiple socialization among dogs (and cats) is that they become fearful of one another only if they first meet in adulthood. I have usually kept both dogs and cats at home, and if they’re introduced to one another, carefully, when they’re young, they can become great friends. The illustration below shows one of my cats, Splodge, performing a tail-up rub, a sign of social bonding, on my Labrador re-triever Bruno, while he is wagging his tail in greeting (although I suspect neither understood much of what the other was saying).
Interspecies socialization expressed as species-typical greeting behavior
Sheep-guarding dog with its flock
Some traditional uses of dogs exploit this flexibility. The sheep-guarding breeds, such as the Great Pyrenees and the Anatolian Karabash, if raised with sheep, grow up to behave as if the flock is their family, although of course they behave like dogs rather than like sheep. I say “of course” because dogs’ capability to bond to two or even more species at the same time is so obvious that we take it for granted. Such a capacity, however, is highly unusual in the animal kingdom as a whole. Most animals are programmed by evolution to learn about just their own species and no other. Indeed, hand-raised animals often have great difficulty adjusting to living with their own kind, as zookeepers once found, to their dismay, when first trying to breed endangered species of carnivores, especially some of the wild cats.
Domestic dogs don’t appear to lose their species identity, even as they form attachments to humans. Not only do they learn about how to interact with other species, but there is no evidence to suggest that this in any way disadvantages them in terms of how they interact with other dogs.
The capacity to adopt multiple identities is unusual, but its origins must lie in regular biological processes. Likewise, since the capacity for interaction with humans can’t have sprung from nowhere, its antecedents must lie in the social behavior of the wolf. While I’m highly critical of the old “lupomorph” model when it’s applied to social structures, as a biologist my instinct is to look for something pre-existing for evolution to work on. Since dogs are neotenized wolves, it is logical to look for the answer in the behavior of wolf cubs and juveniles rather than in that of adult wolves.
When wolf cubs are born, they are looked after by other wolves. They learn the characteristics of those individuals based on the eminently reasonable assumption that they must be their parents or, in a large pack with existing helpers, their close relatives.4 When puppies are born, they are usually looked after by both their mother and their owner. Their mother’s characteristics are slotted into the “parent” category, simply because she is there and looking after them. This learning will be retained throughout life, forming the basis for one set of social preferences—namely, for members of their own species (as happens in both wolves and feral dogs). Their owners’ characteristics, since they don’t match this first category, will be slotted into a second category, generated spontaneously, because they are there and are also caring for them. Apart from this parallel recognition arrangement, there is no reason why everything else about these early social preferences should not be based on the same model—that of parent and offspring. Indeed, it is hard to imagine what an alternative model might be.
Put another way, we humans hijack dogs’ normal kin recognition mechanisms. The domestic dog puppy’s unusual capacity for multiple socialization is the mechanism whereby we can insert ourselves into their social milieu and substitute ourselves into a role that, in the wild, would be served by their parents. Until weaning is complete, the bond with the human owner is probably weaker than with the mother, but after that, attachment to humans is reinforced every day, when we feed our dogs, play games with them, and reward them during training. There are fewer opportunities for pet dogs to reinforce attachments to one another. Even in a multi-dog household, it is the humans who act as the parental figures, providing food, controlling where the dogs are at any given time of day, and so on. (There are of course a few intentional exceptions to this scenario, such as hunting dogs housed in packs and sled-dogs, whereby leadership from one dog is essential to the coordination of the team.)
Is this really imprinting? Dogs certainly imprint onto their mothers, but science has yet to determine whether they also imprint onto their first owners. Imprinting, in the narrow sense of a bond formed to a primary carer, cannot account for the generally outgoing nature of dogs and, more specifically, for how easy it is for many dogs to change their allegiance from one owner to another. During the early stages of their lives, most mammals learn both the general identity of their species and the specific identities of the individuals around them, especially those that look after them. Normally, the latter characteristic leads to the more powerful attachment—but not so in the dog, which shows a much greater flexibility, presumably as a consequence of domestication. However, imprinting, or something very much like it, does play a strong role in directing the dog’s preferences for who to approach and who to avoid. These preferences are set up early on in the dog’s life—specifically, during the socialization period.
Even though dogs can possess several “friendly” categories simultaneously (a capacity unusual among mammals), each individual has its boundaries. This is well exemplified by some dogs’ distrust of children. How do dogs know that children are little humans and not another species entirely? The answer appears to be that they don’t. Children are distinctly different from adult humans in a number of respects—the way they move, the sounds they make, and—probably of particular significance to dogs—the way they smell. Dogs that were never expos
ed to children during puppyhood can be very wary of them when they first meet them as adults, although, being dogs, they can easily be trained to overcome this initial reluctance. On the other hand, if their first encounter with a child involves the pulling of their tail and ears, such dogs can easily become irritable and snappy with other children. The dog generalizes between children, treating them as a category rather than as individuals. In the same way, during socialization, puppies must generalize between one adult human and another. Although puppies undoubtedly come to recognize some people as individuals, unfamiliar people are presumably categorized as “friendly” based on their similarity to the first few people the puppy has met.
This is why it is so important to (gently) introduce puppies to as wide a selection of people as possible: men as well as women (people wearing different kinds of clothes), men with beards as well as clean-shaven men, and so on.5 This process serves to expand the boundaries of what the dog categorizes as “adult human.” If the template is left too narrow, perhaps because the puppy meets only one or two kennel-maids during the whole of its sensitive period, it may react to the appearance of men with fear and anxiety. This is one of the (several) reasons why owners have difficulties with dogs from puppy farms and pet shops: The puppies’ concept of what the human race looks like is often too narrow, and they default to fearful avoidance of every other two-legged animal they meet.
As we have seen, the organization of the dog’s social brain is different from that of most other mammals. It can form multiple, on-demand, representational spaces for each of the species that the puppy encounters during the socialization period. This capacity may have a parallel in the way that young children learn languages. Many children around the world—though not so many in the United Kingdom or the United States as elsewhere—grow up hearing two or more languages spoken, and their brains adapt quite well to this circumstance: Each language seems to be stored separately, such that the child quickly becomes competent at not mixing them up when forming sentences. The change in the dog’s social brain may have been a product of domestication; alternatively, it may have arisen as a pre-adaptation to domestication in certain wolves that no longer exist in the wild today. Regardless, any dog that only meets other dogs until it is fourteen weeks old develops only one such space—defined initially by its littermates and mother, because they are all that is available, but potentially extendable to all types of dog a little later on in its life. The evidence suggests that a dog born in a human household develops two such spaces, one for dogs and one for humans (again, each with the capacity to expand to accommodate other types of dog, and other types of human, that don’t respectively look/sound/smell like the owner’s family). A dog born into a human household also containing a dog-friendly cat may develop three such spaces. And it’s possible that dogs born into households with small children develop yet another space—or perhaps they learn to generalize between adult and infant humans and thus essentially conceive of them as part of the same continuum of two-legged animals.
Dog Sense Page 16