Imprinting and Habituation
Posted on August 25th, 2016
Learning can happen before birth. Joe Hutto1 lived in the Wind River Mountains of Wyoming, where he got to know mule deer. Over the course of seven years, Hutto habituated them to his presence and was able to integrate himself into their society. Recognizing individuals allowed him to discern family relationships and to observe how the deer conducted their day-to-day lives. One deer who became pregnant happened to be very close to Hutto, and allowed him to follow her to where she would lie in her final weeks of her pregnancy. She even allowed him to lie down with her, put his head on her belly, and listen to her baby. He talked to the baby, and sang to it. Then, for several days, she was nowhere to be found. Hutto was worried. And then she appeared at his door. In the distance was an anxious youngster. Joe said hello to the little one, and he came running forward. Evidently the little one recognized his voice, which he had come to trust before he was born.
Learning before birth is not limited to mammals. We are thrilled by the mystery of sea turtles, who somehow return to the place of their birth to give birth themselves, several years later. No one seems to understand how they can do this. Surely their beach does not have a distinctive scent, or distinctive “look” from the sea. So how could they show up where they were born? I think I have the answer.
We built our house in the woods. One day I looked up our new driveway, and there was a huge turtle sitting there, staring at the house. I walked her to the side of the house, so she could continue down the hill to the river, and half an hour later, she was back in the driveway, staring at the house. Unlike my car’s GPS, which is happy to reroute me when I make a mistake, this turtle must have returned to a magnetic meridian that she used to guide her travel between pond and river. From her size, she might have been 30 years old, and had certainly made this trip between pond and river many times.
On another day, a big snake came down the driveway, tracing the turtle’s route. Our house was again in the way, but Mrs. Snake dealt with the issue with less evident confusion. She spent the night in the brush near our front door, and the next day continued on to the river — I could tell from the sound of the Blue Jays down near the river just where she now was. She apparently used about the same route as Mrs. Turtle, and was also making a semi-annual commute between pond to river.
On another day, I needed to go out the front door, and swung it open. A big turtle fell in. She had been standing on her back legs, struggling to get in through the glass. I don’t think she was the same turtle I’d previously seen, so this commuter route was starting to look like it once handled a lot of traffic.
So I thought I’d figured out the commuter route for these reptiles. But what happened next left me amazed. One day I stepped out onto the front porch to find a walnut up against the house. No, not a walnut. A tiny turtle, who’d flipped over on his back trying to get into the house. This little guy must have been born just a month or two earlier. He must have been born on the bank of the pond, and must be headed down to the river. As I thought about it, I realized that he had made this trip before: inside an egg, inside mom, he must have taken the trip from river to pond. On the trip, in the darkness of his eggshell, he must have sensed the critical magnetic meridian, and memorized it. Now he could do it all by himself. We think of turtles as not teaching their young anything, but this critical information was something that he must have learned from mom.
And so that could explain how a turtle hatched on a beach in the ocean could possibly figure out how to get back there when it was an adult: it could memorize while in the egg, either before or after the egg was laid.
What do turtles, snakes, and mule deer have to do with horses? Plenty. Youngsters have much to learn. A horse won’t wait for your trainer to arrive. He’ll need to get started earlier than that. And so a foal that is about to be born likely has a good idea of who he is. He likely knows one or two human voices, knows his mom’s voice, knows the voices of some of the others in the pasture.
“Imprinting“ is a word that is often heard, and is used by laymen very casually to describe some connection that has formed between two animals. The popular horse literature is full of references to imprinting, and the value of imprinting foals on humans.
A book Imprint Training of the Newborn Foal has been heavily promoted by its author, and has apparently been widely read. It won the 2012 Western Horseman Award, and happens to be published by Western Horseman, where the author happens to be a contributing editor of Western Horseman Magazine. Never shy about self-promotion, Miller writes about himself “Recognized internationally as one of the foremost authorities on equine behavior, Dr. Robert M. Miller has been named the recipient of the 2012 Western Horseman Award… The subsequent release of the book with the same title propelled Miller into the center of the emerging “Natural Horsemanship” movement and made him one of the most sought out lecturers at veterinary schools, equine symposiums and clinics on equine behavior.2“
Imprinting may be defined as the process in which a very young animal bonds with some other animal or thing. The term was first used to describe chicks who, at birth, quickly learned to follow their mothers on land and in the water. A similar attachment could be made if chicks were hatched in an incubator, and then provided with a box on a moving toy train, or a caretaker, to follow. The imprinting seemed to favor the first large moving object encountered. Konrad Lorenz used the term Prägung to describe what had happened, and this word translates to “imprinting.3“
Having hand-raised many baby birds with the idea that they would attach to me and be better companions, I can attest to the power of imprinting, as well as the damage it can do. Amelia and Buster had five babies that we hand-raised, taking them away from their parents at two weeks. These five cockatiels became great buddies of ours. On Sunday mornings we’d open the door to their room and call them, and they’d all fly down the stairs and join us for a session of “coffee, papers, and babies in bed.” We learned the meanings of many of the words they used — I estimated over 100 words used to signify their internal states in different contexts. But when it came time to raise babies, the boys never figured it out. Stewball and Freckles both were good at courtship, at mating, at sitting on eggs. They took the tougher day shift, so their wives could be out foraging in the room and relaxing. But when the little ones hatched, things went badly. Stewball knew how to feed the babies, and did a good job of that. (He still regurgitates on my knee to show me what a great spouse he’d be.) But his grooming was excessive, and he wouldn’t stop at cleaning up formula or adjusting a few feathers: he’d pull all the feathers out of the babies heads, one by one. And Freckles never learned what to do with a baby after it had hatched. We’d find a baby lying in the corner of the nest box, with Freckles busy sitting on the remaining unhatched eggs.
Bean was one that Freckles ignored, and we took him away from his dad when he was just a few hours old (and his eyes were still closed). His early days were spent in an incubator on my desk, on a different floor of the house than the other birds lived on. Until he fledged, he never saw his father or mother. But then we returned him to the room with the others. He immediately flew straight to his Dad, and hasn’t been far from his side since. We’ve never been able to understand how he decided who to bond with, but perhaps he had already bonded while in the egg, listening to his dad whisper sweet things to his mom in the nest box.4 Today Freckles and Bean share a dialect, making them easy to distinguish from the others.
Imprinting can certainly give a bird two identities. Our hand-raised birds seem to view themselves as birds most of the time, but some of them are very comfortable at times being a person. Stewball, for instance, is now sitting on my knee, grooming his feathers. Soon I will be going downstairs to watch TV. He’ll likely choose to come with me, and watch TV with us until his biological clock tells him it is bedtime. Then he’ll say the word that means “I need to go up.” We’ll take him back to his room, where he will spend the night with 6 other birds, including his wife. When I take him back upstairs to their room, he may make a kissing sound as he gets closer — an indication he is fantasizing about being with his wife. But then, as he flies from my shoulder to her, he switches to the cockatiel word for love. For this word, at least, Stewball is bilingual.
Early research focused on the following reaction of precocial birds, something that is now called “filial imprinting”. Filial imprinting is useful in fostering a mother-offspring bond, and makes perfect sense. Even if a bird could learn to follow a man in boots or follow a toy train, in nearly every case the big moving thing nearby is mom, and learning to follow her is a key to survival. We can be comfortable believing that such a feat did not originate with birds, but that young dinosaurs of many species might have also followed their moms.
Filial imprinting seems to have been found in every species of bird that has been studied. We are all familiar with pictures of ducklings following a human or a dog that they have imprinted on. Whether filial imprinting occurs in other species is an open question. While there is a huge amount of early learning in mammals, it is not clear that any of this learning should be called “imprinting.” While the general public is comfortable with the word “imprinting” when talking about young mammals such as foals, scientists don’t use the term. I won’t either, but I’ll need to account for the positive effects of early exposure, so keep reading.
The idea of sexual imprinting soon developed, as cases were reported in which a chick raised by foster parents might show sexual attraction as an adult to the species that had done the rearing. Sexual imprinting seems to be possible throughout the world of birds. Klaus Immelmann5 reviews literature that finds:
- An individual bird of one color that is reared by foster parents of the same species but a different color will prefer to later pair with another of the foster parent color. This has been found in ducks, domestic fowl, domestic and feral pigeons, zebra finches, and Bengalese finches.
- Sexual imprinting can occur when humans are the foster parent, and for 25 species ranging from herons, storks, and owls to crows and meadowlarks, a bird fostered by a human may choose a human to pair and mate with.6
- Sexual imprinting can occur when the eggs of one species are hatched and raised by foster parents of another species7.
In contrast to the willingness of birds to engage in sexual imprinting, and the willingness of researchers to study it, sexual imprinting has scarcely been examined in mammals, perhaps because it does not occur. One study found that mice raised by a different subspecies of mouse seemed to prefer that different subspecies as partners when mating.8 There have been many reports of males of various species of mammals trying to mate with things outside their species — a dog under the dining table mating with your leg, for instance — but all of these stories derive from lust and confusion, rather than imprinting. G once mounted his Parelli ball while we were playing with it, but he never met a Parelli ball until he was 8, and had not imprinted on it.
I believe it is safe to conclude that sexual imprinting does not occur in mammals.
Miller‘s book “Imprint Training“ advocates for intensely, intimately handling newborn foals, pinning them down and doing this in very long sessions at birth, when it first stands, and when it first walks. Clinton Anderson seems to advocate equally rough treatment of a foal in a video.9 Of course we should listen to Anderson, because (according to him), “Clinton and Downunder Horsemanship are recognized as world leaders in the equestrian industry and continue to offer the very best in innovation, inspiration and instruction.” The techniques proposed by Miller and Anderson do not seem to have anything to do with imprinting, however, but rather with roughing up the newborn. As understood by scientists, parents don’t manhandle their babies during imprinting. They care for them. The baby figures who to love and follow.
However, a number of studies conclude that the “imprinting” advocated by Miller and Anderson do not work, and is not a good idea.
- A study of an imprint training procedure conducted at birth on the reactivity of foals at age 1, 2 and 3 months indicated that the procedure failed to result in a significant difference in the reactivity of trained foals, as measured by changes in heart rate, time needed to complete tasks and foal behavior.10
- Williams and others studied 131 foals and divided them into different treatment groups: no imprint training, imprint training four times (at birth, 12, 24 and 48 h after birth), or imprint training once (at birth, 12, 24, 48, or 72 h after birth). Foals then received minimal human handling until they were tested at 6 months. The researchers concluded that neither the number of imprint training sessions (0, 1, or 4) nor the timing of imprint training sessions (none, birth, 12, 24, 48, or 72 h after birth) influenced the foal’s behavior at 6 months of age.11 In this study, imprint training did not result in better behaved, less reactive foals.
- Hausberger and others studied 21 breeding farms and 170 horses in France, finding that those with easy and calm yearlings and young horses were farms where handling occurs mainly around weaning and/or in the following year, whereas farms with fearful young horses were characterized by either very intensive and permanent handling (from imprinting to daily halter fitting, handling, leading etc.) or by no handling at all after weaning and the following year. To produce a calm horse, the best approach seems to be moderation in the handling of foals.12
Familiarity and Comfort: Another Means of Learning to Recognize Kin
We know that kin recognition occurs throughout the animal kingdom, including single-celled organisms. There does not seem to be a general theory of how this happens, so I’m free to offer my personal views here. First, it seems unlikely that each species developed its own means of deciding who is kin. So we need to consider a thread that could run through the entire animal kingdom. Such a thread could be that of familiarity.
- All organisms have had some experience with themselves. If they have a sense of smell, then their own odor is surely familiar. Many animals have hearing, and can make sounds; such sounds will be familiar.
- Repeated exposure breeds familiarity, and familiarity breeds comfort. Individuals are drawn to those that are comforting. In the course of doing this, comfort breeds greater familiarity, strengthening the bond between individuals.
- The more another individual smells or sounds or looks like us, the more likely they are to be kin. But in many species, kin recognition could simply be an artifact of familiarity.
Familiarity could account for both “normal” kin recognition (that is, a wolf raised by wolves) and “abnormal” kin recognition (a child raised by wolves). But it doesn’t account for kin recognition in animals that don’t have the degree of parenting offered by birds, mammals, alligators, and some fish.
How does familiarity breed comfort? It might be because familiarity lowers plasma corticosterone levels in birds,13 which underlie stress. It may be that familiarity shapes the effects of oxytocin, making us want to associate with and protect those we are familiar with, and be more violent or aggressive to those we are not familiar with. Whatever the mechanism, it seems likely that hormone levels play some role.
An instinct is an unlearned fixed action patten that is triggered by some stimulus. In his fabulous book “Illumination in the Flatwoods: A season with the wild turkey”, Joe Hutto14 describes how very young turkeys walking through the woods were able to behave differently toward poisonous and non-poisonous snakes on their first encounters. Because his turkeys had never been out of his sight, Hutto could be sure that these encounters were their first. It seemed clear to me that some clues to species identification were buried in these turkey’s brains at birth, and guided their reactions appropriately.
Instinct might explain how turtles choose partners. Turtles have almost no contact between parent and progeny. Dad inseminates mom and leaves. Mom lays eggs and leaves. The only real contact is while junior is in the egg, inside mom. But turtles don’t hang out in schools or flocks. They live solitary lives, and are found together only when something of common interest has drawn them, such as a feeding station on a dock in the river. Instinct, rather than acquired familiarity, must explain turtle choice of partners. But just exactly how this works is a mystery — at least to me.
Other reptiles, though, get more nurturing in childhood. Mrs. Alligator, for instance, carefully builds a nest, guards the nest from predators, and as the babies hatch, helps them get out of their shells. She carries them to nearby water in her mouth, and protects them for a year or more. For mama alligator, some mix of instinct and childhood experience may be crucial to her success as a mother.
People who have the chance to work with foals will often make a claim that they spend time with them so that they will imprint on humans. Certainly spending time with a foal gives them a good headstart in understanding and accepting the ways of the bipedal world.
Familiarity seems like a perfectly useful explanation of how a foal might learn to recognize his kin. And there are a number of studies that suggest that early exposure to humans might be good for foals. In one experiment,15 lamb twins were used to determine the effect of exposure to humans. Lambs were fed milk replacer and handled four times a day for five minute periods at the ages of 1-3, 3-5, 5-7, or 7-9 days. Those lambs that received this 40 minutes of human contact at the age of 1-3 days were less timid and more willing to make contact with a human than those exposed later in life or their twins, who were not exposed. But even if we are willing to extrapolate from lambs to horse foals, we should not extrapolate from 1-3 days to 1-3 years. Early contact seems to be far more important in building comfort with human contact.
By the definition used by scientists, there is a sensitive period that is critical for imprinting: During this period, the youngster is best able to learn who it is, and who it should follow. As this period of greatest sensitivity comes to an end, exposure produces weaker learning, weaker tendencies to follow. The abruptness of the end of the sensitive period may depend on the species. But in the studies which use the term “filial imprinting”, the critical period is a matter of hours or days, not weeks or months.
This is not to say that later contact with an animal is without benefit. Handling birds and mammals under positive circumstances can lower their stress when people are present, decreasing the effects of humans on their health, fecundity, productivity, and welfare.
We should also expect that early gentle handling might lead to improved learning capabilities when working with human trainers. Williams et al16 review this literature: Foals which received handling sessions that lasted varying periods from one week to 18 months, beginning at weaning, learned more quickly and had fewer errors on a learning task than foals that did not receive any handling. Foals that received more handling learned the quickest and had fewer errors than those foals that received less handling;17 Williams et al also cite a study finding that foals handled 5 days/week beginning 24 h after birth and ending 42 days after birth were trained to lead more quickly than those handled beginning at 42 days and lasting until 84 days after birth.
Short periods of positive or reinforcing handling can alleviate animal stress in the presence of people, decreasing its impact on animal health18, fecundity19, productivity20 and welfare21. In chickens, daily habituation to non-threatening people increases egg production22 and allows them to gain weight faster with less feed.23 Food rewards and gentle handling decrease the heart rate, adrenal response and flight distance of sheep in the presence of people24. Gently stroking pigs whenever they approach people, increases approaches towards people, growth rate and feed-conversion efficiency25. We should assume that at all ages, increased familiarity with people will improve a horse’s comfort with them, and in turn, will improve their well-being. So spend some quality time with your horse!
How much benefit you get from contact with your horse may depend on many things. Here are a few:
- Five daily sessions of 20 minutes each will likely produce more benefit than one session of 100 minutes. In general, repeated distributed exposures will allow for a dissipation of satiation with each other, and you’ll get more bang for your buck. Of course, if you must drive 20 minutes for such a session, massed exposure as a single 100 minute session is more practical.
- Quality does matter. You are teaching your horse that you can be trusted, that you are gentle, that you won’t hurt him. Every time you behave otherwise and betray the developing trust, the more work you will need to put in to restore it. So if you are in a foul mood, stay home. If your horse doesn’t want to do what you want to do, change your plans to suit his. Remember that while familiarity with a consistently pleasant person can breed comfort, familiarity with the unpleasant can breed contempt.
- Ensure that your rules for kindness are followed by others who interact with your horse. Your horse will both distinguish between people and generalize to all people. So when their vet comes to judge the Pony Club contestants, of course the ponies will move off in different directions — distinguishing between people, and wanting to avoid the vet. But if your horse was repeatedly twitched at the track, even if you would never twitch him, he may fear your hand near his head for years afterward — generalizing to all people, and wanting to avoid hands near his head.
- If your time with your horse must be limited, give him as big a dose as you can. Speak softly. Rub him. Scratch his chest and neck. Let him see you from all angles, and both of his sides, coming and going. Spend that time doing what he loves. Carrots won’t hurt: he’ll associate his happiness with your presence.
This is an excerpt from a recent draft of “Horse Play”, a book I’m writing about how humans can have more fun with horses. The first edition of the book should be completed sometime in 2017, and initially published for the Kindle. I would be grateful for constructive comments on this piece.
1 This is the most remarkable book you may read this year: Hutto, J. Touching the Wild: Living with the Mule Deer of Deadman Gulch 1st Edition Skyhorse Publishing. April 1, 2014 320 pp
2 Miller, R.M. “Western Horseman Magazine names Dr. Miller ‘2012 estern Horseman Award Honoree'” http://www.robertmmiller.com/20wehoofye.html
3 Prägung also translates as “coining”, “stamping”, and “engraving”.
4 Chicks will begin peeping from within the egg before hatching, and listen to the sounds of the mother while in the egg. Auditory fillial imprinting in birds begins before birth. See Gottlieb G (1965) Imprinting in relation to parental and species identification by avian neonates. J Comp Physiol Psychol 59: 345-356
5 Immelmann, K. (1972). Sexual and other long-term aspects of imprinting in birds and other species. Advances in the Study of Behavior, 4, 147-174.
6 Klinghammer, E. 1967. Factors influencing choice of mate in altricial birds. In “Early Behavior: Comparative and Developmental Approaches” (H. W. Stevenson, ed.), pp. 5-42, Wiley, New York.
7 Immelmann, K. (1972). Op. Cit.
8 Mainardi, D., Scudo, F. M.. and Barbieri, D. 1965. Assortative mating based on early learning: population genetics. Ateno Parmense 36, 583-605.
9 DUHorseman “Foal Training: Touch and Rub” https://www.youtube.com/watch?v=N4A8rCZZFfU
10 Williams, J.L., Friend, T.H., Toscano, M.J., Collins, M.N., Sisto-Burt, A. and Nevill, C.H. (2002) The effect of early training sessions on the reactions of foals at 1, 2 and 3 months of age. Appl. anim. behav. Sci. 77, 105-114.
11 Williams, J. L., Friend, T. H., Collins, M. N., Toscano, M. J., Sisto-Burt, A., & Nevill, C. H. (2003). Effects of imprint training procedure at birth on the reactions of foals at age six months. Equine veterinary journal, 35(2), 127-132.
12 Hausberger, M., Henry, S., Richard, M.-A., 2004a. Expériences précoces et développement du comportement chez le poulain. In : Compte-rendu de la 30ème Journée de la Recherche Equine, 3 mars 2004, Paris, pp. 155-164
13 Barnett, J. L., Hemsworth, P. H., Hennessy, D. P., McCallum, T. H. & Newman, E. A. 1994. The effects of modifying the amount of human contact on behavioral, physiological and production responses of laying hens. Appl. Anim. Behav. Sci., 41, 87–100.
14 Hutto, J. (2006). Illumination in the Flatwoods: A season with the wild turkey. Globe Pequo
15 Markowitz, T. M., Dally, M. R., Gursky, K., & Price, E. O. (1998). Early handling increases lamb affinity for humans. Animal Behaviour, 55(3), 573-587.
16 Williams, J. L., Friend, T. H., Collins, M. N., Toscano, M. J., Sisto-Burt, A., & Nevill, C. H. (2003). Op cit.
17 Heird, J.C., Whitaker, D.D., Bell, R.W., Ramsey, C.B. and Lokey, C.E. (1986) The effects of handling at different ages on the subsequent learning ability of 2-yearold horses. Appl. anim. behav. Sci. 15, 15-25.
18 Maier, S. F., Watkins, L. R. & Fleshner, M. 1994. Psychoneuroimmunology: the interface between behaviour,brain, and immunity. Am. Psychol., 1004–1017.
19 Hemsworth, P. H., Barnett, J. L. & Hansen, C. 1986a. The influence of handling by humans on the behaviour, reproduction and corticosteroids of male and female pigs. Appl. Anim. Behav. Sci., 15, 303–314.
20 Seabrook, M. F. 1972. A study to determine the influence
of the herdsman’s personality on milk yield. J. Agric. Labour Sci., 1, 44–59; Apple, J. K., Unruh, J. A., Minton, J. E. & Bertlett, J. L.
1993. Influence of repeated restraint and isolation stress and electrolyte administration on carcass quality and muscle electrolyte content in sheep. Meat Sci., 35, 191–203.
21 Dawkins, M. S. 1980. Animal Suffering: The Science of
Animal Welfare. London: Chapman & Hall.
22 Barnett, J. L., Hemsworth, P. H., Hennessy, D. P., McCallum, T. H. & Newman, E. A. 1994. The effects of modifying the amount of human contact on behavioral, physiological and production responses of laying hens. Appl. Anim. Behav. Sci., 41, 87–100.
23 Hemsworth, P. H., Coleman, G. J., Barnett, J. L. & Jones, R. B. 1994. Behavioural responses to humans and the productivity of broiler chickens. Appl. Anim. Behav. Sci., 41, 101–114.
24 Hutson, G. D. 1985. The influence of barley food rewards on sheep movement through a handling system. Appl. Anim. Behav. Sci., 14, 263–273.
25 Hemsworth, P. H. & Barnett, J. L. 1991. The effects of aversively handling pigs, either individually or in groups, on their behaviour, growth, and corticosteroids. Appl. Anim. Behav. Sci., 30, 61–72.