How an instinct is learned: early experience

Starting developmental studies we first of all should take into account major differences in ontogenetic scenarios of species.

In mammals and birds two main types of ontogenetic scenarios are usually distinguished. Some animals are born in a relatively undeveloped, helpless state and very dependant on their parents for survival. These animals are known altricial animals. Tree nesting birds, rats and humans can serve as examples. Other animals are said to be precocial and are born almost fully developed and are able to move about. Examples include poultry (and of course wild ducks, galliforms, and turkeys), hoofed animals and some others, for example, guinea pigs and hears.

It is important to note that taxonomically closed species can possess principally different types of development. For instance, hears and guinea pigs are precocial whereas rabbits, rats, mice, hamsters and many other rodents are known as altricial. What may be even more important is that there are a great many of specific behavioural types of development within each of these two major categories. For example, in small rodents Baiomys tavlori young are adhere by suction to a mother for a whole day liberating her only at night so she can collect some food. Young rats and mice enjoy mother’s good graces for very short periods round the clock. In wild rabbits suckling is possible for pups for a few minutes only once a day, and young tree-shrews see their mother shortly once two days (for a review, see: Manning, 1979,).

Different schemes of interaction between parents and offspring in combination with effects of early experience, and effects of maturation of nerve and motor system result in a variety of ontogenetic scenarios. That is why it is difficult to squeeze behaviour of species into the limits of general schemes. However, we can consider several sets of examples to illustrate sophisticated inter-relations of different factors that shape animal behaviour. We will be focusing here on impact of processes of maturation and early experience on development of species-specific behaviour.

Determination of the provenance of a species-typical behaviour is possible by the use of the so called “ Kaspar-Hauser “(deprivation) experiments. “Kaspar-Hauser” - monkeys, chicks and other subjects received their name from a real prototype: an early 19th century " wild child" found wandering the streets of Nuremberg which was thought to be the princely heir to the royal throne of Baden. Kaspar seemed to be raised in strong deprivation and hardly could behave like a human being. Adopted by a kind tutor, Hauser was taught the ways of civilised society; meanwhile, growing political machinations threatened to destroy him, and finally Hauser was found dead (probably killed) five years after he was first discovered.

In deprivation experiments with animals subjects are given no opportunity to learn the skill components under investigation. For nest-building, for example, young birds might be prevented from seeing a nest or nesting material until their arrival at breeding age. If these birds are then immediately able to build a nest successfully, nest building does not depend on these sorts of experience. Spalding (1873) first applied this approach to reveal innate components in behaviour of birds, and Cuvier used this method to observe dam building in beavers. Ladygina-Kotts (1935) revealed innate features in chimpanzee’s nest building. Further many authors have used deprivation procedure in order to separate innate and learned components in animal behaviour. This method is often criticised because the " deprived" environment is still an environment so it is difficult to obtain clear results. Nevertheless, this approach sometimes allows lifting the veil of mystery from developmental problems.

Another experimental procedure that helps to separate components of behaviour is cross fostering. Cross fostering techniques, in which infants are taken from their biological parents and reared by unrelated parents from the same and even from alien species is widely used in behavioural research. Many cross fostering experiments have demonstrated that members of species retain at least main features of their species specific behaviour and do not follow habits of their foster parents. There are many stories about how people switch the eggs of a brooding duck with those of a brooding hen, later to enjoy the anxious antics of the hen when her brood takes to the water, and on the other hand the futile efforts of the duck to coax her hatchlings into the duck pond.

Let us consider examples illustrating how the development of behaviour in infant animals depends upon maturation, individual and social experience.

In many instances the developing behaviour patterns appear very clumsy. Only gradually does the initial lack of coordination disappear which may be the result of maturation processes, learning processes, or a combination of both. Maturation closely interacts with practice that corresponds rather to beating of nerve tracts than to learning. Actually, practice improves behaviour regardless of reinforcement.

The development of pecking in newly hatched chicks is an example of the interaction between maturation and practice in the development of behaviour. Newly hatched chicks have an inherited tendency to peck at objects which contrast with the background. Cruze (1935) studied how this improvement occurs. He measured pecking accuracy by testing chicks individually in a small arena with a black floor onto which he scattered several grains of millet. Each chick was allowed 25 pecks; each peck was scored as a hit or miss. Cruze used 10 groups of chicks of different age and different time being kept in dark (from 24 to 120 hours) and in light (from zero to 12 hours) to practice pecking. He concluded that as the chicks mature there is a steady improvement in accuracy even if they have not had any opportunity to practice pecking. At any age, 12 hours of practice greatly improves accuracy. So, pecking improves as a consequence of both maturation and practice.

The title of this issue “How an instinct is learned” is borrowed from the Hailman’s (1967) monograph about the development of “instinctive” behaviour in herring gulls. Herring gull chicks peck at a red spot on their parents' bill to induce them to regurgitate food. Hailman (1967) tested Lorenz's claim that this behaviour is innate. It turned out that at birth herring gull chicks peck equally often at a model of their own species and a model of a laughing gull. Moreover, they peck not only at their parents’ beak but at other parts of their head and body as well and thus have a hazy idea of how their real parents look like. After 6 days in the nest they show a preference for the model of their own species. In this case pecking improves as a consequence of maturation, practice and learning because the chicks are rewarded with food by their parents if they peck precisely at a relevant part of their beaks (which is marked by a red spot).

Eibl-Eibesfeldt’s (1961 a, 1970) classic experiments with squirrels (Sciurus vulgaris) demonstrate how learning interacts with maturation and how behaviour units integrate into one functional whole. Squirrels possess the movements of gnawing and prying, but they must learn how to employ these behaviour patterns effectively to open a nut. Experienced squirrels can do this with a minimum of wasted effort. They gnaw a furrow on the broad side of a nut from base to tip, possibly a second one, wedge their lower incisors into the crack and break the nut open into two halves. Inexperienced squirrels, on the other hand, gnaw without purpose, cutting random furrows until the nut breaks at one place or another. The first improvements in the technique can be seen when the furrows run parallel to the grain of the nut and are concentrated on the broad side of the nut. The squirrel follows the path of least resistance, and in this way the activity of the squirrel is guided in a specific direction by the very structure of the nut. The squirrel continues with its attempts to pry, and it keeps repeating those actions that have led to success. In this way most squirrels acquire the most efficient prying technique. Adult squirrels seem to make short work of gnawing nuts in very similar ways but we know now that although their behaviour sequences contain fixed action patterns as elements, these elements are combined by learning into acquired coordinations (Eibl-Eibesfeldt, 1970). Promptov (1940) described many examples of similar development of behaviour in birds and concluded that such a similarity when most of members of species possess the same elements of innate behaviours and have to learn the same results in species-specific stereotype.

Cross fostering experiments help us to estimate to what extend members of species develop their species-specific way of life. A common human practice with cross fostering is switching the eggs in poultry, for instance, between hens and ducks. Slavery in ants is an experiment with switching eggs conducted by Nature. As Hö lldobler and Wilson (1995) give this, the terms slavery and slave-making are employed loosely; the activity is more akin to the capture and domestication. Some way or another, members of one ant species kidnap the eggs of another species and raise them in their home. Well, cocoons, not eggs, and this amendment is important because this allows slave makers to obtain nearly ready workers and thus save on raising their own brood at the stages of eggs and larvae. Being hatched in a foster family, “slaves” feel themselves at home, and they seem not take behaviours of their slave makers over. Ant species that serve as slaves belong to the subgenus Serviformica which is characterised by sole foraging and high agility and enterprise of members.

In our laboratory, we carried out several cross fostering experiments in order to reveal details of behaviour of both slaves and slave makers (Harkiv, 1997; Reznikova, 1996, 2004). We chose Formica sanguinea slave makers because these ants are able to live without slaves and can completely serve themselves, in contrast to highly particularised amazon-ants of the genus Polyergus that can only fight but not work with their sickle-shaped mandibles and are fully dependent on their slaves. However, F. sanguinea as slave makers differ essentially from F. cunicularia and other species of the subgenus Serviformica (their potentially slaves) by characteristics of movements, the contour of a searching trajectory (as the shuttle-movement of a pointer and yaw-movement of a foxhound) and a manner of foraging. For an eye of a man that is not a specialist on ants, these members of the genus Formica are very similar (by their sizes, images, and colour). In our experiments we forced not only F. sanguinea to adopt pupae of F. cunicularia, but vice-versa as well, so several laboratory groups of potential slaves became kings for a few days. Being hatched in foster families, adopted ants behave as members of those families. It turned out that natural slaves (F. cunicularia) take some intimate features of behaviours of their natural slave makers, namely, several details of running movements and contours of searching trajectories. Several quantitative characteristics of behaviours in slaves’ ethograms also became nearer to members of foster families. Experimenters then were able to distinguish between free living F. cunicularia and adopted individuals. The slaves, however, kept all character features of their agile and solely foraging manner which differ them essentially from group foraging and solid slave makers. In contrast, ants of slave making species, now adopted as “slaves” did not imitate any details of behaviours of members of their forced “slave makers” and kept all details of their innate behavioural features including movements, trajectories, and foraging manner. Moreover, they occupied high positions in family hierarchy. These results suggest that only minor shifts in ants’ behaviour can be caused by fostering, and that subdominating species have more tendencies to change their behaviour than dominants.

It is interesting that results similar to ant studies were obtained in cross fostering experiments with canine species. Mainardi (1976) asked his fox terrier Blue to adopt a 10-days old fox Kochis. The experimenter was lucky to observe many interesting details of partnership between Kochis and dogs. This firstly concerned playing behaviour. Both dogs and foxes usually use highly stereotyped behavioural patterns in their games. Like an enslaved ant in our experiments, Kochis behaved as a member of his own species but some details of his behavioural repertoire shifted to the side of his social environment, that is, to the dog’s side. Again as in ants, the difference was quantitative and concerned frequency of display of several behaviours shared by dogs and foxes in nature. Being rare as elements of playing behaviour in a “normal” fox, these elements seemed to be distinctly more frequent in Kochis’ playing behaviour. Like members of our research group who easily distinguished between enslaved ants and free living members of the same species, the dogs easily recognised the “hybrid” behaviour, and they behaved rather differently toward a “normal” fox and the fox raised by the dog as a foster mother.

There are many other examples obtained from cross fostering experiments that illustrate how conservatively members of different species keep details of their species specific behaviour. For instance, Hinde and Tinbergen (1958) described how young tits learn to hold large pieces of food by their legs in order to make pecking it to bits more convenient. Young chaffinches are not able to learn this behaviour even being raised by tit foster parents.

The development of bird song illustrates how genetic and environmental factors sophistically interact during the development of behaviour in different species (Slater, 2003). There is a wide variety of variants of song development in birds, from fully originate (and innate) to fully mocking (and obtained by imitation). In the majority of bird species all elements of their vocal repertoire are innate as well as the structure of the species-specific song (Nottenbohm, 1970). That is why if you buy a yellow domestic chick and ask your home canary to raise it, you will nevertheless enjoy cock-crows in the near future. However, under the same circumstances, a young bullfinch will please you with a depleted variant of a canary’s song.

Let us try to clarify this question and return to the chaffinch first. In contrast to, say, young bullfinches and green finches which can learn to imitate song of other species being infants, chaffinches can not do this. Deprived from hearing songs of their own species and being presented by songs of other species during play back experiments, they sing only their species specific songs and the same with Kaspar-Hauser chaffinches that have heard nothing at early age. The only species to which chaffinches are able to follow is a tree pipit. The song of this species contains one element resembling an element of chaffinch’s song, although these songs differ a lot by their structure. The chaffinches are predisposed to distinguish and reproduce this element in their own song (Thorpe, 1961). It is somewhat different in the zebra finch (Taeniopygia guttata), which learns its song from those who feed it. If a society finch feeds a young zebra finch, they will learn the society finch song, although zebra finches are singing in the adjacent cage. However, if they are fed by both society finches and zebra finches, they will learn the song of the zebra finch. Thus a preference for the song of the species as the model becomes evident (Immelman, 1972).

Marler’s (1970), now classic, experiments revealed one of the most complex types of the interaction between innate and environmental factors in the development of the bird song. He studied white crowned sparrows that appeared to have geographically stable dialects. Within the same species, there are regional variations in bird song. Although these differences could be interpreted as evidence for a genetic basis for bird song, research has shown that young birds learn the dialect from adults in their area. There were three variants of the development of bird song in Marler’s experiments, that is, (1) development under normal conditions; (2) development in isolation from white crown sparrow song, and (3) development after deafening. Under normal condition, from 10 to 50 days of age, the young male's template accepts the adult male white crowned sparrow song as a model; for example, it rejects the swamp swallow song as a model. The improved template now specifies the dialect he has to learn. The young bird does not sing, but the model is remembered for two months or more. The maturing male begins singing its sub song (similar to babbling in human children) at about 150 days of age. During this period vocal output is gradually matched to the dialect specified by the improved template. At about 200 days of age full song begins, it is a copy of the model he learned in his youth.

If infant birds are raised in sound proofed chambers in a laboratory, they emit a crude but recognisable song that contains elements from the normal song. As the bird cannot learn a dialect, it does not sing and retains its basic unimproved template for two months or more. The maturing male begins sub song (about 150 days). Vocal output develops to match specifications of the unimproved template. There is no dialect, but some species qualities persist. Full song begins, based on unimproved template (about 200 days).

Marler explained this by postulating that young birds are born with a crude template of what their species song should sound like. They match this template to the song they hear around them during development, so that the template is sharpened. When the bird is isolated during this memorisation phase, all it can produce is the crude template. The song of a deafened bird is even cruder than that produced by the isolated bird because although the deafened bird may have an exact template, it cannot hear its own output, so it cannot compare the song that it sings with the internal template.

The white crowned sparrow may be unusual in having a sensitive period for memorisation that is over before the bird itself begins to sing. Other birds may show a longer period during which they learn a song (Slater, 1983). Returning to song development of zebra finches on the base of recent studies, it is now more – but not completely- clear what choice young birds make of the tutors from which they copy. While timing is largely restricted to a sensitive phase there is some flexibility in this so that sounds heard earlier or later may sometimes be produced if experience is restricted. Young birds prefer tutors similar in song and appearance to those adult males with which they have earlier experience, but they also agree in their preference for some tutors over others for reasons yet to be determined (Riebel et al., 2005). It now appears that most songbirds come equipped with innately encoded song types which are then activated by auditory experience, stored in memory and then winnowed down to a set of songs as a function of social interaction with community members (Marler, 1997; Slater, 2003).

There are some, yet surprisingly limited, data indicating that types of development of vocal repertoires are distributed oddly in primates. Firsov (Firsov, 1983; Firsov and Plotnikov, 1981) raised infant chimpanzees under artificial feeding in full isolation from their own species, and clearly demonstrated that they develop species specific vocalisation containing all the same elements with normally raised animals. Hammerschmidt et al. (2001) studied six squirrel monkeys (Saimiri sciureus) for their vocal development over the first 20 months of their life, using a multi-parametric acoustic analysis. Four of the animals were normally raised, one animal (“Kaspar Hauser”) was deprived of adult species-specific calls, and one animal was congenitally deaf. Both acoustically deprived animals remained within the variability range of the normally raised animals, suggesting that the ontogenetic changes found were mainly maturational. At the same time, Hauser (2000) argues that vervet monkeys learn at least part of types of their calls. Vervet’s acoustic signals are considered a part of their “symbolic language”, a topic to which we will return in Parts VIII and IX.