The ways behavioural traditions spread

The phrase “population-specific behavioural traditions” is used to describe behaviours that have the following properties (Nagell, Olguin and Tomasello, 1993):

1. They are acquired through experience, rather than being innate.

2. They are found throughout a well-defined population.

3. They persist from one generation to the next.

4. They are absent in other populations of the same species.

The spread of novel feeding methods through a population, as a particular case of fixing population-specific behavioural traditions, has been documented for a number of terrestrial and avian species (Roper 1986). Two of the most famous cases are milk-bottle top opening by birds in Britain (Fisher and Hinde 1949), and washing sweet potatoes (yams) by Japanese macaques (Macaca fuscata) (Kawai 1965). In both cases, the spread was initially thought to be due to imitation, but more recent work has cast doubt on this (Sherry and Galef 1984; Whiten 1989). Let us consider briefly these two examples together with some analogous studies which appreciate the role of simpler forms of learning than imitation.

Blue tits and great tits in Britain are notorious for their ability to break through the foil tops of milk bottles in order to drink the cream at the top. This skill is believed to have originated in a small group (Fisher and Hinde 1949), and its spread to the rest of the population has been attributed to imitation. However, the results from a series of experiments by Sherry and Galef (1984, 1990) using black-capped chickadees, suggest that the spread of this habit was promoted by more simple than imitation means of social learning. If a bird should come across a bottle that has already been opened, it will drink the milk. Once it has drunk from the bottle, apparently the bird will be very much more likely to break through the foil tops in the future. Pavlovian conditioning provides one explanation for this outcome (see Pearce, 2000 for details). Sherry and Galef (1990) report that their subjects were unlikely to open foil tops when they were tested in isolation. In an attempt to answer the question of how the birds came to open foil tops in the first place, experimenters examined the behaviour of a naive bird that had access to a foil covered container of cream when it could see another naive bird in an adjacent cage. The mere presence of this second bird was sufficient to encourage the first bird to peck at the foil cap and eventually open it. Sherry and Galef (1990) consider social facilitation as the main mechanism responsible for the origins and perhaps spread of milk-bottle opening among certain birds. The reasons for social facilitation of pecking in this concrete situation are not fully understood, but the presence of the second bird may serve to reduce fear, or to encourage foraging responses, in the experimental subject.

An example of fixing of behavioural tradition in primates is provided by a group of Japanese macaque monkeys who wash sweet potato (yams) before eating them (Kawai 1965; Itani and Nishimura, 1973). In 1952, on the island of Koshima, scientists were providing a group of 22 Japanese macaques with sweet potatoes dropped in the sand. An 18-month-old female named Imo found she could solve the problem by washing the potatoes in a nearby stream. Imo’s name has become legendary as one of the first personalized innovative animal described in scientific literature. The researchers also scattered grains along the beach. The monkeys had to pick the grains from the sand, one grain at a time. Then Imo threw a handful of sandy grain in the water. The sand sank and the grain floated, making it easy to scoop up. Again, other members of Imo's troop eventually learned how to throw their grain in the water.

By March, 1958, 15 of the 19 young monkeys (aged two to seven years) and 2 of the 11 adults were washing sweet potatoes. Up to this time, the propagation of the innovative behaviour was on the individual basis, along family lines and playmate relationships. Most of the young monkeys began to wash the potatoes when they were one to two and a half years old. Males older than 4 years, who had little contact with the young monkeys, did not acquire the behaviour. By 1959, the sweet potato washing was no longer a new behaviour to the group. Monkeys that had acquired the behaviour as juveniles were growing up and having their own babies. This new generation of babies learned sweet potato washing behaviour through the normal cultural pattern of the young imitating their mothers. By January, 1962, almost all the monkeys in the Koshima troop, excepting those adults born before 1950, were observed to be washing their sweet potatoes. If an individual monkey had not started to wash sweet potatoes by the time he was an adult, he was unlikely to learn it later, regardless of how widespread it became among the younger members of the troop.

Nagell et al. (1993) have suggested that the spread of this habit is due in part to stimulus enhancement. The attention of a naive monkey can be drowning to a potato when it sees another monkey to pick one up. The naive monkey may then pick up its own potato and for social reasons follow the experienced monkey into the river. At this point, the naive monkey may learn by accident the benefits that accrue from placing the potato in the water.

Indeed, stable embedding of new feeding technique in wild populations does not necessarily mean that there is imitation underlying cultural transmission. Behavioural habits can be based on mechanisms of social learning which are simpler than imitation.

For instance, stimulus enhancement explains the acquisition of pine-cone stripping behaviour of black rats. Terkel (1996) found that although naive rats never learned to strip cones unaided, the animals were capable of learning the trick if partially striped cones were provided, and especially so if they were exposed to cones with progressively fewer rows of scales removed. Young rats pay close attention to whatever their mother is eating, and often manage to steal partially-eaten cones from her.

Combination of social facilitation, stimulus enhancement and individual learning are likely to underlie forming of “subcultures”, or behaviourally specialised “cultural clans” in animals. There are a lot of examples in literature. For instance, populations of crows in Kamchatka specialise in different techniques of getting food from humans. Some flocks regularly steal alms at cemeteries whereas others track skiers in winter and gatherers of mushrooms in summer stealing food from them when they make stops. Dolphins in Shark Bay show a similar specific foraging specialisation - feeding by humans at Monkey Mia beach - in which not all of the population takes part. This variation appears to be maintained by vertical cultural transmission, since most of the dolphins taking advantage of the feeding are offspring of females which were themselves fed (Smolker et al. 1997); hence the specialisation is likely learned while swimming with the mother.

Clans of Norway rats specialise on catching fishes or frogs, stealing fishes from fishing nets, harvesting molluscs, and stealing eggs and chicks from birds’ nests. Clans dwelling on different sides of a lake display different techniques of catching frogs. Galef (1980) has conducted laboratory experiments simulating his own observation in nature on how Norway rats dive for molluscs. It turned out that young pups are able to adopt this technique from their mothers.

Being lucky to catch first manifestations of novel behaviour within a wild population and then monitoring it during long periods, several researchers have reported on very interesting cases of inculcation of new habits, mainly, feeding technique. For instance, the regular cracking of palm tree nuts with the aid of two stones (“hammer” and “anvil”) by Japanese macaques was fixed from the very first case and then monitored for 20 years. During this time, about 80% of population had adopted this method (Huffman and Nishie, 2001). Spread of a novel feeding technique was described in humpback whales (see: Rendell and Whitehead, 2001 for a detailed review). In the southern Gulf of Maine, a novel complex feeding technique, '”lobtail feeding”, was first observed in 1981, and by 1989 had been adopted by nearly 50% of the population (Weinrich et al. 1992).

Not only new feeding techniques can be transmitted socially. Social transmission can also apply to group-specific vocalizations, courtship displays, grooming postures and so on.

A good example of the transmission of a character posture in social groups of apes has come from primatological studies. This concerns a so-called “grooming handclasp”, a unique grooming posture in which two individuals sit facing one another, simultaneously raise one arm overhead, and support the other by holding hands or wrists to create an " A-frame" posture. The grooming handclasp was first observed by McGrew and Tutin (1978) in a chimpanzee community inhabiting the Mahale Mountains in Tanzania, whereas the same pattern has never been reported for the chimpanzees of Gombe Stream, who live only 170 Km to the north. The authors believe it " unlikely that the two populations had time to differentiate markedly through genetic drift" (McGrew and Tutin, 1978). DeWaal and Seres (1997) suggested that learning is the most likely mechanism underlying differences in behaviour between populations of the same species that live within a distance at which genetic exchange is likely or possible. These authors found the grooming handclasp developed spontaneously in a captive group of approximately 20 chimpanzees in the Field Station of the Yerkes Regional Primate Research Center, Georgia. Researchers followed the development of this new social custom during a five year period. In the beginning, handclasps were always initiated by the same adult female named Georgia. She initiated the posture mainly with her adult female kin. In the second year Georgia initiated the pattern with several partners, mostly immediate adult kin. In later years, these relatives began initiating the pattern at rates similar to or higher than those of Georgia herself. Over the years the posture increased in frequency and duration and spread to the majority of adults and also to a few adolescents and older juveniles. When the apparent originator Georgia was removed from the colony, the pattern nevertheless persisted.

Another well documented local traditions is the rhythmic hand- and foot-clapping during grooming in captive apes’ community has been described in bonobos (Pan paniscus) at the San Diego Zoo. Over the years, transmission of this pattern took place: these group-specific gestures were adopted by several individuals introduced as juveniles into the San Diego colony (de Waal, 1989).

It is worth to note that, in contrast to the cases of spread of novel feeding technique described before, transmission of the new grooming posture is based on a highly stereotyped behavioural sequence which apparently displays in the “at once and entirely” manner in chimpanzee and bonobo originators. The role of social learning can’t be doubted in a process of infection of community members but the role of inherited predisposition probably is not less. We will consider this problem in the next section.