The effects of demonstrator social status and prior foraging success on social learning in laying hens

Opportunities for social learning within a group of animals are likely to be influenced by the social dynamics of that group. Some individuals may be more influential demonstrators than others even when there are no differences in their skill level or performance. In this study of domestic hens, Gallus gallus domesticus, differences in demonstrator salience were examined. From 24 separate flocks we selected as demonstrators a dominant cockerel, a dominant hen, a mid-ranking hen or a subordinate hen. Demonstrators were pretrained to perform an operant discrimination task to obtain food. Six observers from each flock individually watched the demonstrator perform the task for four 5-min sessions held on consecutive days. On the fifth day observers were tested individually in the operant chamber. We analysed data from 19 flocks, where there were no quantitative differences in demonstrator performance. Observer hens of relatively high social status performed more correct operant pecks than observer hens of relatively low social status. Demonstrator category also had a significant effect on subsequent observer behaviour. Hens that had observed cockerels performed very few general pecks or operant pecks. Hens that had observed dominant hens performed more operant pecks, but hens that had observed sub-ordinate hens performed more general pecks in the chamber. The results suggested either that there was an interaction between dominance and gender in demonstrator salience or that dominant hens might have been influential because of some factor imperfectly associated with their dominance status. A possible candidate was the foraging ability of the dominant hens. In a second experiment using the same protocol, we manipulated the prior foraging success of dominant hens from four additional flocks but this had no significant effect on their subsequent influence as demonstrators. Copyright 1999 The Association for the Study of Animal Behaviour.     

Testing for imitative and nonimitative social learning in the budgerigar using a two-object/two-action test

Male and female juvenile budgerigars, Melopsittacus undulatus, were allowed to observe a conspecific demonstrator using its beak to remove one of two distinctively coloured objects (i.e. a blue and a black stopper) from a hole in the lid of a box and eating seed from within. Both objects could be removed by either pulling up or pushing down. When subsequently allowed access to both stoppers, and rewarded with food for all removal responses, regardless of the object to which they were made and their direction, observer birds removed both stoppers in the same direction as their demonstrator. This effect was present on the first occasion when observers removed a stopper, and persisted over at least 24 trials. Female observers made more removal responses than males, but conspecific observation had equivalent effects on direction of responding in males and females. All observers tended to approach the same object as their demonstrator when the objects were discriminable using both spatial and colour cues, but not when they differed in colour alone. Contrary to previous findings, these results suggest that robust behavioural matching effects can be obtained in budgerigars, and that these birds are capable of motor imitation or emulation. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Interaction between individual experience and social learning in dogs

We investigated the interaction between individual experience and social learning in domestic dogs,Canis familiaris . We conducted two experiments using detour tests, where an object or food was placed behind a transparent, V-shaped wire-mesh fence, such that the dogs could get the reward by going around the fence. In some groups, two open doors were offered as an alternative, easier way to reach the reward. In experiment 1 we opened the doors only in trial 1, then closed them for trials 2 and 3. In experiment 2 other dogs were first taught to detour the fence with closed doors after they had observed a detouring human demonstrator, then we opened the doors for three subsequent trials. In experiment 1 all dogs reached the reward by going through the doors in trial 1, but their detouring performance was poor after the doors had been closed, if they had to solve the task on their own. However, dogs in the experimental group that were allowed to watch a detouring human demonstrator after the doors had been closed showed improved detouring ability compared with those that did not receive a demonstration of detouring. In experiment 2 the dogs tended to keep on detouring along the fence even if the doors had been opened, giving up a chance to get behind the fence by a shorter route. These results show that dogs can use information gained by observing a human demonstrator to overcome their own mistakenly preferred solution in a problem situation. In a reversed situation social learning can also contribute to a preference for a less adaptive behaviour. However, only repeated individual and social experience leads to a durable manifestation of maladaptive behaviour. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

The social transmission of spatial information in homing pigeons

We adapted a technique to explore the social transmission of spatial information in homing pigeons Columba livia. Five demonstrator pigeons were first trained to find a food goal within an indoor arena. This arena consisted of nine lidded cups laid out within a 12x12 grid on the floor. The task was to find the goal cup and flip the lid to obtain the food hidden within. Once the demonstrators had reached criterion the experiment proper began. During stage 1 of the experiment, 10 target birds, which had not previously been trained to find the goal, were introduced to the spatial task either in isolation or paired with a demonstrator. We measured how long they took to complete the task, the number of squares crossed on the grid, and the number of incorrect lids flipped. In stage 2, the target birds were introduced to the arena a second time, by themselves, and we compared the performance of the birds in the two treatments. The pigeons that had been introduced to the task with a demonstrator in stage 1 walked further and made more incorrect choices when searching for the food goal in stage 2 than the pigeons that were introduced to the task alone. This indicates that pigeons learn a spatial, food-finding task more effectively when performing the task alone than when accompanied by a knowledgeable conspecific. We discuss possible reasons for this in the light of previous experiments. Copyright 1999 The Association for the Study of Animal Behaviour.     

Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea

We quantified the acoustic characteristics of the habitats of two wild populations of pygmy marmosets, in Amazonian Ecuador to evaluate their effects on vocal signal structure. We obtained measures of ambient noise, sound attenuation and reverberation through recordings and broadcasts of exemplars of two short-range vocalizations and one long-range vocalization of the marmosets. Ambient noise levels differed among habitats. The calls of pygmy marmosets had frequencies that coincided with relatively quiet regions of the ambient noise spectra of the habitats. The three vocalization types were degraded similarly in all habitats. The two short-range signals, with a pulsatile structure, were more affected by reverberation than was the long-range, less pulsatile vocalization. This degradation could be used by the marmosets to estimate the distance of the caller animals. We obtained data on context of vocalizations from six groups of pygmy marmosets, three from each population, in both the dry and rainy seasons. The use of Trills, J calls and Long calls was related to the distance between the calling animal and the potential receivers suggesting that marmosets are using the calls in a way appropriate to the effects of habitat acoustics. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Rats smell: odour-mediated local enhancement, in a vertical movement two-action test

In two experiments, hungry rats, Rattus norvegicus, were present in one side of an operant chamber while a conspecific demonstrator in the adjacent compartment moved a single lever either up or down for a food reward. During a subsequent test session, in which these rats were allowed access to the lever for the first time, all responses were rewarded regardless of their direction. In experiment 1, rats that were prevented from observing the direction of lever movement by means of a screen showed a reliable demonstrator-consistent response bias, while rats that had observed the direction of lever movement and in addition had access to any odour cues deposited on the lever did not. In experiment 2, each rat observed another rat (the ‘viewed’ demonstrator) moving a lever either up or down. They were then transferred into the test compartment of a different operant chamber in which another rat (the ‘box’ demonstrator) had moved the lever in the same direction as the viewed demonstrator or in the opposite direction. These observer rats showed a reliable preference for their box demonstrator's direction, but responded in the opposite direction to their viewed demonstrator. Taken together, the results of these experiments suggest that directional responding by rats in a vertical movement two-action test is influenced by demonstrator-deposited odour cues in addition to visual experience of a demonstrator's behaviour. Furthermore, while odour-mediated local enhancement gave rise to demonstrator-consistent responding, visual observation of a conspecific appeared to have the reverse effect. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Social learning directs feeding preferences in the zebra finch, Taeniopygia guttata

We tested sexually mature zebra finches to see whether social learning influenced their feeding preferences, in particular whether they followed the preference of a male or a female demonstrator, of a red-ringed or a green-ringed male, and of a familiar or an unfamiliar male. Each observer was exposed to two demonstrators feeding at different-coloured hoppers, and then tested with a choice of hoppers to see which of the two colours they preferred. Males showed no preference between male and female demonstrators when choosing from which colour of food hopper to feed, but females preferred to feed from the hopper colour the male demonstrator had used. Both males and females exposed to male demonstrators wearing red or green leg rings fed preferentially from the same colour hopper as the red-ringed demonstrators had used. Finally, male birds exposed to familiar and unfamiliar demonstrators, preferred the food hopper from which the familiar demonstrator had fed. We interpret the results as indicating differences between the demonstrators in the amount of attention they attracted from observers.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Tolerated mouth-to-mouth food transfers in common marmosets

In this paper we describe tolerated mouth-to-mouth food transfers in captive adult common marmosets, where an animal approached a conspecific that has recently received a piece of food, opened the other’s mouth forcefully, and picked food pieces out of it. Tolerated mouth-to-mouth food transfers occurred between animals of both sexes. They were observed when the possessor was subordinate as well as when it was dominant, and in four dyads they were observed in both directions. We argue that this behaviour might have a social function and that the cooperative breeding system of marmosets might have facilitated its evolution.     

Social exploitation of intermittently available foods and the social reinstatement of food preference

To determine whether Norway rats, Rattus norvegicus, could use socially acquired information to track recurrences of an intermittently available food (experiment 1), we allowed observer rats to interact every 2-3 days with demonstrator rats fed one of two diets, then determined the amount of each diet eaten by observers. We found that observer rats showed repeated significant increases in their preferences for foods their respective demonstrators had eaten. Because social interactions repeatedly enhanced preference for a food, we reasoned that after the socially induced food preference of an animal (A1) had waned, that preference might be reinstated in A1 by interaction with a conspecific (A2) in whom A1 had previously induced a preference for the food. In experiment 2, we demonstrated such social reinstatement of a food preference. Copyright 2000 The Association for the Study of Animal Behaviour.     

Hormonal correlates of being an innovative greylag goose, Anser anser

A number of studies have focused on the spread of foraging innovations within animal populations, but only rarely have individual dispositions of becoming innovative been considered. With two groups of individually marked, hand-reared greylag goslings we investigated hormonal and behavioural correlates related to the individual's ability to perform operant tasks. During individual tests 6 weeks after hatching, goslings were given small food containers covered by lids. In the following winter the sibling groups were tested in a social set-up at a food dispenser, which the geese could activate by pulling a flap. We analysed individual faecal samples collected at 2, 6 and 12 weeks of age, and also after the individual tests, for excreted corticosterone and testosterone metabolites by enzyme immunoassay. During the individual test, 18 of 23 individuals learned to remove the lids. These 18 birds excreted higher faecal corticosterone concentrations than their respective controls 2 weeks after hatching. At the food dispensers, only four males became food producers; all the others scrounged. These four were in the group of 18 that were successful in the individual test and again tended, although not significantly, to have higher faecal corticosterone 2 weeks after hatching than the scroungers. In one of the groups, excreted corticosterone increased and excreted testosterone decreased after the individual test. Goslings successfully removing lids at 6 weeks raised their faecal corticosterone to a significantly greater extent than the unsuccessful individuals. Our results suggest that becoming an innovator may be contingent upon individual coping styles. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Capuchins do cooperate: the advantage of an intuitive task

We used a cooperative pulling task to examine proximate aspects of cooperation in captive brown capuchin monkeys, Cebus apella. Specifically, our goal was to determine whether capuchins can learn the contingency between their partner's participation in a task and its successful completion. We examined whether the monkeys visually monitored their partners and adjusted pulling behaviour according to their partner's presence. Results on five same-sex pairs of adults indicate that (1) elimination of visual contact between partners significantly decreased success, (2) subjects glanced at their partners significantly more in cooperative tests than in control tests in which no partner-assistance was needed, and (3) they pulled at significantly higher rates when their partner was present rather than absent. Therefore, in contrast to a previous report by Chalmeau et al. (1997, Animal Behaviour, 54, 1215-1225), cooperating capuchins do seem able to take the role of their partner into account. However, the type of task used may be an important factor affecting the level of coordination achieved. Copyright 2000 The Association for the Study of Animal Behaviour.     

Task‐Dependent Differences in Learning by Subordinate and Dominant Wild Arabian Babblers

Learning and innovation abilities have been studied extensively in flocking birds, but their importance and relevance in cooperatively breeding birds have been relatively unexplored. We studied the acquisition of novel foraging skills in 14 groups of wild, cooperatively breeding Arabian babblers (Turdoides squamiceps). While in a previous study we found that subordinate individuals were usually the first to learn to remove black rubber lids from a foraging grid, here we show that dominant individuals were the first to succeed in shifting from these black rubber lids to newly introduced white rubber lids. We also found that in all groups where one forager learned to shift to the white lids, the rest of the foragers also learned to do so, suggesting that this behaviour may be transmitted among group members. Although dominant individuals were almost always the first to remove white lids, once starting to remove white lids, dominants and subordinates learned equally well to prefer white over black lids based on differential reinforcement (food was provided only under white lids). Together with our previous study, our results suggest that differences in learning between dominants and subordinates may be task‐specific, which may represent different cognitive strategies: subordinates may explore a more diverse range of foraging opportunities, while dominants may be better at generalizing from familiar tasks to similar ones.     

Social factors determine cooperation in marmosets

We investigated which factors determine cooperative behaviour of common marmosets, Callithrix jacchus, in an instrumental task. During the approach phase each of eight individuals of a family group learned in isolation to pull a handle moving a bowl with attractive food towards its reach. In the following two experimental phases we used 16 dyads. In a dyadic training phase we assessed whether the partners were willing to manipulate the apparatus and to share food. In the subsequent cooperation test we examined whether they were willing to cooperate at a slightly modified apparatus whose solution required one individual (the producer) to pull the handle and the other (the scrounger) to grasp the bowl. Although all individuals were willing to cooperate with at least one partner, only half of the dyads solved the task in the cooperation phase. Examination of the factors that correlated with success in this phase revealed that primarily those dyads cooperated in which the dominant subject took the role of the scrounger and the subordinate took the role of the producer. However, in these successful dyads the dominant animal did not force the subordinate partner to pull the handle. Rather, the partners of cooperative dyads shared the reward and pulled equally often in both the dyadic training and the cooperation test. Thus, cooperation of marmosets in an instrumental task seems to depend on a specific distribution of roles and the tolerance of higher-ranking individuals.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Individual differences in the use of social information in foraging by captive great tits

We investigated individual differences in copying behaviour of captive great tits, Parus major, by analysing their response to a tutor indicating a new feeding site. We used two groups, each of seven male birds, labelled 'fast' and 'slow' explorers based on previous studies in which consistent individual differences in the speed of exploring were found. The birds were trained to search for food hidden in a number of differently coloured and shaped feeders, and later to search in only one type of feeder. During the tests, food was absent and the birds were observed in two different situations: alone or in the presence of a tutor, a bird that had been trained to feed in a different kind of feeder. When alone, slow birds readily extended their search to other feeders while fast birds did not change their routine of visiting the previously rewarded ones. In the presence of the tutor, the opposite occurred: slow birds did not change their behaviour while fast birds significantly increased their visits to the feeders indicated by the tutor. Fast and slow individuals thus differ in their foraging and copying behaviour, consistent with the producer-scrounger model. Copyright 2000 The Association for the Study of Animal Behaviour.     

Ultrasonic vocalization by female mice in the presence of a conspecific carrying food cues

In female mice, Mus domesticus, reunion with a same-sex conspecific is associated with intense ultrasonic vocalization. We examined whether the palatability of a familiar food eaten by a demonstrator mouse and the motivational state of the conspecific observer could modulate the number of ultrasonic calls uttered during female-female interaction in NMRI mice. A pilot study indicated that these calls were uttered almost exclusively by the observer member of the pair. Observers were either food deprived or not deprived and demonstrators were offered either no food, a palatable diet or an unpalatable diet. We monitored both the number of ultrasounds (range 65-75 kHz) uttered and a series of behavioural parameters during the first 3 min of social interaction after 24 h of separation. Observers investigated the nose area of demonstrators fed on the unpalatable diet more than the same area of demonstrators not given food. No differences were found in demonstrators' behaviour. Ultrasonic calls were given immediately after female-female reunion and were affected by both the motivational state of the observer and the salience of the information carried by the conspecific. These results suggest that the motivational state of the observer affects ultrasonic calling towards a demonstrator conspecific. Nondeprived animals produced more calls towards demonstrators fed on palatable food, whereas food-deprived subjects vocalized more to fed conspecifics, independently of the palatability of the food eaten by the demonstrator. We suggest that ultrasonic vocalization in female mice can facilitate proximity with a conspecific and the number of these calls is modulated by the salience of the information carried by the companion. Copyright 2000 The Association for the Study of Animal Behaviour.     

Socially biased learning among adult cottontop tamarins (Saguinus oedipus)

We presented adult cottontop tamarins (Saguinus oedipus) with a novel foraging task that had been used previously to examine socially biased learning of juvenile observers [Humle & Snowdon, Animal Behaviour 75:267–277, 2008]. The task could be solved in one of two ways, and thus allowed for an analysis of behavioral matching between an observer and a skilled demonstrator (trained to use one of the two methods exclusively). Because the demonstrator was an adult in both this study and the juvenile study, the influence of the observer's age could be isolated and examined, as well as the behavior of demonstrators toward observers of different ages. Our main goals were to (1) compare adults and juveniles acquiring the same task to identify how the age of the observer affects socially biased learning and (2) examine the relationship between socially biased learning and behavioral matching in adults. Although adults spent less time observing the trained demonstrators than did juveniles, the adults were more proficient at solving the task. Furthermore, even though observers did not overtly match the behavior of the demonstrator, observation remained an important factor in the success of these individuals. The findings suggested that adult observers could extract information needed to solve a novel foraging task without explicitly matching the behavior of the demonstrator. Adult observers begged much less than juveniles and demonstrators did not respond to begging from adult. Skill acquisition and the process of socially biased learning are, therefore, age‐dependent and are influenced by the behavioral interactions between observer and demonstrator. To what extent this holds true for other primates or animal species still needs to be more fully investigated and considered when designing experiments and interpreting results. Am. J. Primatol. 72:287–295, 2010. © 2009 Wiley‐Liss, Inc.     

Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii)

We describe temporal patterns of change in paternal behaviour and urinary concentrations of the steroid hormones testosterone (T) and oestradiol (E(2)) in male black tufted-ear marmosets, Callithrix kuhlii, relative to the birth of their young, and test predictions of the hypotheses that (1) high levels of T are incompatible with paternal care and (2) levels of T and E(2)vary with a father's prior experience in his family group. After young were born, levels of urinary T and E(2)remained near prepartum concentrations and rates at which fathers carried infants were below peak levels until the approximate time that postpartum mating ordinarily occurs, suggesting a possible trade-off between readiness to mate and paternal behaviour in C. kuhlii. Infant-carrying behaviour of fathers occurred at its highest rate 3-4 weeks after parturition and coincided with significant declines in urinary levels of T and E(2), providing preliminary support for the hypothesis that these hormones are antagonistic to paternal behaviour. Urinary T and E(2)declined among fathers regardless of whether their young survived to weaning or died at birth, indicating that variation in these hormones after parturition occurs even in the absence of continued stimuli from infants. When adjusted for declines ordinarily associated with aging, urinary T tended to be lower among fathers with a great deal of prior experience caring for young compared with fathers having little or no experience, suggesting that either experience affects T levels of fathers, or that T levels influence fathers' chances of successfully rearing infants. Overall, our results suggest that in male C. kuhlii, T, and possibly E(2), play an important role in balancing the expression of paternal care with that of other reproductive behaviours. Copyright 2000 The Association for the Study of Animal Behaviour.     

Social anxiety, relationships and self-directed behaviour among wild female olive baboons

Self-directed behaviour (SDB) can be used as a behavioural indicator of stress and anxiety in nonhuman primates (Maestripieri et al. 1992, Animal Behaviour, 44, 967-979). We investigated the effect of nearest neighbours' relative dominance status on the SDB of sexually mature female olive baboons, Papio anubis. When the animal nearest to (within 5 m of) a female was a dominant individual, SDB rates (a combined measure of self-scratching, self-grooming, self-touching, body shaking and yawning) increased by ca. 40% over those observed when the nearest neighbour was a subordinate. The results indicate that (1) SDB can be used as a measure of uncertainty during the social interactions of cercopithecine primates and (2) as there was considerable variation in SDB response according to the nature of the dominant individual, SDB can be used to assess relationship security (i.e. the perceived predictability of a relationship for one partner). Finally, in combination with measures of affiliation rate, SDB may provide insight into relationship value. Copyright 1999 The Association for the Study of Animal Behaviour.     

Does darkening signal submission in territorial contests between juvenile Atlantic salmon, Salmo salar ?

Communication by means of visual signals occurs during the competitive, aggressive and sexual interactions of many animals. Some animals such as fish are able to change their body coloration rapidly, and there is evidence that this is used as a means of signalling. However, the precise meaning of such signals is rarely understood. We examined whether (1) darkness in juvenile Atlantic salmon is associated with submission, and (2) changing to a darker colour could act as a signal to the opponent and hence induce a change in its behaviour. We found that both the sclera of the eye and the overall body coloration tended to darken in fish that were losing territorial encounters, while victors retained their original coloration. The darkening was rapid and usually occurred during a period of sustained attacks by the opponent; however, the aggression level decreased as soon as the losing fish had become darker. We suggest that the darkening of the losing fish was associated with submission and may result in a change in the behaviour of its opponent, so minimizing the potential risk of injury during unnecessarily prolonged fights. Copyright 1999 The Association for the Study of Animal Behaviour.     

Suckling behaviour does not measure milk intake in horses, Equus caballus

Studies of parental investment in mammals have frequently used suckling behaviour to estimate energy transfer from mother to offspring, and consequently to measure maternal input. Such studies assume that the more an offspring sucks, the more milk it will receive. This assumption has been questioned, and a review of the literature found little support for it. To test if suckling behaviour provided an accurate index of milk or energy intake we used a radioactive isotope technique to label the milk of thoroughbred mares and to measure milk transfer to foals. We found no significant linear relationship between usual measures of suckling behaviour and milk or energy intake. No behaviours associated with suckling nor with characteristics of mares and foals improved the relationship; only the number of butts associated with each suck episode even approached significance. If we had used suckling behaviour to test theories on differential maternal investment our conclusions would have been in error. For example, female foals tended to suck for longer than males did but there was no difference in the amount of milk transferred. Consequently, we show that measures of suckling behaviour do not adequately predict milk intake in the domestic horse and we suggest that conclusions about differential maternal investment in mammals based on suckling behaviour are likely to be in error. Copyright 1999 The Association for the Study of Animal Behaviour.