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.     

Avoidance of potentially harmful food cannot be socially transmitted between rats

The social transmission of food preferences(STFP) is a behavioural task of olfactory memory, in which an observer rat learns safe food odours from a demonstrator rat, and shows preference for this odour in a subsequent choice test. However, previous studies have failed to detect the transmission of information about food of potential danger and food aversion using STFP test. In this study, we tested how demonstrators' health affects the exchange of odour information and whether observers can learn danger information from an unhealthy demonstrator. As expected, the observer rat formed an odour preference after interacting with a demonstrator rat that had just eaten food containing a new odour, however, odour preference rather than aversion was also formed after interacting with a demonstrator rat injected with LiCl(used to induce gastric malaise). Furthermore, anaesthetized demonstrator rats and half-anaesthetized demonstrator rats, which showed obvious motor deficits suggesting an unhealthy state, also socially transmitted food preferences to observers. These results suggest that the social transmission of food preferences task is independent of a demonstrators' health, and that information about dangerous foods cannot be transmitted using this behavioural task.     

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.     

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.     

Dogs acquire food preferences from interacting with recently fed conspecifics

Social transmission of food preferences has been documented in many species including humans, rodents, and birds. In the current experiment, 12 pairs of domestic dogs (Canis familiaris) were utilized. Within each pair, one dog (the demonstrator) was fed dry dog food flavored with either basil or thyme. The second dog (the observer) interacted with one demonstrator for 10 min before being given an equal amount of both flavored foods. Observers exhibited a significant preference for the flavored diet consumed by their demonstrators, indicating that dogs, like rats, prefer foods smelled on a conspecific's breath.     

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.     

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.     

Ultrasonic vocalizations and social learning of food preferences by female Norway rats

We examined whether ultrasonic vocalizations facilitate social learning of food preferences in female Norway rats, Rattus norvegicus. Females produced ultrasonic vocalizations at higher rates when they were reunited with a familiar conspecific if one member of the reunited pair had eaten an unfamiliar food while the pair members were separated. However, the influence of demonstrator rats on food choices of their observers was as great in pairs of rats that had been devocalized surgically as it was in sham-operated controls. The latter result is not consistent with the hypothesis that ultrasonic vocalizations facilitate social learning of food preferences in Norway rats.     

Acquisition of flavour preferences in pigs through interactions with conspecifics that had previously consumed flavoured protein solutions

It is known that pigs can acquire flavour preferences by brief social interactions with conspecifics that previously consumed a flavoured solid feed. However, there is no information about whether a flavoured solution could support flavour preferences through social transmission. Ninety-six pigs (49 days old) were housed in 12 pens (8 pigs/pen). Four animals per pen were randomly selected to act as observers and four as demonstrators. Demonstrator animals were temporarily moved to an empty pen where a protein solution was offered (porcine digestive peptides (PDPs), 4% weight/volume) with the addition of 0.075% aniseed (six pens) or garlic (six pens) powdered artificial flavours for 30 min. Afterwards, demonstrators were returned to interact with observer animals for 30 min. A choice test (30 min) between aniseed and garlic PDP was performed for each observer group after the interaction. Observers showed a higher intake of solutions previously consumed by their demonstrator conspecifics (648 v. 468 ml; SEM 61.36, P < 0.05). As with flavoured solid feeds, protein solutions containing artificial flavours can create preferences in pigs for those flavours through social transmission from conspecifics.     

Innovative Individuals Are Not Always the Best Demonstrators: Feeding Innovation and Social Transmission in Serinus canaria

Background

Feeding innovation occurs when individuals choose a novel, unknown type of food and/or acquire new feeding skills. Here we studied feeding innovation and social transmission of the new feeding habit in canaries. Adult canaries eat a wide variety of seeds but avoid larger ones such as those of sunflowers. We determined whether adults of both sexes are equally prone to innovate when confronted with sunflower seeds and whether free-interactions facilitate transmission of the new feeding habit in a sex-dependent manner.

Methodology/Principal Findings

First we determined which sex was more innovative, i.e., was more successful at husking and eating the novel seeds. Males were clearly more innovative than females. Due to this, experienced males served as model for either male or female observers in three different conditions (free interaction with a demonstrator, visual interaction with a demonstrator placed behind a transparent wall and access to seeds in the presence of a non-demonstrating bird). During free interactions, the new feeding habit was only transmitted to females. In contrast, transmission of seed handling to male observers only occurred if demonstrator and observer were separated by the transparent wall. Indeed, aggressive behaviors between males prevented social transmission during free interactions. Finally, we studied the influence of the less innovative females in feeding-habit transmission. First, we obtained female demonstrators by making them freely interact with male demonstrators. Once they acquired innovative responses to sunflower seeds we studied feeding-habit transmission towards male and female observers. Observers of both sexes learned during free interactions with female demonstrators. No aggressive behavior occurred. Males were also able to learn after visual interactions with the female demonstrator.

Conclusions/Significance

Our results show that the most innovative individuals (males) are not always the best demonstrators, and that social relationship and sex are crucial factors for the spread of a new feeding habit among canaries. These factors determine the kind of interaction between individuals and the time spent together, thus affecting the transmission of novel habits within the population.     

Social Facilitation of Eating Familiar Food in Tufted Capuchins (<Emphasis Type="Italic">Cebus apella</Emphasis>): Does it Involve Behavioral Coordination?

Social facilitation of eating familiar foods might serve to synchronize eating activities within groups. We aimed to assess whether capuchins (Cebus apella) are prompted to eat when observing other conspecifics eating a familiar food. Subjects were 8 male captive-born tufted capuchins. One pair of capuchins acted as demonstrators for the other 6 observer subjects. In the Experimental condition, the demonstrator pair was given fresh chow in addition to having access to the leftover food and ate continuously. In the Control condition, the demonstrator pair had access to food leftover from the morning feed and ate very little. The initiation of feeding by the demonstrator pair prompted the initiation of feeding behavior in the observers, and the latter ate significantly more of their leftovers in the Experimental than in the Control condition. The tempo ofthe social facilitation of eating familiar foods in capuchins supportisomorphic coordination, a process that occurs when one individuals activity focuses the attention of another individual to the same activity, thereby increasing behavioral similarity in a group.     

Imitation of lever-pressing ‘strategies’ during the operant conditioning of albino rats

This experiment was carried out on ninety-one male Wistar rats in order to study the ability to learn by observation in an operant conditioning situation. All rats were trained on a ‘multiple’ schedule over twelve daily sessions. Four observer groups were constituted: One control group and three groups paired with demonstrator rats which used well-known and distinct lever-pressing ‘strategies’. During each session, 15 min of demonstration or simple presence of a naïve companion were followed by 30 min of training. It was shown that the rats which were paired with a demonstrator have a higher response rate than controls, but only during the first session. During the eleven following sessions, no significant differences could be observed between the four observer groups. Nevertheless, if we consider the percentage of utilization of the various ‘strategies’ by each rat, we can notice significant correlations between demonstrators and observers, during the last three sessions.     

Social Learning in the Caracara Chimango,Milvago chimango (Aves: Falconiformes): an Age Comparison

Milvago chimango is a gregarious raptor showing great ecological plasticity. Their ability to explore new resources has allowed them to survive in areas with increasing human modification. In this study, we evaluated the social learning ability in wild‐caught individuals of M. chimango. In particular, we tested whether an ‘observer’ individual could improve the acquisition of a novel behaviour by watching a ‘demonstrator,’ and we examined the effects of age of both observers and demonstrators on social learning. We measured the ability of 18 observers to open an opaque Plexiglas box containing food, and we compared their performance to that of 10 control birds who did not watch a demonstrator solve the task. Prior to watching a demonstrator, only two of the observers and two of the control birds were able to open the box. After watching a demonstrator, 67% of observers were able to open the box, outperforming control birds in speed and success. Juvenile observers were more successful and faster than adults at contacting and opening the box. The age of the demonstrator did not influence the observers’ likelihood of success. These results showed that M. chimango are able to learn a box‐opening task with a hidden food reward by observing the behaviour of a conspecific and that this behaviour persisted over several days. Social learning ability in M. chimango might allow certain behavioural patterns, such as those related to novel resource acquisition in modified environments, to be socially transmitted among individuals in a population.     

Social Transfer of Predation Risk Information Reduces Food Locating Ability in European Minnows (Phoxinus phoxinus)

Little is known about how food location ability of animals is affected by social information of predation risk. This question was therefore addressed in an experimental study where naïve ‘observer’ European minnows (Phoxinus phoxinus) were allowed to search for food in a maze in the presence or absence of a predator (Salmo trutta). Observer minnows were accompanied by conspecific demonstrators which had previously been trained in the same maze either in the presence or absence of the predator. Observer minnows were most likely to locate food when the predator was absent both during their trial and during the pre‐training of demonstrators. When demonstrators had been trained with predators, observer success in locating the food was halved, although they were never exposed to predation risk themselves. When observers were exposed to predation risk their probability of locating food was further reduced regardless of the experience of their demonstrators. Our results show that predation risk can affect the foraging ability of minnows both directly and indirectly through social information from conspecifics. We conclude that social information may influence and constrain individual behavioural decisions, especially in rapidly changing environments where private information is often insufficient.     

True imitation in marmosets

Marmosets, Callithrix jacchus, observed a demonstrator removing the lids from a series of plastic canisters to obtain a mealworm. When subsequently allowed access to the canisters, marmosets that observed a demonstrator using its hands to remove the lids used only their hands. In contrast, marmosets that observed a demonstrator using its mouth also used their mouth to remove the lids. Since hand and mouth demonstrators brought about identical changes in the canisters, the differential test behaviour of the observer groups suggests that they learned about the demonstrator's behaviour. Furthermore, marmosets that had not been given the opportunity to observe a demonstrator prior to testing had a low probability of mouth opening, even if the canisters were previously opened by a mouth-opening demonstrator in an olfactory control experiment. Corroborating Bugnyar & Huber's (1997, Animal Behaviour, 54, 817-831) earlier findings, our results provide further evidence that marmosets can imitate. Copyright 2000 The Association for the Study of Animal Behaviour.     

Social learning influences the preferences of domestic hens for novel food

It has been argued that social learning helps animals either avoid noxious substances or identify food items, but evidence suggests that avian social learning is fundamentally different from that of mammals. In two experiments, we investigated whether the preferences of domestic hens, Gallus g. domesticus, for novel food were influenced by observing the feeding behaviour of conspecifics. In experiment 1, we attempted to confirm that birds can develop socially learnt aversions to unpalatable foods. Despite demonstrators showing a highly visible ‘disgust reaction’ after eating unpalatable coloured food, observers did not develop aversions to similarly coloured food. In experiment 2, we aimed to determine whether preferences for palatable food were socially learnt, and whether the extent of a demonstrator's preference for novel food affected the magnitude of the observer's socially learned preference. Demonstrators ate coloured food of standard or high palatability, or did not peck food at all. When the demonstrators pecked more frequently or fed more quickly from the food, the observers consumed a greater proportion of food of the same colour; however, this was only when the food was red, not green. We argue this indicates an unlearned aversion to red food, overcome by social learning of the food being highly palatable. The results provide no evidence that adult hens learn aversions through observing disgust reactions, but show that hens are sensitive to the extent of demonstrator preferences for palatable food. The data do not support the hypothesis that avian social learning is fundamentally different from that of mammals. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Observational visuospatial encoding of the cache locations of others by western scrub-jays (<Emphasis Type="Italic">Aphelocoma californica</Emphasis>)

Western scrub-jays (Aphelocoma californica) hide food and rely on spatial memory to recover their caches at a later date. They also rely on observational spatial memory to steal caches made by other individuals. Successful pilfering may require an understanding of allocentric space because the observer will often be in a different position from the demonstrator when the caching event occurs. We compared cache recovery accuracy of pairs of observers that watched a demonstrator cache food. The pattern of recovery searches showed that observers were more accurate when they had observed the caching event from the same viewing direction as the demonstrator than when they had watched from the opposite direction. Search accuracy was not affected by whether or not the tray-specific local cues provided left–right landmark information (i.e. heterogeneous vs. homogeneous local cues), or whether or not the caching tray location was rotated. Taken together, these results suggest that observers have excellent spatial memory and that they have little difficulty with mental rotation.     

Network analyses support the role of prey preferences in shaping resource use patterns within five animal populations

Individual variation is an inherent aspect of animal populations and understanding the mechanisms shaping resource use patterns within populations is crucial to comprehend how individuals partition resources. Theory predicts that differences in prey preferences among consumers and/or differences in the likelihood of adding new resources to their diets are key mechanisms underlying intrapopulation variation in resource use. We developed network models based on optimal diet theory that simulate how individuals consume resources under varying scenarios of individual variation in prey preferences and in the willingness of consuming alternate resources. We then investigated how the structure of individual–resource networks generated under each model compared to the structure of observed networks representing five classical examples of individual diet variation. Our results support the notion that, for the studied populations, individual variation in prey preferences is the major factor explaining patterns in individual–resource networks. In contrast, variation in the willingness of adding prey does not seem to play an important role in shaping patterns of resource use. Individual differences in prey preferences in the studied populations may be generated by complex behavioral rules related to cognitive constraints and experience. Our approach provides a pathway for mapping foraging models into network patterns, which may allow determining the possible mechanisms leading to variation in resource use within populations.     

Spread of social information and dynamics of social transmission within Drosophila groups

Understanding how behavioral diversity arises and is maintained is central to evolutionary biology. Genetically based inheritance has been a predominant research focus of the last century; however, nongenetic inheritance, such as social transmission, has become a topic of increasing interest [1]. How social information impacts behavior depends on the balance between information gathered directly through personal experience versus that gleaned through social interactions and on the diffusion of this information within groups [2, 3]. We investigate how female Drosophila melanogaster use social information under seminatural conditions and whether this information can spread and be maintained within a group, a prerequisite for establishing behavioral transmission [4]. We show that oviposition site choice is heavily influenced by previous social interactions. Naive observer flies develop a preference for the same egg-laying medium as experienced demonstrator flies conditioned to avoid one of two equally rewarding media. Surprisingly, oviposition site preference was socially transmitted from demonstrators to observers even when they interacted in a cage with only unflavored, pure agar medium, and even when the observer flies had previous personal experience with both rewarding media. Our findings shed light on the diffusion process of social information within groups, on its maintenance, and ultimately, on the roots of behavioral local adaptation.     

The effects of dietary macronutrients on flight ability,energetics, and fuel metabolism of yellow‐rumped warblers Setophaga coronata

The catabolism of protein from organs and muscles during migratory flight is necessary to produce glucose, key metabolic intermediates, and water, but may have negative effects on flight range and refueling at stopovers. We tested the hypothesis, suggested by previous studies, that birds that eat high‐protein insect diets use more protein for fuel in flight than those that eat high‐carbohydrate fruits. First, we fed migratory yellow‐rumped warblers synthetic fruit or mixed insect/fruit diets, and measured metabolic rates and fuel mixture under basal conditions and during exercise in a hop/hover wheel respirometer. Birds eating the fruit diet had greater plasma triglyceride and non‐esterified fatty acid concentrations, and the higher protein mixed diet increased plasma uric acid only during feeding. Diet did not affect metabolic rates or the fuel mixture under resting or exercise conditions. We then fed yellow‐rumped warblers synthetic diets that differed only in the relative proportion of carbohydrate and protein (60:15 versus 15:60 as % dry mass) and tested them in wind tunnel flights lasting up to six hours. Birds fed the high carbohydrate diet became heavier and fatter than when fed the high protein diet. Plasma uric acid concentration was increased and plasma phospholipid concentration was decreased by the high protein diet in the pre‐flight state (after a 3 h fast), but diet only affected plasma phospholipids during flight (lower in high protein birds). Neither diet nor amount of body fat affected the rate of loss of lean mass or fat during flight. Inter‐individual or seasonal differences in diet do not appear to influence the amount of protein catabolized during endurance flight. However, birds fed the high carbohydrate diet had greater voluntary flight duration, independent of body fatness, suggesting that there may be other performance benefits of high carbohydrate diets for migratory birds.