Interspecific social networks promote information transmission in wild songbirds

Understanding the functional links between social structure and population processes is a central aim of evolutionary ecology. Multiple types of interactions can be represented by networks drawn for the same population, such as kinship, dominance or affiliative networks, but the relative importance of alternative networks in modulating population processes may not be clear. We illustrate this problem, and a solution, by developing a framework for testing the importance of different types of association in facilitating the transmission of information. We apply this framework to experimental data from wild songbirds that form mixed-species flocks, recording the arrival (patch discovery) of individuals to novel foraging sites. We tested whether intraspecific and interspecific social networks predicted the spread of information about novel food sites, and found that both contributed to transmission. The likelihood of acquiring information per unit of connection to knowledgeable individuals increased 22-fold for conspecifics, and 12-fold for heterospecifics. We also found that species varied in how much information they produced, suggesting that some species play a keystone role in winter foraging flocks. More generally, these analyses demonstrate that this method provides a powerful approach, using social networks to quantify the relative transmission rates across different social relationships.     

How does hunger affect convergence on prey patches in a social forager?

Internal state, in this case hunger, is known to influence both the organisation of animal groups and the social foraging interactions that occur within them. In this study, we investigated the effects of hunger upon the time taken to locate and converge upon hidden simulated prey patches in a socially foraging fish, the threespine stickleback (Gasterosteus aculeatus). We predicted that groups of food‐deprived fish would find and recruit to prey patches faster than recently fed groups, reasoning that they might search more rapidly and be more attentive to inadvertent social information produced by other foragers. Instead we saw no difference between the two groups in the time taken to find the patches and found that in fact, once prey patches had been discovered, it was the recently fed fish that converged on them most rapidly. This finding is likely due to the fact that recently fed fish tend to organise themselves into fewer but larger subgroups, which arrived at the food patch together. Hunger has a significant impact upon the social organisation of the fish shoals, and it appears that this has a stronger effect upon the rate at which they converged upon the food patches than does internal state itself.     

Shoal and prey patch choice by co-occurring fishes and prawns: inter-taxa use of socially transmitted cues

Animals can use socially transmitted information to learn about the distribution and quality of resources without incurring the costs associated with having to search for and sample them first hand. Recently, it has been shown that the use of chemical social information specific to patterns of diet and habitat use is an important mechanism underpinning recognition and social organization in shoaling fishes. In this study we revealed that the use of resource-specific chemical information is not limited to conspecifics, or even members of the same taxon. In a series of laboratory experiments, we showed that threespine sticklebacks (Gasterosteus aculeatus) could recognize similar patterns of habitat use in common prawns (Leander serratus), preferentially orientating towards groups of prawns exposed to the same habitats as themselves, and even selecting foraging patches located close to them. Prawns were seen to use habitat-specific cues generated by conspecifics, but not by sticklebacks, suggesting that the benefits of forming these heterospecific social association patterns may be unequal for prawns and fishes. Our findings suggest that some species might use co-occurring, unrelated species as information centres in order to orient and locate resources within their surroundings.     

Information flow through threespine stickleback networks without social transmission

Social networks can result in directed social transmission of learned information, thus influencing how innovations spread through populations. Here we presented shoals of threespine sticklebacks (Gasterosteous aculeatus) with two identical foraging tasks and applied network-based diffusion analysis (NBDA) to determine whether the order in which individuals in a social group contacted and solved the tasks was affected by the group's network structure. We found strong evidence for a social effect on discovery of the foraging tasks with individuals tending to discover a task sooner when others in their group had previously done so, and with the spread of discovery of the foraging tasks influenced by groups' social networks. However, the same patterns of association did not reliably predict spread of solution to the tasks, suggesting that social interactions affected the time at which the tasks were discovered, but not the latency to its solution following discovery. The present analysis, one of the first applications of NBDA to a natural animal system, illustrates how NBDA can lead to insight into the mechanisms supporting behaviour acquisition that more conventional statistical approaches might miss. Importantly, we provide the first compelling evidence that the spread of novel behaviours can result from social learning in the absence of social transmission, a phenomenon that we refer to as an untransmitted social effect on learning.     

The dining etiquette of desert baboons: the roles of social bonds, kinship, and dominance in co-feeding networks

To better understand how individual relationships influence patterns of social foraging in primate groups, we explored networks of co-feeding in wild desert baboons (Papio ursinus). To minimize the risk of aggression and injury associated with contest competition, we expected that individual group members would choose to co-feed with those group-mates that are most likely to show tolerance and a willingness to share food patches. We tested two alternative hypotheses about who those group-mates might be: the "social bonds hypothesis" predicts that preferred foraging partners will be those with whom individuals share strong social bonds, indexed by grooming, whereas the "kinship hypothesis" predicts that preferred foraging partners will be relatives. We also investigated and controlled for the effects of dominance rank, given that competitive ability is known to shape foraging patterns. Social network analyses of over 5,000 foraging events for 14 adults in a single troop revealed that baboon co-feeding was significantly correlated with grooming relationships but not genetic relatedness, and this finding was also true of the female-only co-feeding network. Dominant individuals were also found to be central to the co-feeding network, frequently sharing food patches with multiple group-mates. This polyadic analysis of foraging associations between individuals underlines the importance of dominance and affiliation to patterns of primate social foraging.     

The role of conformity in foraging when personal and social information conflict

There is currently considerable interest in the interplay betweenpersonal and social information in decision-making processes.Two experiments are presented exploring the relative use ofprior personal information and subsequent social informationin foraging decisions of guppies. Experiment 1 tested the assumptionthat when the use of information acquired through personal experienceis not costly, conflicting social information will be ignored.The assumption was confirmed because, when given a choice betweenfeeding at two food patches, at one of which they had previouslyseen conspecifics feed, individual fish with prior experienceof feeding at the alternative site chose the alternative, whereasfish with no prior experience chose the site at which theirconspecifics had fed. Experiment 2 tested theoretical predictionsthat when the use of information acquired through personal experienceis potentially costly, conflicting social information will beweighed more heavily than will personal information. The predictionwas confirmed because, when given a choice between feeding attwo food patches, one at which they had previously seen conspecificsfeed and one behind a visual barrier, individual fish with priorexperience of feeding behind the barrier chose the site at whichtheir conspecifics had fed. These findings suggest that conformitycan promote social learning in naïve individuals, but priorexperience can insulate individuals from conformity providedthe costs of relying on that experience are small. In addition,the experiments highlight the fact that personal and socialinformation are not always weighed equally.     

Learning rules for social foragers: implications for the producer-scrounger game and ideal free distribution theory

In population games, the optimal behaviour of a forager depends partly on courses of action selected by other individuals in the population. How individuals learn to allocate effort in foraging games involving frequency-dependent payoffs has been little examined. The performance of three different learning rules was investigated in several types of habitats in each of two population games. Learning rules allow individuals to weigh information about the past and the present and to choose among alternative patterns of behaviour. In the producer-scrounger game, foragers use producer to locate food patches and scrounger to exploit the food discoveries of others. In the ideal free distribution game, foragers that experience feeding interference from companions distribute themselves among heterogeneous food patches. In simulations of each population game, the use of different learning rules induced large variation in foraging behaviour, thus providing a tool to assess the relevance of each learning rule in experimental systems. Rare mutants using alternative learning rules often successfully invaded populations of foragers using other rules indicating that some learning rules are not stable when pitted against each other. Learning rules often closely approximated optimal behaviour in each population game suggesting that stimulus-response learning of contingencies created by foraging companions could be sufficient to perform at near-optimal level in two population games.     

Use of Social Information in Seabirds: Compass Rafts Indicate the Heading of Food Patches

Ward and Zahavi suggested in 1973 that colonies could serve as information centres, through a transfer of information on the location of food resources between unrelated individuals (Information Centre Hypothesis). Using GPS tracking and observations on group movements, we studied the search strategy and information transfer in two of the most colonial seabirds, Guanay cormorants (Phalacrocorax bougainvillii) and Peruvian boobies (Sula variegata). Both species breed together and feed on the same prey. They do return to the same feeding zone from one trip to the next indicating high unpredictability in the location of food resources. We found that the Guanay cormorants use social information to select their bearing when departing the colony. They form a raft at the sea surface whose position is continuously adjusted to the bearing of the largest returning columns of cormorants. As such, the raft serves as a compass signal that gives an indication on the location of the food patches. Conversely, Peruvian boobies rely mainly on personal information based on memory to take heading at departure. They search for food patches solitarily or in small groups through network foraging by detecting the white plumage of congeners visible at long distance. Our results show that information transfer does occur and we propose a new mechanism of information transfer based on the use of rafts off colonies. The use of rafts for information transfer may be common in central place foraging colonial seabirds that exploit short lasting and/or unpredictably distributed food patches. Over the past decades Guanay cormorants have declined ten times whereas Peruvian boobies have remained relatively stable. We suggest that the decline of the cormorants could be related to reduced social information opportunities and that social behaviour and search strategies have the potential to play an important role in the population dynamics of colonial animals.     

An exploration of the relationship between recruitment communication and foraging in stingless bees

Social information is widely used in the animal kingdom and can be highly adaptive. In social insects, foragers can use social information to find food, avoid danger, or choose a new nest site. Copying others allows individuals to obtain information without having to sample the environment. When foragers communicate information they will often only advertise high-quality food sources, thereby filtering out less adaptive information. Stingless bees, a large pantropical group of highly eusocial bees, face intense inter- and intra-specific competition for limited resources, yet display disparate foraging strategies. Within the same environment there are species that communicate the location of food resources to nest-mates and species that do not. Our current understanding of why some species communicate foraging sites while others do not is limited. Studying freely foraging colonies of several co-existing stingless bee species in Brazil, we investigated if recruitment to specific food locations is linked to 1) the sugar content of forage, 2) the duration of foraging trips, and 3) the variation in activity of a colony from 1 day to another and the variation in activity in a species over a day. We found that, contrary to our expectations, species with recruitment communication did not return with higher quality forage than species that do not recruit nestmates. Furthermore, foragers from recruiting species did not have shorter foraging trip durations than those from weakly recruiting species. Given the intense inter- and intraspecific competition for resources in these environments, it may be that recruiting species favor food resources that can be monopolized by the colony rather than food sources that offer high-quality rewards.     

Use of Social and Ecological Information in Tamarin Foraging Decisions

A major consequence of group living is that foragers may rely on social information in addition to ecological information to locate feeding sites. Although conspecifics can provide cues as to the spatial location of food patches, individual foraging decisions also must include some assessment of the likelihood of obtaining access to a resource other group members seek. This likelihood differs in the 2 models generally proposed to explain intragroup social foraging: the information-sharing model and the producer-scrounger model. We conducted an experimental field study on wild groups of emperor (Saguinus imperator) and saddleback (S. fuscicollis) tamarins to determine the foraging strategies adopted by individual group members and their relationship to social rank, food intake, and the ability to use ecological and social information in making intra-patch foraging decisions. Individual tamarins applied different behavioral strategies compatible with a finder-joiner paradigm to solve foraging problems. About half of the individuals in each study group initiated 74%–90% of all food searches and acted as finders. Most alpha individuals adopted a joiner strategy by monitoring the activities of others' to obtain a reward. The individual arriving first at a reward platform enjoyed a finder's advantage. Despite differences in search effort, both finders and joiners presented similar abilities in learning to associate ecological cues with the presence of food rewards at our experimental feeding stations. We conclude that within a group foraging context, tamarins integrate social and ecological information in decision-making.     

Fish don't read textbooks: juvenile salmon prove ignorant of foraging theory

The rules governing the selection of feeding patches by foraging animals is an area of intense interest. Much work has focussed on the development of theoretical models that predict when individuals should switch patches. Tests of these models have often been conducted in laboratory environments, but it is not clear how much influence patch‐switching decisions have on population‐level parameters such as growth and distribution in more complex natural environments. We used juvenile Atlantic salmon as a model species to investigate the effects of randomly fluctuating food levels on growth and site selection. We used PIT technology to monitor in detail individuals' patterns of patch use and activity in an artificial stream, at natural densities. This allowed us experimental control of food supplies and sufficient replication, while retaining many features of a natural system. Only a few individuals of high social rank switched patches as predicted by an appropriate foraging model; otherwise, although frequent, patch‐switching was not related to food availability. Thus, while laboratory experiments indicate that this species has the potential to choose foraging sites on the basis of food availability, it is unlikely that this behavioural mechanism is of great importance in natural systems; further tests of foraging models under natural conditions are essential if we are to understand their effects at the level of populations.     

The Payoffs to Producing and Scrounging: What Happens when Patches are Divisible?

Although many group-foraging models assume that all individuals search for and share their food equally, most documented instances of group foraging exhibit specialized use of producer and scrounger strategies. In addition, many of the studies have focused on groups with strong individual asymmetries exploiting food that is not easily divisible. In the present study we describe individual foraging behavior of relatively nonaggressive flock foragers exploiting divisible clumps of food. Two experiments, one with flocks of spice finches and another with flocks of zebra finches, suggest that divisibility of food patches may have important consequences for social foraging behavior. Neither dominance nor the distribution and quality of food patches affect the relative advantage that producing individuals enjoy over those that scrounge. Specialized producers and scroungers are absent from flocks of both species. Systems where patches are shared may differ fundamentally from those where patches are monopolized by scroungers.     

Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus)

For social species, being a member of a cohesive group and performing activities as a coordinated unit appear to provide a mechanism for the efficient transmission of information about food. Social learning about food palatability was investigated in two captive primates, Saguinus fuscicollis and S. labiatus, which form stable and cohesive mixed-species groups in the wild. We explored whether an induced food aversion toward a preferred food is modified during and after social interaction with non-averse conspecifics or congeners. Sets of intra- and interspecific pairs were presented with two foods, one of which was considered distasteful by one of the pairs (the other was palatable), and their behavior was compared pre-interaction, during interaction, and post-interaction. For the aversely-conditioned individuals of both species, the change in social context corresponded to a change in their preference for the food that they considered unpalatable, regardless of whether they had interacted with a conspecific or congeneric pair, and the change in food preference was maintained post-interaction. In a control condition, in which averse individuals did not have the opportunity to interact with non-averse animals, S. fuscicollis sampled the preferred food, but not as quickly as when given the opportunity to interact. We conclude that the social learning demonstrated here may allow individual tamarins to track environmental change, such as fruit ripening, more efficiently than asocial learning alone, because social learners can more quickly and safely focus on appropriate behavior by sharing up-to-date foraging information. Furthermore, since the behavior of congeners, as well as conspecifics, acts to influence food choice in a more adaptive direction, social learning about food palatability may be an advantage of mixed-species group formation to tamarins of both species.     

Long‐Distance Calling by the Willow Tit,Poecile montanus,Facilitates Formation of Mixed‐Species Foraging Flocks

The occurrence of mixed‐species foraging flocks is a worldwide phenomenon in terrestrial bird communities. Previous studies suggest that individuals participating in flocks might derive benefits in terms of improved feeding efficiency and/or reduced risk of predation. However, very little is known about how individuals establish mixed‐species flocks. Here, I provide the first experimental evidence that long‐distance calling by the willow tit, Poecile montanus, facilitates the establishment of mixed‐species flocks at a foraging patch. Observations at experimental foraging patches showed that willow tits that find a food source produce long‐distance calls, particularly when they are isolated from conspecific flockmates. The probability of long‐distance calling was negatively correlated with the number of heterospecific foraging individuals near the food source. A playback experiment confirmed that calls attract both conspecific and heterospecific members of foraging flocks. This study demonstrates that willow tits use long‐distance calls to attract conspecific flockmates to foraging patches, and these calls can also facilitate the formation of mixed‐species flocks on patches.     

Communal Roosting of Wintering Red Kites Milvus milvus (Aves,Accipitridae): Social Feeding Strategies for the Exploitation of Food Resources

Social feeding strategies of wintering red kites are analyzed in relation to age, food, roost-sites and differences from kite residents. Whereas young and adult wintering kites gathered at roost sites almost daily, adult residents did not, and immature residents only occasionally. Kites using roost sites feed more often on prey prelocated by others, while lone roosters also forage and discover food alone. After finding food, kites tend to shift to a new roost site and foraging area. Two details of the ‘information centre’ hypothesis are confirmed in our study: carcasses are unpredictably found patches, divisible between several individuals. But carcasses disappeared fast in the study area, and no increase with time in the number of birds consuming a carcass was observed, so that information transmission was unconfirmed. When kites leave the roost in groups no leader is detectable. It seems that other types of social foraging are operating, and the model best matching our results is network foraging.     

Social learning about egg-laying substrates in fruitflies

Social learning, defined as learning from other individuals, has had dramatic effects on some species, including humans, in whom it has generated a rich culture. As a first step in examining the evolution of and mechanisms underlying social learning in insects, we tested for social learning in fruitflies (Drosophila melanogaster). Focal females (observers) that experienced novel food together with mated females (models), who had laid eggs on that food, subsequently exhibited a stronger preference for laying eggs on that food over another novel food compared with focal females that experienced the food alone. We observed no social learning, however, when observers experienced food with potentially more ambiguous social information provided by the presence of either virgin models or aggregation pheromone. This first documentation of social learning about egg-laying substrates in fruitflies builds on recent data indicating intricate use of social information by fruitflies and opens up exciting avenues for research on the evolution and neurogenetics of social learning using biology''s major model system.     

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.     

Foraging zebra finches (Taeniopygia guttata) are public information users rather than conformists

Social learning enables adaptive information acquisition provided that it is not random but selective. To understand species typical decision-making and to trace the evolutionary origins of social learning, the heuristics social learners use need to be identified. Here, we experimentally tested the nature of majority influence in the zebra finch. Subjects simultaneously observed two demonstrator groups differing in relative and absolute numbers (ratios 1 : 2/2 : 4/3 : 3/1 : 5) foraging from two novel food sources (black and white feeders). We find that demonstrator groups influenced observers'' feeder choices (social learning), but that zebra finches did not copy the majority of individuals. Instead, observers were influenced by the foraging activity (pecks) of the demonstrators and in an anti-conformist fashion. These results indicate that zebra finches are not conformist, but are public information users.     

Spatial memory during foraging in prosimian primates: Propithecus edwardsi and Eulemur fulvus rufus

A variety of anthropoids travel efficiently from one food source to another, although there is disagreement over how this is accomplished over large-scale space. Mental maps, for example, require that animals internally represent space, geometrically locate landmarks, use true distance and direction, and generate novel shortcuts to resources. Alternately, topological or route-based maps are based on a network of fixed points, landmarks and routes so that one food patch can be linked with another. In this study we describe travel patterns between food sources for two prosimian species found in southeastern Madagascar, Propithecus edwardsi and Eulemur fulvus rufus. Both species are dependent on fruit and have large home range sizes. By comparing interpatch distances, patch size and turning angles, we found that both species prefer nearest neighbor food patches and P. edwardsi travels in relatively straight lines. The amount of backtracking seen in E. f. rufus may be linked to their large group size and dependence on large-crowned fruit trees. We suggest that the goal-oriented foraging of both prosimian species is dependent on a topological or route-based map. These are rare behavioral data relevant to ecological and social contexts of primate cognitive evolution.     

Public information for solitary foragers: timber rattlesnakes use conspecific chemical cues to select ambush sites

Many animals use public information (PI) gathered from conspecificsto assess the quality of potential foraging locations. To date,research on this phenomenon has focused almost exclusively onsocial foragers that live in groups and monitor nearby individuals.PI is potentially available to solitary foragers as well, inthe form of cues (such as chemical cues) that persist in theenvironment after conspecifics are no longer present. In thisstudy, I examined the response of a solitary sit-and-wait predator,the timber rattlesnake (Crotalus horridus), to chemical cuesfrom conspecifics that had recently fed as opposed to thosethat had been deprived of food. Experiments with a T-maze indicatedthat timber rattlesnakes always follow conspecific chemicaltrails out of the maze, regardless of whether or not the individualleaving the trail had recently fed. However, an enclosure choicetest found that individuals are more likely to select ambushsites in areas with chemical cues from conspecifics that hadrecently fed. These results indicate that snakes may use conspecificchemical cues not only to find mates, shelter sites, and hibernaculabut also profitable food patches. Additionally, this study highlightsthe possibility that other solitary foragers may use PI to guidetheir foraging behavior.