Social and spatial effects on genetic variation between foraging flocks in a wild bird population

Social interactions are rarely random. In some instances, animals exhibit homophily or heterophily, the tendency to interact with similar or dissimilar conspecifics, respectively. Genetic homophily and heterophily influence the evolutionary dynamics of populations, because they potentially affect sexual and social selection. Here, we investigate the link between social interactions and allele frequencies in foraging flocks of great tits (Parus major) over three consecutive years. We constructed co‐occurrence networks which explicitly described the splitting and merging of 85,602 flocks through time (fission–fusion dynamics), at 60 feeding sites. Of the 1,711 birds in those flocks, we genotyped 962 individuals at 4,701 autosomal single nucleotide polymorphisms (SNPs). By combining genomewide genotyping with repeated field observations of the same individuals, we were able to investigate links between social structure and allele frequencies at a much finer scale than was previously possible. We explicitly accounted for potential spatial effects underlying genetic structure at the population level. We modelled social structure and spatial configuration of great tit fission–fusion dynamics with eigenvector maps. Variance partitioning revealed that allele frequencies were strongly affected by group fidelity (explaining 27%–45% of variance) as individuals tended to maintain associations with the same conspecifics. These conspecifics were genetically more dissimilar than expected, shown by genomewide heterophily for pure social (i.e., space‐independent) grouping preferences. Genomewide homophily was linked to spatial configuration, indicating spatial segregation of genotypes. We did not find evidence for homophily or heterophily for putative socially relevant candidate genes or any other SNP markers. Together, these results demonstrate the importance of distinguishing social and spatial processes in determining population structure.     

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.     

Social networks predict patch discovery in a wild population of songbirds

Animals use social information in a wide variety of contexts. Its extensive use by individuals to locate food patches has been documented in a number of species, and various mechanisms of discovery have been identified. However, less is known about whether individuals differ in their access to, and use of, social information to find food. We measured the social network of a wild population of three sympatric tit species (family Paridae) and then recorded individual discovery of novel food patches. By using recently developed methods for network-based diffusion analysis, we show that order of arrival at new food patches was predicted by social associations. Models based only on group searching did not explain this relationship. Furthermore, network position was correlated with likelihood of patch discovery, with central individuals more likely to locate and use novel foraging patches than those with limited social connections. These results demonstrate the utility of social network analysis as a method to investigate social information use, and suggest that the greater probability of receiving social information about new foraging patches confers a benefit on more socially connected individuals.     

Mixed company: a framework for understanding the composition and organization of mixed‐species animal groups

Mixed‐species animal groups (MSGs) are widely acknowledged to increase predator avoidance and foraging efficiency, among other benefits, and thereby increase participants' fitness. Diversity in MSG composition ranges from two to 70 species of very similar or completely different phenotypes. Yet consistency in organization is also observable in that one or a few species usually have disproportionate importance for MSG formation and/or maintenance. We propose a two‐dimensional framework for understanding this diversity and consistency, concentrating on the types of interactions possible between two individuals, usually of different species. One axis represents the similarity of benefit types traded between the individuals, while the second axis expresses asymmetry in the relative amount of benefits/costs accrued. Considering benefit types, one extreme represents the case of single‐species groups wherein all individuals obtain the same supplementary, group‐size‐related benefits, and the other extreme comprises associations of very different, but complementary species (e.g. one partner creates access to food while the other provides vigilance). The relevance of social information and the matching of activities (e.g. speed of movement) are highest for relationships on the supplementary side of this axis, but so is competition; relationships between species will occur at points along this gradient where the benefits outweigh the costs. Considering benefit amounts given or received, extreme asymmetry occurs when one species is exclusively a benefit provider and the other a benefit user. Within this parameter space, some MSG systems are constrained to one kind of interaction, such as shoals of fish of similar species or leader–follower interactions in fish and other taxa. Other MSGs, such as terrestrial bird flocks, can simultaneously include a variety of supplementary and complementary interactions. We review the benefits that species obtain across the diversity of MSG types, and argue that the degree and nature of asymmetry between benefit providers and users should be measured and not just assumed. We then discuss evolutionary shifts in MSG types, focusing on drivers towards similarity in group composition, and selection on benefit providers to enhance the benefits they can receive from other species. Finally, we conclude by considering how individual and collective behaviour in MSGs may influence both the structure and processes of communities.     

Individuals in foraging groups may use vocal cues when assessing their need for anti-predator vigilance

Many studies of social species have reported variation in the anti-predator vigilance behaviour of foraging individuals depending on the presence and relative position of other group members. However, little attention has focused on how foragers assess these variables. It is commonly assumed that they do so visually, but many social species produce frequent calls while foraging, and these 'close' calls might provide valuable spatial information. Here, we show that foraging pied babblers (Turdoides bicolor) are less vigilant when in larger groups, in the centre of a group and in closer proximity to another group member. We then show that foragers are less vigilant during playbacks of close calling by more individuals and individuals on either side of them when compared with calls of fewer individuals and calls on one side of them. These results suggest that foragers can use vocal cues to gain information on group size and their spatial position within a group. Future studies of anti-predator vigilance should consider the relative importance of both visual and vocal monitoring of group members.     

Social carry‐over effects underpin trans‐seasonally linked structure in a wild bird population

Spatial structure underpins numerous population processes by determining the environment individuals' experience and which other individuals they encounter. Yet, how the social landscape influences individuals' spatial decisions remains largely unexplored. Wild great tits (Parus major) form freely moving winter flocks, but choose a single location to establish a breeding territory over the spring. We demonstrate that individuals' winter social associations carry‐over into their subsequent spatial decisions, as individuals breed nearer to those they were most associated with during winter. Further, they also form territory boundaries with their closest winter associates, irrespective of breeding distance. These findings were consistent across years, and among all demographic classes, suggesting that such social carry‐over effects may be general. Thus, prior social structure can shape the spatial proximity, and fine‐scale arrangement, of breeding individuals. In this way, social networks can influence a wide range of processes linked to individuals' breeding locations, including other social interactions themselves.     

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.     

Social transmission of nectar-robbing behaviour in bumble-bees

Social transmission of acquired foraging techniques is rarely considered outside of a vertebrate context. Here, however, we show that nectar robbing by bumble-bees (Bombus terrestris)-an invertebrate behaviour of considerable ecological significance-has the potential to spread through a population at the accelerated rates typical of social transmission. Nectar robbing occurs when individuals either bite through the base of a flower to 'steal' nectar (primary robbing) or use robbing holes that others have made (secondary robbing). We found that experience of foraging from robbed flowers significantly promoted the development of primary robbing in previously legitimate foragers, thus implying that the acquisition of nectar robbing by one individual will facilitate its adoption in others. Our findings suggest that the positive feedback effects of social transmission may potentially play an ecologically important role in the relationship between plants and pollinators.     

Experimental manipulation of avian social structure reveals segregation is carried over across contexts

Our current understanding of animal social networks is largely based on observations or experiments that do not directly manipulate associations between individuals. Consequently, evidence relating to the causal processes underlying such networks is limited. By imposing specified rules controlling individual access to feeding stations, we directly manipulated the foraging social network of a wild bird community, thus demonstrating how external factors can shape social structure. We show that experimentally imposed constraints were carried over into patterns of association at unrestricted, ephemeral food patches, as well as at nesting sites during breeding territory prospecting. Hence, different social contexts can be causally linked, and constraints at one level may have consequences that extend into other aspects of sociality. Finally, the imposed assortment was lost following the cessation of the experimental manipulation, indicating the potential for previously perturbed social networks of wild animals to recover from segregation driven by external constraints.     

Bottlenose dolphin (Tursiops truncatus) social structure in the Shannon Estuary,Ireland, is distinguished by age‐ and area‐related associations

Social and network analyses that incorporate information on individuals within a population enhance our knowledge of complex species. In this study, the social structure of wild bottlenose dolphins in the Shannon Estuary, Ireland, was analyzed by examining the dynamics of the whole population and then of individuals classed by sex, age, and area. One hundred and twenty‐one dolphins were identified during 522 sightings between 2012 and 2015. The mean half‐weight association index (HWI) of the population was 0.07 ± 0.02. The highest HWIs for individuals of known sex were for female‐male pairs. Mean within‐class HWI was significantly higher than mean between‐class HWI for both age and area classes. Ordinations and sociograms were used to visualize social networks. Permutation tests revealed nonrandom associations for the population overall and both between and within classes. Temporal analyses showed associations persisting for >1,000 d. The whole population's best fit model was for two levels of casual acquaintances. Movement analyses demonstrated the use of the inner estuary by only 25% of the population revealing a potential community division by area. The difference between mean HWI when socializing (0.09 ± 0.03) compared to foraging (0.06 ± 0.03) was significant. These results highlight the importance of localized research, reflecting the complexity found in bottlenose dolphin societies globally.     

Individual-level personality influences social foraging and collective behaviour in wild birds

There is increasing evidence that animal groups can maintain coordinated behaviour and make collective decisions based on simple interaction rules. Effective collective action may be further facilitated by individual variation within groups, particularly through leader–follower polymorphisms. Recent studies have suggested that individual-level personality traits influence the degree to which individuals use social information, are attracted to conspecifics, or act as leaders/followers. However, evidence is equivocal and largely limited to laboratory studies. We use an automated data-collection system to conduct an experiment testing the relationship between personality and collective decision-making in the wild. First, we report that foraging flocks of great tits (Parus major) show strikingly synchronous behaviour. A predictive model of collective decision-making replicates patterns well, suggesting simple interaction rules are sufficient to explain the observed social behaviour. Second, within groups, individuals with more reactive personalities behave more collectively, moving to within-flock areas of higher density. By contrast, proactive individuals tend to move to and feed at spatial periphery of flocks. Finally, comparing alternative simulations of flocking with empirical data, we demonstrate that variation in personality promotes within-patch movement while maintaining group cohesion. Our results illustrate the importance of incorporating individual variability in models of social behaviour.     

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.     

Species importance in a heterospecific foraging association network

There is a growing recognition of the need to integrate non‐trophic interactions into ecological networks for a better understanding of whole‐community organization. To achieve this, the first step is to build networks of individual non‐trophic interactions. In this study, we analyzed a network of interdependencies among bird species that participated in heterospecific foraging associations (flocks) in an evergreen forest site in the Western Ghats, India. We found the flock network to contain a small core of highly important species that other species are strongly dependent on, a pattern seen in many other biological networks. Further, we found that structural importance of species in the network was strongly correlated to functional importance of species at the individual flock level. Finally, comparisons with flock networks from other Asian forests showed that the same taxonomic groups were important in general, suggesting that species importance was an intrinsic trait and not dependent on local ecological conditions. Hence, given a list of species in an area, it may be possible to predict which ones are likely to be important. Our study provides a framework for the investigation of other heterospecific foraging associations and associations among species in other non‐trophic contexts.     

Functional traits determine heterospecific use of risk‐related social information in forest birds of tropical South‐East Asia

In birds and mammals, mobbing calls constitute an important form of social information that can attract numerous sympatric species to localized mobbing aggregations. While such a response is thought to reduce the future predation risk for responding species, there is surprisingly little empirical evidence to support this hypothesis. One way to test the link between predation risk reduction and mobbing attraction involves testing the relationship between species’ attraction to mobbing calls and the functional traits that define their vulnerability to predation risk. Two important traits known to influence prey vulnerability include relative prey‐to‐predator body size ratio and the overlap in space use between predator and prey; in combination, these measures strongly influence prey accessibility, and therefore their vulnerability, to predators. Here, we combine community surveys with behavioral experiments of a diverse bird assemblage in the lowland rainforest of Sumatra to test whether the functional traits of body mass (representing body size) and foraging height (representing space use) can predict species’ attraction to heterospecific mobbing calls. At four forest sites along a gradient of forest degradation, we characterized the resident bird communities using point count and mist‐netting surveys, and determined the species groups attracted to standardized playbacks of mobbing calls produced by five resident bird species of roughly similar body size and foraging height. We found that (1) a large, diverse subcommunity of bird species was attracted to the mobbing calls and (2) responding species (especially the most vigorous respondents) tended to be (a) small (b) mid‐storey foragers (c) with similar trait values as the species producing the mobbing calls. Our findings from the relatively lesser known bird assemblages of tropical Asia add to the growing evidence for the ubiquity of heterospecific information networks in animal communities, and provide empirical support for the long‐standing hypothesis that predation risk reduction is a major benefit of mobbing information networks.     

Social associations in common carp (Cyprinus carpio): Insights from induced feeding aggregations for targeted management strategies

Heterogeneity in social interactions can have important consequences for the spread of information and diseases and consequently conservation and invasive species management. Common carp (Cyprinus carpio) are a highly social, ubiquitous, and invasive freshwater fish. Management strategies targeting foraging carp may be ideal because laboratory studies have suggested that carp can learn, have individual personalities, a unique diet, and often form large social groups. To examine social feeding behaviors of wild carp, we injected 344 carp with passive integrated transponder (PIT) tags and continuously monitored their feeding behaviors at multiple sites in a natural lake in Minnesota, USA. The high‐resolution, spatio‐temporal data were analyzed using a Gaussian mixture model (GMM). Based on these associations, we analyzed group size, feeding bout duration, and the heterogeneity and connectivity of carp social networks at foraging sites. Wild carp responded quickly to bait, forming aggregations most active from dusk to dawn. During the 2020 baiting period (20 days), 133 unique carp were detected 616,593 times. There was some evidence that feeding at multiple sites was constrained by basin geography, but not distance alone. GMM results suggested that feeding bouts were short, with frequent turnover of small groups. Individual foraging behavior was highly heterogeneous with Gini coefficients of 0.79 in 2020 and 0.66 in 2019. “Superfeeders”—those contributing to 80% of total cumulative detections (top 18% and top 29% of foragers in 2020 and 2019 respectively)—were more likely to be detected earlier at feeding stations, had larger body sizes, and had higher network measures of degree, weighted degree, and betweenness than non‐superfeeders. Overall, our results indicate that wild carp foraging is social, easily induced by bait, dominated by large‐bodied individuals, and potentially predictable, which suggests social behaviors could be leveraged in management of carp, one of the world''s most recognizable and invasive fish.     

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.     

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.     

Immature gannets follow adults in commuting flocks providing a potential mechanism for social learning

Group travel is a familiar phenomenon among birds but the causes of this mode of movement are often unclear. For example, flocking flight may reduce flight costs, enhance predator avoidance or increase foraging efficiency. In addition, naive individuals may also follow older, more experienced conspecifics as a learning strategy. However, younger birds may be slower than adults so biomechanical and social effects on flock structure may be difficult to separate. Gannets are wide‐ranging (100s–1000s km) colonial seabirds that often travel in V or echelon‐shaped flocks. Tracking suggests that breeding gannets use memory to return repeatedly to prey patches 10s–100s km wide but it is unclear how these are initially discovered. Public information gained at the colony or by following conspecifics has been hypothesised to play a role, especially during early life. Here, we address two hypotheses: 1) flocking reduces flight costs and 2) young gannets follow older ones in order to locate prey. To do so, we recorded flocks of northern gannets commuting to and from a large colony and passing locations offshore and used a biomechanical model to test for age differences in flight speeds. Consistent with the aerodynamic hypothesis, returning flocks were significantly larger than departing flocks, while, consistent with the information gathering hypothesis, immatures travelled in flocks more frequently than adults and these flocks were more likely to be led by adults than expected by chance. Immatures did not systematically occupy the last position in flocks and had similar theoretical airspeeds to adults, making it unlikely that they follow, rather than lead, for biomechanical reasons. We therefore conclude that while gannets are likely to travel in flocks in part to reduce flight costs, the positions of immatures in those flocks may result in a flow of information from adults to immatures, potentially leading to social learning.     

Foraging ecology drives social information reliance in an avian eavesdropping community

Vertebrates obtain social information about predation risk by eavesdropping on the alarm calls of sympatric species. In the Holarctic, birds in the family Paridae function as sentinel species; however, factors shaping eavesdroppers' reliance on their alarm calls are unknown. We compared three hypothesized drivers of eavesdropper reliance: (a) foraging ecology, (b) degree of sociality, and (c) call relevance (caller‐to‐eavesdropper body‐size difference). In a rigorous causal‐comparative design, we presented Tufted Titmouse (Baeolophus bicolor) alarm calls to 242 individuals of 31 ecologically diverse bird species in Florida forests and recorded presence/absence and type (diving for cover or freezing in place) of response. Playback response was near universal, as individuals responded to 87% of presentations (N = 211). As an exception to this trend, the sit‐and‐wait flycatcher Eastern Phoebe (Sayornis phoebe) represented 48% of the nonresponses. We tested 12 predictor variables representing measures relevant to the three hypothesized drivers, distance to playback speaker, and vulnerability at time of playback (eavesdropper's microhabitat when alarm call is detected). Using model‐averaged generalized linear models, we determined that foraging ecology best predicted playback response, with aerial foragers responding less often. Foraging ecology (distance from trunk) and microhabitat occupied during playback (distance to escape cover) best predicted escape behavior type. We encountered a sparsity of sit‐and‐wait flycatchers (3 spp.), yet their contrasting responses relative to other foraging behaviors clearly identified foraging ecology as a driver of species‐specific antipredator escape behavior. Our findings align well with known links between the exceptional visual acuity and other phenotypic traits of flycatchers that allow them to rely more heavily on personal rather than social information while foraging. Our results suggest that foraging ecology drives species‐specific antipredator behavior based on the availability and type of escape cover.     

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.