Coupled information networks drive honeybee (Apis mellifera) collective foraging.

Collective behaviour by eusocial insect colonies is typically achieved through multiple communication networks that produce complex behaviour at the group level but often appear to provide redundant or even competing information. A classic example occurs in honeybee (Apis mellifera) colonies, where both the dance communication system and robust scent-based mechanisms contribute to the allocation of a colony's workforce by regulating the flow of experienced foragers among known food sources. Here we analysed social connectivity patterns during the reactivation of experienced foragers to familiar feeding sites to show that these social information pathways are not simply multiple means to achieve the same end but intersect to play complementary roles in guiding forager behaviour. Using artificial feeding stations, we mimicked a natural scenario in which two forager groups were simultaneously collecting from distinct patches containing different flowering species. We then observed the reactivation of these groups at their familiar feeding sites after interrupting their foraging. Social network analysis revealed that temporarily unemployed individuals interacted more often and for longer with foragers that advertised a familiar versus unfamiliar foraging site. Due to such resource-based assortative mixing, network-based diffusion analysis estimated that reactivation events primarily resulted from interactions among bees that had been trained to the same feeding station and less so from different-feeder interactions. Both scent- and dance-based interactions strongly contributed to reactivation decisions. However, each bout of dance-following had an especially strong effect on a follower's likelihood of reactivation, particularly when dances indicated locations familiar to followers. Our findings illustrate how honeybee foragers can alter their social connectivity in ways that are likely to enhance collective outcomes by enabling foragers to rapidly access up-to-date information about familiar foraging sites. In addition, our results highlight how reliance on multiple communication mechanisms enables social insect workers to utilise flexible information-use strategies that are robust to variation in the availability of social information.

Biased cultural transmission of a social custom in chimpanzees.

Cultural transmission studies in animals have predominantly focused on identifying between-group variation in tool-use techniques, while immaterial cultures remain understudied despite their potential for highlighting similarities between human and animal culture. Here, using long-term data from two chimpanzee communities, we tested whether one of chimpanzees' most enigmatic social customs-the grooming handclasp-is culturally transmitted by investigating the influence of well-documented human transmission biases on their variational preferences. After identifying differences in style preferences between the communities, we show that older and dominant individuals exert more influence over their partners' handclasp styles. Mothers were equally likely to influence their offspring's preferences as nonkin, indicating that styles are transmitted both vertically and obliquely. Last, individuals gradually converged on the group style, suggesting that conformity guides chimpanzees' handclasp preferences. Our findings show that chimpanzees' social lives are influenced by cultural transmission biases that hitherto were thought to be uniquely human.

Social transmission in the wild can reduce predation pressure on novel prey signals.

Social transmission of information is taxonomically widespread and could have profound effects on the ecological and evolutionary dynamics of animal communities. Demonstrating this in the wild, however, has been challenging. Here we show by field experiment that social transmission among predators can shape how selection acts on prey defences. Using artificial prey and a novel approach in statistical analyses of social networks, we find that blue tit (Cyanistes caeruleus) and great tit (Parus major) predators learn about prey defences by watching others. This shifts population preferences rapidly to match changes in prey profitability, and reduces predation pressure from naïve predators. Our results may help resolve how costly prey defences are maintained despite influxes of naïve juvenile predators, and suggest that accounting for social transmission is essential if we are to understand coevolutionary processes.

The modularity of a social group does not affect the transmission speed of a novel, socially learned behaviour, or the formation of local variants.

The structure of a group is critical in determining how a socially learnt behaviour will spread. Predictions from theoretical models indicate that specific parameters of social structure differentially influence social transmission. Modularity describes how the structure of a group or network is divided into distinct subgroups or clusters. Theoretical modelling indicates that the modularity of a network will predict the rate of behavioural spread within a group, with higher modularity slowing the rate of spread and facilitating the establishment of local behavioural variants which can prelude local cultures. Despite prolific modelling approaches, empirical tests via manipulations of group structure remain scarce. We experimentally manipulated the modularity of populations of domestic fowl chicks, Gallus gallus domesticus, to affect the transmission of a novel foraging behaviour. We compared the spread of behaviour in populations with networks of high or low modularity against control populations where social transmission was prevented. We found the foraging behaviour to spread socially between individuals when the social transmission was permitted; however, modularity did not increase the speed of behavioural spread nor lead to the initial establishments of shared behavioural variants. This result suggests that factors in the social transmission process additional to the network structure may influence behavioural spread.

The role of food transfers in wild golden lion tamarins (Leontopithecus rosalia): Support for the informational and nutritional hypothesis.

Callitrichidae is a unique primate family not only in terms of the large number of food transfers to infants but also for the prevalence of transfers that are initiated by the adults. It has been hypothesized that, as well as provisioning infants, callitrichid food transfers might function to teach the receiver what food types to eat. If food provisioning has a teaching function, we would expect successful food transfers to be more likely with food types that are novel to the juveniles. We would also expect juveniles to learn about foods from those transfers. We introduced different types of food (some familiar, some novel) to wild groups of golden lion tamarins (Leontopithecus rosalia). While novel foods were not more successfully transferred than familiar food in the experiment, transfers were more successful (i.e., the receiver obtained food) when the donor had previous experience with that food. Moreover, we found evidence suggesting that food transfers influenced the future foraging choices of juveniles. Our findings are consistent with the first and third criteria of the functional definition of teaching, which requires that tutors (the adults) modify their behavior in the presence of a naïve individual (a juvenile), and that the naïve individual learns from the modified behavior of the demonstrator. Our findings are also consistent with the provisioning function of food transfer. Social learning seems to play an important role in the development of young tamarins' foraging preferences.

Detecting and quantifying social transmission using network-based diffusion analysis.

Although social learning capabilities are taxonomically widespread, demonstrating that freely interacting animals (whether wild or captive) rely on social learning has proved remarkably challenging. Network-based diffusion analysis (NBDA) offers a means for detecting social learning using observational data on freely interacting groups. Its core assumption is that if a target behaviour is socially transmitted, then its spread should follow the connections in a social network that reflects social learning opportunities. Here, we provide a comprehensive guide for using NBDA. We first introduce its underlying mathematical framework and present the types of questions that NBDA can address. We then guide researchers through the process of selecting an appropriate social network for their research question; determining which NBDA variant should be used; and incorporating other variables that may impact asocial and social learning. Finally, we discuss how to interpret an NBDA model's output and provide practical recommendations for model selection. Throughout, we highlight extensions to the basic NBDA framework, including incorporation of dynamic networks to capture changes in social relationships during a diffusion and using a multi-network NBDA to estimate information flow across multiple types of social relationship. Alongside this information, we provide worked examples and tutorials demonstrating how to perform analyses using the newly developed nbda package written in the R programming language.

Personality composition determines social learning pathways within shoaling fish.

In shaping how individuals explore their environment and interact with others, personality may mediate both individual and social learning. Yet increasing evidence indicates that personality expression is contingent on social context, suggesting that group personality composition may be key in determining how individuals learn about their environment. Here, we used recovery latency following simulated predator attacks to identify Trinidadian guppies (Poecilia reticulata) that acted in a consistently bold or shy manner. We then employed network-based diffusion analysis to track the spread of a novel foraging behaviour through groups containing different proportions of bold and shy fish. Informed associates promoted learning to a greater extent in bold individuals, but only within groups composed predominately of bold fish. As the proportion of shy fish within groups increased, bold individuals instead emerged as especially effective demonstrators that facilitated learning in others. Individuals were also more likely to learn overall within shy-dominated groups than in bold-dominated ones. We demonstrate that whether and how individuals learn is conditional on group personality composition, indicating that selection may favour traits enabling individuals to better match their behavioural phenotype to their social environment.

Integrating Genetic, Environmental, and Social Networks to Reveal Transmission Pathways of a Dolphin Foraging Innovation.

Cultural behavior, which is transmitted among conspecifics through social learning [1], is found across various taxa [2-6]. Vertical social transmission from parent to offspring [7] is thought to be adaptive because of the parental generation being more skilled than maturing individuals. It is found throughout the animal kingdom, particularly in species with prolonged parental care, e.g., [8, 9]. Social learning can also occur among members of the same generation [4, 10, 11] or between older, non-parental individuals and younger generations [7] via horizontal or oblique transmission, respectively. Extensive work on primate culture has shown that horizontal transmission of foraging behavior is biased toward species with broad cultural repertoires [12] and those with increased levels of social tolerance [13, 14], such as great apes. Vertical social transmission has been established as the primary transmission mechanism of foraging behaviors in the Indo-Pacific bottlenose dolphin (Tursiops aduncus) population of Shark Bay, Western Australia [6, 9, 15, 16]. Here, we investigated the spread of another foraging strategy, "shelling" [17], whereby some dolphins in this population feed on prey trapped inside large marine gastropod shells. Using a multi-network version of "network-based diffusion analysis" (NBDA), we show that shelling behavior spreads primarily through non-vertical social transmission. By statistically accounting for both environmental and genetic influences, our findings thus represent the first evidence of non-vertical transmission of a foraging tactic in toothed whales. This research suggests there are multiple transmission pathways of foraging behaviors in dolphins, highlighting the similarities between cetaceans and great apes in the nature of the transmission of cultural behaviors. VIDEO ABSTRACT.

Social culture in bonobos.

Van Leeuwen et al. found that two peculiar interactive behaviors (social scratching and groom slapping) transmitted socially through bonobo networks across six European zoos.

Network-based diffusion analysis reveals context-specific dominance of dance communication in foraging honeybees.

The honeybee (Apis mellifera) dance communication system is a marvel of collective behaviour, but the added value it brings to colony foraging efficiency is poorly understood. In temperate environments, preventing communication of foraging locations rarely decreases colony food intake, potentially because simultaneous transmission of olfactory information also plays a major role in foraging. Here, we employ social network analyses that quantify information flow across multiple temporally varying networks (each representing a different interaction type) to evaluate the relative contributions of dance communication and hive-based olfactory information transfer to honeybee recruitment events. We show that virtually all successful recruits to novel locations rely upon dance information rather than olfactory cues that could otherwise guide them to the same resource. Conversely, during reactivation to known sites, dances are relatively less important, as foragers are primarily guided by olfactory information. By disentangling the contributions of multiple information networks, the contexts in which dance communication truly matters amid a complex system full of redundancy can now be identified.

Wild primates copy higher-ranked individuals in a social transmission experiment.

Little is known about how multiple social learning strategies interact and how organisms integrate both individual and social information. Here we combine, in a wild primate, an open diffusion experiment with a modeling approach: Network-Based Diffusion Analysis using a dynamic observation network. The vervet monkeys we study were not provided with a trained model; instead they had access to eight foraging boxes that could be opened in either of two ways. We report that individuals socially learn the techniques they observe in others. After having learnt one option, individuals are 31x more likely to subsequently asocially learn the other option than individuals naïve to both options. We discover evidence of a rank transmission bias favoring learning from higher-ranked individuals, with no evidence for age, sex or kin bias. This fine-grained analysis highlights a rank transmission bias in a field experiment mimicking the diffusion of a behavioral innovation.

Learning strategies and long-term memory in Asian short-clawed otters (Aonyx cinereus).

Social learning, where information is acquired from others, is taxonomically widespread. There is growing evidence that animals selectively employ 'social learning strategies', which determine e.g. when to copy others instead of learning asocially and whom to copy. Furthermore, once animals have acquired new information, e.g. regarding profitable resources, it is beneficial for them to commit it to long-term memory (LTM), especially if it allows access to profitable resources in the future. Research into social learning strategies and LTM has covered a wide range of taxa. However, otters (subfamily Lutrinae), popular in zoos due to their social nature and playfulness, remained neglected until a recent study provided evidence of social learning in captive smooth-coated otters (Lutrogale perspicillata), but not in Asian short-clawed otters (Aonyx cinereus). We investigated Asian short-clawed otters' learning strategies and LTM performance in a foraging context. We presented novel extractive foraging tasks twice to captive family groups and used network-based diffusion analysis to provide evidence of a capacity for social learning and LTM in this species. A major cause of wild Asian short-clawed otter declines is prey scarcity. Furthering our understanding of how they learn about and remember novel food sources could inform key conservation strategies.

Multi-network-based diffusion analysis reveals vertical cultural transmission of sponge tool use within dolphin matrilines.

Behavioural differences among social groups can arise from differing ecological conditions, genetic predispositions and/or social learning. In the past, social learning has typically been inferred as responsible for the spread of behaviour by the exclusion of ecological and genetic factors. This 'method of exclusion' was used to infer that 'sponging', a foraging behaviour involving tool use in the bottlenose dolphin (Tursiops aduncus) population in Shark Bay, Western Australia, was socially transmitted. However, previous studies were limited in that they never fully accounted for alternative factors, and that social learning, ecology and genetics are not mutually exclusive in causing behavioural variation. Here, we quantified the importance of social learning on the diffusion of sponging, for the first time explicitly accounting for ecological and genetic factors, using a multi-network version of 'network-based diffusion analysis'. Our results provide compelling support for previous findings that sponging is vertically socially transmitted from mother to (primarily female) offspring. This research illustrates the utility of social network analysis in elucidating the explanatory mechanisms behind the transmission of behaviour in wild animal populations.

Long-term decline in survival and reproduction of dolphins following a marine heatwave.

One of many challenges in the conservation of biodiversity is the recent trend in the frequency and intensity of extreme climatic events [1]. The Shark Bay World Heritage Area, Western Australia, endured an unprecedented marine heatwave in 2011. Catastrophic losses of habitat-forming seagrass meadows followed [2], along with mass mortalities of invertebrate and fish communities [3]. Our long-term demographic data on Shark Bay's resident Indo-Pacific bottlenose dolphin (Tursiops aduncus) population revealed a significant decline in female reproductive rates following the heatwave. Moreover, capture-recapture analyses indicated 5.9% and 12.2% post-heatwave declines in the survival of dolphins that use tools to forage and those that do not, respectively. This implies that the tool-using dolphins may have been somewhat buffered against the cascading effects of habitat loss following the heatwave by having access to a less severely affected foraging niche [4]. Overall, however, lower survival has persisted post-heatwave, suggesting that habitat loss following extreme weather events may have prolonged, negative impacts on even behaviourally flexible, higher-trophic level predators. VIDEO ABSTRACT.

Choosing a sensible cut-off point: assessing the impact of uncertainty in a social network on the performance of NBDA.

Network-based diffusion analysis (NBDA) has become a widely used tool to detect and quantify social learning in animal populations. NBDA infers social learning if the spread of a novel behavior follows the social network and hence relies on appropriate information on individuals' network connections. Most studies on animal populations, however, lack a complete record of all associations, which creates uncertainty in the social network. To reduce this uncertainty, researchers often use a certain threshold of sightings for the inclusion of animals (which is often arbitrarily chosen), as observational error decreases with increasing numbers of observations. Dropping individuals with only few sightings, however, can lead to information loss in the network if connecting individuals are removed. Hence, there is a trade-off between including as many individuals as possible and having reliable data. We here provide a tool in R that assesses the sensitivity of NBDA to error in the social network given a certain threshold for the inclusion of individuals. It simulates a social learning process through a population and then tests the power of NBDA to reliably detect social learning after introducing observational error into the social network, which is repeated for different thresholds. Our tool can help researchers using NBDA to select a threshold, specific to their data set, that maximizes power to reliably quantify social learning in their study population.

Correction to: Strategic crossing of biomass and harvest index-source and sink-achieves genetic gains in wheat.

[This corrects the article DOI: 10.1007/s10681-017-2040-z.].

Social learning in otters.

The use of information provided by others to tackle life's challenges is widespread, but should not be employed indiscriminately if it is to be adaptive. Evidence is accumulating that animals are indeed selective and adopt 'social learning strategies'. However, studies have generally focused on fish, bird and primate species. Here we extend research on social learning strategies to a taxonomic group that has been neglected until now: otters (subfamily Lutrinae). We collected social association data on captive groups of two gregarious species: smooth-coated otters (Lutrogale perspicillata), known to hunt fish cooperatively in the wild, and Asian short-clawed otters (Aonyx cinereus), which feed individually on prey requiring extractive foraging behaviours. We then presented otter groups with a series of novel foraging tasks, and inferred social transmission of task solutions with network-based diffusion analysis. We show that smooth-coated otters can socially learn how to exploit novel food sources and may adopt a 'copy when young' strategy. We found no evidence for social learning in the Asian short-clawed otters. Otters are thus a promising model system for comparative research into social learning strategies, while conservation reintroduction programmes may benefit from facilitating the social transmission of survival skills in these vulnerable species.

Social networks predict selective observation and information spread in ravens.

Animals are predicted to selectively observe and learn from the conspecifics with whom they share social connections. Yet, hardly anything is known about the role of different connections in observation and learning. To address the relationships between social connections, observation and learning, we investigated transmission of information in two raven (Corvus corax) groups. First, we quantified social connections in each group by constructing networks on affiliative interactions, aggressive interactions and proximity. We then seeded novel information by training one group member on a novel task and allowing others to observe. In each group, an observation network based on who observed whose task-solving behaviour was strongly correlated with networks based on affiliative interactions and proximity. Ravens with high social centrality (strength, eigenvector, information centrality) in the affiliative interaction network were also central in the observation network, possibly as a result of solving the task sooner. Network-based diffusion analysis revealed that the order that ravens first solved the task was best predicted by connections in the affiliative interaction network in a group of subadult ravens, and by social rank and kinship (which influenced affiliative interactions) in a group of juvenile ravens. Our results demonstrate that not all social connections are equally effective at predicting the patterns of selective observation and information transmission.

Bayesian Model Selection with Network Based Diffusion Analysis.

A number of recent studies have used Network Based Diffusion Analysis (NBDA) to detect the role of social transmission in the spread of a novel behavior through a population. In this paper we present a unified framework for performing NBDA in a Bayesian setting, and demonstrate how the Watanabe Akaike Information Criteria (WAIC) can be used for model selection. We present a specific example of applying this method to Time to Acquisition Diffusion Analysis (TADA). To examine the robustness of this technique, we performed a large scale simulation study and found that NBDA using WAIC could recover the correct model of social transmission under a wide range of cases, including under the presence of random effects, individual level variables, and alternative models of social transmission. This work suggests that NBDA is an effective and widely applicable tool for uncovering whether social transmission underpins the spread of a novel behavior, and may still provide accurate results even when key model assumptions are relaxed.

How New Caledonian crows solve novel foraging problems and what it means for cumulative culture.

New Caledonian crows make and use tools, and tool types vary over geographic landscapes. Social learning may explain the variation in tool design, but it is unknown to what degree social learning accounts for the maintenance of these designs. Indeed, little is known about the mechanisms these crows use to obtain information from others, despite the question's importance in understanding whether tool behavior is transmitted via social, genetic, or environmental means. For social transmission to account for tool-type variation, copying must utilize a mechanism that is action specific (e.g., pushing left vs. right) as well as context specific (e.g., pushing a particular object vs. any object). To determine whether crows can copy a demonstrator's actions as well as the contexts in which they occur, we conducted a diffusion experiment using a novel foraging task. We used a nontool task to eliminate any confounds introduced by individual differences in their prior tool experience. Two groups had demonstrators (trained in isolation on different options of a four-option task, including a two-action option) and one group did not. We found that crows socially learn about context: After observers see a demonstrator interact with the task, they are more likely to interact with the same parts of the task. In contrast, observers did not copy the demonstrator's specific actions. Our results suggest it is unlikely that observing tool-making behavior transmits tool types. We suggest it is possible that tool types are transmitted when crows copy the physical form of the tools they encounter.