Andrew Berdahl

Emergent Sensing of Complex Environments by Mobile Animal Groups

The Power of the Collective Sensing the environment is generally considered to require significant cognitive sampling and comparison, not to mention time. However, species that do not necessarily have the cognitive ability, or the time, have also proven to be quite adept at sensing and evaluating their environment. Berdahl et al. (p. 574) show that in shiners, a species of schooling fish, mere attraction to, and movement toward, neighboring individuals allows the group to track preferred darkness in a variable-light environment. Living in a group amplifies the reach of an individuals capacity to sense environmental changes. The capacity for groups to exhibit collective intelligence is an often-cited advantage of group living. Previous studies have shown that social organisms frequently benefit from pooling imperfect individual estimates. However, in principle, collective intelligence may also emerge from interactions between individuals, rather than from the enhancement of personal estimates. Here, we reveal that this emergent problem solving is the predominant mechanism by which a mobile animal group responds to complex environmental gradients. Robust collective sensing arises at the group level from individuals modulating their speed in response to local, scalar, measurements of light and through social interaction with others. This distributed sensing requires only rudimentary cognition and thus could be widespread across biological taxa, in addition to being appropriate and cost-effective for robotic agents.

Signalling and the Evolution of Cooperative Foraging in Dynamic Environments

Understanding cooperation in animal social groups remains a significant challenge for evolutionary theory. Observed behaviours that benefit others but incur some cost appear incompatible with classical notions of natural selection; however, these behaviours may be explained by concepts such as inclusive fitness, reciprocity, intra-specific mutualism or manipulation. In this work, we examine a seemingly altruistic behaviour, the active recruitment of conspecifics to a food resource through signalling. Here collective, cooperative behaviour may provide highly nonlinear benefits to individuals, since group functionality has the potential to be far greater than the sum of the component parts, for example by enabling the effective tracking of a dynamic resource. We show that due to this effect, signalling to others is an evolutionarily stable strategy under certain environmental conditions, even when there is a cost associated to this behaviour. While exploitation is possible, in the limiting case of a sparse, ephemeral but locally abundant nutrient source, a given environmental profile will support a fixed number of signalling individuals. Through a quantitative analysis, this effective carrying capacity for cooperation is related to the characteristic length and time scales of the resource field.

The evolution of distributed sensing and collective computation in animal populations

Many animal groups exhibit rapid, coordinated collective motion. Yet, the evolutionary forces that cause such collective responses to evolve are poorly understood. Here, we develop analytical methods and evolutionary simulations based on experimental data from schooling fish. We use these methods to investigate how populations evolve within unpredictable, time-varying resource environments. We show that populations evolve toward a distinctive regime in behavioral phenotype space, where small responses of individuals to local environmental cues cause spontaneous changes in the collective state of groups. These changes resemble phase transitions in physical systems. Through these transitions, individuals evolve the emergent capacity to sense and respond to resource gradients (i.e. individuals perceive gradients via social interactions, rather than sensing gradients directly), and to allocate themselves among distinct, distant resource patches. Our results yield new insight into how natural selection, acting on selfish individuals, results in the highly effective collective responses evident in nature. DOI: http://dx.doi.org/10.7554/eLife.10955.001

On the evolutionary interplay between dispersal and local adaptation in heterogeneous environments

Dispersal, whether in the form of a dandelion seed drifting on the breeze, or a salmon migrating upstream to breed in a nonnatal stream, transports genes between locations. At these locations, local adaptation modifies the gene frequencies so their carriers are better suited to particular conditions, be those of newly disturbed soil or a quiet river pool. Both dispersal and local adaptation are major drivers of population structure; however, in general, their respective roles are not independent and the two may often be at odds with one another evolutionarily, each one exhibiting negative feedback on the evolution of the other. Here, we investigate their joint evolution within a simple, discrete‐time, metapopulation model. Depending on environmental conditions, their evolutionary interplay leads to either a monomorphic population of highly dispersing generalists or a collection of rarely dispersing, locally adapted, polymorphic sub‐populations, each adapted to a particular habitat type. A critical value of environmental heterogeneity divides these two selection regimes and the nature of the transition between them is determined by the level of kin competition. When kin competition is low, at the transition we observe discontinuities, bistability, and hysteresis in the evolved strategies; however, when high, kin competition moderates the evolutionary feedback and the transition is smooth.

Collective animal navigation and migratory culture : from theoretical models to empirical evidence

Animals often travel in groups, and their navigational decisions can be influenced by social interactions. Both theory and empirical observations suggest that such collective navigation can result in individuals improving their ability to find their way and could be one of the key benefits of sociality for these species. Here, we provide an overview of the potential mechanisms underlying collective navigation, review the known, and supposed, empirical evidence for such behaviour and highlight interesting directions for future research. We further explore how both social and collective learning during group navigation could lead to the accumulation of knowledge at the population level, resulting in the emergence of migratory culture. This article is part of the theme issue ‘Collective movement ecology’.

Collective behavior as a driver of critical transitions in migratory populations

BackgroundMass migrations are among the most striking examples of animal movement in the natural world. Such migrations are major drivers of ecosystem processes and strongly influence the survival and fecundity of individuals. For migratory animals, a formidable challenge is to find their way over long distances and through complex, dynamic environments. However, recent theoretical and empirical work suggests that by traveling in groups, individuals are able to overcome these challenges and increase their ability to navigate. Here we use models to explore the implications of collective navigation on migratory, and population, dynamics, for both breeding migrations (to-and-fro migrations between distinct, fixed, end-points) and feeding migrations (loop migrations that track favorable conditions).ResultsWe show that while collective navigation does improve a population’s ability to migrate accurately, it can lead to Allee effects, causing the sudden collapse of populations if numbers fall below a critical threshold. In some scenarios, hysteresis prevents the migration from recovering even after the cause of the collapse has been removed. In collectively navigating populations that are locally adapted to specific breeding sites, a slight increase in mortality can cause a collapse of genetic population structure, rather than population size, making it more difficult to detect and prevent.ConclusionsDespite the large interest in collective behavior and its ubiquity in many migratory species, there is a notable lack of studies considering the implications of social navigation on the ecological dynamics of migratory species. Here we highlight the potential for a previously overlooked Allee effect in socially migrating species that may be important for conservation and management of such species.

Inferring the rules of social interaction in migrating caribou

Social interactions are a significant factor that influence the decision-making of species ranging from humans to bacteria. In the context of animal migration, social interactions may lead to improved decision-making, greater ability to respond to environmental cues, and the cultural transmission of optimal routes. Despite their significance, the precise nature of social interactions in migrating species remains largely unknown. Here we deploy unmanned aerial systems to collect aerial footage of caribou as they undertake their migration from Victoria Island to mainland Canada. Through a Bayesian analysis of trajectories we reveal the fine-scale interaction rules of migrating caribou and show they are attracted to one another and copy directional choices of neighbours, but do not interact through clearly defined metric or topological interaction ranges. By explicitly considering the role of social information on movement decisions we construct a map of near neighbour influence that quantifies the nature of information flow in these herds. These results will inform more realistic, mechanism-based models of migration in caribou and other social ungulates, leading to better predictions of spatial use patterns and responses to changing environmental conditions. Moreover, we anticipate that the protocol we developed here will be broadly applicable to study social behaviour in a wide range of migratory and non-migratory taxa. This article is part of the theme issue ‘Collective movement ecology’.

Collective movement in ecology: from emerging technologies to conservation and management

Recent advances in technology and quantitative methods have led to the emergence of a new field of study that stands to link insights of researchers from two closely related, but often disconnected disciplines: movement ecology and collective animal behaviour. To date, the field of movement ecology has focused on elucidating the internal and external drivers of animal movement and the influence of movement on broader ecological processes. Typically, tracking and/or remote sensing technology is employed to study individual animals in natural conditions. By contrast, the field of collective behaviour has quantified the significant role social interactions play in the decision-making of animals within groups and, to date, has predominantly relied on controlled laboratory-based studies and theoretical models owing to the constraints of studying interacting animals in the field. This themed issue is intended to formalize the burgeoning field of collective movement ecology which integrates research from both movement ecology and collective behaviour. In this introductory paper, we set the stage for the issue by briefly examining the approaches and current status of research in these areas. Next, we outline the structure of the theme issue and describe the obstacles collective movement researchers face, from data acquisition in the field to analysis and problems of scale, and highlight the key contributions of the assembled papers. We finish by presenting research that links individual and broad-scale ecological and evolutionary processes to collective movement, and finally relate these concepts to emerging challenges for the management and conservation of animals on the move in a world that is increasingly impacted by human activity. This article is part of the theme issue ‘Collective movement ecology’.

Social interactions shape the timing of spawning migrations in an anadromous fish

Mass migrations are found throughout the animal kingdom and are often undertaken by coordinated social groups. However, surprisingly little is known about how social interactions influence migratory timing. Anadromous fishes such as salmon make extensive breeding migrations between marine and freshwater ecosystems. Returning adult salmon tend to move in discrete temporal pulses, which are typically thought to be triggered by abiotic environmental stimuli (e.g. changes in river flow or temperature). However, most studies reveal only weak correlations between abiotic factors and the timing of spawning runs. Here, we demonstrate that social interactions provide a plausible alternative or additional explanation for such patterns. We first provide an example of the phenomenon using 20 years of data on sockeye salmon, Oncorhynchus nerka , ascending a stream in pulses in the absence of any obvious environmental triggers. Next, we present a model that reproduces the pulses observed in the data, simply by including social interactions among individuals. Deviations between the empirical data and the social model results suggest that salmon may alter their individual behaviour in response to annual fluctuations in density. We hope our results, demonstrating the role that social influence can play on migration timing, will motivate further studies exploring how social interactions may shape the movements of other migratory taxa. Understanding how individuals integrate social information with internal and exogenous drivers of migratory behaviour is vital, particularly in the face of a changing climate, which is changing both the cues used for, and the optimal timing of, migrations.

Fitness trade-offs of group formation and movement by Thomson's gazelles in the Serengeti ecosystem

Collective behaviours contributing to patterns of group formation and coordinated movement are common across many ecosystems and taxa. Their ubiquity is presumably due to altering interactions between individuals and their predators, resources and physical environment in ways that enhance individual fitness. On the other hand, fitness costs are also often associated with group formation. Modifications to these interactions have the potential to dramatically impact population-level processes, such as trophic interactions or patterns of space use in relation to abiotic environmental variation. In a wide variety of empirical systems and models, collective behaviour has been shown to enhance access to ephemeral patches of resources, reduce the risk of predation and reduce vulnerability to environmental fluctuation. Evolution of collective behaviour should accordingly depend on the advantages of collective behaviour weighed against the costs experienced at the individual level. As an illustrative case study, we consider the potential trade-offs on Malthusian fitness associated with patterns of group formation and movement by migratory Thomsons gazelles in the Serengeti ecosystem. This article is part of the theme issue ‘Collective movement ecology’.