Responsive robotic prey reveal how predators adapt to predictability in escape tactics.

To increase their chances of survival, prey often behave unpredictably when escaping from predators. However, the response of predators to, and hence the effectiveness of, such tactics is unknown. We programmed interactive prey to flee from an approaching fish predator (the blue acara, Andinoacara pulcher) using real-time computer vision and two-wheeled robots that controlled the prey's movements via magnets. This allowed us to manipulate the prey's initial escape direction and how predictable it was between successive trials with the same individual predator. When repeatedly exposed to predictable prey, the predators adjusted their behavior before the prey even began to escape: prey programmed to escape directly away were approached more rapidly than prey escaping at an acute angle. These faster approach speeds compensated for a longer time needed to capture such prey during the subsequent pursuit phase. By contrast, when attacking unpredictable prey, the predators adopted intermediate approach speeds and were not sensitive to the prey's escape angle but instead showed greater acceleration during the pursuit. Collectively, these behavioral responses resulted in the prey's predictability having no net effect on the time taken to capture prey, suggesting that unpredictable escape behavior may be advantageous to prey in fewer circumstances than originally thought. Rather than minimizing capture times, the predators in our study appear to instead adjust their behavior to maintain an adequate level of performance during prey capture.

Personality variation is eroded by simple social behaviours in collective foragers.

The movement of groups can be heavily influenced by 'leader' individuals who differ from the others in some way. A major source of differences between individuals is the repeatability and consistency of their behaviour, commonly considered as their 'personality', which can influence both position within a group as well as the tendency to lead. However, links between personality and behaviour may also depend upon the immediate social environment of the individual; individuals who behave consistently in one way when alone may not express the same behaviour socially, when they may be conforming with the behaviour of others. Experimental evidence shows that personality differences can be eroded in social situations, but there is currently a lack of theory to identify the conditions where we would expect personality to be suppressed. Here, we develop a simple individual-based framework considering a small group of individuals with differing tendencies to perform risky behaviours when travelling away from a safe home site towards a foraging site, and compare the group behaviours when the individuals follow differing rules for aggregation behaviour determining how much attention they pay to the actions of their fellow group-members. We find that if individuals pay attention to the other members of the group, the group will tend to remain at the safe site for longer, but then travel faster towards the foraging site. This demonstrates that simple social behaviours can result in the repression of consistent inter-individual differences in behaviour, giving the first theoretical consideration of the social mechanisms behind personality suppression.

Temperature and turbidity interact synergistically to alter anti-predator behaviour in the Trinidadian guppy.

Due to climate change, freshwater habitats are facing increasing temperatures and more extreme weather that disrupts water flow. Together with eutrophication and sedimentation from farming, quarrying and urbanization, freshwaters are becoming more turbid as well as warmer. Predators and prey need to be able to respond to one another adaptively, yet how changes in temperature and turbidity interact to affect predator-prey behaviour remains unexplored. Using a fully factorial design, we tested the combined effects of increased temperature and turbidity on the behaviour of guppy shoals (Poecilia reticulata) in the presence of one of their natural cichlid predators, the blue acara (Andinoacara pulcher). Our results demonstrate that the prey and predator were in closest proximity in warmer, turbid water, with an interaction between these stressors showing a greater than additive effect. There was also an interaction between the stressors in the inter-individual distances between the prey, where shoal cohesion increased with temperature in clear water, but decreased when temperature increased in turbid water. The closer proximity to predators and reduction in shoaling in turbid, warmer water may increase the risk of predation for the guppy, suggesting that the combined effects of elevated temperature and turbidity may favour predators rather than prey.

Predators attacking virtual prey reveal the costs and benefits of leadership.

A long-standing assumption in social behavior is that leadership incurs costs as well as benefits, and this tradeoff can result in diversified social roles in groups. The major cost of leadership in moving animal groups is assumed to be predation, with individuals leading from the front of groups being targeted more often by predators. Nevertheless, empirical evidence for this is limited, and experimental tests are entirely lacking. To avoid confounding effects associated with observational studies, we presented a simulation of virtual prey to real fish predators to directly assess the predation cost of leadership. Prey leading others are at greater risk than those in the middle of groups, confirming that any benefits of leading may be offset by predation costs. Importantly, however, followers confer a net safety benefit to leaders, as prey leading others were less likely to be attacked compared with solitary prey. We also find that the predators preferentially attacked when solitary individuals were more frequent, but this effect was relatively weak compared with the preference for attacking solitary prey during an attack. Using virtual prey, where the appearance and behavior of the prey can be manipulated and controlled exactly, we reveal a hierarchy of risk from solitary to leading to following social strategies. Our results suggest that goal-orientated individuals (i.e., potential leaders) are under selective pressure to maintain group cohesion, favoring effective leadership rather than group fragmentation. Our results have significant implications for understanding the evolution and maintenance of different social roles in groups.

Fish Avoid Visually Noisy Environments Where Prey Targeting Is Reduced.

AbstractThe environment contains different forms of ecological noise that can reduce the ability of animals to detect information. Here, we ask whether animals adapt their behavior to either exploit or avoid areas of their environment with increased dynamic visual noise. Three-spined sticklebacks (Gasterosteus aculeatus) were immersed in environments with a simulated form of naturally occurring visual noise-moving light bands that form on underwater substrates caused by the refraction of light through surface waves. We tested whether this form of visual noise affected fish's habitat selection, movements, and prey-targeting behavior. Fish avoided areas of the environment with increased visual noise and achieved this by increasing their activity as a function of the locally perceived noise level. Fish were less likely to respond to virtual prey in environments with increased visual noise, highlighting a potential impact that visual noise has on their perceptual abilities. Fish did not increase or decrease their refuge use in environments with increased visual noise, providing no evidence that visual noise increased either exploratory or risk-aversive behavior. Our results indicate that animals can use simple behavioral strategies to avoid visually noisy environments, thereby mitigating the impacts that these environments appear to have on their perceptual abilities.

The measure of spatial position within groups that best predicts predation risk depends on group movement.

Both empirical and theoretical studies show that an individual's spatial position within a group can impact the risk of being targeted by predators. Spatial positions can be quantified in numerous ways, but there are no direct comparisons of different spatial measures in predicting the risk of being targeted by real predators. Here, we assess these spatial measures in groups of stationary and moving virtual prey being attacked by three-spined sticklebacks (Gasterosteus aculeatus). In stationary groups, the limited domain of danger best predicted the likelihood of attack. In moving groups, the number of near neighbours was the best predictor but only over a limited range of distances within which other prey were counted. Otherwise, measures of proximity to the group's edge outperformed measures of local crowding in moving groups. There was no evidence that predators preferentially attacked the front or back of the moving groups. Domains of danger without any limit, as originally used in the selfish herd model, were also a poor predictor of risk. These findings reveal that the collective properties of prey can influence how spatial position affects predation risk, via effects on predators' targeting. Selection may therefore act differently on prey positioning behaviour depending on group movement.

Response to resources and parasites depends on health status in extensively grazed sheep.

A fundamental question in animal ecology is how an individual's internal state and the external environment together shape species distributions across habitats. The increasing availability of biologgers is driving a revolution in answering this question in a wide range of species. In this study, the position of sheep (Ovis aries) from Global Positioning System collars was integrated with remote sensing data, field sampling of parasite distributions, and parasite load and health measures for each tagged individual. This allowed inter-individual variation in habitat use to be examined. Once controlling for a positive relationship between vegetation productivity and tick abundance, healthier individuals spent more of their time at sites with higher vegetation productivity, while less healthy individuals showed a stronger (negative) response to tick abundance. These trends are likely to represent a trade-off in foraging decisions that vary between individuals based on their health status. Given the rarity of studies that explore how animal distributions are affected by health and external factors, we demonstrate the value of integrating biologging technology with remote sensing data, traditional ecological sampling and individual measures of animal health. Our study, using extensively grazed sheep as a model system, opens new possibilities to study free-living grazing systems.

Regulation between personality traits: individual social tendencies modulate whether boldness and leadership are correlated.

Although consistent behavioural differences between individuals (i.e. personality variation) are now well established in animals, these differences are not always expressed when individuals interact in social groups. This can be key in important social dynamics such as leadership, which is often positively related to personality traits such as boldness. Individuals consistently differ in how social they are (their sociability), so if other axes of personality variation, such as boldness, can be suppressed during social interactions, this suppression should be stronger in more sociable individuals. We measured boldness (latency to leave a refuge when alone) and sociability (time spent with a conspecific) in three-spined sticklebacks (Gasterosteus aculeatus) and tested the boldness-leadership association in pairs of these fish. Both boldness and sociability were repeatable, but were not correlated. When splitting the data between the 50% most sociable and 50% less sociable fish, boldness was more strongly associated with leadership in less rather than more sociable individuals. This is consistent with more sociable fish conforming to their partner's behaviour due to their greater social tendency. One axis of personality variation (sociability) can thus modulate the relationship between others (boldness and leadership), with potential implications for selection on personality variation in social animals.

Anthropogenic noise pollution from pile-driving disrupts the structure and dynamics of fish shoals.

Noise produced from a variety of human activities can affect the physiology and behaviour of individual animals, but whether noise disrupts the social behaviour of animals is largely unknown. Animal groups such as flocks of birds or shoals of fish use simple interaction rules to coordinate their movements with near neighbours. In turn, this coordination allows individuals to gain the benefits of group living such as reduced predation risk and social information exchange. Noise could change how individuals interact in groups if noise is perceived as a threat, or if it masked, distracted or stressed individuals, and this could have impacts on the benefits of grouping. Here, we recorded trajectories of individual juvenile seabass (Dicentrarchus labrax) in groups under controlled laboratory conditions. Groups were exposed to playbacks of either ambient background sound recorded in their natural habitat, or playbacks of pile-driving, commonly used in marine construction. The pile-driving playback affected the structure and dynamics of the fish shoals significantly more than the ambient-sound playback. Compared to the ambient-sound playback, groups experiencing the pile-driving playback became less cohesive, less directionally ordered, and were less correlated in speed and directional changes. In effect, the additional-noise treatment disrupted the abilities of individuals to coordinate their movements with one another. Our work highlights the potential for noise pollution from pile-driving to disrupt the collective dynamics of fish shoals, which could have implications for the functional benefits of a group's collective behaviour.

How predation shapes the social interaction rules of shoaling fish.

Predation is thought to shape the macroscopic properties of animal groups, making moving groups more cohesive and coordinated. Precisely how predation has shaped individuals' fine-scale social interactions in natural populations, however, is unknown. Using high-resolution tracking data of shoaling fish (Poecilia reticulata) from populations differing in natural predation pressure, we show how predation adapts individuals' social interaction rules. Fish originating from high predation environments formed larger, more cohesive, but not more polarized groups than fish from low predation environments. Using a new approach to detect the discrete points in time when individuals decide to update their movements based on the available social cues, we determine how these collective properties emerge from individuals' microscopic social interactions. We first confirm predictions that predation shapes the attraction-repulsion dynamic of these fish, reducing the critical distance at which neighbours move apart, or come back together. While we find strong evidence that fish align with their near neighbours, we do not find that predation shapes the strength or likelihood of these alignment tendencies. We also find that predation sharpens individuals' acceleration and deceleration responses, implying key perceptual and energetic differences associated with how individuals move in different predation regimes. Our results reveal how predation can shape the social interactions of individuals in groups, ultimately driving differences in groups' collective behaviour.

The anti-predator role of within-nest emergence synchrony in sea turtle hatchlings.

Group formation is a common behaviour among prey species. In egg-laying animals, despite the various factors that promote intra-clutch variation leading to asynchronous hatching and emergence from nests, synchronous hatching and emergence occurs in many taxa. This synchrony may be adaptive by reducing predation risk, but few data are available in any natural system, even for iconic examples of the anti-predator function of group formation. Here, we show for the first time that increased group size (number of hatchlings emerging together from a nest) reduces green turtle (Chelonia mydas) hatchling predation. This effect was only observed earlier in the night when predation pressure was greatest, indicated by the greatest predator abundance and a small proportion of predators preoccupied with consuming captured prey. Further analysis revealed that the effect of time of day was due to the number of hatchlings already killed in an evening; this, along with the apparent lack of other anti-predatory mechanisms for grouping, suggests that synchronous emergence from a nest appears to swamp predators, resulting in an attack abatement effect. Using a system with relatively pristine conditions for turtle hatchlings and their predators provides a more realistic environmental context within which intra-nest synchronous emergence has evolved.

Potential Leaders Trade Off Goal-Oriented and Socially Oriented Behavior in Mobile Animal Groups.

Leadership is widespread across the animal kingdom. In self-organizing groups, such as fish schools, theoretical models predict that effective leaders need to balance goal-oriented motion, such as toward a known resource, with their tendency to be social. Increasing goal orientation is predicted to increase decision speed and accuracy, but it is also predicted to increase the risk of the group splitting. To test these key predictions, we trained fish (golden shiners, Notemigonus crysoleucas) to associate a spatial target with a food reward ("informed" individuals) before testing each singly with a group of eight untrained fish who were uninformed ("naive") about the target. Informed fish that exhibited faster and straighter paths (indicative of greater goal orientation) were more likely to reach their preferred target and did so more quickly. However, such behavior was associated with a tendency to leave untrained fish behind and, therefore, with failure to transmit their preference to others. Either all or none of the untrained fish stayed with the trained fish in the majority of trials. Using a simple model of self-organized coordination and leadership in groups, we recreate these features of leadership observed experimentally, including the apparent consensus behavior among naive individuals. Effective leadership thus requires informed individuals to appropriately balance goal-oriented and socially oriented behavior.

How to catch more prey with less effective traps: explaining the evolution of temporarily inactive traps in carnivorous pitcher plants.

Carnivorous Nepenthes pitcher plants capture arthropods with specialized slippery surfaces. The key trapping surface, the pitcher rim (peristome), is highly slippery when wetted by rain, nectar or condensation, but not when dry. As natural selection should favour adaptations that maximize prey intake, the evolution of temporarily inactive traps seems paradoxical. Here, we show that intermittent trap deactivation promotes 'batch captures' of ants. Prey surveys revealed that N. rafflesiana pitchers sporadically capture large numbers of ants from the same species. Continuous experimental wetting of the peristome increased the number of non-recruiting prey, but decreased the number of captured ants and shifted their trapping mode from batch to individual capture events. Ant recruitment was also lower to continuously wetted pitchers. Our experimental data fit a simple model that predicts that intermittent, wetness-based trap activation should allow safe access for 'scout' ants under dry conditions, thereby promoting recruitment and ultimately higher prey numbers. The peristome trapping mechanism may therefore represent an adaptation for capturing ants. The relatively rare batch capture events may particularly benefit larger plants with many pitchers. This explains why young plants of many Nepenthes species additionally employ wetness-independent, waxy trapping surfaces.

Collective states, multistability and transitional behavior in schooling fish.

The spontaneous emergence of pattern formation is ubiquitous in nature, often arising as a collective phenomenon from interactions among a large number of individual constituents or sub-systems. Understanding, and controlling, collective behavior is dependent on determining the low-level dynamical principles from which spatial and temporal patterns emerge; a key question is whether different group-level patterns result from all components of a system responding to the same external factor, individual components changing behavior but in a distributed self-organized way, or whether multiple collective states co-exist for the same individual behaviors. Using schooling fish (golden shiners, in groups of 30 to 300 fish) as a model system, we demonstrate that collective motion can be effectively mapped onto a set of order parameters describing the macroscopic group structure, revealing the existence of at least three dynamically-stable collective states; swarm, milling and polarized groups. Swarms are characterized by slow individual motion and a relatively dense, disordered structure. Increasing swim speed is associated with a transition to one of two locally-ordered states, milling or highly-mobile polarized groups. The stability of the discrete collective behaviors exhibited by a group depends on the number of group members. Transitions between states are influenced by both external (boundary-driven) and internal (changing motion of group members) factors. Whereas transitions between locally-disordered and locally-ordered group states are speed dependent, analysis of local and global properties of groups suggests that, congruent with theory, milling and polarized states co-exist in a bistable regime with transitions largely driven by perturbations. Our study allows us to relate theoretical and empirical understanding of animal group behavior and emphasizes dynamic changes in the structure of such groups.

Inferring the structure and dynamics of interactions in schooling fish.

Determining individual-level interactions that govern highly coordinated motion in animal groups or cellular aggregates has been a long-standing challenge, central to understanding the mechanisms and evolution of collective behavior. Numerous models have been proposed, many of which display realistic-looking dynamics, but nonetheless rely on untested assumptions about how individuals integrate information to guide movement. Here we infer behavioral rules directly from experimental data. We begin by analyzing trajectories of golden shiners (Notemigonus crysoleucas) swimming in two-fish and three-fish shoals to map the mean effective forces as a function of fish positions and velocities. Speeding and turning responses are dynamically modulated and clearly delineated. Speed regulation is a dominant component of how fish interact, and changes in speed are transmitted to those both behind and ahead. Alignment emerges from attraction and repulsion, and fish tend to copy directional changes made by those ahead. We find no evidence for explicit matching of body orientation. By comparing data from two-fish and three-fish shoals, we challenge the standard assumption, ubiquitous in physics-inspired models of collective behavior, that individual motion results from averaging responses to each neighbor considered separately; three-body interactions make a substantial contribution to fish dynamics. However, pairwise interactions qualitatively capture the correct spatial interaction structure in small groups, and this structure persists in larger groups of 10 and 30 fish. The interactions revealed here may help account for the rapid changes in speed and direction that enable real animal groups to stay cohesive and amplify important social information.

Multiple environmental stressors affect predation pressure in a tropical freshwater system.

Environmental change can alter predator-prey dynamics. However, studying predators in the context of co-occurring environmental stressors remains rare, especially under field conditions. Using in situ filming, we examined how multiple stressors, including temperature and turbidity, impact the distribution and behaviour of wild fish predators of Trinidadian guppies (Poecilia reticulata). The measured environmental variables accounted for 17.6% of variance in predator species composition. While predator species differed in their associations with environmental variables, the overall prevalence of predators was greatest in slow flowing, deeper, warmer and less turbid habitats. Moreover, these warmer and less turbid habitats were associated with earlier visits to the prey stimulus by predators, and more frequent predator visits and attacks. Our findings highlight the need to consider ecological complexity, such as co-occurring stressors, to better understand how environmental change affects predator-prey interactions.

A multi-scale review of the dynamics of collective behaviour: from rapid responses to ontogeny and evolution.

Collective behaviours, such as flocking in birds or decision making by bee colonies, are some of the most intriguing behavioural phenomena in the animal kingdom. The study of collective behaviour focuses on the interactions between individuals within groups, which typically occur over close ranges and short timescales, and how these interactions drive larger scale properties such as group size, information transfer within groups and group-level decision making. To date, however, most studies have focused on snapshots, typically studying collective behaviour over short timescales up to minutes or hours. However, being a biological trait, much longer timescales are important in animal collective behaviour, particularly how individuals change over their lifetime (the domain of developmental biology) and how individuals change from one generation to the next (the domain of evolutionary biology). Here, we give an overview of collective behaviour across timescales from the short to the long, illustrating how a full understanding of this behaviour in animals requires much more research attention on its developmental and evolutionary biology. Our review forms the prologue of this special issue, which addresses and pushes forward understanding the development and evolution of collective behaviour, encouraging a new direction for collective behaviour research. This article is part of a discussion meeting issue 'Collective behaviour through time'.

Conformity and differentiation are two sides of the same coin.

Variation between individuals is a key component of selection and hence evolutionary change. Social interactions are important drivers of variation, potentially making behaviour more similar (i.e., conform) or divergent (i.e., differentiate) between individuals. While documented across a wide range of animals, behaviours and contexts, conformity and differentiation are typically considered separately. Here, we argue that rather than independent concepts, they can be integrated onto a single scale that considers how social interactions drive changes in interindividual variance within groups: conformity reduces variance within groups while differentiation increases it. We discuss the advantages of placing conformity and differentiation at different ends of a single scale, allowing for a deeper understanding of the relationship between social interactions and interindividual variation.

Shoaling behaviour in response to turbidity in three-spined sticklebacks.

Many fresh and coastal waters are becoming increasingly turbid because of human activities, which may disrupt the visually mediated behaviours of aquatic organisms. Shoaling fish typically depend on vision to maintain collective behaviour, which has a range of benefits including protection from predators, enhanced foraging efficiency and access to mates. Previous studies of the effects of turbidity on shoaling behaviour have focussed on changes to nearest neighbour distance and average group-level behaviours. Here, we investigated whether and how experimental shoals of three-spined sticklebacks (Gasterosteus aculeatus) in clear (<10 Nephelometric Turbidity Units [NTU]) and turbid (~35 NTU) conditions differed in five local-level behaviours of individuals (nearest and furthest neighbour distance, heading difference with nearest neighbour, bearing angle to nearest neighbour and swimming speed). These variables are important for the emergent group-level properties of shoaling behaviour. We found an indirect effect of turbidity on nearest neighbour distances driven by a reduction in swimming speed, and a direct effect of turbidity which increased variability in furthest neighbour distances. In contrast, the alignment and relative position of individuals was not significantly altered in turbid compared to clear conditions. Overall, our results suggest that the shoals were usually robust to adverse effects of turbidity on collective behaviour, but group cohesion was occasionally lost during periods of instability.

Virtual prey with Lévy motion are preferentially attacked by predatory fish.

Of widespread interest in animal behavior and ecology is how animals search their environment for resources, and whether these search strategies are optimal. However, movement also affects predation risk through effects on encounter rates, the conspicuousness of prey, and the success of attacks. Here, we use predatory fish attacking a simulation of virtual prey to test whether predation risk is associated with movement behavior. Despite often being demonstrated to be a more efficient strategy for finding resources such as food, we find that prey displaying Lévy motion are twice as likely to be targeted by predators than prey utilizing Brownian motion. This can be explained by the predators, at the moment of the attack, preferentially targeting prey that were moving with straighter trajectories rather than prey that were turning more. Our results emphasize that costs of predation risk need to be considered alongside the foraging benefits when comparing different movement strategies.