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.

Contrasting stripes are a widespread feature of group living in birds, mammals and fishes.

Grouping is a widespread form of predator defence, with individuals in groups often performing evasive collective movements in response to attack by predators. Individuals in these groups use behavioural rules to coordinate their movements, with visual cues about neighbours' positions and orientations often informing movement decisions. Although the exact visual cues individuals use to coordinate their movements with neighbours have not yet been decoded, some studies have suggested that stripes, lines, or other body patterns may act as conspicuous conveyors of movement information that could promote coordinated group movement, or promote dazzle camouflage, thereby confusing predators. We used phylogenetic logistic regressions to test whether the contrasting achromatic stripes present in four different taxa vulnerable to predation, including species within two orders of birds (Anseriformes and Charadriiformes), a suborder of Artiodactyla (the ruminants), and several orders of marine fishes (predominantly Perciformes) were associated with group living. Contrasting patterns were significantly more prevalent in social species, and tended to be absent in solitary species or species less vulnerable to predation. We suggest that stripes taking the form of light-coloured lines on dark backgrounds, or vice versa, provide a widespread mechanism across taxa that either serves to inform conspecifics of neighbours' movements, or to confuse predators, when moving in groups. Because detection and processing of patterns and of motion in the visual channel is essentially colour-blind, diverse animal taxa with widely different vision systems (including mono-, di-, tri-, and tetrachromats) appear to have converged on a similar use of achromatic patterns, as would be expected given signal-detection theory. This hypothesis would explain the convergent evolution of conspicuous achromatic patterns as an antipredator mechanism in numerous vertebrate species.

Fine-scale behavioural adjustments of prey on a continuum of risk.

In the wild, prey species often live in the vicinity of predators, rendering the ability to assess risk on a moment-to-moment basis crucial to survival. Visual cues are important as they allow prey to assess predator species, size, proximity and behaviour. However, few studies have explicitly examined prey's ability to assess risk based on predator behaviour and orientation. Using mosquitofish, Gambusia holbrooki, and their predator, jade perch, Scortum barcoo, under controlled conditions, we provide some of the first fine-scale characterization of how prey adapt their behaviour according to their continuous assessment of risk based on both predator behaviour and angular distance to the predator's mouth. When these predators were inactive and posed less of an immediate threat, prey within the attack cone of the predator showed reductions in speed and acceleration characteristic of predator-inspection behaviour. However, when predators became active, prey swam faster with greater acceleration and were closer together within the attack cone of predators. Most importantly, this study provides evidence that prey do not adopt a uniform response to the presence of a predator. Instead, we demonstrate that prey are capable of rapidly and dynamically updating their assessment of risk and showing fine-scale adjustments to their behaviour.

Paternal personality and social status influence offspring activity in zebrafish.

BACKGROUND: Evidence for the transmission of non-genetic information from father to offspring is rapidly accumulating. While the impact of chemical and physical factors such as toxins or diet on the fitness of the parents and their offspring have been studied extensively, the importance of behavioural and social circumstances has only recently been recognised. Behavioural traits such as personality characteristics can be relatively stable, and partly comprise a genetic component but we know little about the non-genetic transmission of plastic behavioural traits from parents to offspring. We investigated the relative effect of personality and of social dominance as indicators at the opposite ends of the plasticity range on offspring behaviour in the zebrafish (Danio rerio). We assessed male boldness, a behavioural trait that has previously been shown previously to possess genetic underpinnings, and experimentally manipulated male social status to assess the association between the two types of behaviour and their correlation with offspring activity. RESULTS: We found a clear interaction between the relatively stable and putative genetic effects based on inherited differences in personality and the experimentally induced epigenetic effects from changes in the social status of the father on offspring activity. CONCLUSIONS: Our study shows that offspring behaviour is determined by a combination of paternal personality traits and on-genetic effects derived from the social status of the father.

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.

Proto-cooperation: group hunting sailfish improve hunting success by alternating attacks on grouping prey.

We present evidence of a novel form of group hunting. Individual sailfish (Istiophorus platypterus) alternate attacks with other group members on their schooling prey (Sardinella aurita). While only 24% of attacks result in prey capture, multiple prey are injured in 95% of attacks, resulting in an increase of injured fish in the school with the number of attacks. How quickly prey are captured is positively correlated with the level of injury of the school, suggesting that hunters can benefit from other conspecifics' attacks on the prey. To explore this, we built a mathematical model capturing the dynamics of the hunt. We show that group hunting provides major efficiency gains (prey caught per unit time) for individuals in groups of up to 70 members. We also demonstrate that a free riding strategy, where some individuals wait until the prey are sufficiently injured before attacking, is only beneficial if the cost of attacking is high, and only then when waiting times are short. Our findings provide evidence that cooperative benefits can be realized through the facilitative effects of individuals' hunting actions without spatial coordination of attacks. Such 'proto-cooperation' may be the pre-cursor to more complex group-hunting strategies.

Multi-scale inference of interaction rules in animal groups using Bayesian model selection.

Inference of interaction rules of animals moving in groups usually relies on an analysis of large scale system behaviour. Models are tuned through repeated simulation until they match the observed behaviour. More recent work has used the fine scale motions of animals to validate and fit the rules of interaction of animals in groups. Here, we use a Bayesian methodology to compare a variety of models to the collective motion of glass prawns (Paratya australiensis). We show that these exhibit a stereotypical 'phase transition', whereby an increase in density leads to the onset of collective motion in one direction. We fit models to this data, which range from: a mean-field model where all prawns interact globally; to a spatial Markovian model where prawns are self-propelled particles influenced only by the current positions and directions of their neighbours; up to non-Markovian models where prawns have 'memory' of previous interactions, integrating their experiences over time when deciding to change behaviour. We show that the mean-field model fits the large scale behaviour of the system, but does not capture the observed locality of interactions. Traditional self-propelled particle models fail to capture the fine scale dynamics of the system. The most sophisticated model, the non-Markovian model, provides a good match to the data at both the fine scale and in terms of reproducing global dynamics, while maintaining a biologically plausible perceptual range. We conclude that prawns' movements are influenced by not just the current direction of nearby conspecifics, but also those encountered in the recent past. Given the simplicity of prawns as a study system our research suggests that self-propelled particle models of collective motion should, if they are to be realistic at multiple biological scales, include memory of previous interactions and other non-Markovian effects.

Fast and accurate decisions through collective vigilance in fish shoals.

Although it has been suggested that large animal groups should make better decisions than smaller groups, there are few empirical demonstrations of this phenomenon and still fewer explanations of the how these improvements may be made. Here we show that both speed and accuracy of decision making increase with group size in fish shoals under predation threat. We examined two plausible mechanisms for this improvement: first, that groups are guided by a small proportion of high-quality decision makers and, second, that group members use self-organized division of vigilance. Repeated testing of individuals showed no evidence of different decision-making abilities between individual fish. Instead, we suggest that shoals achieve greater decision-making efficiencies through division of labor combined with social information transfer. Our results should prompt reconsideration of how we view cooperation in animal groups with fluid membership.

Inferring the rules of interaction of shoaling fish.

Collective motion, where large numbers of individuals move synchronously together, is achieved when individuals adopt interaction rules that determine how they respond to their neighbors' movements and positions. These rules determine how group-living animals move, make decisions, and transmit information between individuals. Nonetheless, few studies have explicitly determined these interaction rules in moving groups, and very little is known about the interaction rules of fish. Here, we identify three key rules for the social interactions of mosquitofish (Gambusia holbrooki): (i) Attraction forces are important in maintaining group cohesion, while we find only weak evidence that fish align with their neighbor's orientation; (ii) repulsion is mediated principally by changes in speed; (iii) although the positions and directions of all shoal members are highly correlated, individuals only respond to their single nearest neighbor. The last two of these rules are different from the classical models of collective animal motion, raising new questions about how fish and other animals self-organize on the move.

Cuttlefish adopt disruptive camouflage under dynamic lighting.

Many animals avoid detection or recognition using camouflage tailored to the visual features of their environment.1,2,3 The appearance of those features, however, can be affected by fluctuations in local lighting conditions, making them appear different over time.4,5 Despite dynamic lighting being common in many terrestrial and aquatic environments, it is unknown whether dynamic lighting influences the camouflage patterns that animals adopt. Here, we test whether a common form of underwater dynamic lighting, consisting of moving light bands that can create local fluctuations in the intensity of light ("water caustics"), affects the camouflage of cuttlefish (Sepia officinalis). Owing to specialized pigment cells (chromatophores) in the skin,6 these cephalopod mollusks can dynamically adjust their body patterns in response to features of their visual scene.7,8,9 Although cuttlefish resting on plain or patterned backgrounds usually expressed uniform or disruptive body patterns, respectively,10,11,12 exposure to these backgrounds in dynamic lighting induced stronger disruptive patterns regardless of the background type. Dynamic lighting increased the maximum contrast levels within scenes, and these maximum contrast levels were associated with the degree of cuttlefish disruptive camouflage. This adoption of disruptive camouflage in dynamically lit scenes may be adaptive, reducing the likelihood of detection, or alternatively, it could represent a constraint on visual processing.

A horizon scan of global biological conservation issues for 2024.

We present the results of our 15th horizon scan of novel issues that could influence biological conservation in the future. From an initial list of 96 issues, our international panel of scientists and practitioners identified 15 that we consider important for societies worldwide to track and potentially respond to. Issues are novel within conservation or represent a substantial positive or negative step-change with global or regional extents. For example, new sources of hydrogen fuel and changes in deep-sea currents may have profound impacts on marine and terrestrial ecosystems. Technological advances that may be positive include benchtop DNA printers and the industrialisation of approaches that can create high-protein food from air, potentially reducing the pressure on land for food production.

Initiators, leaders, and recruitment mechanisms in the collective movements of damselfish.

Explaining how individual behavior and social interactions give rise to group-level outcomes and affect issues such as leadership is fundamental to the understanding of collective behavior. Here we examined individual and collective behavioral dynamics in groups of humbug damselfish both before and during a collective movement. During the predeparture phase, group activity increased until the collective movement occurred. Although such movements were precipitated by one individual, the success or failure of any attempt to instigate a collective movement was not solely dependent on this initiator's behavior but on the behavior of the group as a whole. Specifically, groups were more active and less cohesive before a successful initiation attempt than before a failed attempt. Individuals who made the most attempts to initiate a collective movement during each trial were ultimately most likely to lead the collective movement. Leadership was not related to dominance but was consistent between trials. The probability of fish recruiting to a group movement initiative was an approximately linear function of the number of fish already recruited. Overall, these results are consistent with nonselective local mimetism, with the decision to leave based on a group's, rather than any particular individual's, readiness to leave.

Multi-scale inference of interaction rules in animal groups using Bayesian model selection.

Inference of interaction rules of animals moving in groups usually relies on an analysis of large scale system behaviour. Models are tuned through repeated simulation until they match the observed behaviour. More recent work has used the fine scale motions of animals to validate and fit the rules of interaction of animals in groups. Here, we use a Bayesian methodology to compare a variety of models to the collective motion of glass prawns (Paratya australiensis). We show that these exhibit a stereotypical 'phase transition', whereby an increase in density leads to the onset of collective motion in one direction. We fit models to this data, which range from: a mean-field model where all prawns interact globally; to a spatial Markovian model where prawns are self-propelled particles influenced only by the current positions and directions of their neighbours; up to non-Markovian models where prawns have 'memory' of previous interactions, integrating their experiences over time when deciding to change behaviour. We show that the mean-field model fits the large scale behaviour of the system, but does not capture fine scale rules of interaction, which are primarily mediated by physical contact. Conversely, the Markovian self-propelled particle model captures the fine scale rules of interaction but fails to reproduce global dynamics. The most sophisticated model, the non-Markovian model, provides a good match to the data at both the fine scale and in terms of reproducing global dynamics. We conclude that prawns' movements are influenced by not just the current direction of nearby conspecifics, but also those encountered in the recent past. Given the simplicity of prawns as a study system our research suggests that self-propelled particle models of collective motion should, if they are to be realistic at multiple biological scales, include memory of previous interactions and other non-Markovian effects.

The presence of territorial damselfish predicts choosy client species richness at cleaning stations.

Mutualisms are driven by partners deciding to interact with one another to gain specific services or rewards. As predicted by biological market theory, partners should be selected based on the likelihood, quality, reward level, and or services each partner can offer. Third-party species that are not directly involved in the interaction, however, may indirectly affect the occurrence and or quality of the services provided, thereby affecting which partners are selected or avoided. We investigated how different clients of the sharknose goby (Elacatinus evelynae) cleaner fish were distributed across cleaning stations, and asked what characteristics, relating to biological market theory, affected this distribution. Through quantifying the visitation and cleaning patterns of client fish that can choose which cleaning station(s) to visit, we found that the relative species richness of visiting clients at stations was negatively associated with the presence of disruptive territorial damselfish at the station. Our study highlights, therefore, the need to consider the indirect effects of third-party species and their interactions (e.g., agonistic interactions) when attempting to understand mutualistic interactions between species. Moreover, we highlight how cooperative interactions may be indirectly governed by external partners.

Predatory trumpetfish conceal themselves from their prey by swimming alongside other fish.

Many animals use camouflage to avoid detection by others, yet even the most inconspicuous objects become detectable against the background when moving1,2. One way to reduce detection while moving would be to 'hide' behind the movements of objects or other animals3. Here, we demonstrate experimentally that a common marine predator, the trumpetfish (Aulostomus maculatus), can conceal its approach from its prey by performing a behaviour known as 'shadowing' - swimming closely next to another, larger and non-predatory fish3,4,5. Our findings reveal how predators can actively use another animal as a form of concealment to reduce detection by prey.

A global biological conservation horizon scan of issues for 2023.

We present the results of our 14th horizon scan of issues we expect to influence biological conservation in the future. From an initial set of 102 topics, our global panel of 30 scientists and practitioners identified 15 issues we consider most urgent for societies worldwide to address. Issues are novel within biological conservation or represent a substantial positive or negative step change at global or regional scales. Issues such as submerged artificial light fisheries and accelerating upper ocean currents could have profound negative impacts on marine or coastal ecosystems. We also identified potentially positive technological advances, including energy production and storage, improved fertilisation methods, and expansion of biodegradable materials. If effectively managed, these technologies could realise future benefits for biological diversity.

Vocally mediated consensus decisions govern mass departures from jackdaw roosts.

In the early morning, large groups of up to hundreds or even thousands of roosting birds, sometimes comprising the entire roost population, often take off together in sudden mass departures. These departures commonly occur in low-light conditions and structurally complex habitats where access to visual cues is likely to be restricted. Roosting birds are often highly vocal, leading us to hypothesise that vocalisations, which can propagate over large distances, could provide a means of enabling individuals to agree on when to depart - that is to establish a consensus1 - and thus coordinate the timing of mass movements. Investigations of the role of acoustic signals in coordinating collective decisions have been limited to honeybees2 and relatively small vertebrate groups (<50 individuals)3-5 and have rarely included experimental validation2,3. Here, by combining field recordings with a large-scale experimental manipulation, we show that jackdaws (Corvus monedula) use vocalisations to coordinate mass departures from winter roosts. This provides empirical evidence for vocally-mediated consensus decision-making in large vertebrate groups.