Article

The Dynamics of Coordinated Group Hunting and Collective Information Transfer among Schooling Prey

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Abstract

Predator-prey interactions are vital to the stability of many ecosystems. Yet, few studies have considered how they are mediated due to substantial challenges in quantifying behavior over appropriate temporal and spatial scales. Here, we employ high-resolution sonar imaging to track the motion and interactions among predatory fish and their schooling prey in a natural environment. In particular, we address the relationship between predator attack behavior and the capacity for prey to respond both directly and through collective propagation of changes in velocity by group members. To do so, we investigated a large number of attacks and estimated per capita risk during attack and its relation to the size, shape, and internal structure of prey groups. Predators were found to frequently form coordinated hunting groups, with up to five individuals attacking in line formation. Attacks were associated with increased fragmentation and irregularities in the spatial structure of prey groups, features that inhibit collective information transfer among prey. Prey group fragmentation, likely facilitated by predator line formation, increased (estimated) per capita risk of prey, provided prey schools were maintained below a threshold size of approximately 2 m(2). Our results highlight the importance of collective behavior to the strategies employed by both predators and prey under conditions of considerable informational constraints.

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... Understanding the detailed behavior of predators is therefore essential to understanding the ecology and evolution of their interactions with prey (Lima 2002;Hein et al. 2020). For instance, the dynamics of collective motion in schooling fish is not merely influenced by their immediate response to predators (Magurran and Pitcher 1987;Handegard et al. 2012;Cade et al. 2020), but is governed by attraction and orientation rules that may themselves have evolved to promote the formation of coherent mobile groups causing cognitive or sensory confusion in predators . Likewise, hunting mode has been found to influence the group size dependence of attack frequency and catch success in raptors attacking flocking waders, leading to conflicting selection pressures on group size according to which predator species are present (Cresswell and Quinn 2010). ...
... Nowhere is the challenge of making field observations clearer than in the case of predators attacking massive three-dimensional prey aggregations. The best examples to date have come from sonar studies of pelagic predators attacking schooling fish (Similä 1997;Nottestad and Axelsen 1999;Axelsen et al. 2001;Gerlotto et al. 2006;Handegard et al. 2012), and from videographic studies of aerial predators attacking murmurating birds (Carere et al. 2009;Procaccini et al. 2011;Storms et al. 2019). The former have successfully related predator attack behavior to shoal size, shape, and density, but have not yet allowed the individual outcomes of these behaviors to be observed (Handegard et al. 2012); the latter have been able to record individual outcomes, but have focused on the dynamics of the prey's collective motion, rather than the dynamics of the predator's attack (Carere et al. 2009;Procaccini et al. 2011;Storms et al. 2019). ...
... The best examples to date have come from sonar studies of pelagic predators attacking schooling fish (Similä 1997;Nottestad and Axelsen 1999;Axelsen et al. 2001;Gerlotto et al. 2006;Handegard et al. 2012), and from videographic studies of aerial predators attacking murmurating birds (Carere et al. 2009;Procaccini et al. 2011;Storms et al. 2019). The former have successfully related predator attack behavior to shoal size, shape, and density, but have not yet allowed the individual outcomes of these behaviors to be observed (Handegard et al. 2012); the latter have been able to record individual outcomes, but have focused on the dynamics of the prey's collective motion, rather than the dynamics of the predator's attack (Carere et al. 2009;Procaccini et al. 2011;Storms et al. 2019). Hence, there are few good examples of empirical studies relating the outcomes of attacks on massive three-dimensional prey aggregations to the individual behaviors of predators and prey. ...
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Aggregation can reduce an individual’s predation risk, by decreasing predator hunting efficiency or displacing predation onto others. Here, we explore how the behaviors of predator and prey influence catch success and predation risk in Swainson’s hawks Buteo swainsoni attacking swarming Brazilian free-tailed bats Tadarida brasiliensis on emergence. Lone bats including stragglers have a high relative risk of predation, representing ~5% of the catch but ~0.2% of the population. Attacks on the column were no less successful than attacks on lone bats, so hunting efficiency is not decreased by group vigilance or confusion. Instead, lone bats were attacked disproportionately often, representing ~10% of all attacks. Swarming therefore displaces the burden of predation onto bats outside the column—whether as isolated wanderers not benefitting from dilution through attack abatement, or as peripheral stragglers suffering marginal predation and possible selfish herd effects. In contrast, the hawks’ catch success depended only on the attack maneuvers that they employed, with the odds of success being more than trebled in attacks involving a high-speed stoop or rolling grab. Most attacks involved one of these two maneuvers, which therefore represent alternative rather than complementary tactics. Hence, whereas a bat’s survival depends on maintaining column formation, a hawk’s success does not depend on attacking lone bats—even though their tendency to do so is sufficient to explain the adaptive benefits of their prey’s aggregation behavior. A hawk’s success instead depends on the flight maneuvers it deploys, including the high-speed stoop that is characteristic of many raptors. Swarming bats emerging from a massive desert roost reduce their predation risk by maintaining tight column formation, because the hawks that predate them attack peripheral stragglers and isolated wanderers disproportionately. Whereas a bat’s predation risk depends on maintaining its position within the column, the catch success of a hawk depends on how it maneuvers itself to attack, and is maximized by executing a high-speed dive or rolling grab maneuver.
... The data from a century ago allowed the rough estimation of the population size and therefore inspired mathematical models of population dynamics. The data from the recent past allows the reconstruction of individual trajectories of individuals in swarms (Buhl et al., 2006;Cavagna et al., 2010;Francisco et al., 2020;Graving et al., 2019;Handegard et al., 2012;Strandburg-Peshkin et al., 2013). This precise nature of the data inspired models that depict the detailed movement or decision behavior of schooling fish (e.g. ...
... Here, by focusing on a dominant selection pressure, namely predation, I neglect other mechanisms, as for example resource exploration and exploitation (Brush et al., 2016;Hein et al., 2015;Monk et al., 2018;Wood and Ackland, 2007) whose ESS can also depend on the resource abundance (Brush et al., 2016;Monk et al., 2018;Wood and Ackland, 2007). This emphasizes the importance to study collective behavior in the wild (Francisco et al., 2020;Graving et al., 2019;Handegard et al., 2012;Hansen et al., 2020) to provide more empirical input on actual relevant behavioral mechanisms as well as variability of behavior across different contexts. However, I have shown that even by combining two opposing selection mechanisms (see Sect. 6.4), which on their own favor ordered or disordered state respectively, the critical point does not correspond to an evolutionary attractor, it remains an evolutionary highly unstable point. ...
... Due to the dynamic nature of the behavior, one needs to follow the trajecory of the shoal and the predator. There have been great attempts to monitor predator prey group interaction in the wild (Axelsen et al., 2001;Gerlotto et al., 2006;Handegard et al., 2012;Pitcher, 1996;Price et al., 2013;Similä, 1997). However, most of the work is based on sonar recording. ...
Thesis
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Im ersten Teil analysiere ich die Selbstorganisation zur Kritikalität (hier ein Phasenübergang von Ordnung zu Unordnung) und untersuche, ob Evolution ein möglicher Organisationsmechanismus ist. Die Kernfrage ist, ob sich ein simulierter kohäsiver Schwarm, der versucht, einem Raubtier auszuweichen, durch Evolution selbst zum kritischen Punkt entwickelt, um das Ausweichen zu optimieren? Es stellt sich heraus, dass (i) die Gruppe den Jäger am besten am kritischen Punkt vermeidet, aber (ii) nicht durch einer verstärkten Reaktion, sondern durch strukturelle Veränderungen, (iii) das Gruppenoptimum ist evolutionär unstabiler aufgrund einer maximalen räumlichen Selbstsortierung der Individuen. Im zweiten Teil modelliere ich experimentell beobachtete Unterschiede im kollektiven Verhalten von Fischgruppen, die über mehrere Generationen verschiedenen Arten von größenabhängiger Selektion ausgesetzt waren. Diese Größenselektion soll Freizeitfischerei (kleine Fische werden freigelassen, große werden konsumiert) und die kommerzielle Fischerei mit großen Netzbreiten (kleine/junge Individuen können entkommen) nachahmen. Die zeigt sich, dass das Fangen großer Fische den Zusammenhalt und die Risikobereitschaft der Individuen reduziert. Beide Befunde lassen sich mechanistisch durch einen Aufmerksamkeits-Kompromiss zwischen Sozial- und Umweltinformationen erklären. Im letzten Teil der Arbeit quantifiziere ich die kollektive Informationsverarbeitung im Feld. Das Studiensystem ist eine an sulfidische Wasserbedingungen angepasste Fischart mit einem kollektiven Fluchtverhalten vor Vögeln (wiederholte kollektive Fluchttauchgängen). Die Fische sind etwa 2 Zentimeter groß, aber die kollektive Welle breitet sich über Meter in dichten Schwärmen an der Oberfläche aus. Es zeigt sich, dass die Wellengeschwindigkeit schwach mit der Polarisation zunimmt, bei einer optimalen Dichte am schnellsten ist und von ihrer Richtung relativ zur Schwarmorientierung abhängt.
... We model our predator-agents to resemble the motion of the robotic falcon [24] in order for our results to be comparable with the empirical data. Thus, hunting in our model is based on direct pursuit [24,31], a common strategy of attack by peregrine falcons (Falco peregrinus) on flocks [32]. Each simulation includes only one predator. ...
... Thirdly, through short-term hysteresis [5]: during the progression of a collective turn, as the predator approaches, the past state of the flock (shape and relative positions of flock members) affects its next state. Both flock shape and internal structure relate to what each individual experiences in terms of predator threat (angle of attack and escape direction) and social coordination (deviation from the flock's heading and relative position to the centroid), and affect the propagation of information concerning changes in heading through the group [31]. To our knowledge, the effect of hysteresis is new in the context of collective escape. ...
... Predation is known to affect the coordination within groups of prey [31,54,55]. An example is a decrease in the minimum separation distance [54] and an increase in the number of interacting neighbors [55] in the presence of a predator. ...
Article
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Bird flocks under predation demonstrate complex patterns of collective escape. These patterns may emerge by self-organization from local interactions among group-members. Computational models have been shown to be valuable for identifying what behavioral rules may govern such interactions among individuals during collective motion. However, our knowledge of such rules for collective escape is limited by the lack of quantitative data on bird flocks under predation in the field. In the present study, we analyze the first GPS trajectories of pigeons in airborne flocks attacked by a robotic falcon in order to build a species-specific model of collective escape. We use our model to examine a recently identified distance-dependent pattern of collective behavior: the closer the prey is to the predator, the higher the frequency with which flock members turn away from it. We first extract from the empirical data of pigeon flocks the characteristics of their shape and internal structure (bearing angle and distance to nearest neighbors). Combining these with information on their coordination from the literature, we build an agent-based model adjusted to pigeons’ collective escape. We show that the pattern of turning away from the predator with increased frequency when the predator is closer arises without prey prioritizing escape when the predator is near. Instead, it emerges through self-organization from a behavioral rule to avoid the predator independently of their distance to it. During this self-organization process, we show how flock members increase their consensus over which direction to escape and turn collectively as the predator gets closer. Our results suggest that coordination among flock members, combined with simple escape rules, reduces the cognitive costs of tracking the predator while flocking. Such escape rules that are independent of the distance to the predator can now be investigated in other species. Our study showcases the important role of computational models in the interpretation of empirical findings of collective behavior.
... One major predator adaptation, presumably arising when prey collective behaviours reduce a predator's hunting success to below the level required for survival and reproduction, is for predators to form groups to improve the chances of detecting and capturing prey (Beauchamp, 2013). Social seabird predators experience enhanced prey detection (Thiebault, Mullers, Pistorius, & Tremblay, 2014), group-hunting spotted sea trout (Cynoscion nebulosus) can deconstruct the collective functioning of prey groups (Handegard et al., 2012), and spinner dolphin (Stenella longirostris) pods can corner hard to capture prey (Benoit-Bird & Au, 2009). Together these group strategies can be incredibly successful for the predator. ...
... Predators in groups have access to a pool of social information from other members, which can be transferred through cues -like the sounds a bat makes when catching prey (Dechmann et al., 2009), or by signals -like the vocalisations swallows use to recruit conspecifics (Brown, Brown, & Shaffer, 1991). Second, group hunting can enhance prey capture (Beauchamp, 2013), enabling predators to corral, confuse and dismantle prey collectives (Handegard et al., 2012), or cooperatively subdue large, dangerous prey (Stander, 1992). Spotted hyenas (Crocuta crocuta) show aspects of both these functions when they hunt herds of zebra (Equus burchelli); the pack forces zebra into a dense, moving herd, and then singles out one slower or weakened individual that the entire pack works to bring down (Kruuk, 1972). ...
... Line-formation is a common group-level strategy used by such collective predators, and can function to herd prey into dense groups and prevent escape (Benoit-Bird & Au, 2009;Partridge et al., 1983). Group hunting by predators has also been shown to facilitate the capture of collective prey by inhibiting collective information transfer within prey groups (Handegard et al., 2012). ...
... Brunton, 1997;Hobson, 1963;Parrish, 1989) and towards the back of the group (e.g. Handegard et al., 2012;Krause et al., 2017). In relation to this, previous work has shown that individuals in such positions actually have poorer access to salient social information, as well as visual information of what happens outside the group (Rosenthal et al., 2015). ...
... Furthermore, differential likelihood to be attacked is often used as a proxy for predation risk (Krause, 1994) because of difficulties in quantifying successful attacks (e.g. Handegard et al., 2012), predators failing to ever successfully attack (e.g. Parrish, 1989;Romenskyy et al., 2020), or it being impossible for predators to consume their prey (e.g. ...
... In contrast to previous work that only investigated the likelihood for an individual to be targeted (e.g. Handegard et al., 2012;Ioannou et al., 2012;Romenskyy et al., 2020), we could therefore also assess in detail what features are associated with targeted fish subsequently avoiding being caught. We compared individuals that were targeted yet successfully evaded capture (n = 34) with those individuals that were caught (n = 83), and considered as potential relevant features those that were found to be important in predicting which individual was targeted (see above), pike's vision of its target at the time of attack, the targeted individual's maximum speed, acceleration, and turning rate (max change in orientation), and pike's maximum acceleration, all in the same standard 0.5 s time window until the time of attack. ...
Preprint
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Predation is one of the main evolutionary drivers of social grouping. While it is well appreciated that predation risk is likely not shared equally among individuals within groups, its detailed quantification has remained difficult due to the speed of attacks and the highly-dynamic nature of collective prey response. Here, using high-resolution tracking of solitary predators (Northern pike) hunting schooling fish (golden shiners), we not only provide detailed insights into predator decision-making but show which key spatial and kinematic features of predator and prey influence individual's risk to be targeted and survive attacks. Pike tended to stealthily approach the largest groups, and were often already inside the school when launching their attack, making prey in this frontal "strike zone" the most vulnerable to be targeted. From the prey's perspective, those fish in central locations, but relatively far from, and less aligned with, neighbours, were most likely to be targeted. While the majority of attacks (70%) were successful, targeted individuals that did manage to avoid capture exhibited a higher maximum acceleration response just before the attack and were further away from the pike's head. Our results highlight the crucial interplay between predators' attack strategy and response of prey in determining predation risk in mobile animal groups.
... 'many wrongs principle'; Codling, Pitchford, & Simpson, 2007;Larkin & Walton, 1969;Simons, 2004). It could also decrease risk of predation (Handegard et al., 2012). ...
... Moreover, traveling in schools comprised of their closest kin may have additional advantages for larvae. Collectively, they have higher chances of recognizing dangerous predators, identifying food sources and cues (Handegard et al., 2012), and navigating to a suitable habitat (Berdahl, Westley, Levin, Couzin, & Quinn, 2016;Couzin, 2007;Torney, Berdahl, & Couzin, 2011;Torney, Neufeld, & Couzin, 2009). In schools of fish, it has also been shown that the ability to sense odor cues increases with group size (Hall, Burton, Margrey, & Graves, 1982) and coral reef fish larvae particularly rely on such cues when recruiting home (Paris et al., 2013). ...
Article
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Coral reef fish larvae are tiny, exceedingly numerous, and hard to track. They are also highly capable, equipped with swimming and sensory abilities that may influence their dispersal trajectories. Despite the importance of larval input to the dynamics of a population, we remain reliant on indirect insights to the processes influencing larval behavior and transport. Here, we used genetic data (300 independent single nucleotide polymorphisms) derived from a light trap sample of a single recruitment event of Dascyllus abudafur in the Red Sea (N = 168 settlers). We analyzed the genetic composition of the larvae and assessed whether kinship among these was significantly different from random as evidence for cohesive dispersal during the larval phase. We used Monte Carlo simulations of similar‐sized recruitment cohorts to compare the expected kinship composition relative to our empirical data. The high number of siblings within the empirical cohort strongly suggests cohesive dispersal among larvae. This work highlights the utility of kinship analysis as a means of inferring dynamics during the pelagic larval phase.
... The broad hypothesis is that collective motion of animal groups arise due to application of simple rules of interaction between individuals, similar to those used in theoretical models [5]. Collective motion has proved to be a rich field of study [1], with the development of many models that incorporate individual-level interactions to simulate the grouplevel patterns produced by a wide range of biological systems [2][3][4][6][7][8] and, more recently, methods for inferring the presence and form of such interactions directly from observations of animals [1,[9][10][11][12][13][14][15][16][17][18]. ...
... There are numerous studies that use both data and simulation to investigate these relationships and evidence suggests that the risk of predation is lower when prey form ordered compact formations [15]. While specific mechanisms are not fully understood, this has been attributed to factors such as increased information transfer within ordered formations [12] and confusion of predators [61]. In this study, it can be observed that more ordered, compact and higher-speed collective movement of the defensive formation reflect patterns associated with reduced risk of predation on prey in predator-prey studies. ...
Article
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Movement, positioning and coordination of player formations is a key aspect for the performance of teams within field-based sports. The increased availability of player tracking data has given rise to numerous studies that focus on the relationship between simple descriptive statistics surrounding team formation and performance. While these existing approaches have provided a high-level a view of team-based spatial formations, there is limited research on the nature of collective movement across players within teams and the establishment of stable collective states within game play. This study draws inspiration from the analysis of collective movement in nature, such as that observed within schools of fish and flocking birds, to explore the existence of collective states within the phases of play in soccer. Order parameters and metrics describing group motion and shape are derived from player movement tracks to uncover the nature of the team’s collective states and transitions. This represents a unique addition to the current body of work around the analysis of player movement in team sports. The results from this study demonstrate that sequences of ordered collective behaviours exist with relatively rapid transitions between highly aligned polar and un-ordered swarm behaviours (and vice-versa). Defensive phases of play have a higher proportion of ordered team movement than attacking phases, indicating that movements linked with attacking tactics, such as player dispersion to generate passing and shooting opportunities leads to lower overall collective order. Exploration within this study suggests that defensive tactics, such as reducing the depth or width to close passing opportunities, allows for higher team movement speeds and increased levels of collective order. This study provides a novel view of player movement by visualising the collective states present across the phases of play in football.
... One of the most studied benefits of being in a group is the facilitated detection of behaviorally significant cues in the environment, as information about their presence can quickly spread across a large group of individuals 12 . In the context of threat detection, most research has focused on actively emitted signals, such as alarm calls and foot stamping (reviewed in refs. ...
... Predator and prey both use motion cues to detect each other using these to make decisions about when and how to strike or whether and how to escape [39][40][41][42] . Furthermore, prey animals also use motion cues from other prey as an indirect cue of a predator's presence 4,12,43 . We believe that the current study opens a new path to study how animals in groups integrate motion cues generated by predators, their own movement, and that of others to select the appropriate defensive responses. ...
Article
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Living in a group allows individuals to decrease their defenses, enabling other beneficial behaviors such as foraging. The detection of a threat through social cues is widely reported, however, the safety cues that guide animals to break away from a defensive behavior and resume alternate activities remain elusive. Here we show that fruit flies display a graded decrease in freezing behavior, triggered by an inescapable threat, with increasing group sizes. Furthermore, flies use the cessation of movement of other flies as a cue of threat and its resumption as a cue of safety. Finally, we find that lobula columnar neurons, LC11, mediate the propensity for freezing flies to resume moving in response to the movement of others. By identifying visual motion cues, and the neurons involved in their processing, as the basis of a social safety cue this study brings new insights into the neuronal basis of safety in numbers.
... In those environments, we observed schools of free-ranging juvenile gulf menhaden (Brevoortia patronus), a planktivorous forage species that plays an important ecological role as a source of prey for many piscivorous species. The collective behavioural state of each fish school was quantified using six behavioural parameters commonly employed to quantify dynamic collective tendency in schooling fish: school area, group speed, angular velocity, orientational alignment (polarization), coherence of rotation (rotational order) (Attanasi et al. 2014), and correlation strength (degree of influence on neighbours) (Cavagna et al. 2008;Handegard et al. 2012). We hypothesize that the non-natural environmental conditions induced by the WCS will elicit changes in the schooling state of freely behaving fish schools, particularly in response to predation. ...
... The school area was calculated based on the school boundary detection algorithm and is a local 2D projection approximation of the total area coverage occupied by the school (Handegard et al. 2012). The group speed was derived by centre-of-mass measurements of the school and its change in position with respect to time over the course of the response, normalized to the initial computed speed of the school. ...
Article
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Animal groups are known to exhibit collective behaviours that allow for effective responses to predators and environmental factors. Habitats with high levels of structural complexity have been shown to influence the collective tendencies of these animal aggregations. However, the effect of anthropogenically induced habitat complexity on collective tendency is still unknown. We examined the effect of a water control structure (WCS), located in an estuarine salt marsh system, on the collective behaviours of free ranging juvenile Gulf menhaden (Brevoortia patronus), a schooling forage fish. Using an acoustic imaging sonar, behavioural observations prior to and during predator attacks were collected in an open marsh canal as well as in the vicinity of the WCS. We found that fish in schools responded to the WCS by swimming in a less aligned and cohesive manner, while maintaining an increased ability to transfer social information. Our results demonstrate that collective tendency in schooling fish is affected by the presence of anthropogenically introduced habitat complexity, prior to and during predator attack. Our study, thus, strengthens the idea that the complex environmental conditions induced by the presence of man-made structures may play a large role in structuring collective behaviour and trophic interactions in aquatic environments.
... However, dynamical animal groups differ from lattice models [37,38] due to their dynamical neighborhood which may induce self-sorting of individuals according to their individual behavioral parameters [39][40][41]. This, in turn, has likely direct evolutionary consequences as for example predators may attack certain swarm regions more frequently [42][43][44]. ...
... Here, by focusing on a dominant selection pressure, namely predation, we neglect other mechanisms, as for example resource exploration and exploitation [31,52,55,57] whose ESS can also depend on the resource abundance [31,52,57]. This emphasizes the importance to study collective behavior in the wild [44,[70][71][72] to provide more empirical input on actual relevant behavioral mechanisms as well as variability of behavior across different contexts. However, we have shown that even by combining two opposing selection mechanisms (see S1 Text, Sec. ...
Article
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According to the criticality hypothesis , collective biological systems should operate in a special parameter region, close to so-called critical points, where the collective behavior undergoes a qualitative change between different dynamical regimes. Critical systems exhibit unique properties, which may benefit collective information processing such as maximal responsiveness to external stimuli. Besides neuronal and gene-regulatory networks, recent empirical data suggests that also animal collectives may be examples of self-organized critical systems. However, open questions about self-organization mechanisms in animal groups remain: Evolutionary adaptation towards a group-level optimum (group-level selection), implicitly assumed in the “criticality hypothesis”, appears in general not reasonable for fission-fusion groups composed of non-related individuals. Furthermore, previous theoretical work relies on non-spatial models, which ignore potentially important self-organization and spatial sorting effects. Using a generic, spatially-explicit model of schooling prey being attacked by a predator, we show first that schools operating at criticality perform best. However, this is not due to optimal response of the prey to the predator, as suggested by the “criticality hypothesis”, but rather due to the spatial structure of the prey school at criticality. Secondly, by investigating individual-level evolution, we show that strong spatial self-sorting effects at the critical point lead to strong selection gradients, and make it an evolutionary unstable state. Our results demonstrate the decisive role of spatio-temporal phenomena in collective behavior, and that individual-level selection is in general not a viable mechanism for self-tuning of unrelated animal groups towards criticality.
... 5,6 This paucity of studies is unsurprising because predator-prey interactions in the field are difficult to observe. Furthermore, the focus in recent studies on predator-prey interactions has been on the collective behavior of the prey 7-10 rather than on the behavior of the predator (but see Ioannou et al. 11 and Handegard et al. 12 ). Here we present a field study that investigated the anti-predator benefits of waves produced by fish at the water surface when diving down collectively in response to attacks of avian predators. ...
... A shot successfully induced waves that were similar in number, size, and speed to those produced post-attack by kingfishers (Figures 4A and 4B; see STAR Methods for details). We alternated between shots into the fish school and control shots that were shot at the same distance to the bird but into an area outside the fish school and thus did not induce any waves (SI_-stats_7; shots: n = 75, median [min-max] waves = 4 [1][2][3][4][5][6][7][8][9][10][11][12][13][14][15], controls: n = 37, 0 [0-0], Wilcoxon signed-rank test: V = 2,850, p < 0.001; Figure 4B; see also Figure 3A for comparison to natural kiskadee attacks). Experimentally triggering waves on average doubled waiting times in kiskadees (mean; control, 21.9 s; shot, 42.9 s), supporting a causal link between the occurrence of post-attack waves and the delay of bird attacks. ...
Article
The collective behavior of animals has attracted considerable attention in recent years, with many studies exploring how local interactions between individuals can give rise to global group properties.1, 2, 3 The functional aspects of collective behavior are less well studied, especially in the field,⁴ and relatively few studies have investigated the adaptive benefits of collective behavior in situations where prey are attacked by predators.⁵,⁶ This paucity of studies is unsurprising because predator-prey interactions in the field are difficult to observe. Furthermore, the focus in recent studies on predator-prey interactions has been on the collective behavior of the prey7, 8, 9, 10 rather than on the behavior of the predator (but see Ioannou et al.¹¹ and Handegard et al.¹²). Here we present a field study that investigated the anti-predator benefits of waves produced by fish at the water surface when diving down collectively in response to attacks of avian predators. Fish engaged in surface waves that were highly conspicuous, repetitive, and rhythmic involving many thousands of individuals for up to 2 min. Experimentally induced fish waves doubled the time birds waited until their next attack, therefore substantially reducing attack frequency. In one avian predator, capture probability, too, decreased with wave number and birds switched perches in response to wave displays more often than in control treatments, suggesting that they directed their attacks elsewhere. Taken together, these results support an anti-predator function of fish waves. The attack delay could be a result of a confusion effect or a consequence of waves acting as a perception advertisement, which requires further exploration.
... In this study, although all predators used different methods of feeding, they all exhibited predation bias toward shrimp with black gill. Both red drum and spotted seatrout are schooling fish (Wilson and Nieland, 1994;Handegard et al., 2012). When schooling fish encounter prey, feeding activity can signal to other fish that prey are in the area (Keenleyside, 1955). ...
... When schooling fish encounter prey, feeding activity can signal to other fish that prey are in the area (Keenleyside, 1955). Additionally, schooling fish, such as spotted seatrout, often strike together, placing more pressure on prey and increasing the likelihood for prey consumption (Handegard et al., 2012). In contrast, blue crabs in this study appeared to be more territorial and aggressive towards other crabs, and when in proximity to one another, seemed more focused on other crabs rather than on shrimp prey (Gooding, personal observation). ...
Article
Parasites can kill hosts directly, but also indirectly, by enhancing susceptibility to environmental factors and biotic interactions. In the United States South Atlantic Bight region of the northwest Atlantic Ocean, white shrimp (Penaeus setiferus) support a substantial commercial fishery and are also valuable prey for many marine and estuarine species. Since the late 1990s, a condition known as black gill has been observed in penaeid shrimp in the South Atlantic Bight. In this region, black gill has been linked to an apostome ciliate that elicits an innate immune response in shrimp, manifested through the melanization of gill tissues, which impedes respiratory functions and hemolymph ion regulation. The objective of this study was to determine if black gill subjects shrimp to higher rates of predation by red drum (Sciaenops ocellatus), spotted seatrout (Cynoscion nebulosus), and blue crab (Callinectes sapidus). A series of simultaneous prey choice mesocosm experiments was conducted, during which single-species predators were able to consume shrimp that were both symptomatic and asymptomatic of black gill over a four-hour period. Predator species were 1.4 to 3.0 times more likely to consume symptomatic shrimp than asymptomatic shrimp. The hinderance of shrimp physiology and escape responses due to gill melanization likely increases the vulnerability of shrimp to predation. This study emphasizes that mortality from parasitic infections is not always direct and that black gill may have a significant impact on penaeid shrimp through secondary, or indirect, mortality.
... Although competition for food increases with the group size (Rieucau et al. 2015), shoaling may make feeding more effective by improving sampling efficiency and providing more time for feeding (Pitcher and Parrish 1993) as well as by enabling cooperative hunting (Handegard et al. 2012). Schooling fish also gain a hydrodynamic advantage (Hemelrijk et al. 2014) and can learn from others (Laland et al. 2011). ...
Chapter
When we try to improve the welfare of fish in aquaculture, public and private aquaria, and experimental research we need to take into account how fish live in their natural environments. There is enormous diversity in the world of fishes. Each species has adapted to specific habitats and co-existing species, with their anatomical, physiological, and behavioural traits in concert enabling them to survive, grow and reproduce. Fish species have different life histories with regard to longevity, rate of growth, age of reproduction, and number of reproductions and offspring. The great diversity of ways in which fish eat and avoid being eaten results in a wide range of patterns of activity and movement, while reproductive behaviour shows remarkable variation, ranging from mass spawning to long-term pair bonds. Fish may live as solitary individuals, in shoals, or huge schools. They use a set of sensors to obtain an integrated view of their environment, and communicate using various sensory channels. To behave in an adaptive way, they require the mechanisms to do what they need to do to survive and prosper. Physiological adaption to environmental variations is crucial, but rapid changes in the environment caused by human activities can impair welfare and even cause selective mortality, leading to genetic changes throughout entire populations. Fish may be classified into proactive and reactive species with different basic “personalities”, and only species with the appropriate personality are suitable for farming.
... Later larvae of N. viridula produce their own aggregation pheromone that is attractive at low to intermediate concentrations, but repellent at high concentrations (Bengtsson 2008). The advantages of living in a group have been examined in earlier publications (Handegard et al. 2012). A widely accepted benefit of aggregation behavior is enhanced protection against predators (Cocroft 2002), e.g., by the "dilution of risk" (Treherne and Foster 1982;Watt et al. 1997;Aukema and Raffa 2004;Morrell and James 2007), since an individual is less exposed to potential predators when in an aggregation. ...
Chapter
Myrmecochory or plant seed dispersal by ants is a widely spread phenomenon. Seeds of such plants bear specialised lipid-rich appendages, elaiosomes, for attracting ants. Ant workers collect the seeds and usually carry them to their nests. The ant species complex in the ecosystem is continuously changing in time and space, and the question arises about the effect of the spatial distribution of different ant species in the ecosystem on the number and distribution of myrmecochorous plants with different dispersal strategies. In this chapter, we model the population dynamics of two myrmecochorous plants having various dispersal strategies in an ecosystem with two ant species differing in their seed preferences, colony territory size, and location of their waste piles. We find a correlation between the number of nests of different ant species and the stability of the ecosystem. In particular, if one ant species would partially or totally disappear from the system, this could cause dramatic changes in the plant populations as well. Another example treated in this chapter deals with animal aggregations, which are especially common in insects. The aggregations may result from an uneven distribution of resources or because an attraction of individuals to each other may be more efficient in defending the group against predators in general and each member of the group in particular. Tree trunks and other cylindrical objects, where aggregated insects live, represent a specific environment for predator-prey interactions, which is fundamentally different from the planar one. For a better understanding of the predator-prey interaction in a cylindrical space, we applied a numerical model that allows testing the effect of interactions between predator and aggregated prey on the plane and on the cylinder, taking into consideration different abilities of predators to visually detect the prey in these two types of space. It is shown that the aggregation in conjunction with a specific environment may bring additional advantages for the prey. When one prey subgroup aggregates on the other side of the tree trunk and becomes invisible for the predator, it will survive with a higher probability. After all, the predator moving along one side of the tree will finally loose the major group of the prey completely.
... Specifically, our proposal is that what most distinguishes living systems is their causal and informational architecture (see, e.g., Walker (2017)) and that modern information measures, such as transfer entropy (Schreiber 2000), causal information flow (Ay and Polani 2008), effective information (Hoel et al. 2013), causal specificity (Griffiths et al. 2015), integrated information (Oizumi et al. 2014), and integrated spatiotemporal patterns (Polani et al. 2016) to name just a few, all hold promise to provide insights into the diversity and richness of biological processes from an information-theoretic perspective thus allowing windows into how we can characterize the informational and causal structure of life across a variety of spatial and temporal scales. Velocity and directional information, for example, are physical quantities often studied in the context of coordinated motion of fish schools (Handegard et al. 2012) and starling flocks (Cavagna et al. 2010). The propagation of this type of information across a collective has also been modeled with tools from statistical physics . ...
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Collective behavior is widely regarded as a hallmark property of living and intelligent systems. Yet, many examples are known of simple physical systems that are not alive, which nonetheless display collective behavior too, prompting simple physical models to often be adopted to explain living collective behaviors. To understand collective behavior as it occurs in living examples, it is important to determine whether or not there exist fundamental differences in how non-living and living systems act collectively, as well as the limits of the intuition that can be built from simpler, physical examples in explaining biological phenomenon. Here, we propose a framework for comparing non-living and living collectives as a continuum based on their information architecture: that is, how information is stored and processed across different degrees of freedom. We review diverse examples of collective phenomena, characterized from an information-theoretic perspective, and offer views on future directions for quantifying living collective behaviors based on their informational structure.
... Later larvae of N. viridula produce their own aggregation pheromone that is attractive at low to intermediate concentrations, but repellent at high concentrations (Bengtsson 2008). The advantages of living in a group have been examined in earlier publications (Handegard et al. 2012). A widely accepted benefit of aggregation behavior is enhanced protection against predators (Cocroft 2002), e.g., by the "dilution of risk" (Treherne and Foster 1982;Watt et al. 1997;Aukema and Raffa 2004;Morrell and James 2007), since an individual is less exposed to potential predators when in an aggregation. ...
Book
Basic laws of nature are rather simple, but observed biological structures and their dynamic behaviors are unbelievably complicated. This book is devoted to a study of this “strange” relationship by applying mathematical modeling to various structures and phenomena in biology, such as surface patterns, bioadhesion, locomotion, predator-prey behavior, seed dispersal, etc. and revealing a kind of self-organization in these phenomena. In spite of diversity of biological systems considered, two main questions are (1) what does self-organization in biology mean mathematically and (2) how one can apply this knowledge to generate new knowledge about behavior of particular biological system? We believe that this kind of “biomimetics” in computer will lead to better understanding of biological phenomena and possibly towards development of technical implications based on our modeling.
... Behavioral coordination is inextricably linked with sociality, and synchrony is a ubiquitous component of that coordination. Behavioral coordination/synchrony is essential for a wide range of behaviors including: schooling/flocking (Boinski and Garber, 2000;Greenberg, 2001), group living (Conradt and Roper, 2005;Focardi and Pecchioli, 2005), hunting (Handegard et al., 2012;Bailey et al., 2013), and heterospecific communication [reviewed in Duranton and Gaunet (2016)]. In general it is clear that behavioral synchrony promotes social cohesion (Pays et al., 2007;King and Cowlishaw, 2009), affiliation (Sakai et al., 2010), and prosocial behavior (Van Baaren et al., 2004;Ashton-James et al., 2007;Gueguen et al., 2009) (reviewed in Duranton and Gaunet, 2016). ...
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Our understanding of the behavioral and physiological mechanisms of monogamy largely comes from studies of behavioral interactions unique to pair-bonded individuals. By focusing on these highly marked behaviors, a remarkable conservation in the mechanisms underlying pair bonding has been revealed; however, we continue to know very little about the range of behavioral and neurobiological mechanisms that could explain the great diversity of pair-bonding phenotypes that exists both within and across species. In order to capture the dynamic nature of bonds over time and across contexts, we need specific, operationally-defined behavioral variables relevant across such a diversity of scenarios. Additionally, we need to be able to situate these behavioral variables within broader frameworks that allow us to interpret and compare patterns seen across species. Here I review what is known about behavioral synchrony with respect to pair bonding and discuss using synchrony as such a variable as well as a framework to expand on our understanding of pair bonding across timescales, contexts and species. First, I discuss the importance of behavioral synchrony and parental coordination for reproductive success in monogamous biparental bird species. Second, I highlight research documenting the critical importance of interpersonal coordination for human social relationships. Finally, I present recent work that experimentally bridges these lines of research by quantifying moment-to-moment behavioral synchrony during brief social interactions in zebra finch dyads. All together, these distinct perspectives support the notion that synchrony (1) is a shared premise for sociality across species, (2) is deeply shaped by social experiences, and (3) exists across timescales, behaviors, and levels of physiology. Conceptualizing pair bonding through the framework of behavioral synchrony is likely to facilitate a deeper understanding of the nuances of how social experiences and interactions impact the brain and behavior.
... Increases in swimming speed may indicate fright or anxiety associated with a perceived threat (e.g., predation risk: Neo et al., 2014), and changes are highly correlated with alterations in group inter-individual distance and alignment, or orientation (Kent et al., 2019). An increase in interindividual distance, as observed over time during this study, may be costly, with isolated individuals more susceptible to predation (Handegard et al., 2012). Noise can distract from the detection of an additional stimulus, and therefore reduce information sharing. ...
Article
Behavioral guidance systems are commonly used in freshwater fish conservation. The biological relevance of sound to fish and recorded responses to human-generated noise supports the viability of the use of acoustics as an effective stimulus in such technologies. Relatively little information exists on the long-term responses and recovery of fish to repeated acoustic exposures. In a controlled laboratory study, the response and tolerance of Eurasian minnow (Phoxinus phoxinus) shoals to tonal signals (150 Hz of 1 s pulse duration) differing only in temporal characteristics (“continuous,” “slow,” “intermediate,” or “fast” pulse repetition rate) were investigated. In comparison to independent control groups, fish increased their mean group swimming speed, decreased inter-individual distance, and became more aligned in response to the onset of all four acoustic treatments. The magnitude of response, and time taken to develop a tolerance to a treatment differed according to pulse repetition rate. Groups were found to have the greatest and longest lasting response to tone sequences tested in this study when they were pulsed at an intermediate rate of 0.2 s-1. This study illustrates the importance of understanding the response of fish to acoustic signals, and will assist toward the development of longer-term effective acoustic guidance systems.
... However, while there is ample empirical evidence that information exchanges affect the way in which agents move in space [27,31,[38][39][40], a feedback mechanism has not been considered so far within the context of epidemic processes. Here, we propose a reference model that introduces a feedback between the agents' mobility and an internal degree of freedom, characterizing the information spreading across the population. ...
Article
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Populations of mobile agents—animal groups, robot swarms, or crowds of people—self-organize into a large diversity of states as a result of information exchanges with their surroundings. While in many situations of interest the motion of the agents is driven by the transmission of information from neighboring peers, previous modeling efforts have overlooked the feedback between motion and information spreading. Here we show that such a feedback results in contagion enhanced by flocking. We introduce a reference model in which agents carry an internal state whose dynamics is governed by the susceptible-infected-susceptible (SIS) epidemic process, characterizing the spread of information in the population and affecting the way they move in space. This feedback triggers flocking, which is able to foster social contagion by reducing the epidemic threshold with respect to the limit in which agents interact globally. The velocity of the agents controls both the epidemic threshold and the emergence of complex spatial structures, or swarms. By bridging together soft active matter physics and modeling of social dynamics, we shed light upon a positive feedback mechanism driving the self-organization of mobile agents in complex systems.
... Here, by focusing on a dominant selection pressure, namely predating, we neglect other mechanisms, as for example resource exploration and exploitation [48,30,45] whose ESS can also depend on the resource abundance [30,45]. This emphasizes the importance to study collective behavior in the wild [61,62,63,64] to provide more empirical input on actual relevant behavioral mechanisms as well as variability of behavior across different contexts. However, we have shown that even by combining two opposing selection mechanisms (see SI Sect. ...
Preprint
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According to the criticality hypothesis, collective biological systems should operate in a special parameter region, close to so-called critical points, where the collective dynamics undergoes a qualitative change between different dynamical regimes. Critical systems exhibit unique properties, which may benefit collective information processing such as maximal responsiveness to external stimuli. Besides neuronal and gene-regulatory networks, recent empirical data supports that also animal collectives may be examples of self-organized critical systems. However, open questions about self-organization mechanisms in animal groups remain: Evolutionary adaptation towards group-level optima (group-level selection), often implicitly assumed in the criticality hypothesis, is in general not a reasonable mechanism in fission-fusion groups composed of non-related individuals. Furthermore, previous theoretical work relies on non-spatial models, which ignore potentially important spatial self-organization effects. Here, using a generic, spatially-explicit model of schooling prey being attacked by a predator, we show first that schools operating at criticality perform best. However, this is not due to optimal response of the prey to the predator, as suggested by the ``criticality hypothesis'', but rather due to the spatial structure of the prey school at criticality. Secondly, by investigating individual-level evolution, we show that the critical point is not an evolutionary stable state. On the contrary, strong spatial self-sorting effects increase the selection strength, and make it an evolutionary unstable state. Our results show that in collective behavior spatio-temporal dynamics are important, and that individual-level selection does not in general provide a robust proximate mechanism in support of the ``criticality hypothesis'' in animal groups.
... Grouping is often a defensive strategy to reduce the likelihood of individuals being attacked through detection, dilution, confusion, or self-herd effects [1][2][3][4]. Because isolated individuals are more likely to be targeted by predators [5][6][7][8], individuals in groups often move to maintain cohesion by escaping from predators in the same direction as other group members [9,10]. Many models aimed at explaining such coordinated movements assume animals rely primarily on visual information to infer neighbours' movements and positions [11], although the mechanosensory lateral line system may also play a role in communication among social fishes [12,13]. ...
Article
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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 Artiodac-tyla (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.
... Specifically, it quantifies how the speed and heading of an individual is influenced by that of its neighbours. It has been used to demonstrate leader-follower relationships (Strandburg-Peshkin et al. 2018), to evaluate how social context influences locomotory decision-making (Tomaru et al. 2016) and to examine how predator-prey interactions are shaped by information transfer among prey (Marras et al. 2012) and between predators and prey (Handegard et al. 2012;Hu et al. 2015). These technologies and techniques offer opportunities to further expand our understanding of the ways in which animals utilise socially transmitted information to inform their patterns of behaviour under different ecological contexts. ...
Article
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The behaviour of animals is strongly influenced by the detection of cues relating to foraging opportunity or to risk, while the social environment plays a crucial role in mediating their behavioural responses. Despite this, the role of the social environment in the behaviour of non-grouping animals has received far less attention than in social species. Here, we present the results of an experiment on a cryptic species of goby (Pseudogobius sp.), which does not form social groups in its natural habitat. Gobies were presented sequentially with chemical cues relating to food, conspecific alarm and control, while in the presence of conspecifics. The intermittent locomotory behaviour of the gobies, which is typical of many cryptic animals, was influenced by the type of cues presented. Gobies decreased the duration of bouts of stasis in the presence of food cues and were generally more active. By contrast, those detecting alarm cues decreased the duration of movement bouts and were generally less active. In line with previous studies involving shoaling species, gobies in the presence of food cues adopted a more dispersed distribution, while clustering together in the presence of alarm cues. Finally, we used calculations of transfer entropy as a means of inferring information transfer among experimental subjects. In contrast to previous studies that have focused on social species, transfer entropy between gobies was detectable only in the conspecific alarm treatment. Taken together, our results show that members of this cryptic species detect and respond to chemical cues by adjusting their movement and distancing to conspecifics. Furthermore, they augment their own information with social cues but only when they perceive a threat. Significance statement Animals are routinely exposed to an array of cues within their environment that convey valuable information about risk and foraging opportunities and must adapt their behaviour accordingly. To facilitate this, animals often use information arising from the behaviour of conspecifics to inform their own responses; however, this has rarely been considered in species which do not exhibit strong grouping tendencies. We used a non-shoaling fish, the goby (Pseudogobius sp.), to examine both their responses to ecologically relevant cues and the effect of the social environment on these responses. The gobies adapted their distances relative to one another according to the cues present and responded most strongly to information arising from conspecifics (measured as transfer entropy) in the presence of a potential threat. This demonstrates the potential importance of social information even to species that do not live in social groups with others of their own kind.
... Furthermore, extremely high densities necessary for saturation of visual projection in bird flocks would require interindividual distances, which would make collisions very likely for empirically derived parameters (5). These extremely high densities are more likely to occur in large schools of pelagic fish, such as sardines or herring (35,36). The simplest solution for avoiding saturation of the visual projection field is to abandon the restriction of a binary visual projection. ...
Article
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Classical models of collective behavior often take a “bird’s-eye perspective,” assuming that individuals have access to social information that is not directly available (e.g., the behavior of individuals outside of their field of view). Despite the explanatory success of those models, it is now thought that a better understanding needs to incorporate the perception of the individual, i.e., how internal and external information are acquired and processed. In particular, vision has appeared to be a central feature to gather external information and influence the collective organization of the group. Here, we show that a vision-based model of collective behavior is sufficient to generate organized collective behavior in the absence of spatial representation and collision. Our work suggests a different approach for the development of purely vision-based autonomous swarm robotic systems and formulates a mathematical framework for exploration of perception-based interactions and how they differ from physical ones.
... One of these is the ability to make use of information provided by other individuals in the group. For example: a navigating bird may choose its direction of flight in part by following others in the flock [3,4]; foraging animals can use the presence of others at a site as an indicator of food availability [5,6]; fish can effectively avoid predators by following others who are seeking to do the same [7,8]; and demand for consumer items is often driven by their perceived popularity [9], especially amongst high-status individuals [10]. ...
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A bstract Social animals can improve their decisions by attending to the choices made by others. The rewards gained by attending to this social information must be balanced against the costs of obtaining and processing it. Previous work has investigated the behaviour of rational agents that respond optimally to a full sequence of prior decisions. However, such full sequences are potentially difficult to perceive and costly to process. As such, real animals are likely to rely on simpler forms of information when making decisions, which in turn will affect the social behaviour they exhibit. In this paper I derive the optimal policy for rational agents responding to specific simplified forms of social information. I show how the behaviour of agents attending to the total aggregate number of previous choices differs from those attending to more dynamic information provided by the most recent prior decision, and I propose a hybrid strategy that incorporates both information sources to give a highly accurate approximation to the optimal policy with the full sequence. Finally I analyse the evolutionary stability of each strategy depending on the cost of cognition and perception, showing that a hybrid strategy dominates when this cost is low but non-zero, while attending to the most recent decision is dominant when costs are high. These results show that agents can employ highly effective social decision-making rules without requiring unrealistic cognitive capacities, and point to likely ecological variation in the social information different animals attend to.
... In particular, continuous models are characteristic of a macroscopic point of view and rely on the definition of a proper density of agents, whose dynamics are set to obey conservation equations and phenomenological assumptions for their closure [11][12][13][14][15]. Hydrodynamic arguments and Boltzmann-like evolution laws for statistical distributions of individual position and velocity are instead at the basis of mesoscopic kinetic approaches [16][17][18]. Finally, discrete models and cellular automata employ a microscopic perspective and describe the system of interest as a set of single/isolated elements, which are individually considered and behave according to individual rules (based, for instance, on energy minimization or on Newtonian laws) [19][20][21][22][23][24][25]. For the sake of completeness, we recall that spatial organization and collective motion of systems of animals can be also approached with lattice-based models. ...
Article
Collective dynamics in animal groups is a challenging theme for the modelling community, being treated with a wide range of approaches. This topic is here tackled by a discrete model. Entering in more details, each agent, represented by a material point, is assumed to move following a first-order Newtonian law, which distinguishes speed and orientation. In particular, the latter results from the balance of a given set of behavioural stimuli, each of them defined by a direction and a weight, that quantifies its relative importance. A constraint on the sum of the weights then avoids implausible simultaneous maximization/minimization of all movement traits. Our framework is based on a minimal set of rules and parameters and is able to capture and classify a number of collective group dynamics emerging from different individual preferred behaviour, which possibly includes attractive, repulsive and alignment stimuli. In the case of a system of animals subjected only to the first two behavioural inputs, we also show how analytical arguments allow us to a priori relate the equilibrium interparticle spacing to critical model coefficients. Our approach is then extended to account for the presence of predators with different hunting strategies, which impact on the behaviour of a prey population. Hints for model refinement and applications are finally given in the conclusive part of the article. This article is part of the theme issue ‘Multi-scale analysis and modelling of collective migration in biological systems’.
... For cognitive agents, collective activities are often referred to as providing scaffolding or constraints on individual cognitive processes. Collective dynamics are explored in a number of scientific research programs: coordination dynamics (Kelso 2021) and collective behavior (Handegard et al. 2012, Couzin 2018, for example. Several models have been created to examine and explain the interactions that lead to collective patterns of activity, such as the Haken-Kelso-Bunz model of synchronization (Haken et al. 1985) in human dyadic coordination. ...
Article
The study of active matter systems demonstrates the usefulness of considering how interactions might co-constitute agential dynamics. Active matter systems are comprised of self-propelled independent entities which, en masse, take part in complex and interesting collective group behaviors at a far-from-equilibrium state (Menon, 2010, Takatori and Brady 2015). These systems are modelled using very simple rules (Vicsek at al. 1995), which reveal the interactive nature of the collective behaviors seen from humble to highly complex entities. I argue that the study of active matter systems demonstrates the utility of using a minimal approach to agency in studying interactive agential dynamics in more complex systems. I give examples of how this can be useful for thinking about agency in more complex systems by treating interactions as an ontological category (Longino 2021). The examples of coordination dynamics (Kelso 2001) and participatory sense-making (De Jaegher and Di Paolo 2007) are provided to show how understanding agency requires us to look beyond the individuals to the interactive agential dynamics that can guide, scaffold, or constrain their activity.
... The 'rush and grab' strategy of striped marlin appears to be a strategy of many large marine piscivore predators that feed on schooling fish [34,35]. This repeated dashing led to higher prey capture rates per minute in striped marlin compared with sailfish, and future work should assess the energetics of this fast pace strategy in comparison with the attack strategy used by sailfish. ...
Article
Full-text available
Linking morphological differences in foraging adaptations to prey choice and feeding strategies has provided major evolutionary insights across taxa. Here, we combine behavioural and morphological approaches to explore and compare the role of the rostrum (bill) and micro-teeth in the feeding behaviour of sailfish (Istiophorus platypterus) and striped marlin (Kajikia audax) when attacking schooling sardine prey. Behavioural results from high-speed videos showed that sailfish and striped marlin both regularly made rostrum contact with prey but displayed distinct strategies. Marlin used high-speed dashes, breaking schools apart, often contacting prey incidentally or tapping at isolated prey with their rostra; while sailfish used their rostra more frequently and tended to use a slower, less disruptive approach with more horizontal rostral slashes on cohesive prey schools. Capture success per attack was similar between species, but striped marlin had higher capture rates per minute. The rostra of both species are covered with micro-teeth, and micro-CT imaging showed that species did not differ in average micro-tooth length, but sailfish had a higher density of micro-teeth on the dorsal and ventral sides of their rostra and a higher amount of micro-teeth regrowth, suggesting a greater amount of rostrum use is associated with more investment in micro-teeth. Our analysis shows that the rostra of billfish are used in distinct ways and we discuss our results in the broader context of relationships between morphological and behavioural feeding adaptations across species.
... In Ref. (Firth, 2020), Firth made the case that complex contagions might be key to explaining some specific collective animal dynamics, especially those with socially transmittable behaviors. In the case of direct behavioral transmission in mobile animal groups-schooling fish, flocking birds, swarming insects (Handegard et al., 2012;Couzin and Krause, 2003;Krause and Ruxton, 2002;Kastberger, Schmelzer, and Kranner, 2008)-a full understanding of the nature of the propagation is still lacking, with (Rosenthal et al., 2015) proposing that complex contagion might be a possible path due to the highly clustered networks observed in golden shiners (Rosenthal et al., 2015). The markedly fast spread of behaviors within animal groups-such as waves of response, evasive maneuvers in schools of fish (Rosenthal et al., 2015;Radakov, 1973;Mateo, Kuan, and Bouffanais, 2017), and collective turns in flocks of starlings (Attanasi et al., 2014c)-has been a source of inquiry for a long time (Radakov, 1973). ...
Thesis
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Collective dynamics underpin many diverse complex systems e.g., animals, humans, and robotic multi-agent systems where a large number of individuals cooperate. The information that allows for such collective behaviors to emerge flows through an interaction network specific to the ongoing process. Naturally, this yields an intricate interplay between the collective dynamics on the one hand and the features of the interaction network on the other. Therefore, it is of paramount importance to understand the effects that network topological features have on the collective dynamics, to understand how these systems can produce an effective collective response in the presence of changes in their environment, i.e., swarm intelligence. To investigate the influence of the network topology on the collective response, we consider the archetypal leader-follower linear consensus---a distributed deci-\\ sion-making model. Here, we find---through comparing various deterministic graphs and an optimization framework---a nontrivial relationship between the frequency of the driving signal and the optimal network topology. As the pace of the leader increases, the optimal connectivity of the network, in terms of its degree, decreases monotonically. We further demonstrate this rich phenomenology through the use of a swarm of land robots performing a nonlinear heading consensus. As a next step, we go beyond the effects of network degree and study the intricate impact of network clustering and network distance. We find that the flow of information in the leader-follower linear consensus experiences a transition from simple contagion---i.e., based on pairwise interactions---to a complex one---i.e., involving social influence and reinforcement when the pace of the leader increases. We uncover this rich phenomenology---so far limited to threshold-based decision-making processes---and show theoretically that it can be characterized as simple or complex by analyzing the correlations between specific network metrics and the performance of the collective behaviors---here measured as the collective frequency response. We also uncover the complex contagion in a swarm of land robots performing a nonlinear heading consensus. However, limitations with the number of agents led us to develop a large-scale internet-of-things testbed. This large-scale testbed allows us to more fully explore the richness found in the interplay between collective dynamics and network topology as well as tackle some of the challenges that arise in large networked systems. The results presented in this thesis greatly expand our understanding of the effects of network topology on collective dynamics. They have significant ramifications for our understanding of a range of social and animal group behaviors, as well as for the design of cooperative robot systems.
... One of these is the ability to make use of information provided by other individuals in the group. For example: a navigating bird may choose its direction of flight in part by following others in the flock [3,4]; foraging animals can use the presence of others at a site as an indicator of food availability [5,6]; fish can effectively avoid predators by following others who are seeking to do the same [7,8]; and demand for consumer items is often driven by their perceived popularity [9], especially amongst high-status individuals [10]. ...
Article
Full-text available
Social animals can improve their decisions by attending to those made by others. The benefit of this social information must be balanced against the costs of obtaining and processing it. Previous work has focused on rational agents that respond optimally to a sequence of prior decisions. However, full decision sequences are potentially costly to perceive and process. As such, animals may rely on simpler social information, which will affect the social behaviour they exhibit. Here, I derive the optimal policy for agents responding to simplified forms of social information. I show how the behaviour of agents attending to the aggregate number of previous choices differs from those attending to just the most recent prior decision, and I propose a hybrid strategy that provides a highly accurate approximation to the optimal policy with the full sequence. Finally, I analyse the evolutionary stability of each strategy, showing that the hybrid strategy dominates when cognitive costs are low but non-zero, while attending to the most recent decision is dominant when costs are high. These results show that agents can employ highly effective social decision-making rules without requiring unrealistic cognitive capacities, and indicate likely ecological variation in the social information different animals attend to.
... Social living can provide animals with substantial benefits (Ward and Webster, 2016), such as protection from predators (Kenward, 1978;Carere et al., 2009;Handegard et al., 2012;Ioannou et al., 2012), enhanced cognitive performance (Ashton et al., 2018) and greater collective-decision accuracy (Prins, 1996;Simons, 2004;Couzin et al., 2005;Berdahl et al., 2018). To retain these wide-ranging benefits, animals have evolved coordination mechanisms, which enable spatial cohesion on the move (Conradt and Roper, 2005;Couzin et al., 2005). ...
Article
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Remaining cohesive on the move can be beneficial for animal groups. As such, animal groups have evolved coordination mechanisms such as leadership to resolve navigational conflicts of interest. Consistent "leaders" may have an intrinsic advantage over "followers" which compromise on their preferred route to retain cohesion, which highlights the question of the inter-individual variation (phenotype) that can predict leadership. Studies in both birds and fish have revealed that intrinsically faster individuals can lead movements, and leading movements propagate from the front edge of the flock/shoal. However, these experiments are generally conducted in relatively "familiar" environments, where the degree of compromise between the "leaders" and "followers" is low. We suggested that inter-individual differences in route efficiency, while not explanatory of leadership from familiar locations, may emerge as predictors of leadership from unfamiliar locations. We tested this prediction-and the potential impact of multiple other behavioral, morphological and "in-flight" phenotypes on leadership-using two groups of homing pigeons (Columba livia) (N = 16), a classic model species of leadership. We recorded N = 966 unique GPS trajectories from birds in (i) solo and familiar, and (ii) solo and unfamiliar contexts to measure solo speed and solo route efficiency; and (iii) group and familiar, and (iv) group and unfamiliar contexts to assess group leadership. Pigeon leadership hierarchies were similar across environmental context (i.e., familiarity). However, we found that no covariates could consistently predict leadership score in either context.
... Acoustic methods are less affected by the properties of water in which they are deployed (e.g. turbidity) and have been widely used in studies of fish community structure, biomass, behaviour and group dynamic studies (Becker et al., 2017(Becker et al., , 2011Handegard et al., 2012;Martignac et al., 2015). However, acoustic techniques for aquatic faunal identification often describe the difficulties faced (Charef et al., 2010;Lefeuvre et al., 2000;Scalabrin et al., 1996) with some research concluding that when used in isolation acoustic tools are not adequate for accurate identification (Horne, 2000). ...
Article
Assessment and monitoring of marine biodiversity, including fish populations, is essential for evidence-based conservation management of coastal marine resources. The effectiveness of monitoring techniques for stock assessment varies with sea conditions. In dynamic marine environments with high turbidity, such as those found in estuaries, mangroves, coastal straits, fjords, and bays, traditional assessment methods include the use of destructive techniques such as trawling. Hydroacoustic sampling techniques overcome such restrictions, equipment such as echosounders have commonly been used for biodiversity assessments including fish community structure, biomass, behaviour, and dynamics studies. However, hydroacoustic methods have been shown to be less reliable for species identification. The high frequency Adaptive Resolution Imaging Sonar (ARIS) is widely used for underwater object detection and imaging. Our study investigated the suitability of ARIS 3000 for the species identification of North-East Atlantic marine species using experimental aquarium studies, field surveys and multi investigator assessments. Aquaria results showed that 82 % of species were detected by observers, of which five were identified correctly identified consistently. The remaining four species were identified correctly <67 % of the time. During field surveys, a 150 % higher confidence in identification was given to more morphologically distinct groups such as elasmobranchs. Whilst our results highlight the suitability of the ARIS for accurate and repeatable identification of some of the model species used in this study, we have also shown that factors such as size and morphological traits limit the accuracy of identification for all species. We suggest that monitoring techniques combine the use of ARIS sonars alongside other sampling tools for assessing motile faunal communities.
... Similarly, transitions and criticality have been studied in various other biological contexts, ranging from neural activity and brain networks [12,[15][16][17][18] to gene regulatory networks [19] to collective behavior of cells [20]. In the context of animal collectives, signatures of near-criticality have been found in experiments in bird flocks [21], mammals [11], insects [22,23] and fish schools [24], while theoretical models have investigated maximal sensitivity of the system at the critical regime [25][26][27][28]. The possible benefits of criticality to animals within collectives has predominantly been considered with respect to maximal sensitivity or flexibility of the system or the appearance of long-ranged correlations within it [29]. ...
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Living systems such as neuronal networks and animal groups process information about their environment via the dynamics of interacting units. These can transition between distinct macroscopic behaviors. Near such a transition (or critical point) collective computation is generally thought to be optimized, due to the associated maximal sensitivity to perturbations and fast dissemination of information. For biological systems, however, optimality depends on environmental context, making the flexible, context-dependent adoption of different distances to a critical point potentially more beneficial than its unique properties. Here, studying escape waves in schooling fish at two levels of perceived environmental risk, we investigate a) if and how distance to criticality is regulated in response to environmental changes and b) how the individual level benefits derived from special properties of the critical point compare to those achieved via regulation of the group's distance to it. We find that the observed fish schools are subcritical (not maximally responsive and sensitive to environmental cues), but decrease their distance to criticality with increased perceived risk. Considering an individual's hypothetical costs of two detection error types, we find that optimal distance to criticality depends on the riskiness and noisiness of the environment, which may explain the observed behavior. Our results highlight the benefit of evaluating biological consequences of different distances to criticality for individuals within animal collectives. This provides insights into the adaptive function of a collective system and motivates future questions about the evolutionary forces that brought the system to make this particular trade-off.
... Extensions of this model could also be applied to consider predator-prey interactions between multiple predators or prey. For example, some predators hunt in groups (Handegard et al. 2012), which may improve their capture success because a well-timed evasive maneuver against one predator may be poorly timed with respect to other approaching predators. Conversely, the interception abilities of predators that hunt groups of prey may be diminished by disruptions to proportional navigation when the focal prey becomes temporarily occluded by other prey, providing a mechanistic basis for the so-called 'confusion effect' (Landeau and Terborgh 1986). ...
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The rates of interactions between predators and prey are fundamental to population and food web dynamics. Yet, most ecological theory of predator–prey interaction rates deals exclusively with the first phase of an interaction, an encounter, and not the second phase, a capture or escape. Here, we present a simple dynamical model of prey capture that incorporates empirically observed behavioral strategies of pursuit by predators and evasion by prey. We parameterize the model with data from aquatic systems and analyze its dynamics. Our results show that empirically observed outcomes of predator–prey interactions cannot be predicted solely from biomechanical performance traits of predators and prey. Contrary to previous work, we show that it is only through the inclusion of informational constraints – constraints on the rate at which predator and prey process and respond to incoming sensory information – that the full range of empirically observed prey capture rates are predicted by the model. Our analysis also revealed that the outcome of predator–prey interactions can largely be predicted by the product of two measurable traits: the maximum speed of the prey and the sensory‐motor delay that characterizes the time taken for the predator to respond to a change in the relative position of prey. Both of these traits exhibit power‐law scaling with body size, suggesting that simple allometric relationships may characterize the outcome of predator–prey interactions across species. More broadly, our results suggest that informational constraints can have a dominant effect on predator–prey interactions, and that these traits should be considered alongside biomechanical performance to capture the fundamental properties of predator–prey interactions in nature.
... Flying in formation may provide birds with an aerodynamic advantage relative to solo flight, but has also been proposed to serve a social function [96]. Swimming in schools serves an antipredatory purpose [98], and improves efficient foraging activity [97]. In rough-toothed dolphins (Steno bredanensis), synchronized swimming is thought to be an energetic travelling adaptation that also facilitates eavesdropping [99]. ...
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In this perspective paper, we focus on the study of synchronization abilities across the animal kingdom. We propose an ecological approach to studying nonhuman animal synchronization that begins from observations about when, how and why an animal might synchronize spontaneously with natural environmental rhythms. We discuss what we consider to be the most important, but thus far largely understudied, temporal, physical, perceptual and motivational constraints that must be taken into account when designing experiments to test synchronization in nonhuman animals. First and foremost, different species are likely to be sensitive to and therefore capable of synchronizing at different timescales. We also argue that it is fruitful to consider the latent flexibility of animal synchronization. Finally, we discuss the importance of an animal's motivational state for showcasing synchronization abilities. We demonstrate that the likelihood that an animal can successfully synchronize with an environmental rhythm is context-dependent and suggest that the list of species capable of synchronization is likely to grow when tested with ecologically honest, species-tuned experiments. This article is part of the theme issue ‘Synchrony and rhythm interaction: from the brain to behavioural ecology’.
... The development of mathematical models of populations of marine species that live in groups has also been developed by recent studies. If the fish population is large, then a model that takes into account the characteristics of the group will be more suitable for natural conditions, when compared to one that ignores the characteristics of the group [12]. These assumptions have become the basis of the research in this article. ...
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This paper, the model considered is a predator-prey model for an exploited population. Predator and prey species in the offered concept have schooling characteristics. The characteristics of schooling are very similar to behavior in natural ecosystems. Based on the equilibrium analysis obtained five equilibrium points. The equilibrium point is the only one that satisfies the equilibrium model based on the Routh-Hurwitz criteria. Meanwhile, harvesting effort using the chosen equilibrium point was also calculated in the study. The principle of bionomic equilibrium is a method of showing the results of harvesting as a parameter control. Numerical simulations are also carried tor to validate the findings in the research discussion. Parameters taken from assumptions and references become important and critical references. Trajectories show a population of prey and predator one population that continues to be sustainable despite harvesting efforts. Meanwhile, different trajectories are shown by the population of two predators, which experienced a decrease in population growth. Harvesting attempts carried out on predator two continuously until a certain time will result in serious extinctions.
... 4.1 demonstrate the social cohesiveness of the GIM-C model. Existing empirical research has shown that such social cohesiveness benefits agents in different ways (Foster and Treherne 1981;Handegard et al. 2012;Krause et al. 2002;Milinski 1984;Ward et al. 2008). Some parameters that affect the decision pattern of GIM-C are also investigated in Sects. ...
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For decades, both empirical and theoretical models have been proposed to explain the patterns and mechanisms of collective decision-making (CDM). The most-studied CDM scenario is the best-of-n problem in a static environment. However, natural environments are typically dynamic. In dynamic environments, the visual occlusions produced by other members of a large-scale group are also common. Hence, some agents of a group are less informed than others, and their state uncertainties increase. This paper develops a new model referred to as the generalized Ising model with dynamic confidence (GIM-C) to reduce the state uncertainty induced by visual occlusions. The proposed model first estimates the expected rewards of possible actions with dynamic confidence weighting. It then gives the probability of choosing each action based on the generalized Ising model with an external field defined by the last stage’s results. Numerical simulations demonstrate that GIM-C shares the key feature of social cohesion with previous CDM models. Furthermore, in order to illustrate the efficiency of the proposed GIM-C, the collecting foraging task is considered, where a large-scale group of agents is required to obtain rewards with the presence of a dynamic predator and visual occlusions. The good performance of GIM-C in the collecting foraging task demonstrates that dynamic confidence weighting is efficient in reducing the state uncertainty introduced by visual occlusions. The proposed GIM-C also demonstrates the importance of enhancing the influence of informed agents in CDM problems in a dynamic environment with visual occlusions.
... Animals coordinate their behavior with other individuals for benefits, including increased opportunities to mate, greater migratory and foraging efficiency, less chance of being attacked, and better energy costs (Handegard et al., 2012;Berdahl et al., 2013;Jolles et al., 2019). Several researchers have focused their research on the study of the neurogenetic bases of collective behavior in order to understand how individuals can form complex social networks among themselves, improving their survival as occurs in social animals like fishes, ducks, bees, or flies (Becher et al., 2010;Bialek et al., 2014;Ramdya et al., 2017). ...
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Among individuals, behavioral differences result from the well-known interplay of nature and nurture. Minute differences in the genetic code can lead to differential gene expression and function, dramatically affecting developmental processes and adult behavior. Environmental factors, epigenetic modifications, and gene expression and function are responsible for generating stochastic behaviors. In the last decade, the advent of high-throughput sequencing has facilitated studying the genetic basis of behavior and individuality. We can now study the genomes of multiple individuals and infer which genetic variations might be responsible for the observed behavior. In addition, the development of high-throughput behavioral paradigms, where multiple isogenic animals can be analyzed in various environmental conditions, has again facilitated the study of the influence of genetic and environmental variations in animal personality. Mainly, Drosophila melanogaster has been the focus of a great effort to understand how inter-individual behavioral differences emerge. The possibility of using large numbers of animals, isogenic populations, and the possibility of modifying neuronal function has made it an ideal model to search for the origins of individuality. In the present review, we will focus on the recent findings that try to shed light on the emergence of individuality with a particular interest in D. melanogaster .
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Shoaling, the formation of social groupings in fish, can provide benefits including reduced predation risk. However, it can also inflict costs including increased competition for resources, transmission of parasites, and salience to predators. Trinidadian guppies exhibit inter-population variation in shoaling behavior where individuals coexisting with large piscivorous predators (high predation localities) spend most of their time in shoals and those coexisting with an ambush predator, Rivulus hartii (recently, Anablepsoides hartii), that preys primarily on smaller guppies (low predation localities) do not. It has been suggested that this predator selects for reduced shoaling because doing so reduces salience to the predator. Here, as far as we know, we perform the first test of this idea. First, we investigated the effectiveness of shoaling in encounters with this predator. In survival trials, where one rivulus interacted with a group of guppies, we found that the predator was more likely to attack individuals in shoals than singletons. However, we also found that attacks directed at shoals were less likely to succeed. This suggests that the optimal strategy for guppies co-existing with this predator is to reduce shoaling to reduce the probability of being attacked, and to form shoals when an attack is initiated. We then asked if guppies modified their shoaling behavior in response to visual and olfactory cues from this predator during development. We found changes in guppy behavior in response to the treatment: guppies increased shoaling behavior when there was heightened risk of predation.
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How does the spread of behavior affect consensus-based collective decision-making among animals, humans or swarming robots? In prior research, such propagation of behavior on social networks has been found to exhibit a transition from simple contagion—i.e, based on pairwise interactions—to a complex one—i.e., involving social influence and reinforcement. However, this rich phenomenology appears so far limited to threshold-based decision-making processes with binary options. Here, we show theoretically, and experimentally with a multi-robot system, that such a transition from simple to complex contagion can also bed observed in an archetypal model of distributed decision-making devoid of any thresholds or nonlinearities. Specifically, we uncover two key results: the nature of the contagion—simple or complex—is tightly related to the intrinsic pace of the behavior that is spreading, and the network topology strongly influences the effectiveness of the behavioral transmission in ways that are reminiscent of threshold-based models. These results offer new directions for the empirical exploration of behavioral contagions in groups, and have significant ramifications for the design of cooperative and networked robot systems. In consensus-based collective dynamics, the occurrence of simple and complex contagions shapes system behavior. The authors analyze a transition from simple to complex contagions in collective decision-making processes based on consensus, and demonstrate it with a swarm robotic system.
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Pattern formation and collective behaviour in animal aggregations is highly complex and occurs across many scales, over a wide range of environmental conditions. The patterns found in collective behaviour may be modulated by the environmental habitat in which a group is located. Here, we consider whether habitat context influences the collective behaviour of fish schools under threat of predation in a dynamic salt marsh system. By comparing collective responses of wild forage fish prior to and during predator attack across three environmental contexts, we examine whether schooling state is influenced by the habitat that fish schools reside in. Our results indicate that habitat context had a much stronger effect on collective state relative to predation. The habitats studied (both a marsh edge habitat and a higher complexity habitat) induced changes in the behavioural state of fish schools compared to a free-field context, which demonstrates an alteration of the collective behaviours performed by the school. This suggests that other ecological factors, such as the local environment, plays a larger role than predation risk in structuring the spatial and temporal group level patterns found in collective behaviour.
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The beautiful dynamic patterns and coordinated motion displayed by groups of social animals are a beautiful example of self-organization in natural farfrom-equilibrium systems. Recent advances in active-matter physics have enticed physicists to begin to consider how their results can be extended from microscale physical or biological systems to groups of real, macroscopic animals. At the same time, advances in measurement technology have led to the increasing availability of high-quality empirical data for the behavior of animal groups both in the laboratory and in the wild. In this review, I survey this available data and the ways that it has been analyzed. I then describe how physicists have approached synthesizing, modeling, and interpreting this information, both at the level of individual animals and at the group scale. In particular, I focus on the kinds of analogies that physicists have made between animal groups and more traditional areas of physics.
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Theoretical physics predicts optimal information processing in living systems near transitions (or pseudo-critical points) in their collective dynamics. However, focusing on potential benefits of proximity to a critical point, such as maximal sensitivity to perturbations and fast dissemination of information, commonly disregards possible costs of criticality in the noisy, dynamic environmental contexts of biological systems. Here, we find that startle cascades in fish schools are subcritical (not maximally responsive to environmental cues) and that distance to criticality decreases when perceived risk increases. Considering individuals' costs related to two detection error types, associated to both true and false alarms, we argue that being subcritical, and modulating distance to criticality, can be understood as managing a trade-off between sensitivity and robustness according to the riskiness and noisiness of the environment. Our work emphasizes the need for an individual-based and context-dependent perspective on criticality and collective information processing and motivates future questions about the evolutionary forces that brought about a particular trade-off.
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Coordinated and ordered collective behaviors that emerge from decentralized and local self-organizing interactions among individuals widely exists in many biological groups. The classical models often focus on the imitation of biological phenomena with the given position and velocity, but ignore the modeling of individual perception during the emergence of collective behaviors. Based on the mechanism of visual perception, we present a model named visual perception-decision-propulsion (VPDP) and clearly define several evaluation indicators to explore the emergence of collective obstacle avoidance in flocks. Within this model, there is no centralized control and no information exchange among individuals. Instead, individuals interacting with others merely rely on the perceptual information represented by whether the visual field is occupied by neighbors. We demonstrate that our model effectively achieves collective obstacle avoidance, preserving a safe distance between individuals and obstacles while maintaining relatively good coherence. Moreover, the sensitivity analysis of the parameters indicates the robustness of our VPDP model. Hence, this paper provides a novel model for collective obstacle avoidance based on visual perception as well as a detailed analysis.
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Collective behaviour, such as shoaling in fish, benefits individuals through a variety of activities such as social information exchange and anti-predator defence. Human driven disturbance (e.g. anthropogenic noise) is known to affect the behaviour and physiology of individual animals, but the disruption of social aggregations of fish remains poorly understood. Anthropogenic noise originates from a variety of activities and differs in acoustic structure, dominant frequencies, and spectral complexity. The response of groups of fish may differ greatly, depending on the type of noise, and how it is perceived (e.g. threatening or attractive). In a controlled laboratory study, high resolution video tracking in combination with fine scale acoustic mapping was used to investigate the response of groups of European minnows (Phoxinus phoxinus) to signals of differing acoustic complexity (sinewave tones vs octave band noise) under low (150 Hz) and high (2200 Hz) frequencies. Fish startled and decreased their mean group swimming speed under all four treatments, with low frequency sinewave tones having the greatest influence on group behaviour. The shoals exhibited spatial avoidance during both low frequency treatments, with more time spent in areas of lower acoustic intensity than expected. This study illustrates how noise can influence the spatial distribution and social dynamics within groups of fish, and due to the high potential for freshwater aquatic environments to be influenced by anthropogenic activity, wider consequences for populations should be further investigated.
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A relatively simple and local interaction between individuals produces coordinated and ordered collective behaviors that are widespread at all levels of biological groups. Group chase and escape is an important aspect in the field of collective behavior, particularly in regard to predation events in species interactions. Compared with other aspects of collective behavior, less research has been performed on this aspect, and the existing models are constructed only from the phenomenological perspective. We present an individual-based model named Visual Perception-Decision-Propulsion to explore the group chase and escape of biological groups and define several evaluation indicators to assess different aspects of this problem. Within this model, 2 types of self-propulsion individuals, i.e., predators and prey, are considered, and we consider the alignment and repulsion term between homogeneous individuals. Chase and escape are described as the escape (or chase) term between heterogeneous individuals. Based on the model, we identify and distinguish between 2 capture patterns, i.e., cooperative capture and separative capture. Then, we control the internal parameters to analyze the condition of these 2 patterns for production, and the external empirical parameters are adjusted to explore their effect on these 2 patterns. Hence, this paper provides a novel model for group chase and escape based on biological vision to compensate for the shortcomings of classical models and help apply the characteristics of biological groups to human-made swarm systems in the case of confrontation.
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Many prey species have evolved collective responses to avoid predation. They rapidly transfer information about potential predators to trigger and coordinate escape waves. Predation avoidance behaviour is often manipulated by trophically transmitted parasites, to facilitate their transmission to the next host. We hypothesized that the presence of infected, behaviourally altered individuals might disturb the spread of escape waves. We used the tapeworm Schistocephalus solidus, which increases risk-taking behaviour and decreases social responsiveness of its host, the three-spined stickleback, to test this hypothesis. Three subgroups of sticklebacks were placed next to one another in separate compartments with shelter. The middle subgroup contained either uninfected or infected sticklebacks. We confronted an outer subgroup with an artificial bird strike and studied how the escape response spread through the subgroups. With uninfected sticklebacks in the middle, escape waves spread rapidly through the entire shoal and fish remained in shelter thereafter. With infected sticklebacks in the middle, the escape wave was disrupted and uninfected fish rarely used the shelter. Infected individuals can disrupt the transmission of flight responses, thereby not only increasing their own predation risk but also that of their uninfected shoal members. Our study uncovers a potentially far-reaching fitness consequence of grouping with infected individuals.
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Group living is a common strategy used by fishes to improve their fitness. While sociality is associated with many benefits in natural environments, including predator avoidance, this behaviour may be maladaptive in the Anthropocene. Humans have become the dominant predator in many marine systems, with modern fishing gear developed to specifically target groups of schooling species. Therefore, ironically, behavioural strategies which evolved to avoid non-human predators may now actually make certain fish more vulnerable to predation by humans. Here, we use an individual-based model to explore the evolution of fish schooling behaviour in a range of environments, including natural and human-dominated predation conditions. In our model, individual fish may leave or join groups depending on their group-size preferences, but their experienced group size is also a function of the preferences of others in the population. Our model predicts that industrial fishing selects against individual-level behaviours that produce large groups. However, the relationship between fishing pressure and sociality is nonlinear, and we observe discontinuities and hysteresis as fishing pressure is increased or decreased. Our results suggest that industrial fishing practices could be altering fishes’ tendency to school, and that social behaviour should be added to the list of traits subject to fishery-induced evolution.
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Quantifiable estimates of predator–prey interactions and relationships in aquatic habitats are difficult to obtain and rare, especially when individuals cannot be readily observed. To overcome this observational impediment, imaging sonar was used to assess the cooccurrence of predator-size fish and juvenile salmonids, Oncorhynchus spp., at the entrance to a floating surface collector (FSC) in the forebay of North Fork Dam on the Clackamas River, Oregon (USA). Imaging sonar can be used to transform active sound waves into visual data, making it possible to obtain continuous underwater observations on the presence and interspecific interactions between predator-size fish and prey (juvenile salmonids). Hourly counts of smolt-size fish tracks, diel phase, water clarity and river discharge were used as covariates within a zero-inflated Poisson model to determine how these factors may influence the number of predators in front of the FSC. Both the number of smolt-size fish tracks and diel phase had the strongest effects on the number of predator-size fish tracks, with more predator- size fish tracks observed during the daytime, and as the number of smolt-size fish tracks increased. Additionally, the presence of predator-size fish may affect the abundance and direction of travel of juvenile salmonids, as fewer smolt-size fish were observed when predators were present, and a greater proportion of smolt-size fish were observed travelling away from the FSC when predator-size fish were present. This study provides estimates of predator and prey fish abundance in the vicinity of surface collection systems at moderate-sized hydropower projects and could help resource managers better understand mechanisms that can influence the survival and passage behaviour of juvenile salmonids using surface collection structures at dams.
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Males of many species display conspicuous colors to attract mates and deter rivals, although this benefit can incur an increased predation risk. In the African cichlid fish, Astatotilapia burtoni, males can change both their social status (dominant, DOM, or subordinate, SUB) and primary body color (yellow or blue). We hypothesized that these phenotypes vary in conspicuousness to predators and conspecifics, thus establishing a trade-off between intraspecific signaling and predation. We quantified the spectral reflectance of yellow and blue DOM and SUB males. We then constructed avian and conspecific visual receiver models to determine the relative conspicuousness of each phenotype. We show that there are significant differences in conspicuousness to predators and conspecifics, with the flanks of the yellow DOM males exhibiting more spectral contrast to both avian predators and conspecifics than the flanks of blue DOM males. Our measurements of escape behavior revealed that each morph exhibits distinct anti-predatory responses, with SUB males shoaling for protection, and the more conspicuous yellow DOM males executing more escape responses, potentially compensating for their increased conspicuousness. Our results suggest a novel mechanism for the maintenance of alternative male phenotypes in this species, where dynamically enhanced conspicuousness is offset by plastic changes in behavior.
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Organisms living in hot, arid environments face important risks associated with hyperthermia and dehydration which are expected to become more severe with climate change. To mitigate these risks, individuals often modify behaviour, e.g. reducing activity and seeking shade. These behavioural modifications may affect interactions between individuals, with consequences for the social structure of groups. We tested whether the social structure of cooperative groups of sociable weavers (Philetairus socius ) varied with environmental temperature. We recorded the nature and frequency of interactions at feeders positioned beneath three sociable weaver colonies (N = 49 identified birds) in the Kalahari Desert with respect to environmental temperatures over a 30‐day period. Using random forest models, we examined whether thermal conditions predicted variation in social network structure. We also conducted focal observations of individual weavers to assess functional links between temperature, intensity of heat dissipation behaviour (panting), and immediate effects on social behaviour. Our results suggest that the social structure of weaver colonies becomes less cohesive and more fragmented at extreme and variable environmental temperatures. These changes in network structure appear to be linked with individuals’ heat dissipation behaviour: extreme and variable temperatures were associated with increased panting, which was significantly correlated with an immediate reduction in the frequency of association. Collectively, our results indicate that interactions within groups could be disturbed by environmental temperature variation and extremes. Changing temperature regimes could therefore affect the functioning of animal societies by altering social networks. This article is protected by copyright. All rights reserved.
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Models of group living assume that the hunting success of predators and per capita predation risk of prey decrease with increasing prey group size. In contrast to numerous studies documenting anti-predator advantages of group living, little is known about the choice of predators for particular prey groups. Two shoals of guppies,Poecilia reticulata, which differed in size (2 versus 5 fish, 5 versus 10, 2 versus 10, 10 versus 16), were simultaneously presented to individual blue acara cichlid fish,Aequidens pulcher, and the shoal that was attacked first, the number of subsequent attacks and the total time cichlids spent near each shoal during a 3-min period were recorded. For all three criteria, the cichlids showed a significant preference for the larger of the two shoals, resulting in a higher per capita risk in terms of first attack and attack duration for individuals in larger shoals. Further trials, in which guppy activity was manipulated by using different water temperatures, showed that the cichlids preferred a smaller over a larger shoal if the larger shoal was kept in cold water (i.e. exhibited less movement). This result demonstrated that the visual conspicuousness of the shoal, and not its size per se, was the key factor for the cichlids' choice of a prey shoal. In a final experiment, wherein cichlids were given an opportunity to attack free-swimming shoals (comprised 1-8 individuals), predator hunting success decreased with increasing shoal size. We conclude that, despite the over-proportionately high attack risk for individuals in large shoals, per capita predation risk is lower than in small shoals, and joining larger shoals should be advantageous for individual guppies. Cichlids, however, would do better in terms of hunting success by attacking small rather than large shoals. Potential implications of such predator preference for larger shoals are discussed.
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Forty years ago, May proved that sufficiently large or complex ecological networks have a probability of persisting that is close to zero, contrary to previous expectations. May analysed large networks in which species interact at random. However, in natural systems pairs of species have well-defined interactions (for example predator-prey, mutualistic or competitive). Here we extend May's results to these relationships and find remarkable differences between predator-prey interactions, which are stabilizing, and mutualistic and competitive interactions, which are destabilizing. We provide analytic stability criteria for all cases. We use the criteria to prove that, counterintuitively, the probability of stability for predator-prey networks decreases when a realistic food web structure is imposed or if there is a large preponderance of weak interactions. Similarly, stability is negatively affected by nestedness in bipartite mutualistic networks. These results are found by separating the contribution of network structure and interaction strengths to stability. Stable predator-prey networks can be arbitrarily large and complex, provided that predator-prey pairs are tightly coupled. The stability criteria are widely applicable, because they hold for any system of differential equations.
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Flocking is a typical example of emergent collective behavior, where interactions between individuals produce collective patterns on the large scale. Here we show how a quantitative microscopic theory for directional ordering in a flock can be derived directly from field data. We construct the minimally structured (maximum entropy) model consistent with experimental correlations in large flocks of starlings. The maximum entropy model shows that local, pairwise interactions between birds are sufficient to correctly predict the propagation of order throughout entire flocks of starlings, with no free parameters. We also find that the number of interacting neighbors is independent of flock density, confirming that interactions are ruled by topological rather than metric distance. Finally, by comparing flocks of different sizes, the model correctly accounts for the observed scale invariance of long-range correlations among the fluctuations in flight direction.
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Acoustic noise is known to have a variety of detrimental effects on many animals, including humans, but surprisingly little is known about its impacts on foraging behaviour, despite the obvious potential consequences for survival and reproductive success. We therefore exposed captive three-spined sticklebacks (Gasterosteus aculeatus) to brief and prolonged noise to investigate how foraging performance is affected by the addition of acoustic noise to an otherwise quiet environment. The addition of noise induced only mild fear-related behaviours--there was an increase in startle responses, but no change in the time spent freezing or hiding compared to a silent control--and thus had no significant impact on the total amount of food eaten. However, there was strong evidence that the addition of noise increased food-handling errors and reduced discrimination between food and non-food items, results that are consistent with a shift in attention. Consequently, noise resulted in decreased foraging efficiency, with more attacks needed to consume the same number of prey items. Our results suggest that acoustic noise has the potential to influence a whole host of everyday activities through effects on attention, and that even very brief noise exposure can cause functionally significant impacts, emphasising the threat posed by ever-increasing levels of anthropogenic noise in the environment.
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1. How group size affects predator attack and success rate, and so prey vulnerability, is important in determining the nonlethal consequences of predation risk on animal populations and communities. Theory predicts that both predator attack success rate and the dilution effect decline exponentially with group size and that selection generates optimal group sizes at a ‘risk threshold’ above which antipredation benefits are outweighed by costs, such as those owing to higher attack rates. 2. We examined whether flock size risk thresholds for attack rate, success rate or dilution differed, and therefore whether the strength of selection for group size differed for these three factors, using a system of redshank Tringa totanus flocks being hunted by Eurasian sparrowhawks Accipiter nisus. We also asked which of the three thresholds, on their own or in combination, predicted the most commonly observed group size. 3. Mean redshank flock size increased with a very gradual quadratic function (i.e. approximately linearly) with population size, although at a rate half that possible; when population size was not limiting, individuals almost always avoided flocks of less than 30 and birds were frequently in flocks up to at least 80. Sparrowhawk attack rate showed a quadratic relationship with flock size and peaked at 55 redshanks. Sparrowhawk attack success rate, however, declined exponentially, becoming less steep at flock sizes of about 40 and remaining uniformly low (a 95% decrease) by 70. Combined with dilution, individual risk of death per attack decreased by 95% when group size reached 30 (20 for the dilution effect alone). 4. Redshanks most commonly formed group sizes that gained the maximum individual predation risk reduction. They also commonly formed group sizes far above any further substantial advantages from the dilution effect or from reducing attack rate, but that continued to reduce predation risk by lowering attack success rate. Individuals did not always form the largest groups possible which we suggest is because individual variation in risk-taking subdivides the population. This places a constraint on the ability of individuals to compensate for predation risk and will have a variety of important effects on animal populations.
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Many of life's most fascinating phenomena emerge from interactions among many elements--many amino acids determine the structure of a single protein, many genes determine the fate of a cell, many neurons are involved in shaping our thoughts and memories. Physicists have long hoped that these collective behaviors could be described using the ideas and methods of statistical mechanics. In the past few years, new, larger scale experiments have made it possible to construct statistical mechanics models of biological systems directly from real data. We review the surprising successes of this "inverse" approach, using examples form families of proteins, networks of neurons, and flocks of birds. Remarkably, in all these cases the models that emerge from the data are poised at a very special point in their parameter space--a critical point. This suggests there may be some deeper theoretical principle behind the behavior of these diverse systems.
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Predators and food are the keys to understanding fish shoals; synchronised co-operation defeats predators, and optimal food gathering in shoals reflects a shifting balance between joining, competing in, or leaving the group. In the wild, predators may arrive while shoaling fish are feeding, and so vigilance is a crucial behaviour. Once detected, predator defence takes precedence over feeding, since an animal’s life is worth more than today’s dinner.
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The approach of a predator model induces rapid changes in the locomotory behaviour of individuals at the periphery of flotillas of a marine insect, the ocean skater Halobates robustus Barber. There is an abrupt and substantial increase in velocity, frequency of turning, the number of apparently random encounters between individuals and also the frequency of changes in light reflection from the body surfaces. These behavioural responses are postulated to cause predator confusion and, less frequently, to initiate rapid, synchronous dispersal of the flotillas. Interactions between individuals in the flotillas mediate a rapid transmission of avoidance behaviour through the flotilla which, in our field experiments, greatly exceeded the speed of approach of a predator model. This behaviour (named the Trafalgar Effect) enables individuals to initiate avoidance behaviour before the approaching predator can be seen.
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Bird flocking is a striking example of collective animal behaviour. A vivid illustration of this phenomenon is provided by the aerial display of vast flocks of starlings gathering at dusk over the roost and swirling with extraordinary spatial coherence. Both the evolutionary justification and the mechanistic laws of flocking are poorly understood, arguably because of a lack of data on large flocks. Here, we report a quantitative study of aerial display. We measured the individual three-dimensional positions in compact flocks of up to 2700 birds. We investigated the main features of the flock as a whole (shape, movement, density and structure) and we discuss these as emergent attributes of the grouping phenomenon. Flocks were relatively thin, of various sizes, but constant proportions. They tended to slide parallel to the ground and, during turns, their orientation changed with respect to the direction of motion. Individual birds kept a minimum distance from each other that was comparable to their wing span. The density within the aggregations was nonhomogeneous, as birds were packed more tightly at the border than the centre of the flock. These results constitute the first set of large-scale data on three-dimensional animal aggregations. Current models and theories of collective animal behaviour can now be tested against these data.
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Flocks of dunlin (Calidris alpina) were filmed during rapid aerial manoeuvres. Two types of manoeuvres were identified: (a) course-change movements in which the entire flock altered course, and (b) rotation movements in which individual birds rotated on their sagittal axes without necessarily changing direction. Either manoeuvre could make a flock's overall appearance shift suddenly from light to dark (or vice versa) as the birds oriented first with their light ventral, then with their dark dorsal, plumage toward the observer. Slow-motion analysis revealed that the average time required by a majority of birds in camera view to change orientations during a manoeuvre was 196 ms (sd=137 ms). ‘Self-generated synchrony’ is a possible mechanism for this highly coordinated group behaviour.
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During predator–prey encounters, a high locomotor performance in unsteady manoeuvres (i.e. acceleration, turning) is desirable for both predators and prey. While speed increases with size in fish and other aquatic vertebrates in continuous swimming, the speed achieved within a given time, a relevant parameter in predator–prey encounters, is size independent. In addition, most parameters indicating high performance in unsteady swimming decrease with size. Both theoretical considerations and data on acceleration suggest a decrease with body size. Small turning radii and high turning rates are indices of manoeuvrability in space and in time, respectively. Manoeuvrability decreases with body length, as minimum turning radii and maximum turning rates increase and decrease with body length, respectively. In addition, the scaling of linear performance in fish locomotion may be modulated by turning behaviour, which is an essential component of the escape response. In angelfish, for example, the speed of large fish is inversely related to their turning angle, i.e. fish escaping at large turning angles show lower speed than fish escaping at small turning angles. The scaling of unsteady locomotor performance makes it difficult for large aquatic vertebrates to capture elusive prey by using whole-body attacks, since the overall manoeuvrability and acceleration of small prey is likely to be superior to that of large predators. Feeding strategies in vertebrate predators can be related to the predator–prey length ratios. At prey–predator ratios higher than approximately 10−2, vertebrate predators are particulate feeders, while at smaller ratios, they tend to be filter feeders. At intermediate ratios, large aquatic predators may use a variety of feeding methods that aid, or do not involve, whole body attacks. Among these are bubble curtains used by humpback whales to trap fish schools, and tail-slapping of fish by delphinids. Tail slapping by killer whales is discussed as an example of these strategies. The speed and acceleration achieved by the flukes of killer whales during tail slaps are higher and comparable, respectively, to those that can be expected in their prey, making tail-slapping an effective predator behaviour.
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The remarkable collective action of organisms such as swarming ants, schooling fish and flocking birds has long captivated the attention of artists, naturalists, philosophers and scientists. Despite a long history of scientific investigation, only now are we beginning to decipher the relationship between individuals and group-level properties. This interdisciplinary effort is beginning to reveal the underlying principles of collective decision-making in animal groups, demonstrating how social interactions, individual state, environmental modification and processes of informational amplification and decay can all play a part in tuning adaptive response. It is proposed that important commonalities exist with the understanding of neuronal processes and that much could be learned by considering collective animal behavior in the framework of cognitive science.
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Vision is not required in order for fish to school. Five individual saithe, Pollachius virens, were able to join schools of 25 normal saithe swimming in an annular tank, while blinded with opaque eye covers. Test fish maintained position within the school indefinitely and responded to short-term movements of individuals within the school, although quantitative differences in reaction time and schooling behavior were noted. Five fish with lateral lines cut at the opercula were unable to school when wearing opaque eye covers. Although it is unlikely that blind saithe could school in the wild, the constraints of the apparatus permitted a demonstration of a role of the lateral line organ in schooling.
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One commonly cited benefit to animals that forage in groups is an increase in the probability of detecting a predator, and a decrease in the time spent in predator detection. A mathematical model (Pulliam 1973) predicts a negative relationship between group size and vigilance rates. Over fifty studies of birds and mammals report that the relationship at least partly explains why individuals forage in groups. This review evaluates the strength of these conclusions based on their evidence. Those variables that may confound the relationship between vigilance and group size are outlined, and their control is assessed for each study. The variables I consider to be important include the density and type of food; competition between individuals; the proximity to both a safe place and the observer; the presence of predators; the visibility within the habitat; the composition of the group; the ambient temperature and the time of day. Based on these assessments, most of the studies fail to adequately demonstrate an unambiguous relationship between vigilance behavior and group size. Nevertheless, many studies reveal interesting features of the relationship between vigilance and group size that should provide fruitful avenues for future research.
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Scaling from individual movement and decision-making to population structure is central to ecology; recent studies of African elephant populations which have taken this approach have shed new light on how complex, multi-level social systems are organized.