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Social Organisation and Information Transfer in Schooling Fish

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Abstract

IntroductionCollective motionEmergent collective motion in the absence of external stimuliResponse to internal state and external stimuli: Information processing within schoolsInformational status, leadership and collective decision-making in fish schoolsThe structure of fish schools and populationsSocial networks and individual identitiesCommunity structure in social networksConclusions and future directionsAcknowledgementsReferences
... In animal groups that move collectively such as fish shoals and bird flocks, individuals are generally understood to use cues from the position and movement of other individuals, rather than intentional signals, to coordinate movement (Ioannou, Couzin, James, Croft, & Krause, 2011;Lemasson et al., 2018). Sudden accelerations or changes of direction may indicate that a neighbour has detected a predator or food, while more gradual changes in speed and direction are likely to indicate the future locations of neighbours (Ioannou, Singh, & Couzin, 2015). ...
... Studies of collective motion are increasingly considering the underlying sensory mechanisms explicitly (Lemasson, Anderson, & Goodwin, 2013;Pita, Moore, Tyrrell, & Fern andez-Juricic, 2015;Strandburg-Peshkin et al., 2013). Vision and the lateral line are the primary sensory inputs used in shoaling by fish (Ioannou et al., 2011), with vision generally accepted to be important for the attraction between neighbours (Partridge & Pitcher, 1980), while the lateral line modulates repulsion to avoid collisions (Faucher et al., 2010). ...
... There is growing interest in studying the effects of multiple stressors on animal behaviour (Côt e et al., 2016;Harding et al., 2019), particularly as anthropogenic activity is increasingly recognized as having effects on multiple environmental parameters (Halfwerk & Slabbekoorn, 2015). Collective behaviour is particularly important for fish (Ioannou et al., 2011) and aquatic habitats are particularly vulnerable to multiple stressors (Ormerod, Dobson, Hildrew, & Townsend, 2010). For example, climate change increases both acidification through dissolved carbon dioxide and water temperature (Pistevos et al., 2017). ...
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Collective movement is critical to the survival of some animals. Despite substantial progress in understanding animal collectives such as fish shoals and bird flocks, it is unknown how collective behaviour is affected by changes in multiple environmental conditions that can interact as stressors. Using a fully factorial repeated-measures design, we tested the independent and combined effects of darkness and acoustic noise on the collective motion of three-spined sticklebacks, Gasterosteus aculeatus, quantified using high-resolution tracking data from video. Corresponding to the importance of vision in shoaling behaviour, darkness increased nearest-neighbour distances and reduced coordination, measured as speed correlations and differences in directional heading between nearest neighbours. Although individual swimming speeds were not impacted by darkness, the group's centre of mass was slower, an emergent effect of reduced polarisation (i.e. greater group disorder) in darkness. While additional acoustic noise had no detectable effect on these variables, it altered group structure, with fish being more likely to be found side by side one another. Fish were also further from the arena wall (i.e. showed reduced wall following) when there was additional acoustic noise. There was only weak evidence for additive or interactive effects of the two stressors. Across the different environmental contexts, there were consistent, repeatable differences between groups (i.e. group personality variation) in the speed, turning angle and distance from the arena wall of individuals, but the only collective behaviour that was repeatable was group polarization. Our study demonstrates that multiple stressors can have independent effects that impact different aspects of behaviour and highlights the need for empirical studies on multiple stressors as their effects can be unpredictable.
... Information acquisition and the associated cognitive tasks necessary for decision-making processes can be accomplished by individual fish, but can be performed more efficiently when animals form groups (Giraldeau, 1984;Ioannou et al., 2011). A group is viewed as a collection of individuals who may have to compromise their own motives to conform to a mean group level behaviour (Brown and Irving, 2014). ...
... For example, single golden shiners perform poorly when tested under different light conditions for their preferred habitat, but the task is solved more easily when in groups as a result of social dynamics (Berdahl et al., 2013). Schooling behaviour may thus represent an alternative evolutionary strategy for solving complex problems compared with developing a more advanced individual cognitive ability (Ioannou et al., 2011). Future cognitive assays on the polarization selection lines will target aspects of cognition that more closely adhere to decision-making in a collective motion context. ...
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The evolution of collective behaviour has been proposed to have important effects on individual cognitive abilities. Yet, in what way they are related remains enigmatic. In this context, the ‘distributed cognition’ hypothesis suggests that reliance on other group members relaxes selection for individual cognitive abilities. Here, we test how cognitive processes respond to evolutionary changes in collective motion using replicate lines of guppies ( Poecilia reticulata ) artificially selected for the degree of schooling behaviour (group polarization) with >15% difference in schooling propensity. We assessed associative learning in females of these selection lines in a series of cognitive assays: colour associative learning, reversal-learning, social associative learning, and individual and collective spatial associative learning. We found that control females were faster than polarization selected females at fulfilling a learning criterion only in the colour associative learning assay, but they were also less likely to reach a learning criterion in the individual spatial associative learning assay. Hence, although testing several cognitive domains, we found weak support for the distributed cognition hypothesis. We propose that any cognitive implications of selection for collective behaviour lie outside of the cognitive abilities included in food-motivated associative learning for visual and spatial cues.
... Although grouping can be beneficial regardless of coordination level, highly coordinated groups likely provide enhanced benefits to individuals due to increased efficiency of information transfer between group members and enhanced predator confusion. That being said, the mechanisms that link between coordinated movement and individual predation avoidance and foraging efficiency are still not well understood (Ioannou et al. 2011). ...
... Rapid information transfer across well coordinated and cohesive shoals may reduce individual predation risk via early warning about approaching predators (Godin and Morgan 1985;Magurran and Higham 1988;Makris et al. 2006), the coordination of escape waves and manoeuvres during predator attack (Partridge 1980;Pitcher and Wyche 1983;Magurran and Pitcher 1987;Vabø and Nøttestad 1997;Parrish 1999;Axelsen et al. 2001;Gerlotto et al. 2006), and due to enhanced predator confusion (Ioannou et al. 2011). In support of this, Herbert-Read et al. (2017) found that guppies (Poecilia reticulata) from populations with naturally high predation levels formed more cohesive shoals than those from populations with low predation rates, suggesting a direct link between shoal cohesion and predation pressure. ...
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Shoaling behaviour is commonly displayed by fishes and is thought to reduce predation and increase foraging efficiency. Shoaling relies on coordination between individuals, with higher cohesion and alignment among individuals within a shoal providing greater net benefits of this behaviour. Whilst single species often shoal together in conspecific groups, mixed-species shoaling is frequently observed and has been identified as an important determinant of individual fitness for the multiple species involved. Despite their prevalence, the structure of mixed-species shoals and the mechanisms by which individuals gain protection from predators and enhance their foraging efficiency are not as well understood as for single-species shoals. In fact, mixed-species shoals may be less coordinated than single-species shoals, raising the intriguing question of why fishes form mixed-species shoals when this behaviour could be less beneficial than single-species shoaling. Here we used in situ stereo-video techniques to compare within and between shoal differences in cohesion and alignment, for mixed- and single-species shoals containing the tropical vagrant Indo pacific sergeant major damselfish, Abudefduf vaigiensis, in temperate waters. As expected, mixed-species shoals were less aligned than single-species shoals. However, within mixed-species shoals conspecifics were more cohesive and aligned than were heterospecifics, suggesting coordinated single-species subgroups formed within larger mixed-species shoals. The formation of subgroups may mitigate costs associated with differences between species, therefore enhancing benefits of mixed-species shoaling. As such, multiple levels of social structure may exist within mixed-species shoals that could facilitate growth and survival for vagrant A. vaigiensis in temperate regions. More broadly, this research highlights the importance of considering detailed internal structures of mixed-species shoals when trying to understand cost–benefit trade-offs experienced by individuals.
... massaging and cleaning the anemone, aggressively chasing or biting heterospecific competitors, potential eggs predators or anemone predators), to conclude whether or not subordinates may be directly or indirectly assisting with care. Alternatively, subordinates could simply have spent less time far when eggs were present because they were copying the behaviours of their larger group members, preferring to stay close to them to enhance group cohesiveness and reap the benefits of doing so (Ioannou et al. 2011(Ioannou et al. , 2017Paijmans et al. 2019). Furthermore, individuals may display consistency in behavioural traits, as has been shown in other anemonefishes (Wong et al. 2013Barbasch & Buston 2018) and in A. mccullochi with respect to boldness and aggression , which may explain variation in behaviour. ...
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Animals are faced with a fundamental risk-reward trade-off when making decisions about foraging in the presence of predation, yet little is known about how social, reproductive and environmental factors mediate this trade-off. In the marine environment, anemonefishes provide a model system for investigating the determinants of risk–reward trade-offs, because they live in size- and sex-structured groups within protective sea anemones tentacles, yet feed predominantly in the water column where they are at risk of predation. Furthermore, exposure to changing tides means the availability of planktonic food covaries with their risk of predation. Therefore, we examined how tide, sex and status, and the presence of eggs influenced the time that Amphiprion mccullochi spent at different distances from their anemone, a proxy for foraging effort and predation risk. We found that individuals significantly adjusted their time spent far and close to the anemone depending on the tide, status and the presence of eggs, and that these adjustments can be explained in light of threat sensitive behaviour. This study illustrates the relative importance of environmental and social factors on intraspecific variation in foraging and antipredator behaviour and bolsters our understanding of the decision’s individuals make to balance the costs and benefits of foraging over temporal and spatial scales.
... This requires cooperation between the fish in the shoals, where each pays a cost of diving as their contribution to generating the wave, but all fish in the shoal benefit by deterring further attacks. However, in large shoals of fish, like the mollies, individuals often exchange membership between different groups, a pattern known as fission-fusion dynamics 18 . Under these conditions, it would be unexpected that such cooperation could evolve, as this usually requires close relatedness between cooperating individuals or being able to recognise others so that reciprocation can establish 19 . ...
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A new study on fish shows that the patterns collective animal groups display when they are disturbed can dissuade predators from attacking.
... To be clear, this is not to say that there is no emergent cognition. Self-organized processes are paradigmatic models for emergent phenomena, and cognition is no exception at it, for collective behaviors, such as collective motion patterns or collective predator avoidance patterns, do emerge from individual interactions (Ioannou et al., 2011). Individuals do communicate or interact with one another in these selforganized, social processes, but the collective, sometimes emergent outcome relies mostly on individual cognitions trapped in non-linear feedback loops that are characteristic of selforganized processes. ...
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Recently, psychological phenomena have been expanded to new domains, crisscrossing boundaries of organizational levels, with the emergence of areas such as social personality and ecosystem learning. In this contribution, we analyze the ascription of an individual-based concept (personality) to the social level. Although justified boundary crossings can boost new approaches and applications, the indiscriminate misuse of concepts refrains the growth of scientific areas. The concept of social personality is based mainly on the detection of repeated group differences across a population, in a direct transposition of personality concepts from the individual to the social level. We show that this direct transposition is problematic for avowing the nonsensical ascription of personality even to simple electronic devices. To go beyond a metaphoric use of social personality, we apply the organizational approach to a review of social insect communication networks. Our conceptual analysis shows that socially self-organized systems, such as isolated ant trails and bee’s recruitment groups, are too simple to have social personality. The situation is more nuanced when measuring the collective choice between nest sites or foraging patches: some species show positive and negative feedbacks between two or more self-organized social structures so that these co-dependent structures are inter-related by second-order, social information systems, complying with a formal requirement for having social personality: the social closure of constraints. Other requirements include the decoupling between individual and social dynamics, and the self-regulation of collective decision processes. Social personality results to be sometimes a metaphorical transposition of a psychological concept to a social phenomenon. The application of this organizational approach to cases of learning ecosystems, or evolutionary learning, could help to ground theoretically the ascription of psychological properties to levels of analysis beyond the individual, up to meta-populations or ecological communities.
... Larger groups are also statistically more likely to contain individuals that make decisions more rapidly, for example because these individuals are less risk averse (i.e., are bolder (Ioannou & Dall, 2016)), hungrier (Balaban-Feld et al., 2019), or better informed . If these individuals can disproportionately influence group decisions through leadership (Ioannou et al., 2011), decision speed can increase via this 'pool-of-competence' effect (Liker & Bókony, 2009;Morand-Ferron & Quinn, 2011;Bisazza et al., 2014). This mechanism relies on variation between individuals within the group and on faster decision makers disproportionally influencing the outcome, for example through greater confidence in their opinion (Marshall et al., 2017). ...
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While larger groups tend to be better at making decisions, very few studies have explored how ecological variables, including predation pressure, shape how group size affects decision making. Our cross-population study of wild-caught guppies ( Poecilia reticulata ) shows that leading individuals from larger groups made faster decisions when deciding to leave the start area and reach the junction of a Y-maze, which allows for compromise over timing. However, at the junction of the Y when the fish needed to make a mutually exclusive decision that does not allow for compromise, there was no effect of group size in high predation fish on decision speed. In fish from low predation habitats, speed was fastest at the intermediate group size with a decline in speed in the largest group size. These results challenge the view that decision making always improves with group size and shows this effect depends on ecological and decision-making conditions.
... Group-living in fishes is strongly linked to foraging efficiency and predator avoidance Paijmans et al. 2019;Ward et al. 2020). Fish shoals often exhibit fission-fusion dynamics where individuals switch between groups (Hoare and Krause 2003;Ioannou et al. 2011) except in some species such as the daffodil cichlid (Neolamprologus pulcher), which live in stable societies (Taborsky et al. 2005). Shoal size, species composition, body size, familiarity and competitive ability of shoal mates are common criteria used for choosing shoals (Kleinhappel et al. 2016; Bartolini et al. 2016;Seguin and Gerlai 2017;Marlin et al. 2019). ...
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Many piscine species form fission-fusion societies where decisions to leave or join a shoal are influenced by factors such as shoal size, familiarity and species. Individuals exhibit distinct shoaling preferences based on behavioural traits such as boldness and sociability. In this study, we examined the link between shoaling decisions and behavioural traits in a hatchery reared population of an endangered megafish, the Deccan mahseer (Tor khudree). We found that this fish exhibits preference for larger shoals when presented with choices of 2 vs 4 and 2 vs 8 shoal sizes. However, no preference for isolated familiar or unfamiliar conspecifics over invasive heterospecifics was observed. Moreover, individual shoaling preferences did not correlate with their boldness or sociability. These results suggest that juvenile hatchery reared mahseers reintroduced into natural habitats may shoal with invasive species and modifying their social behaviour by amending rearing practices could improve outcomes of restocking interventions.
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Collective behaviors in biological systems such as coordinated movements have important ecological and evolutionary consequences. While many studies examine within‐species variation in collective behavior, explicit comparisons between functionally similar species from different taxonomic groups are rare. Therefore, a fundamental question remains: how do collective behaviors compare between taxa with morphological and physiological convergence, and how might this relate to functional ecology and niche partitioning? We examined the collective motion of two ecologically similar species from unrelated clades that have competed for pelagic predatory niches for over 500 million years—California market squid, Doryteuthis opalescens (Mollusca) and Pacific sardine, Sardinops sagax (Chordata). We (1) found similarities in how groups of individuals from each species collectively aligned, measured by angular deviation, the difference between individual orientation and average group heading. We also (2) show that conspecific attraction, which we approximated using nearest neighbor distance, was greater in sardine than squid. Finally, we (3) found that individuals of each species explicitly matched the orientation of groupmates, but that these matching responses were less rapid in squid than sardine. Based on these results, we hypothesize that information sharing is a comparably important function of social grouping for both taxa. On the other hand, some capabilities, including hydrodynamically conferred energy savings and defense against predators, could stem from taxon‐specific biology.
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Cognitive abilities were studied in rainbow trout, the first continental fish production in Europe. Increasing public concern for the welfare of farmed-fish species highlighted the need for better knowledge of the cognitive status of fish. We trained and tested 15 rainbow trout with an operant conditioning device composed of self-feeders positioned in front of visual stimuli displayed on a screen. The device was coupled with a two-alternative forced-choice (2-AFC) paradigm to test whether rainbow trout can discriminate 2-D photographs of conspecifics (S+) from different visual stimuli (S-). The S- were applied in four stages, the last three stages representing increasing discrimination difficulty: (1) blue shapes; (2) black shape (star); (3) photograph of an object (among a pool of 60); (4) photograph of another fish species (among a pool of 60). Nine fish (out of 15) correctly managed to activate the conditioning device after 30–150 trials. The rainbow trout were able to discriminate images of conspecifics from an abstract shape (five individuals out of five) or objects (four out of five) but not from other fish species. Their ability to learn the category "fish shape" rather than distinguishing between conspecifics and heterospecifics is discussed. The successful visual discrimination task using this complex operant conditioning device is particularly remarkable and novel for this farmed-fish species, and could be exploited to develop cognitive enrichments in future farming systems. This device can also be added to the existing repertoire of testing devices suitable for investigating cognitive abilities in fish. https://rdcu.be/cdmZX
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There is no information on whether the daily foraging movements of fish shoals are the result of chance, the collective will of all shoalmates, or the leadership of a few individuals. This study tested the latter possibility. Shoals of 12 golden shiners, Notemigonus crysoleucas, were trained to expect food around midday in one of the brightly lit corners of their tank. They displayed daily food-anticipatory activity by leaving the shady area of their tank and spending more and more time in the food corner up to the normal time of feeding. Past this normal time they remained in the shade, even on test days when no food was delivered. Most of these experienced individuals were then replaced by naïve ones. The resulting ratio of experienced:naïve fish could be 5:7, 3:9 or 1:11. On their own, naïve individuals would normally spend the whole day in the shade, but in all tests the experienced individual(s) were able to entrain these more numerous naïve fish out of the shade and into the brightly lit food corner at the right time of day. Entrainment was stronger in the 5:7 than in the 1:11 experiment. The test shoals never split up and were always led by the same fish, presumably the experienced individuals. These results indicate that in a strongly gregarious species, such as the golden shiner, a minority of informed individuals can lead a shoal to food, either through social facilitation of foraging movements or by eliciting following behaviour. Copyright 2000 The Association for the Study of Animal Behaviour.
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Leadership is not an inherent quality of animal groups that show directional locomotion. However, there are other factors that may be responsible for the occurrence of leadership in fish shoals, such as individual differences in nutritional state between group members. It appears that front fish have a strong influence on directional shoal movements and that individuals that occupy such positions are often characterised by larger body lengths and lower nutritional state. Potential interactions between the two factors and their importance for positioning within shoals need further attention. Initiation of directional movement in stationary shoals and position preferences in mobile shoals need to be addressed separately because they are potentially subject to different constraints. Individuals that initiate a swimming direction may not necessarily be capable of the sustained high swimming performance required to keep the front position or have the motivation to do so, for that matter. More empirical and theoretical work is necessary to look at the factors controlling positioning behaviour within shoals, as well as overall shoal shape and structure. Tracking of marked individuals whose positioning behaviour is monitored over extended time periods of hours or days would be useful. There is an indication that shoal positions are rotated by individuals according to their nutritional needs, with hungry fish occupying front positions only for as long as necessary to regain their nutritional balance. This suggests that shoal members effectively take turns at being leaders. There is a need for three-dimensional recordings of shoaling behaviour using high-speed video systems that allow a detailed analysis of information transfer in shoals of different size. The relationship between leadership and shoal size might provide an interesting field for future research. Most studies to date have been restricted to shoals of small and medium size and more information on larger shoals would be useful.
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Used chi-square contingency and binomial homogeneity tests. Results obtained with the 1st method suggest that after 1 month at liberty tagged and untagged fish were randomly mixed in some cases and after 3-5 months at liberty they were randomly mixed with one another in nearly all cases. Results obtained with the 2nd method indicate somewhat less rapid mixing. -from Author
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Exploring Animal Social Networksshows behavioral biologists how to apply social network theory to animal populations. In doing so, Croft, James, and Krause illustrate the connections between an animal's individual behaviors and how these, in turn, influence and are influenced by behavior at the population level. . . . Valuable for readers interested in using quantitative analyses to study animal social behaviors.
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The mechanism of aggregation behaviour of sticklebacks, Gasterosteus aculeatus , in response to fright stimuli simulating an aerial predator was investigated. The results provide evidence for the hypothesis that during aggregation individual fish minimize the approach time to a conspecific (time minimization hypothesis). The first experiment investigated how the approach time depends on the body orientation of a fish and on the initial distance to a conspecific. These data were interpolated and used in experiment 2 to predict the approach behaviour of individual fish in particular model constellations involving three fish whose positions were controlled with the help of glass cylinders. In the final experiment, the hypothesis of time minimization was tested on freely aggregating shoals. Fish at the shoal periphery started the aggregation process significantly earlier than central conspecifics and over 95% of the focal fish approached their nearest neighbour in time as predicted by the model.