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  1. Author Response

    Reviewer #1 (Public Review):

    The authors set out to consider more the role of the predator in predator-prey interactions, particularly from a collective locomotion aspect. This is an aspect which at times has been overlooked, with many theories, experiments and models focusing largely on the prey response, independent of how the predator behaves. The major strengths are the (1) excellent writing, (2) quality of the figures, (3) quantity of data, and (4) question tackled. The major weaknesses are (1) the volume of information (as a reader, it is quite hard to distil key points from the sheer volume of what has been presented), (2) the confined captive environment making it difficult to draw comparisons with a wild-type scenario, and (3) lack of clarity about the wider implications of the work outside of the immediate field.

    We thank the reviewer for their thoughtful review and positive comments. To address the weaknesses highlighted by the reviewer, we have revised our manuscript throughout.

    Reviewer #2 (Public Review):

    The manuscript describes a laboratory-based predator-prey experiment in which pike hunt shiner fish as a way to gain insight into the selective pressures driving the evolution of collective behavior. Unlike the predictions of classical theoretical work in which prey on the edge of social groups are considered to be at highest risk of predation, the fish in the center of the school were primarily targeted by the pike. This is because the pike uses a hunting behavior in which it slowly moves to the center of the school, seemingly undetected, until it rapidly attacks prey directly in front of its snout. This study also differs from previous studies in that both the predator and prey motion are examined, and the success of predation attempts was precisely determined. While the study demonstrates why shiners would be under selective pressure to avoid the center of a school, I am not convinced that the results explain why shiners evolved to have schooling behavior.

    The reviewer indeed highlights one of the main findings of our study, that fish closer to the group center are more at risk of being attacked by pike. They also give a proper account of its possible explanation, and highlight some of the main ways in which our study differs from previous work. The reviewer states that our results do not explain why shiners evolved to school. We agree and note that we also don’t claim this anywhere in the manuscript. Rather, we state our study provides important new insights about differential predation risk in groups of prey and highlight the important role of predator attack strategy and decision-making and prey response, with potential repercussions for the costs and benefits of grouping.

    We have considerably revised our introduction to better explain the importance of understanding differential predation risk in animal groups (lines 36-50): A key challenge in the life of most animals is to avoid being eaten. Via effects such as enhanced predator detection (Lima, 1995; Magurran et al., 1985), predator confusion (Landeau and Terborgh, 1986), and risk dilution effects (Foster and Treherne, 1981; Turner and Pitcher, 1986), individuals living and moving in groups can reduce their risk of predation (Ioannou et al., 2012; Krause and Ruxton, 2002; Pitcher and Parrish, 1993; Ward and Webster, 2016). This helps explain why strong predation pressure is known to drive the formation of larger and more cohesive groups (Beauchamp, 2004; Krause and Ruxton, 2002; B. Seghers, 1974). However, the costs and benefits of grouping are not shared equally among individuals within groups, and besides differential food intake and costs of locomotion, group members themselves may experience widely varying risks of predation (Handegard et al., 2012; Krause, 1994; Krause and Ruxton, 2002). Where and who predators attack within groups not only has major implications for the selection of individual phenotypes, and thereby the emergence of collective behaviour and the functioning of animal groups (Farine et al., 2015; Jolles et al., 2020; Ward and Webster, 2016), but also shapes the social behaviour of prey and the properties and structure of prey groups. Hence, a better understanding of the factors that influence predation risk within animal groups is of fundamental importance.

    And in the discussion now better explain the potential evolutionary consequences of the findings of our work (lines 456-466): Predation is seen as one of the main factors to shape the collective properties of animal groups (Herbert-Read et al., 2017) and has so far generally been seen as to drive the formation of larger, more cohesive groups that exhibit collective, coordinated motion (see e.g. Beauchamp, 2004; Ioannou et al., 2012; B. H. Seghers, 1974). Our finding that central individuals are more at risk of being predated could actually have the opposite effect, with schooling having a selective disadvantage and over time result in weaker collective behaviour and less cohesive schools. However, we do not deem this likely as selection is likely to be group-size dependent, as discussed above. Furthermore, our multi-model inference approach revealed that, despite more central individuals experiencing higher predation risk, being close to others inside the school was still associated with a lower risk of being targeted. As most prey experience many types of predators, including sit-and-wait predators and active predators that hunt for prey, the extent and direction of such selection effects will depend on the broader predation landscape in which prey find themselves.

    Major strengths of the paper include the precise recording of the location and orientation of all fish at all times during the experiments. This indeed provides a rich dataset that can be used to search for the factors that predict the likelihood of attack and escape with higher statistical power.

    The major concern I have about the manuscript is that the results somewhat contradict the aim of the paper as expressed in the introduction and discussion: that predator-prey interactions explain the emergent evolution of collective behavior. Figure 2C shows that fish in smaller clusters or those that were totally isolated experienced lower rates of predation and were not included in any subsequent analyses. This would suggest that shiners experiencing predation from pike would be under strong selection to avoid schooling behavior altogether. Can you compare the likelihood of predation for individuals in non-central school locations compared to individuals outside of schools altogether? It might be helpful to investigate whether other predators of shiners use predation strategies that target prey on the edge of the school to help explain why schooling could be useful. Did the likelihood of schooling decrease throughout the trials?

    The reviewer makes a good point regarding the observation that pike tended to mainly attack individuals in the main school, questioning if this would result in a selective disadvantage for schooling. We would like to point out that this result is regarding the likelihood to attack an individual, not the likelihood for a successful attack. If we look at the later we find 5 out of 8 attacks away from the main school were successful, a ratio that is actually similar to that of the main school. More importantly, when wanting to understand how predation risk is linked to group size one needs to look at the per capita risk. If we do that for the group size we used in our study, despite a moderately elevated risk of being predated in a large group, the shiners in the main school still had considerably lower individual risk to be killed than those that occurred in small sub-groups or were alone. We would like to note that in our study the shiners did not really show proper fission-fusion behaviour and by far the majority of the time the shiners were in one large cohesive school. Therefore, we feel our dataset is not suitable for a proper investigation about the role of group size in predation risk.

    We now clarify these points in the discussion (lines 467-471): While the finding that pike were more likely to attack the main school may also appear to indicate a selective disadvantage to school, calculating the per-capita-risk for each individual would actually reveal it is still safest to be part of the main school. Nevertheless, as the shiners in our study rarely exhibited fission-fusion dynamics we feel our dataset is not appropriate to make proper inferences about how predation risk is linked to group size.

    We have also slightly extended the relevant sentences in the results to further clarify the clustering results (lines 144-150): We found that, by and large, the shiners were organised in one large, cohesive school at the time of attack and rarely showed fission-fusion behaviour (merging and splitting of schools) during the trials. Only occasionally there were one or two singletons besides the main school (25 attacks) or multiple clusters of more than two fish (12 attacks Figure 2C), which tended to exist relatively briefly (mean school size: 36.5 ± 0.8). In more than 80% of these cases, pike still targeted an individual in the main cluster (Figure 2C).

    We now also provide more discussion about other predator types being likely to attack central prey (lines 343-354): That predators may actually enter groups and strike at central individuals is not often considered (Hirsch and Morrell, 2011), possibly because it contrasts with the long-standing idea that predation risk is higher on the edge of animal groups (Duffield and Ioannou, 2017; Krause, 1994; Krause and Ruxton, 2002; Stankowich, 2003). However, our finding is in line with the predictions of theoretical work that suggest that the extent of marginal predation may depend on attack strategy and declines with the distance from which the predator attacks (Hirsch and Morrell, 2011). Furthermore, increased risk of individuals near the centre of groups may be more widespread than currently thought. Predators not only exhibit stealthy behavioural tactics that enable them to approach and attack central individuals, as we show here, but may also do so by attacking groups from above (Brunton, 1997) or below (Clua and Grosvalet, 2001; Hobson, 1963; but see Romey et al., 2008), and by rushing into the main body of the group (Handegard et al., 2012; Hobson, 1963; Parrish et al., 1989).

    We furthermore discuss the potential role of group size on the observed effects (lines 441-455): In particular, while group size is not expected to effect much whether ambush predators are likely to attack internal individuals, the specific risk of central individuals could both be hypothesized to decrease with group size, such as if the predator is more likely to attack when surrounded by prey, or to not be affected by it, such as if the predator actively targets central individuals. Whatever the process, the observed findings are likely for prey that move in groups of somewhat intermediate size; for very large groups, such as the huge schools encountered in the pelagic, ambush predators may simply not be able to attack the group centre due to spatial constraints. More generally, the tendency for predators to attack the centre of moving groups may depend on the medium in which the predator-prey interactions occur. As in the air there is potential for (fatal) collisions, and on land it is physically difficult for predators to enter groups and predators’ size advantage tends to be more limited, predators may be less likely to go for the group centre as compared to in aquatic or mixed (e.g. aerial predator hunting aquatic prey) systems. Hence, the important interplay we highlight between predator attack strategy and prey response may have different implications across different predator prey systems and warrants concerted further research effort.

    Finally, in response to the reviewer’s question if the likelihood to school decreased through the trials, we did not see a change in packing faction (median nearest-neighbour distance) with repeated exposure to the pike, but shiners increasingly avoided the area directly in front of the pike’s head (lines 182-186): While the shiners did not show a change in their packing fraction (median nearest-neighbour distance) with repeated exposure to the pike (F1,52 = 1.81, p = 0.185), they increasingly avoided the area directly in front of the pike’s head (Appendix 2 – Figure 1A) resulting in the pike attacking from increasingly further away (target distance: F1,52 = 45.52, p < 0.001, see Appendix 2 – Figure 1B,C). See also further Appendix 2.

    I am also curious whether tank size affects the behavior of the fish, both of the shiners and the pike. The pike seem to be approximately 1/3 the shortest length of the tank, and 6 inches of depth have constrained the movement to be mostly in the 2D plane. A lack of open space might limit the pike's ability to hunt in any way other than this stealthy strategy. Has this stealthy hunting strategy been described in other experiments in larger or more naturalistic conditions? Does open space affect the shiners' propensity to school? Although the manuscript describes that shiners tend to school near the surface of water, does the shallow depth affect the pike's behavior? The manuscript states that some pike never attacked -- were these the largest in the study?

    While the tank is small relative to the real world, we actually decided on this size of ~2m2 based on previous experimental work on predator-prey dynamics. As we stated in the methods of the original manuscript (lines 543-545) we expect that if a much larger space would have been used, pike would actually still show the same approach and attack behaviour linked to their stealthy attack strategy. The stealthy hunting behaviour of pike and similar predators and their ability to thereby get very close to their prey has been described elsewhere (see e.g. references on lines 332-344 of the original manuscript).

    We now better explain the potential limitation of the arena size in the discussion (lines 472-480): Laboratory studies on predator-prey dynamics like ours do, of course, have their limitations. Although the size of the arena we used (~2m2) is in line with behavioural studies with large schools of fish (e.g. Sosna et al., 2019; Strandburg-Peshkin et al., 2013) and experiments with live predators attacking schooling prey (Bumann et al., 1997; Magurran and Pitcher, 1987; Neill and Cullen, 1974; Romenskyy et al., 2020; Theodorakis, 1989), compared to conditions in the wild the prey and predator had limited space to move. However, as pike are ambush predators they tend to move relatively little to search for prey and rather rely on prey movement for encounters (Nilsson and Eklöv, 2008). Increasing tank size would have made effective tracking extremely difficult, or impossible, and while a much larger tank is expected to considerably increase latency to attack, we expect it to have relatively little effect on the observed findings.

    We agree that the shallow depth of the tank is a limitation of our study and may have somewhat restricted the pikes’ natural behaviour, although pilot experiments showed that the pike exhibited normal movements and attack behaviours. Fish were tested in very shallow water to be able to acquire detailed individual-based tracking of the schools as well as compute features related to the visual field of the fish. We would also like to note that both shiners and pike can often be found in the littoral zone and come in very shallow water of only a few 10s of cm (see e.g. Krause et al., 2000b; Pierce et al., 2013; Skov et al., 2018), with some experimental work furthermore showing that pike may actually prefer shallow water (Hawkins et al., 2005). We don’t think that increasing the depth of the tank would have considerably changed the predatory behaviour of the pike, as the pike would be expected to still use their stealthy approach to get close to their prey even if the prey school would be more three-dimensional.

    We now provide a much more extensive discussion of the limited depth used in the discussion (lines 480-494): In terms of water depth, fish were tested in relatively very shallow water. This was primarily done to be able to keep track of individual identities and compute features related to the visual field of the fish. Shiners naturally school in very shallow water conditions as well as near the surface in deeper water in the wild (Hall et al., 1979; Krause et al., 2000b; Stone et al., 2016) and also pike primarily occur in the shallow littoral zone, sometimes only a few of tens of cm deep (Pierce et al., 2013; Skov et al., 2018). Furthermore, pilot experiment showed the pike did exhibit normal swimming and attack behaviour with attack speeds and acceleration comparable to previous work (Domenici and Blake, 1997; Walker et al., 2005). Recent other work on predator-prey dynamics did not find a considerable impact of adding the third dimension to their analyses (Romenskyy et al., 2020). Still, the water depth used is a limiting factor of our study and in the future this type of work should be extended to deeper water while still keeping track of individual identities over time. We expect that adding the third dimension would not change the stealthy attack behaviour of the pike and therefore still put more central individuals most at risk, but possibly attack success would be reduced because of increased predator visibility and prey escape potential in the vertical plane, which remains to be tested.

    We did not observe a relationship between pike size and tendency to attack.

    Reviewer #3 (Public Review):

    While it has long been clear that animals in groups (e.g., fish schools) benefit in terms of safety in numbers, there has also been a keen interest in which animals in the group are at higher versus lower risk (e.g., those in front, or along the edges) and how that might depend on the predator's attack strategy. This study addresses these important predator-prey details using a common predatory fish (northern Pike) attacking schools of prey fish (golden shiners). A strength of the study is that it uses cutting-edge video tracking and computational/statistical methods that allow it to quantify and follow each fish's (1 predator and 40 prey in a group) spatial position, relative spacing, orientation and even each individual's visual field and movement throughout each of 125 attacks. Most (70%) of these attacks were successful, but many were not. The variation in attack success allowed the investigators to do statistical analyses to identify key predator and prey behaviors that are associated with successful vs. unsuccessful attacks.

    The study yielded numerous interesting insights. While conventional wisdom pictures predators initiating an attack from outside of the group thus putting individuals at the group's edge at greatest risk, this study found that pike typically approached the school of prey headon both in terms of the group's orientation and direction of movement, and often stealthily moved within the group before initiating an attack. To understand which prey individual was targeted by the predator, the highly quantitative video analyses examined 11 measures of each individual prey's position and orientation at the time that the pike initiated its attack. Of course, pike showed a strong tendency to target one of the 3 closest prey, particularly prey that were more or less directly in front of the pike. However, contrary to conventional wisdom, the analysis showed that targeted prey were closer to the center than the edge, and that an individual's position and orientation relative to other nearby prey also played an important role in whether it might be targeted by the predator. Not surprisingly, analyses showed that targeted prey were more likely to escape if they were further from the predator's head and if they exhibited higher maximum acceleration. Interestingly, during the actual strike, on average, the predator accelerated to a speed about 50% faster than the velocity of the targeted prey.

    A limitation of the study (that the authors describe and discuss) is that it was conducted in a tank with no spatial refuges whereas in nature, pike are often found in areas with vegetation, and schools of prey can often potentially respond to the presence of a predator by moving towards refuge (e.g., vegetation). Also, the study was done in very shallow water (6 cm) -- likely shallower than many, if not most, natural predator-prey interactions for these species. In deeper water, the predator-prey interaction might be better analyzed in three dimensions (i.e., also accounting for variation in vertical height in the water), though the authors argue that this conventional idea is not necessarily true.

    Overall, this study provides an impressive example of the use of modern technology and statistical analyses allows us to better describe and understand the fine-scale behaviors that affect an interaction of high importance for ecology and evolution.

    We thank the reviewer for the care and attention put in their review and their detailed objective assessment of our study.

    Regarding refuge use, it is true that in the wild pike are often found in areas with vegetation, but it is actually predominantly younger pike seeking refuge among vegetation from predators themselves, including from cannibalism by larger pike (see Skov & Lucas, 2018 Chapter 5). Vegetation is also used by pike as background camouflage rather than a refuge per se, but due to their elongated body and narrow frontal body pike are able to approach and ambush prey when no vegetation is available, as we show in our study. During pilot experiments we did provide pike with refuges, but as they never used them, and it would provide a hiding place for hiding, which would have considerably impacted our ability to investigate predation risk within the schools, no refuges were provided during the experiment.

    We now added an explanation about not using refuges in the discussion (lines 495502): For our experiments we used a testing arena without any internal structures such as refuges. This was a strategic decision as providing a more complex environment would have impacted the ability of the shiners to school in large groups and would have led fish to hide under cover. Although studying predator-prey dynamics in more complex environments would be interesting in its own regard, it would not have allowed us to study the questions we are interested in about the predation risk of free-schooling prey. Furthermore, pilot experiments indicated that the pike never used refuges (consistent with previous work, see Turesson and Brönmark, 2004), so they were not further provided during the actual experiment.

    Regarding the shallow depth of the tank, we now better acknowledge this limitation and explain our reasoning (lines 480-482): In terms of water depth, fish were tested in relatively very shallow water. This was primarily done to be able to keep track of individual identities and compute features related to the visual field of the fish. We would also like to note that both shiners and pike spent a lot of their life in the littoral zone and occur in very shallow water of only a few 10s of cm (see e.g. Krause et al., 2000b; Pierce et al., 2013; Skov et al., 2018). Although the limited vertical space may have restricted the pikes’ natural behaviour to some extent, they did exhibit normal swimming and attack behaviour with attack speeds and acceleration comparable to previous work (Domenici and Blake, 1997; Walker et al., 2005). We now better discuss the limitation of the shallow depth used in the discussion on lines 477-494 (see also our responses above).

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  2. Evaluation Summary:

    This study, which will be of interest to behavioral ecologists, uses highly quantitative video tracking approaches to understand the predictors of predators' success in attacking schooling fish and will be of interest to behavioral, evolutionary, and movement ecologists. While some of the results seem unsurprising (e.g., that predators tend to successfully capture prey that are closer to them), the manuscript as a whole highlights the importance of tracking the perspective of the predator as well as of the prey, and shows that animals that are central to a group may sometimes be the most vulnerable. Although the experiments and data analyses are commendable, the manuscript would benefit from more careful discussion of its overall implications for the evolution of collective behavior, including potential limits of the experimental design.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

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  3. Reviewer #1 (Public Review):

    The authors set out to consider more the role of the predator in predator-prey interactions, particularly from a collective locomotion aspect. This is an aspect which at times has been overlooked, with many theories, experiments and models focusing largely on the prey response, independent of how the predator behaves. The major strengths are the (1) excellent writing, (2) quality of the figures, (3) quantity of data, and (4) question tackled. The major weaknesses are (1) the volume of information (as a reader, it is quite hard to distil key points from the sheer volume of what has been presented), (2) the confined captive environment making it difficult to draw comparisons with a wild-type scenario, and (3) lack of clarity about the wider implications of the work outside of the immediate field.

    Read the original source
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  4. Reviewer #2 (Public Review):

    The manuscript describes a laboratory-based predator-prey experiment in which pike hunt shiner fish as a way to gain insight into the selective pressures driving the evolution of collective behavior. Unlike the predictions of classical theoretical work in which prey on the edge of social groups are considered to be at highest risk of predation, the fish in the center of the school were primarily targeted by the pike. This is because the pike uses a hunting behavior in which it slowly moves to the center of the school, seemingly undetected, until it rapidly attacks prey directly in front of its snout. This study also differs from previous studies in that both the predator and prey motion are examined, and the success of predation attempts was precisely determined. While the study demonstrates why shiners would be under selective pressure to avoid the center of a school, I am not convinced that the results explain why shiners evolved to have schooling behavior.

    Major strengths of the paper include the precise recording of the location and orientation of all fish at all times during the experiments. This indeed provides a rich dataset that can be used to search for the factors that predict the likelihood of attack and escape with higher statistical power.

    The major concern I have about the manuscript is that the results somewhat contradict the aim of the paper as expressed in the introduction and discussion: that predator-prey interactions explain the emergent evolution of collective behavior. Figure 2C shows that fish in smaller clusters or those that were totally isolated experienced lower rates of predation and were not included in any subsequent analyses. This would suggest that shiners experiencing predation from pike would be under strong selection to avoid schooling behavior altogether. Can you compare the likelihood of predation for individuals in non-central school locations compared to individuals outside of schools altogether? It might be helpful to investigate whether other predators of shiners use predation strategies that target prey on the edge of the school to help explain why schooling could be useful. Did the likelihood of schooling decrease throughout the trials?

    I am also curious whether tank size affects the behavior of the fish, both of the shiners and the pike. The pike seem to be approximately 1/3 the shortest length of the tank, and 6 inches of depth have constrained the movement to be mostly in the 2D plane. A lack of open space might limit the pike's ability to hunt in any way other than this stealthy strategy. Has this stealthy hunting strategy been described in other experiments in larger or more naturalistic conditions? Does open space affect the shiners' propensity to school? Although the manuscript describes that shiners tend to school near the surface of water, does the shallow depth affect the pike's behavior? The manuscript states that some pike never attacked -- were these the largest in the study?

    Read the original source
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  5. Reviewer #3 (Public Review):

    While it has long been clear that animals in groups (e.g., fish schools) benefit in terms of safety in numbers, there has also been a keen interest in which animals in the group are at higher versus lower risk (e.g., those in front, or along the edges) and how that might depend on the predator's attack strategy. This study addresses these important predator-prey details using a common predatory fish (northern Pike) attacking schools of prey fish (golden shiners). A strength of the study is that it uses cutting-edge video tracking and computational/statistical methods that allow it to quantify and follow each fish's (1 predator and 40 prey in a group) spatial position, relative spacing, orientation and even each individual's visual field and movement throughout each of 125 attacks. Most (70%) of these attacks were successful, but many were not. The variation in attack success allowed the investigators to do statistical analyses to identify key predator and prey behaviors that are associated with successful vs. unsuccessful attacks.

    The study yielded numerous interesting insights. While conventional wisdom pictures predators initiating an attack from outside of the group thus putting individuals at the group's edge at greatest risk, this study found that pike typically approached the school of prey head-on both in terms of the group's orientation and direction of movement, and often stealthily moved within the group before initiating an attack. To understand which prey individual was targeted by the predator, the highly quantitative video analyses examined 11 measures of each individual prey's position and orientation at the time that the pike initiated its attack. Of course, pike showed a strong tendency to target one of the 3 closest prey, particularly prey that were more or less directly in front of the pike. However, contrary to conventional wisdom, the analysis showed that targeted prey were closer to the center than the edge, and that an individual's position and orientation relative to other nearby prey also played an important role in whether it might be targeted by the predator. Not surprisingly, analyses showed that targeted prey were more likely to escape if they were further from the predator's head and if they exhibited higher maximum acceleration. Interestingly, during the actual strike, on average, the predator accelerated to a speed about 50% faster than the velocity of the targeted prey.

    A limitation of the study (that the authors describe and discuss) is that it was conducted in a tank with no spatial refuges whereas in nature, pike are often found in areas with vegetation, and schools of prey can often potentially respond to the presence of a predator by moving towards refuge (e.g., vegetation). Also, the study was done in very shallow water (6 cm) -- likely shallower than many, if not most, natural predator-prey interactions for these species. In deeper water, the predator-prey interaction might be better analyzed in three dimensions (i.e., also accounting for variation in vertical height in the water), though the authors argue that this conventional idea is not necessarily true.

    Overall, this study provides an impressive example of the use of modern technology and statistical analyses allows us to better describe and understand the fine-scale behaviors that affect an interaction of high importance for ecology and evolution.

    Read the original source
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