Schooling Fish Under Attack Are Not All Equal: Some Lead,Others Follow

Animal groups such as fish schools, bird flocks and insect swarms appear to move so synchronously that they have long been considered egalitarian, leaderless units. In schooling fish, video observations of their spatial-temporal organization have, however, shown that anti-predator manoeuvres are not perfectly synchronous and that individuals have spatial preferences within the school. Nonetheless, when facing life-or-death situations, it is not known whether schooling fish react to a threat following a random or a hierarchically-based order. Using high-speed video analysis, here we show that schooling fish (Golden grey mullet, Liza aurata) evade a threat in a non-random order, therefore individuals that are first or last to react tend to do so repeatedly over sequential stimulations. Furthermore, startle order is strongly correlated with individual positional preferences. Because school members are known to follow individuals that initiate a manoeuvre, early responders are likely to exert the strongest influence on the escape strategy of the whole school. Our results present new evidence of the intrinsic heterogeneity among school members and provide new rules governing the collective motion of gregarious animals under predator attack.     

Behavior pattern (innate action) of individuals in fish schools generating efficient collective evasion from predation

The schooling of fishes is one typical animal social behavior. One primary function of fish school is to protect members when attacked by predators. One main way that the school reduces the predator's chance of making a successful kill is to confuse the predator as it makes its strike. This may be accomplished by collective evasion behaviors organized through integration of motions of individual fish made based on their innate actions (behavior patterns). In order to investigate what kind of behavior pattern of individuals can generate the efficient collective evasion of a school, we present a model of evasion behavior pattern which consists of three component behavior patterns, schooling, cooperative escape, and selfish escape behavior patterns and the rule for choice of one among them with proper timing. Each fish determines its movement direction taking into account simultaneously three kinds of elemental motions, mimicking its neighbors, avoiding collisions with its nearest neighbors, and escaping from an approaching predator. The weights of three elemental motions are changed depending on which component behavior pattern the fish carries out. The values of the weights for three component behavior patterns can be definitively determined under the condition that the collective evasion of the school becomes the most efficient, that is, the probability that any member is eaten by the predator becomes minimum.     

Hypoxia and the antipredator behaviours of fishes

Hypoxia is a phenomenon occurring in marine coastal areas with increasing frequency. While hypoxia has been documented to affect fish activity and metabolism, recent evidence shows that hypoxia can also have a detrimental effect on various antipredator behaviours. Here, we review such evidence with a focus on the effect of hypoxia on fish escape responses, its modulation by aquatic surface respiration (ASR) and schooling behaviour. The main effect of hypoxia on escape behaviour was found in responsiveness and directionality. Locomotor performance in escapes was expected to be relatively independent of hypoxia, since escape responses are fuelled anaerobically. However, hypoxia decreased locomotor performance in some species (Mugilidae) although only in the absence of ASR in severe hypoxia. ASR allows fish to show higher escape performance than fish staying in the water column where hypoxia occurs. This situation provides a trade-off whereby fish may perform ASR in order to avoid the detrimental effects of hypoxia, although they would be subjected to higher exposure to aerial predation. As a result of this trade-off, fishes appear to minimize surfacing behaviour in the presence of aerial predators and to surface near shelters, where possible. For many fish species, schooling can be an effective antipredator behaviour. Severe hypoxia may lead to the disruption of the school unit. At moderate levels, hypoxia can increase school volume and can change the shuffling behaviour of individuals. By altering school structure and dynamics, hypoxia may affect the well functioning of schooling in terms of synchronization and execution of antipredator manoeuvres. School structure and volume appear to be the results of numerous trade-offs, where school shape may be dictated by the presence of predators, the need for energy saving via hydrodynamic advantages and oxygen level. The effects of hypoxia on aquatic organisms can be taxon specific. While hypoxia may not necessarily increase the vulnerability of fish subject to predation by other fish (since feeding in fish also decreases in hypoxia), predators from other taxa such as birds, jellyfish or aquatic mammals may take advantage of the detrimental effects of hypoxia on fish escape ability. Therefore, the effect of hypoxia on fish antipredator behaviours may have major consequences for the composition of aquatic communities.     

Effects of successive predator attacks on prey aggregations

We study the cumulative effect of successive predator attacks on the disturbance of a prey aggregation using a modelling approach. Our model intends to represent fish schools attacked by both aerial and underwater predators. This individual-based model uses long-distance attraction and short-distance repulsion between prey, which leads to prey aggregation and swarming in the absence of predators. When intermediate-distance alignment is added to the model, the prey aggregation displays a cohesive displacement, i.e., schooling, instead of swarming. Including predators, i.e. with repulsion behaviour for prey to predators in the model, leads to flash expansion of the prey aggregation after a predator attack. When several predators attack successively, the prey aggregation dynamics is a succession of expanding-grouping-swarming/schooling phases. We quantify this dynamics by recording the changes in the simulated prey aggregation radius over time. This radius is computed as the longest distance of individual prey to the aggregation centroid, and it is assumed to increase along with prey disturbance. The prey aggregation radius generally increases during flash expansion, then decreases during grouping until reaching a constant lowest level during swarming/schooling. This general dynamics is modulated by several parameters: the frequency, direction (vertical vs. horizontal) and target (centroid of the prey aggregation vs. random prey) of predator attacks; the distance at which prey detect predators; the number of prey and predators. Our results suggest that both aerial and underwater predators are more efficient at disturbing fish schools by increasing their attack frequency at such level that the fish cannot return to swarming/schooling. We find that a mix between aerial and underwater predators is more efficient at disturbing a fish school than a single type of attack, suggesting that aerial and underwater foragers may gain mutual benefits in forming foraging groups.     

Antipredator Benefits of Schooling Behaviour in a Cyprinodontid Fish,the Banded Killifish (Fundulus diaphanus)

Fish schools are believed to provide antipredator benefits to their members. Two potential antipredator benefits, the dilution and confusion effects, of schooling were investigated in the laboratory using banded killifish (Fundulus diaphanus). Individual risk of being attacked and killed by a fish predator (white perch, Morone americana) declined with increasing killifish school size in a manner closely predicted by the dilution hypothesis. Perch were apparently not confused by schooling killifish since fish in groups of one did not suffer a disproportionately greater predation rate than fish in all larger school sizes. However, killifish straggling from the school were preferentially attacked and more successfully captured compared with school members. Schooling in the banded killifish therefore confers a considerable antipredator benefit to individual group members, at least through a dilution effect, and straying from a school has an associated increased risk of mortality to predation, which selects for schooling behaviour.     

The three-dimensional structure of schools in the minnow, Phoxinus phoxinus (L.)

A photographic technique is described for determining the three-dimensional position of fish schooling in front of a mirror in a flow tank. School structure is discussed in terms of the distance, horizontal bearing, and elevation of nearest neighbours. Nearest neighbour distances were measured snout-to-snout. A technique of analysis is described which considers the probability distribution of nearest neighbours in space. At speeds of flow 0 to 0·125 metres per second it was possible to show that Phoxinus, a facultative schooler, tended to maintain a school structure as previously reported for obligate schooling species. The structure was present only in a dynamic statistical sense and not in the sense of a rigid crystal lattice. Minnows maintained themselves at approximately 0·9 of their body length from each other under normal conditions and the bearings of neighbour fish suggested an attempt to maintain an optimum packing at this distance. At high speeds of flow the school structure tended to break up as fish sought areas of refuge from the current. All minnow schools were ellipsoidal in shape. The strategic and tactical methods by which schooling fish derive anti-predator advantage are discussed in relation to the school structure.     

Cooperative societies in three- dimensional space: On the origins of aggregations,flocks, and schools,with special reference to dolphins and fish

In three-dimensional open space habits, and to a lesser degree open terrestrial habitats, cooperative groupings of animals have repeatedly evolved. These cooperative systems have been observed in a wide variety of animal taxa, ranging from sea urchins to cetaceans. Various attempts have been made to relate the origins of such patterns to kin or altruism theory. An evolutionary stable strategy appears to be involved.We propose a graded series of group structures of increasing complexity by means of which three-dimensional groupings could have evolved without recourse to either group selection or even necessarily kin selection or reciprocal altruism. These structures are asocial and social aggregations, and polarized schools. Social aggregations and polarized schools allow cooperative feeding and avoidance of predation. They confer three predation-related advantages over living alone for animals in open environments: (1) the dilution effect of large prey numbers relative to those of predators, (2) the encounter effect, which provides some protection from searching predators, and (3) the confusion effect by means of which visual tracking by a predator is confounded. We suggest that the gaze stabilization system of the visual system is involved in the most advanced version of the confusion effect.In polarized schools members sense and react to each other, forming a sensory integration system (SIS). This system allows detection and transmission of information across a school, flock, or herd in three dimensions. Because members watch beyond their immediate neighbors the transmission of such group reactions can greatly exceed the reaction speed of individual members, or any predator. Because the confusion effect and the SIS depend upon uniformity of behavior the polarized school is uncommonly difficult and perhaps impossible to cheat against. We perceive this as a key factor in the establishment of the evolutionarily stable strategy of schooling.Polarized schools and aggregations are considered as the extremes of a behavioral continuum. Because in daytime the polarized school is a safer place to be and because the aggregation allows more freedom of movement for such activities as food finding, groups in open space oscillate between the these extremes during varying levels of predation.The social complexity of fish schools seems modest whereas dolphin schools show the complexities of fairly typical mammalian organization. Occupancy of open space by both oceanic dolphins and schooling fish seems to have fostered promiscuous mating. In both open water fish and mammals elements of a cooperative disposition occur, which involves both cooperation and suppression of some aspects of individuality. Such dispositional elements allow the automatic support of a cooperative society. Dolphin schools, which during daytime rest or danger react like fish schools, express typical mammalian organization at other times. Dolphin echolocation has probably allowed the expression of mammalian behavior patterns at sea because it confers a major advantage over shark predators. The expression of mammalian social complexity may have required both kin and reciprocal altruistic patterns in different species.     

How plankton copepods avoid fish predation: From individual responses to variations of the life cycle

Analysis of original and published data on predator avoidance by marine and freshwater plankton copepods, a major diet of many young fishes, suggests that individual defense mechanisms play a minor role in copepod anti-predator behavior. Capture success by planktivorous fish depends largely on prey visibility and the ability of the prey to escape. Copepods have almost no chance to avoid relatively large fish when encountered, but they can be ranked according to their ability to escape from larvae and fries. In contrast to small pelagic fish, which are also under heavy predation pressure, copepods rely more on prevention of the threat of predation than on active attempts to escape. Seeking a refuge in habitats non-accessible to predators would be more effective for these small and rather slow animals. Retreat into such refuges is accomplished by vertical and horizontal migrations, either diel, seasonal or ontogenetic. A decrease in activity (feeding, metabolism, reproduction, movement), resulting in diapause in deep water layers in its most pronounced version, is the ultimate attempt by copepods to separate from their predators, both in time and in space.     

School density affects the strength of collective avoidance responses in wild‐caught Atlantic herring Clupea harengus: a simulated predator encounter experiment

An experimental study in a semi‐controlled environment was conducted to examine whether school density in wild‐caught Atlantic herring Clupea harengus affects the strength of their collective escape behaviours. Using acoustics, the anti‐predator diving responses of C. harengus in two schools that differed in density were quantified by exposing them to a simulated threat. Due to logistical restrictions, the first fish was tested in a low‐density school condition (four trials; packing density = 1·5 fish m^?3; c. 6000 fish) followed by fish in a high‐density school condition (five trials; packing density = 16 fish m^?3; c. 60 000 fish). The C. harengus in a high‐density school exhibited stronger collective diving avoidance responses to the simulated predators than fish in the lower‐density school. The findings suggest that the density (and thus the internal organization) of a fish school affects the strength of collective anti‐predatory responses, and the extent to which information about predation risk is transferred through the C. harengus school. Therefore, the results challenge the common notion that information transfer within animal groups may not depend on group size and density.     

Effects of size on predation risk,behavioural response to fish,and cost of reduced feeding in larval Ischnura verticalis (Coenagrionidae: Odonata)

Summary We used laboratory studies to examine the role of predation risk and cost of anti-predator behaviour in determining the behavioural response of several larval instars of Ischnura verticalis to a fish predator (Lepomis gibbosus). Smaller larvae were less susceptible to fish predation than larger larvae. Smaller larvae depressed movement to a greater degree in the presence of fish than did larger larvae; large larvae were generally less active than small larvae regardless of fish presence. Reduced feeding resulted in smaller larvae suffering more in terms of reduced growth than did large larvae. In general, our results tend to support the hypothesis that individuals that suffer high costs of anti-predator behaviour but little risk of predation may only exhibit anti-predator behaviours in the presence of predators, whereas individuals with a higher risk of predation and a lower cost of anti-predator behaviour may evolve anti-predator mechanisms that are in effect even in the absence of predators.     

Shifting the balance between foraging and predator avoidance: the importance of food distribution for a schooling pelagic forager

It is widely held that when predator avoidance conflicts with other activities, such as feeding, avoidance of predators often takes precedence. In this study, we examine how predation risk and food distribution interact to influence the schooling behavior and swimming speed of foraging juvenile walleye pollock, Theragra chalcogramma. Fish were acclimated to either spatially and temporally clumped, or spatially and temporally dispersed food for 3 weeks. Fish were then monitored while feeding in the absence and presence of predatory sablefish, Anoplopoma fimbria. Fish foraging for clumped food swam rapidly in a loose school when predators were absent, but swam more slowly and adopted more cohesive schooling in the presence of predators, trading-off foraging opportunity for decreased vulnerability to predators. Fish foraging for dispersed food swam about slowly and did not engage in cohesive schooling in either the absence or presence of predators. These fish accepted greater predation risk in order to continue foraging, suggesting that the cost of schooling, in terms of decreased foraging opportunity, was greater when food was dispersed than when it was clumped. This lower responsiveness to predators among fish receiving dispersed food demonstrates that predator avoidance does not always take precedence over other activities, but rather, that a balance is maintained between predator avoidance and feeding, which shifts as food distribution changes.     

Is there safety‐in‐numbers for prey?

The abundance of prey affects the rate of predation, but little consensus exists on whether this enhances or reduces per capita mortality. Studies of aggregating prey in marine habitats generally emphasise that the probability of predation of any individual is the reciprocal of the number of prey within a school. A field experiment tested the alternative hypotheses that predation by predatory fish on schooling prey (1) increased with an increase in the number of prey per school and that this caused (2) survival to be lower in schools with more individuals. The number of prey (juvenile Acanthochromis polyacanthus ) per school was manipulated in replicate treatments with natural densities of large predatory fish (open plots) and treatments without large predatory fish (exclusion cages). Large predatory fish preyed on juveniles in a density-dependent manner and this was the key source of density-dependent mortality in plots open to all predators. There was some suggestion that small predatory fish also prey on juveniles in a density-dependent manner, but this was weak and did not translate into density-dependent mortality of juveniles. It would appear that aggregation of prey may be a successful strategy against predation from some predators, but not always every predator, or all predators in combination.     

Reduction in predator defense in the presence of neighbors in a colonial fish

Predation pressure has long been considered a leading explanation of colonies, where close neighbors may reduce predation via dilution, alarming or group predator attacks. Attacking predators may be costly in terms of energy and survival, leading to the question of how neighbors contribute to predator deterrence in relationship to each other. Two hypotheses explaining the relative efforts made by neighbors are byproduct-mutualism, which occurs when breeders inadvertently attack predators by defending their nests, and reciprocity, which occurs when breeders deliberately exchange predator defense efforts with neighbors. Most studies investigating group nest defense have been performed with birds. However, colonial fish may constitute a more practical model system for an experimental approach because of the greater ability of researchers to manipulate their environment. We investigated in the colonial fish, Neolamprologus caudopunctatus, whether prospecting pairs preferred to breed near conspecifics or solitarily, and how breeders invested in anti-predator defense in relation to neighbors. In a simple choice test, prospecting pairs selected breeding sites close to neighbors versus a solitary site. Predators were then sequentially presented to the newly established test pairs, the previously established stimulus pairs or in between the two pairs. Test pairs attacked the predator eight times more frequently when they were presented on their non-neighbor side compared to between the two breeding sites, where stimulus pairs maintained high attack rates. Thus, by joining an established pair, test pairs were able to reduce their anti-predator efforts near neighbors, at no apparent cost to the stimulus pairs. These findings are unlikely to be explained by reciprocity or byproduct-mutualism. Our results instead suggest a commensal relationship in which new pairs exploit the high anti-predator efforts of established pairs, which invest similarly with or without neighbors. Further studies are needed to determine the scope of commensalism as an anti-predator strategy in colonial animals.     

Inspection and evaluation of host plant by the butterfly Mechanitis lysimnia (Nymph., Ithomiinae) before laying eggs: a mechanism to reduce intraspecific competition

Parasites of all kinds affect the behaviour of their hosts, often making them more susceptible to predators. The associated loss in expected future reproductive success of infected hosts will vary among individuals, with younger ones having more lose than older ones. For this reason, young hosts would benefit more by opposing the effects of parasites than old ones. In a laboratory study, the effects of the trematode Telogaster opisthorchis on the anti-predator responses of the upland bully (Gobiomorphus breviceps) and of the common river galaxias (Galaxias vulgaris) were examined in relation to fish age. In a bully population where parasites were very abundant, the magnitude of the fish's anti-predator responses decreased as the number of parasites per fish increased, and this effect was significantly more pronounced in age 2 + and, to a lesser extent, age 3 + fish than in age 1 + fish. In another bully population where parasites were 10 times less abundant, similar effects were noticeable but not significant, whereas no effects of parasites on the responses of galaxiids to predators were apparent. Differences in the abundance of parasites and in their sites of infection in fish may explain the variability among host populations or species. However, in the bully population with high parasite abundance, parasitism has age-dependent effects on responses to predators, providing some support for the prediction that young fish with high expected future reproductive success invest more energy into opposing the effects of parasites than do older fish.     

Discriminating between Hungry and Satiated Predators: The Response of Guppies (Poecilia reticulata) from High and Low Predation Sites1

Fixed anti-predator activities are costly because they limit the ability of the prey to take advantage of short term temporal patchiness in predation pressure. The ability to discriminate between hungry and satiated predators and a flexible response to the differential threat can help to lower the costs of anti-predator behavior. In this study Trinidadian guppies (Poecilia reticulata) were found to distinguish between hungry and satiated predators. In Trinidad, populations of guppies experience different levels of predation from piscivorous fish. Individuals taken from populations with chronically high predation pressure responded stronger to the hungry predator than those from low predation sites.     

四种鲤科鱼类对捕食胁迫行为响应的种间比较

为了比较早期捕食胁迫经历和当前环境中存在的捕食者对鱼类行为的影响,并考查这些影响是否存在种间差异,研究分别考查了测定环境(有、无捕食者存在)对有、无捕食胁迫经历的鳊(Parabramis pekinensis)、草鱼(Ctenopharyngodon idellus)、鲫(Carassius auratus)和中华倒刺鲃(Spinibarbus sinensis)等4种鲤科鱼类探索性、活跃性和勇敢性的影响。结果发现:早期捕食胁迫经历与当前环境条件对鱼类行为产生截然不同的影响,且存在较大的种间差异。无捕食胁迫经历的鳊、草鱼和中华倒刺鲃均会对陌生的捕食者乌鳢(Channa argus)做出行为响应,提示这3种鱼可能对陌生捕食者具有一定的识别能力,但这种识别与猎物鱼通过捕食胁迫经历获得的识别仍具有一定差距;具有捕食胁迫经历的鳊和中华倒刺鲃在空白环境中未表现出反捕食行为,可能是节约能量的一种策略。总体而言,草鱼对捕食胁迫经历和测定环境处理反应更为敏感,而中华倒刺鲃的反应则相对保守。但当周围环境中存在捕食者时, 4种鲤科鱼类均会通过维持较高运动状态的方式来应对捕食者。维持这种应激状态可能对猎物鱼...     

A theoretical model of shoaling behavior based on a consideration of patterns of overlap among the visual fields of individual members

We propose a hypothetical visual field overlap (VFO) model for shoaling behavior. While solitary individuals have the disadvantage of a substantial blind zone to their rear, the overlapping visual fields among shoal members allows the shoal to collectively view nearly 360°. A highly polarized shoal (i.e., a school) would be less advantageous than randomly oriented shoals because a substantial area blind to all school members (common blind zone) would occur at some distance behind the school. However, in situations where fishes must orient in one direction, the visual fields of individuals in the school overlap such that the common blind zone is considerably farther behind than the blind zone of any particular fish. A simple geometric relationship between school width, the blind angle, and the distance to the common blind zone predicts that larger schools can detect predators at a greater distance than smaller schools. Additionally, the model provides a novel explanation for the nearly universally observed tendency for fish to school together with like-sized individuals. Finally, the effect of school shape on the visual field overlap pattern would have a strong impact on predator–prey interactions. However, our model does not directly take into account the range of visibility or social interaction affects and applies only to small groups. The VFO model suggests that schooling may have arisen as an adaptation to enhance feeding efficiency by reducing the need for individual vigilant behavior while oriented into the current for feeding. We believe the VFO model promises to provide insight into the behavioral ecology of shoaling fishes and that it is highly amenable to both field and laboratory testing.     

School fidelity in fishes: The yellow perch pattern

School fidelity concerns the cohesiveness of social aggregations over time, as measured by the regularity or repeatability with which known individuals re-occur as members of a school. School fidelity was measured by divers who observed yellow perch (Perca flavescens) marked with individually recognizable tags in Cazenovia Lake, New York. Yellow perch were facultative schoolers, with individual differences in schooling tendency (measured as percentage of time in schools) accounting for different numbers of observations of schooled versus solitary fish. The greatest co-occurrence was found between fish with strong schooling tendencies, but within this group co-occurrence was random. Home ranges overlapped greatly between individuals, yet co-occurrence was more a function of schooling tendency than of overlapping home ranges. Individuals with overlapping home ranges but with weak schooling tendencies seldom co-occurred. Home range size increased directly with schooling tendency: the distances that individuals moved apparently depended on the movements of the schools they joined, with strongly schooling fish remaining in schools longer. Individuals joined and left schools frequently; this also reflects a lack of fidelity between fish. Fish schools that form primarily for predator avoidance may show higher levels of fidelity than do schools that form for foraging or hydrodynamic efficiency.     

The Diel Activity of Crucian Carp, Carassius Carassius, in Relation to Chemical Cues from Predators

Chemical cues from piscivorous fish and prey alarm substances often cause rapid fright responses in prey. However little is known of how piscivore-related chemical cues affect prey behaviour over periods longer than a few hours. Here we have investigated how chemical cues from piscivorous northern pike, Esox lucius, affect habitat choice and diel activity of crucian carp, Carassius carassius, over an extended period 11 days. At the beginning of the experiment control fish were nocturnal while fish in the pike cue treatment were aperiodic. After 11 days, control fish had become more strongly nocturnal and displayed two activity peaks during early and late night whereas fish in the pike cue treatment were still aperiodic with no activity peaks. Habitat choice was aperiodic in both treatments throughout the experiment. In both treatments, more fish were found in the vegetation zone than in the open habitat. This was most pronounced when pike cues were present. These results demonstrate that short-term anti-predator responses to chemical cues from predators can translate into long-term adjustments of diel periodicity. Further, the results did not support the idea that crucian carp should switch to nocturnal activity in response to visually hunting predators. Control fish were nocturnal and chemical cues from pike did not make this pattern more pronounced.     

Predator-induced morphology enhances escape locomotion in crucian carp

Fishes show a remarkable diversity of shapes which have been associated with their swimming abilities and anti-predator adaptations. The crucian carp (Carassius carassius) provides an extreme example of phenotypic plasticity in body shape which makes it a unique model organism for evaluating the relationship between body form and function in fishes. In crucian carp, a deep body is induced by the presence of pike (Esox lucius), and this results in lower vulnerability to gape-limited predators, such as pike itself. Here, we demonstrate that deep-bodied crucian carp attain higher speed, acceleration and turning rate during anti-predator responses than shallow-bodied crucian carp. Therefore, a predator-induced morphology in crucian carp enhances their escape locomotor performance. The deep-bodied carp also show higher percentage of muscle mass. Therefore, their superior performance in escape swimming may be due to a combination of higher muscle power and higher thrust.