Effects of an infectious fungus, Batrachochytrium dendrobatidis, on amphibian predator-prey interactions

The effects of parasites and pathogens on host behaviors may be particularly important in predator-prey contexts, since few animal behaviors are more crucial for ensuring immediate survival than the avoidance of lethal predators in nature. We examined the effects of an emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis, on anti-predator behaviors of tadpoles of four frog species. We also investigated whether amphibian predators consumed infected prey, and whether B. dendrobatidis caused differences in predation rates among prey in laboratory feeding trials. We found differences in anti-predator behaviors among larvae of four amphibian species, and show that infected tadpoles of one species (Anaxyrus boreas) were more active and sought refuge more frequently when exposed to predator chemical cues. Salamander predators consumed infected and uninfected tadpoles of three other prey species at similar rates in feeding trials, and predation risk among prey was unaffected by B. dendrobatidis. Collectively, our results show that even sub-lethal exposure to B. dendrobatidis can alter fundamental anti-predator behaviors in some amphibian prey species, and suggest the unexplored possibility that indiscriminate predation between infected and uninfected prey (i.e., non-selective predation) could increase the prevalence of this widely distributed pathogen in amphibian populations. Because one of the most prominent types of predators in many amphibian systems is salamanders, and because salamanders are susceptible to B. dendrobatidis, our work suggests the importance of considering host susceptibility and behavioral changes that could arise from infection in both predators and prey.     

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保持与捕食者的距离, 并随时保持警惕较为关键。     

Monoxenous and heteroxenous parasites of fish manipulate behavior of their hosts in different ways

Adaptive host manipulation hypothesis is usually supported by case studies on trophically transmitted heteroxenous endoparasites. Trematodes and cestodes are among efficient manipulators of fish, their common intermediate hosts. In this review paper, new data on modifications of host fish behavior caused by monoxenous ectoparasitic crustaceans are provided together with a review of effects caused by heteroxenous parasites. Differences in modifications of host behavior caused by heteroxenous and monoxenous parasites are discussed. Manipulation by heteroxenous parasites enhances availability of infected fish to predators--definitive hosts of the parasites. Fine-tuned synchronization of modified anti-predator behavior with a certain phase of the trematode Diplostomum spathaceum development in the eyes of fish, their second intermediate host, was shown. Modifications of behavior are habitat specific. When juvenile salmonids are in the open water, parasites impair their cooperative anti-predator behavior; in territorial bottom-dwelling salmonids, individual defense behavior such as sheltering is the main target of manipulation. It was shown that monoxenous ectoparasitic crustaceans Argulus spp. decreased motor activity, aggressiveness and increased shoal cohesiveness of infected fish. Such a behavior facilitates host and mate searching in these parasites, which often change their hosts, especially during reproduction. Reviewed experimental data suggest that heteroxenous parasites manipulate their host mainly through impaired defense behavior, e.g. impairing shoaling in fish. Alternatively, monoxenous parasites facilitate shoaling that is profitable for both parasites and hosts. Coordination of modified host behavior with the parasite life cycle, both temporal and spatial, is the most convincing criterion of the adaptive value of host manipulation.     

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.     

The effect of Echinorhynchus borealis (Acanthocephala) infection on the anti-predator behavior of a benthic amphipod

In benthic habitats, predators can generally not be detected visually, so olfaction may be particularly important for inducing anti-predation behaviors in prey organisms. Manipulative parasites infecting benthic hosts could suppress these responses so as to increase the probability of predation and thus trophic transmission. We studied how infection with the acanthocephalan Echinorhynchus borealis affects the response of the benthic amphipod Pallasea quadrispinosa to water conditioned by burbot (Lota lota), the parasite's definitive host. In normal lake water, refuge use by infected and uninfected amphipods was similar, but when exposed to burbot-conditioned water, uninfected amphipods spent much more time hiding than infected amphipods. Thus, rather than affecting ambient hiding behavior, E. borealis infection seems to alter host response to a predator. A group of amphipods sampled from a postglacial spring that is devoid of fish predators exhibited only a weak response to burbot-conditioned water, perhaps suggesting these anti-predator behaviors are costly to maintain. The hiding behavior of spring and infected amphipods was very similar. If the reduced refuge use by the spring amphipods reflects adaptation to a predator-free environment, this indicates that E. borealis severely weakens its host's anti-predator behavior. Presumably this increases the likelihood of parasite transmission.     

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.     

Multiple predator defence strategies in Daphnia pulex and their relation to native habitat

Daphnia may respond with an array of anti-predator defences(behavioural, morphological and life history) to a chemicalcue (kairomone) exuded by its predators: fish and Chaoborus.Given the wide array of potential responses, it is an interestingquestion whether anti-predator defences are coupled or independentof each other. Since anti-predator responses are costly andeven possessing the genetic information to respond to a certainpredator might involve a cost, clones may only react to predatorsthey co-occur with in nature. In this study, we provide evidencefor an uncoupling of responses by Daphnia pulex in several anti-predatordefences against Chaoborus. We were unable to detect a correlationbetween behavioural (migration), morphological (neck-spine induction)and life history [growth rate, neonate size and size at firstreproduction (SFR)] responses. Furthermore, anti-predator responsesdid not always comply with what is commonly believed. We foundthat Daphnia clones can migrate up or down when exposed to fishor Chaoborus kairomone and that population growth rate, neonatesize and SFR can increase or decrease in response to Chaoboruskairomone. We also show patterns in anti-predator defences thatseem to relate to the habitat from which clones were derived.Daphnia clones that were collected in habitats with Chaoborusas the dominant predator tended to react strongly to Chaoboruskairomone by migrating upward and producing neck-spines. Themigration behaviour against fish kairomone in these clones wasoften an unexpected upward migration. The Daphnia clone thatco-existed with fish predators showed a downward migration inthe presence of fish as well as Chaoborus kairomone. Clonesthat had occurred with either both or no predators had mixedresponses. We sometimes found an upward migration in combinationwith smaller body size as a response to Chaoborus kairomone.This may be interpreted as a behavioural defence against Chaoborusand a life-history defence against fish. Daphnia seem not toexhibit defence behaviour against predators they do not co-occurwith. It might be costly for Daphnia to maintain genetic informationto respond to these predators and protect that information fromgenetic drift.     

Interactions among social monitoring,anti-predator vigilance and group size in eastern grey kangaroos

Group size is known to affect both the amount of time that prey animals spend in vigilance and the degree to which the vigilance of group members is synchronized. However, the variation in group-size effects reported in the literature is not yet understood. Prey animals exhibit vigilance both to protect themselves against predators and to monitor other group members, and both forms of vigilance presumably influence group-size effects on vigilance. However, our understanding of the patterns of individual investment underlying the time sharing between anti-predator and social vigilance is still limited. We studied patterns of variation in individual vigilance and the synchronization of vigilance with group size in a wild population of eastern grey kangaroos (Macropus giganteus) subject to predation, in particular focusing on peripheral females because we expected that they would exhibit both social and anti-predator vigilance. There was no global effect of group size on individual vigilance. The lack of group-size effect was the result of two compensating effects. The proportion of time individuals spent looking at other group members increased, whereas the proportion of time they spent scanning the environment decreased with group size; as a result, overall vigilance levels did not change with group size. Moreover, a degree of synchrony of vigilance occurred within groups and that degree increased with the proportion of vigilance time peripheral females spent in anti-predator vigilance. Our results highlight the crucial roles of both social and anti-predator components of vigilance in the understanding of the relationship between group size and vigilance, as well as in the synchronization of vigilance among group members.     

How does the presence of a conspecific individual change the behavioral game that a predator plays with its prey?

Behavioral games predators play among themselves may have profound effects on behavioral games predators play with their prey. We studied the behavioral game between predators and prey within the framework of social foraging among predators. We tested how conspecific interactions among predators (little egret) change the predator–prey behavioral game and foraging success. To do so, we examined foraging behavior of egrets alone and in pairs (male and female) in a specially designed aviary consisting of three equally spaced pools with identical initial prey (comet goldfish) densities. Each pool was comprised of a risky microhabitat, rich with food, and a safe microhabitat with no food, forcing the fish to trade off food and safety. When faced with two versus one egret, we found that fish significantly reduced activity in the risky habitat. Egrets in pairs suffered reduced foraging success (negative intraspecific density dependence) and responded to fish behavior and to their conspecific by changing their visiting regime at the different pools—having shorter, more frequent visits. The time egret spent on each visit allowed them to match their long-term capture success rate across the environment to their capture success rate in the pool, which satisfies one aspect of optimality. Overall, egrets in pairs allocated more time for foraging and changed their foraging tactics to focus more on fish under cover and fish ‘peeping’ out from their shelter. These results suggest that both prey and predator show behavioral flexibility and can adjust to changing conditions as needed in this foraging game.     

Parasites,info-disruption,and the ecology of fear

There is growing interest in the ecological consequences of fear, as evidenced by the numerous studies on the nonconsumptive, trait-mediated effects of predators. Parasitism, however, has yet to be fully integrated into research on the ecology of fear, despite it having direct negative and often lethal effects on hosts and being the most common life history strategy on the planet. This might at least be partly due to the traditional, but untested, assumption that anti-parasite responses are weak relative to anti-predator responses. To test this hypothesis, we quantified the activity and location responses of Bufo americanus tadpoles to one of six chemical cues: water; cercariae of Echinostoma trivolvis, a trematode which infects and can kill amphibians; a snail releasing E. trivolvis cercariae; an uninfected snail; food; or conspecific alarm chemicals signaling predation. There is also literature encouraging research on the context dependency and pollution-induced disruption of fear responses. Consequently, before quantifying responses to the chemical cues, half of the B. americanus were exposed to the herbicide atrazine (201 μg/l for 4 days), a reported inhibitor of fear responses in fish. Tadpoles were attracted to food, were indifferent to an uninfected snail, avoided alarm chemicals, and exhibited avoidance and elevated activity in response to a snail shedding cercariae and cercariae alone. Atrazine had no detectable effects on B. americanus’ responses to the tested cues despite the use of a higher concentration and longer exposure duration than has been repeatedly shown to inhibit chemical cue detection in fish. The magnitude of anti-parasite and anti-predator responses were qualitatively similar, suggesting that the fear of disease and its ecological consequences could be comparable to that of predation. Consequently, we call for a greater integration of parasites into research on the ecology of fear and trait-mediated indirect effects.     

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.     

Risk sensitivity in three juvenile (Age-0) flatfish species: Does estuarine dependence promote risk-prone behavior?

Pleuronectid flatfish are generally thought to use stereotypical anti-predator behavior to reduce encounters with potential predators, including burial, maintaining a low profile on the bottom, cryptic coloration, and reduced activity. However, a series of laboratory experiments demonstrate significantly different predation rates on juvenile (Age-0) English sole (Parophrys vetulus), northern rock sole (Lepidopsetta polyxystra), and Pacific halibut (Hippoglossus stenolepis) by Age-2 Pacific halibut predators, suggesting differing anti-predator strategies and/or capabilities among species. In this study, behavioral attributes that control how conspicuous juvenile flatfish are to their predators, such as burial, body posture, and activity levels, were examined both in the presence and absence of perceived predation risk. English sole exhibited risk-prone behavior; they tended to bury less, exhibit an arched body posture (with head elevated off the bottom), and were more active in both the absence and presence of predators when compared to the other two species. Conversely, rock sole exhibited risk-averse behavior, being buried, inactive, with a flat body posture regardless of predation risk. Halibut demonstrated risk-sensitive behavior; behaving like English sole in the absence of predation risk, and shifted to behavior similar to that of rock sole in the face of predation risk. As an estuarine dependent species, English sole recruit to an environment that tends to be highly turbid reducing encounters with predators. As a result English sole, may have “relaxed” anti-predator behaviors in comparison to northern rock sole and Pacific halibut which recruit to less turbid coastal nurseries.     

Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission

A host’s first line of defense in response to the threat of parasitic infection is behavior, yet the efficacy of anti-parasite behaviors in reducing infection are rarely quantified relative to immunological defense mechanisms. Larval amphibians developing in aquatic habitats are at risk of infection from a diverse assemblage of pathogens, some of which cause substantial morbidity and mortality, suggesting that behavioral avoidance and resistance could be significant defensive strategies. To quantify the importance of anti-parasite behaviors in reducing infection, we exposed larval Pacific chorus frogs (Pseudacris regilla) to pathogenic trematodes (Ribeiroia and Echinostoma) in one of two experimental conditions: behaviorally active (unmanipulated) or behaviorally impaired (anesthetized). By quantifying both the number of successful and unsuccessful parasites, we show that host behavior reduces infection prevalence and intensity for both parasites. Anesthetized hosts were 20–39% more likely to become infected and, when infected, supported 2.8-fold more parasitic cysts. Echinostoma had a 60% lower infection success relative to the more deadly Ribeiroia and was also more vulnerable to behaviorally mediated reductions in transmission. For Ribeiroia, increases in host mass enhanced infection success, consistent with epidemiological theory, but this relationship was eroded among active hosts. Our results underscore the importance of host behavior in mitigating disease risk and suggest that, in some systems, anti-parasite behaviors can be as or more effective than immune-mediated defenses in reducing infection. Considering the severe pathologies induced by these and other pathogens of amphibians, we emphasize the value of a broader understanding of anti-parasite behaviors and how co-occurring stressors affect them.     

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.     

Behavioral responses of native prey to disparate predators: naiveté and predator recognition

It is widely accepted that predator recognition and avoidance are important behaviors in allowing prey to mitigate the impacts of their predators. However, while prey species generally develop anti-predator behaviors through coevolution with predators, they sometimes show accelerated adoption of these behaviors under strong selection pressure from novel species. We used a field manipulation experiment to gauge the ability of the common ringtail possum (Pseudocheirus peregrinus), a semi-arboreal Australian marsupial, to recognize and respond to olfactory cues of different predator archetypes. We predicted that ringtails would display stronger anti-predator behaviors to cues of the invasive European red fox (Vulpes vulpes) in areas where fox impacts had been greatest, and to cues of the native lace monitor (Varanus varius) in areas of sympatry compared with allopatry. We found that ringtails fled quickly and were more alert when exposed to the fecal odors of both predators compared to neutral and pungent control odors, confirming that predator odors are recognized and avoided. However, these aversive responses were similar irrespective of predator presence or level of impact. These results suggest that selection pressure from the fox has been sufficient for ringtails to develop anti-predator behaviors over the few generations since foxes have become established. In contrast, we speculate that aversive responses by ringtails to the lace monitor in areas where this predator is absent reflect recent coexistence of the two species. We conclude that rapid evolution of anti-predator behaviors may occur when selection is strong. The maintenance of these behaviors should allow re-establishment of predator–prey relationships if the interactants regain sympatry via range shifts or management actions to reintroduce them to their former ranges.     

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.     

Innate and Learned Shoaling Preferences Based on Body Coloration in Juvenile Mollies,Poecilia latipinna

Shoaling offers fish enhanced protection from predators through a phenomenon known as the confusion effect. This phenomenon depends on a high degree of phenotypic homogeneity within a shoal, which may confuse predators that have difficulty in targeting a single individual as prey. Accordingly, fish typically choose shoalmates with similar phenotypic characteristics to themselves. In the molly (Poecilia latipinna), dramatic differences in body coloration have been shown to affect shoalmate choice in adults. Here, we show that juvenile mollies (50 d old) were capable of shoaling and that early experience impacted shoalmate choice. When raised in isolation, mollies chose shoalmates with similar body coloration to their own. When raised with other juvenile mollies, test fish chose to associate with individuals of the same coloration as the fish with whom they had been reared. These results show that P. latipinna are capable of the behavioral plasticity that has been demonstrated in other fish species, and that early experience affects the impact of body coloration on shoaling decisions in this species.     

Captive-born collared peccary (<Emphasis Type="Italic">Pecari tajacu</Emphasis>, Tayassuidae) fails to discriminate between predator and non-predator models

Captive animals may lose the ability to recognize their natural predators, making conservation programs more susceptible to failure if such animals are released into the wild. Collared peccaries are American tayassuids that are vulnerable to local extinction in certain areas, and conservation programs are being conducted. Captive-born peccaries are intended for release into the wild in Minas Gerais state, southeastern Brazil. In this study, we tested the ability of two groups of captive-born collared peccaries to recognize their predators and if they were habituated to humans. Recognition tests were performed using models of predators (canids and felids) and non-predators animals, as well as control objects, such as a plastic chair; a human was also presented to the peccaries, and tested as a separate stimulus. Anti-predator defensive responses such as fleeing and threatening displays were not observed in response to predator models. Predator detection behaviors both from visual and olfactory cues were displayed, although they were not specifically targeted at predator models. These results indicate that collared peccaries were unable to recognize model predators. Habituation effects, particularly on anti-predator behaviors, were observed both with a 1-h model presentation and across testing days. Behavioral responses to humans did not differ from those to other models. Thus, if these animals were to be released into the wild, they should undergo anti-predator training sessions to enhance their chances of survival.     

Anti-predator behavior of gelada baboons

The anti-predator behavior of gelada baboons has been observed to consist of simple flight (i.e. they flee to cliffs after becoming alarmed by potential predators). However, active antipredator behavior was observed in a recently found gelada population in Arsi, Ethiopia. This population showed frequent active counter-attacks and severe mobbing at predators. Males fought domestic dogs on the plain and exhibited a systematic mobbing behavior towards a leopard on the cliff face to chase it off. These active anti-predator behaviors are the first confirmed reports on gelada baboons and may provide a useful insight for the understanding of the process of evolutionary adaptation to highland habitats by gelada baboons, as well as for the origin of this small southern population.     

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.