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Predator-Prey Relations in Fish Abattle of Intellects

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Predator-Prey Relations in Fish Abattle of Intellects U Predator-prey relations in fish abattle of intellects By Johanneke Oosten Supervized by Charlotte Hemelrijk 22-09-2006, Theoretical Biology, RuG D 931 r Index Introduction 2 How shoaling protects fish from, or exposes them to predatIon 3 The many eyes theory Shoal aggregation 4 Shoal-segregation 5 Size-segregation 11 Inspection behaviour 12 Schooling and evasion patterns 15 How predators deal with shoaling prey 17 Predator preferences 18 Hunting co-operatively 20 Ambushing prey 21 How predator-prey interactions are modified by learning 23 Alarm cues and learning by personal experience 24 Social learning 26 Ontogeny 27 Learned or genetic 27 Learning by predators 27 Conclusions 28 Appendix: fish names and families 30 References 32 Introduction Until the 1970's research on predator-prey inter- ics in less predator-dense areas. So it seems protec- actions in fish was rare. But in the last few decades, tion from predation is a major advantage of shoaling interest in the topic has grown explosively. By now (Seghers 1974: guppies; Magurran 1986: minnows). there are thousands of articles on the topic. One as- In this review I will focus on how this protection pect that has received special attention is learning. by shoaling arises.Iwill show that shoaling does Research makes it increasingly clear that fish are not not always protect, but may expose their members the anti-social, memory-impaired blobs they were to predation instead. In addition Iwill discuss vari- once thought to be, but that they are intelligent crea- ous techniques employed by predators to deal with tures that form social relationships with their shoal shoaling prey. Finally I will show how these predator- mates and perform sophisticated techniques to out- prey interactions are shaped by learning. wit their predators and / or prey (Laland et al 2003; In the course of this review it will become clear Bshary et al 2002). that the theories commonly used to explain the Many fish species live in groups or shoals. Shoals anti-predator benefits of shoaling are difficult to tt al :2004) found that banded killifish provide their members with advantages, such as a prove with empirical data. In their attempts to do crease their shoal size when exposed to choice of breeding partner, as well as disadvantages, so, researchers use experimental set-ups, so tightly Iarrn cues and decrease it when exposed such as food competition (Krause & Ruxton 2002). controlled, that their naturalness becomes doubtful. to food odours. When both were present When shoaling fish detect a predator they aggre- Also, the number of species used in research is lim- intermediate shoals were formed. gate, forming a more compact shoal (e.g. Templeton ited, casting doubt on the universality of our current & Shriner 2005: guppies; Ferrari et al 2005: fathead knowledge. minnows; Brown et al 2004: glowlight tetras; Magur- The text is accompanied by examples from vari- ran & Pitcher 1987: European minnows). Also, several ous studies. These either illustrate the issues dis- studies find that fish living in predator-dense areas cussed or add an extra dimension to them. spend more time aggregated than their conspecif- e How shoaling protects fish from, or exposesthem to predation In this chapter I will describe how shoaling fish may respond when they detect a predator. I will discuss how these responses may protect them from or expose them to predation. Then I will show how shoal- ing may aid fish in evading a predator's attack. 7. fathead minnow banded killifish threespine stickleback northern redbelly dace Image 1: a shoal of mackerel has detected approaching skipjack and has aggregated into a tight ball (from BBC's The Blue Planet) Shoal aggregation When a fish shoal detects a predator, its members additional benefit of having many eyes is that part often aggregate (e.g. Templeton & Shriner 2005: gup- of the shoal can keep watch while the rest forages, pies; Ferrari et al 2005: fathead minnows) (image 1). rests, etc.. In support of the many-eyes-theory van- Possibly aggregation provides protection from pre- ous studies find that, compared to individuals, shoals 4 dation. I will discuss four theories that explain how detect approaching predators sooner (Godin et al this protection may arise: the-many-eyes theory, the 1988: guppies; Magurran et al 1985: minnows; Tre- selfish herd theory; the dilution effect, the confusion effect. herne & Foster 1980: marine insect, but see Godin & Morgan 1985: banded killifish). Morgan &Godin (1985) found that information trans- Theory 1: the many-eyes-theory Prey will only benefit by their shoal mates' vigi- mission in shoals of banded killifish was independ- According to the many-eyes-theory, compared to an lance if information is transmitted fastacross the ent of shoal size, i.e. independent of the number of individual, a shoal will detect a predator sooner and shoal (Krause & Ruxton 2002). This seems to be the individuals in a shoal, and about twice as high as ap- keep better track of its movements, because a shoal case (Morgan & Godin 1985; Webb 1982). Webb proaching predator speed. with many fish has many eyes watching in many di- (1982) showed that the delay between escape stim- rections. This can save lives: predators' capture suc- ulus, such as a predator, and escape responsewas cess increases when prey are unaware of their pres- smaller for shoals than for individuals. This fast infor- ence (Turesson & Bränmark 2004, Webb 1982: pike; mation transmission was dubbed the Trafalgar effect Krause et al 1998a: rock bass). A fish that is aware of (Treherne & Foster 1981), in reference to theuse of danger can anticipate the moment of a predator's flag signals in Trafalgar's fleet (Krause & Ruxton 2002). strike. The exact tell-tale signs are unclear, but may Possibly the information Is transferred faster if the involve an unnatural stillness in the predator's body shoal mates are doser together. This may beone rea- (Magurran & Pitcher 1987: pike hunting minnows). An son for fish to aggregate on detection of a predator. 1 Foraging fish are less alert Theory 1: the selfish herd theory Foraging reduces vigilance: Godin & Smith Hamilton (1971) suggested that shoal aggrega- (1988) showed that foraging guppies were more tion occurs as a side-effect of fish seeking protection vulnerable to predation than non-foraging conspe- behind each other's backs. He postulated the selfish cifics. Vertically foraging fish are even less respon- herd theory: fish surround themselves by as many sive to their environment than horizontally foraging neighbours as possible so that a predator (that at- ones (Krause & Godin 1996: guppies). Krause & Go- tacks the first prey it encounters) attacks a shoal mate din (1996) suggest that vertically foraging fish may first (image 2). have: Several studies have tried to find empirical sup- - a smaller visual horizon. port for the selfish herd theory by determining if - a greater probability of visual obstacles (such as mortality rate by predation is higher in the shoal's vegetation) periphery than in its centre (table 1). Most studies - an increased difficulty of performing a quick find that the periphery is indeed the most danger- escape. ous area. Only one study found the opposite (Parr- When a predator is detected fish may change ish 1989). She describes how black seabass split up their foraging posture to better observe the preda- shoals of 25 Atlantic silversides by ramming into the Image 2: according to the selfish herd theory fish try tor (Godin 1986: banded killifish; Foam et al 2004: centre. Central fish suddenly found themselves In the to minimize the number of search trajectories lead- convict cichlids; Krause & Godin 1996: guppies). Of- periphery. The author notes, however, that had the ing from the predator to oneself. By aggregating, ten they stop foraging entirely (e.g. Abrahams 1995: shoal been larger, the predator may have attacked many trajectories will lead to shoal mates instead. brook sticklebacks; Godin & Smith 1988: guppies; a more peripheral part, since its main goal probably Godin 1986: banded killifish). Vigilance reduction was to split off a piece of the shoal. Still, predator tac- may also cause starved guppies and guppies enjoy- tics like these make central positions less attractive: ing high food-densities to suffer higher predation the optimal shoal position may in part depend on rates (Godin & Smith 1988: guppies; Godin 1986: the predator's hunting strategy (Parrish 1989). banded killifish). Krause & Ruxton (2002) wandered why fish do Problems proving the selfish herd theory not take advantage of their shoal mates' vigilance, Stankowich (2003) shows that the studies In table while lazing about themselves. They suggest that 1 are difficult to compare, because they differ in their the vigilance of others is not as good as being vigi- definitions of 'periphery' and 'centre He also argues lant yourself. Predators may prefer to attack un- that the selfish herd principle is not required to ex- wary prey (Krause & Godin 1996). Also, transfer of plain their results. He suggests that the increased pre- information across the shoal may be fastest when dation rate in the shoal's periphery could be caused all fish are alert. Inattentive fish may cause small but by a predator's active selection: it may prefer specific fatal delays. phenotypes that commonly reside in the periphery, e.g. smaller, younger or hungrier fish. Table 1: mortality by predation in shoals' centre and periphery (excerpt from Stankowich 2003) Article Preyspecies Predation rare penphery> predation rote centre? Krause & Tegeder 1994 Three-spine sticklebacks Periphery>Centre Krause 1993 Minnows Periphery>Centre Barber & Huntingford 1996 Minnows Periphery>Centre Parrish et al 1989 Flat-iron herring Centre = periphery Parrish 1989 Atlantic silversides Periphery<Centre Table 2: predators preferences for shoals Article Predatorspecies Prey species Preference for o2tocking largeitt shoals? Morgan &Godin 1985 White perch Banded killifish Preferred shoal over solitary fish Krause & Godin 1995 Blue acara cichlids Trinidadian guppies Preferred larger over smaHer shoal Botham et al 2005 Pike cichlids.
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