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ANIMAL BEHAVIOUR, 2007, 74, 1743e1751doi:10.1016/j.anbehav.2007.04.013

Rapid bystander assessment of intrinsic fighting ability:

behavioural and heart rate responses in rainbow trout

JOHAN HOJESJO, PETER ANDERSSON, ANDERS ENGMAN & JORGEN I. JOHNSSON

Department of Zoology, Animal Ecology, Goteborg

(Received 18 August 2006; initial acceptance 20 October 2006

final acceptance 5 April 2007; published online 24 September 2007; MS. number: 9081R)

The ability of bystanders to assess the intrinsic fighting ability of potential opponents with and withoutcontest information was examined in an experimental study using rainbow trout, Oncorhynchus mykiss.Behavioural and heart rate responses were monitored for bystanders observing size-matched conspecificsbefore and after a staged contest with an opponent. The results suggest that bystanders can rapidly andaccurately assess the intrinsic fighting ability/quality of a potential opponent. Within 10 s, bystanders in-creased their visual exposure towards opponents subsequently becoming subordinate and decreased theirexposure towards opponents becoming dominant. Male bystanders showed higher visual exposuretowards opponents than did females, regardless of the sex of the opponent. This immediate behaviouralresponse was subsequently (24 h after the first exposure) followed by elevated heart rate in bystandersexposed to dominant opponents, probably reflecting a physiological stress response. Apparently,bystanders used reliable size-independent cues allowing a rapid behavioural response. The delayed physi-ological response probably arises from the chemical cues associated with the presence of a dominantopponent, or a combination of initial visual cues and subsequent continuous exposure to chemicalcues. The results suggest that bystanders are able to rapidly assess the intrinsic fighting ability of a simi-lar-sized potential opponent without information about its contest success against other individuals.This ability can be utilised by bystanders to withdraw from costly contest with low winning probability.Thus, escalated conflicts may be less common in nature than previously suggested by laboratory studies.

� 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Keywords: fighting ability; heart rate; Oncorhynchus mykiss; preassessment; rainbow trout

Escalation of animal conflicts over resources can imposea number of costs, for example increased energeticexpenditure (Pucket & Dill 1985; Chellappa & Hunting-ford 1989), accumulation of harmful by-products (Sned-don et al. 1999), increased risk of injury (Abbott & Dill1985; Enquist et al. 1990) and reduced vigilance, whichmay increase the risk of being preyed upon (Jakobssonet al. 1995; Griffiths et al. 2004). Because of these costs, se-lection has promoted the ability to assess the resourceholding potential of an opponent (Parker 1974).

According to the sequential assessment model (Enquist& Leimar 1983), opponents are assumed to obtain increas-ingly accurate information about their relative strength asthe contest unfolds. Thus, when asymmetries in fighting

Correspondence: J. Hojesjo, Department of Zoology, Animal Ecology,University of Goteborg, Box 463, SE-405, 30 Goteborg, Sweden (email:johan.hojesjo@zool.gu.se).

1740003e3472/07/$30.00/0 � 2007 The Association for the S

ability are large, contests are expected to be resolvedquickly without escalation while escalation becomes in-creasingly likely when asymmetries are small (Leimar &Enquist 1984). Recent studies suggest that also uninvolvedanimals can gather information about potential oppo-nents. When animals differ in size, or signal status withbadges (Bradbury & Vehrencamp 1998) bystanders can as-sess the fighting ability of conspecifics without prior infor-mation about their contest success. In some assessmentsituations, however, information on size or badges of sta-tus may be lacking or unreliable (Rohwer & Rohwer 1978).

Whereas bystander effect is a more general term for anyinformation that can be extracted by observing otherindividuals, eavesdropping is defined as the extraction ofinformation that can only be gained from interactions(McGregor & Dabelsteen 1996). Eavesdropping on contestbehaviour has been found to affect behaviour in subse-quent contests against observed opponents (Coultieret al. 1996; Johnsson & Akerman 1998; Oliviera et al.

3tudy of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

ANIMAL BEHAVIOUR, 74, 61744

1998), suggesting that preassessment can reduce contestcosts and influence hierarchy formation (Dugatkin 2001;Earley & Dugatkin 2002). Conversely, animals involvedin aggressive interactions can change their behaviourwhen being watched (i.e. the audience effect: Evans & Mar-ler 1994; McGregor & Peake 2000; Doultrelant et al. 2001).

Previous research shows that threatening situations caninduce cardioventilatory responses in animals. For exam-ple, in predation threatened mammals, bradycardia (de-creasing heart rate) is associated with freezing or hidingand tachycardia (increasing heart rate) with flight ordefence (Moen et al. 1978; Smith et al. 1981; Espmark &Langvatn 1985). Salmonid fish respond to predator attackswith bradycardia and flight followed by a tachycardic re-sponse, which may serve to supply the body with oxygenin case the predator should appear again (Hojesjo et al.1999; Johnsson et al. 2001b). To our knowledge, it hasnot previously been studied whether the intrinsic fightingability or contest success of potential opponents influ-ences the cardioventilatory responses of bystanders.However, other physiological responses to competitive sit-uations have been shown. For example, androgen levelsincreased in male cichlids, Oreochromis mossambicus, ob-serving fights between other conspecific males suggestingthat androgens may act as competition hormones that re-spond to the social environment, preparing the individualfor competitive situations (Oliviera et al. 2001). The inter-actions between social status and neuroendocrine regula-tion are complex (reviewed by Johnsson et al. 2006),suggesting that behavioural and physiological responsesto assessment and contest situations in animals are intrin-sically linked. It thus seems likely that fish should showvariation in their heart rate response to physiologicallyprepare for a conflict, depending on their assessment ofthe intrinsic fighting ability of the potential opponent.

The aim of this study was to address the hypotheses (1)that bystanders can rapidly assess the intrinsic fightingability of size-matched opponents with unknown socialstatus, and (2) that the recent contest success of

opponents affects the behavioural and physiological re-sponse of bystanders. To test these hypotheses we mon-itored the behavioural and cardioventilatory response ofrainbow trout (bystanders) observing size-matched con-specifics 10 min before, 5 h after, and 1 day after a stagedcontest with a size-matched opponent. By determiningthe sex of the fish after the experiment we were alsoable to investigate any sex differences in behaviour andcardioventilatory responses.

METHODS

This study was performed between 14 March and 15 April2005. One year old (1þ) rainbow trout, Oncorhynchusmykiss, originating from Vanneans fish farm AB (195 kmsouth east of Gothenburg) were transported to the depart-ment of Zoology, University of Gothenburg. After 5 daysof acclimatization in large fish tanks (150 � 75 � 75 cm),with food (artificial pellets) provided in excess, the troutwere anaesthetised with 2-phenoxyethanol (0.5 ml/litre),measured for weight and fork length. Furthermore, to al-low individual identification in subsequent contests, theadipose fin was marked by a cut in one of the opponents(i.e. every third fish) during anesthetization. Marks werealternated between treatments to eliminate any behaviou-ral differences due to marking stress. However, no adverseeffects due to the fin cuts could be observed in any of thefish. Fish were then transferred to the experimental aquar-ium (120 litres, 40 � 48 � 64 cm). Experimental aquariawere divided into three compartments and the fish to bestudied (the bystander) was placed in compartment F.The two opponents were placed in compartments EX

and Ey (Fig. 1). To minimize possible effects of size on be-haviour (Huntingford et al. 1990), fish within the sameaquarium were sized matched on the basis of length(� 1 cm). The aquaria were filled with water (10�C) toa depth of approximately 22 cm with a flow through

31 cm

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FWater outlet

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Figure 1. Experimental aquarium viewed from above. Compartment F (with the focal fish and electrode cage) was separated from compart-

ments EX and Ey (with exposure fish y) by a transparent Plexiglas. Fish in compartment F (focal fish) were visually exposed to one of the ex-

posure fish (EX or Ey) by hoisting an opaque plastic sliding hatch positioned in front of the transparent Plexiglas. The contest area was the

combined area of compartment EX and Ey. Contests were initiated by hoisting the opaque plastic sliding hatch initially separating compartmentEX and Ey. Hatches could be hoisted upwards and downwards from a distance using attached strings. All the dividers and hatches were per-

forated, allowing water to run freely through the compartments.

HOJESJO ET AL.: RAPID ASSESSMENT OF FIGHTING ABILITY 1745

rate of 3 litres/min and a photoperiod of 15 h of light and9 h of dark.

The experiment, which was divided in three parts,started 36 h after the fish had been introduced into theexperimental aquarium. First (I) behavioural and heartrate responses of the bystander were monitored for 7 min.After 2 min the opaque sliding hatch was hoisted andvisual contact with a randomly chosen opponent wasallowed for the next 5 min (through a transparent parti-tion). Thereafter, the opaque sliding hatch was lowered toterminate the visual contact. After a 5-min recoveryperiod, the opaque hatch and the hatch physicallyseparating the two opponents were simultaneouslyhoisted allowing the bystander to watch a 10-min dyadicencounter between the two opponents (Fig. 1).

An opponent was ranked as dominant if it won most ofthe aggressive interactions with its opponent and ifaccompanying differences in colour (O’Connor et al.1999) and position (closest to the centre of the combinedarea of compartments EX and Ey, see Fig. 1) could be ob-served. After the dyadic encounter the two opponentswere again separated by the opaque hatch. In part two(II), 5 h after the dyadic encounter, the bystander wasagain exposed to the same opponent as in part I, now as-signed as either dominant or subordinate based on theoutcome of the dyad. Behavioural and heart rate responsesof the bystander were again recorded as in part I (2 min be-fore and 5 min after visual exposure). In part three (III), onthe following day (24 h after the first exposure), the focalfish was again exposed to the same individual as in parts Iand II. Final recordings of behavioural and heart rate re-sponses were taken as in parts I and II.

Using 10 aquaria at a time, this procedure wasrepeated until 15 replicates of dominant exposures and15 replicates of subordinate exposures were yielded.Those replicates where no dominance could be deter-mined were not used in the analysis. The most commontype of interaction recorded was display, either lateral orfrontal, where one or both fish erect all fins and attackswhere one fish charges at the other. Nips also occurredbut were less common. We did not observe anyabnormal behaviour or any injury to any of the fishduring the experiments. It is not possible to sex juvenilerainbow trout when alive. Therefore, after the trials, thefish was killed with an overdose of 2-phenoxyethanoland a blow on the head. Sex was determined by gonadalinspection. In total, 90 fish were used and killed in theexperiments.

Activity and Position

Compartment F, with the bystander fish, was dividedinto four equally sized subsections (Fig. 2) and an indexbased on visual exposure and distance to the opponentwas calculated; a bystander positioned straight in frontof the opponent achieved index 3 or 4 depending onthe distance (4 being closer the opponent) whereas a by-stander positioned beside the gate achieved and index of1 or 2 where fish in section 1 partly would be visually iso-lated from the opponent.

An index based on the activity of the fish was calculatedwhere: 1 ¼motionless at the bottom; 2 ¼maintainingposition in the lower half of the water column;3 ¼maintaining position in the upper half of the watercolumn; 4 ¼ actively swimming. The visual exposureindex and activity index of the bystander were recordedevery 10 s, 2 min before and 5 min after the exposure ofthe opponent fish.

Heart Rate

Heart rate was monitored parallel with the behaviouralobservations using a noninvasive method. The weakbiopotentials generated from the heart and ventilatorymuscles were recorded directly from the water by externalstainless steel electrodes allowing heart rate and behaviourto be studied simultaneously (Goodman & Weinberger1971; Hojesjo et al. 1999; Johnsson et al. 2001b; Fig. 3).The signals were amplified and filtered through a GrassAC (model CP511) amplifier. The resulting electrocardio-gram was recorded and processed with a laptop computer,using Lab view 5.1 (National Instruments Austin, TX,U.S.A.) software.

Treatment of Data

For the statistical analyses 12 time periods were used:the six 10-s periods immediately before and six after visualexposure. Heart rate was calculated as averages of the same10-s periods, using a software programme written in LabView 5.1 (National Instruments). The three dependentvariables, activity, position and heart rate, were analysedin separate repeated measurement analyses of covariance(Systat 11 Richmond, CA, U.S.A.) with time (the 12 time

Right hatchLeft hatch

4

3 2

1 4

32

1

Figure 2. The classification of the ‘visual exposure index’ based on

the distance and visual exposure to the opponent.

Signal output

Electrode grid

Electrode cage

Figure 3. Electrode cage and grid, viewed from the focal side of the

aquarium.

ANIMAL BEHAVIOUR, 74, 61746

periods) as the repeated measures factor, treatment (twolevels, subordinate and dominant) and sex (two levels,males and females) as independent class variables, andweight as a continuous covariate. All interactions wereinitially included in the model but removed stepwise ifnot significant. To clarify the presentation of the resultsonly P values below 0.10 are presented.

RESULTS

The average length and weight of the bystanders were16.9 cm (� 3.2 SE) and 56.5 g (� 3.0 SE), respectively.There were no differences in either weight or length be-tween bystanders being exposed to a dominant or subordi-nate opponent (two-sample t test, P > 0.10 both cases).The bystanders consisted of 16 males and 14 femaleswith no difference in either weight or length betweenthe sexes (two-sample t test, P > 0.10 both cases).

The two opponents and the bystander were sizematched within 1 cm and the average overall weightand length of the opponent did not differ from the sizeof the bystander (P > 0.1 both cases). The rank and sexof the opponent in relation to the sex of the bystanderare presented in Table 1.

The response of the bystander was not affected by thesex of the opponent neither for position, activity norheart rate (P > 0.10 all cases). Therefore, to simplify thepresentation of the results, the sex of the opponent fishhas been excluded from the analyses below.

Behavioural Responses

Visual exposureDuring the first exposure, there was no overall change

in visual exposure index over time (F11.286 ¼ 1.57,P ¼ 0.107) and no overall difference between bystandersexposed to dominant or subordinate opponent(F11.286 ¼ 0.15, P ¼ 0.702). However, there was a signifi-cant interaction between time and treatment(F11.286 ¼ 1.87, P ¼ 0.043), where bystanders increasedtheir visual exposure towards subordinate opponentsand decreased their exposure towards dominant oppo-nents. This response was rapid, detectable 10 s after expo-sure (Fig. 4). Furthermore, there was an overall effect of sexwhere bystander males had higher visual exposure thanfemales (F1.26 ¼ 4.47, P ¼ 0.044). No overall difference invisual exposure due to weight was revealed (F1.26 ¼ 3.20,P ¼ 0.085), but there was a significant interaction between

Table 1. The sex of the bystander and sex and rank of the opponentfish

Bystander(sex)

Opponent (sex and rank)

Femalesubodinate

Femaledominant

Malesubordinate

Maledominant

Female 3 5 3 3Male 4 3 5 4

weight and time (F11.286 ¼ 2.08, P ¼ 0.022) where smallerindividuals increased their visual exposure to the oppo-nent relatively more compared with larger individuals.

All bystanders had lower visual exposure index duringthe minute prior to exposure in part II (2.1 � 0.19 SE)compared with the same period in part I (2.79 � 0.18 SE;P ¼ 0.004, Z ¼ �2.90, N ¼ 30; Fig. 4), which may reflect

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Figure 4. The change in visual exposure of the bystander towards

subordinate and dominant opponents in (a) prior the dyadic en-

counter between the two opponent (part I), (b) 5 h after the dyadicencounter (part II) and (c) 24 h after the dyadic encounter (part III).

Error bars denote standard error of groups means (�SE). The dashed

line separates the period prior and after exposure.

HOJESJO ET AL.: RAPID ASSESSMENT OF FIGHTING ABILITY 1747

an avoidance response following the conflict between thetwo opponents. No other significant effect could be de-tected during part II. On the second day (part III) therewas again a significant interaction between time and treat-ment (F11.286 ¼ 2.33, P ¼ 0.009). However, the responsewas now reversed with the bystander decreasing their ex-posure to subordinate opponents and increasing their ex-posure to dominant opponents. This response was slowerthan during part 1, detectable after 40 s.

ActivityDuring the first exposure (part I), there was an increase

in activity after the opening of the hatch (F11.286 ¼ 3.26,P < 0.001; Fig. 5) but no overall difference because ofthe rank of the opponent or the sex or weight of thebystander (P > 0.1 both cases). However, a significantinteraction between time and weight was found(F11.286 ¼ 2.32, P ¼ 0.010) where smaller individuals in-creased their activity relatively more compared with largerindividuals after the exposure.

During the second exposure (part II) there was a strongtendency that bystanders exposed to dominant individ-uals were less active than bystanders exposed to sub-ordinates (F1.26 ¼ 4.13, P ¼ 0.052). No other significantdifferences in activity were found during part II andpart III.

Physiological (Heart Rate) Responses

During the first exposure (part I), there was a nearlysignificant bradycardia (decreasing heart rate) over time(F11,154 ¼ 1.805, P ¼ 0.057) but no overall difference be-tween bystanders exposed to subordinate or dominant op-ponent (Fig. 6). No interaction between treatment andtime could be detected. Furthermore, there were no overalldifferences because of sex or weight but a significant inter-action between weight and time (F11,154 ¼ 1.99, P ¼ 0.033)where smaller individual had less pronounced bradycardiacompared with larger individuals.

No significant effects could be detected during thesecond exposure (part II) but on the second day (partIII), bystanders exposed to dominant opponents had anoverall higher heart rate compared with bystanders ex-posed to subordinate opponent (F11,13 ¼ 4.93, P ¼ 0.045;Fig. 6). No other significant effects could be detected.

DISCUSSION

Within 10 s after exposure bystanders changed position toreduce their visual contact with opponents later becomingdominant, whereas they increased exposure towards op-ponents becoming subordinate. This novel finding sup-ports our hypothesis that bystanders have the ability torapidly (within 10 s) assess the intrinsic fighting abilityof conspecifics before any information on fighting abilityand/or status is available from the interaction. Previously,it has been suggested that eavesdropping on interactingindividuals can give the bystander valuable informationon relative fighting ability, condition and motivation

(e.g. McGregor & Dabelsteen 1996). In this study, the by-stander apparently used some other reliable cue allowinga rapid behavioural response.

Olfactory cues are well known to induce fright reactionsin fish (Smith 1997) and can also influence social

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DominantSubordinate

Figure 5. The change in activity of the bystander when exposed to

subordinate and dominant opponents in (a) prior the dyadic en-

counter between the two opponent (part I), (b) 5 h after the dyadic

encounter (part II) and (c) 24 h after the dyadic encounter (part III).Error bars denote standard error of groups means (�SE). The dashed

line separates the period prior and after exposure.

ANIMAL BEHAVIOUR, 74, 61748

behaviour and aggression in salmonids (Griffiths &Armstrong 2000). In our experiment water was allowedto circulate between the three compartments (Fig. 1).Therefore, olfactory cues were available before the visualexposure. Since the behavioural response coincided withthe visual exposure it is unlikely that olfactory cues were

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Figure 6. The change in heart rate (beats/min) during the exposureof the bystander towards subordinate and dominant opponents in

(a) prior the dyadic encounter between the two opponent (part I),

(b) 5 h after the dyadic encounter (part II) and (c) 24 h after the dy-

adic encounter (part III). Error bars denote standard error of groupsmeans (�SE). The dashed line separates the period prior and after

exposure.

used exclusively, although they might have been used incombination with visual cues. Although olfactory cuesfrom the two opponents were more or less mixed, salmo-nids have excellent ability to detect chemical cues (Stabell1981; Hara 1993) and might still have been able to sepa-rate cues from the two individuals combining these withspatial and/or visual cues. Since the two opponent fishwere size matched (� 1 cm) and no obvious difference inpigmentation or behaviour could be observed, the by-stander apparently used subtle visual cues, less obviousfor the human eye. It is well known that subordinate sal-monids darken during social interactions (Keenleyside &Yakamoto 1962) which is believed to act as a signal mod-ifying social behaviour, thereby reducing costly interac-tions (O’Connor et al. 1999). Such differences were alsoobserved after our dominance contests where the winningfish signalled its status with erected fins and brighter col-oration. However, no such obvious cues were availableto the bystander before the contest, again suggestingthat more subtle cues were used to allow the rapid re-sponse. It is also possible that opponent signalling wasinfluenced by the presence of the bystander since visualcontact between opponent and focal fish were bidirec-tional (i.e. the audience effect: Doultrelant et al. 2001).Keenleyside & Yakamoto (1962) found that aggressivesalmon, Salmo salar, developed a vertical band throughoutthe eye during agonistic encounters. The intensity of theband was also more pronounced in dominant fish,whereas the eye of a submissive fish generally appeareddarker than normal. It is plausible that eye colour couldact as a signal of intrinsic fighting ability even prior anyinformation based on eavesdropping is available, a possi-bility which needs further investigation.

As mentioned above, we did not observe any obviousstatus signalling from the opponent to the bystander priorto the staged contest. Nevertheless, as the bystander andthe opponent had visual contact (which would generallybe the case under natural conditions) any signal convey-ing intrinsic fighting ability may have been influenced bythe presence of the bystander (i.e. a form of audienceeffect). The importance of visual contact between thebystander and the individual from which information isgained needs further study (see McGregor & Peake 2000).Bystanders showed week bradycardia, a decrease in heartrate, during the first exposure which did not differ be-tween treatments. This is consistent with previous studieson fish and other taxa where bradycardia has been associ-ated with freezing or hiding to prevent detection by pred-ators (e.g. Johnsson et al. 2001b).

During the second exposure (five hours after thecontest) no difference between treatments in visualexposure index could be detected. Interestingly, all by-standers were now further away from the opponentcompared with the first exposure (Fig. 4). However, the ac-tivity level tended to be lower for bystanders exposed toa dominant individual. This response did not change sig-nificantly over time, suggesting a general response to thepresence of a dominant opponent. Interestingly, this re-sponse was established sometime after the 15 min of thefirst exposure but prior the second visual exposure(Fig. 5). Hence, it is possible that a combination of initial

HOJESJO ET AL.: RAPID ASSESSMENT OF FIGHTING ABILITY 1749

visual exposure and the following olfactory exposure wassufficient to create this difference in activity betweentreatments.

During the third exposure (24 h after the contest) theactivity level for bystanders exposed to dominant fishhad increased again and no differences in activity levelbetween bystanders exposed to a subordinate andbystanders exposed to a dominant opponent could bedetected (Fig. 2). Surprisingly, there was time-dependenttreatment effect where bystanders exposed to dominantopponents had higher visual exposure index than thoseexposed to subordinates. This result is contrary to the im-mediate response during part I, but here the response wasslower, occurring 40e50 s after visual exposure. Thisresponse does not support the hypothesis that dominantindividuals should be avoided (Oliviera et al. 1998).However, it is possible that the attention of the opponentmainly was directed towards its contestant during the firstday, whereas the absence of physical and visual contactwith the contestant on the next day may have causedthe opponent to direct its attention more towards the by-stander. Therefore, bystanders may have felt more threat-ened by the dominant fish during the third exposure,maintaining a higher level of vigilance to monitor its ac-tions. This interpretation is also supported by the physio-logical response, where bystanders exposed to dominantindividuals had an overall higher heart rate, which mayindicate a physiological stress response which would beadaptive to prepare for encounters with an aggressiveopponent (Winberg & Nilsson 1993).

The physiological responses of the bystander in thisstudy probably arose from the chemical cues associatedwith the presence of a dominant opponent or a combina-tion of initial visual cues and subsequent continuousexposure to olfactory cues. Physiological responses to-wards stress are relatively well documented in teleostfishes (see reviews by Pickering & Pottering 1995) andstress generally results in an almost instant activation ofthe sympathetic nervous system and an release in cate-cholamines (Nilsson 1984; Reid et al. 1995; Fabbri et al.1998). In subordinate fish elevated plasma levels of corti-sol have been reported (Winberg & Lepage 1998; Overliet al. 1999) and subordinate Arctic charr continue toshow elevated brain serotonergic activity even after longterm social interaction in stable dominance hierarchies.Also when dominance relations have not been settledstress-mediated physiological response can mobilize en-ergy for use during agonistic interactions (e.g. Winberg& Nilsson 1993; Johnsson et al. 2006). The delayed tachy-cardic response to aggressive dominant opponents, asshown in this study, might serve to prepare the bystandersfor fight or flight, a function that previously has beenattributed to tachycardic responses to predation threat(Espmark & Langvatn 1985; Johnsson et al. 2001b).

The sex of the opponent did not affect the behaviouralor physiological response of the bystanders. However, theimmediate response to opponents during part I differedbetween male and female bystanders. Interestingly, malebystanders were more visually exposed to the opponentthan were females. This might reflect differences inaggressive motivation and/or boldness between juvenile

males and females. Previous studies on juvenile rainbowtrout suggest that males are more aggressive than females(Johnsson & Akerman 1998) and similar sex-specificaggression patterns have been reported in brown trout,Salmo trutta, where males also tended to be more boldthan females (Johnsson et al. 2001a). Sex-specific juvenilebehaviour is common in mammals and birds (Hunting-ford & Turner 1987; Biben 1998), but has received limitedattention in fish, where it may arise through several mech-anisms (Johnsson et al. 2001a). For example, as a correlatedresponse to sexually selected gene actions promotingdifferential behaviour in adult males and females duringreproduction. In salmonids males compete for femalesand are more aggressive than females during spawning(Petersson & Jarvi 1997).

Agonistic interactions between individuals can haverelatively long-lasting modifying effects on the behaviourand physiology of fish (reviewed by Johnsson et al. 2006)as well as in other taxa (Huntingford & Turner 1987), butthe timescale of bystander effects is less well studied.Recent field experiment on birds suggests that the songbehaviour of male wrens can be influenced by songoverlap (playbacks simulating territorial intrusions) for1e5 days, suggesting that bystander effects can be rela-tively long lasting (Hall et al. 2005; Amrhein & Erne2006). The results of the present study suggest that by-stander effects can influence the behaviour and physiol-ogy in fish for at least 24 h. The effects of environmentalconditions and the relative importance of visual and olfac-tory cues in this context need further investigation.

In summary, this study suggests that bystanders are ableto rapidly assess the fighting ability of a potential oppo-nent without eavesdropping information from its inter-actions with other individuals. This immediate avoidanceis subsequently followed by a physiological responsereflected in an increased heart rate. The quick assessmentof a potential competitor is probably not perfect but mayreduce costs associated with competition by settling domi-nance relationships faster (Enquist et al. 1990; Griffiths et al.2004) and/or allow bystanders to avoid getting involved inconflicts at all when the chances of winning are small. Thepresent knowledge about social interactions is to a largeextent based on laboratory studies where opponents cannotwithdraw from the area of conflict (Sloman & Armstrong2002). Rapid preassessment of the fighting ability of po-tential opponents may help bystanders to quickly decideto withdraw from a conflict. Thus, costly escalated interac-tions may be less common in nature than previously sug-gested by laboratory studies.

Acknowledgments

Michael Axelsson provided valuable assistance withprogramming and heart rate monitoring. J. H. and J. I. J.were financed by the Swedish Research Council forEnvironment, Agricultural Sciences and Spatial Planning.This research adhered to the Association for the Study ofAnimal Behaviour/Animal Behavior Society Guidelines forthe Use of Animals in Research. The experiment wasapproved by the Ethical Committee for Animal Research

ANIMAL BEHAVIOUR, 74, 61750

in Goteborg (license 199/2002), and comply with currentlaws in Sweden.

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