ORIGINAL PAPER

Behavioural syndromes in juvenile brown trout(Salmo trutta); life history, family variation and performancein the wild

Johan Höjesjö & Bart Adriaenssens & Torgny Bohlin &

Christopher Jönsson & Illka Hellström &

Jörgen I. Johnsson

Received: 24 August 2010 /Revised: 18 February 2011 /Accepted: 5 April 2011 /Published online: 3 May 2011# Springer-Verlag 2011

Abstract The main aims of this study were to investigate(1) the occurrence and strength of the shyness–boldnessbehavioural syndrome in brown trout fry, (2) whether thissyndrome is associated with paternal migratory life history,(3) whether fry survival and growth in the wild isassociated with paternal life history and/or boldness and(4) whether offspring performance showed maternal effects.Nine female migratory trout were each crossed with onemigratory and one resident male and the offspring wereraised in hatchery tanks until first feeding. The behaviouralstudies showed that fry that responded bold towards a novelobject also accepted a novel food item earlier andresponded more aggressively towards their own mirrorimage. Principal component analysis showed that thisshyness–boldness syndrome (PC1) explained 34% of thebehavioural variation. Offspring boldness was not affectedby paternal migratory life history, but significant effects ofthe female parent suggested maternal and/or genetic effects.Deviations from this pattern (PC2), where some individualsbehaved less aggressively and performed more approachesto food, explained an additional 17% of the variation inbehaviour, and was significantly influenced by length andpaternal migratory life history. Fry growth and survival innature was not associated with boldness (PC1) or PC2,suggesting that alternative behavioural strategies can besuccessful in nature. However, female parent effects onvariation in fry size persisted over the first growth period inthe wild, suggesting that these effects may influence

offspring fitness during early life when major selectionoccurs.

Keywords Animal personality . Life history . Behaviouralsyndrome . Dominance . Fitness . Maternal effects

Although natural selection generally is believed to reducegenetically based phenotypic variation, even fitness-relatedtraits often vary both between and within populations(Mousseau and Roff 1987). Unfolding the adaptive mecha-nisms for creating and/or preserving such a phenotypicvariation is therefore a major challenge in evolutionarybiology. One example of this is the variation in salmonidfishes regarding migratory tendency, which offers an excellentopportunity to study questions about associations between life-history patterns and behaviour (Andersson 1994; Lack 1943;McKeown 1984; Lundberg 1988; Jonsson and Jonsson 1993).

The variation in migration tendency among salmonidpopulations is more strongly genetically determined thanwithin populations (e.g. Hendry et al. 2003). Regardless ofthe extent to which migration is conditionally or geneticallydetermined, the decision to migrate mitigates a range ofchanges in physiology, morphology (Folmar and Dickhoff1980; Price and Schreck 2003; Dingle 2006) and behaviour,including cessation of territorial behaviour (Keenleysideand Yamamoto 1962; Hutchison and Iwata 1997). Taylorand Larkin (1986) therefore suggested a positive correlationbetween aggression and residence period in the stream.However, Lahti et al. (2001) found sea-run populations ofbrown trout to be more aggressive than the lake-run andresident populations.

Behavioural switches involved in adopting a migratorylife style may affect a fundamental axis of behaviourpreviously described as the “shy–bold continuum” (Wilson

Communicated by T. Bakker

J. Höjesjö (*) : B. Adriaenssens : T. Bohlin :C. Jönsson :I. Hellström : J. I. JohnssonDepartment of Zoology, Animal Ecology, University of Göteborg,Box 463, 405 30 Göteborg, Swedene-mail: johan.hojesjo@zool.gu.se

Behav Ecol Sociobiol (2011) 65:1801–1810DOI 10.1007/s00265-011-1188-0

et al. 1994). Shy individuals react to unfamiliar situationsby retreating or becoming quiet and vigilant, whereas boldindividuals become actively exploratory in the samesituations (Wilson et al. 1993). Behavioural variation alongthe shy–bold continuum has been demonstrated in a widevariety of species, including fish (Bakker 1986; Wilson etal. 1993, 1994; Gosling 2001; Réale et al. 2007; Sih andBell 2008) and is often associated with other behaviourssuch as aggressiveness or activity (Huntingford 1976; Réaleet al. 2007; Sih and Bell 2008). It remains unclear howboldness and other “personality” traits associate with fitnessand growth in nature (Sih et al. 2004; Biro and Stamps2008; Smith and Blumstein 2008). Wilson et al. (1994)suggested that bold and shy strategies may persist togetherdue to frequency-dependent processes which may begenetically determined and/or conditional (e.g. MaynardSmith 1982; Hutchings and Myers 1994; Dingemanse et al.2009). Similarly, negative frequency-dependent selectionhas been attributed to the consistence of alternative matinggenotypes within a population (e.g. Gross 1985; Myers etal. 1986; Partridge and Harvey 1988).

Here we used sea trout as a model species. Sea troutpopulations generally consist both of resident and migrantforms and the tendency to migrate within the population is to alarge extent frequency dependent and conditionally triggered(Hendry et al. 2003). Males are more likely than females toremain resident in the stream, probably due to the weakercorrelation between fecundity and size in males whencompared to females. Generally though, all fish remainresident in the stream during the first 2–3 years before a partof the population migrates to the sea (Hendry et al. 2003;Bohlin et al. 1994). The main aims of this study were toinvestigate (1) the occurrence of the shy–bold syndrome inbrown trout fry, and (2) whether the boldness syndrome isaffected by paternal migratory life history. We hypothesised,according to Taylor and Larkin (1986), that offspring ofparental resident fish should be more bold and aggressive thanoffspring of parental migratory fish. We also investigated (3)whether fry survival and growth in the wild is associated withboldness and/or paternal migratory life history. (4) Femaleeffects on offspring performance were also investigated.

Methods

In October 2004, adult females (migratory, Nfemales=9,mean length� SE ¼ 453� 35mm) and adult males (mi-gratory males, Nmigratory males=9, mean length� SE ¼447� 20mm; resident males, N s t a t i ona ry ma le s = 9,mean length� SE ¼ 188� 10mm) were caught in Swedenby standardised electrofishing techniques in RiverNorumsån (latitude 58° N 11° E). At this point, wehad no information of any genetic difference between

migratory and resident males. These two alternative tacticswhere easily classified in the field based on size and colourwhere resident males always were smaller and darker in theircolouration (O’Connor et al. 1999). A tissue sample from thepectoral fin was collected from each individual and later onused for genetic analysis. Eggs of each female were split upand artificially fertilised with milt from one migratory andone resident male, respectively (see Johnsson et al. 1993 andVøllestad and Quinn 2003 for a similar setup). Hence, thedifference between the males is both that the resident malesremain in the stream but they are also smaller and probablywould have adopted an alternative reproductive strategy(sneaker strategy). This nested full-sib, half-sib breedingdesign yielded 18 full-sib families and nine pairs of half-sibfamilies in which offspring share a common female parentwhile male parents differ (and their life-history strategy).Following fertilisation the eggs were moved to the E.ONHatchery in Laholm and incubated in hatchery tanks accordingto parental origin (N=18, 42×42 cm, water depth 15 cm). Fryhatched between 10 and 15 March 2005, and behaviouralobservations took place at the fish farm in Laholm inconnection with the onset of exogenous feeding (pellet),approximately 2 weeks after yolk sac absorption between the10th and 24th of May 2005.

The behavioural study was carried out on 11 blocks (N=20or 40 fish, formed into ten or 20 pairs, per block, in total 360fry were used). In order to minimise bias due to differencesin ontogenetic development and learning over time, fry fromevery family with one to three replicates of each of the 18resident–migrant family pairings were tested within eachblock and size matched to a maximum difference of 1 mm.Before each trial, individuals were anaesthetised with2-phenoxyethanol (0.5 ml/l) and measured for totallength to the nearest millimetres. Each individual wasonly observed once in each assay. To distinguishbetween competitors in the dyadic contests, we cut theadipose fin in random order of either the juvenile ofmigratory origin or of stationary origin. We know fromprevious experiments that removal of the adipose findoes not affect behaviour of juveniles (e.g. Sundström et al.2003). Following anaesthetisation, single fish were moved toone half of a 2-l plastic aquarium (13 cm wide×20 cm long×13 cm deep), fed pellets in excess and acclimatised to thenext day. Each aquarium was divided into two equal halvesby an opaque plastic divider, with one half housing a residentand the other a migrant trout originating from differentmothers. All aquaria contained gravel substratum andeach were constantly provided with fresh water from thenearby River Lagan with an ambient temperature ofapproximately 12°. At the end of the study, juvenilesfrom every family had been paired together. To avoidany effects due to different tanks, we randomisedallocation of families among the tanks.

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Scores of individual behaviour

The next day, all acclimatised juveniles were individuallyscored for behaviour for 4 min using direct observations ineach of three different contexts: exploration of a novelobject, exploration of a novel prey and aggression.

Novel object

In the first experiment we observed the reaction of eachindividual to a novel object; a washer (φ12 mm) attachedto a fishing line. Novel object trials have been used as astandard method in a wide variety of species to asses anindividual’s position within the shyness–boldness continu-um (e.g. Wilson et al. 1993). The novel object was lowereddown gently to the centre of the compartment, and werecorded the number of approaches and attacks towards it.If a response started with an approach and ended withattack, only the most escalated behaviour was recorded.

Novel prey

The next trial followed directly after the novel objectexperiment, and was performed in an almost identical manner.However, instead of a novel object, novel food was added tothe surface (adult frozen brine shrimp, Artemia franciscana).Ten brine shrimps were added with a pipette in each of twofeeding bouts (after 60 and 180 s, respectively) to ensure aconstant influx of prey in the water column. During the4 min observation we again recorded the number ofapproaches and attacks towards the novel food.

Aggression

Following the novel prey test, we used mirror imagestimulation to evaluate the (intrinsic) aggression level of eachindividual (Gallup 1968; Johnsson et al. 2003; Vøllestad andQuinn 2003). Before this third experiment, the substratum ofeach compartment was cleared from excessive food particlesthat would otherwise distract the focal fish. For individualsthat ate all prey a sham food clearing was performed in orderto standardise experimental conditions. A mirror was gentlyfixed next to the plastic opaque divider and the number ofapproaches (swim against mirror) and attacks (fish attackedits mirror image as if it was a real opponent ) towards themirror was recorded during 4 min. After finishing a set ofthree trials, we repeated the same procedures on theindividual in the adjacent compartment of the same aquarium.

Social ranks

After finishing individual observations, we gently lifted thedivider between adjacent compartments and enabled con-

tact between the two juveniles, one of migratory and one ofstationary origin. During the following 10 min we studieddyadic contest behaviour in order to assess the relative rankwithin each pair of juveniles. Generally, social ranks indyads are settled through a number of interactions, startingwith display and often further escalating through chase,attack and bite (Keenleyside and Yamamoto 1962; Höjesjöet al. 1998; Johnsson and Åkerman 1998). In all the dyadiccontests, dominant fish delivered more bites and attacks,maintained a more central position and/or obtained brightercolour relative to subordinates (O’Connor et al. 1999).Once dyadic observations were concluded, all fish werekilled with an overdose of 2-phenoxyethanol and kept forgenetic analyses (see below).

Performance in the wild

On 25 May, the remaining individuals from each familywere brought back to river Norumsån and released into thesame pool to measure performance in the wild; a mean of158 individuals (range, 34–257) per family was released. Inorder to separate these fish from wild during recapture theiradipose fin were cut prior to release. On 5 September,electrofishing was conducted from 200 m downstream therelease point to 100 m upstream allowing us to estimateaverage growth, survival and dispersal from the pool foreach family group of fry. The location of each recapturedfish was recorded with an accuracy of 10 m (10 msections). All recaptured fish were later genotyped todetermine their parental origin (see below). Juvenile browntrout in this population are very stationary and seldommove further than 200 m (Kaspersson and Höjesjö 2009).Therefore, recapture rate provides a good estimate ofsurvival in the wild. Previous experiments have alsorevealed that movement of introduced fish in a novelenvironment is restricted (Bohlin et al. 2002).

Molecular methods

Assessment of family origin of experimental fish wasperformed using ten microsatellite loci Str15, Str60, Str73(Estoup et al. 1993), Ssa85, Ssa197 (O’Reilly et al. 1996),One9 (Scribner et al. 1996), Bs131 (Estoup et al. 1998),Strutta58 (Poteaux 1995), Ssa408 (Cairney et al. 2000) andSsOSL417 (Slettan et al. 1995). DNA extractions, poly-merase chain reactions, allele scoring and assignmentanalyses are described in Dannewitz et al. (2003). Assess-ment of family origin of experimental fish was performedby comparing the alleles at a given locus from eachexperimental fish with the alleles in each of the potentialparental crosses. Potential parental crosses with allelesincompatible with those of a particular offspring wereexcluded from the set of possible crosses. The markers used

Behav Ecol Sociobiol (2011) 65:1801–1810 1803

gave an extremely high discriminatory power, and 87.5% ofthe experimental fish could be assigned unambiguously to asingle parental pair.

Treatment of data and statistical analysis

Behavioural axes

We used Spearman correlations to describe associationsbetween measured behaviours and principal component anal-ysis (PCA) to summarise their associations, thereby limiting thenumber of variables describing behaviour and reducing therisk of auto-correlations. Only principal components (PC)with eigenvalue greater than one (Kaiser–Guttman criterion)were selected in further analysis. This resulted in two PCcomponents describing all the behaviours. Before analysis,we transformed PC1 with y=ln(x+4) to normalise its distri-bution (Kolmogorov–Smirnov test; NS within each family).

Sources of variation in behavioural axes

Sources of variation in PC scores were analysed in a nestedANCOVA model with female parent and male parent(nested within female parent) as random effects. Paternallife-history strategy was added as a fixed effect. We furtheradded time of behavioural testing (day after emergence) asa random factor and offspring length as a covariate to thismodel to adjust for effects of age and body size. Analysiswas started with a full model containing all possibleinteractions, and reduced by removing non-significantinteractions while retaining the main effects. The use ofmale parents differing in life history maximises thepossibility to detect among sires variation, yet causes siresto be a non-random sample of the natural population. As aresult, heritability scores were not calculated and ouranalyses aim at qualitatively showing the contribution ofgenetic and maternal effects on behaviour.

Social status

Effects of male parent life history and family on the proportionof won dyadic contests per family were assessed with non-parametric binomial and chi-square tests, respectively.

Family differences in length

Length variation between juveniles from different familiesbefore release was analysed with an ANOVA model similarto the above ANCOVA model but with length as adependent variable instead of covariate. This model wasrepeated on length measures of recaptured fry without dateas a random factor (fish were recaptured on the same day).Again, we started with the model including all possible

interactions and reduced this by removing non-significanthigher interactions.

Effects of behaviour on social ranks, and performancein the wild

Mean PC values per family were calculated as familyestimates of behaviour described by PC1 and PC2.Association between these family estimates of behaviourand dyadic contest performance (proportion dyads won perfamily), growth (mean per family), family recapture rateand movement (mean position rank per family) wereinvestigated with Spearman rank correlation. Differencesin movement between families were analysed with binomialregression. Because scores of movement were not normallydistributed, they were categorised to a binomial value (0 or 1)and entered as independent in this regression model withsimilar independent variables as for recapture length. We usedk-means clustering as a method to partition scores incategories (k=2). This method objectively divides scores inclusters depending upon their distribution and resulted in onecluster grouping individuals recaptured between 50 m down-and 50 m upstream the release location (category 1) and aremaining cluster grouping all individuals recaptured furtherthan 50 m downstream (category 0). Using Spearman rankcorrelations the following associations were tested: length atrecapture and moved distance between release and recapture,mean family length and mean family (absolute) growth,proportion of won dyads per family and mean values forfamily growth and movement and survival rate

Results

Behavioural syndromes

Despite relatively low effect size, most scores of behaviourwere correlated after controlling for false discovery rate(Table 1). PCA resulted in two principal componentstogether summarising 51% of the variation in the observedbehaviours (Table 2). PC1 summarised the main axis ofbehaviour with high scores indicating bold and aggressiveindividuals (i.e. the shy–bold syndrome) and with highloadings for all behavioural scores across contexts exceptapproaches to novel prey. PC2 describes scores of behav-iour deviating from this general pattern, with high scoresindicating individuals that were less aggressive than theaverage and performed more approaches to the prey.

Family differences in length

Initial length was 28.1 mm (±0.31 SE) and differed betweenoffspring from different females (ANOVA, F8,7=34.51,

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p<0.0001), whereas offspring from male parents differingin life history (ANOVA, F1,3=0.40, p=0.57) or differentmale parents within each female (ANOVA, F8,83=1.13,p=0.35) had similar length. Also time of measurementaffected length, reflecting growth throughout the experi-ment (ANOVA, F10,6=18.50, p=0.001), and the higherorder interaction between male parent, female parent andtime of measurement affected length, suggesting differentgrowth trajectories between families and/or rearing tanks(ANOVA, F74,168=1.61, p=0.006). No other interactionswere significant.

Sources of variation in behavioural syndromes

PC1 was significantly affected by the identity of the femaleparent, but not by male parent life-history strategy or maleidentity (Table 3, Fig. 1a). Variation in behaviour describedby PC2, on the other hand, was significantly affected by

male parent life history where offspring from stationarymales had higher levels of PC2 behaviour (moreapproaches towards novel prey and less attacks towardsthe mirror) than those from migratory males (Table 3,Fig. 1b). Length also affected this behaviour, with largerindividuals having lower PC2 scores (Table 3). Femaleidentity or male identity within each female did not affectPC2 (Table 3, Fig. 1b).

Dyad performance

Dominance rank was determined in 78.9% of the dyads. Inthe remaining dyads the fish did not interact. Theproportion of dyadic contests won varied between offspringfrom different families (Fig. 2), but the male migratory typehad no effect, as roughly half of the dyadic contests (70 of142) were won by the offspring of a resident male(Binomial test, p=0.93). The proportion of won dyads didnot correlate with family estimates for PC1 (Spearmanranked correlation; rho=0.11, N=18, p=0.66), PC2 (rho=0.13, N=18, p=0.62) or average length of offspring withineach family (rho=−0.16, N=18, p=0.54).

Performance in the wild

Eighty-eight of 2,682 released individuals were recaptured(3.28%), of which 77 were identified to family. The averagerecapture location was downstream the release point withan average downstream movement of 40 m (range 190 m).Small fish moved further downstream than large individuals(rho=0.261, N=77, p=0.02). Offspring from families withlarge average body length were larger also at recapture(rho=0.69, N=15, p=0.004). As a result, differences inlength between offspring from different female parents werealso present after recapture (ANOVA: F8,7=4.46, p=0.03).Distance moved from release was not affected by differ-ences between male parents mated with the same femaleparent (Wald=2.68, df=5, p=0.8), male parent life history

Table 2 PCA analysis on offspring behaviour

Principal components PC1 PC2

Novel object

Approach 0.584 0.359

Attack 0.608 0.132

Novel prey

Approach 0.327 0.549

Attack 0.660 0.253

Aggression

Approach 0.599 −0.475Attack 0.635 −0.555Eigenvalue 2.02 1.05

Percent of total variance 33.62 17.44

Loadings, eigenvalues and explained variance are given for the twoemerging principal components. Only components with eigenvalueabove 1 were retained (Kaiser–Guttman criterion). Loadings withabsolute value above 0.5 are shown in bold

Attack novelobject

Approachnovel prey

Attack novelprey

Approachmirror

Attackmirror

Approach novelobject

rho 0.336 0.219 0.246 0.248 0.218

p <0.0001 <0.0001 <0.0001 <0.0001 <0.0001

Attack novelobject

rho 0.127 0.405 0.313 0.368

p 0.016 <0.0001 <0.0001 <0.0001

Approach novelprey

rho 0.268 0.125 0.106

p <0.0001 0.018 0.044

Attack novelprey

rho 0.231 0.206

p <0.0001 <0.0001

Approach mirror rho 0.521

p <0.0001

Table 1 Correlation matrixfor the different offspringbehaviours

N=360 for all tests, p values inbold remain significant afterfollowing the procedures forcontrolling false discovery rate(Benjamini and Hochberg 1995)

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Dependent factor Effects d.f. F value p value

Offspring PC 1 Length (mm) 1.331 2.57 0.11

Date 10.331 6.77 <0.001

Male parent LH 1.8 2.92 0.13

Female parent 8.9 4.47 0.02

Male parent LH (female parent) 8.331 0.91 0.51

Offspring PC 2 Length (mm) 1.331 4.42 0.04

Date 10.331 0.53 0.87

Male parent LH 1.8 7.74 0.02

Female parent 8.8 1.55 0.27

Male parent LH (female parent) 8.331 1.50 0.16

Table 3 Nested ANCOVAtesting for the effects of femaleparent, male parent life history(male parent LH), offspringlength and date of measurementon the two behavioural axes oftheir offspring

Fig. 1 Variation in PCsbetween different families.Each of nine females was matedwith a different migratory andstationary male. Bars representmeans±SE. a PC1 wastransformed as ln(PC1+4).b PC2 (+1)

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(Wald=0.60, df=1, p=0.44) or female parent (Wald=4.13,df=8, p=0.85). Also none of the family estimates forbehaviour predicted differences in the proportion ofrecaptured individuals (in PC1 rho=−0.14, N=17, p=0.58;PC2 rho=−0.10, N=17, p=0.69), growth (in PC1 rho=0.08,N=15, p=0.77; PC2 rho=0.05, N=15, p=0.87) or move-ment (in PC1: rho=−0.11, N=15, p=0.69; PC2: rho=−0.19,N=15, p=0.50) between families in the field. The proportionof dyads won by offspring of each family was a poorpredictor of survival (rho=0.02, N=17, p=0.95), growthrate (rho=0.05, N=15, p=0.85) or movement (rho=−0.36,N=15, p=0.19).

Discussion

The shy–bold syndrome

The behaviour of brown trout fry showed weak butsignificant consistency across the three different contexts.Fry that responded bold towards a novel object alsoaccepted a novel food item earlier and responded moreaggressively towards their own mirror image. This shy–bold syndrome, represented by PC1, explained 34% of thebehavioural variation. This is consistent with previous workidentifying the shy–bold syndrome in a range of species(Wilson et al. 1993, 1994; Sih and Bell 2008). Deviationsfrom the shy–bold syndrome (PC2), where less aggressiveindividuals performed more approaches to the foodexplained 17% of the remaining behavioural variation.

However, based on the output from the analyses neitherboldness (PC1) nor PC2 seemed to be associated withgrowth or survival in the wild suggesting that several

behavioural strategies can yield similar fitness in browntrout fry. This result is inconsistent with recent theoriessuggesting that behavioural syndromes (e.g. boldness)can be explained by their association with growthvariation among life-history strategies, a specific predic-tion being that bold individuals should show fastergrowth associated with higher mortality rate (Stamps2007; Biro and Stamps 2008; Careau et al. 2008). Ourresults rather add to the view that the link between growthrate and behaviour is often flexible and dependent onspecific environmental conditions (Sundbaum and Näslund1998; Höjesjö et al. 2004; Sneddon et al. 2006). However,due to the relatively low statistical power in this study wemight have been unable to detect some correlations betweenbehaviour, growth and survival.

Paternal life-history effects

Similarly, our study could not detect any effect of paternallife history on fry growth or survival in the wild. Althoughsuch effects may manifest themselves later in life by gene–environment interactions, our results seem to indicate thatthe choice of migratory strategy in salmonid fishes is to alarge extent conditional within populations (see e.g. thereview in Hendry et al. 2003; Olsson et al. 2006), as hasalso been shown in many other species, including birds(Schwabl 1983). This is also consistent with a previousstudy on brown trout showing that the decision to mature in1+ brown trout is associated with the body condition theprevious fall (Bohlin et al. 1994), and also with anexperiment showing similar levels of aggression instream-resident and migratory brown trout fry (Bohlin et al.2002). However, the lack of paternal life-history effects on

Fig. 2 Proportion of dyadiccontests won by offspring indifferent families. The dashedline indicates the point of equalamount of dyadic contests wonand lost

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parr behaviour and performance per se does not necessarilymean that migration tendency is purely conditional. It couldsimply mean that migrants are as well adapted to theircommon riverine environment as are the residents.

Not all behavioural variation of fry could be explainedby the shyness–boldness syndrome (PC1). Deviations fromthis pattern were caused by some individuals that were lessaggressive and made more approaches to the food (PC2).This second axis of behaviour was influenced by parentalmale type, where resident males showed more tendency forthis behavioural pattern. The biological significance of thisbehavioural pattern should be interpreted with caution, butwarrants further investigation on the behavioural effects ofpaternal life history.

Female parent effects

Offspring boldness was significantly affected by maternity.Due to the limited number of tanks available all individualwithin one half-sib group were reared together. Even if thisis a weakness in our study, tank conditions were verysimilar and the tank effects were likely to be small. Wetherefore believe that the observed effects were mainly dueto differences among sib groups. Previous studies haveshown that genetic variation affects agonistic and risk-taking behaviour in salmonids (Johnsson and Abrahams1991; Riddell and Swain 1991; Lahti et al. 2001; Vøllestadand Quinn 2003; Sundström et al. 2004). In addition,aggressive and dominant individuals have been reported tohave higher standard metabolic rate with a narrow scope, i.e. ahigh energetic expenditure, forcing them to be moreaggressive in order to gain access to food (Cutts et al.2002). However, the absence of strong paternal effectsmay suggest that the maternal environment might havebeen more important than genetic effects in our study(Falconer and Mackay 1996). Interestingly, a recent studyon brown trout showed evidence for substantial maternaleffects on fry metabolism, affecting growth and energeticneeds of fry after yolk absorption (Regnier et al. 2010).Such differences can arise, for instance, through variationin provisioning of energy or hormones to the eggs by differentfemales. In addition to egg energy contents, birds are shown tomanipulate the levels of androgen hormones provided to theegg (as reviewed in Groothuis et al. 2005). As a consequence,chicks tend to differ in growth (e.g. Schwabl 1996) andbehaviour (e.g. aggression, Müller et al. 2009), suggesting apotential additional maternal control over behavioural andgrowth strategies of their young. To our knowledge, studiesof such hormonal mechanisms in fish are rare (but seeMcCormick 1998; Sloman 2010), and may provide aninteresting area of future research.

Einum and Fleming (1999) have demonstrated thatvariation in egg size leads to more extreme asymmetries

in growth and fitness when habitat conditions are poor,suggesting that these effects are often underestimated inhatchery-reared individuals. This view is supported by theresults of the present study, where the female effect onvariation in fry size persisted over the first growth period inthe wild, suggesting that these effects may influenceoffspring fitness during early life when major selectionoccurs in salmonid streams (Elliott 1994).

Acknowledgements We are grateful to the staff at Laholm fish farmfor taking care of the fish and to Rasmus Kaspersson, Linus Anderssonand James Orpwood for great field assistance. We also thank Ian Flemingand Alison M. Bell for helpful comments on the manuscript. JH and JIJwere financed by the Swedish Research Council for AgriculturalResearch and Spatial Planning. The experiments were approved by theEthical Committee for Animal Research in Gothenburg (License 132/2005) and comply with the laws in Sweden.

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