Fish behavioral types and their ecological consequences€¦ · PERSPECTIVE Fish behavioral types...

PERSPECTIVE

Fish behavioral types and their ecological consequencesGary G. Mittelbach, Nicholas G. Ballew, and Melissa K. Kjelvik

Abstract: Fish have proven to be model organisms for the study of animal personalities, and a rich literature documentsconsistent interindividual behavioral differences in a variety of species. However, relatively few studies have examined theecological consequences of such consistent interindividual differences in behaviors in fish or other organisms, especially underfield conditions. In this review and perspective, we discuss the factors that may lead to the formation and maintenance ofbehavioral types in fish populations. We then examine what is known about the effects of personality variation on individualgrowth and survival, breeding behaviors and reproductive success, habitat use, diet, and ontogenetic niche shifts, migration anddispersal, as well as potential consequences for species interactions and ecosystem functioning. We focus as much as possible onstudies conducted under natural or seminatural conditions, as such field studies are most relevant to elucidating the ecologicalconsequences of behavioral variation. Finally, we discuss the potential importance of consistent individual differences inbehaviors to fisheries management and conservation, specifically examining consequences for recreational and commercialfishing, hatchery rearing, and stock enhancement.

Résumé : Les poissons s’avèrent être des organismes modèles pour l’étude des personnalités animales, et de nombreuses étudesdocumentent l’existence de différences comportementales cohérentes entre individus au sein d’espèces variées. Assez peud’études ont toutefois examiné les conséquences écologiques de telles différences cohérentes entre individus chez les poissonsou d’autres organismes, plus particulièrement dans des conditions naturelles. Dans la présente synthèse, nous abordons lesfacteurs qui pourraient mener a la formation et au maintien de différents types comportementaux dans les populations depoissons. Nous examinons ensuite l’état des connaissances sur les effets des variations de personnalité sur la croissance et lasurvie individuelles, les comportements et le succès de reproduction, l’utilisation de l’habitat, le régime alimentaire, et leschangements de niche, la migration et la dispersion ontogéniques, ainsi que les conséquences possibles sur les interactions entreespèces et la dynamique des écosystèmes. Nous mettons l’accent, dans la mesure du possible, sur les études réalisées dans desconditions naturelles ou semi-naturelles parce que ces études de terrain sont les plus pertinentes pour élucider les conséquencesécologiques des variations comportementales. Enfin, nous abordons l’importance éventuelle de différences individuelles co-hérentes sur le plan des comportements pour la gestion et la conservation des espèces halieutiques, en examinant plusparticulièrement les conséquences sur la pêche sportive et commerciale, l’élevage en écloserie et la mise en valeur des stocks.[Traduit par la Rédaction]

IntroductionFish, like many other vertebrates, show consistent individual

differences in behavior despite maintaining a high degree of be-havioral plasticity. These consistent interindividual differences inbehavior have been variously termed animal personalities (Dallet al. 2004), behavioral profiles (Groothuis and Trillmich 2011),temperaments (Réale et al. 2007), coping styles (Koolhaas et al.1999), or behavioral syndromes (Sih et al. 2004a, 2004b). Much ofthe large and rapidly expanding literature on animal personalitiesinvolves studies with fish (Stamps 2007), and it was early work byHuntingford (1976, 1982) with sticklebacks, and Ehlinger andWilson (1988) and Wilson et al. (1993, 1994) with sunfish, thatprovided some of the first evidence that individuals may exhibitconsistent differences in behavioral traits within a population(e.g., individuals may be relatively shy or bold, aggressive ortimid). Wilson et al. (1993) suggested that such consistent behav-ioral differences between individuals represented more than ran-dom variation around an adaptive mean. Rather, “individualdifferences are interpreted not as the raw material on which nat-ural selection acts but as the end product of natural selection”(Wilson et al. 1993: page 255). That is, variation in behavioral traits

may be maintained within a population because such variationrepresents different adaptive solutions to a complex environment(e.g., Wolf and McNamara 2012).

Although studies of animal personalities initially struggled togain traction against the idea that variation in phenotype is ex-pected within a population and therefore does not require a spe-cial explanation (Wilson 1998), subsequent years have validatedthe early insights of Huntingford, Wilson, and their colleagues.Today the study of consistent individual differences in behaviorenjoys a vigorous growth, as evidenced by the publication of anumber of recent reviews (e.g., Sih et al. 2004a, 2004b; Réale et al.2007; Sih and Bell 2008; Stamps and Groothuis 2010; Wolf andWeissing 2012), including three reviews devoted specifically tofish (Toms et al. 2010; Budaev and Brown 2011; Conrad et al. 2011).As Wolf and McNamara (2012) note, three key features associatedwith personalities have been observed in a variety of species:(i) variation, individuals differ in their behaviors; (ii) consistency,individual differences in behaviors are stable over time; and(iii) correlations, certain behavioral traits (e.g., boldness, aggres-sion, and exploration) tend to be correlated among individuals.

Although consistent individual differences in behavior are nowwell documented in fish and other organisms, for the most part

Received 24 October 2013. Accepted 24 February 2014.

Paper handled by Associate Editor Dylan Fraser.

G.G. Mittelbach, N.G. Ballew, and M.K. Kjelvik. W.K. Kellogg Biological Station and Department of Zoology, Michigan State University, HickoryCorners, MI 49060, USA.Corresponding author: Gary G. Mittelbach (e-mail: [email protected]).

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Can. J. Fish. Aquat. Sci. 71: 1–18 (2014) dx.doi.org/10.1139/cjfas-2013-0558 Published at www.nrcresearchpress.com/cjfas on 26 February 2014.

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http://dx.doi.org/10.1139/cjfas-2013-0558

these studies have been conducted in the laboratory under sim-plified and highly controlled conditions. Studies of behavioraltrait variation under natural or seminatural conditions are stillquite rare (e.g., Fraser et al. 2001; Biro et al. 2007; Adriaenssens andJohnsson 2011a). While laboratory studies have opened the door tothe rich array of behavioral diversity found in nature, a key ques-tion before us is what are the ecological consequences of consis-tent individual differences in behavior to organisms in the wild(Dingemanse and Réale 2005; Archard and Braithwaite 2010;Bolnick et al. 2011; Adriaenssens and Johnsson 2011a; Sih et al.2012; Wolf and Weissing 2012). These ecological consequencesinclude potential effects on an individual’s survival and reproduc-tive success, population dynamics (through influences on species’vital rates, e.g., growth, fecundity, and survival), communitystructure and species diversity (through influences on species in-teractions), and on the conservation and management of naturalresources (Fig. 1). To understand these consequences of animalpersonalities, we need to study organisms in the complex envi-ronments found in nature (Stamps and Groothuis 2010).

Our goal in this paper is to review what is known about theecological consequences of behavioral trait variation in fishes atthe individual, population, and community levels, including theconsequences of personality for the conservation and manage-ment of fishes. More than 20 years ago, Wilson et al. (1993) notedthat the ecological consequences of such consistent individualdifferences had not been studied in a natural population of anyspecies. Despite the explosion of research into animal personali-ties since the paper of Wilson et al, the ecological and evolution-ary consequences of consistent interindividual differences inbehavioral traits in natural populations are only now coming intofocus (Bolnick et al. 2011; Dall et al. 2012; Sih et al. 2012; Wolf andWeissing 2012). We begin our review with a short description of

terminology and measurement issues in the study of animal per-sonalities, followed by a discussion of the proximate and ultimatefactors that may lead to consistent interindividual differences inbehavior. We then examine what is known about the ecologicalconsequences of behavioral types in fishes, including effects atthe individual, population, and community levels. We focus asmuch as possible on studies conducted under natural or semi-natural conditions, as such field studies are most relevant toelucidating the ecological consequences of behavioral variation.Finally, we discuss the potential importance of consistent individ-ual differences in behavior to fisheries management and conser-vation, specifically examining consequences for recreational andcommercial fishing, hatchery rearing, and stock enhancement.

Terminology and measurementMultiple terms surround the discussion of animal personalities,

which has led to considerable debate in the literature. Table 1 listsmany of the terms used in the study of animal personalities anddefines how we use these terms in the current paper. The termsanimal personality, temperament, and coping style have beenused more or less synonymously (Réale et al. 2007). These termsdescribe consistent differences between individuals in behaviorsacross contexts over some period of time and are most often usedto refer to general behavioral patterns (e.g., individual differencesin boldness, activity, and aggressiveness and the relationshipsbetween them). We use the term behavioral type to describe anindividual’s phenotype (e.g., bold versus shy; aggressive versustimid) relative to other individuals in the population.

One of the challenges in assessing personality traits in fish andother species is the fact that behavior can be extremely plastic;individuals often respond to changes in their environment byadjusting their behaviors to meet current conditions. Further,

Fig. 1. The consequences of variation in fish behavioral types may be expressed at different levels of ecological organization (from individualsto ecosystems) and have implications for conservation and management, as well as basic biology.

Level of organization Biological effects Conservation and management

Population,Community, and Ecosystem

Individual

Consistent individual differences in behaviors (e.g., shy vs bold, aggressive vs �mid)

size at maturity, size at harvest, vulnerability to commercial catch gear, vulnerability to recreationalangling

diet, habitat use, growth, survival, ontogenetic niche shifts,reproductive success

social structure, group feeding rate, population dynamics, species interactions, nutrient dynamics

domestication, stocking success, migration, return rate, harvestable population


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individuals may differ in their degree of behavioral plasticity,which at the individual level could affect the measurement ofpersonality traits (Nussey et al. 2007; Dingemanse et al. 2010) andat the population level could affect stability and population per-sistence in response to environmental change (Dingemanse andWolf 2013). A useful framework for examining personality traitsin light of behavioral plasticity is the concept of behavioral reac-tion norms (Fig. 2). The reaction norm framework illustrates howindividual differences in personality traits can be assessed acrossmultiple contexts to examine consistency of behavioral types andthe extent of behavioral plasticity within and between individuals(Réale et al. 2007; Dingemanse et al. 2010). For example, Budaevand Brown (2011) provide a table of over a dozen measures thathave been used to assess boldness in fish (e.g., predator inspec-tion, foraging under predation risk, latency to emerge from cover,behavior in an open field, etc.). Measuring individuals in a numberof these contexts would allow for the development of reactionnorms that would more accurately characterize an individual’spersonality type.

The behavioral reaction norm approach also provides an oppor-tunity to identify which measures actually quantify the same per-sonality trait. The few studies that have investigated correlationsamong different personality measures that were thought to quan-tify the same trait have found some surprising results (Carter et al.2013; Garamszegi et al. 2013). For example, two measures that areoften assumed to quantify aggression were investigated in yellow-bellied marmots (Marmota flaviventris). While both measures wererepeatable over time, they were independent from each other(Blumstein et al. 2012). A similar result was found when investi-gating two measures that are often assumed to quantify boldness(i.e., response to a novel object and response to a predator; Carteret al. 2012). These results show how different ways of measuringa personality trait may not be interchangeable, providing addi-tional justification for taking a reaction norm approach.

The application of behavioral reaction norms is still relativelynew and not yet widely applied. Nevertheless, numerous studiesof behavioral types in fish and other organisms provide resultsthat allow us to explore the ecological consequences of personal-ity variation, as long as we are careful in our interpretation and

recognize that different ways of measuring a personality trait like“boldness” may in fact measure different things (Réale et al. 2007).Finally, while this review and prospectus focuses on personalityvariation in fish and its ecological consequences, we want to em-phasize the wealth of studies that exist for other taxa. These stud-ies provide a broader context in which to view the results fromfishes, and we refer readers to publications by Réale et al. (2000),Dall et al. (2004), and Dingemanse and Réale (2005), as well as thereview papers cited in the Introduction, as an entry point to theliterature on animal personalities in birds, mammals, and othergroups.

The evolution and maintenance of variation in behavioraltraits

Fitness tradeoffsThe fitness consequences of behavioral traits are often context-

dependent. For example, bold behavioral types may be less fitthan shy behavioral types in an environment with high levels ofpredation, while the opposite may be true in an environmentwithout predators. Behavioral ecologists have focused on fitnesstradeoffs as an important mechanism to explain the generationand maintenance of variation in behavioral traits within a popu-lation, both on ecological and evolutionary time scales. For exam-ple, consider the situation where individuals that are bolder aremore likely to encounter predators, resulting in higher mortalityrates. Now imagine that these bolder individuals are also morelikely to encounter more prey per unit foraging time and there-fore experience higher feeding rates, resulting in higher energygains and growth (Stamps 2007). As a result, under this hypothet-ical scenario, a potential tradeoff between energy gain and sur-vival would exist that could maintain variation in boldness.

Mangel and Stamps (2001) developed a simple model to showhow tradeoffs between growth and survival can result in a rangeof individual growth rates that all yield equivalent fitness (asmeasured by r in the Euler–Lotka equation), thus favoring themaintenance of multiple behavioral types within a population.Similarly, models for the evolution of interindividual differencesin dispersal rates have been developed under the premise that the

Table 1. Glossary of terms related to animal personality.

Term Definition

Behavior / behavioralresponse

An individual’s action or response at a given time in a given context.

Behavioral / personalitytrait

A behavioral pattern that characterizes consistent individual differences in behavior in a given type of situation.For example, boldness characterizes consistent individual differences in behavior in situations that involve risk.

Behavioral / personalitytype

An individual’s consistent response over a given period of time relative to other individuals for one or morebehavioral traits. For example, an individual could be relatively bold or shy in situations that involve risk taking.

Animal personality A behavioral pattern that can describe multiple behavioral traits and the relationship between those traits acrosstime (Réale et al. 2007; Stamps and Groothuis 2010).

Differential consistency Consistency between individuals in a particular behavior (or behavioral trait) across time (Stamps and Groothuis2010).

Contextual generality Consistency between individuals in behaviors measured in different contexts (e.g., activity in a safe, familiarenvironment and activity in an unfamiliar environment).

Structural consistency Consistency across time in the correlation between two behaviors in a group (Stamps and Groothuis 2010).

Behavioral syndrome Correlated suites of behaviors. Such correlations may occur within an individual (i.e., an individual’s tendency tobehave in a certain way may be correlated across contexts or over time). In this sense, behavioral syndromes andanimal personalities describe similar phenomena. A behavioral syndrome also may describe a correlationbetween two or more behavioral traits between individuals in a population (e.g., boldness and aggression arecommonly correlated when examined in a group of individuals; Sih and Bell 2008).

Pace-of-life syndrome A suite of covarying behavioral, physiological, and life-history phenotypic traits arrayed on a continuum from“slow” to “fast” lifestyles.

Note: Definitions refer to how terms are used in the current text and are not meant to resolve disputes in meaning. See also Stamps and Groothuis (2010); Wolf andWeissing (2012).


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expected fitness of “dispersers” equals the expected fitness of“stayers”, due to a growth–mortality tradeoff (Hamilton and May1977; Frank 1986; Johst and Brandl 1999; Ronce et al. 2000).

Fish often face situations in nature where there is a potentialtradeoff between increased feeding rate and reduced survival(Lima 1998; Mangel and Stamps 2001). For example, (i) open-water(pelagic habitats) may contain richer food resources but posehigher predation risk (e.g., Werner and Hall 1988; Gliwicz et al.2006), (ii) daytime foraging may yield a higher feeding rate butgreater risk of predation than nocturnal foraging (e.g., Fraser andMetcalfe 1997; Metcalfe et al. 1999; Ryer and Hurst 2008), and(iii) more active foragers may encounter more prey (or richer habitats)and grow faster but suffer higher mortality rates (e.g., Werner andAnholt 1993; Fraser et al. 2001; Biro et al. 2004, 2006; Sundströmet al. 2004). Fitness tradeoffs can also occur spatially (e.g., one areaof a habitat favors one behavioral type, while another area favorsa different one), temporally within generations (e.g., across devel-opment or across genetically linked behavioral traits), and tempo-rally between generations (e.g., frequency-dependent selection).

Interindividual differences in metabolism and stateWhile fitness tradeoffs provide a powerful mechanism that may

select for a variety of (equal fitness) behavioral types within apopulation, the maintenance of consistent behavioral types orpersonalities over time requires more than just a fitness tradeoff.To see this, consider the following question: what prevents indi-viduals from continually shifting back and forth between differ-ent behavioral types that have equivalent fitness? Or, stated inanother way — why do we find differential consistency (as definedin Table 1) in behavioral types within a population (e.g., individu-als that are consistently bolder than others over time)? One pos-sibility is that individuals differ in their relatively unchangingphysiological traits (e.g., resting metabolic rate or the size of met-abolically costly organs); therefore, the behavioral type that re-sults in the optimal value of the growth–mortality tradeoff differsdepending on physiological state. A number of authors (Stamps2007; Biro and Stamps 2010; Houston 2010) have suggested thatconsistent individual differences in physiological state could bean important factor promoting the formation of individual differ-ences in personality. The first step in examining this hypothesis isto determine whether individuals differ consistently in theirphysiological traits (e.g., resting metabolic rates or potentialgrowth rate); the second step is to determine whether any suchdifferences in physiological measures are correlated with behav-ioral traits (see Biro and Stamps (2010) for a review of the literature

on resting metabolic rate and their relationship to behavioraltraits).

Recently, it has been suggested that behavioral traits may co-vary with a whole suite of physiological and life-history traits,such that these covarying phenotypic traits can be effectivelygrouped under the umbrella of a “pace-of-life syndrome” (Réaleet al. 2010). Figure 3 illustrates the potential integration of life-history, behavioral, and physiological traits along a pace-of-lifecontinuum from “slow” to “fast”. Evidence for a pace-of-life syn-drome in fish or other organisms is still tentative (Adriaenssensand Johnsson 2009). However, Biro and Stamps (2008) show thatbehavioral traits are linked to life-history variation in a variety oforganisms, including fish. For example, activity rates and bold-ness are positively related to growth rates in rainbow trout(Oncorhynchus mykiss; Biro et al. 2004, 2005, 2007), and boldness ispositively related to growth, fecundity, and size at maturity inAtlantic silverside (Menidia menidia; Walsh et al. 2006). The pace-of-life syndrome provides a useful heuristic framework in whichanimal personality studies can be integrated to address how be-havioral traits are maintained within populations, and how theymay have ecological consequences affecting individual growth,survival, and reproductive success, as well as population dynam-ics and successful resource management. Moreover, viewingbehavioral variation in the light of life-history traits and the pace-of-life syndrome allows us to consider the impacts of behavioraltrait variation at different life stages and to better understandwhen and why personality types may be maintained over ontog-eny (e.g., Schürch and Heg 2010; Chervet et al. 2011), even poten-tially across metamorphosis (e.g., Wilson and Krause 2012a,2012b).

There are additional ways in which the “state” of an individualcan affect the relative costs and benefits of different behavioralactions, leading to the generation and maintenance of adaptivebehavioral trait variation within a population (Houston andMcNamara 1999; Dingemanse and Wolf 2010; Luttbeg and Sih2010; Wolf and Weissing 2010, Wolf and McNamara 2012). In thecase of foraging boldness (where taking greater risk yields higherrewards), Luttbeg and Sih (2010) show how positive-feedbackmechanisms can maintain differential consistency in behavioraltraits. For example, if individuals having higher state (e.g., bettercondition, larger size, and more energy reserves) are better atdefending themselves or fleeing from predators, then animalswith higher state will have lower predation risk while being boldand should be bolder than low state individuals (Luttbeg and Sih

Fig. 2. Five scenarios (a–e), each depicting the behavior of four individuals (solid horizontal lines) in two different situations (S1 and S2). Inscenario a, all individuals display the same phenotypes in both S1 and S2 and there is plasticity between situations. In scenario b, there isphenotypic variability in situations S1 and S2 (equal between situations), no plasticity between situations, and consistent interindividualdifferences in phenotype between situations. In scenario c, there is phenotypic variability in situations S1 and S2 (equal between situations),plasticity between situations, and consistent interindividual differences in behavior. In scenario d, there is unequal phenotypic variationbetween situations S1 and S2 (S2 has much more), interindividual differences in plasticity between situations (the individual with the smallestphenotype has high individual plasticity, while the individual with the second smallest phenotype demonstrates a lower level of plasticity),and consistent interindividual differences in behavior (perfect consistency in rank order but less in the raw values). In scenario e, there isphenotypic variability in situations S1 and S2, plasticity between situations, but individuals do not show consistent differences in behavioracross situations because of differential directionality in responses. Modified from Dingemanse et al. (2010).




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2010). Thus, small differences in initial state between individuals(e.g., due to parental provisioning and carryover from larval toadult stages) can lead to a positive-feedback loop between assetsand behaviors, such that “….individuals that already have highstate (assets) would be bold, and thus gain more resources thatmaintain their high state” (Luttbeg and Sih 2010: page 2979). Inaddition, positive feedbacks based on experience or learning canlead to differences in foraging efficiency in a habitat or on a par-ticular prey type that can act to reinforce and maintain behavioraldifferences between individuals (Werner et al. 1981; Dingemanseand Wolf 2010).

Ecological consequences of behavioral types“Surprisingly little attention has been paid to the ecologicaland evolutionary consequences of personality differences”

(Wolf and Weissing 2012: page 452).

In the sections above, we examined the factors thought to drivethe evolution and maintenance of animal personalities in fish andother organisms. These mostly theoretical studies seek to provide“ultimate” evolutionary explanations for the existence of consis-tent differences in behaviors between individuals. In the follow-ing sections, we focus on the ecological consequences of thesebehavioral differences. That is, given the presence of varying be-havioral types within a population, how might this behavioralvariation affect the ecology, management, and conservation offishes. These ecological consequences may include effects on anindividual’s survival and reproductive success, the dynamics ofpopulations (through influences on species’ vital rates, e.g.,growth, fecundity, and survival), effects on community structure

and species diversity (through influences on species interactions),and impacts on the management and conservation of species andfish stocks (e.g., through hatchery rearing and supplementalstocking). We recognize that separating the factors thought toultimately drive the evolution of behavioral types in fishes fromthe more proximate consequences of such behavioral types to theecology of individuals and populations is a somewhat false dichot-omy. Ecology and evolution go hand in hand. Still, this distinctionis useful for highlighting how the existence of behavioral typeswithin a population may impact various aspects of an individual’secology (e.g., growth, survival, diet, and habitat use), as well aspopulation dynamics and species interactions.

Ecological consequences at the individual level

Growth and survivalPersonality traits have the potential to affect an individual at

nearly every stage of development, from a juvenile’s chances ofsurviving to adulthood to an adult’s reproductive success. Wesummarize what is known about the ecological consequences ofbehavioral trait variation in fish at the individual level in Table 2.Table 2 includes both laboratory and field studies. However, in thediscussion below we focus on the results from natural and semi-natural environments, as field studies provide the most directtests of the ecological consequences of behavioral trait variation.Looking first at the impact of boldness, aggressiveness, and explo-ration on individual growth, dispersal, and survival, we find sup-port for a hypothesized growth–mortality tradeoff, although theevidence from field studies is surprisingly limited.

Fraser et al. (2001) found that bolder individuals of the Trinidadkillifish (Rivulus hartti) moved greater distances in the field. More-over, movement distance was positively correlated with individ-ual growth over a 19 month mark–recapture study in a section ofriver containing Rivulus predators. However, in a predator-absentzone, there was no correlation between movement and growth(Fraser et al. 2001). Our own studies with juvenile bluegill (Lepomismacrochirus) in ponds have shown a positive correlation betweenboldness measured in the laboratory and individual growth ratesobserved in the field over periods of 2–6 months (M. Kjelvik andG. Mittelbach, unpublished data). In studies comparing domesticand wild strains of salmon and trout, Sundström et al. (2004) andBiro et al. (2003a, 2003b, 2004) examined the growth, survival, andhabitat use of fish in the presence and absence of predators.Sundström et al. (2004) found a tradeoff between growth andsurvival for strains of coho salmon (Oncorhynchus kisutch) trans-genic for growth hormone (GH) relative to wild salmon. In semi-natural stream channels, GH-transgenic coho fry grew faster thanwild coho fry but suffered higher mortality from predators (non-transgenic coho juveniles) (Sundström et al. 2004). Higher mortal-ity on GH-transgenic fry was most pronounced under low-foodconditions. Other studies have documented increased risk-takingbehavior in GH-transgenic salmon in the laboratory (Abrahamsand Sutterlin 1999; Sundström et al. 2003), as well as increasedmovement by GH-enhanced trout in the wild (Sundt-Hansen et al.2009). Thus, there appears to be an interaction between behavior,growth, and mortality when comparing salmon and trout strainsmodified with GH relative to wild populations (but see Johnssonand Björnsson 2001).

In a series of whole-lake experiments, Biro et al. (2003a, 2003b,2004, 2006) compared the growth, survival, and habitat use ofdomestic (hatchery stock) and wild strains of rainbow trout(Oncorhynchus mykiss). In the presence of avian predators (loons, Gaviaimmer), age 1 domestic trout grained 20% more mass than wildtrout (Biro et al. 2004), and age 0 domestic trout gained 100% moremass than wild trout (Biro et al. 2006). However, domestic trout(age 0 and age 1) suffered 50%–60% greater mortality than wildtrout when predators were present (Biro et al. 2004, 2006). Behav-ioral differences between domestic and wild strains in the field

Fig. 3. A representation of different phenotypic traits along thepace-of-life continuum. Double arrows illustrate presumedcontinuous variation in a trait, with traits grouped under life-historystrategies, behavior, and physiology, and distributed along a pace-of-life continuum from “slow” to “fast”. Modified from Réale et al. (2010).

pace of life

slow fast

life history

long life short life

delayed reproduction early reproduction

slow growth fast growth

low fecundity high fecundity

behavior

shy bold

timid aggressive

low activity high activity

extensive explorer superficial explorer

limited dispersal extensive dispersal

social asocial

physiology

low metabolic rate high metabolic rate

high immune response low immune response

low potential growth rate high potential growth rate

small metabolically costly organs large metabolically costly organs

w faff


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Table 2. Summary of evidence for the ecological consequences of behavioral types in fishes at the individual level.

Consequence Trait(s) Result Study Study method

Dispersal Boldness Bolder fish had a higher propensity to disperse. Fraser et al. 2001 FieldSociability More asocial fish had a higher tendency to disperse. Cote et al. 2010 Laboratory

Social network Boldness Bolder fish had fewer total social connections andthe average strength of the connections were weaker.

Croft et al. 2009 Field

Growth Exploration and aggressiveness Slow explorers grew faster. Aggressiveness wasnot related to growth.

Adriaenssens and Johnsson 2011a Field

Boldness No correlation between boldness and growth. Höjesjö et al. 2011 FieldBoldness Bolder fish grew faster. Ward et al. 2004 Laboratory

Survival Boldness Bolder fish were preyed on more. Dugatkin 1992 LaboratoryExploration and aggressiveness Neither exploration nor aggressiveness was related

to survival.Adriaenssens and Johnsson 2011a Field

Exploration More exploratory individuals had higher survival. Adriaenssens and Johnsson 2011a FieldBoldness No correlation between boldness and survival. Höjesjö et al. 2011 FieldActivity, boldness, and exploration More active, bold, and exploratory individuals

survived longer with predators.Smith and Blumstein 2010 Laboratory

Social status Boldness Bolder fish were more dominant. Dahlbom et al. 2011 LaboratoryAggressiveness, boldness, and activity Males that were more aggressive, bolder, and more active

had higher positions in the dominance hierarchy.McGhee and Travis 2010 LaboratoryColleter and Brown 2011 Laboratory

Reproduction Boldness Females chose bolder males as mates. Godin and Dugatkin 1996 LaboratoryAggressiveness Females chose low or moderately aggressive males,

whereas highly aggressive males were rarely chosen.Ward and Fitzgerald 1987 Laboratory

Boldness and activity Assortative mating based on personality type. Budaev et al. 1999 LaboratoryBoldness and aggressiveness Bolder and more aggressive male zebrafish

fertilized more eggs.Ariyomo and Watt 2012 Laboratory

Survival of offspring duringparental care

Aggressiveness Females that were more aggressive in guardingtheir nests from threats were found to stay ontheir nests longer.

McPhee and Quinn 1998 Field

Habitat use Aggressiveness, boldness, and activity More aggressive individuals were found more frequentlyin open water, whereas less aggressive individualswere found in or near structured refuge. No relationshipbetween boldness and aggression was found.

Kobler et al. 2011 Field

Migration Boldness Bolder fish were found to have a higher propensity to migrate. Chapman et al. 2011 Field

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were not specifically quantified in these experiments. However, ina subsequent field experiment (Biro et al. 2007), the authors ex-amined more directly the behaviors of domestic and wild rainbowtrout strains released into lakes that differed in predation pres-sure from loons. They found that fish from the domestic strainresponded less to the presence of predators, used riskier habitats,and had higher catch rates during the day than did fish from thewild strain. Thus, Biro et al. (2007: page 894) conclude that“greater overall activity and greater daytime use of deep and pe-lagic habitats by the domestic genotype should lead to greatergrowth (given sufficient food) but higher predation mortality”.These and other studies comparing the behaviors, growth, andsurvival of domestic versus wild stocks of salmonid fishes providesome of the clearest evidence for the ecological consequences ofbehavioral trait variation under a growth–mortality tradeoff.

Other studies in natural or seminatural environments provideno support for the expected link between behavioral traits and agrowth–mortality tradeoff. Adriaenssens and Johnsson (2011a)found that shy trout (individuals with low exploration tendencyin the laboratory) actually grew faster than bold trout when re-leased into a natural stream. In a subsequent study, they found nosignificant effects of activity or exploration measured in the lab-oratory on growth in the field, and if we can assume that recoveryfollowing release into the wild is an indication of survival, theyfound that more active individuals had higher survival (Adriaenssensand Johnsson 2011a). In both of the above studies, fish were col-lected from the wild, assayed for behavioral traits in the labora-tory, and then released back into the wild at a site near where theywere collected.

Höjesjö et al. (2011) also found no association between boldnessmeasured on juvenile brown trout (Salmo trutta) reared in thelaboratory and their growth and survival when released into theriver that was the source of the parental stock. However, onlyabout 4% of the released fish were recovered, which raises thequestion of whether the missing fish died or simply moved away.The inability to distinguish mortality from disappearance inrelease–recovery experiments into the wild (especially when recoveryrates are low) greatly hinders the ability to assess the impactof behavioral traits on fish survival (and growth). In Höjesjö et al.(2011), the authors note that juvenile brown trout in their studypopulation are very stationary (seldom moving further than200 m). Thus, recapture should provide a good estimate of survivalin the wild.

Following the pace-of-life syndrome (Fig. 3), we might expectindividuals with bold, active, and asocial behavioral types to havea higher propensity to explore their environment and dispersegreater distances, which could give them an advantage in terms offinding richer habitats. As stated earlier, Fraser et al. (2001) foundthat individual killifish that were bolder in the laboratory dis-persed greater distances when released into the field, and thatindividuals that moved greater distances in the field had highergrowth rates (in stream sections with predatory fish). Bolder indi-viduals of European roach (Rutilus rutilus) also showed a greaterpropensity to migrate (lake to stream) than shy individuals(Chapman et al. 2011), more asocial mosquitofish (Gambusia affinis)moved further from their social conspecifics when simultane-ously introduced to experimental streams (Cote et al. 2010), anddominant brown trout moved longer distances and had largerhome ranges in a radio telemetry study (Höjesjö et al. 2007). Anindividual’s dispersal tendency is likely related to the strength ofits social network (the number of social interactions an individualhas and the strength of those interactions), which itself has beenshown to be affected by an individual’s behavioral type. A studywith guppies investigating the relationship between boldness andsocial networks found a correlation between an individual’s bold-ness (measured by predator inspection and shoaling tendency inthe laboratory) and aspects of its social network in natural shoalsin the field. Bolder individuals were found to have fewer total

social connections and the average strength of the connectionsthey had were weaker than those of shyer individuals (Croft et al.2009). Again, following predictions of the pace-of-life syndrome,we might expect such traits of increased activity and dispersal tocarry with them higher mortality costs, if migrating or dispersinggreater distances increases exposure to predators. However, nostudies that we are aware of have assessed these mortality costs inthe field.

Reproductive successBehavioral traits have the potential to affect the reproductive

success of adults, with both intra- and intersexual selection likelyto be influenced by interindividual variation in behavioral traits(Schuett et al. 2010). Numerous laboratory studies with a variety offish species document positive relationships between boldness,dominance, and reproductive success. For example, in zebrafish(Danio rerio) the boldest and most aggressive males fertilized moreofa female’seggsthantheshyerandlessaggressivemales (AriyomoandWatt 2012), and in guppies (Poecilia reticulata) the females havebeen shown to prefer to mate with bolder males (boldness mea-sured by predator-inspection behavior; Godin and Dugatkin 1996).However, field studies examining the relationship between be-havioral traits and reproductive success are still quite rare. Ourown studies with largemouth bass (Micropterus salmoides) demon-strate that boldness measured in the laboratory is positively cor-related with nesting success in the field (i.e., bolder males weremore successful at building nests and receiving eggs whenstocked into ponds with females than less-bold males; N. Ballewand G. Mittelbach, unpublished data). These apparent fitness ben-efits of being bolder and more aggressive may be offset in othersituations (see Discussion).

Behavioral traits also have the potential to affect offspring sur-vival during periods of parental care. For example, in fish speciesthat build and guard redds or nests (e.g., Salmonidae and Centrar-chidae), bolder, more aggressive individuals are likely to outcom-pete conspecifics to secure better nesting sites, and bolder, moreaggressive individuals may be better at guarding their nests frompotential predators (McPhee and Quinn 1998). A series of studiesby D.P. Philipp and colleagues, using largemouth bass lines thatoriginated from a single wild population and were selected overmultiple generations for increased or decreased vulnerability torecreational angling during the non-nesting season, show that thehigh angling vulnerability line and low angling vulnerability linediffer in parental care behavior and reproductive success (Philippet al. 2009). Male bass from the high vulnerability to angling linedisplayed increased parental care activity and higher reproduc-tive success in ponds with nest predators (juvenile bluegill) com-pared to males from the low vulnerability line (Cooke et al. 2007;Sutter et al. 2012). It is difficult to say how the trait of anglingvulnerability relates to more commonly studied behavioral traitssuch as boldness and aggression. However, our own studies withlargemouth bass show that male bass assayed as more aggressivetowards conspecifics in the laboratory are more diligent at de-fending their nests from potential brood predators (bluegill) inthe field and have higher reproductive success (N. Ballew andG. Mittelbach, unpublished data).

Habitat use and foraging specializationBehavioral traits related to boldness or aggression, foraging

styles, or predator avoidance have the potential to affect habitatuse and resource consumption. For example, a study with bull-heads (Cottus perifretum) found that less aggressive individuals (asassayed in the laboratory) showed a greater propensity to usecomplex habitats (i.e., branch jams) in the field (Kobler et al. 2011).In the same study, there was no correlation between habitat use inthe field and individual differences in activity level measured inthe laboratory. Functional linkages may also exist between behav-ioral traits that confer greater feeding efficiency in particular


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habitats and morphological traits, leading to complex polymor-phisms (Wolf and Weissing 2012). In one of the first studies to lookfor an association between morphological and behavioral traits,Ehlinger and Wilson (1988) examined a foraging polymorphism inpopulations of bluegill sunfish. They found that bluegill collectedfrom a small, Michigan lake clustered into two behavioral (forag-ing mode) types when allowed to feed on open-water prey (zoo-plankton) and benthic prey (damselfly nymphs) in the laboratory(Fig. 4). These behavioral differences between individuals werestable across a 20 week testing period.

Differences in foraging behaviors (hover duration) betweenbluegill individuals corresponded to differences in feeding rate;fish exhibiting relatively short hover durations were more suc-cessful at capturing zooplankton, whereas fish displaying longerhover durations where more successful at capturing damselflynymphs. When Ehlinger and Wilson (1988) compared the mor-phologies of these two behavioral types, they found that mor-phology and behavior were tightly correlated. Fish classified as“vegetation” (benthic) morphological types exhibited long hoverdurations, whereas fish classified as “open-water” morphologicaltypes exhibited short hover durations. Subsequent morphologicalanalyses of sunfish (bluegill and pumpkinseed, Lepomis gibbosus)collected from open-water and littoral habitats in lakes confirmedthe subtle but repeatable morphological distinctions betweenphenotypes associated with pelagic and littoral habitats (Robinsonet al. 1993, 2000).

Selection on morphological and behavioral traits that increasefeeding efficiency on certain prey types or within certain habitatsis likely to go hand-in-hand. Therefore, an important question ishow much does habitat or foraging specialization lead to the de-velopment of animal personalities and the generation of behav-ioral trait variation within a population? Further, might there be

subtle differences in functional morphology between behavioraltypes within populations that have generally gone undetected?The morphological differences between bluegill behavioral typesin the study of Ehlinger and Wilson (1988) were not visible to thenaked eye, but they were detectable with morphometic analyses(e.g., Ehlinger and Wilson 1988; Robinson et al. 1993; Robinsonand Wilson 1996). Other fish species (e.g., threespine stickleback)show distinct resource polymorphisms in morphology, behavior,and resource use in some populations (McPhail 1993) but contin-uous variation in others (Robinson 2000). Thus, how much subtlevariation in morphology and physiology is associated with inter-individual behavioral variation in populations is unknown. Whenviewed in the holistic framework of individual specialization(Bolnick et al. 2011), it is clear that interindividual differences inbehavioral types and personalities may be an expected outcome ofnatural selection acting on populations in a complex environ-ment.

ConclusionsAt the individual level, variation in boldness, activity, and dis-

persal is often hypothesized to result from a tradeoff betweengrowth and mortality (i.e., bolder fish are more active and growfaster but suffer higher mortality). Despite wide-spread accep-tance of a growth–mortality tradeoff as a likely driver of be-havioral variation in fish (Stamps 2007), to date there is littleempirical evidence from field studies and the results are mixed(Table 2). Studies of other taxa (mammals, birds) also provide onlymixed support for the hypothesis that bolder (more exploratory)individuals take more risks to gain food but may suffer highermortality as a result (e.g., Réale and Festa-Bianchet 2003; Dingemanseet al. 2004; Réale at al. 2007; Quinn et al. 2012). The strongestsupport for a growth–mortality tradeoff associated with differ-

Fig. 4. Bluegill sunfish display two distinct behavioral types when foraging on open-water versus vegetation-dwelling prey in the laboratory.Graphed are the foraging behaviors (hover duration when searching) used by individual bluegill when searching for damselfly nymphs in thevegetation and when searching for zooplankton (Daphnia) in the open-water habitat of aquaria. Each point represents the mean hover time(±1 SE) of six feeding trials for a given fish in each habitat. The diagonal line represents equal hover duration in each habitat. Taken fromEhlinger and Wilson (1988).




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ences in boldness or aggression in fish comes from studies of wildversus domesticated strains of trout and salmon (e.g., Biro et al.2003a, 2003b, 2004; Sundström et al. 2004).

Boldness and dominance appear to be positively associated withincreased mating success in the laboratory and in the field, andindividuals more vulnerable to angling exhibit more persistentnest guarding behavior and greater reproductive success in pondstudies with largemouth bass. Boldness and aggression duringreproductive events are likely to have negative consequences foradult energetics, survival and future reproductive success, andthere are many examples of the high cost of parental care in fishes(e.g., Dufresne et al. 1990; Gillooly and Baylis 1999; Steinhart et al.2005). To date, however, no field studies have examined the fullset of correlations between boldness and aggression during thebreeding season, offspring survival, and adult current and futurereproductive success. In the Discussion section, we consider howthe costs and benefits of various behavioral traits may differ at theadult and juvenile life stages. Such life-history asynchrony in theimpact of behavioral traits may provide an additional mechanismfor the maintenance of variation in behavioral traits within apopulation.

Field studies also suggest that habitat heterogeneity andhabitat-specific foraging success may maintain phenotypic poly-morphisms in fish populations that include both behavioral andmorphological traits. For example, in sunfish and sticklebacks,behaviors associated with increased foraging success in limneticversus benthic habitats are also associated with variation in mor-phological traits (fin placement, body shape), resulting in com-plex polyphenisms (e.g., Ehlinger and Wilson 1988; Robinson andWilson 1996; Robinson 2000; Weese et al. 2012). Thus, there aremany opportunities in nature for consistent individual differ-ences in behavior to arise when individuals can exploit differenthabitats and resources. Ecologists, behaviorists, and evolutionarybiologists have joined together to highlight the importance ofstudying how environmental heterogeneity and habitat selectionmay generate and maintain intraspecific variation in popula-tions, including variation in behavioral traits (Adriaenssens andJohnsson 2011a; Araújo et al. 2011; Bolnick et al. 2011; Dall et al.2012; Sih et al. 2012; Wolf and Weissing 2012).

Consequences at the population, community, andecosystem level

Intraspecific variation in behavioral traits can have numerouseffects at the population, community, and ecosystem levels. Re-cent reviews have highlighted the potential for behavioral traitsto affect population dynamics, predator–prey interactions, spe-cies diversity, and ecosystem primary productivity (Sih et al. 2012;Wolf and Weissing 2012). However, when compared to conse-quences at the individual level, far fewer theoretical expectations

have been proposed for population- and community-level conse-quences of multiple behavioral types within traits. Similarly, fewempirical studies have examined the population- and community-level consequences of behavioral trait variation, and (to ourknowledge) no studies have been conducted in natural condi-tions. We summarize in Table 3 the limited number of laboratoryand mesocosm studies on the topic, looking first at studies thathave investigated ecological consequences of variation in behav-ioral traits at the population level, then moving to studies exam-ining consequences to species interactions, and concluding withstudies on consequences to ecosystem functioning.

Population-level consequences of behavioral trait variationhave been investigated in terms of group performance and popu-lation dynamics. For example, shoal composition for boldnessaffects foraging success in guppies. Fish from mixed shoals werefound to feed more than fish from all bold or all shy shoals,indicating that shoals containing a mixture of boldness behav-ioral types may outperform all bold and all shy shoals (Dyer et al.2009). In a study with shoaling European perch, the frequency ofdifferent risk-taking behavioral types within the shoal was shownto affect overall shoal risk-taking behavior, and bold individualshad an especially large effect on shoal behavior (Magnhagen andBunnefeld 2009). A study with threespine sticklebacks investi-gated the effect of a population’s composition of bold and shyindividuals on population social structure. Individuals were as-sayed for boldness in the laboratory (measured as hesitancy tofeed after being startled) and then artificial populations wereformed based on the boldness scores. Populations were composedof either all shy individuals, all bold individuals, or a mix of boldand shy individuals. The all shy populations had stronger socialstructures (measured as the average number of interactions for allindividuals in the population) than the all bold populations. Ad-ditionally, the all shy populations were more cliquish, meaningsocial subgroups appeared to form (Pike et al. 2008). A field studywith roach, while not directly investigating population-level con-sequences, found that bold roach had a higher propensity to mi-grate (lake to stream) than shy roach (Chapman et al. 2011). Roachpractice partial migration (only a fraction of the population mi-grates). Thus, it is easy to see how the frequency of bold behavioraltypes could impact the proportion of the population that mi-grates.

In terms of species interactions, the consequences of behavioraltypes to predator–prey interactions, interspecific competition,and invasive ability have been investigated in a single study foreach type of interaction. In threespine stickleback, boldness wasfound to affect prey risk, with bolder sticklebacks feeding moreheavily on chironomid larvae in laboratory trials (Ioannou et al.2008). In a study that investigated interspecific competition be-

Table 3. Summary of evidence for the ecological consequences of behavioral types in fishes at the population and community level.

Consequence Trait(s) Result Study Study method

Population performance Boldness Full bold and mixed shoals approached food morethan full shy shoals. Mixed shoals fed most.

Dyer et al. 2009 Laboratory

Boldness Shoal group behavior was impacted by the frequencyof boldness types within the shoal. Bold individualsespecially impacted shoal behavior.

Magnhagen andBunnefeld 2009

Laboratory

Social structure Boldness Populations of all shy fish had stronger socialstructures and were more cliquish than populationsof all bold fish.

Pike et al. 2008 Laboratory

Predator–prey Boldness Prey where more heavily preyed upon by bolder fish. Ioannou et al. 2008 Laboratory

Interspecific competition Boldness Bolder behavioral types were found to consumemore prey regardless of species in heterospecificcompetitive foraging trials.

Webster et al. 2009 Laboratory

Invasiveness Boldness No relationship between boldness and invasiveness. Rehage and Sih 2004 Laboratory


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tween two species of sticklebacks (threespine and ninespine),bold behavioral types were found to consume more prey inheterospecific competitive foraging trials, regardless of species(Webster et al. 2009). The only study to date on behavioral traitsand invasiveness found no relationship between the level of bold-ness and invasiveness for four Gambusia species (Rehage and Sih2004).

A key (but unanswered) question in the study of the population-level consequences of animal personalities is whether the amountof variance in behavioral traits within a population matters. Thatis, if populations share the same mean value for a given behav-ioral trait but possess different mixtures of behavioral types, isthere an effect on population dynamics? If behavioral types arenonrandomly distributed in space, such that they select differentforaging habitats (e.g., Wilson et al. 1993), occupy different posi-tions within a shoal (e.g., Ward et al. 2004), or preferentially asso-ciate with like behavioral types, then the mixture of behavioraltypes in a population will matter.

No studies to our knowledge have directly measured the effectsof individual variation in behavioral traits on ecosystem function-ing. However, a few studies suggest the possibility of such a rela-tionship. An outdoor mesocosm study using guppies taken fromnatural streams that differ in predation pressure found that me-socosms containing guppies from the high predation environ-ment contained fewer benthic invertebrates and more algae aftera 28 day period than mesocosms with guppies from the low pre-dation pressure environment (Bassar et al. 2012). In total, 9 of 13ecosystem variables measured by Bassar et al. showed significantriver-of-origin effects. The authors attributed these differentialeffects on ecosystem functioning, in part, to differences in forag-ing behavior by guppies adapted to the different stream environ-ments. However, Bassar et al. (2012) measured only one behavioralvariable directly in their experiment (pecking at the substrate),and this behavior did not differ in fish from high predation andlow predation sites. Thus, it is possible that other phenotypicdifferences between the populations caused the observed ecosys-tem effects. Harmon et al. (2009) and Des Roches et al. (2013)conducted similar types of mesocosm studies comparing theecosystem effects of two threespine stickleback morphotypes(benthic and limnetic; McPhail 1993; Schluter 2000) and foundsignificant effects of stickleback type on a variety of ecosystemfunctions. Again, behavioral variation was not specifically mea-sured in these ecosystem studies, but previous work on stickle-back morphotypes has shown pronounced differences in foragingbehaviors between benthic and limnetic forms (e.g., Schluter1993). Thus, while no studies that we are aware of definitively linkvariation in behavioral traits to effects on ecosystem functioning,the potential for such effects clearly exists and there is abundantopportunity for both theoretical and empirical studies that spe-cifically examine the consequences of interindividual variation inbehavioral types to communities and ecosystems.

Management implications of behavioral typesWhen considering the ecological consequences of behavioral

trait variation at the individual and population level, it is impor-tant to remember that these consequences are dependent on en-vironmental context. For example, bold behavioral types may beless fit than shy behavioral types in an environment with highlevels of predation, while the opposite may be true in an environ-ment without predators. Therefore, human impacts on the envi-ronment, such as recreational angling, commercial fishing, andhatchery-reared stocking programs, are likely to affect the ecolog-ical consequences of consistent interindividual behavioral varia-tion. For example, bolder individuals may be more vulnerable toangling, which could decrease their fitness relative to more timidindividuals and result in the population becoming less bold onaverage. In the same way, hatchery rearing programs may select

for certain behavioral types or selectively alter the way behavioraltraits develop with ontogeny, resulting in hatchery stocks thatdiffer genetically from wild populations (Huntingford 2004;Fraser 2008). In addition, habitat modifications (e.g., adding struc-ture to streams or lakes and construction of fishways) may selec-tively benefit certain behavioral types that have a higherpropensity to use these new habitats than others (e.g., Kobler et al.2011). Unfortunately, at this time there is too little evidence toevaluate many of these management practices in relation to theiruse by (and effects on) different personality types. Thus, we focuson two areas where data are available: fishing and hatchery rear-ing. We summarize in Table 4 what is known about the manage-ment implications of behavioral trait variation and discuss theseimplications in more detail below. We note that many of thestudies summarized in Table 4 have compared behavioral traits ofdifferent groups of fish (high versus low angling vulnerability;domestic versus wild stock), as opposed to comparing behavioraldifferences among individuals within a population.

FishingIt is increasingly recognized that fishing pressure (recreational

angling and commercial fishing) may alter the individual-levelconsequences of behavioral types, which in turn could affect nat-ural selection and the evolution of population characteristics(Uusi-Heikkila et al. 2008; Philipp et al. 2014). For example, innonfished populations of species that build and guard nests orredds, aggressive individuals may defend their nests more vigi-lantly from potential predators, increasing egg and larval survi-vorship. However, the introduction of angling could turn highnest guarding aggressiveness into a detriment if aggressive nestguarding individuals are more likely to be caught than their lessaggressive counterparts (e.g., as shown by Cooke et al. 2007). Re-moval of the nest-guarding parent (even short-term removal bycatch-and-release angling), can greatly increase the probability ofegg and larval mortality (Siepker et al. 2007). Personality traitsalso have the potential to affect angling vulnerability outside ofthe nesting season (though the traits may be different).

The hypothesis that recreational angling can affect the relation-ship between behavior and reproductive success is supported bythe previously mentioned study on reproductive success and pa-rental care in two largemouth bass lines selected for differentvulnerabilities to angling during the non-nesting season. Bassfrom the line selected for high vulnerability to angling showedincreased levels of aggression towards potential nest predatorsand greater diligence of parental care compared with bass fromthe low vulnerability line. Importantly, the high vulnerability linewas also found to have the highest reproductive potential (Sutteret al. 2012). Thus, angling can reduce reproductive success andlower total reproductive output not only in current generationsbut also impact selection for traits associated with nest guardingbehavior, potentially leading to reduced reproductive success andlower total reproductive output in future generations as well.Furthermore, as angling almost certainly selects for traits thatreduce angling vulnerability, high levels of recreational anglingare likely to impact the ability of the population to provide recre-ational angling opportunities in the future. This result was re-cently documented in bass populations that have historicallybeen exposed to different levels of angling intensity (Philipp et al.2014).

As discussed earlier, bolder individuals in some fish specieshave been found to forage more actively and grow faster thantheir shyer counterparts. Angling, however, could alter the eco-logical consequences of boldness, shifting the balance towardsshyer foragers if bold fish are captured more frequently. A recentstudy by Nannini et al. (2011) compared the foraging behaviors ofindividual largemouth bass obtained from the two artificially se-lected high and low angling vulnerability lines previously de-scribed. Contrary to expectations, fish from the low vulnerability




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Table 4. Summary of the effects of angling and hatchery rearing on behavioral traits in fishes and their ecological consequences.

Comparison Variables Result Study Study method

Between individuals Angling vulnerability with reproductivesuccess, antipredator aggression, andparental care

Male bass that have a high vulnerability to angling demonstratedgreater antipredator aggression and parental care and havehigher reproductive success.

Sutter et al. 2012 Field

Between individuals Angling vulnerability and foragingbehavior

Bass that have a low vulnerability to angling foraged morefrequently and also had more successful foraging attempts.

Nannini et al. 2011 Field

Between individuals Boldness, angling vulnerability Bolder bluegill were found to be less vulnerable to angling thanmore timid bluegill.

Wilson et al. 2011 Laboratory and field

Domestic, wild strains Boldness, dominance Domestic fish initiated feeding sooner, but no difference inlatency to approach novel object. Domestic fish bit at novelobject more. All bold fish, regardless of origin, were sociallydominant.

Sundström et al. 2004 Laboratory

Hatchery versus wild rearing;low versus high densityhatcheries

Survival, migration Hatchery-reared fish showed similar survival over three years,but only for fish reared in lower densities and circular tanks.Migration ranges smaller for hatchery fish.

Moore et al. 2012 Field

Between individuals Boldness Behavioral syndromes found between behavior with and withoutpredators, behaviors plastic during 16 weeks in hatcheryenvironment.

Lee and Berejikian 2008 Laboratory

Availability and stability ofstructure

Exploration Individuals reared with stable structure increased explorationwithout predators, but no difference in structure treatmentswith predators.

Lee and Berejikian 2009 Laboratory

Conventional versusenriched rearing

Boldness Individuals subjected to simulated predator attacks, physicalstructure, and natural prey during rearing showed decreasedlevels of boldness relative to individuals that wereconventionally reared.

Roberts et al. 2011 Laboratory

Low, medium, conventionalrearing densities

Survival, exploration, boldness Fish from lower densities consumed more prey, increasedpredator response, located food in a maze faster, and increasedsurvival in field.

Brockmark et al. 2010 Laboratory and field

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line actually captured more prey (and attempted to capture moreprey) than fish from the high vulnerability line. The low vulnera-bility line also had higher prey rejection rates and was more effi-cient at converting consumed prey into growth than the highvulnerability line (Nannini et al. 2011). While this study clearlydemonstrates the potential for angling during the non-nestingseason to have a selective effect on foraging behavior, it also cau-tions against jumping to conclusions about what behavioral typesare likely to be associated with increased angling vulnerability.Only one study that we are aware of has explicitly tested the linkbetween an individual’s boldness and angling vulnerability dur-ing the non-nesting season. Wilson et al. (2011) found that moretimid bluegill were more likely to be caught by angling than theirbolder counterparts in a natural lake — again, a result opposite ofexpectations. These early studies highlight the need for more re-search on the link between fish behavioral traits and responses toangling during the nesting and non-nesting seasons at the indi-vidual and population levels. However, unlike the relatively re-cent focus on the evolutionary impacts of recreational angling,the impacts of commercial fishing on fish life histories, growthrates, and behaviors have been studied for a much longer time.

Several studies over the last two decades have documented thatthe selective harvest of large individuals by commercial fisheriesleads to decreased growth rates in future generations, as well as avariety of other effects (e.g., Conover and Munch 2002; Hutchings2004; Reznick and Ghalambor 2005; Walsh et al. 2006). More re-cently, it has been proposed that commercial harvest may alsoselectively target individuals based on their behavioral type andgrowth rate, irrespective of size. As Uusi-Heikkila et al. (2008; page419) note, “fishing-induced selection directly acting on behavioralrather than on life-history traits per se can be expected in allfisheries that operate with passive gears such as trapping, angling,and gill-netting”. Biro and Post (2008) found exactly this result inan experimental study of rainbow trout in Canadian lakes, wherefaster-growing individuals were found to be more vulnerable toharvest by gill nets irrespective of their size. The authors attrib-uted the greater vulnerability of faster-growing individuals to dif-ferences in their behaviors, as faster-growing fish were moreactive and bolder than their slower-growing, nonharvested coun-terparts (Biro and Post 2008). Even if commercial fishing does notselect directly on behavioral traits, early findings from the pace-of-life syndrome suggest that direct selection on one trait, be it abehavioral trait like boldness or a life-history trait like growthrate, likely leads to indirect selection on a whole suit of correlatedtraits. These effects can have important impacts on species per-formance as well as community dynamics, making it essentialthat fisheries managers consider these effects when making man-agement decisions.

Hatchery rearingHatchery rearing and fish stocking represent the opposite-side

of the coin from fish harvest (i.e., they add rather than remove fishfrom a population). But, like selective harvest, hatchery programsdesigned to supplement the abundance of wild populations canimpact behavioral variation and may have important ecologicalconsequences. It is well known that fish raised in hatchery envi-ronments often perform poorly when stocked into the wild (Arakiet al. 2008) and there is a long-standing debate on whether or nothatchery stocking demographically boosts wild populations. Forthis reason, there is a wealth of literature examining how hatch-ery selection, including both purposeful selection on desirabletraits (such as increased growth rate) and unintentional selectionresulting from rearing experiences, may affect fitness (see reviewsby Huntingford 2004; Huntingford and Adams 2005; Araki et al.2008; Fraser 2008). Changes in behavioral phenotypes due to do-mestication selection have been suggested to be a major factorcontributing to the poor performance of hatchery-reared fishstocked into the wild (Fraser 2008).

Effects of artificial selection on behaviorCommon garden studies demonstrate that offspring from

hatchery-reared adults are often bolder and (or) more aggressivethan those from wild stocks (e.g., Berejikian 1995; Einum andFleming 1997), and laboratory studies comparing the behaviors ofdomestic and wild strains have found that domestic strains tendto be bolder and more aggressive than their wild counterparts(Budaev and Brown 2011; Conrad et al. 2011). For example, fry fromsea-ranched brown trout parents initiated feeding sooner and bitat a novel object more often than fry from wild brown trout par-ents (Sundström et al. 2004). Domesticated strains of fishes oftenundergo selection aimed at increasing production traits such asrapid growth (Huntingford 2004). However, selection for in-creased growth rate can have unintentional consequences onbehavioral trait variation, either by altering variation in the be-havioral traits themselves (e.g., selecting for individuals that aremore bold, aggressive, and active in their feeding behaviors) orselecting on metabolic traits that may cause individuals to actmore boldly to fulfill their metabolic needs (see prior discussionon this topic).

Behavioral traits that confer an advantage to individuals in ahatchery environment may carry a cost in nature. The most obvi-ous examples involve feeding behaviors in the absence or pres-ence of predators. The work by Biro and colleagues discussedearlier nicely documents how domesticated trout strains growfaster but suffer higher mortality than wild fish when stockedinto natural lakes with predators (Biro et al. 2006, 2007). Lookingat foraging behavior in a different context, Adriaenssens andJohnsson (2011b) assayed hatchery-reared and wild-origin browntrout for cognitive tasks such as cryptic prey discovery and mazesolving. They found that hatchery-reared trout had higher feedingrates than wild fish, but they did so with less accuracy. In the wild,lowered accuracy in foraging may incur energetically costly errorssuch as prey misidentification, whereas higher foraging rates maybe advantageous in hatchery settings with consistent food disper-sal (Adriaenssens and Johnsson 2011b).

The behavioral syndromes approach has been applied to deter-mine whether selection on behaviors in the hatchery environ-ment (e.g., propensity to feed in a predator-free environment) mayinfluence the distribution of behaviors expressed in other envi-ronments (e.g., aggressiveness and boldness under predationrisk). For example, Lee and Berejikian (2008) found that juvenilerockfish (Sebastes auriculatis) that fed at high rates in the absence ofa predator also tended to feed at higher rates when a model pred-ator was present. However, they found the behaviors of individu-als were inconsistent across two assay periods (8–12 days apart),suggesting plastic responses and behavioral flexibility. In con-trast, a study using rainbow trout found that individuals wereconsistent in their behaviors over 2–3 days and across safe andunsafe contexts (Conrad and Sih 2009). Behavioral flexibility maybe important when determining whether selection on fast growthrates has unintentional consequences on associated behaviors.Selection may be limited if individuals are capable of changingbehavior in response to their environment. Alternatively, if be-haviors are tightly correlated and not plastic, selection for highgrowth rates is likely to also select for bold and aggressive indi-viduals. Determining the degree to which individuals (or species)differ in their behavioral plasticity (e.g., Fig. 2) and understandinghow early development and rearing environment may affect lev-els of behavioral plasticity are important areas for future research(Dingemanse et al. 2010; Dingemanse and Wolf 2013).

The effects of hatchery rearing environments on behaviorThe process of raising juvenile fish in hatchery environments

has been shown to affect the cognitive pathways that influencebehavior (Huntingford and Adams 2005). Enrichment strategies,such as providing physical structure, decreasing fish densities,feeding with live prey, and introducing simulated predator at-




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tacks, have been suggested to better prepare hatchery fish forstocking (Brown et al. 2003; Lee and Berejikian 2009; Brockmarkand Johnsson 2010; Brockmark et al. 2010; see review in Huntingford2004). All of these modifications to current hatchery conditionshave been shown to benefit hatchery-reared fish in ways thatcould increase post-stocking survival. For example, brown troutassigned to “low” and “moderate” rearing density treatmentsshowed superior skills when tested for their ability to locate food,identify novel prey as resources, and respond to predators(Brockmark et al. 2010). Additionally, when stocked into an exper-imental stream, fish that were reared in high densities showeddecreased survival relative to individuals reared at low or mediumdensity (Brockmark et al. 2010). Individuals that were reared withphysical structure, fed natural prey, and subjected to simulatedattacks showed decreased boldness relative to individuals raisedunder conventional hatchery conditions (Roberts et al. 2011).When comparing both the presence and stability of physicalstructure during rearing, Lee and Berejikian (2009) found thatstable structures (the “unstable” treatment moved structurethroughout the experiment) were important for individuals toassess current risk and display behaviors accordingly. Individualsreared with stable structure were more explorative without pred-ators but showed reduced exploration under predation threat.Thus, there is accumulating evidence suggesting that the hatch-ery experience itself affects behaviors that can have importantimplications for fish stocked into the wild (e.g., impacts on habitatuse, growth, and survival). Encouragingly, these studies demon-strate that carefully considering rearing experiences of hatcheryfish and attempting to replicate natural environments could be apromising direction for hatcheries.

Although a number of studies have investigated individual be-haviors of hatchery-reared fish in laboratory settings and othershave compared how hatchery strains compare to wild strains,comparatively few studies have evaluated how the behaviors ofhatchery-reared fish influence their fitness in natural environ-ments. In one recent study, Moore et al. (2012) examined the fieldsurvival and migration rates of hatchery-reared steelhead troutcompared to fish of wild origin across three years. As an additionalcomponent, the hatchery-reared fish were from two hatcheriesthat differed in rearing environment (stocking density and shapeof tanks). Fish that were reared under lower densities and in cir-cular tanks (thought to decrease effects of density), survived aswell as wild steelhead. However, fish raised at higher densitiesand in rectangular raceways showed decreased survival relative towild fish. Moore et al. (2012) also found that migration ranges forsteelhead from both hatcheries were less than those of wild steel-head. This study suggests that changes in conventional hatcheryrearing may facilitate behavioral flexibility and the developmentof cognitive skills fish need upon entering natural systems. How-ever, to justify these changes, more field studies examining fitnessof individuals subjected to various enrichment regimes areneeded to understand how these changes affect survival in natu-ral conditions.

DiscussionFish have proven to be excellent model organisms for the study

of animal personalities, providing some of the earliest demonstra-tions of behavioral trait variation in any species (e.g., Huntingford1976, 1982; Ehlinger and Wilson 1988) and continuing today as oneof the most studied taxonomic groups (Stamps 2007; Toms et al.2010; Budaev and Brown 2011; Conrad et al. 2011). Still, as Wolf andWeissing (2012) and others have noted, relatively little attentionhas been paid to the ecological consequences of varying behav-ioral types. This comment applies to all species, not just fish, andis especially true of studies conducted in natural or seminaturalenvironments. Our review has sought to summarize what ecolo-gists, behaviorists, and managers know about the ecological con-

sequences of behavioral types at the individual, population, andcommunity or ecosystem levels, including implications for fisher-ies management and conservation. Important research foci in thisarea include the impacts of behavioral trait variation on individ-ual growth and survival, nesting behaviors and reproductive suc-cess, habitat use, diet, and ontogenetic niche shifts, migration anddispersal, commercial and recreational fishing, and hatcheryrearing for supplemental stocking. We discuss these different re-search foci below and suggest avenues for future research.

Examining behavioral type effects on growth and survivalThe concept of a growth–mortality tradeoff is firmly en-

trenched in the ecological literature (e.g., Werner and Anholt1993; Lima 1998), and a growth–mortality tradeoff provides muchof the theoretical underpinning for the maintenance of behav-ioral variation in boldness in fish and other organisms (e.g.,Stamps 2007). Thus, it is surprising that evidence from natural orseminatural environments documenting the effects of variationin boldness and (or) aggression on fish growth or survival is lim-ited and is almost entirely based on comparisons of wild anddomesticated stocks (e.g., Biro et al. 2003a, 2003b). This is not toquestion the reality of a growth–mortality tradeoff, or to doubt itsrelationship to fish behavioral traits, but only to note that muchmore work is needed to examine how individual variation in bold-ness affects growth and survival. Archard and Braithwaite (2010)discuss some of the challenges involved in studying the conse-quences of behavioral traits in wild animals. They note that aparticularly hard nut to crack is the effect of behavioral type onthe survival of free-living individuals, as the recovery of markedindividuals is often very low (see Höjesjö et al. 2011 for an examplewith fish). The low recovery of marked individuals leaves uswondering, are missing individuals dead? Or, have they simplydispersed from the study area? Studies conducted in closed, semi-natural environments (experimental ponds, outdoor raceways, orfenced reaches of streams), where all surviving individuals can be re-covered post-stocking, can provide useful experimental systemsfor testing the growth–mortality tradeoff and its relationship toboldness variation in fishes.

Diet, habitat use, and ontogenetic niche shiftsFish, like many other organisms, show pronounced changes in

diet and habitat as they grow. For example, most piscivorous fishbegin life feeding on zooplankton and benthic invertebrates be-fore reaching a size where they can switch to feeding on other fish(Mittelbach and Persson 1998). Many other fishes occupy protec-tive habitats (e.g., littoral zone vegetation) when small and vulner-able to predators, and then they shift to feeding in more open andriskier habitats when they reach sizes that are less vulnerable topredation (Werner et al. 1983; Werner and Hall 1988). These onto-genetic niche shifts have important consequences for populationdynamics and species interactions (de Roos and Persson 2013).However, a completely unexplored question is — what role doespersonality play in determining the timing and extent of ontoge-netic niche shifts, in fish or other organisms?

Studies documenting ontogenetic niche shifts in diet and hab-itat invariably show considerable variation amongst individuals(e.g., Mittelbach 1981; Werner and Hall 1988; Hjelm et al. 2000).How much of this individual variation in the timing and extent ofontogenetic niche shifts is due to differences in personality? Con-sider for example the study by Post (2003), who examined thefactors contributing to the onset of piscivory in a cohort of young-of-year (YOY) largemouth bass. In bass and other piscivores, be-coming piscivorous in the first summer of life greatly increasesfitness by increasing the probably of surviving through the winter(Buijse and Houthuijzen 1992; Post et al. 1998). Post (2003) foundthat only the largest individuals in the YOY bass cohort from PaulLake, Michigan, were able to successfully transition to feeding onYOY bluegill during their first summer. Further, all bass that grew


Mittelbach et al. 13


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large enough to become piscivorous in their first year were bornearly in the spring (Fig. 5). Birth date, however, was by itself a poorpredictor of either bass size in August or the propensity to shift topiscivory (i.e., many early-born bass did not get large enough tobecome piscivorous; Fig. 5). Why did some early-born bass growquickly and become piscivorous in their first summer, whereasothers did not? Chance could of course played a role (e.g., someindividuals may have been lucky enough to find and consume alarge number of energetically rewarding prey early in life and geta jump on their less-fortunate fellows). However, it is tempting tospeculate that differences in personality may contribute as well.In this case, the hypothesis would be that those early-born bassgrowing large enough to become piscivorous are individuals thatare relatively bold and take greater risks to increase their feedingrate, either by being more active or by using riskier habitats. Nostudies to date have examined the impact of behavioral types onthe timing of ontogenetic niche shifts. This seems a particularlyripe area for future research.

Consistency in behavioral traits across life stages andfitness tradeoffs

Numerous studies have documented consistency in behavioraltraits or behavioral syndromes in fish and other organisms overrelatively short time periods of days and weeks (Bell et al. 2009;Conrad et al. 2011). However, much less is known about consis-tency in behaviors across longer time periods or across life stages.Wilson and Godin (2009) found that shy–bold behavioral typesshowed differential consistency in bluegill sunfish over a 1–3 monthperiod (measured in the field). However, Bell and Stamps (2004)and Edenbrow and Croft (2011) observed little differential consis-tency in individual behavioral types between life stages (e.g., ju-veniles to adults) in threespine sticklebacks and mangrovekillifish (Kryptolebias marmoratus), respectively (measured in thelaboratory). In a study of how behavioral consistency changedacross ontogeny in an Africa cichlid (Steatocranus casuarius),Budaev et al. (1999) found that behaviors (response to a novelenvironment, a novel fish, and a mirror) were not consistent injuveniles (4 and 4.5 months of age), but they were consistent inadults (12–13.5 months). Bell and Stamps (2004) measured threetypes of behavior (activity, aggression toward a conspecific, andboldness under predation risk) at three developmental stages (ju-venile, subadult, and adult) and found that individual behavioraltypes were not stable over ontogeny. In one stickleback popula-tion, the boldness-aggression behavioral syndrome was stableover ontogeny (showed structural consistency), but in anotherpopulation it was not. Edenbrow and Croft (2011) also found thatbehavioral types of boldness and exploration were highly plasticduring ontogeny, but that correlations between these two behav-iors (i.e., bold types were more exploratory) were maintained fromjuvenile to adulthood (structural consistency; see also Schürchand Heg 2010; Chervet et al. 2011).

Studies with aquatic organisms other than fish have observeddifferential consistency in activity traits across life stages (e.g.,tadpole to adult frog (Rana ridibunda; Wilson and Krause 2012a)and nymph to adult damselfly (Lestes congener; Brodin 2009)). Ingeneral, however, we know very little about the differential con-sistency of behavioral traits across life stages (e.g., juvenile toadult) or in individuals undergoing ontogenetic niche shifts (e.g.,freshwater to marine, benthic to pelagic, and insectivorous topiscivorous). Clearly, such long-term differential consistency inbehavioral traits has important implications for fitness and forthe maintenance of variation in behavioral traits in populations(Adriaenssens and Johnsson 2013).

If behavioral traits have differential consistency only over shortintervals, then the potential for fitness tradeoffs to contribute tothe maintenance of variation in behavioral traits is rather limited.However, if behavioral traits are consistent across life stages oracross ontogenetic niche shifts, then there are many more oppor-

tunities for tradeoffs to occur. For example, it is commonly as-sumed that boldness may have a positive effect on individualfitness through increased energy gain and (or) reproductive suc-cess, but it may have a negative effect due to reduced survival(Stamps 2007; Smith and Blumstein 2008). If fish that are rela-tively bold as juveniles are also relatively bold as adults, thenboldness could positively affect fitness at the juvenile stagethrough higher feeding rates or energy gains and at the adultstage through greater reproductive output (per breeding event),but boldness could negatively affect fitness at the juvenile stagedue to decreased survival, and (or) negatively affect reproductivesuccess at the adult stage due to decreased survival during a re-productive event and (or) reduced probability of surviving to re-produce again. Thus, there are multiple ways in which boldnesseffects on growth, fecundity, and survival could trade off to affectlifetime fitness.

To date, studies that have investigated the relationship betweenbehavioral traits and fitness have generally focused on a singlemeasure of fitness (such as survival) at a specific life stage(Dingemanse and Réale 2005; Smith and Blumstein 2008). How-ever, fitness tradeoffs across life stages or between different com-ponents of selection (sexual and viability) provide a potentiallypowerful mechanism for the maintenance of adaptive variation inbehavioral traits. Moreover, if behavioral traits are heritable, thefitness consequences of animal personalities can extend acrossgenerations.

Heritability of behavioral traits and consequences arisingfrom the release of domesticated fish

Although there are relatively few estimates of the heritability ofbehavioral traits in fishes, the evidence suggests that many behav-ioral traits are heritable, with levels of heritability that are gen-erally lower than those for morphological traits, but roughlycomparable to those measured for life-history traits (Bakker 1986;Stirling et al. 2002; Bell 2005; Brown et al. 2007; Dingemanse et al.2009; Chervet et al. 2011). Additionally, researchers have been ableto artificially select stocks of largemouth bass to express high andlow vulnerability to recreational angling (Sutter et al. 2012), dem-onstrating again a strong genetic component to certain aspects offish behavior. The heritability of behavioral traits has many im-portant ecological implications, particularly with regard to themixing of wild and domestic fish stocks.

Fisheries biologists have long been concerned with potentialconsequences of interbreeding between wild, hatchery-reared, or

Fig. 5. Length frequency distribution of young-of-year largemouthbass collected from Paul Lake, Michigan, in late August 1994. Fishwere categorized by age (age determined using daily rings fromotoliths). Age categories represent roughly the youngest 25%, thecentral 50%, and the oldest 25% of fish collected. Only fish >85 mmin length become piscivorous during their first summer of life.Taken from Post (2003).




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escaped farmed fish, particularly salmon, (e.g., Gross 1998). Thisconcern has been largely focused on the detrimental effects ofintroducing nonadaptive life-history traits into wild stocks (caus-ing, for example, a mismatch in the timing or orientation of mi-gration and reproduction). However, interbreeding between wildand domestic stocks (e.g., farmed or hatchery-reared fish) couldinfluence behavioral traits as well, with unknown consequencesfor wild fish. A number of studies comparing domestic and wildstrains of salmon and trout show that hatchery-reared fish, or fishthat have been genetically modified for faster growth, may bebolder, more aggressive, and (or) more risk-prone in their habitatuse, resulting in higher growth rates but reduced survival in na-ture (e.g., Abrahams and Sutterlin 1999; Sundström et al. 2003,2004; Biro et al. 2003a, 2003b, 2004, 2007; Sundt-Hansen et al.2009). To the extent that behavioral traits are heritable and adap-tive, the interbreeding of domestic and wild fish stocks has theclear potential to reduce the fitness of locally adapted stocks.

Commercial and recreational fishing may also select on herita-ble behavioral traits that have unanticipated evolutionary con-sequences. One possibility discussed earlier is the associationbetween boldness and aggression in nest guarding behavior andangling vulnerability in largemouth bass. Male bass that arebolder and more aggressive are more diligent in guarding theiryoung and have higher reproductive success (Cooke et al. 2007).However, bolder, more aggressive bass may also be more vulner-able to recreational angling (Suski and Philipp 2004). Thus, ifboldness and aggression are heritable traits (see Bell 2005), thenincreased fishing pressure may lead to the evolution of reducedboldness and aggression in the population, a reduction in anglingvulnerability, and the unwelcome consequence of a reduction inaverage reproductive success (Sutter et al. 2012). Here again, anunderstanding of the correlations among behaviors, combinedwith a knowledge of their heritabilities and their ecological con-sequences at different life stages, is an important avenue for fu-ture research for the effective management of fish stocks.

SummaryInterindividual variation in behavioral traits is now recognized

to be an important feature of most animal populations, includingfish. In this review, we have sought to highlight some of themechanisms driving the evolution and maintenance of variationin behavioral traits within fish populations, as well as the ecolog-ical consequences of this variation. Field evidence for the ecolog-ical consequences of behavioral trait variation is still quite limitedin any group of organisms. However, there is little doubt thatbehavioral trait variation plays an important role in the growth,survival, and reproductive success of individuals, as well as havingpotential impacts on species interactions and ecosystem function-ing. It is also clear, however, that we must be careful not to jumpto conclusions about the universality of the causes and conse-quences of behavioral trait variation (e.g., the growth–mortalitytradeoff) without more evidence from nature. In fishes, behav-ioral trait variation has added implications for conservation,harvest, and resource management. Biologists and managers rec-ognize the importance of environmental context to the evolutionof behavioral traits and the role that behavioral variation amongindividuals and between populations (wild versus domestic stocks)may play in successful stocking and conservation. Again, moredata from field studies, especially with tagged or marked individ-uals of known behavioral types, is crucial.

AcknowledgementsWe thank Alison Bell, Pat Hanly, David Philipp, and two anon-

ymous reviewers for their comments and suggestions, and forsharing unpublished manuscripts. Our special thanks to JudyStamps for her many insightful comments on an early version ofthe manuscript. Grants from the U.S. National Science Foundation

supported portions of this research (IOS-1210438 to M.K.K. andG.G.M.; IOS-1311455 to N.G.B. and G.G.M.). This is contributionnumber 1732 from the W.K. Kellogg Biological Station.

ReferencesAbrahams, M.V., and Sutterlin, A. 1999. The foraging and antipredator behav-

iour of growth-enhanced transgenic Atlantic salmon. Anim. Behav. 58: 933–942. doi:10.1006/anbe.1999.1229. PMID:10564595.

Adriaenssens, B., and Johnsson, J.I. 2009. Personality and life-history productiv-ity: consistent or variable association? Trends Ecol. Evol. 24: 179–180. doi:10.1016/j.tree.2008.12.003. PMID:19251337.

Adriaenssens, B., and Johnsson, J.I. 2011a. Shy trout grow faster: exploring linksbetween personality and fitness-related traits in the wild. Behav. Ecol. 22:135–143. doi:10.1093/beheco/arq185.

Adriaenssens, B., and Johnsson, J.I. 2011b. Learning and context-specific explora-tion behaviour in hatchery and wild brown trout. Appl. Anim. Behav. Sci.132: 9–99.

Adriaenssens, B., and Johnsson, J.I. 2013. Natural selection, plasticity and theemergence of a behavioural syndrome in the wild. Ecol. Lett. 16: 47–55.doi:10.1111/ele.12011. PMID:23034098.

Araki, H., Berejikian, B.A., Ford, M.J., and Blouin, M.S. 2008. Fitness of hatchery-reared salmonids in the wild. Evol. Appl. 1: 342–355. doi:10.1111/j.1752-4571.2008.00026.x.

Araújo, M.S., Bolnick, D.I., and Layman, C.A. 2011. The ecological causes of indi-vidual specialisation. Ecol. Lett. 14: 948–958. doi:10.1111/j.1461-0248.2011.01662.x. PMID:21790933.

Archard, G.A., and Braithwaite, V.A. 2010. The importance of wild populations instudies of animal temperament. J. Zool. 281(3): 149–160. doi:10.1111/j.1469-7998.2010.00714.x.

Ariyomo, T.O., and Watt, P.J. 2012. The effect of variation in boldness and ag-gressiveness on the reproductive success of zebrafish. Anim. Behav. 83: 41–46. doi:10.1016/j.anbehav.2011.10.004.

Bakker, T.C.M. 1986. Aggressiveness in sticklebacks (Gasterosteus aculeatus L.): abehavior-genetic study. Behav. 98: 1–144. doi:10.1163/156853986X00937.

Bassar, R.D., Ferriere, R., López-Sepulcre, A., Marshall, M.C., Travis, J.,Pringle, C.M., and Reznick, D.N. 2012. Direct and indirect ecosystem effects ofevolutionary adaptation in the Trinidadian guppy (Poecilia reticulata). Am. Nat180: 167–185. doi:10.1086/666611.

Bell, A.M. 2005. Behavioural differences between individuals and two popula-tions of stickleback (Gasterosteus aculeatus). J. Evol. Biol. 18: 464–473. doi:10.1111/j.1420-9101.2004.00817.x. PMID:15715852.

Bell, A.M., and Stamps, J.A. 2004. Development of behavioural differences be-tween individuals and populations of sticklebacks, Gasterosteus aculeatus.Anim. Behav. 68: 1339–1348. doi:10.1016/j.anbehav.2004.05.007.

Bell, A.M., Hankison, S.J., and Laskowski, K.L. 2009. The repeatability of behav-iour: a meta-analysis. Anim. Behav. 77: 771–783. doi:10.1016/j.anbehav.2008.12.022.

Berejikian, B.A. 1995. The effects of hatchery and wild ancestry and experienceon the relative ability of steelhead trout fry (Oncorhynchus mykiss) to avoid abenthic predator. Can. J. Fish. Aquat. Sci. 52(11): 2476–2482. doi:10.1139/f95-838.

Biro, P.A., and Post, J.R. 2008. Rapid depletion of genotypes with fast growth andbold personality traits from harvested fish populations. Proc. Natl. Acad. Sci.U.S.A. 105: 2919–2922. doi:10.1073/pnas.0708159105. PMID:18299567.

Biro, P.A., and Stamps, J.A. 2008. Are animal personality traits linked to life-history productivity? Trends Ecol. Evol. 23: 361–368. doi:10.1016/j.tree.2008.04.003. PMID:18501468.

Biro, P.A., and Stamps, J.A. 2010. Do consistent individual differences in meta-bolic rate promote consistent individual differences in behavior? TrendsEcol. Evol. 25: 653–659. doi:10.1016/j.tree.2010.08.003. PMID:20832898.

Biro, P.A., Post, J.R., and Parkinson, E.A. 2003a. Density-dependent mortality ismediated by foraging activity for prey fish in whole-lake experiments.J. Anim. Ecol. 72: 546–555. doi:10.1046/j.1365-2656.2003.00724.x.

Biro, P.A., Post, J.R., and Parkinson, E.A. 2003b. From individuals to populations:prey fish risk-taking mediates mortality in whole-system experiments. Ecol-ogy, 84: 2419–2431. doi:10.1890/02-0416.

Biro, P.A., Abrahams, M.V., Post, J.R., and Parkinson, E.A. 2004. Predators selectagainst high growth rates and risk-taking behaviour in domestic trout pop-ulations. Proc. R. Soc. B Biol. Sci. 271: 2233–2237. doi:10.1098/rspb.2004.2861.

Biro, P.A., Post, J.R., and Abrahams, M.V. 2005. Ontogeny of energy allocationreveals selective pressure promoting risk-taking behaviour in young fishcohorts. Proc. R. Soc. B Biol. Sci. 272: 1443–1448. doi:10.1098/rspb.2005.3096.

Biro, P.A., Abrahams, M.V., Post, J.R., and Parkinson, E.A. 2006. Behaviouraltrade-offs between growth and mortality explain evolution of submaximalgrowth rates. J. Anim. Ecol. 75: 1165–1171. doi:10.1111/j.1365-2656.2006.01137.x.PMID:16922852.

Biro, P.A., Abrahams, M.V., and Post, J.R. 2007. Direct manipulation of behaviourreveals a mechanism for variation in growth and mortality among preypopulations. Anim. Behav. 73: 891–896. doi:10.1016/j.anbehav.2006.10.019.

Blumstein, D.T., Petelle, M.P., and Wey, T.W. 2012. Defensive and social aggres-sion: repeatable but independent. Behav. Ecol. 24: 457–461.

Bolnick, D.I., Amarasekare, P., Araújo, M.S., Bürger, R., Levine, J.M., Novak, M.,




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onl

y.

http://dx.doi.org/10.1006/anbe.1999.1229

http://www.ncbi.nlm.nih.gov/pubmed/10564595

http://dx.doi.org/10.1016/j.tree.2008.12.003



http://dx.doi.org/10.1093/beheco/arq185

http://dx.doi.org/10.1111/ele.12011


http://dx.doi.org/10.1111/j.1752-4571.2008.00026.x

http://dx.doi.org/10.1111/j.1752-4571.2008.00026.x

http://dx.doi.org/10.1111/j.1461-0248.2011.01662.x

http://dx.doi.org/10.1111/j.1461-0248.2011.01662.x


http://dx.doi.org/10.1111/j.1469-7998.2010.00714.x

http://dx.doi.org/10.1111/j.1469-7998.2010.00714.x

http://dx.doi.org/10.1016/j.anbehav.2011.10.004

http://dx.doi.org/10.1163/156853986X00937

http://dx.doi.org/10.1086/666611

http://dx.doi.org/10.1111/j.1420-9101.2004.00817.x

http://dx.doi.org/10.1111/j.1420-9101.2004.00817.x





http://dx.doi.org/10.1139/f95-838

http://dx.doi.org/10.1139/f95-838

http://dx.doi.org/10.1073/pnas.0708159105







http://dx.doi.org/10.1046/j.1365-2656.2003.00724.x

http://dx.doi.org/10.1890/02-0416

http://dx.doi.org/10.1098/rspb.2004.2861


http://dx.doi.org/10.1111/j.1365-2656.2006.01137.x



Rudolf, V.H.W., Schreiber, S.J., Urban, M.C., and Vasseur, D.A. 2011. Whyintraspecific trait variation matters in community ecology. Trends Ecol. Evol.26: 183–192. doi:10.1016/j.tree.2011.01.009. PMID:21367482.

Brockmark, S., and Johnsson, J.I. 2010. Reduced hatchery rearing density in-creases social dominance, postrelease growth, and survival in brown trout(Salmo trutta). Can. J. Fish. Aquat. Sci. 67(2): 288–295. doi:10.1139/F09-185.

Brockmark, S., Adriaenssens, B., and Johnsson, J.I. 2010. Less is more: densityinfluences the development of behavioural life skills in trout. Proc. R. Soc. BBiol. Sci. 277: 3035–3043. doi:10.1098/rspb.2010.0561.

Brodin, T. 2009. Behavioral syndrome over the boundaries of life-carryoversfrom larvae to adult damselfly. Behav. Ecol. 20: 30–37. doi:10.1093/beheco/arn111.

Brown, C., Davidson, T., and Laland, K. 2003. Environmental enrichment andprior experience of live prey improve foraging behaviour in hatchery-rearedAtlantic salmon. J Fish Biol. 63(s1): 187–196. doi:10.1111/j.1095-8649.2003.00208.x.

Brown, C., Burgess, F., and Braithwaite, V.A. 2007. Heritable and experientialeffects on boldness in a tropical poeciliid. Behav. Ecol. Sociobiol. 62: 237–243.doi:10.1007/s00265-007-0458-3.

Budaev, S., and Brown, C. 2011. Personality traits and behaviour. In Fish cogni-tion and behavior. 2nd ed. Edited by C. Brown, K. Laland, and J. Krause.Wiley-Blackwell Publishing, Oxford, UK. pp. 135–165.

Budaev, S.V., Zworykin, D.D., and Mochek, A.D. 1999. Individual differences inparental care and behaviour profile in the convict cichlid: a correlationstudy. Anim. Behav. 58: 195–202. doi:10.1006/anbe.1999.1124. PMID:10413557.

Buijse, A.D., and Houthuijzen, R.P. 1992. Piscivory, growth, and size-selectivemortality of age 0 pikeperch (Stizostedion lucioperca). Can. J. Fish. Aquat. Sci.49(5): 894–902. doi:10.1139/f92-100.

Carter, A.J., Marshall, H., Heinsohn, R., and Cowlishaw, G. 2012. How not tomeasure boldness: novel object and antipredator responses are not the samein wild baboons. Anim. Behav. 84: 603–609. doi:10.1016/j.anbehav.2012.06.015.

Carter, A.J., Feeney, W.E., Cowlishaw, G., Marshall, H., and Heinsohn, R. 2013.Animal personality: what are behavioural ecologists measuring? Biol. Rev.88: 465–475. doi:10.1111/brv.12007. PMID:23253069.

Chapman, B.B., Hulthén, K., Blomqvist, D.R., Hansson, L., Nilsson, J.,Brodersen, J., Nilsson, P.A., Skov, C., and Brönmark, C. 2011. To boldly go:individual differences in boldness influence migratory tendency. Ecol. Lett.14: 871–876. doi:10.1111/j.1461-0248.2011.01648.x. PMID:21718420.

Chervet, N., Zöttl, M., Schürch, R., Taborsky, M., and Heg, D. 2011. Repeatabilityand heritability of behavioural types in a social cichlid. Int. J. Evol. Biol. 2011.Article ID 321729. doi:10.4061/2011/321729.

Colleter, M., and Brown, C. 2011. Personality traits predict hierarchy rank inmale rainbowfish social groups. Anim. Behav. 81: 1231–1237. doi:10.1016/j.anbehav.2011.03.011.

Conover, D.O., and Munch, S.B. 2002. Sustaining fisheries yields over evolution-ary time scales. Science, 297: 94–96. doi:10.1126/science.1074085. PMID:12098697.

Conrad, J.L., and Sih, A. 2009. Behavioural type in newly emerged steelheadOncorhynchus mykiss does not predict growth rate in a conventional hatcheryrearing environment. J. Fish. Biol. 75: 1410–1426. doi:10.1111/j.1095-8649.2009.02372.x. PMID:20738622.

Conrad, J.L., Weinersmith, K.L., Brodin, T., Saltz, J.B., and Sih, A. 2011. Behav-ioural syndromes in fishes: a review with implications for ecology and fish-eries management. J. Fish. Biol. 78: 395–435. doi:10.1111/j.1095-8649.2010.02874.x. PMID:21284626.

Cooke, S.J., Suski, C.D., Ostrand, K.G., Wahl, D.H., and Philipp, D.P. 2007. Phys-iological and behavioral consequences of long-term artificial selection forvulnerability to recreational angling in a teleost fish. Physiol. Biochem. Zool.80: 480–490. doi:10.1086/520618. PMID:17717811.

Cote, J., Clobert, J., Brodin, T., Fogarty, S., and Sih, A. 2010. Personality-dependent dispersal: characterization, ontogeny and consequences forspatially structured populations. Philos. Trans. R. Soc. B Biol. Sci. 365: 4065–4076. doi:10.1098/rstb.2010.0176.

Croft, D.P., Krause, J., Darden, S.K., Ramnarine, I.W., Faria, J.J., and James, R.2009. Behavioural trait assortment in a social network: patterns and impli-cations. Behav. Ecol. Sociobiol. 63: 1495–1503. doi:10.1007/s00265-009-0802-x.

Dahlbom, S.J., Lagman, D., Lundstedt-Enkel, K., Sundström, L.F., and Winberg, S.2011. Boldness predicts social status in zebrafish (Danio rerio). PLoS ONE, 6(8):e23565. doi:10.1371/journal.pone.0023565. PMID:21858168.

Dall, S.R.X., Houston, A.I., and McNamara, J.M. 2004. The behavioural ecology ofpersonality: consistent individual differences from an adaptive perspective.Ecol. Lett. 7(8): 734–739. doi:10.1111/j.1461-0248.2004.00618.x.

Dall, S.R.X., Bell, A.M., Bolnick, D.I., and Ratnieks, F.L.W. 2012. An evolutionaryecology of individual differences. Ecol. Lett. 15: 1189–1198. doi:10.1111/j.1461-0248.2012.01846.x. PMID:22897772.

de Roos, A.M., and Persson, L. 2013. Population and community ecology of onto-genetic development. Princeton University Press, Princeton, N.J.

Des Roches, S., Shurin, J.B., Schluter, D., and Harmon, L.J. 2013. Ecological andevolutionary effects of stickleback on community structure. PloS ONE, 8(4):e59644. doi:10.1371/journal.pone.0059644. PMID:23573203.

Dingemanse, N.J., and Réale, D. 2005. Natural selection and animal personality.Behaviour, 142: 1159–1184. doi:10.1163/156853905774539445.

Dingemanse, N.J., and Wolf, M. 2010. Recent models for adaptive personalitydifferences: a review. Philos. Trans. R. Soc. B Biol. Sci. 365: 3947–3958. doi:10.1098/rstb.2010.0221.

Dingemanse, N.J., and Wolf, M. 2013. Between-individual differences in behav-ioural plasticity within populations: causes and consequences. Anim. Behav.85: 1031–1039. doi:10.1016/j.anbehav.2012.12.032.

Dingemanse, N.J., Both, C., Drent, P.J., and Tinbergen, J.M. 2004. Fitness conse-quences of avian personalities in a fluctuating environment. Proc. R. Soc. BBiol. Sci. 271: 847–852. doi:10.1098/rspb.2004.2680.

Dingemanse, N.J., Van der Plas, F., Wright, J., Réale, D., Schrama, M., Roff, D.A.,Van der Zee, E., and Barber, I. 2009. Individual experience and evolutionaryhistory of predation affect expression of heritable variation in fish personal-ity and morphology. Proc. R. Soc. B Biol. Sci. 276: 1285–1293. doi:10.1098/rspb.2008.1555.

Dingemanse, N.J., Kazem, A.J.N., Réale, D., and Wright, J. 2010. Behaviouralreaction norms: animal personality meets individual plasticity. Trends Ecol.Evol. 25: 81–89. doi:10.1016/j.tree.2009.07.013. PMID:19748700.

Dufresne, F., Fitzgerald, G.J., and Lachance, S. 1990. Age and size-related differ-ences in reproductive success and reproductive costs in threespine stickle-backs (Gasterosteus aculeatus). Behav. Ecol. 1: 140–147. doi:10.1093/beheco/1.2.140.

Dugatkin, L.A. 1992. Tendency to inspect predators predicts mortality risk in theguppy (Poecilia reticulata). Behav. Ecol. 3: 124–127. doi:10.1093/beheco/3.2.124.

Dyer, J.R.G., Croft, D.P., Morrell, L.J., and Krause, J. 2009. Shoal compositiondetermines foraging success in the guppy. Behav. Ecol. 20: 165–171. doi:10.1093/beheco/arn129.

Edenbrow, M., and Croft, D.P. 2011. Behavioural types and life history strategiesduring ontogeny in the mangrove killifish, Kryptolebias marmoratus. Anim.Behav. 82: 731–741. doi:10.1016/j.anbehav.2011.07.003.

Ehlinger, T.J., and Wilson, D.S. 1988. Complex foraging polymorphism in blue-gill sunfish. Proc. Natl. Acad. Sci. U.S.A. 85: 1878–1882. doi:10.1073/pnas.85.6.1878. PMID:16578831.

Einum, S., and Fleming, I.A. 1997. Genetic divergence and interactions in thewild among native, farmed and hybrid Atlantic salmon. J. Fish. Biol. 50(3):634–651. doi:10.1111/j.1095-8649.1997.tb01955.x.

Frank, S.A. 1986. Dispersal polymorphisms in subdivided populations. J. Theor.Biol. 122(3): 303–309. doi:10.1016/S0022-5193(86)80122-9. PMID:3626575.

Fraser, D.J. 2008. How well can captive breeding programs conserve biodiver-sity? A review of salmonids. Evol. Appl. 1(4): 535–586. doi:10.1111/j.1752-4571.2008.00036.x.

Fraser, D.F., Gilliam, J.F., Daley, M.J., Le, A.N., and Skalski, G.T. 2001. Explainingleptokurtic movement distributions: intrapopulation variation in boldnessand exploration. Am. Nat. 158: 124–135. doi:10.1086/321307. PMID:18707341.

Fraser, N.H.C., and Metcalfe, N.B. 1997. The costs of becoming nocturnal: feedingefficiency in relation to light intensity in juvenile Atlantic salmon. Funct.Ecol. 11: 385–391. doi:10.1046/j.1365-2435.1997.00098.x.

Garamszegi, L.Z., Markó, G., and Herczeg, G. 2013. A meta-analysis of correlatedbehaviors with implications for behavioral syndromes: relationships be-tween particular behavioral traits. Behav. Ecol. 24(5): 1068–1080. doi:10.1093/beheco/art033.

Gillooly, J.F., and Baylis, J.R. 1999. Reproductive success and the energetic cost ofparental care in male smallmouth bass. J. Fish Biol. 54: 573–584. doi:10.1111/j.1095-8649.1999.tb00636.x.

Gliwicz, Z.M., Slon, J., and Szynkarczyk, I. 2006. Trading safety for food: evidencefrom gut contents in roach and bleak captured at different distances offshorefrom their daytime littoral refuge. Freshw. Biol. 51: 823–839. doi:10.1111/j.1365-2427.2006.01530.x.

Godin, J., and Dugatkin, L.A. 1996. Female mating preference for bold males inthe guppy, Poecilia reticulata. Proc. Natl. Acad. Sci. U.S.A. 93: 10262–10267.doi:10.1073/pnas.93.19.10262. PMID:11607706.

Groothuis, G.G., and Trillmich, F. 2011. Unfolding personalities: the importanceof studying ontogeny. Dev. Biol. 53: 641–655. doi:10.1002/dev.20574.

Gross, M.R. 1998. One species with two biologies: Atlantic salmon (Salmo salar) inthe wild and in aquaculture. Can. J. Fish. Aquat. Sci. 55(S1): 131–144. doi:10.1139/d98-024.

Hamilton, M.D., and May, R.M. 1977. Dispersal in stable habitats. Nature, 269:578–581. doi:10.1038/269578a0.

Harmon, L.J., Matthews, B., Des Roches, S., Chase, J.M., Shurin, J.B., andSchluter, D. 2009. Evolutionary diversification in stickleback affects ecosys-tem functioning. Nature, 458(7242): 1167–1170. doi:10.1038/nature07974.PMID:19339968.

Hjelm, J., Persson, L., and Christensen, B. 2000. Growth, morphological varia-tion, and ontogenetic niche shifts in perch (Perca fluviatilis) in relation toresource availability. Oecologia, 122(2): 190–199. doi:10.1007/PL00008846.

Höjesjö, J., Økland, F., Sundström, L.F., Pettersson, J., and Johnsson, J.I. 2007.Movement and home range in relation to dominance; a telemetry study onbrown trout Salmo trutta. J. Fish Biol. 70: 257–268. doi:10.1111/j.1095-8649.2006.01299.x.

Höjesjö, J., Adriaenssens, B., Bohlin, T., Jönsson, C., Hellström, I., andJohnsson, J.I. 2011. Behavioural syndromes in juvenile brown trout (Salmotrutta); life history, family variation and performance in the wild. Behav. Ecol.Sociobiol. 65(9): 1801–1810. doi:10.1007/s00265-011-1188-0.

Houston, A.I. 2010. Evolutionary models of metabolism, behaviour and person-




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. J. F

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http://dx.doi.org/10.1139/F09-185


http://dx.doi.org/10.1093/beheco/arn111


http://dx.doi.org/10.1111/j.1095-8649.2003.00208.x

http://dx.doi.org/10.1111/j.1095-8649.2003.00208.x

http://dx.doi.org/10.1007/s00265-007-0458-3



http://dx.doi.org/10.1139/f92-100



http://dx.doi.org/10.1111/brv.12007


http://dx.doi.org/10.1111/j.1461-0248.2011.01648.x


http://dx.doi.org/10.4061/2011/321729



http://dx.doi.org/10.1126/science.1074085


http://dx.doi.org/10.1111/j.1095-8649.2009.02372.x

http://dx.doi.org/10.1111/j.1095-8649.2009.02372.x


http://dx.doi.org/10.1111/j.1095-8649.2010.02874.x

http://dx.doi.org/10.1111/j.1095-8649.2010.02874.x


http://dx.doi.org/10.1086/520618


http://dx.doi.org/10.1098/rstb.2010.0176

http://dx.doi.org/10.1007/s00265-009-0802-x

http://dx.doi.org/10.1371/journal.pone.0023565


http://dx.doi.org/10.1111/j.1461-0248.2004.00618.x

http://dx.doi.org/10.1111/j.1461-0248.2012.01846.x

http://dx.doi.org/10.1111/j.1461-0248.2012.01846.x




http://dx.doi.org/10.1163/156853905774539445








http://dx.doi.org/10.1093/beheco/1.2.140






http://dx.doi.org/10.1073/pnas.85.6.1878



http://dx.doi.org/10.1111/j.1095-8649.1997.tb01955.x

http://dx.doi.org/10.1016/S0022-5193(86)80122-9


http://dx.doi.org/10.1111/j.1752-4571.2008.00036.x

http://dx.doi.org/10.1111/j.1752-4571.2008.00036.x

http://dx.doi.org/10.1086/321307


http://dx.doi.org/10.1046/j.1365-2435.1997.00098.x

http://dx.doi.org/10.1093/beheco/art033

http://dx.doi.org/10.1093/beheco/art033



http://dx.doi.org/10.1111/j.1365-2427.2006.01530.x

http://dx.doi.org/10.1111/j.1365-2427.2006.01530.x



http://dx.doi.org/10.1002/dev.20574

http://dx.doi.org/10.1139/d98-024

http://dx.doi.org/10.1139/d98-024

http://dx.doi.org/10.1038/269578a0

http://dx.doi.org/10.1038/nature07974


http://dx.doi.org/10.1007/PL00008846

http://dx.doi.org/10.1111/j.1095-8649.2006.01299.x

http://dx.doi.org/10.1111/j.1095-8649.2006.01299.x

http://dx.doi.org/10.1007/s00265-011-1188-0

ality. Philos. Trans. R. Soc. B Biol. Sci. 365: 3969–3975. doi:10.1098/rstb.2010.0161.

Houston, A.I., and McNamara, J.M. 1999. Models of adaptive behaviour. Cam-bridge University Press, Cambridge, UK.

Huntingford, F.A. 1976. The relationship between anti-predator behaviour andaggression among conspecifics in the three-spined stickleback, Gasterosteusaculeatus. Anim. Behav. 24: 245–260. doi:10.1016/S0003-3472(76)80034-6.

Huntingford, F.A. 1982. Do inter- and intraspecific aggression vary in relation topredation pressure in sticklebacks? Anim. Behav. 30: 909–916. doi:10.1016/S0003-3472(82)80165-6.

Huntingford, F.A. 2004. Implications of domestication and rearing conditionsfor the behavior of cultivated fishes. J. Fish. Biol. 65(s1): 122–142. doi:10.1111/j.0022-1112.2004.00562.x.

Huntingford, F., and Adams, C. 2005. Behavioural syndromes in farmed fish:implications for production and welfare. Behaviour, 142: 1207–1221. doi:10.1163/156853905774539382.

Hutchings, J.A. 2004. The cod that got away. Nature, 428: 899–900. doi:10.1038/428899a. PMID:15118707.

Ioannou, C.C., Payne, M., and Krause, J. 2008. Ecological consequences of thebold–shy continuum: the effect of predator boldness on prey risk. Oecologia,157: 177–182. doi:10.1007/s00442-008-1058-2. PMID:18481092.

Johnsson, J.I., and Björnsson, B.T. 2001. Growth-enhanced fish can be competi-tive in the wild. Funct. Ecol. 15(5): 654–659. doi:10.1046/j.0269-8463.2001.00566.x.

Johst, K., and Brandl, R. 1999. Natal versus breeding dispersal: evolution in amodel system. Evol. Ecol. Res. 1(8): 911–921.

Kobler, A., Maes, G.E., Humblet, Y., Volckaert, F.A.M., and Eens, M. 2011. Tem-perament traits and microhabitat use in bullhead, Cottus perifretum: fish as-sociated with complex habitats are less aggressive. Behaviour, 148: 603–625.doi:10.1163/000579511X572035.

Koolhaas, J.M., Korte, S.M., de Boer, S.F., van der Vegt, B.J., van Reenen, C.G.,Hopster, H., de Jong, I.C., Ruis, M.A., and Blokhuis, H.J. 1999. Coping styles inanimals: current status in behavior and stress-physiology. Neurosci. Biobe-hav. Rev. 23: 925–935. doi:10.1016/S0149-7634(99)00026-3.

Lee, J.S., and Berejikian, B.A. 2008. Effects of the rearing environment on averagebehaviour and behavioural variation in steelhead. J. Fish. Biol. 72(7): 1736–1749. doi:10.1111/j.1095-8649.2008.01848.x.

Lee, J.S., and Berejikian, B.A. 2009. Structural complexity in relation to thehabitat preferences, territoriality, and hatchery rearing of juvenile Chinarockfish (Sebastes nebulosus). Environ. Biol. Fishes, 84(4): 411–419. doi:10.1007/s10641-009-9450-2.

Lima, S. 1998. Stress and decision making under the risk of predation: recentdevelopments from behavioral, reproductive, and ecological perspectives.Adv. Study Behav. 27: 215–290. doi:10.1016/S0065-3454(08)60366-6.

Luttbeg, B., and Sih, A. 2010. Risk, resources and state-dependent adaptive be-havioural syndromes. Philos. Trans. R. Soc. B Biol. Sci. 365: 3977–3990. doi:10.1098/rstb.2010.0207.

Magnhagen, C., and Bunnefeld, N. 2009. Express your personality or go alongwith the group: what determines the behaviour of shoaling perch? Proc. R.Soc. B Biol. Sci. 276: 3369–3375. doi:10.1098/rspb.2009.0851.

Mangel, M., and Stamps, J. 2001. Trade-offs between growth and mortality andthe maintenance of individual variation in growth. Evol. Ecol. Res. 3: 583–593.

McGhee, K.E., and Travis, J. 2010. Repeatable behavioural type and stable domi-nance rank in the bluefin killifish. Anim. Behav. 79: 497–507. doi:10.1016/j.anbehav.2009.11.037.

McPhail, J.D. 1993. Ecology and evolution of sympatric sticklebacks (Gasteros-teus): origin of the species pair. Can. J. Zool. 71(3): 515–523. doi:10.1139/z93-072.

McPhee, M.V., and Quinn, T.P. 1998. Factors affecting the duration of nest de-fense and reproductive lifespan of female sockeye salmon, Onchorynchusnerka. Environ. Biol. Fishes, 51: 369–375.

Metcalfe, N.B., Fraser, N.H.C., and Burns, M.D. 1999. Food availability and thenocturnal vs. diurnal foraging trade-off in juvenile salmon. J. Anim. Ecol. 68:371–381. doi:10.1046/j.1365-2656.1999.00289.x.

Mittelbach, G.G. 1981. Foraging efficiency and body size: a study of optimal dietand habitat use by bluegills. Ecology, 62(5): 1370–1386. doi:10.2307/1937300.

Mittelbach, G.G., and Persson, L. 1998. The ontogeny of piscivory and its ecolog-ical consequences. Can. J. Fish. Aquat. Sci. 55(6): 1454–1465. doi:10.1139/f98-041.

Moore, M., Berejikian, B.A., and Tezak, E.P. 2012. Variation in the early marinesurvival and behavior of natural and hatchery-reared Hood Canal steelhead.PloS ONE, 7(11): e49645. doi:10.1371/journal.pone.0049645. PMID:23185393.

Nannini, M.A., Wahl, D.H., Philipp, D.P., and Cooke, S.J. 2011. The influence ofselection for vulnerability to angling on foraging ecology in largemouth bassMicropterus salmoides. J. Fish. Biol. 79: 1017–1028. doi:10.1111/j.1095-8649.2011.03079.x. PMID:21967587.

Nussey, D.H., Wilson, A.J., and Brommer, J.E. 2007. The evolutionary ecology ofindividual phenotypic plasticity in wild populations. J. Evol. Biol. 20(3): 831–844. doi:10.1111/j.1420-9101.2007.01300.x.

Philipp, D., Claussen, J., Koppelman, J., Stein, J., Cooke, S., Suski, C., Wahl, D.,Sutter, D., and Arlinghaus, R. 2014. Fisheries-induced evolution in large-mouth bass — linking vulnerability to angling, parental care, and fitness.

In Proceedings of the Symposium Black Bass Diversity: Multidisciplinary Sci-ence for Conservation, Nashville, Tennessee, 8–10 February 2013. Edited byM.D. Tringali, M.S. Allen, T. Birdsong, and J.M. Long. American FisheriesSociety, Bethesda, Maryland. [In press.]

Philipp, D.P., Cooke, S.J., Claussen, J.E., Koppelman, J., Suski, C.D., andBurkett, D. 2009. Selection for vulnerability to angling in largemouth bass.Trans. Am. Fish. Soc. 138(1): 189–199. doi:10.1577/T06-243.1.

Pike, T.W., Samanta, M., Lindström, J., and Royle, N.J. 2008. Behavioural pheno-type affects social interactions in an animal network. Proc. R. Soc. B Biol. Sci.275: 2515–2520. doi:10.1098/rspb.2008.0744. PMID:18647713.

Post, D.M. 2003. Individual variation in the timing of ontogenetic niche shiftsin largemouth bass. Ecology, 84(5): 1298–1310. doi:10.1890/0012-9658(2003)084[1298:IVITTO]2.0.CO;2.

Post, D.M., Kitchell, J.F., and Hodgson, J.R. 1998. Interactions among adult de-mography, spawning date, growth rate, predation, overwinter mortality, andthe recruitment of largemouth bass in a northern lake. Can. J. Fish Aquat. Sci.55(12): 2588–2600. doi:10.1139/f98-139.

Quinn, J.L., Cole, E.F., Bates, J., Payne, R.W., and Cresswell, W. 2012. Personalitypredicts individual responsiveness to the risks of starvation and predation.Proc. R. Soc. B Biol. Sci. 279: 1919–1926. doi:10.1098/rspb.2011.2227.

Réale, D., and Festa-Bianchet, M. 2003. Predator-induced natural selection ontemperament in bighorn ewes. Anim. Behav. 65: 463–470. doi:10.1006/anbe.2003.2100.

Réale, D., Gallant, B.Y., Leblanc, M., and Festa-Bianchet, M. 2000. Consistency oftemperament in bighorn ewes and correlates with behaviour and life history.Anim. Behav. 60: 589–597. doi:10.1006/anbe.2000.1530. PMID:11082229.

Réale, D., Reader, S.M., Sol, D., McDougall, P.T., and Dingemanse, N.J. 2007.Integrating animal temperament within ecology and evolution. Biol. Rev. 82:291–318. doi:10.1111/j.1469-185X.2007.00010.x. PMID:17437562.

Réale, D., Grant, D., Humphries, M.M., Bergeron, P., Careau, V., andMontiglio, P.O. 2010. Personality and the emergence of the pace-of-life syn-drome concept at the population level. Philos. Trans. R. Soc. B Biol. Sci. 365:4051–4063. doi:10.1098/rstb.2010.0208.

Rehage, J.S., and Sih, A. 2004. Dispersal behaviour, boldness, and the link toinvasiveness: a comparison of four Gambusia species. Biol. Invasions, 6: 379–391. doi:10.1023/B:BINV.0000034618.93140.a5.

Reznick, D.N., and Ghalambor, C.K. 2005. Can commercial fishing cause evolu-tion? Answers from guppies (Poecilia reticulata). Can. J. Fish. Aquat. Sci 62(4):791–801. doi:10.1139/f05-079.

Roberts, L.J., Taylor, J., and Garcia de Leaniz, C. 2011. Environmental enrichmentreduces maladaptive risk-taking behavior in salmon reared for conservation.Biol. Conserv. 144: 1972–1979. doi:10.1016/j.biocon.2011.04.017.

Robinson, B.W. 2000. Trade offs in habitat-specific foraging efficiency and thenascent adaptive divergence of sticklebacks in lakes. Behaviour, 137: 865–888. doi:10.1163/156853900502501.

Robinson, B.W., and Wilson, D.S. 1996. Genetic variation and phenotypic plas-ticity in a trophically polymorphic population of pumpkinseed sunfish(Lepomis gibbosus). Evol. Ecol. 10(6): 631–652. doi:10.1007/BF01237711.

Robinson, B.W., Wilson, D.S., Margosian, A.S., and Lotito, P.T. 1993. Ecologicaland morphological differentiation of pumpkinseed sunfish in lakes withoutbluegill sunfish. Evol. Ecol. 7: 451–464. doi:10.1007/BF01237641.

Robinson, B.W., Wilson, D.S., and Margosian, A.S. 2000. A pluralistic analysis ofcharacter release in pumpkinseed sunfish (Lepomis gibbosus). Ecology, 81:2799–2812. doi:10.1890/0012-9658(2000)081[2799:APAOCR]2.0.CO;2.

Ronce, O., Perret, F., and Olivieri, I. 2000. Evolutionarily stable dispersal rates donot always increase with local extinction rates. Am. Nat. 155(4): 485–496.doi:10.1086/303341. PMID:10753076.

Ryer, C.H., and Hurst, T.P. 2008. Indirect predator effects on age-0 northern rocksole Lepidopsetta polyxystra: growth suppression and temporal reallocation offeeding. Mar. Ecol. Prog. Ser. 357: 207–212. doi:10.3354/meps07303.

Schluter, D. 1993. Adaptive radiation in sticklebacks: size, shape, and habitat useefficiency. Ecology, 74: 699–709. doi:10.2307/1940797.

Schluter, D. 2000. Ecological character displacement in adaptive radiation. Am.Nat. 156(s4): S4–S16. doi:10.1086/303412.

Schuett, W., Tregenza, T., and Dall, S.R.X. 2010. Sexual selection and animalpersonality. Biol. Rev. 85: 217–246. doi:10.1111/j.1469-185X.2009.00101.x. PMID:19922534.

Schürch, R., and Heg, D. 2010. Life history and behavioral type in the highlysocial cichlid Neolamprologus pulcher. Behav. Ecol. 21: 588–598. doi:10.1093/beheco/arq024.

Siepker, M.J., Ostrand, K.J., Cooke, S.J., Philipp, D.P., and Wahl, D.H. 2007. Areview of the effects of catch-and-release angling on black bass, Micropterusspp.: implications for conservation and management of populations. Fish.Manag. Ecol. 14(2): 91–101. doi:10.1111/j.1365-2400.2007.00529.x.

Sih, A., and Bell, A.M. 2008. Insights for behavioral ecology from behavioralsyndromes. Adv. Study Behav. 38: 227–281. doi:10.1016/S0065-3454(08)00005-3.

Sih, A., Bell, A.M., and Johnson, J.C. 2004a. Behavioral syndromes: an ecologicaland evolutionary overview. Trends Ecol. Evol. 19: 372–378. doi:10.1016/j.tree.2004.04.009. PMID:16701288.

Sih, A., Bell, A.M., Johnson, J.C., and Ziemba, R.E. 2004b. Behavioral syndromes:an integrative overview. Q. Rev. Biol. 79: 241–277. doi:10.1086/422893. PMID:15529965.




Can

. J. F

ish.

Aqu

at. S

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http://dx.doi.org/10.1016/S0003-3472(76)80034-6

http://dx.doi.org/10.1016/S0003-3472(82)80165-6

http://dx.doi.org/10.1016/S0003-3472(82)80165-6

http://dx.doi.org/10.1111/j.0022-1112.2004.00562.x

http://dx.doi.org/10.1111/j.0022-1112.2004.00562.x

http://dx.doi.org/10.1163/156853905774539382

http://dx.doi.org/10.1163/156853905774539382

http://dx.doi.org/10.1038/428899a

http://dx.doi.org/10.1038/428899a


http://dx.doi.org/10.1007/s00442-008-1058-2


http://dx.doi.org/10.1046/j.0269-8463.2001.00566.x

http://dx.doi.org/10.1046/j.0269-8463.2001.00566.x

http://dx.doi.org/10.1163/000579511X572035

http://dx.doi.org/10.1016/S0149-7634(99)00026-3

http://dx.doi.org/10.1111/j.1095-8649.2008.01848.x

http://dx.doi.org/10.1007/s10641-009-9450-2

http://dx.doi.org/10.1007/s10641-009-9450-2

http://dx.doi.org/10.1016/S0065-3454(08)60366-6





http://dx.doi.org/10.1139/z93-072

http://dx.doi.org/10.1139/z93-072

http://dx.doi.org/10.1046/j.1365-2656.1999.00289.x

http://dx.doi.org/10.2307/1937300

http://dx.doi.org/10.1139/f98-041

http://dx.doi.org/10.1139/f98-041



http://dx.doi.org/10.1111/j.1095-8649.2011.03079.x

http://dx.doi.org/10.1111/j.1095-8649.2011.03079.x


http://dx.doi.org/10.1111/j.1420-9101.2007.01300.x

http://dx.doi.org/10.1577/T06-243.1



http://dx.doi.org/10.1890/0012-9658(2003)084%5B1298%3AIVITTO%5D2.0.CO;2

http://dx.doi.org/10.1890/0012-9658(2003)084%5B1298%3AIVITTO%5D2.0.CO;2

http://dx.doi.org/10.1139/f98-139






http://dx.doi.org/10.1111/j.1469-185X.2007.00010.x



http://dx.doi.org/10.1023/B%3ABINV.0000034618.93140.a5

http://dx.doi.org/10.1139/f05-079

http://dx.doi.org/10.1016/j.biocon.2011.04.017

http://dx.doi.org/10.1163/156853900502501

http://dx.doi.org/10.1007/BF01237711

http://dx.doi.org/10.1007/BF01237641

http://dx.doi.org/10.1890/0012-9658(2000)081%5B2799%3AAPAOCR%5D2.0.CO;2

http://dx.doi.org/10.1086/303341


http://dx.doi.org/10.3354/meps07303

http://dx.doi.org/10.2307/1940797

http://dx.doi.org/10.1086/303412





http://dx.doi.org/10.1111/j.1365-2400.2007.00529.x

http://dx.doi.org/10.1016/S0065-3454(08)00005-3

http://dx.doi.org/10.1016/S0065-3454(08)00005-3




http://dx.doi.org/10.1086/422893


Sih, A., Cote, J., Evans, M., Fogarty, S., and Pruitt, J. 2012. Ecological implicationsof behavioural syndromes. Ecol. Lett. 15: 278–289. doi:10.1111/j.1461-0248.2011.01731.x. PMID:22239107.

Smith, B.R., and Blumstein, D.T. 2008. Fitness consequences of personality: ameta-analysis. Behav. Ecol. 19: 448–455. doi:10.1093/beheco/arm144.

Smith, B., and Blumstein, D.T. 2010. Behavioral types as predictors of survival inTrinidadian guppies (Poecilia reticulata). Behav. Ecol. 21: 919–926. doi:10.1093/beheco/arq084.

Stamps, J.A. 2007. Growth–mortality tradeoffs and ‘personality traits’ in ani-mals. Ecol. Lett. 10: 355–363. doi:10.1111/j.1461-0248.2007.01034.x. PMID:17498134.

Stamps, J., and Groothuis, T.G.G. 2010. The development of animal personality:relevance, concepts and perspectives. Biol. Rev. 85: 301–325. doi:10.1111/j.1469-185X.2009.00103.x. PMID:19961473.

Steinhart, G.B., Sandrene, M.E., Weaver, S., Stein, R.A., and Marschall, E.A. 2005.Increased parental care cost for nest-guarding fish in a lake with hyperabun-dant nest predators. Behav. Ecol. 16: 427–434. doi:10.1093/beheco/ari006.

Stirling, D.G., Réale, D., and Roff, D. 2002. Selection, structure and the herit-ability of behaviour. J. Evol. Biol. 15: 277–289. doi:10.1046/j.1420-9101.2002.00389.x.

Sundström, L.F., Lõhmus, M., and Johnsson, J.I. 2003. Investment in territorialdefence depends on rearing environment in brown trout (Salmo trutta). Be-hav. Ecol. Sociobiol. 109(8): 701–712. doi:10.1007/s00265-003-0622-3.

Sundström, L.F., Lõhmus, M., Johnsson, J.I., and Devlin, R.H. 2004. Growth hor-mone transgenic salmon pay for growth potential with increased predationmortality. Proc. R. Soc. B Biol. Sci. 271(S5): S350–S352. doi:10.1098/rsbl.2004.0189.

Sundt-Hansen, L., Neregärd, L., Einum, S., Höjesjö, J., Björnsson, B., Hindar, K.,Økland, F., and Johnsson, J. 2009. Growth enhanced brown trout show in-creased movement activity in the wild. Funct. Ecol. 23: 551–558. doi:10.1111/j.1365-2435.2008.01532.x.

Suski, C.D., and Philipp, D.M. 2004. Factors affecting the vulnerability to anglingof nesting male largemouth and smallmouth bass. Trans. Am. Fish. Soc.133(5): 1100–1106. doi:10.1577/T03-079.1.

Sutter, D.A.H., Suski, C.D., Philipp, D.P., Klefoth, T., Wahl, D.H., Kersten, P.,Cooke, S.J., and Arlinghaus, R. 2012. Recreational fishing selectively capturesindividuals with the highest fitness potential. Proc. Natl. Acad. Sci. U.S.A. 109:20960–20965. doi:10.1073/pnas.1212536109. PMID:23213220.

Toms, C.N., Echevarria, D.J., and Jouandot, D.J. 2010. A methodological review ofpersonality-related studies in fish: focus on the shy–bold axis of behavior.International J. Comp. Psychol. 23: 1–25.

Uusi-Heikkila, S., Wolter, C., Klefoth, T., and Arlinghaus, R. 2008. A behavioralperspective on fishing-induced evolution. Trends Ecol. Evol. 23: 419–421.doi:10.1016/j.tree.2008.04.006. PMID:18582988.

Walsh, M.R., Munch, S.B., Chiba, S., and Conover, D.O. 2006. Maladaptivechanges in multiple traits caused by fishing: impediments to populationrecovery. Ecol. Lett. 9: 142–148. doi:10.1111/j.1461-0248.2005.00858.x. PMID:16958879.

Ward, A.J.W., Thomas, P., Hart, P.J.B., and Krause, J. 2004. Correlates of boldnessin three-spined sticklebacks (Gasterosteus aculeatus). Behav. Ecol. Sociobiol. 55:561–568. doi:10.1007/s00265-003-0751-8.

Ward, G., and Fitzgerald, G.J. 1987. Male aggression and female mate choice in

the three-spined stickleback, Gasterosteus aculeatus L. J. Fish. Biol. 30: 679–690.doi:10.1111/j.1095-8649.1987.tb05797.x.

Webster, M.M., Ward, A.J.W., and Hart, P.J.B. 2009. Individual boldness affectsinterspecific interactions in sticklebacks. Behav. Ecol. Sociobiol. 63: 511–520.doi:10.1007/s00265-008-0685-2.

Weese, D.J., Ferguson, M.M., and Robinson, B.W. 2012. Contemporary and his-torical evolutionary processes interact to shape patterns of within-lake phe-notypic divergences in polyphenic pumpkinseed sunfish, Lepomis gibbosus.Ecol. Evol. 2(3): 574–592. doi:10.1002/ece3.72. PMID:22822436.

Werner, E.E., and Anholt, B. 1993. Ecological consequences of the trade-off be-tween growth and mortality rates mediated by foraging activity. Am. Nat.142: 242–272. doi:10.1086/285537. PMID:19425978.

Werner, E.E., and Hall, D.J. 1988. Ontogenetic habitat shifts in bluegill: theforaging rate-predation risk tradeoff. Ecology, 69: 1352–1366. doi:10.2307/1941633.

Werner, E.E., Mittelbach, G.G., and Hall, D.J. 1981. The role of foraging profit-ability and experience in habitat use by the bluegill sunfish. Ecology, 62(1):116–125. doi:10.2307/1936675.

Werner, E.E., Gilliam, J.F., Hall, D.J., and Mittelbach, G.G. 1983. An experimentaltest of the effects of predation risk on habitat use in fish. Ecology, 64(6):1540–1548. doi:10.2307/1937508.

Wilson, A.D.M., and Godin, J.G. 2009. Boldness and behavioral syndromes in thebluegill sunfish, Lepomis macrochirus. Behav. Ecol. 20: 231–237. doi:10.1093/beheco/arp018.

Wilson, A.D.M., and Krause, J. 2012a. Metamorphosis and animal personality: aneglected opportunity. Trends Ecol. Evol. 27: 529–531. doi:10.1016/j.tree.2012.07.003. PMID:22824739.

Wilson, A.D.M., and Krause, J. 2012b. Personality and metamorphosis: is behav-ioral variation consistent across ontogenetic niche shifts? Behav. Ecol. 23:1316–1323. doi:10.1093/beheco/ars123.

Wilson, A.D.M., Binder, T.R., McGrath, K.P., Cooke, S.J., and Godin, J.-G.J. 2011.Capture technique and fish personality: angling targets timid bluegill sun-fish, Lepomis macrochirus. Can. J. Fish. Aquat. Sci. 68(5): 749–757. doi:10.1139/f2011-019.

Wilson, D.S. 1998. Adaptive individual differences within single populations.Philos. Trans. R. Soc. B Biol. Sci. 353: 199–205. doi:10.1098/rstb.1998.0202.

Wilson, D.S., Coleman, K., Clark, A.B., and Biederman, L. 1993. Shy–bold contin-uum in pumpkinseed sunfish (Lepomis gibbosus): an ecological study of a psy-chological trait. J. Comp. Psychol. 107: 250–260. doi:10.1037/0735-7036.107.3.250.

Wilson, D.S., Clark, A.B., Coleman, K., and Dearstyne, T. 1994. Shyness andboldness in humans and other animals. Trends Ecol. Evol. 9: 442–446. doi:10.1016/0169-5347(94)90134-1.

Wolf, M., and McNamara, J.M. 2012. On the evolution of personalities viafrequency-dependent selection. Am. Nat. 179(6): 679–692. doi:10.1086/665656. PMID:22617258.

Wolf, M., and Weissing, F.J. 2010. An explanatory framework for adaptive peso-nality differences. Philos. Trans. R. Soc. B Biol. Sci. 365: 3959–3968. doi:10.1098/rstb.2010.0215.

Wolf, M., and Weissing, F.J. 2012. Animal personalities: consequences for ecol-ogy and evolution. Trends Ecol. Evol. 27: 452–461. doi:10.1016/j.tree.2012.05.001. PMID:22727728.




Can

. J. F

ish.

Aqu

at. S

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m b

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gan

Stat

e U

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rsity

on

04/0

7/14

For

pers

onal

use

onl

y.

http://dx.doi.org/10.1111/j.1461-0248.2011.01731.x

http://dx.doi.org/10.1111/j.1461-0248.2011.01731.x


http://dx.doi.org/10.1093/beheco/arm144



http://dx.doi.org/10.1111/j.1461-0248.2007.01034.x





http://dx.doi.org/10.1093/beheco/ari006

http://dx.doi.org/10.1046/j.1420-9101.2002.00389.x

http://dx.doi.org/10.1046/j.1420-9101.2002.00389.x

http://dx.doi.org/10.1007/s00265-003-0622-3

http://dx.doi.org/10.1098/rsbl.2004.0189

http://dx.doi.org/10.1098/rsbl.2004.0189

http://dx.doi.org/10.1111/j.1365-2435.2008.01532.x

http://dx.doi.org/10.1111/j.1365-2435.2008.01532.x

http://dx.doi.org/10.1577/T03-079.1

http://dx.doi.org/10.1073/pnas.1212536109




http://dx.doi.org/10.1111/j.1461-0248.2005.00858.x


http://dx.doi.org/10.1007/s00265-003-0751-8


http://dx.doi.org/10.1007/s00265-008-0685-2

http://dx.doi.org/10.1002/ece3.72


http://dx.doi.org/10.1086/285537


http://dx.doi.org/10.2307/1941633

http://dx.doi.org/10.2307/1941633

http://dx.doi.org/10.2307/1936675

http://dx.doi.org/10.2307/1937508

http://dx.doi.org/10.1093/beheco/arp018

http://dx.doi.org/10.1093/beheco/arp018




http://dx.doi.org/10.1093/beheco/ars123

http://dx.doi.org/10.1139/f2011-019

http://dx.doi.org/10.1139/f2011-019


http://dx.doi.org/10.1037/0735-7036.107.3.250

http://dx.doi.org/10.1037/0735-7036.107.3.250

http://dx.doi.org/10.1016/0169-5347(94)90134-1

http://dx.doi.org/10.1086/665656

http://dx.doi.org/10.1086/665656







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