FITNESS TRADEOFFS CAN CONTRIBUTE TO THE MAINTENANCE OF VARIATION IN PERSONALITY TRAITS IN
LARGEMOUTH BASS (MICROPTERUS SALMOIDES)
By
Nicholas G. Ballew

A DISSERTATION
Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of
Zoology – Doctor of Philosophy
Ecology, Evolutionary Biology, and Behavior – Dual Major
2014

ABSTRACT
FITNESS TRADEOFFS CAN CONTRIBUTE TO THE MAINTENANCE OF VARIATION IN PERSONALITY TRAITS IN
LARGEMOUTH BASS (MICROPTERUS SALMOIDES)
By
Nicholas G. Ballew
Studies examining selection and fitness differences between phenotypes are essential for our
understanding of evolutionary processes. Although many studies have examined fitness effects of
morphological and life-history traits, studies of selection on personality traits are much less common.
This has been due, in part, to the fact that personality is not easily characterized into phenotypes. In
addition, personality has historically been viewed as highly plastic and therefore less likely to be under
the direct influence of selection. However, recent studies suggest that personality is often consistent
over biologically meaningful time periods. If personality traits are consistent across development, they
have the potential to affect fitness through impacts on survival at the juvenile stage and reproductive
success at the adult stage. Thus, personality traits may have a range of effects on fitness, some of which
could result in tradeoffs. Further, personality likely determines an individual’s vulnerability to human
capture and harvest in a variety of contexts, which means human actions could alter the effects of
personality on fitness. For example, a fish’s personality may affect its vulnerability to capture by
recreational angling, which could alter the relationships between personality and survival and
reproductive success. Moreover, if personality traits are heritable, angling could result in the evolution
of personality traits in angled populations, which could have ecological consequences. Consequently,
studies to explain how personality is generated and maintained by evolution are greatly needed.
Here, I address the fitness consequences of multiple personality traits across life stages and
their heritability in largemouth bass (Micropterus salmoides). Further, I address how angling could alter
these fitness effects. To quantify personality and investigate its consistency, bass were observed in the
laboratory under experimental behavioral contexts at age-1, age-3, age-4, and age-5. Bass behavior was

observed in four contexts: 1) a novel environment, 2) a familiar and safe environment, 3) a social
environment (mirror-test), and 4) an environment in which both food and a predator were present. To
quantify the fitness effects across life stages of the personality traits uncovered in the experimental
behavioral assays, experiments were conducted in outdoor ponds on juvenile survivorship and on adult
reproductive success. Further, bass were subjected to one of three angling contexts: 1) a mesocosm
context, 2) an outdoor pond context, and 3) an outdoor pond context with casts made directly onto bass
nests. Lastly, personality was quantified in two generations of bass to assess personality heritability.
The results showed that bass have context-specific personality traits that underlie the
expression of behavior in each of the four contexts investigated and that the context-specific traits are
sub-modules of a context-general trait, which was identified as boldness. The boldness trait, as well as
some of the context-specific traits, were consistent across multiple years and developmental stages.
Bolder juvenile bass had significantly lower survivorship than their conspecifics while adult bass that
were larger and bolder had significantly higher reproductive success. Additionally, relationships were
found between some of the context-specific traits and juvenile survival and reproductive success. Bolder
bass were more vulnerable to angling in the mesocosm context and bolder nesting males were more
vulnerable to nest angling. Additional relationships were found between some of the context-specific
traits and angling vulnerability. Boldness was the only personality trait that was significantly heritable.
The results of this dissertation demonstrate for the first time that personality traits that are
consistent across development can affect fitness in multiple ways over the course of an individual’s
lifetime. In some environments, these fitness effects can result in tradeoffs that could maintain within
population variation in personality traits. Further, the results indicate that the selective capture of fish
by angling can alter the selective landscape acting on personality traits, which could have significant
evolutionary and ecological consequences and could affect the quality of fisheries.

Copyright by
NICHOLAS G. BALLEW
2014

ACKNOWLEDGEMENTS

I thank Mary Tate Bremigan, Tom Getty, and Kim Scribner for their helpful suggestions during
the design and implementation of my research experiments as well as for their insightful comments on
earlier versions of this dissertation. Additionally, I thank Cristopher Mirque and Matthew Bach for their
help during parts of the data collection process. A special thanks goes to Gary Mittelbach for his integral
role in all phases of this dissertation, from conception to completion. Lastly, this research could not have
been completed if not for grants from the US National Science Foundation (IOS-1311455), Sigma Xi,
Kellogg Biological Station, and the Zoology Department at Michigan State University.

v

TABLE OF CONTENTS

LIST OF TABLES……………………………………………………………………………………………………………………………..…..ix
LIST OF FIGURES………………………………………………………………………............................................................xi
CHAPTER 1: Fish Behavioral Types and their Ecological Consequences………………................................1
ABSTRACT……………………………………………………………………………………………………………………...1
INTRODUCTION…………………………………………………………..………………………………………….………2
Terminology and measurement………………….……………………………………….………4
The evolution and maintenance of variation in behavioral traits…………………6
Fitness tradeoffs……………………………………………………………………………..6
Inter-individual differences in metabolism and state………………………7
ECOLOGICAL CONSEQUENCES OF BEHAVIORAL TYPES…………………………………………………...9
Ecological consequences at the individual level……………………………………..…..10
Growth and survival……………………………………..………………………………..10
Reproductive success……………………………………………………………………..14
Habitat use and foraging specialization…………………………………………..15
Conclusions…………………………………………………………..………………………..17
Consequences at the population, community, and ecosystem level………..….18
MANAGEMENT IMPLICATIONS OF BEHAVIORAL TYPES…………………………………………………..21
Fishing……………………………………………………………….………….………………………..…..22
Hatchery rearing……………………………………………………….…………………………………25
Effects of artificial selection on behavior…………………………………….…..25
The effects of hatchery rearing environments on behavior………….....27
DISCUSSION…………………………………………………………….………………………………………………………29
Examining behavioral type effects on growth and survival……………………….....29
Diet, habitat use, and ontogenetic niche shifts…………………………………………....30
Consistency in behavioral traits across life stages and fitness tradeoffs……….31
Heritability of behavioral traits and consequences arising from the release of
domesticated fish……………………………………………………………………………..………….33
SUMMARY…………………………………………………………………………………………….………………………..35
ACKNOWLEDGEMENTS……………………………………………………………………………………………………35
APPENDIX…………………………………………………………………………………………………………………….….37
LITERATURE CITED………………………………………………………………….……………………………..……....49
CHAPTER 2: The Reliability and Accuracy of Four Behavioral Tests Frequently Used to Quantify
Personality……………………………………………………………………….....................................................................61
ABSTRACT……………………………………………………......................................................................61
INTRODUCTION…………………………………………….....................................................................62
METHODS……………………………………………………......................................................................64
Novel context…………………………………………………….............................................65
Familiar and safe context……………………………………………………...........................66
Social context (mirror test) ………………..............................................................66
Food and predator present context……………………………………………………………...67
vi

Statistical analysis…………………………………………………….....................................67
RESULTS……………………………………………………........................................................................69
DISCUSSION……………………………………………………..................................................................70
ACKNOWLEDGEMENTS…………………………………………………….................................................73
APPENDIX……………………………………………………………………………………………………………………….74
LITERATURE CITED……………………………………………………........................................................80
CHAPTER 3: The Consistency of Personality Traits Across a 4-Year Period in Largemouth Bass
(Micropterus Salmoides)…………………………………………………………………………………………………………….……..84
ABSTRACT…………………………………………………….....................................................................84
INTRDUCTION……………………………………………………...............................................................85
METHODS…………………………………………………….....................................................................88
Study species and husbandry…..…...................................................................88
Behavioral assay procedur.…………...................................................................89
Statistical analysis.………………………...................................................................91
RESULTS……………………………………………………........................................................................93
DISCUSSION……………………………………………………..................................................................95
ACKNOWLEDGEMENTS…..………………………………..................................................................98
APPENDIX……………………………………………………………………………………………………………………….99
LITERATURE CITED……………………………………………………........................................................108
CHAPTER 4: Fitness Tradeoffs Across Development Can Contribute to the Maintenance of Adaptive
Personality Differences………………………………………………………………………………………………………………..……112
ABSTRACT…………………………………………………….....................................................................112
INTRODUCTION……………………………………………....................................................................113
METHODS…………………………………………………….....................................................................115
Study population and husbandry....................................................................115
Behavioral assay procedure……………...............................................................116
Experiments………..……………………....................................................................118
Experiment 1: Juvenile survivorship...................................................118
Experiment 2: Adult reproductive success.........................................118
Experiment 3: Personality heritability................................................120
Statistical analysis……………………......................................................................121
RESULTS..............................................................................................................................123
Experiment 1: Juvenile survivorship................................................................123
Experiment 2: Adult reproductive success......................................................123
Personality heritability....................................................................................124
DISCUSSION........................................................................................................................124
ACKNOWLEDGEMENTS.......................................................................................................127
APPENDIX……………………………………………………………………………………………………………….………128
LITERATURE CITED...............................................................................................................136
CHAPTER 5: Personality Affects Angling Vulnerability in Largemouth Bass (Micropterus Salmoides)...140
ABSTRACT............................................................................................................................140
INTRODUCTION...................................................................................................................141
METHODS............................................................................................................................144
Study population and husbandry.....................................................................144
Behavioral assay procedure.............................................................................145
vii

Angling experiments.........................................................................................147
Experiment 1: Mesocosm context……………..........................................147
Experiment 2: Outdoor pond context…..............................................148
Experiment 3: Outdoor pond context with casts made directly onto bass
nests……………………………………………......................................................148
Statistical analysis................................................................................149
RESULTS................................................................................................................................150
Angling experiment 1: Mesocosm context….....................................................150
Angling experiment 2: Outdoor pond context…................................................150
Angling experiment 3: Outdoor pond context with casts made directly onto bass
nests…………………………………………………..............................................................151
DISCUSSION..........................................................................................................................151
ACKNOWLEDGEMENTS.........................................................................................................154
APPENDIX…………………………………………………………………………………………………………………………155
LITERATURE CITED................................................................................................................162

viii

LIST OF TABLES

Table 1

Glossary of terms related to animal personality...............................................................38

Table 2

Summary of evidence for the ecological consequences of behavioral types in fishes at
the individual level............................................................................................................39

Table 3

Summary of evidence for the ecological consequences of behavioral types in fishes at
the population and community level……….......................................................................41

Table 4

Summary of the effects of angling and hatchery rearing on behavioral traits in fishes and
their ecological consequences.……….................................................................................42

Table 5

Definition of terms………………….………...............................................................................75

Table 6

Behaviors measured in the four behavioral assays, the context for each measurement,
common psychological trait(s) assumed to cause behavior, and other internal states that
could affect each behavior..……………….............................................................................76

Table 7

Intra-class correlation coefficients (values in parenthesis indicate 95% confidence
intervals) between standardized measurements in the four contexts as well the
composite personality traits (boldness and energeticness) generated from a principal
components analysis of the measurements in the four contexts.....................................77

Table 8

Contributions (loadings) of the four context-specific measurements in trial periods 1 and
2 to principal component axis 1 and 2…..…………..............................................................78

Table 9

Behaviors measured in the four behavioral assays, the context for each assay, and the
ages in which the assays were conducted…….………...................................................... 100

Table 10

Correlations between context-specific personality traits within each age. Values are
intra-class correlation coefficients (95% confidence intervals in parenthesis) of the
standardized measurements.…….…………………………………...............................................101

Table 11

Principal components analysis of 3 context-specific traits (safe and familiar context,
social context (mirror-test), and predator and food present context) at 12, 15, 36, 48,
and 60 months of age. Only the loadings (first column for each age) and correlations
(second column for each age) for axis 1 are shown..…….…............................................102

Table 12

Temporal consistency within each personality trait across varying time intervals and at
different ages. Values are Pearson correlation coefficients (95% confidence intervals in
parenthesis)…………………………………………………………...…….…............................................103

Table 13

Regressions of personality trait temporal consistency (log-transformed) as a function of
the time between measurements. Values were weighted by the sample size from each

ix

interval (e.g. N = 122 for the 3 month interval and N = 39 for the 48 month interval). Log
(y) = intercept + slope(x)………………………………………...…….…............................................104
Table 14

Logistic regressions of the effect of length and personality on juvenile survivorship in
two different experimental ponds. One pond was older and contained abundant
macrophytes and invertebrates while the other was newly renovated and contained
little vegetation and a less productive invertebrate community. Each model has 233
degrees of freedom. Survival (Yes/No) = Length + Personality + Pond +
Length:Personality + Length:Pond + Personality:Pond. For comparison, the null model
deviance was 329.89……………………………………………...…….…............................................129

Table 15

Linear regressions of the effect of sex, length, and personality on adult bass
reproductive success. Reproductive success = Sex + Length + Personality + Sex:Length +
Sex:Personality + Length:Personality. Each model has 94 degrees of freedom…..........130

Table 16

Linear regressions of the heritability of each personality trait. Each model has 5 degrees
of freedom. Average offspring personality = Mid-parent personality. Regressions
weighted by number of offspring in each family............................................................131

Table 17

Linear regressions of the effect of length and personality on angling vulnerability in
angling experiment 1 (mesocosm). Each model has 30 degrees of freedom. Angling
vulnerability = Length + Personality + Length:Personality..............................................156

Table 18

Logistic regressions of the effect of length and personality on angling vulnerability in
angling experiment 2 (outdoor pond). Each model has 198 degrees of freedom.
Vulnerable to Angling (Yes/No) = Length + Personality + Length:Personality. For
comparison, the null model deviance was 253.80..........................................................157

Table 19

Linear regressions of the effect of length, nest egg count, and personality on angling
vulnerability in angling experiment 3 (nest guarding males). Angling vulnerability =
Length + Nest Egg Count + Personality + Length:Personality + Egg Count:Personality.
Each model has 30 degrees of freedom……………............................................................158

x

LIST OF FIGURES

Figure 1

The consequences of variation in fish behavioral types may be expressed at different
levels of ecological organization (from individuals to ecosystems) and have implications
for conservation and management, as well as basic biology............................................44

Figure 2

Five scenarios (a-f), each depicting the behavior of four individuals (solid horizontal
lines) in two different situations (S1 and S2). In scenario a, all individuals display the
same phenotypes in both S1 and S2 and there is plasticity between situations. In
scenario b, there is phenotypic variability in situations S1 and S2 (equal between
situations), no plasticity between situations, and consistent inter-individual differences
in phenotype between situations. In scenario c, there is phenotypic variability in
situations S1 and S2 (equal between situations), plasticity between situations, and
consistent inter-individual differences in behavior. In scenario d, there is unequal
phenotypic variation between situations S1 and S2 (S2 has much more), inter-individual
differences in plasticity between situations (the individual with the smallest phenotype
has high individual plasticity while the individual with the second smallest phenotype
demonstrates a lower level of plasticity), and consistent inter-individual differences in
behavior (perfect consistency in rank order but less in the raw values). In scenario e,
there is phenotypic variability in situations S1 and S2, plasticity between situations, but
individuals do not show consistent differences in behavior across situations because of
differential directionality in responses. Modified from Dingemanse et al. (2010)…........45

Figure 3

A representation of different phenotypic traits along the pace-of-life continuum. Double
arrows illustrate presumed continuous variation in a trait, with traits grouped under lifehistory strategies, behavior, and physiology, and distributed along a pace-of-life
continuum from “slow” to “fast”. Modified from Réale et al. (2010)..............................46

Figure 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 the vegetation 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. From Ehlinger and Wilson (1988)...................................47

Figure 5

Length-frequency distribution of young-of-year largemouth bass collected from Paul
Lake, Michigan in late August 1994. Fish were categorized by age (age determined using
daily rings from otoliths). Age categories represent roughly the youngest 25%, the
central 50%, and the oldest 25% of fish collected. Only fish >85 mm in length become
piscivorous during their first summer of life. From Post (2003).......................................48

Figure 6

Plots a) and b) depict two possible outcomes for a test of the convergent validity of two
measurements that may both be theorized to measure boldness. Plot a) would support
the theory that the two measurements quantify the same property while plot b) would
suggest that they do not. Plots c) and d) depict two possible outcomes for a test of the
xi

discriminant validity of two measurements that may be theorized to measure two
different personality traits. Plot c) would support the theory that the two measurements
quantify two different traits while plot d) would not……………………………………………………79
Figure 7

Four hierarchical models illustrating alternative hypotheses for the organization and
structure of personality traits. Model (a) proposes a scenario where a general boldness
trait underlies the expression of behavior in each context. Thus, repeated observations
of inter-individual differences in behavior would yield roughly the same correlations
between any two behaviors observed, regardless of whether the observations were
made in the same or different contexts. Model (b) proposes a scenario where contextspecific personality traits underlie the expression of behavior in each context. These
context-specific traits are all sub-modules of the same general boldness trait. Thus,
repeated observations of behavior in these contexts would all yield positive
correlations. However, repeated observations from within contexts would yield higher
correlations than those between contexts. Model (c) proposes a scenario where semigeneral personality traits underlie the expression of behavior within functionally similar
contexts (e.g. foraging and novelty). Thus, repeated observations of behavior would
yield equivalent correlations regardless of whether the observations were made in the
same or different contexts, as long as the contexts where functionally similar (e.g.
involved novelty). Behaviors expressed in functionally different contexts (e.g. novelty
and feeding) would not be correlated. Model (d) proposes a scenario where contextspecific traits underlie behavior in each context and each of these context-specific traits
are also sub-modules of semi-general traits that underlie behavior in functionally similar
contexts (e.g. foraging and novelty). The semi-general traits are themselves submodules of a general boldness trait. Under this scenario, repeated observations of interindividual differences in behavior from within specific contexts would yield the highest
correlations, inter-individual differences in behavior from within functionally similar
contexts would yield the next highest, and inter-individual differences in behavior across
functionally similar contexts would the lowest (but still significant) correlations.………105

Figure 8

Model illustrating the organization and structure of personality traits based on the
results of this study. A context-specific personality trait influenced behavior across all
ages of development that were investigated in the novel environment context, in the
foraging in the presence of an aerial predator context, and in the mirror-test context. A
boldness personality trait generalized beyond specific functional contexts was found to
underlie each of these context-specific traits. A personality trait also influenced adult
(but not juvenile) behavior in the safe and familiar environment. This personality trait
may have been a context-specific trait (indicated by the dashed line between behavior
and the unidentified trait) or may have been the general boldness trait (indicated by a
dashed line between boldness and the unidentified trait)……………...............................106

Figure 9

Regressions of personality trait temporal consistency (log-transformed) as a function of
the time between measurements in the: a) mirror-test context-specific personality trait,
b) food and predation threat context-specific personality trait, and c) boldness trait.
Values were weighted by the sample size from each interval (e.g. N = 122 for the 3
month interval and N = 39 for the 48 month interval). Log (y) = intercept + slope(x). Solid
black regression lines are statistically significant while dashed grey lines are not………107

xii

Figure 10

Model illustrating the organization and structure of personality traits in this population
of largemouth bass. A context-specific personality trait influenced behavior across all
ages of development that were investigated in the novel environment context, in the
foraging in the presence of an aerial predator context, and in the mirror-test context. A
boldness personality trait generalized beyond specific functional contexts was found to
underlie each of these context-specific traits. A personality trait also influenced adult
(but not juvenile) behavior in the safe and familiar environment. This personality trait
may have been a context-specific trait (indicated by the dashed line between behavior
and the unidentified trait) or may have been the general boldness trait (indicated by a
dashed line between boldness and the unidentified trait)…………………………………………132

Figure 11

a) Average boldness and b) average initial length of bass that survived to the end of the
experiment (grey circles) and bass that did not survive (black circles) in the high
vegetation pond and in the low vegetation pond. Error bars indicate the standard error
of the mean…………………………..…………..…133

Figure 12

The effects of boldness, length, and the interaction between them on adult reproductive
success. The light grey plane represents the relationships between the variables for
males and the dark grey plane represents the relationships between the variables for
females. The circles (light grey = males; dark grey = females) represent individual males
and the lines from the circles to the planes represent residual values……….…………..…134

Figure 13

The heritability of boldness. Each circle represents the average boldness of offspring in a
full-sib family. The numbers below the circles represent the number of offspring in each
family. The trend line (black) is weighted by the number of offspring in each family….135

Figure 14

The effect of initial boldness, length, and the interaction between them on angling
vulnerability in a mesocosm experiment. The circles represent individuals and the lines
from the circles to the plane indicate individual residual values.…………………………....…159

Figure 15

a) Average length, b) average mirror-test context trait, and c) average boldness of bass
that were caught and those that were not caught in an outdoor pond. Error bars
indicate the standard error of the mean…….………….………………………………….…………..….160

Figure 16

Effects of a) length, b) nest egg count, c) the safe and familiar context trait, and d)
boldness on angling vulnerability of nest guarding male bass in an outdoor pond. Solid
black lines indicate significant relationships (b-d) while dashed lines do not…..……..….161

xiii

Chapter 1: Fish Behavioral Types and their Ecological Consequences

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

1

INTRODUCTION
Fish, like many other vertebrates, show consistent individual differences in behavior despite
maintaining a high degree of behavioral plasticity. These consistent inter-individual differences in
behavior have been variously termed: animal personalities (Dall et 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,b). Much of the large and rapidly expanding literature on animal
personalities involves studies with fish (Stamps 2007), and it was early work by Huntingford (1976, 1982)
with sticklebacks, and Ehlinger and Wilson (1988) and Wilson et al. (1993, 1994) with sunfish, that
provided some of the first evidence that individuals may exhibit consistent differences in behavioral
traits within a population (e.g., individuals may be relatively shy or bold, aggressive or timid). Wilson et
al. (1993) suggested that such consistent behavioral differences between individuals represented more
than random variation around an adaptive mean. Rather, “individual differences are interpreted not as
the raw material on which natural 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 variation represents different adaptive solutions to a complex environment (e.g., Wolf and
McNamara 2012).
Although studies of animal personalities initially struggled to gain traction against the idea that
variation in phenotype is expected within a population and therefore does not require a special
explanation (Wilson 1998), subsequent years have validated the early insights of Huntingford, Wilson,
and their colleagues. Today the study of consistent individual differences in behavior enjoys a vigorous
growth, as evidenced by the publication of a number of recent reviews; e.g., Sih et al. 2004a,b; Réale et
al. 2007; Sih and Bell 2008; Stamps and Groothuis 2010; Wolf and Weissing 2012; including three
reviews devoted specifically to fish (Toms et al. 2010; Budaev and Brown 2011; Conrad et al. 2011). As
Wolf and McNamara (2012) note, three key features associated with personalities have been observed

2

in a variety of species: (1) variation: individuals differ in their behaviors, (2) consistency: individual
differences in behaviors are stable over time, and (3) correlations: certain behavioral traits (e.g.,
boldness, aggression, exploration) tend be correlated among individuals.
Although consistent individual differences in behavior are now well documented in fish and
other organisms, for the most part these studies have been conducted in the laboratory under simplified
and highly controlled conditions. Studies of behavioral trait variation under natural or semi-natural
conditions are still quite rare (e.g., Fraser et al. 2001; Biro et al. 2007; Adriaenssens and Johnsson
2011a). While laboratory studies have opened the door to the rich array of behavioral diversity found in
nature, a key question before us is what are the ecological consequences of consistent 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 consequences include potential effects on an individual’s survival and reproductive
success, population dynamics (through influences on species’ vital rates; e.g., growth, fecundity, and
survival), community structure and species diversity (through influences on species interactions), and on
the conservation and management of natural resources (Figure 1). To understand these consequences
of animal personalities, we need to study organisms in the complex environments found in nature
(Stamps and Groothuis 2010).
Our goal in this paper is to review what is known about the ecological consequences of
behavioral trait variation in fishes at the individual, population and community levels, including the
consequences of personality for the conservation and management of fishes. More than twenty years
ago, Wilson et al. (1993) noted that the ecological consequences of such consistent individual
differences had not been studied in a natural population of any species. Despite the explosion of
research into animal personalities since Wilson et al.’s paper, the ecological and evolutionary
consequences of consistent inter-individual differences in behavioral traits in natural populations are

3

only now coming into focus (Bolnick et al. 2011; Dall et al. 2012; Sih et al. 2012; Wolf and Weissing
2012). We begin our review with a short description of terminology and measurement issues in the
study of animal personalities, followed by a discussion of the proximate and ultimate factors that may
lead to consistent inter-individual differences in behavior. We then examine what is known about the
ecological consequences of behavioral types in fishes, including effects at the individual, population, and
community levels. We focus as much as possible on studies conducted under natural or semi-natural
conditions, because such field studies are most relevant to elucidating the ecological consequences of
behavioral variation. Finally, we discuss the potential importance of consistent individual differences in
behavior to fisheries management and conservation, specifically examining consequences for
recreational and commercial fishing, hatchery rearing, and stock enhancement.

Terminology and measurement
Multiple terms surround the discussion of animal personalities, which has led to considerable
debate in the literature. Table 1 lists many of the terms used in the study of animal personalities and
defines how we use these terms in the current paper. The terms “animal personality”, “temperament”,
and “coping style” have been used more or less synonymously (Réale et al. 2007). These terms describe
consistent differences between individuals in behaviors across contexts over some period of time and
are most often used to refer to general behavioral patterns (e.g., individual differences in boldness,
activity, and aggressiveness and the relationships between them). We use the term “behavioral type” to
describe an individual’s phenotype (e.g., bold vs shy, aggressive vs timid) relative to other individuals in
the population.
One of the challenges in assessing personality traits in fish and other species is the fact that
behavior can be extremely plastic; individuals often respond to changes in their environment by
adjusting their behaviors to meet current conditions. Further, individuals may differ in their degree of

4

behavioral plasticity, which at the individual level could affect the measurement of personality traits
(Nussey et al. 2007; Dingemanse et al. 2010) and at the population level could affect stability and
population persistence in response to environmental change (Dingemanse and Wolf 2013). A useful
framework for examining personality traits in light of behavioral plasticity is the concept of behavioral
reaction norms (Figure 2). The reaction norm framework illustrates how individual differences in
personality traits can be assessed across multiple contexts to examine consistency of behavioral types
and the extent of behavioral plasticity within and between individuals (Réale et al. 2007; Dingemanse et
al. 2010). For example, Budaev and Brown (2011) provide a table of over a dozen measures that have
been used to assess boldness in fish (e.g. predator inspection, foraging under predation risk, latency to
emerge from cover, behavior in an open field, etc.). Measuring individuals in a number of these contexts
would allow for the development of reaction norms that would more accurately characterize an
individual’s personality type.
The behavioral reaction norm approach also provides an opportunity to identify which measures
actually quantify the same personality trait. The few studies that have investigated correlations among
different personality measures that were thought to quantify the same trait have found some surprising
results (Carter et al. 2013; Garamszegi et al. 2013). For example, two measures that are often assumed
to quantify aggression were investigated in yellow-bellied marmots. While both measures were
repeatable over time, they were independent from each other (Blumstein et al. 2012). A similar result
was found when investigating two measures that are often assumed to quantify boldness (i.e., response
to a novel object and response to a predator; Carter et al. 2012). These results show how different ways
of measuring a personality trait may not be interchangeable, providing additional justification for taking
a reaction norm approach.
The application of behavioral reaction norms is still relatively new and not yet widely applied.
Never-the-less, numerous studies of behavioral types in fish and other organisms provide results that

5

allow us to explore the ecological consequences of personality 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
personality variation in fish and its ecological consequences, we want to emphasize the wealth of
studies that exist for other taxa. These studies provide a broader context in which to view the results
from fishes and we refer readers to publications by Réale et al. (2000), Dall et al. (2004), and
Dingemanse and Réale (2005), as well as the review papers cited in the Introduction, as an entry point to
the literature on animal personalities in birds, mammals, and other groups.

The evolution and maintenance of variation in behavioral traits
Fitness tradeoffs
The fitness consequences of behavioral traits are often context-dependent. For example, bold
behavioral types may be less fit than shy behavioral types in an environment with high levels of
predation, while the opposite may be true in an environment without predators. Behavioral ecologists
have focused on fitness tradeoffs as an important mechanism to explain the generation and
maintenance of variation in behavioral traits within a population, both on ecological and evolutionary
time scales. For example, consider the situation where individuals that are bolder are more likely to
encounter predators, resulting in higher mortality rates. Now imagine that these bolder individuals are
also more likely to encounter more prey per unit foraging time and therefore experience higher feeding
rates, resulting in higher energy gain (Stamps 2007). As a result, under this hypothetical scenario, a
potential tradeoff between energy gain/growth and survival would exist that could maintain variation in
boldness.
Mangel and Stamps (2001) developed a simple model to show how tradeoffs between growth
and survival can result in a range of individual growth rates that all yield equivalent fitness (as measured

6

by r in the Euler-Lotka equation), thus favoring the maintenance of multiple behavioral types within a
population. Similarly, models for the evolution of inter-individual differences in dispersal rates have
been developed under the premise that the expected fitness of “dispersers” equals the expected fitness
of “stayers”, due to a growth-mortality tradeoff (Hamilton and May 1977; Frank 1986; Johst and Brandl
1999; Ronce et al. 2000).
Fish often face situations in nature where there is a potential tradeoff between increased
feeding rate and reduced survival (Lima 1998; Mangel and Stamps 2001). For example; 1) open-water
(pelagic habitats) may contain richer food resources, but pose higher predation risk (e.g., Werner and
Hall 1988; Gliwicz et al. 2006), 2) daytime foraging may yield a higher feeding rate but greater risk of
predation than nocturnal foraging (e.g., Fraser and Metcalfe 1997; Metcalfe et al. 1999; Ryer and Hurst
2008), and 3) more active foragers may encounter more prey (or richer habitats) and grow faster, but
suffer higher mortality rates (e.g., Werner and Anholt 1993; Fraser et al. 2001; Biro et al. 2004, 2006;
Sundström et al. 2004). Fitness tradeoffs can also occur spatially (e.g. one area of a habitat favors one
behavioral type while another area favors a different one), temporally within generations (e.g. across
development or across genetically linked behavioral traits), and temporally between generations (e.g.
frequency-dependent selection).

Inter-individual differences in metabolism and state
While fitness tradeoffs provide a powerful mechanism that may select for a variety of (equal
fitness) behavioral types within a population, the maintenance of consistent behavioral types or
personalities over time requires more than just a fitness tradeoff. To see this, consider the question:
what prevents individuals from continually shifting back and forth between different behavioral types
that have equivalent fitness? Or, stated in another way - why do we find differential consistency (as
defined in Table 1) in behavioral types within a population (e.g., individuals that are consistently bolder

7

than others over time)? One possibility is that individuals differ in their relatively unchanging
physiological traits (e.g., resting metabolic rate or the size of metabolically costly organs) and therefore
the behavioral type that results in the optimal value of the growth-mortality tradeoff differs depending
on physiological state. A number of authors (Stamps 2007; Biro and Stamps 2010; Houston 2010) have
suggested that consistent individual differences in physiological state could be an important factor
promoting the formation of individual differences in personality. The first step in examining this
hypothesis is to determine whether individuals differ consistently in their physiological traits (e.g.,
resting metabolic rates or potential growth rate); the second step is to determine whether any such
differences in physiological measures are correlated with behavioral traits (see Biro and Stamps (2010)
for a review of the literature on resting metabolic rate and their relationship to behavioral traits).
Recently, it has been suggested that behavioral traits may covary with a whole suite of
physiological and life-history traits, such that these covarying phenotypic traits can be effectively
grouped under the umbrella of a “pace-of-life-syndrome” (Réale et al. 2010). Figure 3 illustrates the
potential integration of life-history, behavioral, and physiological traits along a pace-of-life continuum
from “slow” to “fast”. Evidence for a pace-of-life syndrome in fish or other organisms is still tentative
(Adriaenssens and Johnsson 2009). However, Biro and Stamps (2008) show that behavioral traits are
linked to life-history variation in a variety of organisms, including fish. For example, activity rates and
boldness are positively related to growth rates in rainbow trout, Oncorhynchus mykiss (Biro et al. 2004,
2005, 2007), and boldness is positively related to growth, fecundity, and size at maturity in Atlantic
silverside, Menidia menidia (Walsh et al. 2006). The pace-of-life syndrome provides a useful heuristic
framework in which animal personality studies can be integrated to address how behavioral traits are
maintained within populations, and how they may have ecological consequences affecting individual
growth, survival, and reproductive success, as well as population dynamics and successful resource
management. Moreover, viewing behavioral variation in the light of life-history traits and the pace-of-

8

life syndrome allows us to consider the impacts of behavioral trait variation at different life stages and
to better understand when and why personality types may be maintained over ontogeny (e.g., Schürch
and Heg 2010; Chervet et al. 2011), even potentially across metamorphosis (e.g., Wilson and Krause
2012a,b).
There are additional ways in which the “state” of an individual can affect the relative costs and
benefits of different behavioral actions, leading to the generation and maintenance of adaptive
behavioral trait variation within a population (Houston and McNamara 1999; Dingemanse and Wolf
2010; Luttbeg and Sih 2010; Wolf and Weissing 2010, Wolf and McNamara 2012). In the case of foraging
boldness (where taking greater risk yields higher rewards), Luttbeg and Sih (2010) show how positivefeedback mechanisms can maintain differential consistency in behavioral traits. For example, if
individuals having higher state (e.g., better condition, larger size, more energy reserves) are better at
defending themselves or fleeing from predators, then animals with higher state will have lower
predation risk while being bold and should be bolder than low state individuals (Luttbeg and Sih 2010).
Thus, small differences in initial state between individuals (e.g., due to parental provisioning, carryover
from larval to adult stages) can lead to a positive-feedback loop between assets and behaviors, such that
“….individuals that already have high state (assets) would be bold, and thus gain more resources that
maintain their high state” (Luttbeg and Sih 2010: 2979). In addition, positive feedbacks based on
experience or learning can lead to differences in foraging efficiency in a habitat or on a particular prey
type that can act to reinforce and maintain behavioral differences between individuals (Werner et al.
1981; Dingemanse and Wolf 2010).

ECOLOGICAL CONSEQUENCES OF BEHAVIORAL TYPES
“Surprisingly little attention has been paid to the ecological and evolutionary consequences of
personality differences” (Wolf and Weissing 2012: page 452).

9

In the sections above, we examined the factors thought to drive the evolution and maintenance
of animal personalities in fish and other organisms. These mostly theoretical studies seek to provide
“ultimate” evolutionary explanations for the existence of consistent differences in behaviors between
individuals. In the following sections, we focus on the ecological consequences of these behavioral
differences. That is, given the presence of varying behavioral types within a population, how might this
behavioral variation affect the ecology, management, and conservation of fishes. These ecological
consequences may include effects on an individual’s survival and reproductive success, the dynamics of
populations (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 and fish stocks (e.g., through hatchery rearing and
supplemental stocking). We recognize that separating the factors thought to ultimately drive the
evolution of behavioral types in fishes from the more proximate consequences of such behavioral types
to the ecology of individuals and populations is a somewhat false dichotomy. Ecology and evolution go
hand in hand. Still, this distinction is useful for highlighting how the existence of behavioral types within
a population may impact various aspects of an individual’s ecology (e.g., growth, survival, diet, habitat
use), as well as population dynamics and species interactions.

Ecological consequences at the individual level
Growth and survival
Personality traits have the potential to affect an individual at nearly every stage of development,
from a juvenile’s chances of surviving to adulthood to an adult’s reproductive success. We summarize
what is known about the ecological consequences of behavioral trait variation in fish at the individual
level in Table 2. Table 2 includes both laboratory and field studies. However, in the discussion below we

10

focus on the results from natural and semi-natural environments because field studies provide the most
direct tests of the ecological consequences of behavioral trait variation. Looking first at the impact of
boldness, aggressiveness, and exploration on individual growth, dispersal, and survival, we find support
for a hypothesized growth-mortality tradeoff, although the evidence from field studies is surprisingly
limited.
Fraser et al. (2001) found that bolder individuals of the Trinidad killifish (Rivulus hartti) moved
greater distances in the field. Moreover, movement distance was positively correlated with individual
growth over a 19-month mark-recapture study in a section of river containing Rivulus predators.
However, in a predator-absent zone, there was no correlation between movement and growth (Fraser
et al. 2001). Our own studies with juvenile bluegill (Lepomis macrochirus) in ponds have shown a
positive correlation between boldness measured in the laboratory and individual growth rates observed
in the field over periods of 2-6 months (M. Kjelvik and G. Mittelbach, unpublished data). In studies
comparing domestic and wild strains of salmon and trout, Sundström et al. (2004) and Biro et al.
(2003a,b, 2004) examined the growth, survival and habitat use of fish in the presence and absence of
predators. Sundström et al. (2004) found a trade-off between growth and survival for strains of coho
salmon (Oncorhynchus kisutch) transgenic for growth-hormone (GH) relative to wild salmon. In
seminatural stream channels, GH-transgenic coho fry grew faster than wild coho fry, but suffered higher
mortality from predators (non-transgenic coho juveniles) (Sundström et al. 2004). Higher mortality on
GH-transgenic fry was most pronounced under low food conditions. Other studies have documented
increased risk-taking behavior in GH-transgenic salmon in the laboratory (Abrahams and Sutterlin 1999;
Sundström et al. 2003), as well as increased movement 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 strains modified with GH relative to wild populations (but see Johnsson and
Björnsson 2001).

11

In a series of whole-lake experiments, Biro et al. (2003a,b, 2004, 2006) compared the growth,
survival, and habitat use of domestic (hatchery stock) and wild strains of rainbow trout (Oncorhynchus
mykiss). In the presence of avian predators (loons, Gavia immer), age-1 domestic trout grained 20%
more mass than wild trout (Biro et al. 2004) and age-0 domestic trout gained 100% more mass than wild
trout (Biro et al. 2006). However, domestic trout (age-0 and age-1) suffered 50- 60% greater mortality
than wild trout when predators were present (Biro et al. 2004, 2006). Behavioral differences between
domestic and wild strains in the field were not specifically quantified in these experiments. However, in
a subsequent field experiment (Biro et al. 2007), the authors examined more directly the behaviors of
domestic and wild rainbow trout strains released into lakes that differed in predation pressure from
loons. They found that fish from the domestic strain responded less to the presence of predators, used
riskier habitats, and had higher catch rates during the day than did fish from the wild strain. Thus, Biro et
al. (2007: page 894) conclude that “greater overall activity and greater daytime use of deep and pelagic
habitats by the domestic genotype should lead to greater growth (given sufficient food) but higher
predation mortality”. These and other studies comparing the behaviors, growth, and survival of
domestic versus wild stocks of salmonid fishes provide some of the clearest evidence for the ecological
consequences of behavioral trait variation under a growth-mortality tradeoff.
Other studies in natural or semi-natural environments provide no support for the expected link
between behavioral traits and a growth-mortality tradeoff. Adriaenssens and Johnsson (2011a) found
that shy trout (individuals with low exploration tendency in the lab) actually grew faster than bold trout
when released into a natural stream. In a subsequent study, they found no significant effects of activity
or exploration measured in the laboratory on growth in the field, and if we can assume that recovery
following release into the wild is an indication of survival, they found that more active individuals had
higher survival (Adriaenssens and Johnsson 2011a). In both of the above studies, fish were collected

12

from the wild, assayed for behavioral traits in the laboratory, and then released back into the wild at a
site near where they were collected.
Höjesjö et al. (2011) also found no association between boldness measured on juvenile brown
trout (Salmo trutta) reared in the laboratory and their growth and survival when released into the river
that was the source of the parental stock. However, only about 4% of the released fish were recovered,
which raises the question of whether the missing fish died or simply moved away. The inability to
distinguish mortality from disappearance in release/recovery experiments into the wild (especially when
recovery rates are low) greatly hinders the ability to assess the impact of behavioral traits on fish
survival (and growth). In Höjesjö et al.’s (2011) experiment, the authors note that juvenile brown trout
in their study population are very stationary (seldom moving further than 200 m). Thus, recapture
should provide a good estimate of survival in the wild.
Following the pace-of-life syndrome (Figure 3), we might expect individuals with bold, active,
and asocial behavioral types to have a higher propensity to explore their environment and disperse
greater distances, which could give them an advantage in terms of finding richer habitats. As stated
earlier, Fraser et al. (2001) found that individual killifish that were bolder in the laboratory dispersed
greater distances when released into the field, and that individuals that moved greater distances in the
field had higher growth rates (in stream sections with predatory fish). Bolder individuals of European
roach (Rutilus rutilus) also showed a greater propensity to migrate (lake to stream) than shy individuals
(Chapman et al. 2011), more asocial mosquitofish (Gambusia affinis) moved further from their social
conspecifics when simultaneously introduced to experimental streams (Cote et al. 2010), and dominant
brown trout moved longer distances and had larger home ranges in a radio telemetry study (Höjesjö et
al, 2007). An individual’s dispersal tendency is likely related to the strength of its social network (the
number of social interactions an individual has and the strength of those interactions), which itself has
been shown to be affected by an individual’s behavioral type. A study with guppies investigating the

13

relationship between boldness and social networks found a correlation between an individual’s boldness
(measured by predator inspection and shoaling tendency in the lab) and aspects of its social network in
natural shoals in the field. Bolder individuals were found to have fewer total social connections and the
average strength of the connections they 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 to carry with them higher mortality costs, if migrating or dispersing
greater distances increases exposure to predators. However, no studies that we are aware off have
assessed these mortality costs in the field.

Reproductive success
Behavioral traits have the potential to affect the reproductive success of adults, with both intraand intersexual selection likely to be influenced by inter-individual variation in behavioral traits (Schuett
et al. 2010). Numerous laboratory studies with a variety of fish species document positive relationships
between boldness, dominance, and reproductive success. For example, in zebrafish (Danio rerio) the
boldest and most aggressive males fertilized more of a female’s eggs than the shyer and less aggressive
males (Ariyomo and Watt 2012) and in guppies, females (Poecilia reticulata) have been shown to prefer
to mate with bolder males (boldness measured by predator-inspection behavior; Godin and Dugatkin
1996). However, field studies examining the relationship between behavioral traits and reproductive
success are still quite rare. Our own studies with largemouth bass (Micropterus salmoides) demonstrate
that boldness measured in the laboratory is positively correlated with nesting success in the field; i.e.,
bolder males were more successful at building nests and receiving eggs when stocked into ponds with
females than less-bold males (N. Ballew and G. Mittelbach, unpublished data). These apparent fitness
benefits of being bolder and more aggressive may be offset in other situations (see Discussion).

14

Behavioral traits also have the potential to affect offspring survival during periods of parental
care. For example, in fish species that build and guard redds or nests (e.g., Salmonidae, Centrarchidae),
bolder, more aggressive individuals are likely to outcompete conspecifics to secure better nesting sites,
and bolder, more aggressive individuals may be better at guarding their nests from potential predators
(McPhee and Quinn 1998). A series of studies by D.P. Philipp and colleagues, using largemouth bass lines
that originated from a single wild population and were selected over multiple generations for increased
or decreased vulnerability to recreational angling during the non-nesting season, show that the high
angling vulnerability (HV) line and low angling vulnerability (LV) line differ in parental care behavior and
reproductive success (Philipp et al. 2009). Male bass from the high vulnerability to angling line displayed
increased parental care activity and higher reproductive success in ponds with nest predators (juvenile
bluegill) compared to males from the low vulnerability line (Cooke et al. 2007; Sutter et al. 2012). It is
difficult to say how the trait of angling vulnerability relates to more commonly studied behavioral traits
such as boldness and aggression. However, our own studies with largemouth bass show that male bass
assayed as more aggressive towards conspecifics in the laboratory are more diligent at defending their
nests from potential brood predators (bluegill) in the field and have higher reproductive success (N.
Ballew and G. Mittelbach, unpublished data).

Habitat use and foraging specialization
Behavioral traits related to boldness/aggression, foraging styles, or predator avoidance have the
potential to affect habitat use and resource consumption. For example, a study with bullheads (Cottus
perifretum) found that less aggressive individuals (as assayed in the laboratory) showed a greater
propensity to use complex habitats (i.e., branch jams) in the field (Kobler et al. 2011). In the same study,
there was no correlation between habitat use in the field and individual differences in activity level
measured in the laboratory. Functional linkages may also exist between behavioral traits that confer

15

greater feeding efficiency in particular habitats and morphological traits, leading to complex
polymorphisms (Wolf and Weissing 2012). In one of the first studies to look for an association between
morphological and behavioral traits, Ehlinger and Wilson (1988) examined a foraging polymorphism in
populations of bluegill sunfish. They found that bluegill collected from a small, Michigan lake clustered
into two behavioral (foraging mode) types when allowed to feed on open-water prey (zooplankton) and
benthic prey (damselfly nymphs) in the laboratory (Figure 4). These behavioral differences between
individuals were stable across a 20 week testing period.
Differences in foraging behaviors (hover duration) between bluegill individuals corresponded to
differences in feeding rate; fish exhibiting relatively short hover durations were more successful at
capturing zooplankton whereas fish displaying longer hover durations where more successful at
capturing damselfly nymphs. When Ehlinger and Wilson (1988) compared the morphologies of these
two behavioral types, they found that morphology and behavior were tightly correlated. Fish classified
as “vegetation” (benthic) morphological types exhibited long hover durations, whereas fish classified as
“open-water” morphological types exhibited short hover durations. Subsequent morphological analyses
of sunfish (bluegill and pumpkinseed, Lepomis gibbosus) collected from open-water and littoral habitats
in lakes confirmed the subtle but repeatable morphological distinctions between phenotypes associated
with pelagic and littoral habitats (Robinson et al. 1993; Robinson et al. 2000).
Selection on morphological and behavioral traits that increase feeding efficiency on certain prey
types or within certain habitats is likely to go hand-in-hand. Therefore, an important question is how
much does habitat/foraging specialization lead to the development of animal personalities and the
generation of behavioral trait variation within a population? Further, might there be subtle differences
in functional morphology between behavioral types within populations that have generally gone
undetected? The morphological differences between bluegill behavioral types in the study of Ehlinger
and Wilson (1988) were not visible to the naked eye, but were detectable with morphometic analyses

16

(e.g., Ehlinger and Wilson 1988; Robinson et al. 1993; Robinson and Wilson 1996). Other fish species
(e.g., threespine stickleback) show distinct resource polymorphisms in morphology/behavior/resource
use in some populations (McPhail 1993), but continuous variation in others (Robinson 2000). Thus, how
much subtle variation in morphology and physiology is associated with inter-individual behavioral
variation in populations is unknown. When viewed in the holistic framework of individual specialization
(Bolnick et al. 2011), it is clear that inter-individual differences in behavioral types and personalities may
be an expected outcome of natural selection acting on populations in a complex environment.

Conclusions
At the individual level, variation in boldness, activity, and dispersal is often hypothesized to
result from a tradeoff between growth and mortality (i.e., bolder fish are more active and grow faster,
but suffer higher mortality). Despite wide-spread acceptance of a growth-mortality tradeoff as a likely
driver of behavioral variation in fish (Stamps 2007), to date there is little empirical evidence from field
studies and the results are mixed (Table 2). Studies of other taxa (mammals, birds) also provide only
mixed support for the hypothesis that bolder (more exploratory) individuals take more risks to gain food
but may suffer higher mortality as a result (e.g., Réale and Festa-Bianchet 2003; Dingemanse et al. 2004;
Réale at al. 2007; Quinn et al. 2012). The strongest support for a growth-mortality tradeoff associated
with differences in boldness or aggression in fish comes from studies of wild versus domesticated strains
of trout and salmon (e.g., Biro et al. 2003a,b, 2004; Sundström et al. 2004).
Boldness and dominance appear to be positively associated with increased mating success in the
laboratory and in the field, and individuals more vulnerable to angling exhibit more persistent nest
guarding behavior and greater reproductive success in pond studies with largemouth bass. Boldness and
aggression during reproductive events are likely to have negative consequences for adult energetics,
survival and future reproductive success, and there are many examples of the high cost of parental care

17

in fishes (e.g., Dufrense et al. 1990; Gillooly and Baylis 1999; Steinhart et al. 2005). To date, however, no
field studies have examined the full set of correlations between boldness/aggression during the
breeding season, offspring survival, and adult current and future reproductive success. In the Discussion
section, we consider how the costs and benefits of various behavioral traits may differ at the adult and
juvenile life stages. Such life-history asynchrony in the impact of behavioral traits may provide an
additional mechanism for the maintenance of variation in behavioral traits within a population.
Field studies also suggest that habitat heterogeneity and habitat-specific foraging success may
maintain phenotypic polymorphisms in fish populations that include both behavioral and morphological
traits. For example, in sunfish and sticklebacks, behaviors associated with increased foraging success in
limnetic versus benthic habitats are also associated with variation in morphological traits (fin placement,
body shape), resulting in complex polyphenisms (e.g., Ehlinger and Wilson 1988; Robinson and Wilson
1996; Robinson 2000; Weese et al. 2012). Thus, there are many opportunities in nature for consistent
individual differences in behavior to arise when individuals can exploit different habitats and resources.
Ecologists, behaviorists, and evolutionary biologists have joined together to highlight the importance of
studying how environmental heterogeneity and habitat selection may generate and maintain
intraspecific variation in populations, including variation in behavioral traits (Adriaenssens and Johnsson
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, and ecosystem level
Intraspecific variation in behavioral traits can have numerous effects at the population,
community, and ecosystem levels. Recent reviews have highlighted the potential for behavioral traits to
affect population dynamics, predator-prey interactions, species diversity, and ecosystem primary
productivity (Sih et al. 2012; Wolf and Weissing 2012). However, when compared to consequences at
the individual level, far fewer theoretical expectations have been proposed for population and

18

community level consequences of multiple behavioral types within traits. Similarly, few empirical studies
have examined the population and community level consequences of behavioral trait variation, and (to
our knowledge) no studies have been conducted in natural conditions. We summarize in Table 3 the
limited number of laboratory and mesocosm studies on the topic, looking first at studies that have
investigated ecological consequences of variation in behavioral traits at the population level, then
moving to studies examining consequences to species interactions, and concluding with studies on
consequences to ecosystem functioning.
Population level consequences of behavioral trait variation have been investigated in terms of
group performance and population dynamics. For example, shoal composition for boldness affects
foraging success in guppies. Fish from mixed shoals were found to feed more than fish from all bold or
all shy shoals, indicating that shoals containing a mixture of boldness behavioral types may outperform
all bold and all shy shoals (Dyer et al. 2009). In a study with shoaling European perch, the frequency of
different risk-taking behavioral types within the shoal was shown to affect overall shoal risk-taking
behavior and bold individuals had an especially large effect on shoal behavior (Magnhagen and
Bunnefeld 2009). A study with threespine sticklebacks investigated the effect of a population’s
composition of bold and shy individuals on population social structure. Individuals were assayed for
boldness in the laboratory (measured as hesitancy to feed after being startled) and then artificial
populations were formed based on the boldness scores. Populations were composed of either all shy
individuals, all bold individuals, or were a mix of bold and shy individuals. The all shy populations had
stronger social structures (measured as the average number of interactions for all individuals in the
population) than the all bold populations. Additionally, the all shy populations were more cliquish,
meaning social subgroups appeared to form (Pike et al. 2008). A field study with roach, while not
directly investigating population level consequences, found that bold roach had a higher propensity to
migrate (lake to stream) than shy roach (Chapman et al. 2011). Roach practice partial migration (only a

19

fraction of the population migrates). Thus, it is easy to see how the frequency of bold behavioral types
could impact the proportion of the population that migrates.
In terms of species interactions, the consequences of behavioral types to predator-prey
interactions, inter-specific competition, and invasive ability have been investigated in a single study for
each type of interaction. In threespine stickleback, boldness was found to affect prey risk, with bolder
sticklebacks feeding more heavily on chironomid larvae in laboratory trials (Ioannou et al. 2008). In a
study that investigated inter-specific competition between two species of sticklebacks (threespine and
ninespine), bold behavioral types were found to consume more prey in heterospecific competitive
foraging trials, regardless of species (Webster et al. 2009). The only study to date on behavioral traits
and invasiveness found no relationship between the level of boldness and invasiveness for four
Gambusia species (Rehage and Sih 2004).
A key (but unanswered) question in the study of the population-level consequences of animal
personalities is whether the amount of variance in behavioral traits within a population matters. That is,
if populations share the same mean value for a given behavioral trait but possess different mixtures of
behavioral types, is there an effect on population dynamics? If behavioral types are non-randomly
distributed in space, such that they select different foraging habitats (e.g., Wilson et al. 1993), occupy
different positions within a shoal (e.g., Ward et al. 2004), or preferentially associate with like behavioral
types, then the mixture of behavioral types in a population will matter.
No studies to our knowledge have directly measured the effects of individual variation in
behavioral traits on ecosystem functioning. However, a few studies suggest the possibility of such a
relationship. An outdoor mesocosm study using guppies taken from natural streams that differ in
predation pressure found that mesocosms containing guppies from the high predation environment
contained fewer benthic invertebrates and more algae after a 28 d period than mesocosms with guppies
from the low predation pressure environment (Bassar et al. 2012). In total, 9 of 13 ecosystem variables

20

measured by Bassar et al. showed significant river-of-origin effects. The authors attributed these
differential effects on ecosystem functioning, in part, to differences in foraging behavior by guppies
adapted to the different stream environments. However, Bassar et al. (2012) measured only one
behavioral variable directly in their experiment (pecking at the substrate) and this behavior did not
differ in fish from high predation and low predation sites. Thus, it is possible that other phenotypic
differences between the populations caused the observed ecosystem effects. Harmon et al. (2009) and
Des Roches et al. (2013) conducted similar types of mesocosm studies comparing the ecosystem effects
of two threespine stickleback morphotypes (benthic and limnetic; McPhail 1993; Schluter 2000) and
found significant effects of stickleback type on a variety of ecosystem functions. Again, behavioral
variation was not specifically measured in these ecosystem studies, but previous work on stickleback
morphotypes has shown pronounced differences in foraging behaviors between benthic and limnetic
forms (e.g., Schluter 1993). Thus, while no studies that we are aware of definitively link variation in
behavioral traits to effects on ecosystem functioning, the potential for such effects clearly exists and
there is abundant opportunity for both theoretical and empirical studies that specifically examine the
consequences of inter-individual variation in behavioral types to communities and ecosystems.

MANAGEMENT IMPLICATIONS OF BEHAVIORAL TYPES
When considering the ecological consequences of behavioral trait variation at the individual and
population level, it is important to remember that these consequences are dependent on environmental
context. For example, bold behavioral types may be less fit than shy behavioral types in an environment
with high levels of predation, while the opposite may be true in an environment without predators.
Therefore, human impacts on the environment, such as recreational angling, commercial fishing, and
hatchery-reared stocking programs, are likely to affect the ecological consequences of consistent interindividual behavioral variation. For example, bolder individuals may be more vulnerable to angling,

21

which could decrease their fitness relative to more timid individuals and result in the population
becoming less bold on average. In the same way, hatchery rearing programs may select for certain
behavioral types, resulting in hatchery stocks that differ genetically from wild populations (Huntingford
2004; Fraser 2008). Additionally, the hatchery environment can cause differences in the way behavioral
traits develop with ontogeny. We summarize in Table 4 what is known about the management
implications of behavioral trait variation and discuss these implications in more detail below. We note
that many of the studies summarized in Table 4 have compared behavioral traits of different groups of
fish (high vs. low angling vulnerability; domestic vs. wild stock), as opposed to comparing behavioral
differences among individuals within a population.

Fishing
It is increasingly recognized that fishing pressure (recreational angling and commercial fishing)
may alter the individual-level consequences of behavioral types, which in turn could affect natural
selection and the evolution of population characteristics (Uusi-Heikkila et al. 2008; Philipp et al. in
press). For example, in non-fished populations of species that build and guard nests or redds, aggressive
individuals may defend their nests more vigilantly from potential predators, increasing egg and larval
survivorship. However, the introduction of angling could turn high nest guarding aggressiveness into a
detriment if aggressive nest guarding individuals are more likely to be caught than their less aggressive
counterparts (e.g., as shown by Cooke et al. 2007). Removal of the nest-guarding parent (even shortterm removal by catch-and-release angling), can greatly increase the probability of egg and larval
mortality (Siepker et al. 2007). Personality traits also have the potential to affect angling vulnerability
outside of the nesting season (though the traits may be different).
The hypothesis that recreational angling can affect the relationship between behavior and
reproductive success is supported by the previously mentioned study on reproductive success and

22

parental care in two largemouth bass lines selected for different vulnerabilities to angling during the
non-nesting season. Bass from the line selected for high vulnerability to angling showed increased levels
of aggression towards potential nest predators and greater diligence of parental care compared to bass
from the low vulnerability line. Importantly, the high vulnerability line was also found to have the
highest reproductive potential (Sutter et al. 2012). Thus, angling can reduce reproductive success and
lower total reproductive output not only in current generations but also impact selection for traits
associated with nest guarding behavior, potentially leading to reduced reproductive success and lower
total reproductive output in future generations as well. Furthermore, as angling almost certainly selects
for traits that reduce angling vulnerability, high levels of recreational angling are likely to impact the
ability of the population to provide recreational angling opportunities in the future. This result was
recently documented in bass populations that have historically been exposed to different levels of
angling intensity (Philipp et al. in press).
As discussed earlier, bolder individuals in some fish species have been found to forage more
actively and grow faster than their shyer counterparts. Angling, however, could alter the ecological
consequences of boldness, shifting the balance towards shyer foragers if bold fish are captured more
frequently. A recent study by Nannini et al. (2011) compared the foraging behaviors of individual
largemouth bass obtained from the two artificially selected high and low angling vulnerability lines
previously described. Contrary to expectations, fish from the low vulnerability line actually captured
more prey (and attempted to capture more prey) than fish from the high vulnerability line. The low
vulnerability line also had higher prey rejection rates and was more efficient at converting consumed
prey into growth than the high vulnerability line (Nannini et al. 2011). While this study clearly
demonstrates the potential for angling during the non-nesting season to have a selective effect on
foraging behavior, it also cautions against jumping to conclusions about what behavioral types are likely
to be associated with increased angling vulnerability. Only one study that we are aware of has explicitly

23

tested the link between an individual’s boldness and angling vulnerability during the non-nesting season.
Wilson et al. (2011) found that more timid bluegill were more likely to be caught by angling than their
bolder counterparts in a natural lake – again, a result opposite of expectations. These early studies
highlight the need for more research on the link between fish behavioral traits and responses to angling
during the nesting and non-nesting seasons at the individual and population levels. However, unlike the
relatively recent focus on the evolutionary impacts of recreational angling, the impacts of commercial
fishing on fish life histories, growth rates, and behaviors have been studied for a much longer time.
Several studies over the last two decades have documented that the selective harvest of large
individuals by commercial fisheries leads to decreased growth rates in future generations, as well as a
variety of other effects (e.g., Conover and Munch 2002; Hutchings 2004; Reznick and Ghalambor 2005;
Walsh et al. 2006). More recently, it has been proposed that commercial harvest may also selectively
target individuals based on their behavioral type and growth rate, irrespective of size. As Uusi-Heikkila et
al. (2008; page 419) note, “fishing-induced selection directly acting on behavioral rather than on lifehistory traits per se can be expected in all fisheries that operate with passive gears such as trapping,
angling and gill-netting”. Biro and Post (2008) found exactly this result in an experimental study of
rainbow trout in Canadian lakes, where faster-growing individuals were found to be more vulnerable to
harvest by gill nets irrespective of their size. The authors attributed the greater vulnerability of fastergrowing individuals to differences in their behaviors, as faster-growing fish were more active and bolder
than their slower-growing, non-harvested counterparts (Biro and Post 2008). Even if commercial fishing
does not select directly on behavioral traits, early findings from the pace-of-life syndrome suggest that
direct selection on one trait, be it a behavioral trait like boldness or a life-history trait like growth rate,
likely leads to indirect selection on a whole suit of correlated traits. These effects can have important
impacts on species performance as well as community dynamics, making it essential that fisheries
managers consider these effects when making management decisions.

24

Hatchery rearing
Hatchery rearing and fish stocking represent the opposite-side of the coin from fish harvest; i.e.,
they add rather than remove fish from a population. But, like selective harvest, hatchery programs
designed to supplement the abundance of wild populations can impact behavioral variation and may
have important ecological consequences. It is well known that fish raised in hatchery environments
often perform poorly when stocked into the wild (Araki et al. 2008) and there is a long-standing debate
on whether or not hatchery stocking demographically boosts wild populations. For this reason, there is a
wealth of literature examining how hatchery selection, including both purposeful selection on desirable
traits (such as increased growth rate) and unintentional selection resulting from rearing experiences,
may affect fitness (see reviews by Huntingford 2004; Huntingford and Adams 2005; Araki et al. 2008;
Fraser 2008). Changes in behavioral phenotypes due to domestication selection have been suggested to
be a major factor contributing to the poor performance of hatchery-reared fish stocked into the wild
(Fraser 2008).

Effects of artificial selection on behavior
Common garden studies demonstrate that offspring from hatchery-reared adults are often
bolder and/or more aggressive than those from wild stocks (e.g. Berejekian 1995; Einum and Fleming
1997), and laboratory studies comparing the behaviors of domestic and wild strains have found that
domestic strains tend to be bolder and more aggressive than their wild counterparts (Budaev and Brown
2011; Conrad et al. 2011). For example, fry from sea-ranched brown trout parents initiated feeding
sooner and bit at a novel object more often than fry from wild brown trout parents (Sundström et al.
2004). Domesticated strains of fishes often undergo selection aimed at increasing production traits such
as rapid growth (Huntingford 2004). However, selection for increased growth rate can have

25

unintentional consequences on behavioral trait variation, either by altering variation in the behavioral
traits themselves (e.g., selecting for individuals that are more bold/aggressive/active in their feeding
behaviors), or selecting on metabolic traits that may cause individuals to act more boldly to fulfill their
metabolic needs (see prior discussion on this topic).
Behavioral traits that confer an advantage to individuals in a hatchery environment may carry a
cost in nature. The most obvious examples involve feeding behaviors in the absence or presence of
predators. The work by Biro and colleagues discussed earlier nicely documents how domesticated trout
strains grow faster but suffer higher mortality than wild fish when stocked into natural lakes with
predators (Biro et al. 2006, 2007). Looking at foraging behavior in a different context, Adriaenssens and
Johnsson (2011b) assayed hatchery-reared and wild-origin brown trout for cognitive tasks such as
cryptic prey discovery and maze solving. They found that hatchery-reared trout had higher feeding rates
than wild fish, but they did so with less accuracy. In the wild, lowered accuracy in foraging may incur
energetically costly errors such as prey misidentification, whereas higher foraging rates may be
advantageous in hatchery settings with consistent food dispersal (Adriaenssens and Johnsson 2011b).
The behavioral syndromes approach has been applied to determine whether selection on
behaviors in the hatchery environment (e.g., propensity to feed in a predator-free environment), may
influence the distribution of behaviors expressed in other environments (e.g., aggressiveness, boldness
under predation risk). For example, Lee and Berejikian (2008) found that juvenile rockfish (Sebastes
auriculatis) that fed at high rates in the absence of a predator also tended to feed at higher rates when a
model predator was present. However, they found the behaviors of individuals were inconsistent across
two assay periods (8-12 days apart), suggesting plastic responses and behavioral flexibility. In contrast, a
study using rainbow trout found that individuals were consistent in their behaviors over 2-3 days and
across safe/unsafe contexts (Conrad and Sih 2009). Behavioral flexibility may be important when
determining whether selection on fast growth rates has unintentional consequences on associated

26

behaviors. Selection may be limited if individuals are capable of changing behavior in response to their
environment. Alternatively, if behaviors are tightly correlated and not plastic, selection for high growth
rates is likely to also select for bold and aggressive individuals. Determining the degree to which
individuals (or species) differ in their behavioral plasticity (e.g., Figure 2), and understanding how early
development and rearing environment may affect levels of behavioral plasticity, are important areas for
future research (Dingemanse et al. 2010; Dingemanse and Wolf 2013).

The effects of hatchery rearing environments on behavior
The process of raising juvenile fish in hatchery environments has been shown to affect the
cognitive pathways that influence behavior (Huntingford and Adams 2005). Enrichment strategies, such
as providing physical structure, decreasing fish densities, feeding with live prey, and introducing
simulated predator attacks have been suggested to better prepare hatchery fish for stocking (Brown et
al. 2003; Lee and Berejikian 2009; Brockmark and Johnsson 2010; Brockmark et al. 2010; see review in
Huntingford 2004). All of these modifications to current hatchery conditions have been shown to benefit
hatchery-reared fish in ways that could increase post-stocking survival. For example, brown trout
assigned to “low” and “moderate" rearing density treatments showed 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 experimental stream, fish that were reared in high densities
showed decreased survival relative to individuals reared at low or medium density (Brockmark et al.
2010). Individuals that were reared with physical structure, fed natural prey, and subjected to simulated
attacks showed decreased boldness relative to individuals raised under conventional hatchery
conditions (Roberts et al. 2011). When comparing both the presence and stability of physical structure
during rearing, Lee and Berejikian (2009) found that stable structures (the “unstable” treatment moved
structure throughout the experiment) were important for individuals to assess current risk and display

27

behaviors accordingly. Individuals reared with stable structure were more explorative without
predators, but showed reduced exploration under predation threat. Thus, there is accumulating
evidence suggesting that the hatchery experience itself affects behaviors that can have important
implications for fish stocked into the wild (e.g., impacts on habitat use, growth, and survival).
Encouragingly, these studies demonstrate that carefully considering rearing experiences of hatchery fish
and attempting to replicate natural environments could be a promising direction for hatcheries.
Although a number of studies have investigated individual behaviors of hatchery-reared fish in
lab settings and others have compared how hatchery strains compare to wild strains, comparatively few
studies have evaluated how the behaviors of hatchery-reared fish influence their fitness in natural
environments. In one recent study, Moore et al. (2011) examined the field survival and migration rates
of hatchery-reared steelhead trout compared to fish of wild origin across three years. As an additional
component, the hatchery-reared fish were from two hatcheries that differed in rearing environment
(stocking density and shape of tanks). Fish that were reared under lower densities and in circular tanks
(thought to decrease effects of density), survived as well as wild steelhead. However, fish raised at
higher densities and in rectangular raceways showed decreased survival relative to wild fish. Moore et
al. (2011) also found that migration ranges for steelhead from both hatcheries were less than those of
wild steelhead. This study suggests that changes in conventional hatchery rearing may facilitate
behavioral flexibility and the development of cognitive skills fish need upon entering natural systems.
However, to justify these changes, more field studies examining fitness of individuals subjected to
various enrichment regimes are needed to understand how these changes affect survival in natural
conditions.

28

DISCUSSION
Fish have proven to be excellent model organisms for the study of animal personalities,
providing some of the earliest demonstrations of behavioral trait variation in any species (e.g.,
Huntingford 1976, 1982; Ehlinger and Wilson 1988) and continuing today as one of the most studied
taxonomic groups (Stamps 2007; Toms et al. 2010; Budaev and Brown 2011; Conrad et al. 2011). Still, as
Wolf and Weissing (2012) and others have noted, relatively little attention has been paid to the
ecological consequences of varying behavioral types. This comment applies to all species, not just fish,
and is especially true of studies conducted in natural or semi-natural environments. Our review has
sought to summarize what ecologists, behaviorists, and managers know about the ecological
consequences of behavioral types at the individual, population, and community/ecosystem levels,
including implications for fisheries management and conservation. Important research foci in this area
include the impacts of behavioral trait variation on: individual growth and survival, nesting behaviors
and reproductive success, habitat use, diet, and ontogenetic niche shifts, migration and dispersal,
commercial and recreational fishing, and hatchery rearing for supplemental stocking. We discuss these
different research foci below and suggest avenues for future research.

Examining behavioral type effects on growth and survival
The concept of a growth-mortality tradeoff is firmly entrenched in the ecological literature (e.g.,
Werner and Anholt 1993; Lima 1998), and a growth-mortality tradeoff provides much of the theoretical
underpinning for the maintenance of behavioral variation in boldness in fish and other organisms (e.g.,
Stamps 2007). Thus, it is surprising that evidence from natural or semi-natural environments
documenting the effects of variation in boldness and/or aggression on fish growth or survival is limited
and is almost entirely based on comparisons of wild and domesticated stocks (e.g., Biro et al. 2003a,b).
This is not to question the reality of a growth-mortality tradeoff, or to doubt its relationship to fish

29

behavioral traits, but only to note that much more work is needed to examine how individual variation
in boldness affects growth and survival. Archard and Braithwaite (2010) discuss some of the challenges
involved in studying the consequences of behavioral traits in wild animals. They note that a particularly
hard nut to crack is the effect of behavioral type on the survival of free-living individuals, because the
recovery of marked individuals is often very low (see Höjesjö et al. 2011 for an example with fish). The
low recovery of marked individuals leaves us wondering, are missing individuals dead? Or, have they
simply dispersed from the study area? Studies conducted in closed, semi-natural environments
(experimental ponds, outdoor raceways, or fenced reaches of streams), where all surviving individuals
can be recovered post-stocking, can provide useful experimental systems for testing the growthmortality tradeoff and its relationship to boldness variation in fishes.

Diet, habitat use, and ontogenetic niche shifts
Fish, like many other organisms, show pronounced changes in diet and habitat as they grow. For
example, most piscivorous fish begin life feeding on zooplankton and benthic invertebrates before
reaching a size where they can switch to feeding on other fish (Mittelbach and Persson 1998). Many
other fishes occupy protective habitats (e.g., littoral zone vegetation) when small and vulnerable to
predators, and then shift to feeding in more open and riskier habitats when they reach sizes that are less
vulnerable to predation (Werner et al. 1983; Werner and Hall 1988). These ontogenetic niche shifts have
important consequences for population dynamics and species interactions (de Roos and Persson 2013).
However, a completely unexplored question is - what role does personality play in determining the
timing and extent of ontogenetic niche shifts, in fish or other organisms?
Studies documenting ontogenetic niche shifts in diet and habitat 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 of ontogenetic niche shifts is due to differences

30

in personality? Consider for example the study by Post (2003), who examined the factors contributing to
the onset of piscivory in a cohort of young-of-year (YOY) largemouth bass. In bass and other piscivores,
becoming piscivorous in the first summer of life greatly increases fitness by increasing the probably of
surviving through the winter (Buijse and Hourthuijzen 1992; Post et al. 1998). Post (2003) found that
only the largest individuals in the YOY bass cohort from Paul Lake, Michigan were able to successfully
transition to feeding on YOY bluegill during their first summer. Further, all bass that grew large enough
to become piscivorous in their first year were born early in the spring (Figure 5). Birth date, however,
was by itself a poor predictor of either bass size in August or the propensity to shift to piscivory (i.e.,
many early-born bass didn’t get large enough to become piscivorous; Figure 5). Why did some earlyborn bass grow quickly and become piscivorous in their first summer, whereas others did not? Chance
could of course play a role; e.g., some individuals may have been lucky enough to find and consume a
large number of energetically rewarding prey early in life and get a jump on their less-fortunate fellows.
However, it’s tempting to speculate that differences in personality may contribute as well. In this case,
the hypothesis would be that those early-born bass growing large enough to become piscivorous are
individuals that are relatively bold and take greater risks to increase their feeding rate, either by being
more active or by using riskier habitats. No studies to date have examined the impact of behavioral
types on the timing of ontogenetic niche shifts. This seems a particularly ripe area for future research.

Consistency in behavioral traits across life stages and fitness tradeoffs
Numerous studies have documented consistency in behavioral traits or behavioral syndromes in
fish and other organisms over relatively short time periods of days and weeks (Bell et al. 2009; Conrad et
al. 2011). However, much less is known about consistency in behaviors across longer time periods or
across life stages. Wilson and Godin (2009) found that shy-bold behavioral types showed differential
consistency in bluegill sunfish over a 1-3 month period (measured in the field). However, Bell and

31

Stamps (2004) and Edenbrow and Croft (2011) observed little differential consistency in individual
behavioral types between life stages (e.g., juveniles to adults) in threespine sticklebacks and mangrove
killifish (Kryptolebias marmoratus) respectively (measured in the lab). In a study of how behavioral
consistency changed across ontogeny in an Africa cichlid (Steatocranus casuarius), Budaev et al. (1999)
found that behaviors (response to a novel environment, a novel fish, and a mirror) were not consistent
in juveniles (4 and 4.5 months of age), but were consistent in adults (12-13.5 months). Bell and Stamps
(2004) measured three types of behavior (activity, aggression toward a conspecific, and boldness under
predation risk) at three developmental stages (juvenile, subadult, and adult) and found that individual
behavioral types were not stable over ontogeny. In one stickleback population, the boldness-aggression
behavioral syndrome was stable over ontogeny (showed structural consistency), but in another
population it was not. Edenbrow and Croft (2011) also found that behavioral types of boldness and
exploration were highly plastic during ontogeny, but that correlations between these two behaviors (i.e.,
bold types were more exploratory) were maintained from juvenile to adulthood (structural consistency;
see also Schürch and Heg 2010, Chervet et al. 2011).
Studies with aquatic organisms other than fish have observed differential consistency in activity
traits across life stages: e.g., tadpole to adult frog (Rana ridibunda; Wilson and Krause 2012a), nymph to
adult damselfly (Lestes congener; Brodin 2009). In general, however, we know very little about the
differential consistency of behavioral traits across life stages (e.g., juvenile to adult) or in individuals
undergoing ontogenetic niche shifts (e.g., freshwater to marine, benthic to pelagic, insectivorous to
piscivorous). Clearly, such long-term differential consistency in behavioral traits has important
implications for fitness and for the maintenance of variation in behavioral traits in populations.
If behavioral traits have differential consistency only over short-intervals, then the potential for
fitness tradeoffs to contribute to the maintenance of variation in behavioral traits is rather limited.
However, if behavioral traits are consistent across life stages or across ontogenetic niche shifts, then

32

there are many more opportunities for tradeoffs to occur. For example, it is commonly assumed that
boldness may have a positive effect on individual fitness through increased energy gain and/or
reproductive success, but a negative effect due to reduced survival (Stamps 2007; Smith and Blumstein
2008). If fish that are relatively bold as juveniles are also relatively bold as adults, then boldness could
positively affect fitness at the juvenile stage through higher feeding rates/energy gains and at the adult
stage through greater reproductive output (per breeding event), but negatively affect fitness at the
juvenile stage due to decreased survival, and/or negatively affect reproductive success at the adult stage
due to decreased survival during a reproductive event and/or reduced probability of surviving to
reproduce again. Thus, there are multiple ways in which boldness effects on growth, fecundity, and
survival could trade off to affect lifetime fitness.
To date, studies that have investigated the relationship between behavioral traits and fitness
have generally focused on a single measure of fitness (such as survival) at a specific life stage
(Dingemanse and Réale 2005; Smith and Blumstein 2008). However, fitness tradeoffs across life stages
or between different components of selection (sexual and viability), provide a potentially powerful
mechanism for the maintenance of adaptive variation in behavioral traits. Moreover, if behavioral traits
are heritable, the fitness consequences of animal personalities can extend across generations.

Heritability of behavioral traits and consequences arising from the release of domesticated fish
Although there are relatively few estimates of the heritability of behavioral traits in fishes, the
evidence suggests that many behavioral traits are heritable, with levels of heritability that are generally
lower than those for morphological traits, but roughly comparable 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 able to artificially select stocks of largemouth bass to
express high and low vulnerability to recreational angling (Sutter et al. 2012), demonstrating again a

33

strong genetic component to certain aspects of fish behavior. The heritability of behavioral traits has
many important ecological implications, particularly with regard to the mixing of wild and domestic fish
stocks.
Fisheries biologists have long been concerned with potential consequences of interbreeding
between wild, hatchery-reared, or escaped farmed fish, particularly salmon, (e.g., Gross 1998). This
concern has been largely focused on the detrimental effects of introducing non-adaptive life-history
traits into wild stocks (causing, for example, a mismatch in the timing/orientation of migration and
reproduction). However, interbreeding between wild and domestic stocks (e.g., farmed or hatcheryreared fish) could influence behavioral traits as well, with unknown consequences for wild fish. A
number of studies comparing domestic and wild strains of salmon and trout show that hatchery-reared
fish, or fish that have been genetically modified for faster growth, may be bolder, more aggressive,
and/or more risk-prone in their habitat use, resulting in higher growth rates but reduced survival in
nature (e.g., Abrahams and Sutterlin 1999; Sundström et al. 2003, 2004; Biro et al. 2003a,b, 2004, 2007;
Sundt-Hansen et al. 2009). To the extent that behavioral traits are heritable and adaptive, the
interbreeding of domestic and wild fish stocks has the clear potential to reduce the fitness of locally
adapted stocks.
Commercial and recreational fishing may also select on heritable behavioral traits that have
unanticipated evolutionary consequences. One possibility discussed earlier is the association between
boldness/aggression in nest guarding behavior and angling vulnerability in largemouth bass. Male bass
that are bolder and more aggressive are more diligent in guarding their young and have higher
reproductive success (Cooke et al. 2007). However, bolder/more aggressive bass may also be more
vulnerable to recreational angling (Suski and Philipp 2004). Thus, if boldness and aggression are
heritable traits (see Bell 2005), then increased fishing pressure may lead to the evolution of reduced
boldness/aggression in the population, a reduction in angling vulnerability, and the unwelcome

34

consequence of a reduction in average reproductive success (Sutter et al. 2012). Here again, an
understanding of the correlations among behaviors, combined with a knowledge of their heritabilities,
and their ecological consequences at different life stages, is an important avenue for future research for
the effective management of fish stocks.

SUMMARY
Inter-individual variation in behavioral traits is now recognized to be an important feature of
most animal populations, including fish. In this review, we have sought to highlight some of the
mechanisms driving the evolution and maintenance of variation in behavioral traits within fish
populations, as well as the ecological consequences of this variation. Field evidence for the ecological
consequences of behavioral trait variation is still quite limited in any group of organisms. However,
there is little doubt that behavioral trait variation plays an important role in the growth, survival, and
reproductive success of individuals, as well as having potential impacts on species interactions and
ecosystem functioning. It is also clear, however, that we must be careful not to jump to conclusions
about the universality of the causes and consequences of behavioral trait variation (e.g., the growthmortality tradeoff) without more evidence from nature. In fishes, behavioral trait variation has added
implications for conservation, harvest, and resource management. Biologists and managers recognize
the importance of environmental context to the evolution of behavioral traits and the role that
behavioral variation among individuals and between populations (wild versus domestic stocks) may play
in successful stocking and conservation. Again, more data from field studies, especially with
tagged/marked individuals of known behavioral types, is crucial.

ACKNOWLEDGEMENTS
We thank Alison Bell, Pat Hanly, David Philipp, and two anonymous reviewers for their comments and

35

suggestions, and for sharing unpublished manuscripts. Our special thanks to Judy Stamps for her many
insightful comments on an early version of the manuscript. Grants from the US National Science
Foundation supported portions of this research (IOS-1210438 to MK and GGM; IOS-1311455 to NGB and
GGM). This is contribution number 1732 from the W.K. Kellogg Biological Station.

36

APPENDIX

37

Table 1. Glossary of terms related to animal personality.
Term
Definition
Behavior/ behavioral response

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

Behavioral/personality trait

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/personality type

An individual’s consistent response over a given period of time
relative to other individuals for one or more behavioral 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 across time (Caspi et
al. 2005; Réale et al. 2007; Stamps and Groothuis 2010).

Differential consistency

Consistency between individuals in a particular behavior (or
behavioral trait) across time (Stamps and Groothuis 2010).

Contextual generality

Consistency between individuals in behaviors measured in
different contexts (e.g. activity in a safe, familiar environment
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 to behave in a
certain way may be correlated across contexts or over time). In
this sense, behavioral syndromes and animal personalities
describe similar phenomena. A behavioral syndrome also may
describe a correlation between two or more behavioral traits
between individuals in a population (e.g., boldness and
aggression are commonly 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”
life-styles.

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 and Weissing (2012).

38

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

Field

Sociability

More asocial fish had a higher tendency to disperse.

Cote et al. 2010

Lab

Social network

Boldness

Bolder fish had fewer total social connections and the
average strength of the connections were weaker.

Croft et al. 2009

Field

Growth

Exploration and
Aggressiveness

Slow explorers grew faster. Aggressiveness was not
related to growth.

Adriaenssens and
Johnsson 2011a

Field

Boldness

No correlation between boldness and growth.

Höjesjö et al. 2011

Field

Boldness

Bolder fish grew faster.

Ward et al. 2004

Lab

Boldness

Bolder fish were preyed on more.

Dugatkin 1992

Lab

Exploration 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

Field

Boldness

No correlation between boldness and survival.

Höjesjö et al. 2011

Field

Activity,
Boldness, and
Exploration

More active, bold, and exploratory individuals survived
longer with predators.

Smith and Blumstein
2010

Lab

Survival

39

Table 2 (cont’d).
Consequence

Trait(s)

Result

Study

Study Method

Social status

Boldness

Bolder fish were more dominant.

Dahlbom et al. 2011

Lab

Aggressiveness,
Boldness, and
Activity

Males that were more aggressive, bolder, and more
McGhee and Travis 2010,
active had higher positions in the dominance hierarchy. Colleter and Brown 2011

Boldness

Females chose bolder males as mates.

Godin and Dugatkin 1996 Lab

Aggressiveness

Females chose low or moderately aggressive males,
whereas highly aggressive males were rarely chosen.

Ward and Fitzgerald,
1987

Lab

Boldness and
Activity

Assortative mating based on personality type.

Budaev et al. 1999

Lab

Boldness and
Aggressiveness

Bolder and more aggressive male zebrafish fertilized
more eggs.

Ariyomo and Watt 2012

Lab

Survival of
offspring during
parental care

Aggressiveness

Females that were more aggressive in guarding their
nests from threats were found to stay on their nests
longer.

McPhee and Quinn 1998

Field

Habitat use

Aggressiveness,
Boldness, and
Activity

More aggressive individuals were found more frequently
in open water whereas less aggressive individuals were
found in or near structured refuge. No relationship
between 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

Reproduction

Lab
Lab

40

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 more than
full shy shoals. Mixed shoals fed most.

Dyer et al. 2009

Lab

Boldness

Shoal group behavior was impacted by the frequency of
boldness types within the shoal. Bold individuals
especially impacted shoal behavior.

Magnhagen and
Bunnefeld 2009

Lab

Social structure

Boldness

Populations of all shy fish had stronger social structures
and were more cliquish than populations of all bold
fish.

Pike et al. 2008

Lab

Predator-prey

Boldness

Prey where more heavily preyed upon by bolder fish.

Ioannou et al. 2008

Lab

Interspecific
competition

Boldness

Bolder behavioral types were found to consume more
prey regardless of species in heterospecific
competitive foraging trials.

Webster et al. 2009

Lab

Invasiveness

Boldness

No relationship between boldness and invasiveness.

Rehage and Sih 2004

Lab

41

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
Angling
Male bass that have a high vulnerability to angling
Sutter et al. 2012
Field
individuals
vulnerability with
demonstrated greater anti-predator aggression and
reproductive
parental care and have higher reproductive success.
success, antipredator
aggression, and
parental care
Between
individuals

Angling
vulnerability and
foraging
behavior

Bass that have a low vulnerability to angling foraged
more frequently 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 than more timid bluegill.

Wilson et al. 2011

Lab and Field

Domestic, wild
strains

Boldness,
dominance

Domestic fish initiated feeding sooner, but no
difference in latency to approach novel object.
Domestic fish bit at novel object more. All bold fish,
regardless of origin were socially dominant.

Sundström et al. 2004

Lab

Hatchery vs wild
rearing, low vs.
high density
hatcheries

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. 2011

Field

42

Table 4 (cont’d).
Comparison
Between
individuals

Variables
Boldness

Result
Behavioral syndromes found between behavior with
and without predators, behaviors plastic during 16
weeks in hatchery environment.

Study
Lee and Berejekian 2008

Study Method
Lab

Rearing
conditions with
structure vs.
without structure

Exploration

Individuals reared with stable structure increased
exploration without predators, but no difference in
structure treatments with predators.

Lee and Berejikian 2009

Lab

Conventional vs.
enriched rearing

Boldness

Roberts et al. 2011

Lab

Low, medium,
conventional
rearing densities

Survival,
Exploration,
Boldness

Individuals subjected to simulated predator attacks,
physical structure, and natural prey showed
decreased boldness than conventional rearing.
Fish from lower densities consumed more prey,
increased predator response, located food in a maze
faster, and increased survival in field.

Brockmark et al. 2010

Lab and Field

43

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

44

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

45

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

46

Figure 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 the vegetation 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. From Ehlinger and Wilson (1988).

47

Figure 5. Length-frequency distribution of young-of-year largemouth bass collected from Paul Lake,
Michigan in late August 1994. Fish were categorized by age (age determined using daily rings from
otoliths). Age categories represent roughly the youngest 25%, the central 50%, and the oldest 25% of
fish collected. Only fish >85 mm in length become piscivorous during their first summer of life. From
Post (2003).

48

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CHAPTER 2: The Reliability and Accuracy of Four Behavioral Tests Frequently Used to Quantify
Personality

ABSTRACT
Broad personality traits, such as boldness, entail individual differences in behavior that are
consistent both across contexts and across time. However, broad personality traits are frequently
quantified by measuring behavior in a singular context at a single point in time. For personality
measurements obtained in this way to be valid, the behavioral tests used must yield highly repeatable
and accurate measurements. Unfortunately, the repeatability and accuracy of behavioral tests are rarely
verified. Using largemouth bass (Micropterus salmoides), I investigated the repeatability and accuracy of
behavioral tests commonly employed in fish. I measured behavior in four contexts: 1) novel
environment, 2) familiar and safe environment, 3) social context, and 4) a context with food and a
model predator present. Measurements were repeated two days after initial measurements. Intraclass
correlation coefficients were calculated within tests across trial periods to assess repeatability and
between tests within trial periods to assess accuracy. The behavioral measure in a familiar and safe
context lacked the repeatability necessary for a singular measurement to be used as a reliable
personality trait measure. In contrast, single measures in the other three contexts could be used to
reliably quantify personality. However, each of the three reliable measures contained a degree of
context specificity, making them somewhat inaccurate measures of broad personality traits. When
considering the four context-specific measures in combination, a principal components analysis revealed
a component that was a reliable personality trait measure and that could be identified with a term
independent of any specific context (i.e. boldness). Key Words: Personality traits, behavioral syndromes,
boldness, measurement validity, repeatability, methodology.

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INTRODUCTION
Consistent inter-individual differences in behavior are a common feature of many animal
populations (Stamps and Groothius 2010; Budaev and Brown 2011). Individuals may behave consistently
across different environmental contexts at a single point in time (Garamszegi et al. 2013) and within
contexts across time (Budaev et al. 1999; Bell et al. 2004; Carere et al. 2005). While less common, some
studies have also shown that the relationship between behaviors measured in different contexts can be
consistent across time (Brodin 2009). Thus, while behavior is produced as a stream of actions that can
be adjusted almost instantaneously to match the context at hand, inter-individual consistency in
repeated measures of behavior indicates that behavior is also the product of at least semi-stable traits
(Chaplin et al. 1988). The traits responsible for producing consistency in repeated measures of behavior
are variously termed “personality traits”, “temperament traits”, and “behavioral traits” (Réale et al.
2007).
The study of personality traits may provide answers to questions central to the study of
behavioral ecology, such as, how apparently sub-optimal behaviors persist in populations (Dingemanse
and Wolf 2010). Unfortunately, methodological challenges make the study of personality traits difficult.
One major challenge in the study of personality traits is that it is rarely possible to identify the trait
responsible for producing a behavior in terms of a concrete property, such as a specific gene, brain
function, or physiological mechanism (but see Hariri 2009). As a result, researchers turn to more
abstract psychological descriptions (e.g. boldness, aggressiveness, etc.) to categorize the personality
traits of individuals. The apprehension to use such descriptions has led some researchers to abandon a
trait-based categorical system of psychological descriptors all together and instead simply describe and
catalog the contexts (e.g. predator present, novel environment, etc.) in which personality traits are
observed (Table 5). The overall inability to identify the trait producing behavior is the basis of a recent
perspective article aptly titled “Animal personality: what are behavioral ecologists measuring?” (Carter

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et al. 2013). A related challenge is that even after deciding what trait is being measured, there is often
no direct way to measure it. Researchers have little choice other than to measure personality traits
indirectly through noisy indicator variables (Borsboom, 2008). Specifically, researchers use behavioral
measures, which are thought to be the product of at least semi-stable traits acting in combination with
additional factors, as proxy measures of personality to overcome the methodological challenges of
measuring personality traits. While in general this approach to measuring personality traits is
appropriate, the specific behavioral measures that are employed as proxy measures of personality traits
must be individually validated (Burns 2008).
First, the reliability of a behavioral measurement to serve as a proxy measure of a personality
trait must be investigated. Temporally repeated measures must be taken to verify that a measure is
stable (test-retest reliability). If a behavioral measure lacks stability over repeated measures, it likely
indicates that the behavioral measure is largely affected by unstable states (e.g. hunger level) and/or
unstable contextual effects. Unfortunately, the reliability of behavioral measures is only investigated in
roughly 25% of personality studies (Gosling 2001; Miller et al. 2005). Second, after determining that a
measurement does reliably measure the same property when repeatedly used, the alignment between
the measure and the interpretation made from it must be validated. To do so, the relationship between
measures theorized to quantify the same trait (convergent validity) and measures theorized to quantify
different traits (discriminant validity) must be assessed (Figure 6). Convergent and discriminant validity
are very rarely investigated in personality studies and in the few studies in which they have been
investigated, the specific measures investigated have often been found to be invalid (Miller et al. 2006;
Burns 2008; Beckmann and Biro 2013). Thus, studies that investigate the reliability and accuracy of
measures of personality are sorely needed.
In this study, I investigated the validity of four personality trait measures in largemouth bass
(Micropterus salmoides), a fish species native to eastern North America. Behavior was observed in four

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contexts to obtain proxy measures of personality traits: 1) behavior in a novel environmental context, 2)
behavior in a familiar and safe environmental context, 3) behavior in a social context (mirror test), and
4) behavior in a context containing both food and a model predator (Table 6). The behavior of each bass
was measured in each of the four experimental contexts twice, with a 2-day interval between measures
in the same context. A 2-day interval between trials was chosen because it likely surpasses the stable
period of most highly fluctuating internal states (e.g. hunger level) that could affect the measure, while
at the same time minimizing the amount of plasticity experienced by more stable traits.
I investigated the reliability of each behavioral test by examining the repeatability between the
values obtained from the first and second test in each context. I also assessed relationships between
measurements that have been theorized to measure the same trait (convergent validity); e.g., the length
of time to enter a novel environment and the length of time to approach food in the presence of a
predator have both been interpreted as measures of boldness. Further, I performed a principal
component analysis on the measurements from the four experimental contexts to organize them into
components that may be more readily interpretable as context independent traits that can be described
with common psychological terms. The results of this study help address whether a variety of measures
commonly employed in the study of animal personalities do in fact quantify the personality traits
intended (Carter et al. 2013).

METHODS
Sixty five largemouth bass were collected in June, 2011 from a pond located at the Kellogg
Biological Station experimental pond facility in southwest Michigan. The 65 bass were bred on site from
adult bass that were collected from nearby Wintergreen Lake. Bass ranged from 1 to 3 years of age and
averaged 207.9 ± 67.4 mm in total length (± 1 standard deviation). Bass were individually marked with
colored elastomer gel (a biocompatible pliable polymer; Northwest Marine Technology, Goldsmith et al.

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2003) that was injected subcutaneously at two of seven possible locations. Bass were held in large (1000
liter) outdoor covered tanks for about 4 days. During this time, bass could feed on zooplankton ad
libitum. The day before bass were to be tested, they were transferred to the laboratory and socially
housed in 110 L aquaria (4 bass per aquarium) and again provided with an excess amount of
zooplankton. On the testing day, bass were transferred from the indoor holding aquaria into their own
110 L aquarium. Over the next two days, bass underwent a series of behavioral assays (Table 6). Food
was not available to bass during the two day testing period (except for the foraging trial). Following the
completion of the series of behavioral assays, individuals were transferred back to the 110 L group
holding tanks for one day. They were again provided with an excess amount of zooplankton while in the
holding aquaria. The next day, the bass were returned to the testing aquaria and run through the same
set of behavioral assays (again with no food available). The assays were run in the same order for both
testing periods. Thus, all 65 bass were measured twice in each of the four contexts, with a 2 day-interval
between measures in the same context.

Novel context
The 110 liter testing aquaria were divided into two sections by an opaque vertical partition with
the smaller section making up about 10% of the total volume. Individual bass were transferred into the
smaller section of a testing tank and then left for approximately 45 minutes to recover from handling
and to acclimate to the new environment. After the 45 minute acclimation period, using a pulley system,
the partition was raised approximately 10 centimeters above the floor of the aquarium, allowing the fish
to swim from the smaller section into the larger section. For each trial, I measured the elapsed time
from when the partition was raised until the fish swam into the larger area of the tank (up to 15 min). If
after 15 minutes a fish had not moved to the larger section of the tank, I gently coaxed it out. Once a
fish moved into the larger section of the tank, I lowered the partition so that it could not move back into

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the smaller section. An individual’s score in this context was calculated by subtracting the number of
seconds that a fish waited before moving to the larger portion of the tank from 900 (the maximum trial
length). Thus, individuals with higher scores moved more quickly to the larger section of the tank.
Individuals that did not leave the small section during the trial received a score of 0. Following the trial, I
placed a mirror on the wall in the smaller section of the tank (not visible to the fish). Fish were then left
overnight in the larger section of the tank to acclimate to their new surroundings.

Familiar and safe context
The day after introducing a bass into a testing aquaria, I measured the amount of time the bass
spent moving around the tank in the familiar environment (larger section of the tank). Fish were
observed for 5 minutes and I summed the total time spent swimming (moving) to calculate the total
number of seconds active per trial.

Social context (mirror test)
Immediately following the measurement in the familiar and safe environment trial, I raised the
partition to reveal a mirror on the wall in the smaller section of the tank. Once the partition was raised
the trial commenced. Trials lasted for 10 minutes. I measured the number of bites, tail swipes, and rams
at the mirror. At the end of the trial, the partition was lowered so that the mirror was no longer
viewable. As the partition was lowered, fish in the path of the partition consistently retreated to the
larger section of the tank on their own. The number of bites, tail swipes, and rams were summed
together to get an overall measure in this context. These behaviors were summed together because
each was taken to be a specific form of agonistic behavior and other studies have shown that individuals
often exhibit behavioral specificity so that they tend to primarily use their preferred method of a
behavioral type (one individual may primarily use rams while another primarily uses bites; Uher 2011).

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Food and predator present context
Approximately one hour after observing behavior in the presence of the mirror, a live
earthworm tied to monofilament fishing line (no hook) was lowered into the tank near one end. When
the bass approached the worm, a model bird suspended on a string and pulley system positioned
directly above the worm was released to strike the surface of the water, simulating a predation attempt.
The bird was then quickly lifted from the water, again using the string and pulley system. During this
time, the fish most often retreated to a corner of the tank. Once the bird was appropriately positioned
(10 centimeters above the water surface), the trial commenced. Trials lasted for 15 minutes. I recorded
how many seconds it took the bass to re-approach the worm. An individual’s score was calculated by
subtracting the number of seconds that a fish waited before re-approaching the worm from 900 seconds
(the maximum trial length). Thus, individuals with higher scores re-approached the worm faster.
Individuals that did not re-approach the worm during the trial received a score of 0.

Statistical analysis
All statistical analyses were conducted using R version 2.13 (R Development Core Team 2008).
First, each variable was standardized to a mean of 0 and a standard deviation of 1. Standardizing the
measures removes contextual effects (be it due to the external context or habituation between trials 1
and 2) that may be responsible for producing variation in the behaviors. After standardization, the
measures should only include behavioral variation that results from individual differences in states and
traits (and experimental error that occurred in individual trials). To be appropriate proxies for measures
of traits (as opposed to a state), the measures must exhibit minimal intra-individual variation over short
intervals relative to the amount of inter-individual variation that exists in the measures.

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To assess the appropriateness of the measures as indicator variables (i.e. measures of
personality traits), an intra-class correlation analysis was conducted on the standardized values from the
first and second time periods, within and between each context. Measures used for personality traits
should be highly repeatable and have an intra-class correlation coefficient near 1 over short intervals.
The further an intra-class correlation is from 1 for a measurement of a personality trait that is repeated
over short intervals, the larger the amount of error contained in the measurement, be it due to
experimental error or because the measure is affected by states that are unstable across measurements.
Thus, it is the strength of the correlation that must be considered (including the 95% CI’s), not merely
the presence or absence of significance, when investigating the appropriateness of a measure to serve
as a proxy of a trait.
To investigate the categorization of the measures as the same and as different traits
(convergent and discriminate validity; see Figure 6), I performed a second round of intra-class
correlation tests, this time looking at measures within the same assay trial period. I investigated the
relationship between each of the context-specific measurements to assess if the context-specific
measurements were measures of the same traits, of different traits, or something in between. Further,
to determine whether the measurements in the four different contexts could be re-organized into
components that were interpretable in terms of common psychological terms (e.g., boldness), I
conducted a principal component analysis on the context-specific measurements. I then investigated the
relationship between the component personality traits (more readily interpretable as psychological
traits) and the context-specific traits to examine how closely the context-specific traits approximate the
psychological traits that they are often said to describe.

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RESULTS
Intra-class correlation coefficients (ICCs) were significant (all p. values were below 0.05)
between trial periods 1 and 2 for each of the behaviors measured in the four experimental contexts
(along top left to lower right diagonal in Table 7). However, when it comes to assessing the reliability of
the measures, it is the magnitude of the correlations that are truly of interest. In this regard, three of the
measurements showed moderately high ICCs (0.50-0.69) while the fourth (safe and familiar
environment activity) was significantly lower (ICC = 0.30 with an upper 95% CI bound of 0.50). Significant
ICC values were also obtained between the novel environment, mirror-test context, and food and
predator present measurements taken within the same trial periods (Table 7; above the diagonal are
ICCs between measurements in Trial 1 and below the diagonal are ICCs between measurements in Trial
2). However, it is again the magnitude of the correlations that is more relevant when investigating the
convergent and discriminant validities of the measurements.
A principal component analysis revealed a similar pattern in the relationships between the
context-specific measures. Principal component axis 1 explained 49.7% of the variation across the four
experimental contexts in trial 1 and 46.2% of the variation in these measures in trial 2 (Table 8). Based
on the loadings of the measurements from the four experimental contexts, PC axis 1 was interpreted as
“boldness”. It affected behavior in the novel environment, in the mirror-test context, and when food
and a predator were present. Each of these three behaviors contributed positively and to a similar
extent to PC axis 1 in both trials 1 and 2 (Table 8). PC axis 2 explained 24.7% of the variation in trial 1 and
26.7% of the variation in trial 2. PC axis 2 was interpreted as an energeticness or activity personality
trait. The measurement from the safe and familiar environment was essentially the sole contributor to
PC axis 2 in trial 1 (84%) and trial 2 (89%), with a positive loading. PC axes 3 and 4 explained little of the
variation (16.0% and 9.7% respectively during trial period 1 and 18% and 9.1% during trial period 2),

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with little consistency in the loadings of the context measures onto these PC axes. Thus, further analyses
are focused solely on PC axes 1 and 2.
The boldness component trait calculated from the principal components analysis had a higher
intra-class coefficient between trials 1 and 2 than did the measurements from specific contexts that are
also frequently interpreted as boldness (along the top left to lower right diagonal in Table 7). However,
the ICC for the boldness component was not significantly higher than the ICC calculated from the
measurement in the novel context (often also interpreted as boldness). A similar trend in ICCs was also
displayed between the activity component trait and the measurement in the safe and familiar context.
With regard to the suitability of measurements taken from singular contexts to serve as proxies of more
context-general or context-independent traits, the measure taken in the presence of food and a
predator most closely resembles the boldness component measurement (ICC of 0.803 between
measures from Trial 1 and 0.812 between the measures from Trial 2.) However, the measurement taken
when food and a predator were present was not always a significantly better measure of boldness than
the measurement taken in a novel context (upper 95% CI bound of 0.86 in trial 2) or the measurement
taken in the mirror-test context (upper 95% CI bound of 0.84 in trial 1).

DISCUSSION
Each of the four context-specific measurements in this study showed significant, positive
correlations between trial periods 1 and 2. However, this says little about the reliability of the
measurements and their appropriateness to serve as proxies for personality traits. Researchers must
decide on the magnitude of a correlation under test-retest scenarios that is necessary to consider a
behavioral measurement a suitable proxy measurement for a personality trait. For example, correlations
between repeated behavioral measures of 0.5 (Cohen 1988) and 0.7 (Martin and Bateson 1993) have
been proposed as the lower limit that indicates reliability in a measurement. In the current study, 3 of

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the 4 context-specific measurements had ICCs high enough that they could pass a 0.5 magnitude
correlation criterion and be considered appropriate personality trait measures (e.g. novel environment
context measurement ICC 95% CI was 0.54 – 0.80). However, if a criterion of 0.7 was used, none of the
four context-specific measurements would meet the criterion. Only the boldness component trait
surpassed a 0.7 magnitude correlation.
When compared within each time period, significant ICCs between paired measurements
involving the novel environment, the mirror-test, and/or the food and predator present context suggest
that there is considerable overlap in the personality traits that affect behavior in these different
contexts. If we assume that these context-specific measurements assess the same personality trait, then
the ICCs between these measurements could be used to investigate the convergent validity of the
measures. The ICCs (0.34 – 0.57) between these context-specific measures indicate that a theory
treating each of these measures as the same thing would have a low to moderate degree of validity.
Conversely, if these context-specific measurements were theorized to measure completely different
personality traits (i.e. exploration, aggression, and boldness), the significant ICCs would cast doubt on
the theory that the different measures actually measure different traits. In other words, the ICCs
between these context-specific measurements suggest that the level of overlap in what they measure is
too low to consider them measures of the same trait and too high to consider them measures of
completely different traits. This conclusion is further supported by the result that, while the
relationships between measurements in different contexts across the two time periods tend to have
moderately high intra-class coefficients (e.g. novel environment measure and food and predator present
measure ICC = 0.459), the relationships between measurements within a context (e.g. novel
environment measure ICC = 0.690) tend to be significantly higher. Thus, the results of this study agree
with others (Blumstein et al. 2012; Watanabe et al. 2012; Carter et al. 2012) that indicate that a
psychological descriptor (i.e. boldness) is often a relatively inaccurate description of a personality trait

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measured in any singular context. As a result, personality traits measured with a context-specific
measure are likely most appropriately described in terms of the context in which the measure was
taken, as opposed to a psychologically-based description.
Unfortunately, problems also arise from categorizing traits based solely on the contexts in which
they are measured. The most obvious problem is that different studies may use a variety of different
experimental contexts. Thus, the number of potential contexts used could be very large, making it
difficult to compare results between studies. An option to address this issue is that the number of
contexts could be condensed down to a few basic categories (such as the five contexts suggested by
Réale et al. 2007). However, creating a context-based classification system for personality traits may
give the false impression that traits in the same general category necessarily are the same biological
trait while those in different categories are different traits. For example, measurements taken in a novel
environment and those taken in foraging contexts may be classified into two different categories even
though both measurements to a large degree measure boldness (propensity to take risks). Thus, given
the issues involved in accurately describing and categorizing personality traits, I suggest that the most
appropriate methodological approach is to take measurements in multiple contexts.
By taking measurements in multiple contexts, researchers can identify component traits that
likely represent more accurate measures of psychological traits than any context-specific
measurements. Additionally, researchers can employ a biologically-based categorization system and can
ensure that their methods are valid. I used this approach in the current study and found that
personality traits calculated by principal components analysis of multiple context-specific measurements
were more repeatable than measurements in a single context. Additionally, based on the loadings of
each context-specific measure onto each component, component 1 likely represents the quality of
boldness (willingness to expose oneself to risk) better than any of the context-specific measures.
Although measuring behaviors in multiple experimental contexts involves more time and effort than

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assessing personality traits in a single experimental context, the results of this study show that a
multiple context approach yields more fruitful results.
With the use of appropriate methods, researchers can move beyond the identification and
description of traits to begin to understand the causes and consequences of personality traits. For
example, further investigation into the boldness trait revealed in the current study could help
researchers learn if boldness is explained by differences in sex, size, stage of development, and/or some
other quality of an individual, such as metabolic rate or organ size. Furthermore, the current study
indicates that singular traits (i.e. boldness) may be responsible for producing the behavioral syndromes
often observed between contexts (see also Bell 2005, Dingemanse et al. 2007). If an individual’s
phenotype is relatively stable across relatively long time periods (Sinn 2008; Chervet et al. 2011; Wilson
and Krause 2012), the resulting behavioral syndrome(s) could have important ecological consequences
(Sih et al. 2004; Smith and Blumstein 2008; Conrad et al. 2011; Sih et al. 2012). Further, if the behavioral
syndrome(s) result from a heritable personality trait (Van Oers et al. 2004; Sinn et al. 2006; Norton et al.
2011), the trait could function as an evolutionary constraint preventing individuals from exhibiting
optimal behaviors at different life stages and could contribute to the maintenance of multiple
personality types within a population (Mittelbach et al. 2014).

ACKNOWLEDGEMENTS
I thank Melissa Kjelvick and Mary Bremigan for their comments on a previous version of this
manuscript. A special thanks goes to Gary Mittelbach for his many insightful comments and suggestions
on earlier versions of this manuscript. Grants from the US National Science Foundation (IOS-1311455),
Sigma Xi, Kellogg Biological Station, and the Zoology Department at Michigan State University supported
portions of this research.

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APPENDIX

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Table 5. Definitions of terms.
Term
Personality trait

Definition
Characteristic of an individual that is stable over some time period and is responsible for contributing to the
production of behavior.

Internal state

Characteristic of an individual that can fluctuate greatly over relatively short time periods (mood, hunger
level, etc.)

Psychologically-based
classification system

The use of abstract psychological (e.g. bold, aggressive, etc.) descriptions in the categorization of
personality traits of individuals.

Context-based trait
classification system

The use of contextual information (e.g. predator present, novel environment, etc.) in the description of
personality traits of individuals.

Convergent validity

An assessment of the degree to which a test actually measures what it purports to measure by investigating
the relationships between measures that are theorized to be measurements of the same trait.

Discriminant validity

An assessment of the degree to which a test actually measures what it purports to measure by investigating
the relationships between measures that are theorized to be measurements of different traits.

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Table 6. Behaviors measured in the four behavioral assays, the context for each measurement, common psychological trait(s) assumed to cause
behavior, and other internal states that could affect each behavior.
Behavior
Context for behavior
Psychological trait(s) theorized
Other temporary states that
to produce behavior
could affect behavior
Length of time to enter new
Opportunity to move into novel
Boldness, Exploration
Restlessness
habitat
environment
Amount of time moving

Familiar and safe open-field
environment

Energeticness,

Restlessness, Tiredness

Bites and rams at mirror

Mirror added to open-field
environment

Aggressiveness, Boldness

Irritableness

Length of time to approach food

Model bird predator strikes water
above food

Boldness

Hunger level

Note: A more in depth discussion of this issue as it specifically relates to boldness can be found in Budaev and Brown, 2011.

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Table 7. Intra-class correlation coefficients (values in parenthesis indicate 95% confidence intervals) between standardized measurements in the
four contexts as well the composite personality traits (boldness and energeticness) generated from a principal components analysis of the
measurements in the four contexts.
Measurement
Novel environment
context
Safe and familiar
context

Novel environment
Safe and familiar
Mirror-test
context
context
context
0.690
0.081
0.336
(0.54 – 0.80)
(-0.163 – 0.317)
(0.10 – 0.53)

Food and predator Energeticness*
present context
0.517
-0.303
(0.32 – 0.67)
(-0.51 - -0.07)

Boldness*
0.775
(0.66 – 0.86)

-0.106
(-0.34 – 0.14)

0.300
(0.06 – 0.50)

0.058
(-0.19 – 0.30)

0.194
(-0.05 – 0.42)

0.972
(0.96 – 0.98)

0.008
(-0.23 – 0.25)

Mirror-test context

0.334
(10 – 0.53)

0.241
(0 – 0.46)

0.598
(0.42 – 0.73)

0.555
(0.36 – 0.70)

0.136
(-0.11 – 0.37)

0.648
(0.48 – 0.77)

Food and predator
present context

0.571
(0.38 – 0.71)

0.107
(-0.14 – 0.34)

0.363
(0.13 – 0.56)

0.505
(0.30 – 0.67)

-0.198
(-0.42 – 0.05)

0.812
(0.71 – 0.88)

-0.305
(-0.051 - -0.07)

0.913
(0.86 – 0.95)

0.021
(-0.22 – 0.26)

0.159
(-0.09 – 0.39)

0.336
(0.10 – 0.53)

0.121
(-0.12 – 0.35)

0.689
(0.54 – 0.80)

0.315
(0.08 – 0.52)

0.750
(0.62 – 0.84)

0.803
(0.70 – 0.88)

0.008
(-0.23 – 0.25)

0.734
(0.60 – 0.83)

Energeticness*

Boldness*

Note: Coefficients between measurements across trial periods 1 and 2 within the same parameter are along the top-left to lower-right diagonal.
Coefficients between measurements taken in the first trial period are above the diagonal and those below the diagonal are from the second trial
period. Parameters denoted with an asterisk were obtained from a PCA of the four context specific parameters. Sample size = 65.

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Table 8: Contributions (loadings) of the four context-specific measurements in trial periods 1 and 2 to principal component axis 1 and 2.
Contribution of context specific personality traits to general personality traits
Behavior

Context for behavior

PC axis 1
(Boldness)
Trial 1
26.6%

PC axis 1
(Boldness)
Trial 2
35.6%

Length of time to
enter new habitat

Opportunity to move into
new environment

Amount of time
moving

PC axis 2
(Energeticness)
Trial 1
9.7%

PC axis 2
(Energeticness)
Trial 2
9.1%

Familiar and safe openfield environment

5.4%

0.8%

84.3%

88.7%

Bites and rams at
mirror

Mirror added to openfield environment

31.6%

24.7%

1.6%

0.02%

Length of time to
approach food

Model bird predator
strikes water above food

36.4%

39.0%

4.2%

2.2%

Note: PC axis 1 explains 49.7% of the variation in trial 1 and 46.2 % of the variation in trial 2. PC axis 2 explains 24.6% of the variation in trial 1
and 26.7% of the variation in trial 2.

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Figure 6. Plots a) and b) depict two possible outcomes for a test of the convergent validity of two measurements that may both be theorized to
measure boldness. Plot a) would support the theory that the two measurements quantify the same property while plot b) would suggest that
they do not. Plots c) and d) depict two possible outcomes for a test of the discriminant validity of two measurements that may be theorized to
measure two different personality traits. Plot c) would support the theory that the two measurements quantify two different traits while plot d)
would not.

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Evol. 27:452-461

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CHAPTER 3: The Consistency of Personality Traits Across a 4-Year Period in Largemouth Bass
(Micropterus Salmoides)

ABSTRACT
Most studies that have investigated the temporal consistency of personality traits have been
conducted in the laboratory, with very few studies conducted under natural or semi-natural conditions.
Consequently, little is known about the consistency of personality traits in nature and the potential for
natural selection to act on these traits. Here, I address this question by using a combination of
laboratory and field approaches to obtain estimates of consistency in personality over a 4-year period as
it develops naturally in a free ranging population of largemouth bass (Micropterus salmoides). In the
laboratory, behavior was assayed under four experimental conditions: a novel environment context, a
familiar environment context, a social context, and a feeding under predation risk context. These assays
were conducted on fish at 12, 15, 36, 48, and 60 months of age. Between testing periods, fish lived
freely in large outdoor ponds, where they were exposed to natural conditions of weather, food, social
interactions, and potential predators. The correlational structure between the behavioral
measurements indicated that there were context-specific personality traits underlying behavior in each
context and that the context-specific traits were likely sub-modules of a more general personality trait.
A principal components analysis conducted within each age on the context-specific traits revealed a
context-general trait that was interpreted as boldness. Each of the personality traits displayed temporal
consistency for a period of at least 24 months and the boldness trait was consistent across all four years
of testing. These results indicate that personality traits can be temporally consistent across a significant
portion of an individual’s life history and therefore subject to natural selection.

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INTRODUCTION
Individuals from the same population and at the same developmental stage often display
consistent differences in behavior over time and across contexts (Gosling 2001; Réale et al. 2007; Bell et
al. 2009). This consistent inter-individual variation in behavior is widely accepted as evidence of
phenotypes that underlie the expression of behavior (Araya-Ajoy and Dingemanse 2014; Budaev and
Brown 2013). Though a consensus is yet to be reached on what term best describes these phenotypes
(i.e. behavioral, personality, temperament), several studies have demonstrated that they affect various
components of fitness (Smith and Blumstein 2008; Kontiainen et al. 2009; Ariyomo and Watt 2012).
Further, there is mounting evidence that personality types have a heritable component (Chervet et al.
2011; Ariyomo et al. 2013; Kortet et al. 2014). These results indicate that personality variation within
populations may well be the adaptive outcome of natural selection. However, the potential for
personality to affect lifetime fitness and be a target of natural selection remains unknown, due in large
part to questions surrounding the temporal consistency of personality (Mittelbach et al. 2014).
Temporal consistency in personality is crucial for selection to act on personality types. If
personality types have narrow temporal windows of inter-individual consistency then even if the fitness
effects of personality types are large, temporal flip-flopping of personalities between individuals could
remove the opportunity for selection to act on personality. Conversely, if personality types are
temporally consistent between individuals across an entire lifetime, selection could easily take place
(Stamps and Groothuis 2010; Wolf and Weissing 2010). Numerous studies have documented
consistency in personality traits over relatively short time periods of days and weeks (Conrad et al.
2011). However, a meta-analysis that compared the average consistency observed in personality studies
conducted over a period of less than one year to those conducted over a period greater than one year
found that there was less consistency in periods over one year (Bell et al. 2009). Thus, lifetime
consistency cannot be safely inferred from evidence of short-term consistency (Boulton et al. 2014). As a

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result, there is a critical need for studies that describe the consistency of personality over long time
periods. The number of studies conducted over timeframes that may be considered more
representative of natural life spans is growing (Sinn et al. 2008; Chervet et al. 2011). However, nearly all
of these studies have been carried out in the laboratory and thus may not reflect the level of consistency
that exists in personality under natural conditions (Dingemanse et al 2002; Carere et al. 2005; Wilson
and Krause 2012). This is an important point as it is the temporal consistency of personality under
natural conditions that is relevant for the evolution of personality.
Investigating the temporal consistency of personality traits necessitates measuring the same
trait or traits repeatedly across development. Unfortunately, this task is complicated by the fact that it is
difficult to define and classify the personality traits that will be investigated a priori. This difficulty arises
because the structure and organization of personality traits (and how it may change across
development) is itself an open question (Carter et al. 2013; Garamszegi et al. 2013). For example, the
expression of behavior within a given context may be dictated by a personality trait that applies only to
the given context, by a personality trait that applies to contexts of some narrow category, or by a
personality trait that applies to contexts of some very general category (Figure 7). Further, personality
traits may exist at a combination of different levels, so that quasi-independent personality traits that
apply at one level are sub-modules of more general traits that exist at another level. Additionally, traits
that are defined a priori may not exist at all (or any) stages of development. For example, boldness is
frequently defined as the propensity to take risks. Under this definition, boldness would underlie the
expression of behavior in a range of contexts that involve risk (Figure 7A). However, it is quite possible
that a general boldness trait that underlies behavior in most risky contexts exists at only certain life
stages or does not exist at all. Instead, there may be more specific boldness traits that apply to certain
functional risky contexts (Figure 7C). Thus, an exploratory approach into the structure and temporal
consistency of personality traits is becoming widely accepted as an effective way to avoid difficulties

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that can arise from a priori classifying traits and identifying the behavioral expressions that they trigger
(Budeav 1997; Blumstein et al. 2012; Boulton et al. 2014).
Here, I address the question of temporal personality consistency by using a novel combination
of laboratory and field approaches to obtain accurate estimates of personality traits over a 4-year period
as it develops naturally in a free-living population of largemouth bass (Micropterus salmoides). I
examined individual behaviors in the laboratory at 12, 15, 36, 48, and 60 months of age in four contexts:
1) a novel environment, 2) a familiar and safe environment, 3) a social environment (mirror test), and 4)
an environment where both food and predation risk were present (Table 9). A previous study (Ballew
submitted) revealed that personality underlies largemouth bass behavior in these specific contexts.
Moderate to high correlations were found between measurements of behavior within the same
contexts that were repeated over short time periods and low to moderate correlations were found
between measurements of behaviors across most of the different contexts. This correlational pattern
between measurements of behavioral observations within versus across contexts indicates that contextspecific personality traits underlie behavior in these contexts and that these context-specific traits may
well be sub-modules of a more general trait akin to boldness. However, in the previous study, the
personality traits underlying behavior in these 4 contexts were only investigated at a single point in
time. As a result, the personality traits underlying behavior in each of these contexts at each stage of
development is unknown. Thus, in this study, I employ an exploratory approach to determine the
temporal consistency of the personality traits underlying behavior in these four contexts at each stage of
development.
In this study, I quantified behavior in four contexts over a four year period in a free-living
population of largemouth bass (Micropterus salmoides) to address three main questions. 1) Which
personality trait or traits underlie behavior in each of the four contexts investigated at each stage of
development? 2) What level of temporal consistency (in both magnitude and temporal duration) exists

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in each personality trait? 3) Is the temporal consistency in each of the personality traits dependent on
the temporal duration between measurements? Answers to these questions, especially in populations
exposed to natural conditions, will help address whether personality traits can be temporally consistent
across a significant portion of an individual’s life history and therefore subject to natural selection.

METHODS
Study species and husbandry
Three hundred yearling bass were collected in 2009 from a pond located at the Kellogg
Biological Station experimental pond facility in southwest Michigan. These bass were bred on site from
adult bass collected from nearby Wintergreen Lake. The yearling bass were transferred to the laboratory
facility and were individually marked with colored elastomer gel (a biocompatible pliable polymer;
Northwest Marine Technology, Goldsmith et al. 2003) that was injected subcutaneously at two of seven
possible locations. Random samples from the 300 marked bass were subjected to a behavioral assay
procedure over the course of their development. Bass were behaviorally assayed at approximately 12,
15, 36, 48, and 60 months of age, resulting in the following time intervals between measurements: 3
months, 1 year, 2 years, 3 years, and 4 years. Between assay periods, the bass were kept in an outdoor
pond (30 m dia; 2 m deep) at the Kellogg Biological Station, where they were free-living, could feed on
natural prey, and undergo normal developmental processes. Largemouth bass develop from vulnerable
prey as juveniles to reproductively mature adults at age 3 that exhibit complex breeding behaviors and
show extensive parental care. In most habitats (as in the case of this study population), bass assume the
role of apex predator soon after reaching maturity.
Leading up to each round of behavioral assays, bass were transported to the laboratory area
and kept in large (1000 liter) outdoor covered tanks. During this time, bass could feed on zooplankton
(Daphnia) ad libitum. Bass were transferred to the laboratory the day before they were tested. In the

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laboratory, each bass was identified based on its marks and measured for length. If the marks were no
longer visible, bass were re-marked with a new unique combination of colors and locations not
previously used in the population. Bass were socially housed in 110 L aquaria (four bass per aquarium)
and provided with an excess amount of zooplankton. On the testing day, bass were transferred from the
indoor holding aquaria into their own aquaria where they underwent a series of behavioral assays (Table
9). Upon completion of the assay procedure, the bass were returned to the pond until the next assay
period, then they were re-collected to undergo another round of tests.
Over the 4-year testing period, I repeatedly observed bass behaviors in the laboratory under
four experimental contexts: 1) a novel environment, 2) a familiar and safe environment, 3) a social
environment (mirror-test), and 4) an environment where food and predators were present. Three of
these environmental contexts (numbers 2, 3, and 4) were included in each assay testing period, whereas
the novel environment (number 1) was not employed in the first two rounds of behavioral assays
(conducted at 12 and 15 months of age). An additional alteration to the assay procedure was that
different sized aquaria were used to observe behavior as the bass grew (40 liter aquaria when the bass
where yearlings and 110 liter aquaria once the bass had reached an age of 36 months).

Behavioral assay procedure
The testing aquaria were divided into two sections by an opaque vertical partition with the
smaller section making up about 10% of the total volume. Individual bass were transferred into the
smaller section of a testing tank and then left for approximately 45 minutes to recover from handling
and to acclimate to the new environment. After the 45 minute acclimation period, novel context trials
were initiated. The partition was raised approximately 10 centimeters above the floor of the aquarium
using a pulley system, allowing the fish to swim from the smaller section into the larger section. For each
trial, I measured the elapsed time from when the partition was raised until the fish swam into the larger

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area of the tank (up to 45 minutes). If after 45 minutes a fish had not moved to the larger section of the
tank, I gently coaxed it out. Once a fish moved into the larger section of the tank, I lowered the partition
so that it could not move back into the smaller section. An individual’s score was calculated by
subtracting the number of seconds that it waited before moving to the larger portion of the tank from
2700 (the maximum trial length). Thus, individuals with higher scores moved more quickly to the larger
section of the tank. Individuals that did not leave the small section during the trial received a score of 0.
Following the completion of the novelty trial, I placed a mirror on the wall in the smaller section of the
tank (not visible to the fish). Fish were then left overnight in the larger section of the tank to acclimate
to their new surroundings. The yearling fish were not subjected to the novel environment trial. Instead
of placing them in the smaller section of the tank, yearling bass were simply placed in the larger section
of the tank and left overnight to acclimate to their new surroundings.
The day after introducing a bass into a testing aquarium, I assayed its behavior in a familiar and
safe context. I measured the amount of time the bass spent moving around the tank in the familiar
environment (larger section of the tank). Fish were observed for 5 minutes and I summed the total time
spent swimming (moving) to calculate the total number of seconds active per trial.
Immediately following the measurements taken in the familiar and safe environment trial, I
conducted the social context (mirror-test) trial. I raised the partition to reveal a mirror on the wall in the
smaller section of the tank. Once the partition was raised the trial commenced. Trials lasted for 10
minutes. I measured the number of bites, tail swipes, and rams at the mirror. At the end of the trial, the
partition was lowered so that the mirror was no longer viewable. As the partition was lowered, fish in
the path of the partition consistently retreated to the larger section of the tank. The number of bites,
tail swipes, and rams were summed together to get an overall measure in this context. These behaviors
were summed together because each was taken to be a specific form of agonistic behavior and other
studies have shown that individuals often exhibit behavioral specificity so that they tend to primarily use

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their preferred method of a behavioral type (one individual may primarily use rams while another
primarily uses bites; Uher 2011).
Approximately one hour after observing behavior in the presence of the mirror, the feeding in
the presence of a predator trial was conducted. A live earthworm tied to monofilament fishing line (no
hook) was lowered into the tank near one end. When the bass approached the worm, a model bird
suspended on a string and pulley system positioned directly above the worm was released to strike the
surface of the water, simulating a predation attempt. The bird was then quickly lifted from the water,
again using the string and pulley system. During this time, the fish most often retreated to a corner of
the tank. Once the bird was appropriately positioned (10 centimeters above the water surface), the trial
commenced. I recorded how many seconds it took the bass to re-approach the worm. An individual’s
score was calculated by subtracting the number of seconds that a fish waited before re-approaching the
worm from the maximum trial length. Thus, individuals with higher scores re-approached the worm
faster. Individuals that did not re-approach the worm during the trial received a score of 0. The
maximum trial length was extended from 600 seconds in assays with yearlings to 1800 seconds with
bass 36 months of age and older. This was done in an attempt to reduce the number of non-responders
so that the total behavioral variation could be more fully represented.

Statistical analysis
All statistical analyses were conducted using R version 2.13 (R Development Core Team 2008).
All scores were standardized (mean of 0 and standard deviation of 1) to control for context effects of the
measures (slight differences between rounds of assays in the same trial type, major differences between
trials of different types, habituation resulting in changes to how an individual perceives an environment,
etc.). After removing context effects, the measures represent the traits responsible for producing
behavior (in addition to any error). Standardizing the measurements also removes differences across

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assays conducted at different ages that may be due to stereotypical developmental changes. For
example, yearling bass tended to approach food with a predator present more quickly than older bass.
This observed difference was potentially a developmental one and not due to context effects (Groothuis
and Trillmich 2011). However, measurement standardization does not impact investigations into interindividual consistency across temporal intervals, which is the interest of the current study.
Previous studies on this population of largemouth bass indicate that context-specific traits may
underlie the expression of behavior in each of these contexts during at least some stages of
development (Ballew submitted). Further, these context-specific personality traits may be sub-modules
of a context-general trait akin to boldness. I investigated the correlational structure between behavioral
measures within each age to determine which personality traits were present at each age (question 1).
To do so, I calculated intra-class correlation coefficients, which partition variation into within and
between individual components. The higher the correlation, the greater the proportion of variation that
is due to inter-individual differences. Further, I conducted a principal component analysis on the
context-specific traits at each age to identify context-general traits. As the novel environment measure
was not conducted during every run, it was excluded from the principal component analysis conducted
at each age.
To investigate the temporal consistency within each personality trait, I calculated Pearson
correlation coefficients across several different time intervals (question 2). There were a total of seven
time intervals; 3 months (sample size = 122), 12 months (from 36 to 48 months old; sample size = 93), 12
months (from 48 to 60 months old; sample size = 71), 24 months (from 12 to 36 months old; sample size
= 52), 24 months (from 36 to 60 months old; sample size = 71), 36 months (from 12 to 48 months old;
sample size = 52), and 48 months (from 12 to 60 months old; sample size = 39). To investigate the effect
of interval duration on the temporal consistency of the personality traits (question 3), I performed
regressions of personality trait temporal consistency (log-transformed) as a function of the time

92

between measurements. Values of temporal consistency were weighted by the sample size from each
interval (e.g. N = 122 for the 3 month interval and N = 39 for the 48 month interval).

RESULTS
I examined the magnitude and 95% confidence intervals of the intra-class correlation
coefficients (ICCs) within each time period (fish age) and found that ICCs were significant between
several of the context-specific measures within each age, with magnitudes usually falling between 0.25
and 0.5 (Table 10; comparison of correlations within each column). A principal component analysis of
the measures conducted within each age revealed a similar pattern in the relationships between the
context-specific measures (Table 11; within each column). Based on the loadings of the measurements
from the three experimental contexts used in the principal components analysis, PC axis 1, which
explained between 40% - 55% of the variation within each age, was interpreted as a measure of
“boldness”. Thus, taken together, with the exception of the measurement in the safe and familiar
context, it appears that context-specific traits underlie behavior in each of these contexts at each age
and that they are sub-modules of a general boldness trait (Figure 8).
The structure of the context-specific and context-general personality traits were fairly consistent
across ages. For example, all five of the comparisons between the mirror-test context and the predator
and food present context yielded ICCs between 0.26 and 0.36 (Table 10; bottom row). In addition, the
mirror-test context measurement and the food and predator present context measurement were
consistently highly correlated with PC axis 1 (Table 11; correlation coefficients were all between 0.65
and 0.83). Interestingly, the safe and familiar context measurement had more variability in its
relationship with the boldness component (PC axis 1). In the two runs with yearlings, the safe and
familiar context measurement was weakly correlated with boldness (0.01 and 0.46), whereas in all trials

93

with adults (age 36 months and above), it was moderately to highly correlated with boldness (0.52 –
0.73).
Pearson correlation coefficients were calculated to assess the consistency of each personality
trait across a range of time intervals from 12 to 48 months (Table 12). Pearson correlation coefficients
ranged from 0.27 – 0.53 for each of the three time intervals investigated for the novel context
personality trait (Table 12). Correlation coefficients ranged from 0.08 – 0.51 for each of the seven time
intervals investigated for the mirror-test context personality trait, and from 0.15 – 0.61 for each of the
seven time intervals investigated for the food and predator present context personality trait (Table 12).
The boldness personality trait (PC axis 1) had the highest magnitude and most consistent correlation
coefficients through time. Correlation coefficients for boldness ranged from 0.26 – 0.68 for each of the
seven time intervals and were significantly different from zero in all time intervals except 48 months,
which had a sample size of only 39 fish (Table 12). Correlation coefficients ranged from 0.07 – 0.42 for
each of the seven time intervals investigated for the safe and familiar context measurement.
Regressions (weighted by sample size for each interval) of personality trait temporal consistency
(log-transformed) as a function of the time between measurements were run for the personality traits
to investigate the effect of the temporal interval between measures on trait consistency (Table 13). A
regression was not conducted with the context-specific trait observed in the novel environment as it
was missing several data points. Similarly, a regression was not performed on the measurement in the
safe and familiar context as previous analyses suggested that the trait underlying behavior in this
context may have changed across development. In general, the consistency observed in the personality
traits decreased with an increasing time interval between measures (Figure 9). However, the temporal
decline in consistency was significant only for the mirror-test context personality trait. Boldness (PC axis
1), showed relatively little change in the strength of the correlation between the intervals from 3
months to four years (Figure 9C).

94

DISCUSSION
The results of this study show that context-specific personality traits typically underlie behavior
in each context and that the context-specific traits are sub-modules of a general personality trait akin to
boldness. Moreover, the results show that moderate levels of consistency are maintained over several
years in most of the personality traits. With regard to whether or not the consistency of personality
decreases over long time intervals, the results of this study are mixed. The consistency of personality
decreased significantly over longer time periods for some traits but not others. Taken together, these
results show that personality traits are sufficiently consistent across time to be molded by natural
selection. To my knowledge, the current study represents the longest testing period (4 years) of any free
ranging, non-primate species. Further, the current study provides a comprehensive investigation into
the temporal consistency of several context-specific personality traits, as well as a more general trait
(akin to boldness) that underlies the context-specific traits.
With the exception of the measurement in the safe and familiar context, it appears that contextspecific traits underlie behavior in each of the investigated contexts at each age and that they are submodules of a general boldness trait (Figure 8). Temporal consistency in the relationships between the
context-specific personality traits across developmental stages provides further support for this idea. In
regards to the measurement in the safe and familiar, a less clear pattern emerged. The relationships
between the measurement in the safe and familiar context and each of the other three context-specific
traits varied considerably across ages. This may have been due to slight differences in the methodology
across runs of the behavioral assays (e.g. there was a fourth context added at the adult stage and the
tank size was increased). Alternatively, the fact that the measurement in the safe and familiar context
became more highly correlated with the other context-specific traits as the bass became older may
indicate that the bass perceived the safe and familiar context differently as they aged. Specifically, it

95

appears that while the context itself was safe and familiar, bass may have instead perceived it as risky as
they grew older and, as a result, the personality trait underlying the expression of behavior in this
context may have changed accordingly. This idea is further supported by the results of the principal
components analysis conducted at each age. The change in the correlation between component 1 from
the PCA (interpreted as boldness) and the measure in the safe and familiar context from the juvenile to
the adult stage indicates that the context may have been perceived as risky by adults but not juveniles.
To address the magnitude of consistency maintained across time in each of the personality
traits, I calculated Pearson correlation coefficients across time periods ranging from 3 months to 4 years.
The novel context personality trait demonstrated temporal consistency over the 24 month testing
period that it was observed and the mirror-test context personality trait also demonstrated consistency
up to a 24 month period. The trait observed in the food and predator present context and the boldness
personality trait both demonstrated significant consistency across a 36 month period that crossed from
the juvenile to the adult stage. In terms of the magnitude of consistency, the personality traits tended to
have low to moderate levels of consistency. This result is in line with other studies that have
investigated personality consistency (Bell and Stamps 2004; Sinn et al. 2008). However, it is important to
take the precision of personality trait measurements into consideration when interpreting these results
(Burns 2008).
If measures of personality were precise, one would expect to observe intra-class correlation
coefficients very close to 1 over very short intervals. I investigated the precision of each of these
personality measures over very short intervals and obtained an intra-class correlation coefficient of 0.69
for the novel context personality trait, 0.30 for the safe and familiar context trait, 0.60 for the mirrortest trait, 0.51 for the food and predator context trait, and 0.61 for boldness (Ballew submitted). These
relatively low levels of precision aren’t surprising given that behavioral measures are used as proxies to
quantify personality. Low levels of precision such as this are likely to bias personality consistency

96

estimates downwards. For example, even if boldness was perfectly consistent over the 48 month testing
period, the amount of imprecision in its measurement would make it unlikely to observe levels of
consistency above 0.6. Thus, the estimates for personality consistency presented in this study should be
considered conservative estimates because each measure is lacking in precision (especially the safe and
familiar context measure).
I conducted logarithmic regressions (weighted by sample size) to determine if the temporal
consistency in each of the personality traits is dependent on the temporal duration between
measurements. Except for the mirror-test context personality trait, the magnitude of consistency in the
personality traits did not significantly decrease over longer time intervals. One explanation for this result
is that the sample size (7 for most traits) was too low to comprehensively assess the effect of time on
personality trait consistency. This result is supported by the relatively high R2 values for the effect of
time on the food and predator present context-specific trait (0.40) and the mirror-test context-specific
trait (0.59). However, the R2 value for the boldness trait was only 0.11. This could potentially indicate
that general personality traits such as boldness are more consistent than context-specific traits over long
time periods. To thoroughly address this hypotheses, much more data is needed than this study can
provide.
If personality has evolved, there are both evolutionary and ecological consequences that must
be considered (Wolf and Weissing 2012; Mittelbach et al. 2014). Answers must be sought to explain the
maintenance of adaptive personality differences within populations (Dingemanse and Wolf 2010; Wolf
and McNamara 2012). Additionally, the effects of personality on populations, communities and even
ecosystems must be addressed (Mittelbach et al. 2014). However, before moving on to these larger
issues, it is critical to comprehensively address the potential for selection to act on personality traits and
cause evolution, which is dependent, in part, on the consistency of personality. Very few studies have
investigated the issue of personality trait consistency over long time periods and none of these have

97

been conducted under situations where personality could develop naturally. To my knowledge, the
current study is the first to provide such information and it does so by presenting a comprehensive view
of personality. When all results are taken together, they support the notion that personality traits are
consistent enough across time to allow selection to take place. However, it is important to note that
these results come from a single population with a given evolutionary background that has experienced
a given set of environmental conditions. It is difficult to say how personality consistency may be
impacted in populations that experience different conditions or unstable conditions (e.g. different or
changing predator regimes) over a lifetime. Additionally, different species may exhibit different levels of
consistency. Thus, it is of paramount importance to continue to document the temporal consistency of
personality traits in other species under various environmental scenarios over biologically relevant
durations.

ACKNOWLEDGEMENTS
I thank Gary Mittelbach and Mary Tate Bremigan for their many insightful comments and suggestions on
earlier versions of this manuscript. Additionally, I thank Cristopher Mirque and Matthew Bach for the
help during parts of the data collection process. Grants from the US National Science Foundation (IOS1311455), Sigma Xi, Kellogg Biological Station, and the Zoology Department at Michigan State University
supported portions of this research.

98

APPENDIX

99

Table 9. Behaviors measured in the four behavioral assays, the context for each assay, and the ages in which the assays were conducted.
Behavior
Context
Age observations were made (months)
Length of time to enter new habitat
Opportunity to move into novel environment
36, 48, 60
Amount of time moving

Familiar and safe open-field environment

12, 15, 36, 48, 60

Bites and rams at mirror

Mirror added to open-field environment

12, 15, 36, 48, 60

Length of time to approach food

Model bird predator strikes water above food

12, 15, 36, 48, 60

100

Table 10. Correlations between context-specific personality traits within each age. Values are intra-class correlation coefficients (95% confidence
intervals in parenthesis) of the standardized measurements.
Contexts
Age: 12 months
Age: 15 months
Age: 36 months
Age: 48 months
Age: 60 months
NEC and SFC
NA
NA
0.039
0.275
0.243
(-0.16, 0.23)
(0.07, 0.45)
(0.01, 0.45)
NEC and MTC

NA

NA

0.380
(0.20, 0.54)

0.183
(-0.02, 0.37)

0.297
(0.07, 0.49)

NEC and FPC

NA

NA

0.300
(0.11, 0.467)

0.392
(0.21, 0.55)

0.377
(0.16, 0.56)

SFC and MTC

0.004
( -0.17, 0.18)

-0.019
(-0.20, 0.16)

0.087
(-0.11, 0.28)

0.289
(0.09, 0.46)

0.348
(0.13, 0.54)

SFC and FPC

0.007
(-0.17, 0.18)

0.204
(0.03, 0.37)

0.201
( 0.01, 0.38)

0.311
(0.12, 0.48)

0.279
(0.05, 0.48)

MTC and FPC

0.259
(0.09, 0.42)

0.273
(0.10, 0.43)

0.356
(0.17, 0.52)

0.357
(0.17, 0.52)

0.329
(0.11, 0.52)

Note: NEC = Novel environmental context. SFC = Safe and familiar context. MTC = Mirror-test context. FPC = Food and predator present context.
Sample sizes; 12 months = 122, 15 months = 122, 36 months = 101, 48 months = 93, 60 months = 71.

101

Table 11. Principal components analysis of 3 context-specific traits (safe and familiar context, social context (mirror-test), and predator and food
present context) at 12, 15, 36, 48, and 60 months of age. Only the loadings (first column for each age) and correlations (second column for each
age) for axis 1 are shown.
Loadings (first column) and correlations (second column) to axis 1 at each age
Behavior
Amount of time
moving

Context for behavior
Familiar and safe openfield environment

12 months
0.01
0.01

15 months
16.24
0.46

36 months
26.93
0.62

48 months
30.54
0.71

60 months
32.71
0.73

Bites and rams at
mirror

Mirror added to openfield environment

49.99

0.79

32.15

0.65

31.14

0.67

33.98

0.74

36.07

0.77

Length of time to
approach food

Model bird predator
strikes water above food

50.00

0.79

51.61

0.83

41.92

0.78

35.48

0.76

31.22

0.71

Note: Axis 1 explained 41.8% of the variation at 12 months, 44.1% of the variation at 15 months, 48.1% of the variation at 36 months, 54.3% of
the variation at 48 months, and 54.2% of the variation at 60 months.

102

Table 12. Temporal consistency within each personality trait across varying time intervals and at different ages. Values are Pearson correlation
coefficients (95% confidence intervals in parenthesis).
Interval between
Sample
NEC
SFC
MTC
FPC
Boldness*
measurements
size
Interval = 3 months
(12 – 15 months old)

122

NA

0.095
(-0.09, 0.27)

0.328
(0.16, 0.48)

0.372
(0.21, 0.52)

0.328
(0.16, 0.48)

Interval = 12 months
(36 – 48 months old)

93

0.269
(0.07, 0.45)

0.21
(0.01, 0.40)

0.334
(0.14, 0.50)

0.338
(0.14, 0.51)

0.43
(0.25, 0.59)

Interval = 12 months
(48 – 60 months old)

71

0.525
(0.33, 0.68)

0.422
(0.21, 0.60)

0.511
(0.32, 0.67)

0.610
(0.44, 0.74)

0.68
(0.52, 0.78)

Interval = 24 months
(36 – 60 months old)

71

0.367
(0.15, 0.55)

0.068
(-0.17, 0.30)

0.369
(0.15, 0.56)

0.419
(0.21, 0.59)

0.37
(0.15, 0.55)

Interval = 24 months
(12 – 36 months old)

52

NA

0.093
(-0.19, 0.36)

0.250
(-0.03, 0.49)

0.311
(0.04, 0.54)

0.32
(0.05, 0.54)

Interval = 36 months
(12 – 48 months old)

52

NA

0.314
(0.05, 0.54)

0.194
(-0.08, 0.44)

0.295
(0.02, 0.53)

0.36
(0.09, 0.57)

Interval = 48 months
(12 – 60 months old)

39

NA

0.074
(-0.25, 0.38)

0.076
(-0.25, 0.38)

0.150
(-0.17, 0.44)

0.26
(-0.07, 0.53)

Note: NEC = Novel environmental context. SFC = Safe and familiar context. MTC = Mirror-test context. FPC = Food and predator present context.
*Boldness represents axis one from a principal components analysis performed on the SFC, MTC, and FPC measurements from each age.

103

Table 13. Regressions of personality trait temporal consistency (log-transformed) as a function of the time between measurements. Values were
weighted by the sample size from each interval (e.g. N = 122 for the 3 month interval and N = 39 for the 48 month interval). Log (y) = intercept +
slope(x).

Personality Trait

DoF

Intercept
Coefficient

Intercept
P. value

Slope
Coefficient

Slope
P. value

R-squared

Trait exhibited in mirror-test
context

5

-0.751

0.016

-0.025

0.045

0.586

Trait exhibited with food and a
predator in environment

5

-0.743

0.010

-0.015

0.126

0.402

Boldness

5

-0.825

0.007

-0.007

0.460

0.113

104

Figure 7. Four hierarchical models illustrating alternative hypotheses for the organization and structure of personality traits. Model (a) proposes
a scenario where a general boldness trait underlies the expression of behavior in each context. Thus, repeated observations of inter-individual
differences in behavior would yield roughly the same correlations between any two behaviors observed, regardless of whether the observations
were made in the same or different contexts. Model (b) proposes a scenario where context-specific personality traits underlie the expression of
behavior in each context. These context-specific traits are all sub-modules of the same general boldness trait. Thus, repeated observations of
behavior in these contexts would all yield positive correlations. However, repeated observations from within contexts would yield higher
correlations than those between contexts. Model (c) proposes a scenario where semi-general personality traits underlie the expression of
behavior within functionally similar contexts (e.g. foraging and novelty). Thus, repeated observations of behavior would yield equivalent
correlations regardless of whether the observations were made in the same or different contexts, as long as the contexts where functionally
similar (e.g. involved novelty). Behaviors expressed in functionally different contexts (e.g. novelty and feeding) would not be correlated. Model
(d) proposes a scenario where context-specific traits underlie behavior in each context and each of these context-specific traits are also submodules of semi-general traits that underlie behavior in functionally similar contexts (e.g. foraging and novelty). The semi-general traits are
themselves sub-modules of a general boldness trait. Under this scenario, repeated observations of inter-individual differences in behavior from
within specific contexts would yield the highest correlations, inter-individual differences in behavior from within functionally similar contexts
would yield the next highest, and inter-individual differences in behavior across functionally similar contexts would the lowest (but still
significant) correlations.
105

Figure 8. Model illustrating the organization and structure of personality traits based on the results of this study. A context-specific personality
trait influenced behavior across all ages of development that were investigated in the novel environment context, in the foraging in the presence
of an aerial predator context, and in the mirror-test context. A boldness personality trait generalized beyond specific functional contexts was
found to underlie each of these context-specific traits. A personality trait also influenced adult (but not juvenile) behavior in the safe and familiar
environment. This personality trait may have been a context-specific trait (indicated by the dashed line between behavior and the unidentified
trait) or may have been the general boldness trait (indicated by a dashed line between boldness and the unidentified trait).

106

Figure 9. Regressions of personality trait temporal consistency (log-transformed) as a function of the
time between measurements in the: a) mirror-test context-specific personality trait, b) food and
predation threat context-specific personality trait, and c) boldness trait. Values were weighted by the
sample size from each interval (e.g. N = 122 for the 3 month interval and N = 39 for the 48 month
interval). Log (y) = intercept + slope(x). Solid black regression lines are statistically significant while
dashed grey lines are not.

107

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111

CHAPTER 4: Fitness Tradeoffs Across Development Can Contribute to the Maintenance of Adaptive
Personality Differences

ABSTRACT
The maintenance of inter-individual differences in animal personality is often attributed to
fitness tradeoffs between phenotypes across spatially or temporally heterogeneous environments. Few
studies, however, have examined the potential for fitness tradeoffs across life stages to maintain
different animal personality types. Here, we address the fitness consequences of multiple personality
traits across life stages and their heritability in largemouth bass (Micropterus salmoides). We show that
context-specific personality traits underlie the expression of behavior in: 1) a novel environment, 2) a
familiar and safe environment, 3) a social environment (mirror-test), and 4) an environment in which
both food and predators were present. Further, we show that each of the context-specific traits are submodules of a context-general trait identified as boldness (from principal components analysis). Juvenile
bass that scored higher in the novel environment context, that were more willing to forage in the
predation risk context, and bass that were bolder in general all had significantly lower survivorship than
their conspecifics. In contrast, adult bass that were larger and had higher boldness scores had
significantly higher reproductive success, as did bass that were more active in the familiar environment.
Lastly, the general trait of boldness, but not any of the context-specific personality traits, was heritable
at nearly a statistically significant level. The results of this study demonstrate for the first time that
individual personality traits can affect fitness in multiple ways over the course of an individual’s lifetime.
In this case, boldness decreased survival in juveniles but increased reproductive success in adults. A
previous study with this population of largemouth bass indicated that boldness is consistent across
multiple years and developmental stages. Thus, the fitness tradeoffs across juvenile survival and
reproductive success can contribute to the maintenance of adaptive personality differences in boldness.

112

INTRODUCTION
Studies examining selection and fitness differences between phenotypes are essential for our
understanding of evolutionary processes (Pigliucci and Kaplan 2000). Although many studies have
examined fitness effects of morphological and life-history traits, studies of selection on personality traits
are much less common (Kingsolver et al. 2001; Smith and Blumstein 2008). This paucity in studies has
been due, in part, to the fact that personality is not easily characterized into phenotypes that signify 1) a
set of inter-related mechanisms that are involved in a character’s expression, and 2) a functional
significance (Aray-Ajoy and Dingemanse 2014). In addition, personality has historically been viewed as
highly plastic and therefore less likely to be under the direct influence of selection (West-Eberhard
1989). However, recent methodological advances have made it possible to apply the traditional
phenotypic framework to personality (Dall and Griffith 2014; Ballew in review). Further, two separate
meta-analyses have shown that personality can be consistent over biologically meaningful time periods
(Bell et al. 2009; Garamszegi et al. 2013; see also Ballew submitted). Thus, studies to explain how
personality is generated and maintained by evolution are not only appropriate, they are very much
needed (Sih et al. 2004; Réale et al. 2007; Dingemanse & Wolf 2010).
Personality traits have the potential to affect fitness at nearly every stage of development, from
a juvenile’s chances of surviving to adulthood to an adult’s reproductive success (Mitellbach et al. 2014).
If personality is consistent across life stages, personality traits may result in fitness tradeoffs across life
stages or possibly between different components of selection (e.g. sexual and viability). Moreover, if
personality traits are heritable, as has been found in several studies, the fitness consequences of animal
personalities could extend across generations (Bell 2005; Brown et al. 2007; Dingemanse et al. 2009;
Chervet et al. 2011). Under such circumstances, fitness tradeoffs could be a potentially powerful
mechanism for the maintenance of adaptive variation in personality traits. However, to date, studies
that have investigated the relationship between personality traits and fitness have generally focused on

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a single measure of fitness (such as survival) at a specific life stage (Dingemanse and Réale 2005; Smith
and Blumstein 2008). Here, we address the fitness consequences of multiple personality traits across life
stages and their heritability in largemouth bass (Micropterus salmoides).
To quantify personality, bass were observed in the laboratory under four experimental
behavioral contexts: 1) a novel environment, 2) a familiar and safe environment, 3) a social environment
(mirror-test), and 4) an environment in which both food and predators were present. Previous studies
on this population of largemouth bass indicate that context-specific personality traits underlie the
expression of behavior in each of these contexts and that the context-specific traits are sub-modules of
a context-general trait identified as boldness (Figure 10) (Ballew in review). Further, the boldness trait,
as well as some of the context-specific traits, are consistent across multiple years and life stages (Ballew
submitted). To quantify the fitness effects of these personality traits across life stages (and different
components of selection), field experiments were conducted on juvenile survivorship and on adult
reproductive success. Further, personality was assayed in two generations of bass to assess personality
heritability.
In nature, largemouth bass develop from small juveniles that are very vulnerable to piscivorous
predators, into large adults that are apex predators in their own right. During the early spring,
reproductively mature male bass build nests (shallow depressions in the substrate) in the near-shore
areas of lakes (Heidigner 1975; Philipp et al. 1997). Females are courted by nest-guarding males and lay
their eggs in one or more nests, which are then fertilized by nest-guarding males (or by cuckolding
males). Nesting males then provide sole parental care by guarding nests from potential egg and larval
predators (Ridgway 1988; Philipp et al. 1997). Male bass guard their offspring for 2 weeks or more after
the offspring leave the nest and begin exogenous feeding as a tightly organized school of fry. Thus, bass
have a complex life-history that provides ample opportunities for personality to affect fitness. For
example, boldness could positively affect fitness at the juvenile stage through higher feeding

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rates/energy gains, which could allow juveniles to outgrow predation threats. Boldness also could
positively affect fitness at the adult stage if bolder males have an advantage in intra-sexual competitive
encounters and if bolder bass display more intense courting behaviors. However, boldness could
negatively affect fitness at the juvenile stage if it increases vulnerability to predators. Further, boldness
could negatively affect total reproductive output if bolder bass have shorter lifespans and thus have
fewer reproductive opportunities. Environmental factors such as predator density, refuge availability,
and adult population density likely play a role in determining the effects that boldness has on fitness at
each stage of development. Thus, depending on the environment, the fitness effects of boldness could
compound and make boldness very beneficial, very detrimental, or selectively neutral. We investigated
the fitness effects of personality on juvenile survivorship in two outdoor pond treatments that varied in
refuge availability and its fitness effects on reproductive success in a single treatment that spanned
multiple reproductive seasons.

METHODS
Study population and husbandry
The largemouth bass used in each experiment described below were collected from ponds
located at the Kellogg Biological Station experimental pond facility in southwest Michigan. These bass
were bred on site from adult bass collected from nearby Wintergreen Lake. Bass were transferred to the
laboratory facility and were individually marked with colored elastomer gel (a biocompatible pliable
polymer; Northwest Marine Technology, Goldsmith et al. 2003) that was injected subcutaneously at two
of seven possible locations. The bass were socially housed in aquaria (4 bass per aquarium) and provided
with an excess amount of zooplankton. Bass were measured for length and a tissue sample was taken
for DNA analysis. Bass were then transferred from the holding aquariums into their own testing aquaria
to undergo a series of behavioral assays.

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In the spring of 2011, 101 mature, age-3 bass were run through the behavioral assay procedure
just prior to the reproductive season. All surviving adults were re-assayed in the spring at age-4 (n=93)
and age-5 (n=71). 240 offspring produced from the age-4 bass were collected and they too were run
through the behavioral assay procedure. The 240 offspring were used in an experiment to determine the
effect of personality on juvenile survivorship. Adult bass were used in an experiment to determine the
effect of personality on reproductive success. Further, the adult behavioral assay scores and a subset of
the offspring scores were used to determine the heritability of each personality trait. The details of the
behavioral assay procedure and experiments are provided below.

Behavioral assay procedure
Behavioral assays followed a similar procedure as outlined in previous studies with this
population of largemouth bass (Ballew in review). The testing aquaria were divided into two sections by
an opaque vertical partition with the smaller section making up about 10% of the total volume.
Individual bass were transferred into the smaller section of a testing tank and then left for
approximately 45 minutes to recover from handling and to acclimate to the new environment. After the
45 minute acclimation period, novel context trials were initiated. The partition was raised approximately
10 centimeters above the floor of the aquarium using a pulley system, allowing the fish to swim from
the smaller section into the larger section. For each sample, we measured the elapsed time from when
the partition was raised until the fish swam into the larger area of the tank. Once a fish moved into the
larger section of the tank, we lowered the partition so that it could not move back into the smaller
section. An individual’s score was calculated by subtracting the number of seconds that it waited before
moving to the larger portion of the tank from 2700 (the maximum trial length). Thus, individuals with
higher scores moved more quickly to the larger section of the tank. Individuals that did not leave the
small section during the trial received a score of 0. Following the completion of the novelty trial, we

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placed a mirror on the wall in the smaller section of the tank (not visible to the fish). Fish were then left
overnight in the larger section of the tank to acclimate to their new surroundings.
The day after introducing a bass into a testing aquarium, we assayed its behavior in a familiar
and safe context. We measured the amount of time the bass spent moving around the tank in the
familiar environment (larger section of the tank). Fish were observed for 5 minutes and we summed the
total time spent swimming (moving) to calculate the total number of seconds active per trial.
Immediately following the measurements taken in the familiar and safe environment trial, we
conducted the social context (mirror-test) trial. We raised the partition to reveal a mirror on the wall in
the smaller section of the tank. Once the partition was raised the trial commenced. Trials lasted for 10
minutes. We measured the number of bites, tail swipes, and rams at the mirror. At the end of the trial,
the partition was lowered so that the mirror was no longer viewable. The number of bites, tail swipes,
and rams were summed together to get an overall measure in this context. These behaviors were
summed together because each was taken to be a specific form of agonistic behavior and other studies
have shown that individuals often exhibit behavioral specificity so that they tend to primarily use their
preferred method of a behavioral type (one individual may primarily use rams while another primarily
uses bites; Uher 2011).
Approximately one hour after observing behavior in the presence of the mirror, the feeding in
the presence of a predator trial was conducted. A live earthworm tied to monofilament fishing line (no
hook) was lowered into the tank near one end. When the bass approached the worm, a model bird
suspended on a string and pulley system positioned directly above the worm was released to strike the
surface of the water, simulating a predation attempt. The bird was then quickly lifted from the water,
again using the string and pulley system. During this time, the fish most often retreated to a corner of
the tank. Once the bird was appropriately positioned (10 centimeters above the water surface), the trial
commenced. We recorded how many seconds it took the bass to re-approach the worm. An individual’s

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score was calculated by subtracting the number of seconds that a fish waited before re-approaching the
worm from the maximum trial length. Thus, individuals with higher scores re-approached the worm
faster. Individuals that did not re-approach the worm during the trial received a score of 0.

Experiments
Experiment 1: Juvenile survivorship
In the late summer of 2012, 240 young-of-year bass were individually marked, measured for
size, assayed in the behavioral trials, and then randomly distributed between two experimental ponds
(120 bass per pond). Each pond was approximately 30m in diameter and 2m deep. One pond was about
20 years old, contained well-developed aquatic vegetation, and a productive invertebrate community.
The other pond was newer (renovated 2 years prior to experiment), was mostly free of aquatic
vegetation, and had a less productive invertebrate community base. Three adult largemouth bass
(average total length = 283mm) collected from a nearby lake were stocked into each pond to serve as
potential predators on the juvenile bass. In the summer of 2013, both ponds were drained and all
surviving bass were collected and measured for size. 66 juveniles survived in the vegetated pond and 67
survived in the pond mostly free of vegetation. All adult bass survived in each pond.

Experiment 2: Adult reproductive success
101 age-3, reproductively mature bass were assayed in the behavioral trials in the spring of 2011
and then sexed using methods previously developed by Benz and Jacobs (1986). Bass were randomly
distributed among three experimental ponds (34 bass in two ponds and 33 in one, with a sex ratio of 1819 males to 15 females). Once the reproductive season commenced, ponds were snorkeled daily by an
observer to locate all male nests. When nests were found, an attempt was made to identify the nest
guarding male. Photographs of nests were taken to quantify the number of eggs in each nest.

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Additionally, a sample of approximately 20 eggs was collected from each nest and hatched in the
laboratory. Laboratory hatched larvae were euthanized with MS-222 and then stored in ethanol for later
DNA analysis. This experimental design was continued the following two years (2012 and 2013). In the
spring, the ponds were drained and all surviving adults were collected and identified (age-4 n=93; age-5
n=71). The adults were then taken to the laboratory for approximately 1 week to run them through the
behavioral assays and re-measure them for size. Adults were then placed back into the experimental
ponds to observe the reproductive success. 35 nests with eggs were located over the 3 year study period
(12 age-3 nests, 15 age-4 nests, and 8 age-5 nests).
We extracted DNA from all 101 adults and from up to 5 larvae from each nest (from the subset
of 20 eggs that were collected from each nest and hatched in the laboratory) by using the QIAGEN
DNeasy extraction kit in accordance with the manufacturer’s specifications. We diluted DNA samples to
20 ng/μL and then genotyped them at 10 microsatellite loci; Lma21 (Colbourne et al. 1995), Msaf14,
Msaf17 (Seyoum et al. 2013), MiSaTPW011, MiSaTPW012, MiSaTPW038, MiSaTPW068, MiSaTPW076,
MiSaTPW107, and MiSaTPW173 (Lutz-Carrillo et al. 2008). Amplification was performed using
polymerase chain reaction (PCR) and alleles were separated using gel electrophoresis on a 6%
polyacrylamide gel. Products were visualized using an FMBIOII scanner (Hitachi Inc., Tokyo, Japan). All
gels were independently scored by two experienced laboratory personnel. To estimate genotyping
error, 10% of adults were randomly selected and re-genotyped for all loci. Estimates of expected
heterozygosity, number of alleles, and tests for Hardy-Weinberg Equilibrium were performed using the
program CERVUS 3.0.3 (Kalinowski et al. 2007).
To determine parentage for each nest and ultimately reproductive success for each adult at
each age, a multi-step approach was employed. Firstly, we conducted a preliminary parentage analysis
with unknown parents using the program CERVUS 3.0.3 (Kalinowski et al. 2007). The preliminary
parentage analysis allowed for the successful identification of the sire (or sires) for 25 of the 35 nests. A

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male was visually identified on 23 of those 25 nests. In those 23 cases, the paternal parent assigned to
the nest based on the parentage analysis matched the male identified on the nest 22 times. Thus, the
paternal parent was assumed to be known in all cases in which a male was identified on a nest (31 of the
35 nests). A second parentage analysis was then conducted using CERVUS 3.0.3 with the paternal
parent/s assumed as known for 33 of the nests (31 from visual identification and 2 from the preliminary
parentage analysis) to assign the maternal parent/s for each nest. Ultimately, of the 35 total nests, 34
had 1 or more male assigned at least partial parentage and 27 had 1 or more female assigned at least
partial parentage. The egg score for each nest (calculated from photographs) was then used to
determine the number of fertilized eggs produced by each adult during each reproductive season. In
cases in which a nest had multiple paternity or multiple paternity (based on parentage analysis), the egg
scores were distributed accordingly. For example, if 4 of the 5 larvae in a nest were assigned to male 1
and 1 of the 5 were assigned to male 2, male 1 would be given a reproductive success score = 80% of the
nest egg score while male 2 would be given a reproductive success score = 20% of the nest egg score. If
fertilized eggs from multiple nests were assigned to an adult, the egg scores from each nest were
summed to calculate the adult’s reproductive success. Thus, each adult had a reproductive success score
at age-3, age-4, and age-5.

Experiment 3: Personality heritability
The 240 young-of-year offspring used in the juvenile survival experiment were produced by the
age-4 adult bass used in the reproductive success experiment. Thus, we had personality data for 240
offspring and their 93 potential parents. 159 of the 240 offspring were randomly selected for DNA
analysis. DNA was extracted, amplified, and visualized at 10 microsatellite loci following the methods
described above in the reproductive success experiment. To determine parentage for these 159
samples, we conducted a parentage analysis with unknown parents (the genotypes for the 93 potential

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parents were obtained during the reproductive success experiment) using the program CERVUS 3.0.3
(Kalinowski et al. 2007). After taking into account what was already known about the reproductive
history of this population at 4 years of age (knowledge of the nests that were produced and parentage
for each nest), the results of the parentage analysis allowed for the assignment of 39 of the 159
offspring to parent pairs.

Statistical analysis
All statistical analyses were conducted using R version 2.13 (R Development Core Team 2008).
Previous studies on this population of largemouth bass indicate that context-specific personality traits
underlie the expression of behavior in each of the contexts observed and that correlations exist
between most of the context-specific traits (Ballew in review). To determine if the context-specific traits
are sub-modules of a context-general trait (like boldness), we conducted a principal components
analysis of the four context-specific personality traits. Separate principal components analyses were
conducted for the 240 juvenile bass (which included the 39 used in the heritability study), and for the
adult context-specific personality traits at age-3, age-4, and age-5. The principal components analyses
revealed a general personality trait interpreted as boldness in the juveniles and at each age in the
adults. This result is in line with other studies on this bass population (Ballew in review). Thus, in
addition to the fitness effects of the context-specific traits, the fitness effects of the boldness trait (from
the PCA) were also investigated.
To investigate the effect of personality traits on juvenile survivorship in experiment 1, we first
standardized (mean = 0 and standard deviation = 1) the scores for initial and final length and for each
personality trait. We then performed separate logistic regressions for each personality trait. We
included initial length and pond as covariates; Survival (Yes/No) = Length + Personality + Pond +
Length:Personality + Length:Pond + Personality:Pond.

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To investigate the effect of personality on adult reproductive success in experiment 2, we first
summed the reproductive success values from age-3, age-4, and age-5 to calculate a cumulative
reproductive success score for each adult, which was then standardized to a mean of 0 and a standard
deviation of 1. We standardized the personality and size scores for the adult context-specific personality
traits at age-3, age-4, and age-5. We then calculated average personality scores for each personality trait
within each individual and average size for each individual. If an adult survived over all three years, their
average personality and average size scores were calculated based on their scores at age-3, age-4, and
age-5. For those individuals who did not survive through age-5, the averages were calculated based on
the years in which they were measured. Calculating an average score for each personality trait is
warranted based on the consistency observed in these traits over this this time period (Ballew
submitted). We performed separate linear regressions for each personality trait (with the average
scores) and included sex and average length as covariates; Cumulative reproductive success = Sex +
Length + Personality + Sex:Length + Sex:Personality + Length:Personality.
To investigate the heritability of each personality trait in experiment 3, we used the
standardized personality scores for the adults when they produced the offspring (age-4) and the
standardized personality scores for the offspring (from the total 240 offspring) when they were youngof-year. The 39 offspring that had parentage assigned were produced by 7 families, with a range of 1 to
17 offspring per family. The average offspring personality score for each family was calculated for each
personality trait. We then performed separate linear regressions for each personality trait; Average
offspring personality for the family = Mid-parent personality. The regressions were weighted by number
of offspring in each family. Separate regressions were conducted on each context-specific personality
trait and on the general boldness trait.

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RESULTS
Experiment 1: Juvenile survivorship
A general personality trait interpreted as boldness was uncovered from the principal
components analysis on the four context-specific personality traits. Bolder individuals (higher scores on
axis 1) were significantly less hesitant to enter a novel environment, were more active in the safe and
familiar context, were more aggressive in the mirror-test context, and were less hesitant to approach
the food in the food and predator present context. Overall, boldness explained 48% of the variation
observed in the four context-specific traits.
Logistic regressions of the effect of initial length and personality on juvenile survivorship in two
different pond environments (highly vegetated and not vegetated) revealed that larger juvenile bass had
significantly higher survivorship (Table 14). Further, there was an interaction between pond
environment and length. Initial length had a significantly greater positive effect on survivorship in the
vegetated pond than in the non-vegetated pond (Figure 11b). Additionally, bass that scored higher in
the novel environment context, bass that were more willing to forage in the predation risk context, and
bass that were bolder in general (Axis 1 from PCA) all had significantly lower survivorship than their
conspecifics. Each of these three traits also had a significant interaction with the pond environment.
Bass that were bolder, more exploratory, and more willing to forage had much lower survivorship when
compared to conspecifics in the vegetated pond but not in the non-vegetated pond (Figure 11a).

Experiment 2: Adult reproductive success
A boldness trait similar to the one found in the sample population used in experiment 1 was
uncovered in the sample population used in experiment 2 (Boldness = Axis 1 from PCA and explains 43%
of the variation at age-3, 47% of the variation at age-4, and 48% of the variation at age-5). Linear
regressions of the effect of sex, average length, and average personality on reproductive success

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revealed that bass that were more active in the familiar environment had a significantly higher
reproductive success (Table 15). Additionally, length and personality interacted to effect reproductive
success. Large, bold (Axis 1 from PCA) bass had significantly higher reproductive success than bold, small
bass and large, timid bass and this effect was due primarily to males (Figure 12). Similar interactions
were found between length and exploration in the novel environment and length and aggressiveness in
the mirror context.

Experiment 3: Personality heritability
Small sample size (n=39) made it difficult to assess the heritability of the personality traits via
parent-offspring regressions with a high degree of accuracy. Nonetheless, we found that the general
boldness trait (Axis 1 from the PCA) had a nearly statistically significant heritability of 0.527 (Figure 13;
Table 16 95% confidence interval = -0.031 – 1.084). While none of the context-specific personality traits
were heritable at the statistically significant p<0.05 level, both the novel environment context trait and
the food and predator present context trait displayed moderate levels of heritability in this study
population. Thus, further analysis into the heritability of these traits, as well as the other contextspecific personality traits, is warranted.

DISCUSSION
The results of this study demonstrate for the first time that individual personality traits can
affect fitness in multiple ways over the course of an individual’s lifetime. Under semi-natural conditions
(outdoor ponds), larger and bolder adult bass had higher reproductive success over a 3-year period.
Bolder juveniles spawned by these adults, however, had significantly lower survivorship. Thus, boldness
impacted fitness differently in the adult and juvenile stages. As a result, there may be a fitness tradeoff
between juvenile survivorship and adult reproductive success. As boldness was significantly heritable, it

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appears that in at least some environments, alternative boldness phenotypes may yield similar fitness,
which could maintain variation in boldness within populations. This latter result is in line with a model
that was developed to explain sexual cannibalism in the fishing spider Dolomedes fimbriatus (Arnqvist
and Henriksson 1997). In this study, selection was modeled to favor high levels of aggression in juvenile
females, as it increased growth rate and adult fecundity, but low levels of aggression in adulthood, as it
led to maladaptive pre-copulatory sexual cannibalism. Further, aggression was modeled to be consistent
from the juvenile to the adult stage. As a result, trade-offs across contexts were found that could lead to
a population of individuals that varies dramatically in aggression levels.
While boldness did negatively impact juvenile survivorship, this effect was not observed in both
pond environments. In the pond with dense vegetation, bold juveniles had significantly lower survival
then their more timid conspecifics, but boldness did not significantly affect survivorship in the newly
renovated pond with sparse vegetation. This interaction between boldness and pond type on juvenile
survival could have been due to the fact that in the high vegetation pond in which boldness negatively
affected juvenile survival, vegetation may have served as refuge from predation for juvenile bass that
wished to use it. Shyer bass would likely be more apt to avoid predators when possible, and as a result,
would likely be the ones that would take advantage of the refuge. In contrast, in the pond with low
levels of vegetation, shy individuals had no opportunity to seek refuge from predation. Thus, the
juvenile survivorship in this pond was unaffected by boldness. This result suggests that, in addition to
fitness tradeoffs across development, tradeoffs across fluctuating selection pressures could further act
to maintain variation in personality.
The “trade-off” hypothesis posits that individual fitness varies depending on environmental
context and that contexts fluctuate frequently, resulting in the maintenance of variation (Sih et al.
2004). Studies have demonstrated that fitness consequences for personality traits can vary according to
shifting environmental conditions such as predation pressure (Réale and Festa-Bianchet 2003), food

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availability (Dingemanse et al. 2004), and social condition (Both et al. 2005). However, studies have yet
to demonstrate how common it is for these environmental conditions to shift enough in nature to
significantly reduce (or reverse) the direction of selection. A related idea is that frequency dependent
selection may also operate on personality traits to maintain variation (Sih et al. 2004; Dingemanse and
Réale 2005; Wolf and McNamara 2012).
Larger juveniles survived better in the densely vegetated pond but size did not affect juvenile
survivorship in the sparsely vegetated pond. Further, juveniles in the more densely vegetated pond grew
much faster than in the sparsely vegetated pond, likely due to a higher density of invertebrates. Thus,
the largest juveniles in the densely vegetated pond may have grown fast enough to reach sizes that
allowed them to escape the threat of predation during the course of the experiment. In contrast, in the
sparsely vegetated pond, the largest individuals likely did not grow enough to reach sizes large enough
to escape predation. This differences in growth rate in the two ponds could explain the interaction
effect between length and pond environment on juvenile survival. In addition, past studies have shown
that bolder juveniles grow faster (Ballew submitted). Thus, in the densely vegetated pond, boldness may
have directly negatively affected juvenile survivorship and indirectly positively affected juvenile
survivorship (through faster juvenile growth). This explanation would be consistent with the growthmortality hypothesis that boldness results in reduced survivorship at the early juvenile stage but higher
growth, which could result in increased survivorship at the later juvenile stage and also in increased
reproductive success at the adult stage (Mittelbach et al. 2014).
The results of the current study suggest that selective forces on personality traits in nature can
be substantial and may shape personality variation within the time frame of a single generation. It
should be noted, however, that not all observed variation is attributable to heritable differences. For
example, while each of the context-specific traits investigated in this study had a significant effect on
fitness during at least one life stage, none of the context-specific personality traits were heritable at a

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statistically significant level. This may be in part due to the low power of the parent-offspring test of
heritability conducted in this study. However, other studies have also reported low, and in some cases,
non-significant levels of heritability in personality traits (Bell 2005; Dingemanse et al. 2009; Kortet et al.
2014; reviewed for fish in Mittelbach et al. 2014). Thus, early experience, maternal effects, and paternal
effects are also likely to have relatively large effects on an individual’s personality type (Dingemanse et
al. 2009; Stamps & Groothuis 2010).
Our results demonstrate for the first time that trade-offs across components of fitness, as well
as fluctuating environmental conditions, have the potential to maintain variation in boldness within
populations. Our results also caution against drawing conclusions regarding the overall fitness
consequences of a personality trait from studies conducted on a single component of fitness at a given
stage of development (Smith and Blumstein 2008). To adequately address the fitness consequences of
personality in a species of interest, it is necessary to fully consider the ecology and evolutionary context
of the species, properly characterize personality phenotypes, and assess their level of consistency (Dall
and Griffith 2014; Aray-Ajoy and Dingemanse 2014). Comprehensive studies that investigate the fitness
consequences of personality over its entire length of consistency are needed in order to fully understand
the mechanisms that most commonly shape and maintain personality variation within populations.

ACKNOWLEDGEMENTS
We thank Mary Tate Bremigan for her many insightful comments and suggestions on earlier
versions of this manuscript. Additionally, we thank Cristopher Mirque for his help during parts of the
data collection process. Grants from the US National Science Foundation (IOS-1311455), Sigma Xi,
Kellogg Biological Station, and the Zoology Department at Michigan State University supported portions
of this research.

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APPENDIX

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Table 14. Logistic regressions of the effect of length and personality on juvenile survivorship in two different experimental ponds. One pond was
older and contained abundant macrophytes and invertebrates while the other was newly renovated and contained little vegetation and a less
productive invertebrate community. Each model has 233 degrees of freedom. Survival (Yes/No) = Length + Personality + Pond +
Length:Personality + Length:Pond + Personality:Pond. For comparison, the null model deviance was 329.89.
Personality
Trait

Intercept

Length
Coefficient

Personality
Coefficient

Pond
Coefficient

Length:PT
Coefficient

Length:Pond
Coefficient

PT:Pond
Coefficient

NECT

0.122

0.667**

-0.519*

0.106

0.169

-0.699*

0.553*

Residual
Deviance
from model
311.66

SFCT

0.196

0.604**

-0.295

0.031

0.051

-0.631*

0.231

317.23

MTCT

0.188

0.613**

-0.084

0.065

0.043

-0.682*

-0.075

318.95

FPCT

0.120

0.693**

-0.693**

0.114

0.121

-0.733*

0.732*

309.64

Boldness

0.108

0.671**

-0.657**

0.131

0.155

-0.716*

0.636*

309.48

Note: NECT = Novel environment context trait, SFCT = Safe and familiar context trait, MTCT = mirror-test context trait, FPCT = food and predator
present context trait. * = P ≤ 0.05; ** = P≤ 0.005.

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Table 15. Linear regressions of the effect of sex, length, and personality on adult bass reproductive success. Reproductive success = Sex + Length
+ Personality + Sex:Length + Sex:Personality + Length:Personality. Each model has 94 degrees of freedom.
Personality
Intercept
Sex
Length
Personality
Sex:Length
Sex:PT
Length:PT
R-squared
Trait
Coefficient
Coefficient
Coefficient
Coefficient
Coefficient
Coefficient
NECT
0.011
-0.077
0.013
0.028
0.253
0.270
0.218*
0.149
SFCT

0.076

-0.072

-0.063

0.334*

0.401

-0.202

-0.013

0.130

MTCT

0.067

-0.111

0.165

0.190

0.188

-0.051

0.421**

0.238

FPCT

0.009

-0.038

-0.015

-0.046

0.289

0.204

0.099

0.100

Boldness

0.045

-0.138

0.061

0.100

0.169

0.180

0.219*

0.169

Note: NECT = novel environment context trait, SFCT = Safe and familiar context trait, MTCT = mirror-test context trait, FPCT = food and predator
present context trait. * = P≤ 0.05, ** = P ≤ 0.005.

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Table 16. Linear regressions of the heritability of each personality trait. Each model
has 5 degrees of freedom. Average offspring personality = Mid-parent personality.
Regressions weighted by number of offspring in each family.
Personality Trait
Heritability
95% Confidence Intervals
NECT

0.153

-0.392 – 0.697

SFCT

-0.233

-0.604 – 0.139

MTCT

-0.111

-0.745 – 0.523

FPCT

0.270

-0.228 – 0.769

Boldness

0.527

-0.031 – 1.084

Note: NECT = novel environment context trait, SFCT = Safe and familiar context trait,
MTCT = mirror-test context trait, FPCT = food and predator present context trait.

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Figure 10. Model illustrating the organization and structure of personality traits in this population of largemouth bass. A context-specific
personality trait influenced behavior across all ages of development that were investigated in the novel environment context, in the foraging in
the presence of an aerial predator context, and in the mirror-test context. A boldness personality trait generalized beyond specific functional
contexts was found to underlie each of these context-specific traits. A personality trait also influenced adult (but not juvenile) behavior in the
safe and familiar environment. This personality trait may have been a context-specific trait (indicated by the dashed line between behavior and
the unidentified trait) or may have been the general boldness trait (indicated by a dashed line between boldness and the unidentified trait).
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Figure 11. a) Average boldness and b) average initial length of bass that survived to the end of the experiment (grey circles) and bass that did not
survive (black circles) in the high vegetation pond and in the low vegetation pond. Error bars indicate the standard error of the mean.

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Figure 12. The effects of boldness, length, and the interaction between them on adult reproductive success. The light grey plane represents the
relationships between the variables for males and the dark grey plane represents the relationships between the variables for females. The circles
(light grey = males; dark grey = females) represent individual males and the lines from the circles to the planes represent residual values.

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Figure 13. The heritability of boldness. Each circle represents the average boldness of offspring in a full-sib family. The numbers below the circles
represent the number of offspring in each family. The trend line (black) is weighted by the number of offspring in each family.

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CHAPTER 5: Personality Affects Angling Vulnerability in Largemouth Bass (Micropterus Salmoides)

ABSTRACT
Commercial and recreational fishing can be a strong selective force, however, studies of the
effects of personality on vulnerability to angling are scarce. Here, I investigated if personality traits affect
vulnerability to angling in largemouth bass (Micropterus salmoides) in three different angling contexts.
To quantify personality, behavior was assayed in the laboratory under four experimental conditions: a
novel environment context, a familiar environment context, a social context, and a feeding under
predation risk context. After quantifying personality, fish were subjected to one of three angling
contexts: 1) a mesocosm context, 2) an outdoor pond, and 3) an outdoor pond with casts made directly
onto bass nests. When angling was conducted in a mesocosm, which was likely perceived to contain a
high level of risk, bass that were more risky foragers with predators present in the laboratory were more
vulnerable to angling. Additionally, bass that were bolder in general (boldness obtained from a principal
components analysis of the context-specific behavioral measurements) were also more vulnerable to
angling in the mesocosm context. When angling was conducted in an outdoor pond, which was likely
perceived to contain a low level of risk, bass that were more aggressive in the laboratory were more
vulnerable to angling. Lastly, nest guarding males that were more active in the safe and familiar
environment and were bolder in general were more vulnerable to angling. The results of this study aid in
our understanding of the selective capture of fish by recreational angling, which may have significant
evolutionary and ecological consequences and may affect the quality of fisheries.

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INTRODUCTION
Individuals from the same population and at the same developmental stage often display
consistent differences in behavior over time and across contexts (Gosling 2001; Réale et al. 2007; Bell et
al. 2009). This consistent inter-individual variation in behavior is widely accepted as evidence of
personality types that underlie the expression of behavior (Budaev and Brown 2011; Araya-Ajoy and
Dingemanse 2014). Several studies have demonstrated that personality can affect various components
of fitness (Smith and Blumstein 2008; Kontiainen et al. 2009; Ariyomo and Watt 2012). Further, there is
mounting evidence that personality types have a heritable component (Chervet et al. 2011; Ariyomo et
al. 2013; Kortet et al. 2014; Ballew et al. in prep). These results indicate that personality variation within
populations may well be the adaptive outcome of natural selection (Mittelbach et al. 2014). A study that
compared levels of activity, aggression, and boldness in populations of threespined stickleback supports
this idea (Bell 2005). Stickleback populations differed significantly in mean levels of boldness and
aggressiveness, likely due to differences in predator regime. The idea that personality may be the
adaptive outcome of natural selection has also been recently applied to fisheries research to develop
hypotheses regarding the potential evolutionary consequences of recreational fishing (angling).
A fish’s personality may determine its vulnerability to capture by recreational angling and thus
its survival and fitness (Uusi-Heikkilä et al. 2008; Mittelbach et al. 2014). However, studies of the effects
of personality on angling vulnerability are scarce (Biro and Post 2008; Wilson et al. 2011; Binder et al.
2012; Klefoth et al. 2013). Previous empirical studies on vulnerability to angling have mainly compared
personalities between groups selected for high or low vulnerability to angling (Redpath et al. 2009;
Binder et al. 2012) or groups differing in domestication history (Biro and Post 2008; Klefoth et al. 2013).
For example, artificial selection for vulnerability to angling has been shown to affect foraging behavior in
largemouth bass (Nannini et al. 2011). To date, the relationship between personality and angling
vulnerability has only been investigated at the individual level in one study with bluegill sunfish (Wilson

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et al. 2011), which surprisingly showed that timid fish may be more vulnerable to angling. Thus, there is
great need for more studies that directly investigate the selection pathways that may lead to fisheriesinduced evolution (Uusi-Heikkilä et al. 2008).
Boldness and aggressiveness, in particular, are frequently hypothesized to affect angling
vulnerability (Cooke et al. 2007; Biro and Post 2008; Klefoth et al. 2013). Boldness has been shown to
underlie behaviors such as general activity, space use, foraging behavior, and exploration (Wilson and
McLaughlin 2007; Farwell and McLaughlin 2009; Wilson and Godin 2009). Thus, if a bait or a lure is
perceived by a fish as a risky foraging opportunity, it is easy to see how boldness would affect an
individual’s propensity to strike. Conversely, if striking a bait or a lure represents an aggressive act (as
opposed to a foraging one), then an individual’s angling vulnerability would be more affected by its level
of aggressiveness. However, it is important to note that aggressive behavior, such as biting at
conspecifics, has also been hypothesized to be influenced by boldness, as agonistic interactions carry a
significant level of risk in their own right (Budaev and Brown 2011). Additionally, all angling scenarios
may not be perceived in the same manner and as a result, different scenarios may result in different
selection pathways. For example, lures cast into cover (logs, under docks, etc) may be perceived by fish
as non-risky foraging opportunities while lures cast into open water may be perceived as more risky. In
the same way, in species that build nests or redds and provide parental care, a lure cast onto the nest of
a guarding parent may be perceived very differently than one cast into open water. As such, the
personality traits that affect angling vulnerability in each of these situations may be very different.
Here, I use largemouth bass (Micropterus salmoides) to address if personality traits affect
angling vulnerability. Largemouth bass are particularly amenable to this type of study as they are
abundant in many freshwater systems and are known to exhibit consistent inter-individual differences in
personality across life stages (Philipp et al. 2014; Ballew submitted). In most habitats, largemouth bass
develop from small juvenile fish that are vulnerable to predation into large adults that are apex

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predators in their own right. During the spring, reproductively mature male bass build highly visible
nests in the shallow littoral areas of lakes (Heidigner 1975; Philipp et al. 1997). Females lay eggs in the
nests and then leave the males, who provide sole parental care by guarding the nests from potential egg
and larval predators (Ridgway 1988; Philipp et al. 1997). Bass are a popular target of recreational
fisherman and results from an artificial selection experiment show that largemouth bass have the
potential to adapt to recreational angling (Philipp et al. 2009). Further, angling during the bass
reproductive season is especially popular among a segment of bass anglers.
I investigated the relationship between personality and angling vulnerability in three different
angling contexts. To quantify personality, fish were observed in the laboratory under four experimental
behavioral contexts: 1) a novel environment, 2) a familiar and safe environment, 3) a social environment
(mirror-test), and 4) an environment where food and predators were present. Previous studies on this
population of largemouth bass indicate that context-specific personality traits underlie the expression of
behavior in each of these contexts and that the context-specific traits are sub-modules of a contextgeneral trait identified as boldness (Ballew submitted). After quantifying personality, fish were subjected
to angling in one of three contexts: 1) a mesocosm, 2) a semi-natural outdoor pond, 3) a semi-natural
outdoor pond where casts were made directly onto bass nests.
I predicted that in the mesocosm angling context, bass that hesitate less before approaching
food in the food and predator present context would be caught more frequently than their conspecifics.
In the mesocosm context, I assumed that bass would be aware of the angler overhead and also be
witness to their conspecifics being caught. Thus, I assumed that bass would perceive the mesocosm as a
risky context. I predicted that in the outdoor pond angling context, bass would perceive it to be a
relatively non-risky context and as a result, more aggressive bass in the mirror-test context would be
more vulnerable to angling. Further, I predicted that in the outdoor pond angling context where casts
were made directly onto bass nests, more aggressive males in the mirror-test context would be more

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vulnerable to angling. The rationale behind this prediction is that nest guarding males strike lures to
protect their nests and more aggressive males are expected to be more protective. Lastly, I predicted
that bolder (the context-general personality trait obtained from a principal components analysis of the
context-specific traits) bass would be more vulnerable to angling in all three contexts. Boldness was
predicted to affect angling vulnerability in all three contexts, as opposed to just in the mesocosm,
because even though only the mesocosm context is expected to be perceived as overtly risky, striking at
the lures themselves in the outdoor ponds is may still be perceived to carry a low level of risk. In other
words, the mesocosm context is predicted to be risky in and of itself whereas in the outdoor ponds, it is
direct engagement with the lures that may be perceived as risky. The results of this study will aid in our
understanding of the selective capture of fish by recreational angling, which may have significant
evolutionary and ecological consequences for the affected populations and the quality of the fisheries
(Sutter et al. 2012; Philipp et al. 2014; Mittelbach et al. 2014).

METHODS
Study population and husbandry
The largemouth bass used in each experiment described below were collected from a pond
located at the Kellogg Biological Station experimental pond facility in southwest Michigan. These bass
were bred on site from adult bass collected from nearby Wintergreen Lake. Randomly selected
individuals were transferred to the laboratory facility and were individually marked with colored
elastomer gel (a biocompatible pliable polymer; Northwest Marine Technology, Goldsmith et al. 2003)
that was injected subcutaneously at two of seven possible locations. The bass were socially housed in
aquaria (4 bass per aquarium) and provided with an excess amount of zooplankton. Bass were measured
for length and then transferred from the holding aquaria into their own testing aquariums to undergo a
series of behavioral assays. Upon completion of the assay procedure, bass were subjected to 1 of 3

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angling experiments. Bass subjected to angling experiment 1 were underwent the series of behavioral
assays a second time following the completion of the angling experiment. The bass that were subjected
to angling experiments 1 and 2 were observed in the laboratory under three experimental behavioral
contexts: 1) a familiar and safe environment, 2) a social environment (mirror-test), and 3) an
environment where food and predators were present. Bass from angling experiment 3 were observed in
a novel environment context, in addition to the three behavioral contexts that bass from angling
experiments 1 and 2 were observed in.

Behavioral assay procedure
Behavioral assays followed a similar procedure as outlined in previous studies with this
population of largemouth bass (Ballew in review). The testing aquaria were divided into two sections by
an opaque vertical partition with the smaller section making up about 10% of the total volume.
Individual bass used in angling experiment 3 were transferred into the smaller section of a testing tank
and then left for approximately 45 minutes to recover from handling and to acclimate to the new
environment. After the 45 minute acclimation period, novel context trials were initiated. The partition
was raised approximately 10 centimeters above the floor of the aquarium using a pulley system,
allowing the fish to swim from the smaller section into the larger section. For each sample, I measured
the elapsed time from when the partition was raised until the fish swam into the larger area of the tank
(up to 45 minutes). If after 45 minutes a fish had not moved to the larger section of the tank, I gently
coaxed it out. Once a fish moved into the larger section of the tank, I lowered the partition so that it
could not move back into the smaller section. An individual’s score was calculated by subtracting the
number of seconds that it waited before moving to the larger portion of the tank from 2700 (the
maximum trial length). Thus, individuals with higher scores moved more quickly to the larger section of
the tank. Individuals that did not leave the small section during the trial received a score of 0. Following

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the completion of the novelty trial, I placed a mirror on the wall in the smaller section of the tank (not
visible to the fish). Fish were then left overnight in the larger section of the tank to acclimate to their
new surroundings. Bass subjected to angling experiments 1 and 2 were not observed in the novel
environment trial. Instead of placing them in the smaller section of the tank, bass were simply placed in
the larger section of the tank and left overnight to acclimate to their new surroundings.
The day after introducing a bass into a testing aquarium, I assayed its behavior in a familiar and
safe context. I measured the amount of time the bass spent moving around the tank in the familiar
environment (larger section of the tank). Fish were observed for 5 minutes and I summed the total time
spent swimming (moving) to calculate the total number of seconds active per trial.
Immediately following the measurements taken in the familiar and safe environment trial, I
conducted the social context (mirror-test) trial. I raised the partition to reveal a mirror on the wall in the
smaller section of the tank. Once the partition was raised the trial commenced. Trials lasted for 10
minutes. I measured the number of bites, tail swipes, and rams at the mirror. At the end of the trial, the
partition was lowered so that the mirror was no longer viewable. As the partition was lowered, fish in
the path of the partition consistently retreated to the larger section of the tank. The number of bites,
tail swipes, and rams were summed together to get an overall measure in this context. These behaviors
were summed together because each was taken to be a specific form of agonistic behavior and other
studies have shown that individuals often exhibit behavioral specificity so that they tend to primarily use
their preferred method of a behavioral type (one individual may primarily use rams while another
primarily uses bites; Uher 2011).
Approximately one hour after observing behavior in the presence of the mirror, the feeding in
the presence of a predator trial was conducted. A live earthworm tied to monofilament fishing line (no
hook) was lowered into the tank near one end. When the bass approached the worm, a model bird
suspended on a string and pulley system positioned directly above the worm was released to strike the

146

surface of the water, simulating a predation attempt. The bird was then quickly lifted from the water,
again using the string and pulley system. During this time, the fish most often retreated to a corner of
the tank. Once the bird was appropriately positioned (10 centimeters above the water surface), the trial
commenced. I recorded how many seconds it took the bass to re-approach the worm. An individual’s
score was calculated by subtracting the number of seconds that a fish waited before re-approaching the
worm from the maximum trial length. Thus, individuals with higher scores re-approached the worm
faster. Individuals that did not re-approach the worm during the trial received a score of 0. Upon
completion of this final assay, bass were subjected to 1 of three angling experiments. Additionally, bass
subjected to angling experiment 1 were re-assayed post-angling.

Angling Experiments
Experiment 1: Mesocosm context
36 bass that underwent the behavioral assay procedure were split randomly between two large
(1000 liter) outdoor covered tanks. Bass were left in the tanks for 4 weeks. During the 4 week period,
bass could feed on zooplankton ad libitum. Bass were exposed to a standardized angling procedure
several days each week over the course of the 4 weeks. The angling procedure consisted of first
uncovering the tanks. Then, from a distance of approximately 1 meter away from the edge of the tank,
a hook (baited with an earthworm) was cast into the middle of the tank. 18 casts were made into each
tank and I attempted to catch any bass that struck at the bait. Caught bass were identified and then
returned to the tank. If after 1 minute no bass had struck at the worm, the worm was reeled in. Upon
the completion of a cast (either due to a landing or 1 minute time limit), I waited 1 minute before recasting into the center of the tank. During this 1 minute waiting period, I re-baited the hook (if
necessary). Over the course of the four week angling experiment, one bass died in each tank. At the

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conclusion of the angling experiment, the 34 surviving bass were exposed to the same three behavioral
assays used pre-angling.

Experiment 2: Outdoor pond context
202 bass that underwent the behavioral assay procedure were stocked in an experimental pond
(30 m wide and 2 m deep). Bass were exposed to angling several days each week over the course of a 4
week angling experiment. Angling lasted approximately 1 hour on days that angling took place. While
standing at the edge of the pond, I casted a hook (baited with an earthworm) into the middle of the
pond and then slowly reeled in the worm. If a bass struck at the hook, an attempt was made to land it.
Successfully landed bass were identified and then returned to the pond to simulate catch-and-release
style angling.

Experiment 3: Outdoor pond context with casts made directly onto bass nests
Reproductively mature bass that underwent the behavioral assay procedure in the spring were
split randomly into 3 experimental ponds. I then snorkeled throughout the 3 ponds daily during the bass
reproductive season to locate male nests. When nests were found, photographs were taken to quantify
the number of eggs in each nest. Approximately one hour after finding a nest, I angled for the nest
guarding male. Standing from shore, I made casts onto the nest. If the nest guarding male struck at the
hook (baited with an earthworm), an attempt was made to land it. Successfully landed males were
identified and then returned to their nests. If after 1 minute the male had not struck at the worm, the
worm was reeled in. Up to 5 casts were made on each nest. Males that were caught on the first cast
were given an angling vulnerability score of 5, males caught on the second cast a score of 4, and so on
with males not caught being given a score of 0. I attempted to catch males from 36 nests.

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Statistical analysis
All statistical analyses were conducted using R version 2.13 (R Development Core Team 2008).
Scores for all variables were standardized (mean of 0 and standard deviation of 1). Previous studies on
this population of largemouth bass indicate that context-specific personality traits underlie the
expression of behavior in each of the contexts observed and that correlations exist between most of the
context-specific traits (Ballew in review). To determine if the context-specific traits are sub-modules of a
context-general trait (like boldness), I conducted a principal components analysis of the context-specific
personality traits for the samples used in each of the angling experiments. The principal components
analyses revealed a general personality trait interpreted as boldness in each sample population. This
result is in line with other studies on this bass population (Ballew in review). Thus, in addition to the
context-specific traits, the effect of the boldness trait (from the PCA) on angling vulnerability was also
investigated in each angling experiment.
To investigate the effect of personality traits on angling vulnerability in experiment 1 (mesocosm
context), I performed separate linear regressions for each personality trait and included bass length as a
covariate; angling vulnerability = length + personality + length:personality. To investigate the effect of
personality on angling vulnerability in experiment 2 (outdoor pond context), I performed separate
logistic regressions for each personality trait and included length as a covariate; vulnerable to angling
(Yes/No) = length + personality + length:personality. To investigate the effect of personality on angling
vulnerability in experiment 3 (outdoor pond context with casts made directly onto bass nests), I
performed separate linear regressions for each personality trait and included length and nest egg count
as covariates; angling vulnerability = length + nest egg count + personality + length:personality + nest
egg count:personality. Separate regressions were conducted on each personality trait because the
boldness trait was taken to represent a combination of the traits.

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RESULTS
Angling experiment 1: Mesocosm context
A general personality trait interpreted as boldness was uncovered from the principal
components analysis on the three context-specific personality traits measured prior to exposure to
angling. Bolder individuals (higher scores on axis 1) were significantly more active in the safe and
familiar environment context, more aggressive in the mirror-test context, and less hesitant to approach
the food in the food and predator present context. The principal components analysis on the three traits
measured after exposure to angling produced the same result. Overall, boldness explained 41% of the
variation observed in the three context-specific traits prior to angling and 46% of the variation observed
in the context specific traits after angling.
Linear regressions of the effect of bass length and personality on angling vulnerability in the
1000L holding tanks showed that bass that hesitate shorter periods of time to approach food in the
presence of predators are significantly more vulnerable to angling (Table 17). Further, bass that are
bolder are also significantly more vulnerable to angling. In addition, an interaction between length and
some of the personality traits, such as the initial boldness measure, had a negative effect on angling
vulnerability (Figure 14). Overall, angling vulnerability was moderately determined by the food and
predator present context-specific trait and the interaction between this trait and length (R2 = 0.34 for
pre-angling measurements and 0.31 for post-angling measurements).

Angling experiment 2: Outdoor pond context
A boldness trait similar to the one found in the sample population used in angling experiment 1
was uncovered in the sample population used in angling experiment 2 (Boldness = Axis 1 from PCA and
explains 40% of the variation). Logistic regressions of the effect of length and personality on angling
vulnerability in the experimental pond revealed that larger bass were significantly more vulnerable to

150

angling (Table 18). Additionally, more aggressive bass in the mirror-test context and bolder bass were
more vulnerable to angling (Figure 15). However, only the result in the mirror-test context was
statistically significant (Table 18).

Angling experiment 3: Outdoor pond context with casts made directly onto bass nests
A boldness trait similar to the ones found in the sample populations used in angling experiments
1 and 2 was uncovered in the sample population used in angling experiment 3. Bolder individuals (higher
scores on axis 1) were significantly less hesitant to enter a novel environment, were more active in the
safe and familiar context, were more aggressive in the mirror-test context, and were less hesitant to
approach the food in the food and predator present context. Overall, boldness explained 42% of the
variation observed in the four context-specific traits.
Linear regressions of the effect of bass length, nest egg count, and personality on angling
vulnerability in nest guarding males showed that males guarding nests containing more eggs were
significantly more vulnerable to angling (Table 19). Additionally, each of the personality traits was
positively correlated with angling vulnerability. However, only the safe and familiar context trait and
boldness significantly affected angling vulnerability (Figure 16). Overall, 31% of the variation in nest
guarding male angling vulnerability was determined by the number of eggs being guarded and a male’s
boldness.

DISCUSSION
The results of this study demonstrate that personality can affect angling vulnerability in a range
of angling contexts. Further, the personality trait that affects angling vulnerability depends on the
specifics of the angling context. In the mesocosm context, bolder bass, and specifically those that
hesitated less before foraging in the behavioral assays, were more vulnerable to angling. Thus, it

151

appears that bass struck at the bait in this angling context primarily to forage. In the outdoor pond
context, bass that were more aggressive towards the mirror in the laboratory were more vulnerable to
angling. Thus, it appears that bass strikes in this context were primarily the result of aggressive
responses to the bait. In the outdoor pond context where casts were made directly onto bass nests, the
activity measure in the safe and familiar context had the greatest effect on nest angling vulnerability. I
predicted that strikes at the bait were likely made by bass to protect offspring and as a result, male bass
that were more aggressive in the mirror-test context would be more vulnerable to nest angling. It
appears that strikes were in fact made to protect offspring as bolder males were also more vulnerable to
angling. However, nest angling vulnerability may be determined more by parental diligence as opposed
to overt aggression.
This study demonstrates for the first time that the selective capture of fish by recreational
angling may be dependent on the specifics of the angling context that takes place. This is important to
conservation biologists as the relationship between personality and vulnerability to recreational and
commercial harvesting practices may result in selection pressures that result in fisheries-induced
evolution (Sutter et al. 2012; Philipp et al. 2014; Mittelbach et al. 2014). If personality selection in any of
these angling contexts were to result in fisheries-induced evolution, fished populations would almost
certainly experience a decline in catchability on a population level scale, a scenario that would be
undesirable for recreational anglers (Philipp et al. 2009; Dorow et al. 2010). To date, the majority of
studies on angling vulnerability in fish have focused on life-history or physiological correlates of angling
vulnerability, such as growth rate and resting metabolic rate (Cooke et al. 2007; Redpath et al. 2009).
The current study is set apart from others in that the direct target of selection was investigated.
However, as in prior studies, the current study also found that other factors, in addition to personality
traits, were important for determining angling vulnerability.

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Larger bass were significantly more vulnerable to angling in the outdoor pond context. Why
length may affect angling vulnerability in this context but not the other two is not immediately clear.
However, one possibility is that larger bass may be capable of accelerating towards the lure at a greater
speed and as a result, strike at the lure before their smaller conspecifics. In the mesocosm context, bass
tended to hesitate before striking at the lure and the length of hesitation was dependent on boldness.
Thus, any advantage in swimming speed that length may entail would likely not affect angling
vulnerability in this context. In the angling context focusing on nest guarding males, angling attempts
targeted individual males. Therefore, swimming speed would not be expected to affect angling
vulnerability in this context.
The number of eggs in a male’s nest affected nest guarding male angling vulnerability. This
result is consistent with the hypothesis that the value of a nest to a nest guarding male increases with
the number of eggs it contains. Thus, we would expect males to more diligently protect nests that
contain more eggs. Such a relationship between nest size and nest-guarding male angling vulnerability
has the potential to have major consequences for populations that are heavily fished during the nesting
season. The selective removal (either through harvest or temporary removal resulting from catch-andrelease) of individuals with the greatest potential for high reproductive success has been hypothesized
to have strong effects on individual fitness and population dynamics (Philipp et al. 1997; Suski and
Philipp 2004; Sutter et al. 2012). Thus, in response to either harvest or catch-and-release nest angling,
fish in exploited largemouth bass populations would generally be expected to evolve traits that reduce
their exposure to nest angling. Such an evolutionary response could also reduce the level of diligence
that males display when protecting their nests. The potential ramifications of this adaptive response to
angling on recruitment would of course depend upon the amount of harvest mortality, or for catch-andrelease fisheries, the intensity of catch-and-release angling of male bass on nests (Enberg et al. 2010).
Angling of nest-guarding bass has been a selective force acting on many bass populations in North

153

America for several decades. Thus, many populations are likely to already contain fish that are less
vulnerable to capture than non-fished populations (Sutter et al. 2012; Philipp et al. 2014). If evolutionary
changes in personality and life history prove to reduce recruitment, then management strategies
designed to reduce or even remove the underlying selective pressure (angling nest-guarding male
largemouth bass) may need to be implemented.

ACKNOWLEDGEMENTS
I thank Gary Mittelbach for his many insightful comments and suggestions on earlier versions of this
manuscript. Additionally, I thank Cristopher Mirque and Matthew Bach for their help during parts of the
data collection process. Grants from the US National Science Foundation (IOS-1311455), Sigma Xi,
Kellogg Biological Station, and the Zoology Department at Michigan State University supported portions
of this research.

154

APPENDIX

155

Table 17. Linear regressions of the effect of length and personality on angling vulnerability in angling experiment 1 (mesocosm context). Each
model has 30 degrees of freedom. Angling vulnerability = Length + Personality + Length:Personality.
Personality Trait

Intercept

Personality
Coefficient
0.106

Length:PT
Coefficient
0.310

R-squared

0.045

Length
Coefficient
-0.082

SFCT_1
SFCT_2

-0.029

-0.180

-0.025

0.206

0.07

MTCT_1

-0.002

-0.147

0.107

-0.069

0.04

MTCT_2

0.007

-0.310

0.125

-0.458 *

0.14

FPCT_1

-0.177

-0.109

0.351 *

-0.571 **

0.34

FPCT_2

-0.317

0.031

0.636 **

-0.677 **

0.31

Boldness_1

-0.043

-0.136

0.207

-0.487 *

0.23

Boldness_2

-0.090

-0.172

0.387 *

-0.443

0.17

0.10

Note: SFCT = Safe and familiar context trait, MTCT = mirror-test context trait, FPCT = food and predator present context trait. _1 = scores from
the assays conducted prior to the angling experiment. _2 = scores from the assays conducted after the angling experiment. * = P ≤ 0.05;
** = P ≤ 0.005.

156

Table 18. Logistic regressions of the effect of length and personality on angling vulnerability in angling experiment 2 (outdoor pond context).
Each model has 198 degrees of freedom. Vulnerable to Angling (Yes/No) = Length + Personality + Length:Personality. For comparison, the null
model deviance was 253.80.
Personality Trait

Intercept
-0.843 **

Length
Coefficient
0.846 **

Personality
Coefficient
-0.192

Length:PT
Coefficient
0.256

Residual Deviance
from model
227.81

SFCT
MTCT

-0.780 **

0.899 **

0.393 *

0.508

222.08

FPCT

-0.759 **

0.860 **

0.196

0.089

227.77

Boldness

-0.781 **

0.87 **

0.284

0.203

224.36

Note: SFCT = Safe and familiar context trait, MTCT = mirror-test context trait, FPCT = food and predator present context trait. * = P ≤ 0.05;
** = P ≤ 0.005.

157

Table 19. Linear regressions of the effect of length, nest egg count, and personality on angling vulnerability in angling experiment 3 (nest
guarding males). Angling vulnerability = Length + Nest Egg Count + Personality + Length:Personality + Egg Count:Personality. Each model has 30
degrees of freedom.
Personality
Trait
NECT

Intercept

Egg count
Coefficient
0.470 *

Personality
Coefficient
0.274

Length:PT
Coefficient
0.181

Egg count :PT
Coefficient
-0.288

R-squared

0.058

Length
Coefficient
-0.265

SFCT

0.048

-0.293

0.453 *

0.405 *

0.186

-0.375

0.29

MTCT

0.002

-0.366

0.540 *

0.149

0.010

-0.192

0.22

FPCT

0.036

-0.317

0.519 *

0.223

0.128

-0.231

0.24

Boldness

0.057

-0.308

0.479 *

0.253 *

0.066

-0.213

0.31

0.21

Note: NECT = novel environment context trait, SFCT = Safe and familiar context trait, MTCT = mirror-test context trait, FPCT = food and predator
present context trait. * = P ≤ 0.05.

158

Figure 14. The effect of initial boldness, length, and the interaction between them on angling vulnerability in a mesocosm experiment. The
circles represent individuals and the lines from the circles to the plane indicate individual residual values.

159

Figure 15. a) Average length, b) average mirror-test context trait, and c) average boldness of bass that
were caught and those that were not caught in an outdoor pond. Error bars indicate the standard error
of the mean.
160

Figure 16. Effects of a) length, b) nest egg count, c) the safe and familiar context trait, and d) boldness on angling vulnerability of nest guarding
male bass in an outdoor pond. Solid black lines indicate significant relationships (b-d) while dashed lines do not.
161

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