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SAGE-Hindawi Access to Research
International Journal of Evolutionary Biology
Volume 2011, Article ID 321729, 15 pages
doi:10.4061/2011/321729
Research Article
Repeatability and Heritability of Behavioural Types in
a Social Cichlid
No´
emie Chervet, Markus Z¨
ottl, Roger Sch¨
urch, Michael Taborsky, and Dik Heg
Department of Behavioural Ecology, Institute of Ecology and Evolution, University of Bern, 3032 Hinterkappelen, Switzerland
Correspondence should be addressed to Dik Heg, dik.heg@iee.unibe.ch
Received 11 December 2010; Accepted 28 February 2011
Academic Editor: Kristina M. Sefc
Copyright © 2011 No´
emie Chervet et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
Aim. The quantitative genetics underlying correlated behavioural traits (“animal personality”) have hitherto been studied mainly
in domesticated animals. Here we report the repeatability (R) and heritability (h2) of behavioural types in the highly social cichlid
fish Neolamprologus pulcher.Methods. We tested 1779 individuals repeatedly and calculated the h2of behavioural types by variance
components estimation (GLMM REML), using 1327 offspring from 162 broods from 74 pairs. Results. Repeatability of behavioural
types was significant and considerable (0.546), but declined from 0.83 between tests conducted on the same day, to 0.19 on tests
conducted up to 1201 days apart. All h2estimates were significant but low (e.g., pair identity h2=0.15 ±0.03 SE). Additionally, we
found significant variation between broods nested within the parent(s), but these were not related to several environmental factors
tested. Conclusions. We conclude that despite a considerable R,h2in this cichlid species is low, and variability in behavioural type
appears to be strongly affected by other (non)genetic effects.
1. Introduction
Individuals within animal populations often differ consis-
tently in how they cope with environmental and social chal-
lenges, for instance with some individuals typically reacting
shy and nonaggressively to such (novel) challenges and oth-
ers reacting bold and aggressively [1–3]. Often, these individ-
ual differences are referred to as “behavioural types” or “cop-
ing styles” (e.g., shy, bold), and behavioural traits may covary
amongst each other (e.g., shy individuals are also nonaggres-
sive and nonexplorative, whereas bold individuals are more
aggressive and explorative, e.g., [4]). Correlated behavioural
trait values on the population level are commonly denoted
as animal personalities, behavioural syndromes, or tempera-
ments [5]. Central questions in animal personality research
are (i) whether differences in behavioural types have a
genetic basis, that is, whether they are heritable; (ii) whether
and to what extent individuals remain consistent in their
behavioural traits over time, that is, whether behavioural
responses of individuals are repeatable [6–8].
The genetic components affecting the expression of
different personalities have been well explored in humans
(see reviews e.g., [9–15]), domesticated animals [16,17],
and animal model systems [18–20]. The evolutionary eco-
logical factors responsible for the evolution of variation in
behavioural types remains somewhat enigmatic and difficult
to explain in natural animal populations, despite recent
theoretical advances showing how life-history tradeoffs
might generate and maintain such variation [21,22]. In
principle, consistent individual differences and covariation
in behavioural traits are a paradox in evolutionary biology,
particularly if such differences have a genetic basis. Standard
theory would expect each individual to flexibly adjust their
behaviour to the environment. For instance, in a predator
rich environment each individual should devalue future
fitness in favour of current fitness and adjust their behaviour
accordingly (e.g., hide more and be less explorative).
In the human psychology literature it has been acknowl-
edged that although personality differences have a genetic
basis [9–15], other (social) factors might impinge upon
and alter the expression of human behavioural types over
a lifetime, including for instance life events (like the death
of a partner, [23]). If personalities are truly fixed over
life and can be accurately measured by using standardized
SAGE-Hindawi Access to Research
International Journal of Evolutionary Biology
Volume 2011, Article ID 321729, 15 pages
http://dx.doi.org/10.4061/2011/321729
2 International Journal of Evolutionary Biology
questionnaires (e.g., [24]), or by using standardized obser-
vational assessments (e.g., [25–28]), or behavioural tests
(as used to determine personalities in many invertebrates
and vertebrates, see [2]), the repeatability of behavioural
types should approach one. Clearly, this is not the case in
humans ([29]; where it increases from 0.31 in childhood
to a plateau of 0.73 beyond 50 years of age: [30]) and
in most animal studies [7], which led to the proposition
to incorporate behavioural reaction norms into the ani-
mal personality concept [6]. By incorporating behavioural
reaction norms, animal behaviour can be analysed using
standard game theory, where behavioural strategies may
be governed by internal “state” (e.g., body condition, sex,
status, and reproductive activity), sometimes resulting in
alternative strategies (e.g., depending on morphology or
age), but where these strategies and behaviours are not
necessarily fixed for life (i.e., without the need to assume
the existence of animal personalities). In fact, this has been
the major criticism of animal personality research: if the
long-term stability (“repeatability”, R)isnotproveninany
study population, why not assume that the current variability
between individuals reflects the current variability in “states”
of the individuals tested? Using a meta-analysis, Bell and
others showed that the repeatability estimate significantly
declined with the time interval between the different tests
[7]. As the number of long-term repeatability studies in
animal personality research is still very low [31]andbiased
towards domesticated animals [32–42], our first target is
to test for the long-term repeatability of behavioural types,
using descendants of a wild population of a cooperatively
breeding cichlid, Neolamprologus pulcher.
We use the cichlid N. pulcher as model species, where
individuals have been shown to differ consistently in
behavioural traits (across the bold-shy continuum) in both
the field [43] and the laboratory (stocks derived from
the same field population, [4,39,44–46]). In addition,
males and females have been shown to remain relatively
stable in trait values from the juvenile stage (when they
are the small, subordinate helpers of an adult pair) to
early adulthood (when they are large, subordinate helpers
and reproductively mature [39]). Behavioural types in this
species may also influence sociality, reproduction [46],
and helping behaviour [39,44,47]; and also alloparental
brood care differs consistently between female helpers [47].
The major hypothesis proposed to explain this variabil-
ity in behavioural types suggests that subordinates trade-
offeffort to gain social dominance inside versus outside
their territory, which either selects for distinct life-history
strategies (e.g., nonexplorative, helpful, and risk-aversive
individuals opt for dominance inside their group’s territory,
whereas explorative, bold, and aggressive individuals opt for
dominance outside their group’s territory, which involves
early dispersal and independent breeding [39,48]) or for
diverse ontogenetic trajectories in behavioural types (e.g.,
young fish being risk aversive whereas older fish being risk
prone). Here we expand the time frame of standardised tests
to encompass the lifetime of these fish.
The second target of this study has been to estimate
the genetic variance underlying phenotypic variation in
personality traits in N. pulcher (“heritability” h2[49,50]),
and to compare estimates of Rand h2. Repeatability R
often sets the upper limit to the heritability of a trait,
and both measures are correlated in comparisons across
species or populations, if the phenotypic variances in the
compared units are governed by similar processes involving
additive genetic variance. Any species or population showing
a high heritability in a behavioural trait should also show
a high repeatability in this trait (as genes are more likely
to be involved in the determination of the behaviour).
In contrast, a high repeatability can coincide with a low
heritability, if the behavioural type is based, for instance, on
the (current) internal state of individuals or on their (life-
history) strategy [21]orsocialstrategy[51], which may cause
variation that is largely independent from genetic effects.
Maternal or paternal effects, maternal additive genetic effects
and genotype ×environment interactions may also yield
discrepancies between the heritability and the repeatability
estimates (e.g., with heritability exceeding the repeatability,
[52]). Both low repeatability and low heritability would
indicate that the population exhibits no animal personalities,
particularly if the repeatability diminishes over time.
In Neolamprologus pulcher, personality traits (such as
boldness, aggressiveness, and propensity to explore) are
consistently different between individuals (see references
above) and related to two major life-history decisions:
whether to help and whether to disperse. Furthermore, these
traits are not related to growth rate in fish kept singly [39],
but if living in groups consisting of members with divergent
personality types, shy fish were found to grow quicker in
body length than bold fish [53]. Studies of personalities
are particularly interesting in social species like cichlids and
primates [54], as they may bear similarities to the human
personality axes which incorporate significant aspects of
human behaviour and sociality (e.g., “OCEAN”: Openness,
Conscientiousness, Extraversion, Agreeableness, but with the
possible exception of Neuroticism [24,55–58]). Human and
animal personality differences may be governed by similar
differences in (neuro)physiological responses to environ-
mental challenges and stressful situations [23,59–62]. In
this study we first estimated the repeatability of behavioural
types based on a combined score of boldness, aggressiveness,
and exploration propensity by comparing test results of
individuals obtained successively with intervals ranging from
0 to 1201 days (which approaches the maximum life span
of this species: see [63]). In a second step we estimated the
heritability of these same behavioural types using parent(s)-
offspring regressions and variance component estimations
from offspring derived from different broods of the same
pair.
2. Methods
2.1. Study Species. Descendants of wild caught Neolampro-
logus pulcher (from wild animals collected in 1996, 2006,
and 2009 near Kasalakawe, Zambia, so-called three different
“stocks” and their crossings) were used for this study and
tested in the years 2005–2008 and 2010. These fish are
well-studied cooperative breeders [64], endemic to Lake
International Journal of Evolutionary Biology 3
Tanganyika where they live in breeding groups composed
usually of a dominant breeder male, one to several breeder
females and some helpers [65]. All fish were fed twice a
week with fresh food (JBL Cyclops spp., shrimp, Artemia
spp., mosquito larvae) and the other five days with JBL De
Novo Lake Tanganyika cichlid flake food (except for some
missing days due to absence). This is the standard feeding
regime for all cichlid fish at our laboratory. During 2010 we
additionally fed all individuals on six to seven days per week
with fresh small food items (Artemia freshly hatched eggs and
JBL Cyclops spp., the latter replaced with Daphnia spp. when
all offspring of all broods had grown beyond 10 mm standard
length). This was done to ensure that all offspring received
enough food to grow proficiently and to reach testing age.
Cichlids were kept in tanks within climatised rooms (24–
29◦C, lights on between 08:00–21:00 h).
2.2. Experimental Setup. The experimental setup and tests
performed in 2005 and 2006 were reported in [39](repeated
tests of the same 36 individuals up to 150 days apart by
Roger Sch ¨
urch), tests performed in 2007 were reported in
[4] (repeated tests of the same 272 individuals up to 53
days apart by Susan Rothenberger). In 2008 (unpublished)
repeated tests were performed of 32 individuals by Liana
Lasut, Est´
ee Bochud, and Sebastian Keller (using the same
setup as [4]), and 10 individuals retested in 2010 by No´
emie
Chervet and Dik Heg). These data were used to calculate
the repeatability of behavioural types for time intervals of
up to 1201 days after the first test was done. Individuals
were marked between 2005 and 2008 with colour marks
or fin clips and kept in breeding pairs, or fitted with
PIT transponders and kept in aggregation tanks up to the
moment of re-testing in 2010.
In September 2009 new breeding pairs were established
and allowed to breed without monitoring their clutches (all
“control pairs”), their offspring were tested without any
information about the clutches (and thus offspring were up
to 6 months of age). Between March and August 2010 these
pairs were augmented with more new breeding pairs that
were allowed to breed as follows.
Control pairs (n=19 pairs) were kept in 89 or 93
litre tanks (length ×breadth ×height cm, height water
level cm: 60 ×40 ×40 cm, 37 or 50 ×50 ×40 cm, 37 cm;
resp.) and one clutch was left to hatch inside their tank
(usually the first clutch), and these offspring remained there
until personality testing (Figure 1(a), clutch treatment “with
parents”, see below for more details). All other clutches were
removed on the day of egg laying and put separately to
hatch in a 24-litre tank (40 ×25 ×25 cm, 24 cm; clutch
treatment “isolation”, see below for details). As pairs may
produce a clutch about every other week [66], removal of the
clutches ensured that we knew the identity of the offspring
if they remained with their parents. However, some clutches
remained undetected and were discovered after hatching and
in such cases we removed all the offspring to an isolation tank
as soon as possible. If the parents had very large offspring
in their tank from a previous brood, we allowed them to
hatch and keep a second clutch, as the offspring from the two
broods could be easily distinguished according to their large
size difference (this occurred only in 2 pairs). In 4 pairs a pair
member died when already offspring were present and these
offspring were removed and stored in a separate tank until
personality testing, and the dead partner was replaced with a
new partner.
Cross-breeding pairs (n=38 pairs that produced at least
one clutch, includes 17 pairs from [46]) were kept in 54 or 58
litre tanks (60 ×30 ×33 cm, 30 cm; or 60 ×30 ×35 cm,
32 cm). However, they included repeated measures of the
same female with different males, and vice versa, so in total
19 different females and 20 different males were involved.
The pairs were left together to breed for one and a half
months. In between they were remeasured and reallocated
to different mates. In total, we attempted to mate each
individual with 5 different mates, but were only successful
(i.e., the pair produced at least one clutch in 1.5 months) for
amaximumof4different mates (females: 7 ×1, 8 ×2, 1 ×3
and 3 ×4 mates; males: 7 ×1, 9 ×2, 3 ×3and1×4mates),
partly because we lost and had to replace 4 individuals
intermittently. All clutches were removed into 24-litre tanks
(Figure 1(a), clutch treatment “isolation”), penultimate
clutches were used for the clutch treatment “with parents” (in
their 54 or 58 litre tanks) or “with foster parents” (see below),
to increase the sample sizes for these latter two treatments.
Cross-fostering pairs (n=14 pairs that produced at least
one clutch, in one pair their single clutch did not hatch)
were kept in 54 or 58 litre tanks (60 ×30 ×33 cm, 30 cm;
or 60 ×30 ×35 cm, 32 cm). Their first clutch was removed
into a different empty 54 or 58 litre tank (Figure 1(a),clutch
treatment “cross-fostering”, see below for details), however,
if this clutch did not hatch, the second clutch received the
same treatment. All other clutches were removed into the
treatment “isolation” (24 litre tank). Pairs kept producing
clutches until they were transferred as foster parents to a
foster clutch (see Clutch treatments below).
2.3. Clutch Treatments. All pairs were checked every day
for new broods. Upon detection of a new clutch, we
commenced with a 15 min brood care obser vation, counting
the frequency of cleaning the eggs (each mouth movement
counted) and fanning the eggs (aerating the eggs by vibrating
with body and fins [67]) for the female and the male sepa-
rately [47,66,68]. The minimum distance to the eggs in cm
(with 0 indicating inside the pot(s) containing the eggs) was
also noted for the female and male separately. Unfortunately,
pairs could also lay clutches under/behind the filter or on
the aquarium walls, and these clutches were sometimes not
detected until the fry hatched (which occurs 2 to 3 days
after egg laying). These cases account for some missing data
on clutch size, average egg mass, hatching success (but not
the number of hatched offspring, as fry were immediately
counted), and brood care behaviour. After the brood care
observation, the pot was removed and we counted the
number of eggs (clutch size) and measured the average dry
egg mass (by sampling up to 5 eggs per clutch and weighing
them after 32 h drying in a 70◦C oven). Data on brood care,
clutch size, and egg mass will be treated in detail elsewhere.
The broods in the treatment “with parents” broods
were then immediately placed back with their parents
4 International Journal of Evolutionary Biology
(days)
With parents
Brood care (15min)
Clutch size
Egg mass
065 120 150
Isolation
With fosters
(a)
50 cm
30 cm
Aggression test
Mirror (46 ×15 cm)
Air stone
(b)
30 cm
Boldness test
Novel object
50 cm
(c)
65 cm
Home
compartment
130 cm
Exploration compartment
Removable
opaque partition
Exploration test
(d)
Figure 1: Treatment of the broods and experimental setup of the three behavioural tests (black fish show the starting position of the focal
individual in each test). (a) Offspring remained with their parents (treatment “with parents”); or were isolated and raised only together with
their siblings (treatment “isolation”); or were isolated, raised together with their siblings for 65 days, and from this day onwards received
a foster pair (“with fosters”). Six offspring were removed for behavioural testing on days 120 and 150 each (or fewer offspring if less than
6offspring were still alive on day 120, and fewer offspring if less than 6 not yet tested offspring were still alive on day 150). Offspring
were measured and moved singly to a 40-litre tank depicted in (b, c). After two days acclimatization, each offspring was tested. Note that
offspring were permanently removed to avoid confusion with previously tested offspring. (b) Setup of the aggression test, where aggressive
displays/attacks were scored towards the mirror (either placed left or right), and hiding time inside the pot was measured. (c) Setup of
the boldness test, where latency and shortest distance moved to the novel object was scored (object placed left or right). (d) Setup of the
exploration test, the test started by removing the opaque partition, and latencies plus visits to 10 pots were measured. Note that the home
compartment was either on the left or the right and pots were shifted accordingly, visits to the home compartment pot were not counted.
Offspring and parents were similarly tested according to (b–d).
(Figure 1(a)). The broods in the treatments “isolation”
and “with foster-pair” broods were permanently removed
(Figure 1(a), the pair received a new clean flower-pot halve)
and placed into an isolation net inside a separate 24-litre tank
(“isolation”) or 54/58 litre tank (“with foster-pair”), and the
eggs were incubated using an air stone. Approximately five
days after hatching they were released from their isolation
net. “Isolation” broods were kept in their 24-litre tanks with
their siblings until 55 to 114 days after egg laying, when
they were transferred to a bigger tank (34 to 188 litre) to
accommodate both their size and numbers (as numbers were
highly variable at transfer, ranging between 2 and 67 siblings,
we also used highly variable tank sizes). Two broods with
a single offspring each and three broods with two offspring
each remained in their original tanks, as transfer was not
necessary due to their low number and limitations in the
availability of bigger tanks. “With fosters” brood were kept
together with their siblings in their 54/58-litre tank, until
they received a foster pair from day 65 onwards (Figure 1(a)).
2.4. Body Measurements and Personality Testing. Before the
personality test (on day −2 before testing) or mate exchange
(on day 0 of release with the new mate), each individual
was sexed (external papilla inspection under a dissecting
microscope), measured (standard length SL and total length
TL in 0.1 mm using a dissecting microscope) and weighed
(body mass in mg), and fin clipped for a DNA sample and
for male/female identification within pairs. All offspring
produced in the period September 2009 to March 2010 were
tested in 2010, their parents were tested in March 2010 (5
females had lost their mate before March 2010, so 5 pairs had
missing data for the male parent; 1 male had lost his mate
before March 2010, so 1 pair had missing data for the female
parent). The reasoning for testing all offspring was that they
had experienced a very prolonged time with their parents,
somightbewellsuitedtoserveasabenchmarkforfuture
studies. Offspring produced in the period March to August
2010 were identified by their clutch identifier and clutch
treatment and tested on day 120 since the clutch was laid
International Journal of Evolutionary Biology 5
(Figure 1(a): the six largest siblings, or less if less were alive).
An additional sample of the next 6 largest siblings was taken
for tests on day 150 after clutch production for all “with
parents” treatments, “with foster-parents” treatments, and
the first clutch of the “isolation” treatment (Figure 1(a)).
We were not able to take additional samples for all second
and later clutches of the “isolation” treatments due to time
constraints.
The personality testing procedure has been outlined in
detail in [4,39]. Briefly, boldness and aggressiveness tests
were conducted for each single focal fish inside a 42-litre tank
(Figures 1(b) and 1(c),50×30 ×30 cm; 28 cm water level).
In total, 34 of such tanks were available for testing. Focal fish
were left for two days to acclimate and settle territory around
a single flower pot halve (placed 30 cm from the front glass).
In the aggressiveness test, a mirror was placed along one side
(Figure 1(b)). Here the total time hiding (in seconds) and
aggressive behaviours towards the mirror image were noted:
restrained aggression (frequency of slow approach, fast
approach, head down display, spread fins, s-bending) and
overt aggression (frequency of contact with the mirror, again
5 min total test duration). In the boldness test, a novel object
(Figure 1(c), plastic beetle, plastic funnel, plastic blue half
moon, clay bird, or plastic white cross) was placed in a front
corner (left or right), and the latency to approach this object
(in seconds) plus the closest distance to the object (in cm)
was recorded (5 min total test duration). The exploration test
was conducted in a 400-litre tank, where the fish were left
in a partitioned area with a flower pot half for ten minutes
before testing (Figure 1(d), so-called “home compartment”).
Then the partition wall was removed and the focal fish could
start exploring the unknown part of the tank where ten other
flower pot halves were placed (“exploration compartment”,
Figure 1(d)). Here the time spent moving outside the
pots in any compartment, the latency before leaving the
home compartment (in seconds), and for the exploration
compartment, the latency before entering the first pot, the
number of pots approached, the number of pots entered, and
the number of different pots entered (0–10) were recorded
(again 5 min total test duration). The three tests (boldness,
aggressiveness, and exploration propensity) were conducted
in randomized order. The three tests were repeated one day
later, or rarely on the same day or up to four days later
(due to time constraints and tank constraints). Note that in
2005 and 2006 all three tests were conducted in the 400-litre
tank and the exploration test lasted 10 min (instead of 5min,
observer Roger Sch¨
urch, see [39]). Moreover, due to severe
time constraints, the exploration test could not be conducted
for all focal animals in 2010, as it involved a lot of time lost
in handling fish. See the description of statistical analyses
for details on how we have dealt with these differences in
procedures.
2.5. Statistical Analyses. We used Categorical Principal Com-
ponents analyses CatPCA with two-knot spline transforma-
tions [69] to summarise the three different tests (boldness,
aggressiveness, and exploration propensity) into a single
measure of “behavioural type” (object scores, see also [4]).
To account for the observer effects, each CatPCA was run
separately for each observer (2005-2006: Roger Sch¨
urch
n=216 series of three tests, 2007: Susan Rothenberger
n=1042 series of three tests, 2008: Sebastian Keller/Est´
ee
Bochud/Liana Lasut n=64 series of three tests, bold-
ness/aggressiveness/exploration tests; 2010: Markus Z¨
ottl
n=288 tests, including 264 tests where only aggressiveness
was recorded; No´
emie Chervet n=1412 series of two tests
and Dik Heg n=1268 series of two tests: aggressiveness
and boldness). No´
emie Chervet and Dik Heg also conducted
exploration tests, but these were excluded from the anal-
yses to keep the data amongst the individuals consistent.
This procedure has the advantage that first, all observers
automatically scale to a mean “behavioural type” of zero;
and second, the different test procedures are also scaled
to a mean “behavioural type” of zero (i.e., in 2005-2006
all three tests were conducted inside a 400-litre tank and
the exploration tests lasted 10 min versus in 2007–2010 the
three tests were conducted according to Figures 1(b)–1(d)
and always lasted 5 min). This procedure only assumes that
all observers capture more or less the complete variation
in behavioural types present in the population, which is a
reasonable assumption considering the large number of tests
each observer conducted, and that all original variables had
very high correlations both before and after transformations
in the CatPCA, for each observer separately.
Repeatability was estimated using the VARCOMP and
RELIABILITY procedures in SPSS 17 [70], by extracting the
variance components and the corresponding intraclass cor-
relation coefficients (=repeatability) by using the Restricted
Maximum Likelihood method (REML). The procedure was
run once for the complete data set using VARCOMP
(Restricted Maximum Likelihood Method REML) and once
foreachtimedifference between the first test and the next
test(s) i, where individuals were tested up to 6 six different
times using the RELIABILITY procedure (which was easier to
use in the latter analyses for data management reasons). Time
differences between test iand the first test was calculated in
days and the repeatability was calculated for days =0(test
iconducted on the same day as the first test), 1, 2, 3, 4, 15
(between11and20days),25(between21and30days),35
(between31and40days),45(between41and50days),55
(between 51 and 60 days), 90, 120, 150, 175 (between 151
and 200 days), 225 (between 201 and 250 days), and 930
days (between 732 and 1201 days). To estimate the change
in repeatability over time, these 16 estimates of repeatability
(from 0 to 732–1201 days) were regressed against ln (days +
1) weighted by their sample size (weighted linear regression).
Similarly, change in the test scores (test iminus the first
test) were analysed by regressing this difference against ln
(days + 1).
Heritability was estimated using (1) the mid-parent
versus mid-offspring weighted regression slope (weighted
by the square root of the number of offspring tested
[71]). (2) The intraclass correlation coefficients derived from
the variance components extracted using the VARCOMP
procedureinSPSS17forrandomeffects of the pair identity,
mother identity, and father identity, respectively, using the
REML method. These estimates were verified by using the
minimum norm unbiased estimator method, using both
6 International Journal of Evolutionary Biology
Days between test iand test 1
0 200 400 600 800 1000 1200
Repeatability
−1
−0.5
0
0.5
1
(a)
Days between test iandtest1
0 200 400 600 800 1000 1200
Change in score
−4
−2
0
2
4
(b)
Figure 2: Repeatability of behavioural types significantly declined over time. (a) Pairwise repeatability from the test results (behavioural
type test iversus behavioural type first test), from two test series conducted on the same day 0 (n=44), 1 (n=1435), 2 (n=277), 3 (n=
18), 4 (n=45), 11–20 (n=7),21–30 (n=101), 31–40 (n=101), 41–50 (n=63), 51–60 (n=48), 90 (n=36), 120 (n=36), 150 (n=
36), 151–200 days (n=7), 201–250 days (n=15) and 732–1201 days apart (n=18), respectively. The two low sample sizes of 7 are indicated
with white circles, but do not affect the regression line, as the line was fitted weighing by the sample size. (b) Pairwise changes in the test
series results over time (behavioural type test iminus behavioural type first test, n=2501). Note the maximum time difference between two
tests of 1201 days. See the text for the regression line.
the priors 0 or 1 (MINQUE(0) or MINQUE(1) method:
see [70]), and since the MINQUE estimates were virtually
identical to the REML estimates only the latter are given.
Finally, fixed effects on the brood level were tested by General
Linear Mixed Models, using as random effects pair identity
and brood identity nested within pairs (and extracting
the variance components accordingly). The following fixed
effects were tested: female stock (1996, 2006, 2009), male
stock (1996, 2006, 2009), treatment of the brood (with
parents, with foster parents, isolated), volume of the tank
in litres (both before and after transfer, if offspring were
not transferred volumes were identical), temperature of the
tank in degrees Celcius (both before and—if this applies after
transfer), and body size of the focal offspring (SL mm). Note
that the fixed effects were measured on the brood identity
level, and therefore varied between broods within pairs, and
that the offspring varied in body sizes (both within and
between broods).
Due to replacement of dead mates, we ended with a total
sample size of 74 pairs, 162 broods, and 1327 offspring tested
for the heritability analyses (from 49 individual females and
50 individual males), in one pair the mother was not tested
and in three pairs the father was not tested.
3. Results
3.1. Categorical Principal Component Extraction of Behav-
ioural Types. In total 1779 individuals were tested two to six
times for their behavioural traits (on average 2.41 tests per
individual or 4290 tests in total). Categorical Principal Com-
ponents analyses were run for each observer separately, and
in each case a single factor was extracted with an Eigenvalue
higher than 1 explaining a high proportion of the correlated
behaviours in the one to three tests conducted (Table 1). The
extracted factor scores were saved as the “behavioural type”
of the individual in each test (for the repeatability analyses)
or averaged per individual over all their tests as “behavioural
type” (for the heritability analyses).
3.2. Repeatability of the Behavioural Types. VA R C O M P
analysis (REML) showed significant repeatabilities of the
behavioural types (n=4290 tests of 1779 individuals): the
variance attributed to the individuals was 0.5495, the error
variance was 0.4576, which gives a repeatability (intraclass
correlation coefficient) of 0.5495/(0.5495 + 0.4576) =0.5457
(±0.0149 SE, standard error of the estimate). However, by
comparing the test results pairwise with the first test result
over time (from 0 days between two tests up to 732–1201
days between two tests) it became clear that the repeatability
Rsignificantly declined over time (Figure 2(a); regression
analysis weighted by sample size: R=0.830 ±0.002 −
0.093 ±0.001 ×ln[daysbetweentests+1];F=5864.7, P<
.001,R2=0.72, n=16 pairwise Restimates, ±SE). Both
the intercept and the slope of this regression line (depicted in
Figure 2(a)) were significantly different from zero (t=340.1
and −76.6, resp., both P<.001).
Although the repeatability changed over time, the actual
behavioural type test scores changed very little over time
(Figure 2(b)). On a short-term basis, individuals became
bolder, more aggressive, and explorative compared to their
first test score, but this difference to the first test score rapidly
diminished over time and approached the “no difference”
(marked by the red line in Figure 2(b):y=0). These
changes were modeled with a regression analysis (black line
in Figure 2(b):changeinscore=0.442 ±0.027 −0.065 ±
0.012 ×ln[days between tests + 1]; F=29.1, P<.001,
International Journal of Evolutionary Biology 7
Tab le 1: Categorical Principal Component results for the behavioural testing, for each observer separately (in brackets the year(s) when the
tests were conducted). The variance accounted for is represented by Cronbach’s alpha, and the Eigenvalue is given (% explained variance in
brackets). In each case a single factor score was extracted, and used to characterize the behavioural type of the focal individuals on a testing
day (one test series), used for the repeatability analyses. Scores were then averaged per individual for the heritability analyses (scores from
two to six test series averaged). Tests used for Categorical Principal Component extraction: B =boldness, A =aggression, E =exploration.
ntest series Tests used per series Cronbach’s alpha Eigenvalue
R. Sch¨
urch (2005-2006) 216 B, A, E 0.91 4.95 (61.9%)
S. Rothenberger (2007) 1042aB, A, E 0.94 6.65 (60.5%)
E. Bochud/S. Keller/L. Lasut (2008) 64 B, A, E 0.94 6.93 (63.0%)
M. Z¨
ottl (2010) 288bA 0.85 2.30 (76.7%)
N. Chervet (2010) 1412 B, A 0.90 3.53 (70.4%)
D. Heg (2010) 1268cB, A 0.89 3.49 (69.7%)
aIncludes 72 individuals that were subjected to an additional test series following the procedure of Sch¨
urch and Heg [39] in the 400-litre tank, analysed
separately with CatPCA: Cronbach’s alpha =0.93, Eigenvalue =6.48 (58.9%).
bIncludes 64 individuals for which also the boldness test was conducted, analysed separately with CatPCA: Cronbach’s alpha =0.92, Eigenvalue =3.75 (75.0%).
cIncludes 8 test series were only aggressiveness was scored and analysed separately with CatPCA Cronbach’s alpha =0.86, Eigenvalue =2.36 (78.6%).
Tab le 2: Descriptive statistics of the offspring tested.
Parameter nMean SD Minimum Maximum
Treatment of the brood 1327 nwith parents: 419, with foster parent: 91, isolation: 817
Mother stock 1327 n1996: 1031, 2006: 199, 2009: 97
Father stock 1327 n1996: 1166, 2006: 64, 2009: 97
Tank volume litrea1327 47.87 28.63 24d93
Tank volume litreb1327 88.45 48.13 24d188
Tank temperaturea1219 27.17 1.22 24.25 29.50
Tank temperatureb1219 26.58 0.87 24.25 28.30
Offspring body size SL (mm)c1327 24.11 10.27 7.0 77.0
Offspring behavioural typee1327 −0.01565 0.87857 −2.20393 1.49879
nOffspring without missing values 1219
Volume and water temperature of the offspring raising tanks: abefore and bafter transfer.
cBody size at personality testing.
dAll clutches were produced by pairs in 54-to 93-litre tanks, but eggs and offspring from the treatment “isolation” were incubated and raised from the day of
egg laying onwards inside 24 litre tanks and later transferred to larger tanks (see information given on tank volumes after transfer).
eOffspring behavioural type computed as the average of the average score per offspring—behavioural type-from the Categorical Principal Component analysis.
Note that each offspring was scored at least twice (at least two test series of boldness test, exploration test and aggression test).
R2=0.012, n=2501, ±SE of the estimates, both the inter-
cept and the slope of this regression line were significantly
different from zero: t=16.3and−5.4, resp., both P<.001).
3.3. Heritability of Behavioural Types. The raw data of the
offspringbehaviouraltypescoresaregiveninFigure3
and descriptive data are provided in Table 2. First, we
estimated heritability using weighted regression equations
(weighing the regression analysis by offspring number;
Figure 4,Table2): that is, the mid-parent versus mid-
offspring behavioural types (Figure 4(a)), mother versus
mid-offspring behavioural types (Figure 4(b)), and father
versus mid-offspring behavioural types (Figure 4(c)). Her-
itabilities were significant but low for the mid-parent and
mother versus offspring regressions, and nonsignificant for
the father-offspring regression (Table 3). Moreover, the
heritability estimated from sibling comparisons was high and
significant (last row in Table 3).
We should like to point out that the regression approach
is inferior to the variance components method: first, because
the regression approach assumes the behavioural type of
the parents is measured without error; second, because
the mixed nature of the data can be better accommodated
by the variance components (using the REML method)
and this method can be extended to estimate fixed effects
(GLMM REML method, see below); third, because the
above analyses suggest strong brood identity effects (last row
of Table 3), which should be estimated as a random effect
nested within pair identity effects (again using the GLMM
REML method). We therefore recalculated heritability using
the GLMM REML, once with the pair identity or parent’s
identity (female or male) as random effects (first three rows
in Table 4) and once by adding also a brood identity nested
within pair identity as random effects (last three rows in
Table 4). Heritability estimates were all significant and now
slightly larger than the previous estimates (cf. Table 4with
Table 3).
8 International Journal of Evolutionary Biology
Tab le 3: Heritabilities h2of offspring behavioural type using the weighted regression equation approach for parents versus offspring
(weighing the mid-offspring behavioural type by the square root of the number of offspring tested) and the one-way ANOVA approach
for siblings (with brood identifier as a random factor).
Comparison npairs or parent, noffspring MS df,errordf F Estimates h2±SE
Intercept ±SE Slope ±SE
Midparent-offspring 70, 1272 0.95 1, 276 8.58∗∗ −0.010 ±0.024 ns 0.117 ±0.040∗∗ 0.12 ±0.04
Mother-offspring 49, 1318 2.10 1, 283 12.46∗∗∗ 0.008 ±0.025 ns 0.095 ±0.027∗∗∗ 0.19 ±0.03
Father-offspring 50, 1281 0.07 1, 279 0.44 ns −0.007 ±0.025 ns −0.019 ±0.028 ns 0.00 ±0.03
Siblings 162a, 1327 1.90 161, 1165 3.08∗∗∗ −0.004 ±0.040 ns 0.41 ±0.03
aNumber of broods.
ns: nonsignificant, ∗P<.05, ∗∗P<.01, ∗∗∗ P<.001.
In total 74 pairs with 162 broods were tested (in one pair the mother was untested for behavioural type and in three pairs the father was untested for
behavioural type). MS: mean square.
Heritability estimates are twice the slopes for mother-offspring and father-offspring regressions, and twice the intraclass correlation coefficient for siblings.
Tab le 4: Heritabilities h2of offspring behavioural type using the variance components approach (GLMM REML).
Random
effect(s)
npairs or
parent, n
offspring
Variance pair
or parent
Vari a nce
brood
Vari a nce
error
Asymptotic covariance matrixa
h2±SE
Within pair
or parent Within error
Between pair
or parent
versus error
Pair 74, 1327 0.117∗∗∗ 0.653∗∗∗ 0.000787 0.000677 −0.000046 0.1524 ±
0.0316
Mother 49, 1318 0.121∗∗∗ 0.665∗∗∗ 0.001043 0.000697 −0.000035 0.3082 ±
0.0347
Father 50, 1281 0.097∗∗∗ 0.664∗∗∗ 0.000724 0.000716 −0.000036 0.2560 ±
0.0308
Pair+Brood
within paira74, 1327 0.091∗∗ 0.069∗∗ 0.614∗∗∗ 0.000935 0.000641 −0.000002 0.1182 ±
0.0380
Mother +
Brood within
mothera
49, 1318 0.096∗∗ 0.074∗∗∗ 0.616∗∗∗ 0.001099 0.000649 −0.000007 0.2453 ±
0.0405
Father +
Brood within
fathera
50, 1281 0.076∗0.085∗∗∗ 0.605∗∗∗ 0.000871 0.000647 −0.0000002 0.1980 ±
0.0387
aFor brevity, covariances involving the random brood effects are not given (n=162 broods for 74 pairs, n=160 broods for 49 mothers, n=156 broods for
50 fathers).
∗P<.05, ∗∗ P<.01, ∗∗∗ P<.001.
Heritability estimates are twice the intraclass correlations for mother and father effects, standard errors calculated according to [70].
Interestingly, brood identity random effects remained
significant when nested within their parent(s) (last three
rows in Table 4). This suggests siblings from the same
brood shared a common (environmental) effect on their
behavioural type. To explore potential shared effects, we
added single fixed effects to a base model containing random
effects of pair identity and brood identity nested within pair
(Table 5). However, none of these effects significantly affected
the behavioural types of the siblings: treatment of the brood,
stocks of their parents, tank volumes and water temperatures
during raising, and also offspring body size at testing were all
clearly nonsignificant (Table 5).
4. Discussion
There are three main results. First, repeatability of behavi-
oural type significantly declined over time, that is, for two
tests conducted on the same day repeatability was 0.83, and
for two tests conducted up to 1201 days apart repeatability
was only 0.19. This time period spans the entire expected
maximum life-span of this species, which has been estimated
to be ca. 1000 days [63]. Second, heritability was low but
significant and depended on the random effect fitted (i.e.,
pair, mother, father, or brood identity). Third, a significant
random effect of brood identity within pair identity suggests
a shared effect on the behavioural types of the broods, which
did not depend on (i) the treatment of the broods, (ii) origins
of female and male stocks, (iii) volumes and temperatures
of tanks used to raise the offspring, and (iv) sizes of the
offspring at testing. These three main findings are discussed
in more detail below.
Temporal and systematic changes in behavioural type
have been reported for various animal populations and
for humans (e.g., [20,33,37,40,72–80]), including our
International Journal of Evolutionary Biology 9
Tab le 5: Fixed effects on offspring behavioural type using the variance components approach (GLMM REML). In the base model only
random effects of pair identity and brood identity nested within pair identity were added. Fixed effects were then tested stepwise for entry into
this base model. See Table 2for offspring sample sizes. Treatments of the brood were “with parents”, “with foster parents”, or in “isolation”.
Stocks were from 1996, 2006 or 2009. Volumes, temperatures, and offspring size are continuous (covariate) effects.
Fixed effect Statistics when entered into base model
df Error df F P
Treatment of the brood 2 100.2 0.54 .59
Mother stock 2 72.8 0.21 .81
Father stock 2 65.5 0.18 .83
Tank volume (litre)a1 123.7 0.25 .62
Tank volume (litre)b1 121.3 0.02 .90
Tank temperature (◦C)a1 112.5 0.30 .58
Tank temperature (◦C)b1 112.8 0.21 .65
Offspring body size (SL mm)c1 440.0 0.29 .59
Volume and water temperature of the offspring raising tanks: abefore and bafter transfer.
cBody size at personality testing.
Pairs (sorted according to mean offspring behavioural type)
−1.5−10−0.5 0.5 1 1.5
−3
−2
−1
0
1
2
1
2
1
2
3
4
5
6
3
4
5
6
1
2
7
Number of offspring tested
0 5 10 15 20 25
Frequency of broods
4
8
12
36
38
44
42
46
48
0
10
40
6
2
Mean offspring behavioral type ±SEM per brood
46
Figure 3: Mean offspring behavioural type per brood (±SEM,
n=162 broods), plotted per pair (pairs sorted by the mean
of their offsprings behavioural types). Legend shows the brood
treatments (black symbols: with parents, grey symbols: with foster
parents, white symbols: in isolation) and the order of the brood
produced (pairs produced up to 7 broods). Inset shows the number
of offspring tested per brood (n=162 broods with total 1327
offspring).
study species [39]. Although repeatability is a central role
in animal (and human) personality research [7], it remains
understudied. Clearly, if the repeatability is very low and
also fluctuates or changes systematically over time, this
would make the interpretation of individual differences
in behavioural type liable to criticism and diminish the
relevance of the underlying genetical effects. In our study,
repeatability diminished strongly over time (Figure 2(a)),
but nevertheless the behavioural type scores between two
tests were quite comparable (Figure 2(b)). If two tests
were conducted only a short time apart (e.g., on the same
day), individuals were typically bolder, more aggressive, and
explorative during the second test. This strongly suggests
a training effect on the test scores of the individuals: a
habituation effect which diminishes over time (see [36]
for a similar example). Accordingly, if the two tests were
conducted widely apart in time, test scores of individuals
were on average very similar to each other. We note as a point
of criticism that the change in repeatability over time was
modeled by us using a simple regression model. However,
it is quite likely (as the data in Figure 2(a) suggest) that
the repeatability actually stabilizes to a level of 0.4 to 0.5
after 150 days between two tests. A “break-point regression”
approach would be a way forward to study this, but would
also need more repeatability data from day 150 onwards. We
urge scientists to study the repeatability of behavioural types
in more depth, as it plays a critical role in the concept of
animal personality research, and we concur that these studies
are particularly lacking in fish [39,74,75,81–85].
We found that the heritability of behavioural type was
ca. 0.15 in N. pulcher, which is a rather low estimate
compared to other studies (see meta-analysis in [16]:
mean =0.31). However, heritability estimates may critically
depend on the variance components which were actually
tested, that is, whether the study design allowed testing for
(permanent) environmental effects, maternal and paternal
effects, and maternal additive genetic effects. Studies in
domesticated animals have shown that many genetic and
nongenetic factors may contribute to behavioural phenotype
of the offspring (e.g., [86–91]). Similarly, we found strong
evidence for shared sibling environmental effects (brood
with pair effects in Table 3) and maternal/paternal effects on
behavioural type (discrepancies between pair versus mother
versus father effects in Table 3). This suggests that an animal
10 International Journal of Evolutionary Biology
Mid-parent behavioral type
−1.5
−1
−0.5
0
0.5
1
1.5
Mid-offspring behavioral type
−2−10 12
(a)
Mother behavioral type
−1.5
−1
−0.5
0
0.5
1
1.5
−2−10 1 2
Mid-offspring behavioral type
(b)
Father behavioral type
−1.5
−1
−0.5
0
0.5
1
1.5
−2−10 12
Mid-offspring behavioral type
(c)
Figure 4: Heritability of offspring behavioural type using the regression approach. Symbol sizes represent the number of offspring tested
per brood (pairs: 1 to 54, n=70, excludes broods were one parent was not tested; mothers: 3 to 100, n=49; fathers: 3 to 94, n=50). Note
that multiple broods tested from the same pair or parent, have the same x-axis value in each panel.
model statistical analysis of the behavioural types in N.
pulcher might be a worthwhile enterprise in the future,
to disentangle these variance components. We found no
effects of some important aspects of the offspring’s rearing
environment on their behavioural type (like temperatures,
tank sizes, and clutch treatments).
It is yet unknown how behavioural type (e.g., aggressive
propensity) matches the behaviour shown under natural
conditions (e.g., regarding dominance [92–95], territory
acquisition [94,96,97], mate acquisition [59,98–102], and
mating performance [103]; for review see [85,104]). It would
be of particular interest to know how the behavioural type
affects fitness and therefore is subject to natural selection.
Field studies show that fitness effects of behavioural type
may vary over time [105–107]andspace[37,94,108–119],
and behavioural type scores may not match one to one
with actual behaviour shown in nature (e.g., due to context
dependence, [120,121]). Similarly, although exploration
propensity is part of the behavioural syndrome in N.
pulcher under laboratory conditions, it appears decoupled
from the syndrome under natural conditions (i.e., actual
distances moved in field settings: [43]). Under seminatural
settings, shy fish have more socially positive interactions
with their neighbourhood than bold fish, which is contrary
International Journal of Evolutionary Biology 11
to expectation [4]. However, as expected, bold fish are the
hotspots of an aggressiveness network [4]. The relevance of
all these effects for fitness in N. pulcher remain unclear, as (i)
the effects of behavioural type are always small compared to
other effects known to affect the behaviour and fitness of N.
pulcher (e.g., social status, body size, and sex); (ii) frequencies
of aggression, affiliation, and submission do not scale one
to one on the behavioural type of the focal individual
(Rothenberger et al. manuscript in preparation); (iii) effects
of behavioural type on fitness (survival and reproduction)
have not yet been measured in the field.
In domesticated and laboratory animals behavioural
types (e.g., aggressiveness) are directly subjected to artificial
selection by the experimenters [60,122–136], for instance in
order to reduce injury risk, fear, or anxiety in the animals, or
when they serve as animal model systems. However, in natu-
ral populations it is yet unclear to which extent behavioural
types are subject to natural phenotypic selection, or to which
extent they are coselected with other traits under direct selec-
tion (e.g., age at maturity). Therefore, we consider it to be of
prime importance for future studies to (i) map standardized
behavioural test results (e.g., of aggressive propensity) on
actual behaviour shown in nature under all relevant contexts
(e.g., aggressiveness measured during all life-stages and types
of contests), and (ii) obtain estimates about how different
behavioural types relate directly (or indirectly) to fitness
in the natural situation. Finally, our results suggest other
(non)genetic effects affecting the behavioural type in N. pul-
cher, which should be analysed in more detail in the future.
Acknowledgments
The authours thank the editors for inviting us to contribute
to this special issue. They thank Susan Rothenberger for
behavioural tests performed in 2007, Liana Lasut, Este´
e
Bochud and Sebastian Keller for behavioural tests performed
in 2008, and Kristina Sefc and an anonymous reviewer for
their comments. This study was supported by SNSF grants
30100A0-122511 to M. Taborsky and 3100A0-108473 to D.
Heg. They declare that the results presented in this paper
have not been published previously.
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