ANIMAL BEHAVIOUR, 2008, 75, 547e553
doi:10.1016/j.anbehav.2007.06.011
Available online at www.sciencedirect.com
Repeatability in nest construction by male three-spined
sticklebacks
B. J. RUSH BROOK* , N. J. DI NG EMA N SE†‡ & I. B AR BER* §
*Institute of Biological Sciences, University of Wales Aberystwyth
yAnimal Ecology Group, Centre for Evolutionary and Ecological Studies, University of Groningen
zDepartment of Behavioural Biology, Centre for Behaviour and Neurosciences, University of Groningen
xDepartment of Biology, University of Leicester
(Received 2 February 2007; initial acceptance 30 March 2007;
final acceptance 29 June 2007; published online 24 October 2007; MS. number: 9257)
Structures built by animals may convey useful information about the builder that may be used by conspecifics in quality assessment. In fish, nest construction has been suggested to reflect qualities of individual
builders, but little is known about how consistent individual differences are over time. If nest construction
does reliably reflect builder quality, then we expect consistent variation between individuals in this extended phenotypic trait. We test this hypothesis in male three-spined sticklebacks, Gasterosteus aculeatus,
by measuring the repeatability of nest characteristics. We encouraged males, caught from four populations
in mid-Wales, U.K., to complete three consecutive nests under standardized laboratory conditions. We
quantified a number of structural components and design characteristics of nests and estimated repeatability (r) of these traits. Within populations, the number of threads used, the area of the nest and the mass of
substrate deposited on top of the nest were all repeatable within males (0.39 < r < 0.51), showing that individual male three-spined sticklebacks differed consistently in the size and composition of the nests they
produced. Our data support the hypothesis that nest characteristics may reveal important information
about the quality of individual males, and that they may, at least in part, be under genetic control. We discuss these findings in the context of the evolution of nest characteristics in sticklebacks and other species.
Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Keywords: evolution; Gasterosteus aculeatus; nest building; repeatability; stickleback; structure
Nests are constructed by animals from all vertebrate phyla
(von Frisch 1975), and their primary function is to provide
protection for developing offspring from the physical and
biological environment (Hansell 2005). However, in nestbuilding species, variation in the structure and the location of the nest can affect not only offspring survival
(Bult & Lynch 1997; Spencer 2002; Vinyoles et al. 2002;
Warner & Andrews 2002; Burton 2006; Raventos 2006),
but also mate acquisition (Johnson & Searcy 1993; Takahashi & Kohda 2002; Östlund-Nilsson & Holmlund 2003;
Correspondence and present address: I. Barber, Department of Biology,
University of Leicester, University Road, Leicester LE1 7RH, U.K.
(email: [email protected]). B. J. Rushbrook is now at the Wiltshire Wildlife
Trust, Elm Tree Court, Devizes, Wiltshire SN10 1NJ, U.K. N. J. Dingemanse is a member of both the Centre for Evolutionary and Ecological
Studies, and the Centre for Behaviour and Neurosciences at the University of Groningen, PO Box 14, 9750 AA Haren, the Netherlands.
0003e 3472/08/$34.00/0
Eckerle & Thompson 2006). Nest structure and design
can, therefore, be regarded as extended phenotypic traits
(see Dawkins 1999) that are shaped by both natural and
sexual selection.
Observed variation in nest characteristics may be influenced by both genetic and environmental factors. For
example, the size of the nest built by individual male
penduline tits, Remiz pendulinus Olphe-Galliard 1891, is
consistent across successive nesting attempts throughout
a breeding season, despite temporal changes in female
preferences, suggesting that aspects of construction may
be under a certain degree of genetic control (Hoi et al.
1996; Schleicher et al. 1996). On the other hand, longtailed tits, Aegithalos caudatus (Lin. 1758), reduce the
mass of feathers incorporated into their nests when temperatures increase, suggesting that they are able to gauge
the thermal environment within the nest and adjust
nest-building behaviour accordingly (McGowan et al.
2004).
547
Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
548
ANIMAL BEHAVIOUR, 75, 2
To understand how extended traits such as nest building
evolve, we need insight into both the heritability of and
the selection pressures acting on such traits (Endler 1986).
One approach to identifying probable genetic variation in
nest-building behaviour is to encourage individual
builders to complete multiple nests under fixed environmental conditions and measure the consistency, or ‘repeatability’, of the nest structure across nesting attempts.
Repeatability (r) in this context is defined as the proportion of observed total phenotypic variation that is explained by differences between individuals (Falconer &
Mackay 1996). Repeatability therefore indicates the
amount of variation in a trait measured on more than
two occasions that is a result of differences between individuals. If there is a high degree of variability in the trait
over time within individuals, for example between individuals, repeatability values are low. Conversely, where
there is a high level of variability between individuals,
compared with within individuals, repeatability values
are high.
Species that build multiple nests successively within
one season offer an ideal opportunity to study the repeatability of nest construction, with consistency of nest
location and form across building attempts potentially
indicating heritable variation in the trait (Schleicher et al.
1996; Kamel & Mrosovsky 2004, 2005). Repeatability
values gained from such studies are clearly not a proxy
for heritable differences, because they may also reflect individual differences in responses to environmental conditions. However, because between-individual variation in
a trait results from the combined influences of environmental and genetic components, repeatability does set
an upper limit to the heritability (h2) of a trait (Boake
1989; Falconer & Mackay 1996). Determining repeatability therefore represents an important first step towards
investigating the potential for genetic variation in nest
construction.
During the breeding season, male three-spined sticklebacks, Gasterosteus aculeatus (Lin. 1758), compete for territories before constructing a nest of filamentous algal and
plant material (van Iersel 1953; Wootton 1976), which
acts as a focal point for courtship and spawning and provides shelter for developing eggs and offspring (Wootton
1976). In sticklebacks, there are indications that variation
in nest construction reflects male quality (Barber et al.
2001) and is used by females in mate choice (Östlund-Nilsson 2001; Östlund-Nilsson & Holmlund 2003). For example, characteristics of nests built by male 15-spined
stickleback, Spinachia spinachia, influence the quality of
protection the nest provides the offspring, and also provide information on quality of the subsequent paternal
care (Östlund-Nilsson 2000, 2001). Therefore, by basing
mate choice on nest characteristics, females gain direct
benefits through improved offspring survival.
Although male three-spined sticklebacks can build
multiple nests within a single breeding season (Wootton
1976), it is not known whether nests built consecutively
by individual males are similar in their structure and
design. The aim of this study was to measure the level of
repeatability in the nest characteristics of individual
male three-spined sticklebacks within populations. We
replicated this experiment for four populations to obtain
a general idea of repeatability within the average
population.
METHODS
Fish Collection and Husbandry
Adult sticklebacks were collected using a 2-m seine
(mesh size 5 5 mm) and hand nets (mesh size
1 1 mm) during March 2005 from four populations in
mid-Wales (U.K.); two lakes, Llyn Frongoch (52 210 4600 N
3 520 2600 W) and Llyn-yr-Oerfa (52 240 0500 N 3 520 1900 W),
and two rivers, the Afon Rheidol (52 240 1600 N 4 020 4900 W)
and the Afon Ystwyth (52 230 5500 N 4 050 0800 W). Previous
studies had shown that, when building under common
conditions identical to those described in the present
study, there were no significant population-level differences in nest composition or structure (B. J. Rushbrook
& I. Barber, unpublished data). The four populations
were therefore used in this study because they were local
and readily sampled, rather than representing an interest
in, or an expectation of, habitat-specific patterns of nesting behaviour. On transfer to the laboratory, fish were
placed in mixed-sex groups in population-specific aquaria
(750 200 380 mm). Conditions within the laboratory
encouraged reproductive development (16:8 h light:dark
photoperiod;
temperature:
X SD ¼ 17:7 0:2 C).
Throughout the experiment, fish were fed daily, ad libitum, on a mixture of chironomid larvae and Daphnia sp.
Nest Building
In late March, five males from each population were
blotted, weighed (0.001 g) and measured (standard
length to 1 mm), and introduced into individual nesting
aquaria (200 350 200 mm). Each aquarium was provided with a sponge airlift biofilter to maintain water
quality, a plastic plant for cover, and a gravel substratum, the front third of which was covered by a layer
of sand. Each male was provided with a bundle of
200, 7-cm-long black polyester threads as nesting material. Preliminary studies demonstrated that males from
each of the four populations readily constructed nests
under these standardized conditions (B. J. Rushbrook, &
I. Barber, unpublished data).
Visual access to gravid females (presented in glass jars)
was provided for two consecutive 10-min periods each day
to encourage nesting activity. Heavily gravid females were
kept in stock throughout the study, and four that
appeared to be in spawning condition were selected
from the stock tanks each day for presentations. Each
day, every male received successive presentations of two of
the four females, chosen at random. These procedures
negated the possibility that any male was presented
consistently with the same female, and countered the
possibility that females affected male nest building. Nesting aquaria were inspected visually on completion of
female presentations, and the date of nest initiation
(defined by the appearance of glued nesting threads
RUSHBROOK ET AL.: REPEATABILITY OF STICKLEBACK NESTS
within a sand pit) was recorded. Once a nest entrance was
visible (van Iersel 1953; Wootton 1976), a gravid female
was released into the tank for up to 5 min and the male’s
behaviour observed. If the male either crept through (van
Iersel 1953; Wootton 1976) or presented the nest entrance
to the female (Wootton 1976), the nest was considered
complete and the female was immediately removed to prevent any further disturbance of the nest. If these behaviours were not observed, unrestrained gravid females
were introduced daily in addition to visual presentations.
The number of days from nest initiation to nest completion was termed ‘construction time’.
On completing a nest, the male was removed from its
tank, and the nest photographed digitally (Canon A70
(Canon Inc., Tokyo, Japan)) in situ, directly from above
(Fig. 1a). Each photograph incorporated a scale bar to calibrate the image analysis software. The nest was then removed on an acetate sheet, taking care to retain the
deposited substrate (Barber et al. 2001), left to dry at
room temperature and placed in a resealable plastic bag.
Unused nesting material was then removed from the
aquarium, fresh material provided, and the original male
returned to the tank. Female presentations were resumed
the following day and the process was repeated until
each male had completed three nests. On completing
the third nest, the male was removed and replaced with
a new male from the same population. Any male that
failed to initiate nesting after 14 days of female presentation was removed from the study (NFrongoch ¼ 0;
NOerfa ¼ 3; NRheidol ¼ 3; and NYstwyth ¼ 2) and replaced
with a new male from the same population. One male
from Llyn Frongoch and one from the Afon Ystwyth
died during experimentation of unknown causes after
completing 1 and 0 nests, respectively. No additional
males were added after the experiment had run for seven
weeks.
Female presentations were made for a total of nine
weeks after which all remaining males were removed.
Sample sizes of males that built three nests were
NFrongoch ¼ 6; NOerfa ¼ 5; NRheidol ¼ 7; and NYstwyth ¼ 9.
Nest Structure
Dried nests were removed from the acetate sheet and
the nesting threads and substrate were separated using
fine forceps. Nesting threads were counted and the mass
of substrate deposited on top of the nest was weighed
(total substrate, to 0.001 g).
Nest Design
Digital images of the nest were manipulated to enhance
contrast and resized for further analysis using Adobe
Photoshop 7.0Ô (Adobe Systems Inc., San Jose, CA,
U.S.A.), and then using ImageTool 3.0Ô (available on the
Internet at http://ddsdx.uthscsa.edu/dig). We made linear
and area measurements from the nest images and generated shape indexes. Nest compactness (Ic) was determined
from the nest image by dividing the bulk area of the nest
by its total area (as described in Barber et al. 2001; Fig. 1a,
b). Nest shape was then approximated by drawing a concave polygon in Microsoft PowerPointÔ (Microsoft Corp.,
Mountain View, CA, U.S.A.) to enclose only those threads
(a)
(b)
(c)
(a)
(b)
(c)
Figure 1. Photographic examples of (a) nests built during the study with diagrammatic representations of (b) total (vertical lines) and bulk
areas (horizontal lines) and (c) nest shape for those nests.
549
550
ANIMAL BEHAVIOUR, 75, 2
Table 1. Description of nest-shape characteristics, including the
method of calculation where appropriate
Characteristics
Area
Perimeter
Major
axis length
Minor
axis length
Elongation
Roundness
Description
The area (mm2) of the nest shape.
The perimeter (mm) of the nest shape.
The major axis length is the greatest distance
(mm) from one end of the nest shape to its
opposite.
The minor axis length is the greatest distance
(mm) across the nest shape perpendicular to
the major axis length.
The ratio of the minor axis to the major axis
length. The result gives a value between
0 and 1. At 1, the object is roughly circular
or square, and as the ratio decreases from 1,
the object becomes more elongated.
Calculated using (4parea)/perimeter2. The
result gives a value between 0 and 1. At 1,
the object is a perfect circle, and as the ratio
decreases from 1, the object becomes less
circular.
whether residuals (both at the individual and observation
levels) deviated from normality (as recommended in Rasbash et al. 2004). Significant departure from normality
was detected for the mass of substrate deposited on the
nest, although square-root transformation removed departures from normality.
Ethical Notes
Individuals that completed three nests were killed using
an overdose of Benzocaine (25 ml/litre 10% w/v Amino
Benzoate in 70% alcohol) and preserved for subsequent
physiological analysis, whereas individuals removed
from the experiment because of inactivity, and those
remaining at the termination of the study, were returned
to their population of origin.
RESULTS
Repeatability of Nest Characteristics
that were either fully intertwined within the nest, or where
both ends had been actively incorporated into the nest;
(Fig. 1a, c). Nest shape polygons were then imported into
ImageTool 3.0Ô where the analysis function was used to
quantify the nest-shape parameters detailed in Table 1.
Statistical Analysis
Generalized linear mixed models were used to obtain
estimates of variances at the different levels (population,
individual, observation). The hierarchical structure of our
models would ideally be specified by fitting population,
individual (nested within population), and observation
(nested within individual) as random effects. However,
because we only sampled four populations, we did not
have enough data to reliably estimate variances at this
level, and following Rasbash et al. (2004), we fitted population as a fixed effect. Individual (27 levels) and observation (nested within individual; 81 levels) were fitted as
random effects. This model structure allowed us to obtain
individual repeatability estimates within the average population. Because nest compactness, nest-shape elongation
and nest-shape roundness data were proportions, these
values were arcsine square-root transformed before
analysis.
To test whether standard length, nest number or day of
introduction affected each nest characteristic, we fitted an
initial full model (including all main effects), and then
fitted all simpler models (see Supplementary material for
details of all models), and used the Akaike’s Information
Criterion (AIC) to select the most parsimonious model
(the model that fits that data best with the fewest parameters). Because our aim was to measure repeatability and
effects of the three fixed effects within populations (see
above), population was fitted as a fixed effect in all
models, irrespective of significance. Differences between
populations were evaluated for the final model, and tested
using the chi-square-distributed Wald statistic to evaluate
statistical significance. For all best models, we tested
The number of threads used by individual males was
repeatable (Table 2), with males generally using a similar
number of nesting threads in each of their three nests
(Fig. 2a). Nest-shape area was also repeatable (Table 2), implying that males typically built three nests of similar size
(Fig. 2b). Furthermore, the total mass of substrate deposited on top of the nest was repeatable (Table 2; Fig. 2c).
We found no evidence of repeatability in any of the other
characteristics measured (Table 2).
Population and Other Explanatory Variables
For a number of nest-building characteristics, one of the
fixed effects (standard length, nest number, or day of
introduction) remained in the most parsimonious model
(Table 3). Initial standard length influenced the amount of
substrate deposited on the nest and the minor axis length,
with larger males depositing a greater total mass of
substrate (parameter estimate SE ¼ 0.050 0.023) and
building wider nests (1.036 0.561). Nest compactness
and construction time increased with nest number
(1.412 0.561 and 0.981 0.394, respectively), and
successive nests were more elongated (0.028 0.017).
Males that were introduced into the study later had shorter
construction times (0.056 0.022) and increased nestshape roundness (0.003 0.001). Nest construction time,
and nest-shape perimeter (hence, nest-shape roundness)
differed between populations (Table 2).
DISCUSSION
We identified considerable variation in both the composition and the size of nests built by male three-spined
sticklebacks within populations, despite all fish being
provided with identical nesting materials and being
encouraged to build under common conditions in the
laboratory. For example, nests showed an 8-fold range in
nest-shape area, an 18-fold variation in the number of
RUSHBROOK ET AL.: REPEATABILITY OF STICKLEBACK NESTS
Table 2. Sources of variation in various nest characteristics
Population
Individual
Characteristics
N
X3
P
X1
P
r
Number of threads
Total substratey (g)
Compactnessz
Area (mm2)
Perimeter (mm)
Major axis (mm)
Minor axis (mm)
Elongationz
Roundnessz
Construction time (d)
81
81
81
81
81
81
81
81
81
81
7.658
1.687
6.861
0.210
9.546
3.056
1.545
1.904
10.954
19.001
0.054
0.640
0.076
0.976
0.023*
0.383
0.672
0.593
0.012*
0.000**
5.643
6.559
2.527
5.487
0.448
3.301
2.409
0.310
2.904
0.000
0.018*
0.010**
0.112
0.019*
0.503
0.069
0.121
0.578
0.088
1.000
0.398
0.505
0.223
0.389
0.081
0.267
0.216
0.066
0.245
0.000
Between-population variation was assessed using a mixed model with individual as random but population as fixed effects (see Methods).
Average within-population repeatability (r) was estimated as the between-individual variation divided by the sum of the between- and withinpopulation variations.
*Significant at P 0.05; **Significant at P 0.01.
ySquare-root transformed.
zArcsine square-root transformed.
Number of threads
in this study do, in fact, influence female choice, or test
the repeatability of nest traits identified in other populations that are selected by females.
A number of between-male characteristics significantly
affected the building and structure of nests in our study.
200
(a)
150
100
50
Nest shape area (mm2)
0
Total substrate mass (g)
threads used, and a 60-fold variation in the total mass of
deposited substrate. This variation was not strongly linked
to the population of origin, and nest structure was highly
variable within and between populations. However, nests
built by individuals across three successive nesting cycles
showed considerable structural consistency. The amount
of nest material used, both in terms of the number of
threads incorporated into the nest and the mass of substrate deposited, was repeatable, as was the size of the
approximated nest shape.
For each of these traits, the between-individual component explained nearly 50% of the total variation, resulting
in a substantial degree of repeatability. Because repeatability analysis can provide anecdotal information on the
potential heritability of a trait by setting an upper
boundary (Cummings & Mollaghan 2006), our results
are consistent with the hypothesis that the structure of
a male’s nest has a genetic component (Schleicher et al.
1996). For example, although the level of heritability of
behaviours varies between species and with the type of behaviour under investigation, an average value of h2 across
a range of behaviours has been calculated at approximately 0.3 (reviewed in Stirling et al. 2002 and references
therein). More studies are now required to further examine the relative contribution of genetic and environmental components of repeatability in these nest-building
traits.
A number of studies in three-spined sticklebacks have
demonstrated the importance of nest structure and nest
location on female choice, and these preferences are often
associated with an increase in offspring survival (Sargent
& Gebler 1980; Sargent 1982; Kraak et al. 1999; ÖstlundNilsson & Holmlund 2003; Ólafsdóttir et al. 2006). Because our results show that aspects of nest structure are
consistently different between individuals over time,
they provide support for the hypothesis that three-spined
sticklebacks nest structure may provide a reliable indicator
of individual quality. To confirm this, it would be necessary to either test whether the repeatable traits identified
4000
(b)
3000
2000
1000
0
5
4
(c)
3
2
1
0
Frongoch
Oerfa
Rheidol
Ystwyth
Figure 2. The range of values, for each male from each of the four
populations under study, for (a) the number of threads used in completed nests, (b) nest-shape area (mm2), and (c) the mass of deposited substrate.
551
552
ANIMAL BEHAVIOUR, 75, 2
Table 3. Models of best fit based on the AIC
AIC
Number of
parameters
Deviance
B
857.564
6
845.564
B(SL)
223.515
7
209.515
B(NN)
B(SL)
B
B
512.556
1328.838
970.671
687.003
7
7
6
6
498.556
1314.838
958.671
675.003
B(SL)
641.621
7
627.621
B(NN)
587.027
B(DI)
576.210
B(NN,DI) 405.303
7
7
8
573.027
562.210
389.303
Characteristics
Number
of threads
Total
substrate*
Compactnessy
Area
Perimeter
Major
axis length
Minor
axis length
Elongationy
Roundnessy
Construction
time
Model
B: basic model (population fixed variable); SL: standard length; NN:
nest number; DI: day of Introduction.
For each nest characteristic, we give the most parsimonious model (a
model that fits the data best with the fewest parameters; for AIC
values of all other alternative models that were fitted, see Supplementary Table).
*Square-root transformed.
yArcsine square-root transformed.
The time of entry of males into the experiment affected
the speed of construction, with males introduced later
completing their nests more quickly. Nest building is
energetically expensive in three-spined sticklebacks (Stanley 1983; Wootton 1985, 1994), and is dependent on condition and food intake prior during the run-up to the
breeding season (Wootton 1984 and references therein).
Because all males used in the study had been collected
from natural populations at the same time, those introduced later in the experiment had experienced longer periods of favourable laboratory conditions, and may have
achieved better condition and/or developed higher levels
of circulating androgens before nesting. Alternatively,
they may have been better adjusted to laboratory conditions (Barber et al. 2001). Nest shape also covaried with
time of introduction, with males introduced later building
nests that were rounder. This finding supports earlier suggestions that male condition can affect nest design (Barber
et al. 2001), because rounder nests are achieved by males
reincorporating loose thread ends back into the nest
(Rushbrook, personal observation), a behaviour that is
probably costly to the male in time and energy.
Fish body size influenced the mass of substrate deposited on the nest, with larger males depositing more
substrate. Deposited substrate may improve a nest’s ability
to withstand disturbance and/or aid in nest camouflage
(Lindström & Ranta 1992; Solis & de Lope 1995), but its
collection and transport is considered energetically expensive (Wootton 1976; Guerra & Ades 2002). Furthermore,
individuals may be exposed to increased predation risk
while collecting nest-building material (Slagsvold & Dale
1996). The mass of substrate deposited may therefore reflect the outcome of a trade-off. If larger males, with increased buccal volume and load-carrying ability, pay
fewer costs when moving substrate than smaller fish, our
results may suggest that the resolution to this trade-off is
size-dependent.
The sequence number of the nest also affected its
structure, with later nests typically being less compact
and more elongated. Low compactness scores arise when
males incorporate fewer thread ends into the nest (Barber
et al. 2001), and more elongate nests have a lower proportion of the nest material incorporated in the egg holding
area of the nest (Rushbrook, personal observation). This
reduced tendency to incorporate nesting threads back
into the nest may result from males spending less time
constructing later nests (Table 3).
In summary, we have identified that nests built consecutively by individual male three-spined sticklebacks show
a substantial degree of repeatability in a number of
characteristics (range 0.39 < r < 0.51), suggesting that between-male variation is consistent over time and potentially provides reliable information to conspecifics. Our
results are consistent with the hypothesis that the structure of a male’s nest has a genetic component. Furthermore, if our values of repeatability provide a reliable
indication of heritability for these traits (which would
need to be confirmed by a formal quantitative genetics
study), then they may compare favourably with those
for other behaviours (Stirling et al. 2002). If nest structure
has a heritable component, then it has the potential to
evolve in response to natural selection. We suggest that
showing repeatability is a necessary first step to investigating the genetic basis of nest building. Detailed multiplegeneration experiments are now required to determine
both the heritability of and genetic correlations among
nest characteristics, as well as the fitness consequences
of nest construction in three-spined sticklebacks, which
provides a tractable model for the investigation of such
questions.
Acknowledgments
We are grateful to Rory Geoghegan for assistance in fish
collection, and to the editor and two anonymous reviewers for constructive comments on an earlier version of
this manuscript. B. J. R. acknowledges the support of
a U.K. Natural Environment Research Council studentship
(NER/S/A/2003/11389). N. J. D. was supported by the
Netherlands Organisation for Scientific Research (NWO
grant 863.05.002).
Supplementary Data
Supplementary data associated with this article can be
found, in the online version, at doi:10.1016/j.anbehav.
2007.06.011.
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