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Behavioral Ecology Vol. 12 No.

4: 390396

Nests as ornaments: revealing construction by


male sticklebacks
Iain Barber, David Nairn, and Felicity A. Huntingford
Fish Biology Group, Division of Environmental and Evolutionary Biology, IBLS, University of Glasgow,
Scotland, UK
Nests are built by animals from a variety of taxa, and serve as receptacles for eggs and developing offspring. Where nests are
built solely or mainly by one sex, they also have the potential to serve as extended ornaments, because aspects of construction
potentially reveal or amplify characteristics of the builder to prospective mates. Here, we develop novel indices to quantify nest
structure and examine variation in temporal and structural aspects of nest construction in relation to morphological, immunological, and physiological traits in male three-spined sticklebacks, Gasterosteus aculeatus. Wild-caught male sticklebacks that
began construction within 3 days of being transferred to the laboratory built neater nests than fish that took longer to start,
and we present alternative testable hypotheses that could explain this pattern. Various characteristics of nest-building males
correlated with nest structure. The relative weight of the building males kidneywhich secretes a glue-like protein used in
nest building and whose development is androgen-dependentcorrelated positively with nest neatness. We also found males
with enlarged spleens (an indicator of immune stress) to construct less compact nests. The structure of a nest may therefore
be important not only in determining its functional capacity, but may also act as a quality-revealing ornament. We suggest that
females may gain valuable information regarding male health status and androgen levels from nest inspection. Key words:
carotenoids, fish, Gasterosteus aculeatus, nest architecture, nest building, nest construction, nest quality, Pisces, sexual selection,
sticklebacks. [Behav Ecol 12:390396 (2001)]

nimals build nests to serve as receptacles for eggs and


provide a safe environment for the early growth and development of offspring (Collias and Collias, 1976, 1984). Nest
builders (which are normally one or both of the parents) may
influence the functional capacity of a nest by site selection
and by the quality of their construction. There is increasing
evidence that both factors may have important consequences
for the success of a breeding attempt (Bult and Lynch, 1997;
Hoi et al., 1994, 1996; Thompson and Furness, 1991). We
therefore expect that, in species where construction is carried
out solely or mainly by one sex (generally males), members
of the choosing sex (generally females) should prefer builders
of nests that are well adapted to local conditions as mates
(Collias and Victoria, 1978; Hoi et al., 1994, 1996; Johnson
and Searcy, 1993).
However, preferences for sexual partners that build nests
with particular characteristics may evolve for other reasons.
Since nests and other artifacts may be viewed as phenotypic
expressions of the builders genes (Dawkins, 1982), females
may also benefit by selecting males that are proficient at building such structures if their construction reliably signals some
intrinsic aspect of builder quality. Nest-building activity may
therefore be viewed as a sexually selected behavior (Soler et
al., 1998) and the nest as an ornament, in the same way as
are secondary sexual characters (Andersson, 1994). Aspects of
nest structure could even function as non-costly amplifiers
(sensu Hasson, 1990, 1991), making it easier for females to
discriminate high from low quality builders.
Although females appear to prefer mates that build nests
with certain characteristics in some species (e.g., Collias and

Address correspondence to I. Barber, who is now at Edward Llwyd


Building, Institute of Biological Sciences, University of Wales Aberystwyth, Penglais Campus, Aberystwyth, Ceredigion SY23 3DA Wales,
UK. E-mail: iab@aber.ac.uk.
Received 25 May 1999; revised 17 August 2000; accepted 24 August
2000.
 2001 International Society for Behavioral Ecology

Victoria, 1978; Hoi et al., 1994; Sikkel, 1995), it is unclear


whether this preference stems from a choice for the nest per
se, or for some correlated quality of the builder. Male bowerbirds construct elaborately decorated bowers (which are not
nests, but courtship arenas) and females prefer builders of
higher quality bowers as mates (Borgia, 1985b). Males that are
able to maintain high quality bowers are also those most able
to withstand raids from other males (Borgia, 1985a), suggesting that they are dominant individuals and that females use
the bower as a marker of male quality (Borgia et al., 1985).
If nest structure reveals traits of the builder that may be correlated with either his paternal ability or his genetic quality,
in the same way as do bowers, then nest-inspecting females
could use this information in mate choice decisions. An important first step is to measure the extent of interindividual
variation in nest construction, and determine whether nest
variation is related to such traits in the builder. Here, we provide one of the first examinations of relationships between
correlates of builder quality and nest construction, in a fish,
the three-spined stickleback Gasterosteus aculeatus.
The three-spined stickleback as a nest builder
Although the rule among the birds and mammals, nesting has
a diffuse taxonomic distribution among the fishes (Hansell,
1984). In nest-building fishes, males generally construct the
nest alone and then solicit matings from multiple females.
Nest construction in sticklebacks is reasonably well documented (Rowland, 1994; Wootton, 1976). Following construction of a pit in a sandy substratum, the male lays down a mat
of filamentous algae and other vegetation, may cover this partly with substratum carried to the nest by mouth, and finally
forms a tunnel through which the female can pass during
spawning (Wootton, 1976). Nest materials are secured by a
glue, produced in the kidney, that contains a glycoprotein,
Spiggin, the secretion of which is under the control of androgenic hormones ( Jakobsson et al., 1999). On completing the
nest, males court gravid females and attempt to lead them
back to the nest to spawn, then fertilizing the eggs. After collecting eggs for a period of between 1 and 10 days, the male

Barber et al. Nests as ornaments

switches to the parental phase (Kraak et al., 1999a), during


which he actively repels potential egg predators, fans oxygenated water through the nest and removes unfertilized eggs
and dead or diseased embryos (Wootton, 1982). Stickleback
nests therefore serve as receptacles for developing embryos
and provide protection from water currents and the attentions
of both con- and heterospecific predators (Potts, 1984).
As part of an experimental study examining maternal and
paternal effects on fry performance, we photographed and
collected nests, constructed under controlled conditions and
from standardized materials by males from which we subsequently gathered data on physiology, behavior, and morphology (including coloration). Here, we develop techniques for
quantifying nest structure and examine relationships between
nest construction and builder traits. Our aim is to test the
hypothesis that nest structure could reliably reveal fitness-correlating traits of constructing males.
MATERIALS AND METHODS
Fish collection and nest building
Male sticklebacks collected at the beginning of the 1997
breeding season (mid-April) from Inverleith pond, Edinburgh, Scotland (5555 N, 0310 W) were transferred to the
laboratory in separate containers and released into individual
nesting aquaria (20 20 35 cm). Each aquarium was provided with a fine gravel substratum, an airlift filter, a plastic
plant and standardized artificial nesting material, comprising
250-ml sand and two hundred 6-cm long black polyester
threads. Sticklebacks from this and other (though not all,
Candolin U, personal communication) populations readily
use polyester threads, which mimic naturally available nest
building materials, such as strands of unicellular algae and
other vegetation. Inverleith males build typical nests, as described by Wootton (1976), which can be fully inspected by
females. During the period of the study, food (chironomid
larvae) was supplied daily, to excess.
To facilitate nest construction, males were presented twice
daily for periods of 20 min with gravid females in glass jars.
We recorded two temporal aspects of nest building: the number of days taken to begin construction following introduction
to the nesting tanks (pre-building lag) and the number of
days from nest initiation to completion (construction time).
Once the nest was completed (the day when a male first
crept through his nest during courtship directed towards a
stimulus female) the builder was removed and photographed
within 30 s under standard conditions, to allow subsequent
determination of sexual coloration.
Measurement of nuptial coloration
We adopted Frischknechts (1993) photography protocol, and
an analysis protocol described by Villafuerte and Negro
(1998) to measure male nuptial coloration. Fish placed within
a water-filled glass cell were photographed under controlled
illumination conditions against a uniform black background
and color transparencies were scanned into a PC and analyzed
using PhotoShop 4.0 software (Adobe Systems Inc., California, USA). Areas of carotenoid-based nuptial coloration on
both the ventral and lateral surfaces of each male were captured using the magic wand function of the package (Villafuerte and Negro, 1998) and brightness values (on a scale
of 0255) of the red, blue and green components of the selected pixels recorded. We calculated two components of male
nuptial coloration. We calculated coloration intensity by dividing the brightness value of the red component by the sum of
the red, green, and blue component values, and expressed
this as an index, R (Frischknecht, 1993). We also measured
the area of nuptial coloration on both the lateral and ventral

391

surfaces of nesting males, A, and calculated residuals from the


relationship with male length. We used the residual values to
describe the body size-corrected area of the nuptial coloration, rA. (Detailed photography and analysis protocols are
provided in Barber et al., 2000).
Screening for immune status and body condition
After being photographed, males were sacrificed by an overdose of Benzocaine anaesthetic and immediately weighed
(wet weight, to 0.001 g) and measured (total length, to 1
mm). Each male was then dissected, and the weights of the
liver, spleen, and kidney were recorded to 0.0001 g. We calculated relative liver weight (or hepatosomatic index, HSI,
which is an index of medium term energy reserves in sticklebacks; Chellappa et al., 1995), relative kidney weight (RKW,
an indicator of the level of androgen secretion in breeding
male sticklebacks; Borg and Mayer, 1995) and the relative
spleen weight (RSW, which increases under stress associated
with disease or parasite infection; Bruno et al., 1998; Byrne et
al., 1998). The presence of any Schistocephalus solidus plerocercoids, parasites recorded in the body cavity of some fish
from the study population, was also recorded.
Nest removal and analysis
Following removal of males from their nesting aquaria we
photographed nests in situ from above. Nests were then loosened from the substratum and slid onto acetate sheets while
underwater; we took care to exclude non-structural unattached substratum and to retain deposited substratum. Nests
were dried to constant weight at room temperature and separated into constituent parts.
We quantified several aspects of nest composition, both by
direct measurement and by image analysis of in situ photographs. Our measurements are detailed in Table 1 and shown
visually for a sample of nests in Figure 1. We combined some
of the nest attributes to create two indices, with the aim of
revealing information regarding structural attributes of nests.
The index of neatness (In, the proportion of visible thread
ends that were anchored or covered over by substratum) reflected how fastidious the builder had been at securing loose
threads. The index of compactness (Ic, the proportion of nest
area through which basal substratum could not be seen) provided a measure of nest density (see Table 1). Although we
combined different factors to develop In and Ic, the indices
themselves were closely correlated (r .513, n 38, p .001;
Figure 2), suggesting that both reflected some intrinsic aspect
of nest structure.
Statistical analysis
Inter-relationships between nest and male characteristics were
examined using Pearson correlations (Minitab v12). Proportional data (including nest quality indices) were arcsine
square root transformed prior to statistical analysis (Sokal and
Rohlf, 1995). Bonferroni-style corrections to correlation analyses are not reported, since these would have reduced statistical power considerably (see arguments presented by Rothman, 1990).
RESULTS
Characteristics of nest-building males
Physiological, coloration, and morphological characteristics of
the nest-building males examined in our study are presented
in Table 2. Length and weight correlated strongly among
these males (equation of the fitted regression line: weight
0.00004 length2.8237, r2 .75), so we used length alone as
a measure of body size in our analysis, and the exponent to
calculate body condition factor {BCF [(weight, in g)/

Behavioral Ecology Vol. 12 No. 4

392

Table 1
Definitions and summary statistics of measurements taken from nests constructed by male three-spined sticklebacks
Nest character

Definition

N*

Substratum weight
Number of threads (N threads)
Number of thread ends (N ends)

Total weight of substratum deposited on top of the nest


Number of threads used in the nest
Number of nonanchored thread ends protruding from
the nest
Area covered by minimum area polygon enclosing all
visible nest material
Area covered by portion of the nest through which no
basal substratum was visible

42
42
42

Total area (A

tot

Bulk area (A

bulk

Neatness index, In

Abulk
Atot

Compactness index, Ic

Nends
2(Nthreads)

Mean ( SD)
1.87 g (1.77g)
148.0
( 46.6)
64.9
( 38.0)

Range
0.005.78 g
37200
0170

39

4665 mm2 ( 1739 mm2)

18028577 mm2

39

1901 mm2 ( 842 mm2)

4293523 mm2

42

0.77 ( 0.14)

0.481.00

39

0.45 ( 0.25)

0.121.00

* 42 males built nests. Data are reduced in some cases because nest area measurements could not be made from three nests.

(length, in mm2.8237)] 105}. Of the 58 males caught in the


field, 42 completed nests within 17 days of transfer to nesting
tanks and 16 failed to build nests within that time. Six nonbuilders died before the end of the study, whereas all nest
builders survived.

Nest structure and temporal aspects of construction


Among nest-building males, both the length of the pre-building lag period and the length of construction time varied considerably (see Table 2). Examination of the pre-building lag
data suggested that fish were either early or late nesters (bi-

Figure 1
Photographs of representative nests built by male sticklebacks during the study, with diagrammatic representations showing the various
quantitative measurements made for each nest.

Barber et al. Nests as ornaments

393

correlate with either index of nest structure or with the weight


of deposited substratum (0.147 r .089, all p .377).
Nest structure and male coloration
Both the size-corrected area (rA) and the intensity (R) of nuptial coloration varied greatly between building males (see Table 2). However, there was little evidence that coloration was
associated with nest structure. The rA of the males nuptial
coloration correlated marginally significantly with nest neatness, but not with compactness or weight of deposited substratum, and there were no significant relationships between
R and nest structure (see Table 3).

Figure 2
The relationship between the two indices of nest structure for nests
built by male sticklebacks in our study.

Nest structure and parasite infection


Only three of the 42 nest-building males were found to harbor
S. solidus plerocercoids, precluding rigorous statistical analysis. However, when the nest data were ranked and examined
in terms of builder infection status, compactness index rankings of the three nests built by infected fish were concentrated
in the lower one-third of ranks of all nests analyzed. In addition, the RKW of infected fish also tended to be lower; no
infected fish ranked in the top two-thirds with respect to this
character.
DISCUSSION

modal distribution with peaks around 23 and 56 days; Figure 3, main). Early nesters (those taking 3 days to initiate
construction) built neater nests than late nesters (t test, t
2.60, df 38, p .013; Figure 3, inset), but the compactness
of nests built by early and late nesters did not differ (t test, t
0.84, df 34, P .40). Males exhibiting longer construction times built more compact (r .358, n 38, p .027)
nests and incorporated more deposited substratum (r .318,
n 42, p .040), but there was no significant correlation
between construction time and nest neatness (r .206, n
38, p .197).
Nest structure and male physiological traits
Perhaps surprisingly, neither male body length nor BCF correlated with nest neatness, compactness, or with the weight of
deposited substratum (length, 0.080 r .229, all p .150;
BCF, 0.281 r .072, all p .087). The RKW of nesting
males correlated positively both with the neatness (r .360,
n 38, p .026) and compactness (r .350, n 37, p
.036) of the nests they built, but not with the weight of substrate deposited (r .164, n 36, p .325). RSW correlated
negatively and significantly with the total weight of deposited
substratum (r .366, n 37, p .026) and with nest compactness (r .397, n 35, p .018), but only marginally
with nest neatness (r .267, n 36, p .11). HSI did not

In our study, reproductively active male sticklebacks from a


single annual population exhibited remarkable variation in
temporal and structural aspects of nest construction, despite
being provided with identical building materials. The nest
construction variables we measured also correlated with certain traits of building males, suggesting that in populations
where females are able to view the whole nest, inspection may
provide useful information regarding male quality.
Of particular interest was the relationship between relative
kidney weight of the builder and nest neatness and compactness. During nest construction, male sticklebacks stick strands
of nesting material together, and to the substratum, using glue
produced by the kidney (Wootton, 1976). The development
and size of the kidney is affected by levels of circulating androgens such as 11-ketotestosterone (Borg and Mayer, 1995;
Jakobsson et al., 1996), as is the amount (and possibly the
quality) of glue produced ( Jakobsson et al., 1999). Because
the glue is essential for successful nest construction, males
with relatively small kidneysprobably resulting from low levels of circulating androgensmay be unable to construct neat
nests. The results of our study are consistent with this hypothesis, since relative kidney size correlated positively with both
of our nest indices. Another androgen-dependent trait, the
concentration of carotenoid pigment deposited in the skin of
male sticklebacks, also correlated with aspects of nest struc-

Table 2
Characteristics of nest-building male sticklebacks used in the study
Male character

Mean ( SD)

Range

Total length (mm)


Body weight (g)
Body condition factor (g.mm 2.8237)
Redness intensity, R (proportion)
Area of nuptial coloration, A (mm2)
Relative kidney weight (g.g1 body weight)
Relative spleen weight (g.g1body weight)
Relative liver weight (g.g1 body weight)
Pre-building lag (days)
Construction time (days)

42
42
42
42
42
38
37
38
42
42

44.60
0.94
2.05
0.46
84.4
0.045
0.003
0.024
4.0
6.0

3955
0.601.79
1.352.94
0.410.53
15.170.5
0.0270.078
0.0010.005
0.0110.035
117
112

(
(
(
(
(
(
(
(
(
(

3.32)
0.25g)
0.24)
0.03)
35.1)
0.011)
0.001)
0.005)
2.9)
3.9)

Behavioral Ecology Vol. 12 No. 4

394

Figure 3
The relationship between nest
neatness and the length of the
pre-building lag. The main figure shows the frequency distribution of observed pre-building lag periods (the time between arrival in the laboratory
and initiation of nest building)
for the 42 male sticklebacks
that completed nests in our
study. Hatched bars show
males that initiated nest building within 3 days following
transfer to nesting tanks (early
nesters) and open bars show
those taking longer than 3 days
(late nesters). The inset figure
shows the mean ( SE) nest
neatness indices of early nesters (hatched bars) and late
nesters (open bars). Early nesters built significantly neater
nests than late nesting fish (see
text for statistical details).

ture in a recent field study (Guderley and Guevara, 1998),


suggesting a hormonal link between coloration, glue production, and nest structure. However, although we found a marginally significant positive correlation between nest neatness
and the extent of sexual coloration, there was a general lack
of correlation between nest structure and male color. This
suggests either that kidney enlargement and the development
of sexual coloration are under the control of separate hormones that act at least partly independently, or that there are
factors that confound the relationship between hormone levels and sexual coloration in this population. Further research
examining the hormonal control of nuptial coloration development and sexual behaviors such as nest building would be
of considerable value in addressing this complex area.
Nest structure also correlated with temporal aspects of construction in our study. Males that began building soon after
transfer to the laboratory eventually constructed neater nests
than males that exhibited a longer lag. We can think of two
possible explanations for this pattern. First, despite collecting
males early in the season, it remains a possibility that some
males may have already constructed a nest and obtained
spawnings prior to capture. These males may have required
time to switch from a parental to a re-nesting phase, and subsequently built low-quality nests because of energetically demanding investment in earlier breeding attempts (Smith and
Wootton, 1999). Alternatively, the favorable conditions in our
study may have elevated the status of low quality individuals,
which may not naturally have become territory holders and
instead resorted to alternative (sneaky) breeding tactics in
the wild (Kynard, 1978; Rico et al., 1992). This scenario could
Table 3
Results of Pearsons correlation analyses between aspects of male
coloration and nest structure
Color measurement
Nest attribute

rA

sq-rt asin-transformed In
sq-rt asin-transformed Ic
Weight of deposited
substratum

r .312, p .047
r .233, p .159
r .199, p .206

r .211, p .186
r .006, p .972
r .020, p .901

explain both the pre-building lag, as such fish prepare physiologically for nesting, and alsoif nest quality is an honest
correlate of male qualitythe poor quality nests. Interestingly,
Jamieson and Colgan (1992) found that late-nesting males
were more likely to become sneakers in a laboratory study.
Although we can provide no evidence to distinguish between
these two hypotheses for the correlation between building lag
and final nest quality, they could be tested experimentally.
In one of the only other studies linking nesting behavior to
male traits, male common gobies Pomatoschistus microps that
built nests with little sand cover were in poorer nutritional
condition and more likely to cannibalize their offspring than
those that covered their nests more extensively (Kvarnemo et
al., 1998). We did not detect a relationship between the
weight of deposited substratum and male body condition factor or HSI, two medium-term indices of nutritional condition,
but we did find a negative correlation with relative spleen
weight. Enlarged spleens are an indicator of immune stress
associated with disease and parasite infection in fish (Arnott
et al., 2000; Bruno et al., 1998; Byrne et al., 1998). The small
number of males infected with S. solidus parasitesimportant
pathogens in our study population (Tierney, 1991)also
tended to build less compact nests.
Sticklebacks base nest site choices on many factors including the presence or absence of cover (e.g., Cleveland, 1994;
Jenni, 1972; Kraak et al., 2000), water depth (Kraak et al.,
2000; Mori, 1994) and distance to shore (see reviews by Rowland, 1994; Whoriskey and Fitzgerald, 1994). Females are
known to prefer males that build nests close to vegetation,
and such nests are more likely to last until fry-hatching (Kraak
et al., 1999b). Yet although the selection of nest site influences
mate attractiveness and the survival of embryos and fry (e.g.,
Kynard, 1978; Moodie, 1972; Sargent and Gebler, 1980), research on avian taxa has suggested that variation in the structure of the nest itself may also provide differential resistance
to adverse environmental conditions or predation attempts
(e.g., Mller, 1990). Stickleback nests are susceptible to the
action of local water currents and disturbances from predators, and both cause losses in natural habitats (Mori, 1995).
It would be interesting to know whether certain nest characteristics (e.g., compactness, neatness, or weight of deposited
substratum) influence resistance to perturbation events or
predation attempts, or female choice. Variation in nest con-

Barber et al. Nests as ornaments

struction may be particularly important in habitats where nest


site acquisition is not a reliable indicator of male quality, for
example in habitats that are structurally uniform, where natural preferences for nest sites are disrupted (e.g., in the presence of predators; Candolin and Voigt, 1998; Jones and Paszkowski, 1997) or in unpredictable habitats (Hamilton WJ et
al., 1997). Although we did not examine the effects of nest
structure on offspring performance, there is evidence from
other groups that such variation does have an important influence on the success of offspring raised from them (Bult
and Lynch, 1997; Grubbauer and Hoi, 1996; Hamilton HH et
al., 1997; Hoi et al., 1994, 1996).
Conclusions
The relationships identified in our study, between nest structure and immunological and secondary sexual characters of
the male builder, suggest that females may gain important
information regarding the male builder by inspecting a nest.
In addition, our finding that nest quality co-varies with the
development of an androgen-dependent tissuethe kidney,
which is responsible for the production of glueidentifies a
mechanism by which nest structure may reliably signal male
quality. As well as the nest having an obvious functional capacity as a receptacle for eggs, aspects of its construction may
therefore serve additionally as condition dependent ornaments.
This study arose from research funded by a UK Natural Environment
Research Council (NERC) grant (GR3/10349). All procedures were
carried out in accordance with local and national animal welfare
guidelines. We are very grateful to Sarah Kraak and Ulrika Candolin
for constructive criticism of earlier versions of the manuscript and to
Steve Arnott, Victoria Braithwaite, and Michael Hansell for helpful
comments. I.B. is in receipt of a NERC research fellowship.

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