Behavioral Ecology Vol. 12 No. 4: 390-396
© 2001 International Society for Behavioral Ecology
Nests as ornaments: revealing construction by male sticklebacks
Fish Biology Group, Division of Environmental and Evolutionary Biology, IBLS, University of Glasgow, Scotland, UK
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{at}aber.ac.uk .
Received 25 May 1999; revised 17 August 2000; accepted 24 August 2000.
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ABSTRACT |
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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 male's kidney—which secretes a glue-like protein used in nest building and whose development is androgen-dependent—correlated 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.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Animals 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 builder's 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 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 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.
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MATERIALS AND METHODS |
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Fish collection and nest building
Male sticklebacks collected at the beginning of the 1997 breeding season (mid-April) from Inverleith pond, Edinburgh, Scotland (55°55' N, 03°10' W) were transferred to the laboratory in separate containers and released into individual nesting aquaria (20 x 20 x 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 Frischknecht's
(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
4.0TM 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 0-255) 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
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.
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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).
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RESULTS |
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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 x 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)/ (length, in mm2.8237)] x 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 non-builders died before the end of the study, whereas all nest builders survived.
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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-modal distribution with peaks around 2-3 and 5-6 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).
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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 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 male's 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).
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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.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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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 kidneys—probably resulting
from low levels of circulating androgens—may 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 structure 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 explain both the pre-building lag, as
such fish prepare physiologically for nesting, and also—if nest quality
is an honest correlate of male quality—the 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 parasites—important
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.,
Møller, 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
construction 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 tissue—the kidney, which is
responsible for the production of glue—identifies 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."
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ACKNOWLEDGEMENTS |
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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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