Behavioral Ecology Vol. 11 No. 5: 465-471
© 2000 International Society for Behavioral Ecology
Combs and sexual selection in black grouse (Tetrao tetrix)
a Department of Population Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18 D SE-75236 Uppsala, Sweden b Department of Animal Ecology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18 D SE-75236 Uppsala, Sweden c University of Jyväskylä, Department of Biological and Environmental Sciences, PO Box 35, FIN-40351, Jyväskylä, Finland d Arctic Centre, University of Lapland, PO Box 122, FIN-96101 Rovaniemi, Finland
Address correspondence to P. T.Rintamäki. E-mail: pekka.rintamaki{at}ebc.uu.se .
Received 2 June 1999; revised 15 October 1999; accepted 17 December 1999.
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ABSTRACT |
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We studied supra-orbital combs in lekking black grouse (Tetrao tetrix) in relation to sexual selection at five leks in Finland 1991-1998 and four leks in Sweden 1992-1995. Comb size was estimated in two ways: by observing its natural size in the field at different behaviors ("observed comb size"), and by measuring the comb size from captured birds ("measured comb size"). The size of combs is highly variable, and individuals can change it within seconds. Males express their larger combs during display, as compared to other behaviors. Observed mean comb sizes were larger on leks with a higher number of males and a higher number of copulations. Measured and observed comb sizes and copulatory success did not significantly correlate when all males where analyzed, but a positive and significant relationship between observed comb size and copulatory success was found within males that achieved copulations. Measured comb length correlated positively with the amount of testosterone. While females were present on the lek, displaying and successful males showed the largest observed comb size. When we compared observed comb size during fighting between successful and unsuccessful males and correlated comb size of pairs of fighting males with their fighting activity, no significant differences in comb size were found. The result that comb size correlated significantly with an increase in testosterone level and that larger comb size, within successful males, predicted higher copulatory success suggests that combs may be a cue for females to assess male quality. The lack of a significant relationship between observed comb size and fighting behavior suggests that comb size either has minor importance in male-male signaling on the lek or that males may express similar-sized combs during fighting to avoid serious fights and thus risk of comb injuries.
Key words: black grouse, combs, copulatory success, sexual selection, Tetrao tetrix.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Integumentary structures in the plumage or on parts of the body have evoked the interest in their function in sexual signaling since Darwin. Such ornaments may have evolved through intra- and/or intersexual selection (i.e., they are signals between males or help females to assess males; Zuk, 1991
). Supra-orbital
combs and wattles are fairly common in gallinaceous birds, but they also occur
in other taxonomically unrelated bird families
(Holder and Montgomerie,
1993a). Brightly colored skin parts are particularly common in the
Tetraonids (Johnsgard, 1983),
and their function in a sexual selection context has mainly been studied in
nonlekking grouse species, both in the context of male-male signaling
(Allee et al., 1939;
Graves et al., 1985;
Ligon et al., 1990;
Moss et al., 1979;
Myhre, 1980) and female choice
(Brodsky, 1988;
Hannon and Eason, 1995;
Holder and Montgomerie, 1993a;
Zuk et al., 1990b). However,
few studies of the importance of fleshy structures have been done in lekking
species (Gratson et al., 1991;
see also Johnson and Boyce,
1991; Spurrier et al.,
1991). This is somewhat surprising because many lekking grouse
show conspicuous structures of this kind during display. Furthermore, the
possibility of combs serving as signals is especially plausible in lekking
species because males on the lek form tightly clumped aggregations where combs
may be observed and compared at a close distance by conspecifics. Thus, both
choosy females and competing males should have good opportunities to observe
and compare many male combs simultaneously.
Comb and wattle ornaments are usually more conspicuous in males than in
females (Owens and Short,
1995), which may indicate their function as ornaments. Expression
of combs and wattles is directly connected to androgen production (i.e.,
testosterone; Ligon et al.,
1990; Moss et al.,
1979; Owens and Short,
1995; Zuk et al.,
1995), whereas feather ornament size seldom depends on current
levels of testosterone secretion (Stokkan
et al., 1988; Witschi,
1961). It is also possible that androgens not only increase the
expression of sexual ornaments, but also suppress the immune function
(Folstad and Karter, 1992).
Thus, combs may be particularly useful as honest signals for prospecting
females, if these traits provide females with accurate information on current
male condition. For example, in red jungle fowl (Gallus gallus), the
size of combs and wattles may reflect individual variation in parasitemia,
disease resistance, nutritional status, and general health
(Allee et al., 1939;
Johnson et al., 1993;
Zuk et al., 1990a). An
alternative, or additional explanation for the occurrence of combs and wattles
is that they may be important in male-male aggressive signaling
(Zuk, 1991). Studies in red
grouse (Lagopus lagopus scoticus), red jungle fowl, and rock
ptarmigan (Lagopus mutus) have indeed suggested that variation in the
size of fleshy structures are linked to variations in levels of aggression
(Allee et al., 1939;
Graves et al., 1985;
Holder and Montgomerie, 1993a;
Moss et al., 1979).
In the present study we examined whether comb size was related to testosterone levels, to a suite of behavioral and territorial traits, and to copulation success. We also investigated whether comb size differed among rivaling males.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Data collection
During 1992-1998 we gathered data on observed comb size from four black grouse leks in central Sweden and from one in central Finland. In Sweden one lek was studied in 1992, 1993, and 1995 (lek no. 1), another in 1993 and 1995 (lek no. 2), and two in 1997 (leks no. 4 and 5); the data from Finland derives from one lek in 1995, 1997, and 1998 (lek no. 3). For details of the study areas and general methods, see Rintamäki et al. (1995a
,b,
1999) and
Höglund et al.
(1997). All leks used in
observed comb size analyses were situated on open bogs, and lek size varied
from 3 to 13 resident males (mean ± SD, 7 ± 3 males). In
Finland, the majority of the males (77%) were color banded, enabling us to
recognize the birds individually; in Sweden only a few males were ringed.
Resident males (see below) on leks are very faithful to specific territories
and show individual plumage variation, allowing identification of individuals.
To avoid replication of data on individuals, we included only the first year
of observation for males present at a lek in more than 1 year. Leks were
observed with binoculars (8-10x) and telescopes (20-60x) from
hides positioned close to leks (10-40 m to males).
Male characteristics
For each male, we used the number of observed copulations as an estimate of
his total copulatory success. In black grouse, females usually copulate only
once, if a copulation is not disrupted, and DNA fingerprinting has confirmed
that the male seen copulating sires all chicks in the clutch
(Alatalo et al., 1996a). We
examined male behaviors, territory characteristics, and the number of males at
the lek in the context of both measured and observed comb size (these measures
are defined below). Behavior was divided into three main categories: display
(rookooing; the principal vocal display, flutter jump, and hissing), fighting,
and other activities (standing still, walking, preening, eating). We also
noted individual differences in rates of lek attendance. Activities were
calculated as proportions of how much time each male spent in each activity in
relation to other activities. Rate of attendance was calculated as presence on
the lek in relation to the male(s) with the highest attendance; the male with
the highest attendance was given a score of 100%. During scan sampling, we
plotted each male's location to the closest 1 m on the maps using a 10 x
10-m grid system on each lek. Territory location was then defined in terms of
the distance from the territory center to the lek center (median of all male
positions), and territory size was calculated as the diameter (meters) of an
ellipse within which 90% of the observation points were situated (average for
horizontal and vertical diameters). This method excludes occasional positions
outside a male's territory. We included only resident males that were
regularly attending the lek (25% attendance or more in relation to the most
attendant male) because males with lower values were often nonterritorial
juveniles or males that had unstable territories. These males were difficult
to identify during the 1- to 2-min scan sampling of the resident males. Eight
males were occasionally seen and omitted (11% of the males included in the
study), with a mean ± SD attendance rate of 11% ± 7%.
Combs
The red combs of grouse are distinct during the mating season
(Gjesdal, 1977), and males are
able to change comb size rapidly (in a few seconds;
Rintmäki et al., personal observations from
captured males) by controlling blood circulation in the comb tissue
(Holder and Montgomerie,
1993a). However, although males can control comb size, they cannot
hide their combs completely. Because the size of the comb of captured males
does not provide accurate information about how males express combs on the
lek, we developed a rank system (1 to 5, observational comb size; see
Figure 1 for explanations) by
which we estimated each male's comb size when scan-sampling the males. In
addition to observed comb size estimates, we measured combs of 17 adult males
captured during the mating season at five leks in 1991 in Finland. Different
studies of grouse have used different methods to estimate comb size (see,
e.g., Brodsky, 1988;
Holder and Montgomerie, 1993a;
Zuk et al., 1992). As in the
red jungle fowl studies (e.g., Chappell et
al., 1997) we believed comb length to be the most reliable measure
because the length appears to change less rapidly as compared to vertical comb
height. We measured the maximum nonflattened horizontal comb length (to the
nearest 0.1 mm) from one side of the head by using digital calipers.
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Observational comb size estimates were taken when females were both present
and absent from the lek (leks 3-5 only). On leks 1-2, the low number of female
visits prevented us from using observations from these leks in the analyses.
Black grouse males respond to the presence of females by increasing their
activity
(Höglund et
al., 1997), and we therefore checked whether comb size was
affected by female attendance.
Reliability of observational comb estimates
In spite of detailed instructions to observers, the observed comb size is
likely to be more prone to errors among observers than are the direct
measurements. To see how reliable our observed comb estimates were, we
compared between-observer variation at lek 3. At a given moment two observers
independently ranked a specific male comb size. The observation procedure was
repeated 25 times on a total of 5 mornings including 10 different males and 7
behaviors. Of 25 comb estimates, 23 were identical, and both the observers
obtained a mean rank of 4.0 (SDs for observers were 0.58 and 0.65) with
identical minimum and maximum observed comb size ranks of 3.0 and 5.0. The
result was also significantly repeatable
(Lessels and Boag, 1987;
R =.89, F = 17.7, p <.001). In the two cases
when observers' estimates differed, the estimate difference was one rank.
Therefore we consider that estimated observational comb size is accurate
enough to detect differences between males and behaviors (note also sample
sizes and SEs given in Table
1). To correct for lek site and study year and to minimize
possible differences among observers, we used Kendall's nonparametric partial
rank order correlation analysis.
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Comb size during different behaviors and territorial features, the
relationship with copulatory success, and the difference between fighting
pairs of males
To study how observed comb size was related to different behaviors and
territorial features, we first performed correlations of observed and measured
comb sizes with different male characteristics
(Table 2). Thereafter we
correlated measured and observed comb sizes during different behaviors with
the total copulatory success of each male
(Table 3). Finally, to study
observed combs and the male-male signaling hypothesis, we performed two tests.
We first looked at differences in observed comb size between different
fighting pairs of males that had different copulatory success using paired
t tests. If successful males show larger observed combs during
fighting, this might imply that combs are used by males to signal dominance
relationships (Graves et al.,
1985; Holder and Montgomerie,
1993a; Moss et al.,
1979). Second, if there is no significant difference between
observed comb sizes of fighting males with different copulatory success, combs
may not be important in signaling dominance between males, or alternatively,
signaling similar-sized combs may prevent fights that could cause comb
injuries. To see if the comb sizes of pairs of fighting males depended on how
often they fought with each other, we correlated comb size differences of
these male pairs during fighting with the their fighting activity (the number
of fights by each male pair divided by the total number of fights of all male
pairs).
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Measured comb and testosterone
The testosterone measurement procedure has been reported elsewhere
(Alatalo et al., 1996b).
Briefly, we captured 17 males during the mating season between 16 April and 7
May. Blood was collected from the basilic wing vein, and plasma was separated
with a centrifuge (10 min at 10,000 rpm). Plasma levels of testosterone were
measured (in duplicate) by a single radioimmunoassay after extraction and
partial purification on diatomaceous earth-glycol microcolumns. To study the
relationship between measured comb size and testosterone levels, we correlated
comb horizontal length with testosterone levels. We used one-tailed p
values because the expectation based on earlier studies (see above) was that
larger comb size is related to higher testosterone titers.
Statistical analyses
We used both parametric and nonparametric tests to analyze our data. All
tests are two-tailed unless otherwise stated. Resampling (randomization) tests
were done by simulating original values 5000 times. When more than one
variable was included in the analyses, we corrected the p values for
multiple tests (Ury, 1976).
Means include SD or SE values.
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RESULTS |
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Comb expression
Males showed the largest combs when rookooing (mean ± SD = 3.7 ± 0.6, n = 73 males) and fighting (3.5 ± 0.5, n = 65), with a significant difference between these behaviors (Wilcoxon matched-pairs signed-rank test, t = 4.05, n = 61, p <.001). When males were inactive (engaged in "other activities"), their comb sizes were clearly smaller (2.8 ± 0.8, n = 69) than when fighting (t = 6.25, n = 59, p <.001) and rookooing (t = 7.02, n = 69, p <.001). Comb size estimates showed the same direction during female presence, although observed comb sizes were higher for all behaviors when females were present (Table 1).
The mean observed comb size was larger on larger leks than on smaller leks (females not present; Spearman rank order correlation: rs =.68, n = 10 leks, p <.05). The relationship was even more clear when we correlated observed mean comb size during display with lek size (rs =.71, n = 10, p <.01, Figure 2) and fighting (rs =.77, n = 10, p <.01), but not in the case of other activities (rs =.18, n = 10, ns). Positive and significant correlations between observed comb size and lek size may suggest that males with larger combs prefer larger leks. That observed comb size during other activities was much more weakly correlated with lek size than other behaviors suggests that this is not the case. However, to test this directly, we compared male observed comb sizes from which we had information from 2 years at different lek sizes. We then found that eight out of nine males had, on average, 0.5 smaller (mean ± SD = -0.45 ± 0.39) observed comb ranking when displaying on smaller leks than on larger leks (sign test, p <.02).
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Combs, male characteristics, and testosterone
Table 2 summarizes
correlations between male mean observed and measured comb size and different
behaviors and lek attributes. After correcting for multiple tests, none of the
characteristics correlated significantly with male observed comb size,
irrespective of female presence. Further, measured comb size was not
significantly correlated with male territorial features and behavioral
characteristics. Measured comb length was significantly correlated with
log-transformed testosterone levels, both in all males (r =.45,
n = 17, p =.04), and within successful males (r
=.58, n = 9, p =.05).
Comb size and female presence
We examined the effect of female presence on comb size on one lek (lek 3,
years 1995, 1997, and 1998) by following the comb sizes of the same males
(n = 22 different males including 5 nonterritorial individuals) when
females were not present on the lek and when one or more females were present.
The interval between subsequent observations was 
10 min, allowing us to
detect male responses in comb size in relation to female presence. The
observed mean comb size (mean ± SD) during all behaviors (display,
fighting, other) was significantly affected by the presence of females (comb
size, females not present: 3.84 ± 0.68; females present: 4.02 ±
0.70; Wilcoxon signed-rank test: t = 4.21, n = 163,
p <.001, where mean = comb size according to a rank 1-5). The
result was the same despite male behavior (display, females not present: 4.08
± 0.71 and present: 4.30 ± 0.68, t = 3.05, n =
79, p =.002, fighting, females not present: 3.63 ± 0.57 and
present: 3.78 ± 0.62, t = 2.6, n = 73, p
=.009). Because female presence influences male comb size, we analyzed our
data both when females were present and when they were not.
Combs and copulatory success
Mean observed comb size of all males on leks correlated significantly with
the number of copulations on the lek (Spearman rank order correlation:
rs =.88, n = 10 leks, p <.01,
Figure 3). The relationship was
positive, but nonsignificant, when we correlated mean measured comb size and
the number of copulations (rs =.32, n = 4 leks,
ns), probably because we did not have information on measured comb sizes of
all males and because of low statistical power due to few leks. When all males
where included in the analysis, mean observed comb size, comb size during
rookooing, fighting, and other activities were not significantly correlated
with male copulatory success, either when females were present or absent
(Table 3). During female
presence at a lek with only successful males (
1 copulation) included in
the analyses, however, males with the largest mean combs and largest combs
during rookooing enjoyed the highest copulatory success
(Table 3, Figure 4), although the
relationship was not clearly linear. There seems to be a threshold within
successful males; those with observed comb size 4 during display seem to
enjoy higher copulatory success (Figure
4). Measured comb size was not significantly correlated with
copulatory success within successful males, although the association was in
the same direction as that obtained from observed comb size analysis
(Table 3).
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Comb size and male-male signaling
The mean difference in comb rank between two fighting males was on average
0.12 when we included only successful males in the analyses (in the paired
test the observed comb size during fighting of more successful males was
compared to that of less successful ones, t = 0.91, df = 21,
p =.37, n = 3.3 ± 3.3 comb observations per fighting
male pair). In the previous analysis more successful males had, on average,
slightly larger combs. When we added into the previous analysis male pairs
that had higher copulatory success versus no success, the mean difference in
comb rank during fighting was on average -0.07 (t = -0.66, df = 63,
p =.51, n = 4.7 ± 6.0 comb observations per fighting
male pair). Finally, unsuccessful (copulation = 0) males showed the least
difference in comb size during fighting (mean difference = -0.05, t =
-0.29, df = 24, p =.77, n = 3.4 ± 5.2 comb
observations per fighting male pair). When we correlated the observed comb
size difference of each male pair with their fighting activity, we did not
find a significant relationship (all males included: rs
=.07, n = 89, ns, and only successful males: rs
=.05, n = 22, ns).
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DISCUSSION |
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Combs and female choice
It has been suggested that individuals have to trade resources allocated to maintain immunological defense against an increased expression of sexual ornaments (Folstad and Karter, 1992
; Sheldon and Verhulst,
1996). The hypothesis predicts that hormones cause the expression
of sexual ornaments while suppressing immune function, and that the costs of
an ornament would be lower for individuals in better physiological condition
(Nur and Hasson, 1984;
Sheldon and Verhulst, 1996).
In willow ptarmigan and red jungle fowl, comb size depends on individual
differences in testosterone levels
(Stokkan, 1979;
Zuk et al., 1995), and red
jungle fowl males (e.g., Ligon and Zwartjes,
1995a,b;
Ligon et al., 1998;
Zuk et al., 1990b) as well as
ptarmigan males (Brodsky, 1988;
Hannon and Dobush, 1997;
Hannon and Eason, 1995) with
larger combs tend to enjoy higher copulation success than males with smaller
combs. High testosterone levels clearly are associated with black grouse
copulatory success (Alatalo et al.,
1996b), and we here add the finding that measured comb length
correlates positively with male testosterone levels. In addition, larger
observed comb size predicts higher copulatory success among successful black
grouse males. Hence, results obtained from both nonlekking and lekking species
generally fit with the expectations of the immunocompetence handicap
hypothesis and suggest that females may use comb size to evaluate male current
condition.
In black grouse, using the data of all males, however, copulatory success
was not associated with comb size, either when measured at capture or when
observed in undisturbed birds participating at the lek. A similar lack of
significant association between comb size and copulatory success has also been
found in another lekking grouse species (e.g., the sharp-tailed grouse,
Tympanuchus phasianellus;
Gratson, 1993;
Gratson et al., 1991). The
distribution of copulations between males is typically skewed on leks, with
only a few of the males achieving many copulations
(Alatalo et al., 1992;
Höglund and
Alatalo, 1995; Kokko and
Lindström, 1997;
Widemo and Owens, 1995). In
the leks included in this study, 64% (SD = 18.4) of the males had no success
at all, while the most successful male on a single lek achieved, on average,
63% (SD = 22.5) of the copulations. In the black grouse, as well as in lekking
species in general, successful males settle in central territories
(Fiske et al., 1998). Thus it
is possible that particular males, depending on other characteristics such as
territory history (Kokko et al.,
1998,
1999) and age
(Kokko, 1997), may be rejected
as mates whatever comb size they are able to show. As an example, a new adult
male displaying in the periphery at lek 3 showed a nearly maximum mean
observed comb size of 4.95 but failed to mate with any female, whereas the two
top males near lek center both achieved 19 copulations and had mean observed
comb ranks of 3.53 and 3.49. Given that females are unlikely to base their
choice solely on comb size, we used only the successful males in the analysis
(more than one copulation) and found that males with larger observed comb
sizes were more successful in achieving copulations. The result was in the
same direction but not significant among measured males. Moreover, observed
comb size during female presence showed a stronger relationship with male
copulatory success than did observed comb sizes when the females were not
evaluating males.
The relationship between comb size and copulatory success suggests that
male comb size may be an honest signal of male quality for black grouse
females. How, then, can we explain the positive relationships between observed
comb size and lek size as well as the relationship between comb size and the
number of copulations? High quality males are more likely to join larger leks,
which black grouse females also seem to prefer
(Alatalo et al., 1992).
However, our result that the same males seem to show smaller combs when
participating in a smaller lek does not support this idea. Also, male comb
size was affected by female presence. We therefore suggest that both the
number of males and the presence of females induce male testosterone
secretion, which, in turn, affects comb size (but see also
Alatalo et al., 1996b;
Wingfield et al., 1990).
Interestingly, the number of copulations was much lower on Swedish leks. This
may be partly due to the lower population density in the Swedish study area
(Höglund and
Stöhr, 1996;
Lindström,
1994).
Combs and male-male signaling
Another reason apart from female choice for the evolution of combs is that
they may be important signals in interactions between males
(Hansen and Rohwer, 1986;
Holder and Montgomerie,
1993a,b;
Zuk, 1991). This explanation
could be particularly pertinent on leks, where males are tightly clustered and
territories are adjacent to each other. Hence, males may use combs to signal
their intentions to other males. Observed comb size clearly differed depending
on behavior, being smaller when males were inactive, medium sized when they
were fighting, and largest during display. This suggests that males indeed
control their comb size according to their behavior.
Similar to our findings, no significant effects of larger comb size on
increased fighting behavior were found in the sharptailed grouse
(Gratson, 1993), which is also
a lekking species. To test directly whether black grouse males use their combs
during fighting, to show dominance, or, on the other hand, whether they hide
their combs (at such situations combs may be of similar sizes), we compared
comb sizes during fighting between pairs of two opponents, one of which was
more successful than the other in achieving copulations and also in situations
between pairs of males that had no success. The results suggested that
observed comb size did not differ significantly between fighting males, either
when comparing males with different success rates or when comparing males that
had no success. In addition, male pairs that fought more in relation to other
male pairs did not seem to differ in comb size.
During fights, males seem to aim to damage the comb of the opponent
(Owens and Short, 1995), and
it has been suggested that because combs are frequently attacked during
male-male interactions, the condition of these ornaments may honestly
advertise male fighting ability (Holder
and Montgomerie, 1993a). Because females show a preference for
combs and males try to hit other males' combs, we suggest that showing less
than maximally erected combs during fights may be a way to avoid injuries and
thus keep the combs in good condition for females to evaluate.
Conclusions: sexual selection
Exaggerated secondary sexual characters, such as combs and wattles, may
provide sampling females reliable cues to use as honest signals of male
quality. We did find support for this idea; black grouse females preferred
males with larger observed combs (and a similar trend for measured combs),
although the result was significant when the analysis was based on successful
males only. Our results that black grouse males showed similar size combs
during fights regardless of their copulatory success and fighting intensity
may suggest that males "hide" their combs during fights in order
to protect them (Holder and Montgomerie,
1993a). In conclusion, we have found evidence that females may use
comb size to evaluate males, but also that males diminish their comb sizes in
male-male interactions, probably to keep them in good condition. Hence we
suggest that the most likely explanation for the existence of combs is female
preference for them.
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ACKNOWLEDGEMENTS |
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The data were collected with the help of Matti Halonen, Matti Hovi, Esa Huhta, Jukka Jokimäki, and Pirkko Siikamäki. We also thank the Finnish Ringing Centre for its cooperation. We received helpful comments on earlier versions of the manuscript from Peder Fiske, Staffan Ulfstrand, Marlene Zuk, and two anonymous referees. R.V.A and O.R. were supported by the Finnish Academy, P.T.R. by the Emil Aaltonen foundation and Nordisk forskerutdanningsakademi (NorFA), E.K. by NorFA, and J.H. and A.L. by the Swedish Natural Sciences Research Council.
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