| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Behavioral Ecology Vol. 13 No. 1: 32-41
© 2002 International Society for Behavioral Ecology
The kinds of traits involved in male—male competition: a comparison of plumage, behavior, and body size in quail
Department of Biology, The University of New Mexico, Albuquerque, NM 87131, USA
Address correspondence to J.C. Hagelin, who is now at the Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Road, Unit 3043, Storrs, CT 06269-3043, USA. E-mail: hagelin{at}sp.uconn.edu .
Received 7 August 1999; revised 27 October 2000; accepted 8 February 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
I compared the role of ornate plumage, behavior, and body size during male—male competition in two species of New World quail. Gambel's quail (Callipepla gambelii) is a highly ornate and dichromatic species, whereas scaled quail (C. squamata) is unornamented and monochromatic. During paired contests between unfamiliar males, high rates of testosterone-mediated behaviors (tidbitting, calling) and large body size (mass, tarsus, and tail length) corresponded to winners. In the highly ornate Gambel's quail, male head plumes also influenced the outcome of contests. Plume enhancement made Gambel's quail more likely to win contests, whereas plume removal made males more likely to lose. Plume position also reflected male status. Winning males erected plumes, whereas losers frequently flattened them. Some plumage ornaments, such as belly patches, did not play a primary role during male contests. Unlike static ornaments, head plumes are highly modifiable and likely signal immediate information regarding a male's intent, similar to a coverable badge. Combined, intrasexual selection favored dynamic traits (fast display rates, modifiable ornaments) and static traits (body size) as indicators of male condition or motivation. In scaled quail only, male size was favored both by male—male competition and female choice. Accordingly, the degree of size dimorphism (tarsus length) is greater in scaled than in Gambel's quail. The frequency of overt aggression (chases, pecks, displacement) also differed between species. Gambel's quail were very aggressive, and subordinates often challenged their opponents. In contrast, scaled quail were less aggressive, and subordinates rarely disputed rank. Interspecific comparison indicated differences in the maintenance of male status and possibly in the honesty of signaling. Both appear to be related to differences in social system.
Key words: behavior, Callipepla gambelii, Callipepla squamata, male—male competition, plumage ornaments, quail, sexual selection.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Intersexual mate choice and intrasexual competition are responsible for the evolution of numerous kinds of secondary sexual traits (reviewed by Andersson, 1994
). Some traits
appear to be relatively static, such as body size, whereas others are more
dynamic or modifiable, such as behavior
(Hill et al., 1999). The same
is true for ornaments, which may be fixed, as opposed to those that are
modifiable with regard to position, size, or hue (e.g.,
Hansen and Rohwer, 1986;
Zucker, 1994).
To understand sexual selection, one must determine the kinds of traits
involved and why they are important. Numerous studies suggest that honest or
condition-dependent signals often play a role; these include both static and
dynamic traits that reliably convey the condition or status of individuals
(e.g., Hill, 1991;
Ligon et al., 1990). Honest
traits may also function in both intra- and intersexual selection
(Berglund et al., 1996;
Mateos and Carranza, 1999)
because reliable assessment of a prospective mate or opponent can result in
direct or indirect benefits to the assessor
(Hill, 1994;
Kirkpatrick and Ryan, 1991;
Kodric-Brown and Brown, 1984;
Rohwer, 1982).
In birds, the bright or ornate plumage of males often exhibits
semipermanent or fixed "badges," such as belly patches, as well as
more dynamic "coverable badges," such as the red epaulettes of
blackbirds, which are modifiable in size
(Hansen and Rohwer, 1986;
Rohwer, 1982;
Røskaft and Rohwer,
1987). Both kinds of ornaments can signal status (Mateos and
Carranza,
1997a,b;
Pärt and
Qvarnström, 1997;
Peek, 1972;
Rohwer, 1975) or influence
mate choice (e.g., Jones and Hunter,
1999; Mateos and Carranza,
1995; Savalli,
1994). Yet, in some species, ornate plumage traits are not the
primary factors involved in sexual selection
(Beani and Dessi-Fulgheri,
1995; Buchholz,
1995,
1997;
Hagelin and Ligon, 2001;
Ligon and Zwartjes, 1995;
Ligon et al., 1990; Rohwer and
Røskraft, 1989. Like other signals, plumage ornaments appear to vary in
their reliability as indicator traits
(Badyaev and Hill, 2000;
Hansen and Rohwer, 1986;
Rohwer, 1982) and may
therefore also vary in function as a social signal.
To gain a better understanding of the kinds of traits associated with
sexual selection, I examined two species of New World quail that exhibit
different secondary sexual characteristics. Gambel's and scaled quail
(Callipepla gambelii and C. squamata) differ drastically
with regard to plumage dichromatism, despite their phylogenetic affinity
(Zink and Blackwell, 1998).
Male Gambel's quail exhibit a long head plume, rusty head patch, and white and
dark belly patches, whereas females are dull in color and less ornate. In
contrast, both sexes of scaled quail are predominately unornamented and
monochromatic (Johnsgard,
1973). Studies of mate choice suggest that male plumage ornaments
are not the primary traits involved in female mating decisions of both species
(Hagelin and Ligon, 2001). An
alternative explanation is that ornaments function during male-male
competition.
Male quail are often aggressive before and during the breeding season
(Ellis and Stokes, 1966;
Johnsgard, 1973). A
male-biased sex ratio is also present in wild populations
(Brown and
Gutiérrez, 1980), providing a
basis for intrasexual conflict. The sex bias is more pronounced in the more
ornate Gambel's quail (Brown and
Gutiérrez, 1980), suggesting that
ornaments may be more emphasized during male contests than in scaled
quail.
The primary objective of this study was to explore and compare male-male competition in both quail species in order to understand the kinds of signals involved in intrasexual selection. In a series of two experiments, I examined the role of ornamental, behavioral, and body-size traits involved in contests between two unfamiliar males. First, I identified traits associated with winners and losers of male contests. Next, I manipulated plumage to examine whether ornament alternations affected the outcome of competitive interactions. The two experiments allowed me to characterize traits that correlated with or were causally related to male status.
The study presented here was conducted in parallel with an investigation of
female mate choice (Hagelin and Ligon,
2001). A secondary aim was to examine the relationship among
sexually dimorphic traits, male status, and female choice. Because intra- and
intersexual selection can affect traits either jointly or separately
(Moore, 1990), differences in
sexual selection can provide insight into patterns of dimorphism between
species (e.g., Webster, 1992;
but see Badyaev and Martin,
2000). I predicted that if both intra- and intersexual selection
favored a particular trait in one species of quail, but not the other, the
magnitude of trait dimorphism may differ between the two species.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Quail were purchased from gamebird breeders as fertile eggs or as 1- to 6-week-olds between June and July 1995-1997. All birds were hatched in incubators and kept in brooders until approximately 7 weeks of age, at which time they were moved to 5 x 7 x 4 m outdoor flight pens. Groups that originated from the same breeder were reared together and visually isolated from other groups. Birds were fed Purina Start and Grow crumble (17% crude protein content), millet, wild vegetation, and water ad libitum. Each individual was banded with a unique combination of colored leg bands as well as a band indicating its rearing group. In January, the sexes were separated into different flight pens. In early March, cohorts of five to seven males that had been reared together were moved to pens identical to those used for male contests (1.25 x 3.25 x 2 m), where they remained for at least 2 weeks before trials began.
Male contests
All male contests took place during the breeding season (late April-late
July) of 1995-1998. Pairs of males were randomly selected and consisted of
individuals that were unfamiliar with each other. The same pairs of males used
in this study were involved in experiments of female mate choice
(Hagelin and Ligon, 2001).
Males were visually isolated from each other before and during female choice
experiments. At least 5 days elapsed before males were used in an intrasexual
contest.
I conducted two experiments involving male contests. First, I used pairs of unmanipulated males to identify any relationship among male status and ornament size, body size, or behavior rates. In the second experiment, I manipulated plumage traits to determine any causal relationship between feather ornaments and winners of paired encounters. Males were used only once in each experiment, except in plume removal trials of scaled quail (see manipulation experiments below). Each pair of males was unique, and individuals participated in no more than one contest per day.
Contest protocol
Male contests were conducted on neutral ground in a 1.25 x 3.25
x 2 m arena that was visually isolated from all other birds. The arena
contained shelters and perches where individuals could safely withdraw. Birds
were observed through a one-way window. After capture and before the start of
the trial, each male was isolated for 3 min in a separate 0.5 x 0.5
x 0.5 m cage covered by a towel. Males were then simultaneously released
into the arena.
A typical trial lasted 10-15 min. At the start, males usually called and displayed behavioral threats to each other. Displays escalated until birds expressed one of three forms of overt aggression: pecking, chasing, or displacement (described below). A trial ended when an opponent no longer attempted to fight, but rather fled the interaction. This often occurred after the first bout of overt aggression, although some opponents fought back before yielding. Trials were run just long enough to determine an asymmetry in male aggression; no male was injured in any trial.
During male contests, I recorded the following displays for each individual:
- Vocalizations, different calls given by males
(Ellis and Stokes, 1966;
Schemnitz, 1994). I recorded
the number of each call type.
- Simple tidbitting, a ritualized foraging display also used during courtship
(Hagelin and Ligon, 2001;
Stokes and Williams, 1971).
During male contests, simple tidbitting appeared to act as a threat.
Aggressors pecked intermittently at the ground when in visual contact with an
opponent. After a fight, losing males sometimes pecked at the ground rapidly
with a hunched body posture and flattened plume (or crest), as if to indicate
submission.
- Formal tidbitting, more ritualized than simple tidbitting, is used during
courtship as well (Hagelin and Ligon,
2001). Males fluff out body and flank feathers while pecking at
the ground. In Gambel's quail, formal tidbitting is a frontal display
accompanied by a unique vocalization, whereas in scaled quail, it is a more
quiet, lateral display (Hagelin and Ligon,
2001).
Overt aggression included chases, where an aggressor typically ran after
its opponent with its beak open, neck outstretched, and plume (or crest)
flattened (Ellis and Stokes,
1966). If an opponent did not fight back, it was often pursued
until it sought shelter. Another form was pecking: an aggressor usually pecked
its opponent at the back of the head or grabbed at wings or back feathers.
Bouts of two or three pecks were common. The third type of aggression was
displacement: upon approach of an aggressor, the opponent moved out of the
way, apparently to avoid conflict.
Measurements
I measured plumage ornaments and body morphology immediately after a
contest. Each individual was measured two more times within 48 h of a trial,
and multiple measures of each trait were averaged. For Gambel's quail,
ornamental measurements included flattened head plume length (distance from
the base of the plume to the tip of the longest plume feather); area of the
rusty head patch (mm2), which is length of the patch (distance from
the base of the head plume to the midpoint of the posterior edge of the patch)
multiplied by patch width (distance between the tips of the two occipital
stripes that outline the sides of the patch); and area of the dark and light
belly patch (mm2). Belly patch areas were determined by multiplying
patch length (distance from the midpoint of the leading edge of the patch to
the midpoint of the bottom edge) by patch width (distance across the
horizontal midline). The dimensions of all patches were measured with digital
calipers.
I used two subspecies of scaled quail. Males of C. s.
castanogastris have a chestnut-colored belly patch, whereas males of
C. s. pallida do not (Schemnitz,
1994). Measurements for scaled quail included crest length and,
where applicable, area of dark belly patch. The protocol for each was like
that described for Gambel's quail. When I tested for differences in belly
patch (see manipulation experiments below), one male of each subspecies was
used. For unmanipulated contests, I randomly selected pairs of unfamiliar
males.
For both species, body size traits (in mm) included mean tarsus length, mean flattened wing chord, tail length, and culmen length (base of cere to tip of beak). I determined mean measures of tarsus and wing length by averaging the length of left and right appendages. Mass was measured to the nearest gram.
In a preliminary investigation, 10 male pairs of each species were tested 3 times, with at least 2 days elapsing between trials. The winner dominated its opponent in at least two of the three trials. In most cases, the winner of the first trial also won the second trial (17/20 pairs: 7/10 pairs for Gambel's quail, 10/10 pairs for scaled quail), suggesting that the protocol for determining winners was accurate, and dominance status within a pair was fairly stable. Behavior of the two subspecies of scaled quail was indistinguishable, indicating that birds primarily differed with regard to belly patch. To minimize stress to the birds, subsequent experiments involved a single contest between each male pair. All experiments were conducted under Animal Welfare Assurance A4023-01 and University of New Mexico Animal Care Protocol 9801-B.
Manipulation experiments
Pairs of males were matched for body size (tarsus, within 1 mm; weight,
within 7 g), and one member of each pair was randomly selected to have one or
multiple ornament(s) manipulated. Table
1 describes the plumage manipulations for both species (see also
Hagelin and Ligon, 2001).
Whenever one ornament was manipulated, care was taken to match males for the
size of other ornaments. Head plumes (or crests) were matched within 2 mm.
Because the size of dark belly patches was quite variable in both species, I
classified males into five categories (1 = smallest patch size, 5 = largest)
by matching each individual as closely as possible to photographs of museum
specimens that represented each size category. Males in a pair were matched
such that their belly patches belonged to the same size category. Due to a
limited number of birds at the time of the crest removal experiment, 20 male
scaled quail were used twice (Table
1). Each pair of males was unique. During a male's first trial it
acted as the control, and in the second trial the male's crest was removed.
Only one male lacked a crest in both trials.
|
Facial ornaments in Gambel's quail
The number of times each male altered its head plume (fully erect versus
flattened) or piloerected its rusty head patch (up versus down) was scored in
27 trials of Gambel's quail. Of these, 15 trials involved unmanipulated pairs,
and 12 trials involved belly patch manipulations, in which facial ornaments of
males remained intact (see manipulation experiments above). I used scores to
calculate the rate at which these ornaments were markedly repositioned.
Statistical analyses of male contests
Interspecific comparison of overt aggression
For each unmanipulated male, I summed the number of pecks, chases, and
displacements for each individual and divided by trial length to calculate an
aggression rate. Because rates were not normally distributed, I used a median
test to compare the rates of winning males between species. I also used a
median test to compare the relative amount of aggression (winner minus loser
male) directed toward competitors. I did not compare interspecific rates of
aggression for losers because losing scaled quail retaliated infrequently.
Instead, for each species, I tallied the number of losers that exhibited at
least one act of aggression toward a winning male. I then tested for
interspecific differences via a two-tailed Fisher's Exact test.
Trials of unmanipulated males
For each species, I subtracted the loser's trait from that of the winning
male and ran winner minus loser (W-L) scores in two-tailed Wilcoxon
signed-rank tests. All behaviors were converted to rates (e.g., number of
vocalizations/trial length) and analyzed via the same method. Spearman rank
correlations were also run for traits that correlated with winning.
Due to the large number of signed-rank tests, the risk of Type I error is
high, and some variables may appear significant by chance
(Rice, 1989). However, the
Bonferroni adjustment (p =.05/number of tests) may be too
conservative, increasing the risk of Type II error. I applied the Bonferroni
adjustment to groups of variables that represented different types of male
traits (ornamental, body size, and behavioral). This method provided a
biologically meaningful way of decreasing Type I error. I also analyzed W-L
scores of all traits simultaneously in a logistic regression with a stepwise
selection procedure. Logistic regression identified independent traits that
best described winners.
Body size sometimes influences the size of ornaments (e.g., larger birds typically have larger crests). When ornamental and body size traits were both associated with winning, I asked whether winners had larger ornaments than losers, even after accounting for differences in size. I ran a linear regression of ornament size against the first principal component of body size (mass, tarsus, wing). Residuals of this regression represented ornament size after the effect of body size had been removed. Ornament residuals were converted to W-L scores and run in a Wilcoxon signed-rank test to determine if winners still differed from losers. Ornament residuals were also used in multiple logistic regression.
Manipulation experiments
I used bionomial tests to determine whether ornament manipulations affected
the outcome of trials. When I removed ornaments, I expected males to have an
increased likelihood of losing. When I augmented ornaments, I predicted that
more ornate males would win. Because each male was used twice during the crest
removal experiments of scaled quail, two data sets were analyzed: the first
trial of each male (n = 10), and all trials (n = 20).
When a manipulation significantly affected trial outcomes, I examined how the ornament's signal content changed by comparing trial length and behaviors between manipulated and unmanipulated contests. If, for example, manipulations increased the asymmetry between males, contests may be resolved more quickly than unmanipulated trials. Likewise, males may be more likely to challenge opponents that lacked ornaments, but less likely to oppose those with enhanced ornaments. I tested for differences using two-sided t tests of unequal variance. Finally, some Gambel's quail involved in an unmanipulated trial were later used in a plumage manipulation. Therefore, I examined any changes in an individual's status following plume removal or enhancement via a Fisher's Exact test. Changes in status for all other manipulations were examined using a binomial test.
Comparisons of male status and female choice
Because the same pairs of males in this study had been used in a parallel
experiment of female choice (Hagelin and
Ligon, 2001), I asked whether winners of intrasexual contests were
the same as those of intersexual mate choice. For each species, I tallied the
number of dominant males that had also been chosen by a female versus those
that were not. I evaluated this pattern with a binomial test. I also assessed
interspecific differences in intra- and intersexual selection with a Fisher's
Exact test.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Interspecific comparisons of overt aggression
Winning males of Gambel's quail exhibited higher rates of overt aggression (pecking, chasing, displacement; mean = 12 acts/15 min) than those of scaled quail (mean = 5 acts/15 min; Z = 2.75 p =.006). On average, winning Gambel's quail exhibited eight more aggressive acts per 15 min than losers, whereas dominant scaled quail exhibited only three (Z = 3.01, p =.003). Subordinate males also retaliated more frequently in Gambel's quail (14/39 trials = 36%) than in scaled quail (3/40 trials = 8%; Fisher's Exact p = 0.002)
Unmanipulated pairs of males
A total of 79 male-male contests produced clear winners (n = 39
trials of Gambel's quail, n = 40 trials of scaled quail). In both
species, rates of male threats, such as calling and tidbitting, were faster in
winners than in losers (Tables
2 and
3). All behaviors used in this
analysis occurred before either bird exhibited overt aggression, which I used
to define the dominance asymmetry. Thus, my protocol avoided the confounding
effect of overt aggression altering the subsequent display rates of an
opponent.
|
|
In Gambel's quail, the size of head plumes and other ornate traits showed no strong relationship with winning (Table 2). However, winning males erected their head plumes and rusty head patches more frequently than losers (plume: t = 18.0, p =.008; rust: t = 30.5, p =.03). Likewise, losers flattened plumes and head patches more often than winners (plume: t = -27.5, p =.002; head patch: t = -50.0, p =.008). Tarsus length, a measure of body size, was also slightly larger for winners of Gambel's quail contests (Table 2).
Crest length of scaled quail was the only ornament of either species that
correlated with winning (Tables
2 and
3). Winning scaled quail were
also larger in size than losers (Table
3). Because body-size traits correlated with crest length
(n = 60, rs 
.32, p 
.01), I ran a
principal component analysis of body size (mass, tarsus, wing), followed by a
linear regression of crest length on the first principal component of body
size (PCA1). PCA1 represented male size, as it was positively weighted for
each trait (.7 tarsus,.6 mass,.3 wing). It also described 54% of the variation
in mass and tarsus and wing length. The regression of crest length versus PCA1
was significant (r2 =.15, F1,118 =
21.3, p <.0001). W-L scores of crest residuals suggested that,
even after accounting for body size, winning scaled quail had slightly longer
crests (1.1 mm on average), than losers (n = 59, T = 428,
p =.0008).
Logistic regression of multiple traits
For Gambel's quail, 22 trials of unmanipulated males contained a complete
set of ornamental, body size, and behavioral rates (simple tidbitting, body
fluffing, calling). The stepwise selection procedure produced a significant
model describing winning males (-2logL 
22 = 28,
p =.001). Call rate (Wald 12 = 8.95,
p =.002) and tarsus length (Wald 12 =
5.49, p =.02) were the best predictors of male status. Formal
tidbitting was not included in the logistic model because it was recorded in
only 13 trials (Table 2).
However, in 12 of these, formal tidbitting was exhibited only by the winning
male (sign test, p =.004, see also
Table 2). Formal tidbitting
also tended to correlate negatively with trial length (rs
= -.53, p =.07) and positively with simple tidbitting
(rs =.5, p =.08), but it was unrelated to male
size (p >.4). Rate of overt aggression also did not correlate with
male size (p >.5).
For scaled quail, 23 trials of unmanipulated males were used in the
logistic regression. Crest residuals (rather than crest length) were used
because of the relationship between crest size and body size (see above). The
logistic procedure selected a significant model that described the traits of
winning males (-2logL 22 = 18.58, p
=.0001). Call rate (Wald 12 = 7.02, p
=.008) and mass (Wald 12 = 3.76, p =.05)
were the best predictors of male status. Formal tidbitting was not included in
the model, as it occurred only in 12 trials. In 11 of these, formal tidbitting
was exhibited only by the winning male (sign test, p =.006, see also
Table 3). The rate of formal
tidbitting correlated negatively with trial length (rs =
-.72, p = 0.01), and although it was unrelated to simple tidbitting
(p =.2), it correlated positively with male size (tarsus:
rs =.54, p =.05; mass: rs
=.64, p =.04) and rate of overt aggression (rs
=.59, p =.04). Overt aggression also exhibited a negative
relationship with size (n = 50; tarsus: rs =
-.29, p =.04; mass: rs = -.27, p
=.06).
Manipulation experiments
Although 20-25 trials were run for each manipulation
(Table 1), only those that
produced clear winners were analyzed (Table
4). In Gambel's quail, males without plumes were more likely to
lose contests, whereas those with elongated plumes were more likely to win
(Table 4). Crest removal in
scaled quail as well as other plumage manipulations in both species did not
appear to alter the outcome of male contests
(Table 4).
|
For plume manipulations of Gambel's quail, contests were shorter in length (elongation: 6.85 min; df = 45, t = 2.0, p =.05; removal: 5.79 min; df = 44, t = 2.77, p =.008) than contests of unmanipulated males (9.42 min). Male behaviors also differed from unmanipulated contests. Losers whose opponents had elongated plumes showed lower rates of overt aggression than losers of unmanipulated contests (0 versus 1 aggressive act/15 min, df = 27, t = 1.7, p =.002). These losers also tended to call less often (1 versus 6 calls/15 min; df = 37, t = 1.82, p =.08). Winning males with elongated plumes did not differ in behavior, however, from unmanipulated winners (p >.3). During plume removal, losers (that lacked plumes) exhibited less aggression than losers of unmanipulated trials (0 versus 1 aggressive act/15 min, df = 36, t = 2.89, p =.006). This may have occurred because their plumed opponents tended to exhibit higher rates of simple tidbitting than winners of unmanipulated trials (50 versus 21 tidbits/15 min; df = 17, t = 1.78, p =.09). Call rates and overt aggression of winners did not differ between manipulated and unmanipulated trails (p >.2).
Gambel's quail used in both types of trials were affected by plume alterations. Males without head plumes were more likely to become subordinate and/or maintain their subordinate status (14:6), whereas males with elongated plumes exhibited the opposite pattern (7:12; one-tailed Fisher's Exact p =.04). For all other manipulations, male status was more likely to remain the same between trials, rather than change (21:9, Z = 2.19, p =.02).
Correlation between female choice and male dominance
Of the 39 pairs of unmanipulated Gambel's quail, 18 winning males (46%)
were also chosen by females. Of the 40 pairs of scaled quail, 28 winning males
(70%) were chosen by females. The number of winning males associated with
female choice differed between the species (Fisher's Exact p =.03).
In Gambel's quail, female choice and dominance showed no relationship
(p =.73). However, in scaled quail, female choice and dominance were
correlated more often than expected by chance (Z = 2.52, p
=.01).
Differences in the pattern of male dominance and female choice may reflect
differences in size dimorphism between the two quail species. In scaled quail,
larger males were favored by both male—male competition
(Table 3) and female choice
(Hagelin and Ligon, 2001),
whereas in Gambel's quail, body size was favored only in male—male
competition (Table 2; Hagelin and Ligon, 2001).
Therefore, I expected the magnitude of size dimorphism to be greater in scaled
quail than in Gambel's quail. A comparison of tarsus length in both
captivereared birds and museum specimens suggests that scaled quail do,
indeed, exhibit greater size dimorphism than Gambel's quail
(Table 5).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Close examination of male—male competition revealed both striking similarities and differences between Gambel's and scaled quail. Although Gambel's quail was nearly twice as aggressive as scaled quail, high rates of displays and large body size were related to winning in both species (Tables 2 and 3). With regard to ornaments, the head plume of Gambel's quail was a primary plumage trait that affected the likelihood of winning (Table 4). Finally, both intra- and intersexual selection appear to operate differently in the two species, with females preferring large, dominant males in scaled quail, but not in Gambel's quail. Although the above information is complex, it reveals insight into the kinds of traits that sexual selection favors, as well as the patterns that underlie male and female behavior.
Traits used in male contests
The traits involved in intrasexual selection are thought to signal
information, such that opponents settle contests and avoid unnecessary or
costly interactions (Andersson,
1994; Berglund et al.,
1996; Maynard Smith,
1982). Such traits may be reliable or honest if they impose costs
to the signaler. For example, behavior can result in direct physiological
costs (Buchanan, 2000;
Folstad and Karter, 1992;
Peters, 2000;
Vehrencamp et al., 1989;
Wingfield et al., 1997).
Traits may also involve indirect social costs (e.g.,
Leonard and Horn, 1995), in
which the signaler bears the burden of underwriting its interests
(Deag and Scott, 1999) and
honesty is maintained via social remediation
(Waas, 1991;
Zahavi, 1977). Alternatively,
when costs are low, dishonest signaling may occur if cheating is profitable
(e.g., Candolin, 2000).
Behavior
In both Gambel's and scaled quail, high rates of calling and tidbitting
were closely associated with winning (Tables
2 and
3). The rate of formal
tidbitting also showed a negative relationship with trial length, indicating
that opponents with large display asymmetries settled contests quickly.
Although the energetic costs of fast display rates are unknown, studies of
castrated Gambel's and scaled quail suggest that displays are related to
testosterone (Hagelin, 2001).
Although unstudied in New World quail, testosterone can impose costs on immune
function (Verhulust et al., 1999). Furthermore, testosterone has been linked
to honest traits that maintain male status in several other galliform species
(Alatalo et al., 1996;
Buchholz, 1997;
Ligon et al., 1990).
In both quail species, high display rates were successful during both
male—male competition (Tables
2 and
3) and female choice
(Hagelin and Ligon, 2001).
This pattern provides further support that male behaviors may contain
functional, rather than arbitrary information
(Berglund et al., 1996;
Hill, 1994;
Kodric-Brown and Brown, 1984;
Mateos and Carranza, 1999). To
more accurately assess signal honesty, future tests need to examine whether
deceitful displays impose social costs and whether females benefit from mating
with males with high display rates
(Berglund et al., 1996;
Hagelin and Ligon, 2001).
Body size
Size is often attributed to intrasexual selection because bigger males have
an increased likelihood of overpowering smaller competitors
(Andersson, 1994;
Ligon, 1999). Likewise, size
is frequently considered honest because it is connected to an underlying
quality of an individual that can be difficult to fake
(Maynard Smith and Harper,
1988; Taylor et al.,
2000). In both species of quail, male size was associated with
status (Tables 2 and
3). Size also correlated
negatively with the rate of overt aggression in scaled quail, suggesting that
larger males did not have to assert aggression as often as smaller males did
to win.
When a pair of male quail face off, or spar, they often stand on tiptoe and
stretch their necks high into the air, making their bodies appear as tall as
possible (Delehanty, 1997;
Gutiérrez
and Delehanty, 1999). Such behaviors have the potential to
honestly reveal size in the process
(Guilford and Dawkins, 1995;
Taylor et al., 2000). However,
dishonest signaling may also be possible because individuals can presumably
adjust their appearance during an interaction.
Ornaments
Although a variety of explanations have been proposed for the evolution and
maintenance of plumage traits involved in male contests (e.g.,
Butcher and Rohwer, 1989;
Huxley, 1938;
Johnstone and Norris, 1993;
Peek, 1972;
Maynard Smith, 1982), all
suggest that ornate feathers signal intent or status. In this study, the head
plume of Gambel's quail was a primary plumage trait involved in male contests.
Winners erected their plumes more frequently than losers. Experimentally
elongated plumes were also associated with winning, whereas plume removal
increased the likelihood of losing (Table
4).
Head plumes are extremely modifiable and dynamic. They are similar to a
coverable badge (Hansen and Rohwer,
1986; Rohwer,
1982) in that they can change rapidly to serve as
"notice" to an opponent
(Maynard Smith, 1991), rather
than simply act as a static badge of status. Dynamic traits on the face or
head are key signals involved in intrasexual contests of several galliform
species (Buchholz, 1997;
Ligon et al., 1990;
Mateos and Carranza, 1997b).
Such ornaments may be favored if they provide more accurate or immediate
information regarding male motivation than a static badge.
Manipulation experiments suggest that Gambel's plumes are used to assess
intent. Apparently wary of an augmented signal, winners threatened males with
enhanced plumes less often than in unmanipulated trials. However, when an
opponent lacked a plume, winners tended to exhibit more displays, as if they
were more certain of winning. It is unclear, however, whether plumes act as
honest signals. In other investigations, exaggerated ornaments caused males to
suffer social costs because they were frequently tested and/or experienced
escalated fights with males of higher status (e.g.,
Møller, 1987;
Rohwer and Rohwer, 1978;
Watson and Parr, 1981). Had
contests run longer, perhaps opponents would have exposed the dishonesty of
augmented plumes.
Clearly, the plumes of quail vary not only in orientation (up versus down)
but also in size. For Gambel's quail, however, natural variation in plume size
may not be as informative as altering plume position. Consistent with this
prediction, I found no evidence that plume length correlated with winning in
trials of unmanipulated males (Table
2). Likewise, in a 3-year field study, plume length was not
related to male status or mating success
(Hagelin, 1999). Instead,
plume manipulations may have created a supernormal signal with regard to
position. Elongated plumes of Gambel's quail hung far forward, similar to an
erect-crested, dominant individual. In contrast, plume removal may have
created an extreme signal of submission (a completely flattened or
deemphasized plume).
The role of crests in scaled quail is more difficult to interpret. Winning
males had slightly longer crests (1.8 mm;
Table 3). However, manipulation
experiments suggested that contest outcome was not dictated by crest length;
males with crests won as frequently as those without
(Table 4). Consequently, crest
size correlated with, but did not appear to be causally related to, male
status. The positive relationship between crest size and status
(Table 3) may be due to greater
feather wear of subordinates (Hagelin and
Ligon, 2001). Abrasion can alter the size of ornate feathers,
potentially making them less reliable indicators
(Buchholz, 1997). Future
studies require data on crest displays, as well as a larger sample of crest
manipulations. Because crests of scaled quail are similar to the dynamic
plumes of Gambel's quail, they may also play a role in intrasexual
signaling.
Ornaments not clearly involved in sexual selection
In both species of quail, males exhibit dimorphic plumage traits, such as
belly patches, that did not appear to be involved in either male—male
competition (Tables
2,3,4)
or female choice (Hagelin,
1999; Hagelin and Ligon,
2001). This curious result demands explanation. I ran a power
analysis to determine the degree to which male ornaments could vary in
experiments, while remaining 80% certain that I did not falsely accept the
null hypothesis of no difference between winners and losers. Correlational
data (Tables 2 and
3) were capable of detecting
medium-size ornamental effects (Cohen,
1988). That is, differences were detectable, even though ornament
sizes of winners and losers overlapped 62-66%. Manipulation trials
(Table 4) could detect
relatively large effects between manipulated males and controls, or a 3:1
departure from the null of 1:1 (Cohen,
1988). Larger data sets are required to assess smaller effect
sizes, including why multiple ornament manipulations of Gambel's quail, which
included plume removal, did not produce a stronger result
(Table 4). However, it appears
that some feather ornaments do not play as prominent a role during male
contests as behavior rate, body size, or head plumes.
The lack of a relationship between the dimorphic plumage of males and
sexual selection has been noted in several avian species
(Beani and Dessi-Fulgheri,
1995; Buchholz,
1995,
1997;
Ligon et al., 1990;
Ligon and Zwartjes, 1995;
Rohwer and Røskraft, 1989). Such results suggest that the conventional
mechanisms of sexual selection (mate choice, male contests) may not entirely
account for the maintenance of dimorphic plumage. Other mechanisms may be
involved. For example, bright males may be favored, if they are less
profitable prey, compared to dull-colored females at nests
(Baker and Parker, 1979). Male
plumage may also function in other social interactions, such as cryptic female
choice (Eberhard, 1996), may
operate in long-distance communication
(Dale and Slagsvold, 1996), or
may reflect status during the nonbreeding season (e.g.,
Senar and Camerino, 1998). If,
however, ornaments reliably indicated status during nonbreeding, it is unclear
why they would not also function during sexual selection
(Hagelin and Ligon, 2001).
Honest signals frequently play a role in multiple social contexts because
assessors benefit by receiving reliable information about the quality of
competitors or mates (Berglund et al.,
1996;
Pärt and
Qvarnström, 1997;
Mateos and Carranza,
1999).
If an ornament spreads among individuals in a population, it may lose both
honesty and function, causing males to switch to other signals, similar to an
evolutionary arms race (Butcher and
Rohwer, 1989; Grether,
1996; Rohwer and
Røskaft, 1989;
Johnstone and Norris, 1993).
Yet, functionless ornaments may persist if they are cheap to produce and
subject to weak selection (Brooks and
Caithness, 1995; Møller
and Pomiankowski, 1993). If some ornaments of quail have lost
their function, it is unclear how weak selection must be in order to maintain
them.
Interspecific patterns of behavior and size
Male—male competition and female choice correlated with male status
in scaled quail, but not in Gambel's quail. Consequently, both intra- and
intersexual selection favored larger males in scaled quail
(Table 3;
Hagelin and Ligon, 2001).
However, in Gambel's quail, only male—male competition favored larger
males (Table 2). Based on the
above pattern, I expected the magnitude of selection on male size to be
stronger in scaled quail than in Gambel's quail. Consistent with prediction,
the degree of size dimorphism was greater in both captive and wild populations
of scaled quail (Table 5).
It is puzzling why two closely related species should diverge so
dramatically with regard to patterns of sexual selection. Why, for example, do
female scaled quail prefer dominant males, but Gambel's females do not? The
result may be related to differences in signal honesty, the maintenance of
male status, and mating system. In scaled quail only, winners of both intra-
and intersexual selection were associated with large size, a common indicator
of quality (see above). Furthermore, formal tidbitting, a key behavior related
to winning, also correlated with male size (mass, tarsus) in scaled quail, but
not in Gambel's quail. The relationship between size and behavior may
facilitate honest signaling in scaled quail, particularly if large males
enforce the status that they signal. Losing scaled quail only rarely
challenged winners, as if they accurately assessed their opponents' status. I
also observed strict social relationships in scaled quail during nonbreeding,
when captive birds exhibited a linear hierarchy that was more rigid than in
Gambel's quail (Hagelin, unpublished data). In the field, honest signaling of
status may also be emphasized in the social relationships of scaled quail.
Both sexes appear to be inseparable from a single mate
(Evans, 1997). In systems with
high levels of social (and presumably genetic) monogamy, both accurate
signaling and assessment of status are likely to be advantageous to both sexes
(Jones and Hunter, 1999).
Unlike scaled quail, size and display rate were not correlated in Gambel's
quail, indicating that assessment of opponents or mates may be more difficult.
Winning males exhibited high rates of aggression, as if to quell the frequent
retaliation of losers. Compared to scaled quail, persistent attacks may be
beneficial in Gambel's quail, given that the sex ratio of wild populations is
more male biased (Brown and
Gutiérrez, 1980). Escalated
fighting would appear to have a greater payoff. Though costly, aggression can
increase the chances of a lower ranking male obtaining higher status
(Senar et al., 1992).
If, however, the result of male—male competition does not reliably
reflect male quality, females may not prefer dominant males
(Qvarnström
and Fosgren, 1998). High rates of aggression might lower mate
quality in Gambel's quail, if, for example, dominant males experience
trade-offs between aggression and parental effort
(Qvarnström
and Fosgren, 1998). Finally, compared to scaled quail, Gambel's
quail may have a more flexible, polygamous mating system, in which both males
and females form sequential mating associations during a single breeding
season (Hagelin, 1999). Taken
together, both captive and field data suggest that social relationships of
Gambel's quail may be more contestable and transitory than in scaled quail.
The key environmental mechanisms that underlie these divergent behaviors,
however, are unstudied.
In conclusion, primary traits favored by intrasexual selection in both Gambel's and scaled quail, such as behavior rate and body size, have the potential to act as honest signals if the traits impose physiological costs and/or there is social control of deception. The same is true for the head plume of Gambel's quail, the primary ornament associated with male status. The head plume is a dynamic trait, capable of providing immediate information about male intent. Some plumage ornaments, such as plumes, may play a more prominent role in sexual selection than others, particularly if they function as reliable, dynamic indicators. In both quail species, interspecific differences in sexual selection were consistent with patterns of body-size dimorphism. However, striking behavioral patterns, such as the correlation between female choice and male—male competition in scaled quail only, require further study. Differences in behavior, such as the rates of overt aggression, may be related to the stability of social relationships in each species and presumably result from different ecological pressures.
|
ACKNOWLEDGEMENTS |
|---|
This study would not have been possible without the expertise of P. Elsner, who directed the construction of quail pens. Thanks to D. Ambrico, C. Chavez, J. Hill, K. Horton, E. Langenburg, J. Liu, J. Ortega, M. Ryan, K. Schardein, and S. Walston, who provided help with field work, data entry, and analysis. I thank E. Bedrick for his patient statistical advice. Research was funded by a National Science Foundation predoctoral fellowship to J.C.H. and grants from the Animal Behaviour Society, Rocky Mountain Pheasant and Waterfowl Association, University of New Mexico Student Research Allocations Committee, and Graduate Research Allocations Committee. My dissertation committee, J.D. Ligon, A. Kodric-Brown, G. Hill, and R. Thornhill provided excellent advice during project synthesis and write-up.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Alatalo RV, Hoglund J, Lundberg A, Rintamaki PT, Silverin B, 1996. Testosterone and male mating success on black grouse leks. Proc R Soc Lond B 263: 1697-1702.
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.
Badyaev AV, Hill GE, 2000. Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration. Biol J Linn Soc 69: 153-172.
Badyaev AV, Martin TE, 2000. Sexual dimorphism in relation to current selection in the house finch. Evolution 54: 3987-997.
Baker RR, Parker GA, 1979. The evolution of bird coloration. Phil Trans R Soc Lond B 287: 63-130.
Beani L, Dessi-Fulgheri F, 1995. Mate choice in the grey partridge, Perdix perdix: role of physical and behavioural male traits. Anim Behav 49: 347-356.[Web of Science]
Berglund A, Bisazza A, Pilastro A, 1996. Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58: 385-399.
Brooks R, Caithness N, 1995. Manipulating a seemingly
nonpreferred male ornament reveals a role in female choice. Proc R Soc
Lond B 261:
7-10.
Brown DE, Gutiérrez RJ, 1980. Sex ratios, sexual selection and sexual dimorphism in quails. J Wildl Manage 44: 198-202.
Buchanan KL, 2000. Stress and the evolution of condition-dependent signals. Trends Ecol Evol 15: 156-160.[Medline]
Buchholz R, 1995. Female choice, parasite load and male ornamentation in wild turkeys. Anim Behav 50: 929-943.
Buchholz R, 1997. Male dominance and variation in fleshy head ornamentation in wild turkeys. J Avian Biol 28: 223-230.
Butcher GS, Rohwer S, 1989. The evolution of conspicuous and distinctive coloration in birds. Curr Ornithol 6: 51-108.
Candolin U, 2000. Increased signalling effort when survival prospects decrease: male-male competition ensures honesty. Anim Behav 60: 417-422.[Web of Science][Medline]
Cohen J, 1988. Statistical power analysis for the behavioral sciences. Hillsdale, New Jersey: Lawrence Erlbaum Associates.
Dale S, Slagsvold T, 1996. Plumage coloration and conspicuousness in birds: experiments with the pied flycatcher. Auk 113: 849-857.[Web of Science]
Deag JM, Scott GW, 1999. "Conventional" signals in avian agonistic displays: integrating theory, data and different levels of analysis. J Theor Biol 196: 155-162.[Web of Science][Medline]
Delehanty DJ, 1997. Mountain quail reproduction and restoration in the Great Basin (PhD dissertation). Reno: University of Nevada.
Eberhard WG, 1996. Female control: sexual selection by cryptic female choice. Princeton, New Jersey: Princeton University Press.
Ellis CR Jr, Stokes AW, 1966. Vocalizations and behavior in captive Gambel quail. Condor 68: 72-80.[Web of Science]
Evans CA, 1997. Reproductive biology of scaled quail Callipepla squamata in southern New Mexico (Master's thesis). Las Cruces: New Mexico State University.
Folstad I, Karter AJ, 1992. Parasites, bright males and the immuno-competence handicap. Am Nat 139: 603-622.[Web of Science]
Grether G.F, 1996. Intrasexual competition alone favors a sexually dimorphic ornament in the rubyspot damselfly Hetaerina americana. Evolution 50: 1949-1957.[Web of Science]
Guilford T, Dawkins MS, 1995. What are conventional signals? Anim Behav 49: 1689-1695.
Gutiérrez RJ, Delehanty DJ, 1999. Mountain quail (Oreortyx picta). In: The birds of North America, no. 321 (Poole A., Gill F, eds). Philadelphia: The Birds of North America.
Hagelin JC, 1999. Sexual selection, plumage ornamentation and behavior of Gambel's and scaled quail (PhD dissertation). Albuquerque: University of New Mexico.
Hagelin JC, 2001. Castration in Gambel's and scaled quail: Ornate plumage and dominance persist, but courtship and threat behaviors do not. Horm Behav 39: 1-10.[Medline]
Hagelin JC, Ligon JD, 2001. Female quail prefer testosterone-mediated traits, rather than the ornate plumage of males. Anim Behav 61: 465-476.
Hansen AJ, Rohwer S, 1986. Coverable badges and resource defense in birds. Anim Behav 34: 69-76.
Hill GE, 1991. Plumage coloration is a sexually selected indicator of male quality. Nature 350: 337-339.[Web of Science]
Hill GE, 1994. Trait elaboration via adaptive mate choice: sexual conflict in the evolution of signals of male quality. Ethol Ecol Evol 6: 351-370.
Hill JA, Enstrom DA, Ketterson ED, Nolan V Jr, 1999.
Mate choice based on static versus dynamic secondary sexual traits in the
dark-eyed junco. Behav Ecol 10:
91-96.
Huxley JS, 1938. Threat and warning coloration in birds, with a general discussion of the biological functions of color. In: Proceedings of the 8th International Ornithological Congress (Jourdain FCR, ed). Oxford: Oxford University Press; 430-455.
Johnsgard PA, 1973. The grouse and quails of North America. Lincoln: University of Nebraska Press.
Johnstone RA, Norris K, 1993. Badges of status and the cost of aggression. Behav Ecol Sociobiol 32: 127-134.[Web of Science]
Jones IL, Hunter FM, 1999. Experimental evidence for mutual interand intrasexual selection favouring a crested auklet ornament. Anim Behav 57: 521-528.[Web of Science][Medline]
Kodric-Brown A, Brown JH, 1984. Truth in advertising: the kinds of traits favored in sexual selection. Am Nat 124: 309-323.[Web of Science]
Kirkpatrick M, Ryan MJ, 1991. The paradox of the lek and the evolution of mating preferences. Nature 350: 33-38.
Leonard ML, Horn AG, 1995. Crowing in relation to status in roosters. Anim Behav 49: 1283-1290.
Ligon JD, 1999. The evolution of avian breeding systems. Oxford: Oxford University Press.
Ligon JD, Thornhill R, Zuk M, Johnson K, 1990. Male-male competition, ornamentation and the role of testosterone in sexual selection in the red jungle-fowl. Anim Behav 40: 367-373.
Ligon JD, Zwartjes PW, 1995. Ornate plumage of male red junglefowl does not influence mate choice by females. Anim Behav 49: 117-125.
Mateos C, Carranza J, 1995. Female choice on morphological features of male ring-necked pheasants. Anim Behav 49: 737-748.
Mateos C, Carranza J, 1997a. The role of bright plumage in male-male interactions in the ring-necked pheasant. Anim Behav 54: 1205-1214.[Web of Science][Medline]
Mateos C, Carranza J, 1997b. Signals in intra-sexual competition between ring-necked pheasant males. Anim Behav 53: 471-485.
Mateos C, Carranza J, 1999. Effects of male dominance and courtship display on female choice in the ring-necked pheasant. Behav Ecol Sociobiol 45: 235-244.[Web of Science]
Maynard Smith J, 1982. Evolution and the theory of games. Cambridge: Cambridge University Press.
Maynard Smith J, 1991. Theories of sexual selection. Trends Ecol Evol 6: 146-151.
Maynard Smith J, Harper DGC, 1988. The evolution of aggression: can selection generate variability. Phil Trans R Soc Lond B 319: 557-570.[Web of Science][Medline]
Møller A.P, 1987. Social control of deception among status signalling house sparrows Passer domesticus. Behav Ecol Sociobiol 20: 307-311.[Web of Science]
Møller AP, Pomiankowski A, 1993. Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32: 167-176.[Web of Science]
Moore AJ, 1990. The evolution of sexual dimorphism by sexual selection: the separate effects of intrasexual selection and intersexual selection. Evolution 44: 315-331.[Web of Science]
Pärt T, Qvarnström A, 1997. Badge size in collared flycatchers predicts outcome of male competition over territories. Anim Behav 54: 893-899.[Web of Science][Medline]
Peek FW, 1972. An experimental study of the territorial function of vocal and visual display in the male red-winged blackbird (Agelaius phoeniceus). Anim Behav 20: 112-118.
Peters A, 2000. Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proc R Soc Lond B 267: 883-889.[Medline]
Qvarnström A, Fosgren E, 1998. Should females prefer dominant males? Trends Ecol Evol 13: 498-501.
Rice WR, 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.[Web of Science]
Rohwer S, 1975. Social significance of avian winter plumage variability. Evolution 29: 593-610.[Web of Science]
Rohwer S, 1982. The evolution of reliable and unreliable badges of fighting ability. Am Zool 22: 531-546.
Rohwer S, Rohwer FC, 1978. Status signaling in Harris' sparrows: experimental deceptions achieved. Anim Behav 39: 1110-1115.
Rohwer S, Røskaft E, 1989. Results of dyeing male yellow-headed blackbirds solid black: implications for the arbitrary identity badge hypothesis. Behav Ecol Sociobiol 25: 39-48.
Røskaft E, Rohwer S, 1987. An experimental study of the function of the red epaulettes and the black body colour of male red-winged blackbirds. Anim Behav 35: 1070-1077.
Savalli UM, 1994. Tail length affects territory ownership in the yellow-shouldered widowbird. Anim Behav 48: 105-111.
Schemnitz SD, 1994. Scaled quail (Callipepla squamata). In: The birds of North America, no. 321 (Poole A., Gill F, eds). Philadelphia: The Birds of North America Inc.
Senar JC, Camerino M, 1998. Status signaling and the
ability to recognize dominants: an experiment with siskins (Carduelis
spinus). Proc R Soc Lond B 265:
1515-1520.
Senar JC, Camerino M, Metcalfe NB, 1992. Fighting as a subordinate in finch flocks: escalation is effective but risky. Anim Behav 43: 862-864.[Web of Science]
Stokes AW, Williams HW, 1971. Courtship feeding in gallinaceous birds. Auk 88: 543-559.[Web of Science]
Taylor PW, Hasson O, Clark DL, 2000. Body postures and patterns as amplifiers of physical condition. Proc R Soc Lond B 267: 917-922.[Medline]
Vehrencamp SL, Bradbury JW, Gibson RM, 1989. The energetic cost of display in male sage grouse. Anim Behav 38: 885-896.[Web of Science]
Verhulst S, Dieleman SJ, Parmentier HK, 1999. A tradeoff between immunocompetence and sexual ornamentation in domestic fowl. Proc Natl Acad Sci 6: 4478-4481.
Waas JR, 1991. The risks and benefits of signaling aggressive motivation: a study of cave-dwelling little blue penguins. Behav Ecol Sociobiol 29: 139-146.[Web of Science]
Watson A, Parr R, 1981. Hormone implants affecting territory size and aggressive and sexual behaviour in red grouse. Ornis Scand 12: 55-61.
Webster MS, 1992. Sexual dimorphism, mating system and body size in New World blackbirds (Icterinae). Evolution 46: 1621-1641.[Web of Science]
Wingfield JC, Jacobs J, Hillgarth N, 1997. Ecological constraints and the evolution of hormone-behaviour interrelationships. Ann NY Acad Sci 807: 22-41.[Web of Science][Medline]
Zahavi A, 1977. Reliability in communication systems and the evolution of altruism. In: Evolutionary ecology (Stonehouse B, Perrins C, eds). London:Macmillian; 253-259.
Zink RM, Blackwell RC, 1998. Molecular systematics of the scaled quail complex (genus Callipepla). Auk 115: 394-403.[Web of Science]
Zucker N, 1994. Social influence on the use of a modifiable status signal. Anim Behav 48: 1317-1324.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  W. F. D. van Dongen and R. A. Mulder Male and female golden whistlers respond differently to static and dynamic signals of male intruders Behav. Ecol., September 1, 2008; 19(5): 1025 - 1033. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. A. Baird, J. M. Hranitz, D. K. Timanus, and A. M. Schwartz Behavioral attributes influence annual mating success more than morphological traits in male collared lizards Behav. Ecol., November 1, 2007; 18(6): 1146 - 1154. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. A. Duckworth Behavioral correlations across breeding contexts provide a mechanism for a cost of aggression Behav. Ecol., November 1, 2006; 17(6): 1011 - 1019. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Pizzari Food, vigilance, and sperm: the role of male direct benefits in the evolution of female preference in a polygamous bird Behav. Ecol., September 1, 2003; 14(5): 593 - 601. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Torok, G. Hegyi, and L. Z. Garamszegi Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers Behav. Ecol., May 1, 2003; 14(3): 382 - 388. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||