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Chapter 3
Bird colors as intrasexual signals of aggression and
dominance
Juan Carlos Senar
Unidad Asociada CSIC,
Museu Ciències Naturals
Barcelona
Darwin (1871) proposed two modes of sexual selection: direct competition between
individuals of the same sex (intrasexual selection) and mate choice (intersexual selection).
Within both contexts, secondary sexual characters function as signals of individual quality
(Bradbury & Davies 1987; Andersson 1994; Berglund et al. 1996). In this chapter, I will review
and summarize studies of intrasexual signaling in birds, in which plumage and bare-part color is
used to signal the fighting ability of individuals.
Recently, it has been stressed that sexual and natural selection are not the only selective
forces shaping animal signals, but that social selection, in which the signal influences the fitness
of signalers and receivers within a social context, can also shape signal evolution (Tanaka 1996;
Wolf et al. 1999). The selective pressures that shape signals of fighting ability are probably
similar whether or not they have evolved by sexual or social selection. The major advantage of
these signals, independent of their origin, is that individuals of unequal fighting ability
competing for limited resources (e.g. females, territories, or food) would not need to risk
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accidental injury or waste energy assessing the relative fighting ability of potential opponents
(Rohwer 1975; Rohwer 1982). There are differences, however, in the expected outcomes of
sexual and social selection. The function of signals that evolved by sexual selection is to drive
off rivals, but this should not be the aim of signals that evolved by social selection. Driving off
rivals would lead to group disruption and, in social species this would be potentially costly for
both contestants. In social species, therefore, the goal is to signal dominance status (Senar et al.
1989; Senar 1990).
Most theoretical developments and empirical work in this area of behavioral ecology has
focused on these signals from the view of “status signaling” and hence from the social
perspective (Maynard Smith & Harper 2003). This is because communication in social species
presents more evolutionary problems but also more complex and interesting patterns (Rhijn
1980; Rhijn & Vodegel 1980; Rohwer 1982; Maynard Smith 1982a; Maynard Smith 1982b;
Maynard Smith & Harper 2003). Hence, I have outlined this chapter from this status-signaling
perspective, but I also provide examples of signals with sexual motivations (mostly territorial
defence).
Superior fighting ability is the most common information provided by elaborate color
patches within the context or intrasexual signaling, but color displays can serve other functions,
such as signaling youth or low competitive ability (within the context of delayed plumage
maturation; Selander 1965; Rohwer 1978a). Bright colors can also function to attract
conspecifics to feeding patches, which can increase the size of flocks and hence the likelihood of
detecting predators (Beauchamp & Heeb 2001). These topics will be reviewed at the end of the
chapter.
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Signaling fighting ability or individual recognition?
The first studies on the role of bird colors as signals of fighting ability were conducted by
Rohwer (1975, 1977, 1978) within the context of social groups. In an attempt to explain the
great variation in size and extent of color patches in the plumage of wintering birds, he proposed
that colored patches could serve as badges of social status. Rohwer’s work led to a controversy
regarding whether the colored patches of feathers in flocking birds in winter had evolved for
status signaling or simply for individual recognition (Shields 1977; Rohwer 1978b). Whitfield
(1987a) reviewed the topic and concluded that, in some species, especially those forming small
and stable flocks, individual recognition was sufficient to explain plumage displays (Whitfield
1986; Ens & Goss-Custard 1986; Watt 1986a; Rohwer & Roskaft 1989). In other species,
however, the correlation found between plumage badges and dominance (Table 3.1) and the
results of experiments (Watt 1986a; Watt 1986b) strongly suggested that such patches of color
had evolved as true signals of status.
Table 3.1 about here
Status signaling or just a correlation?
When success in agonistic encounters is related to plumage traits (Table 3.1), it suggests
that plumage color displays can serve as signals of social status (Fig. 3.1). It has been widely
recognized, however, that a correlation between a plumage trait and dominance is not by itself
evidence for signaling --individuals could assess their social status by other means, and plumage
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could simply be a correlated trait rather than a signal (e.g. Roper 1986; Jones 1990; Slotow et al.
1993b; Fig. 3.1).
Fig. 3.1 about here
Three different approaches have been used to test for a signaling function of plumage
traits (Table 3.2). In most experiments, a plumage trait is manipulated and the experimental
individual introduced into a group to test for gains or reductions in social rank (Table 3.2; Fig.
3.2). Alternatively, in territorial species, the manipulated bird is released into the wild and its
behavior recorded (Fig. 3.3). This experimental approach has produced mixed results, especially
in cases of social species, probably because there are many different masking variables that need
to be taken into account. In the oldest experiments (Rohwer 1977; Rohwer & Rohwer 1978), for
instance, manipulated birds were reintroduced into existing social groups, so that either the
experimental birds were known to flockmates as subordinate (Ketterson 1979), or they withdrew
from recognized dominant flockmates (Shields 1977; Ketterson 1979). Alternatively if the
manipulation prevented any recognition of flock companions, the experimental birds might have
been disadvantaged just because of a prior-residence advantage by the birds in the group (Fugle
et al. 1984a; Järvi et al. 1987b) (see below). To avoid these problems, more recent experimental
approaches have exposed manipulated birds to unfamiliar conspecifics in neutral cages (e.g. Järvi
et al. 1987b; Lemel & Wallin 1993a; McGraw & Hill 2000a), or the plumage of both dominants
and subordinates has been manipulated (e.g. Grasso et al. 1996). However, the introduction of a
manipulated bird into a group is not the best way to test for the signal nature of a trait, because it
potentially confounds the demonstration that the trait is a true signal with the demonstration of
the existance of mechanisms to avoid cheating. For instance, if a bird with an enlarged badge of
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dominance does not defeat presumed dominant flock companions (e.g. Rohwer 1977; Rohwer &
Rohwer 1978; Møller 1987a; Järvi et al. 1987b), it does not mean that the trait is not a signal.
Mechanisms to avoid cheating, such as assessing not only the trait but also behavior, may be
operating (see below).
Fig. 3.2 about here
In experiments in which plumage coloration is manipulated, there is additional confusion
regarding which bird is being tested--the individual whose color has been altered or the
individual(s) reacting to the manipulated bird. Some of these experiments were designed to test
whether the manipulated bird was able to rise in a dominance hierarchy. Although these
experimental tests of dominance recognition implicitly assume a change in the behavior of
unmanipulated birds as a result of the opponent's badge enlargement, they should also test
whether birds show any avoidance of individuals differing in apparent dominance. In other
words, the bird being tested is the individual reacting to the color manipulation. Another
important point for the most convincing tests of status signaling is that the observer should also
record whether birds avoid probable dominants on the first encounter(s) (Geist 1966; Watt
1986a); otherwise, other factors may mask assessment of the color display (see below). In
several studies, dominance relationships were observed over long periods of time (e.g. 30
minutes in Lemel & Wallin (1993a) and one month in Fugle et al. (1984a)), making them
unsuitable as tests of whether plumage signals dominance. Additionally, traits under study
should not only be enlarged but they should also be reduced, a robust technique that is often
difficult to perform and has rarely been used (e.g. Rohwer 1977; Grasso et al. 1996; Senar &
Camerino 1998a).
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Fig. 3.3 about here
Table 3.2 about here
The problems associated with the use of manipulated live birds introduced into a group
may be solved by the use of models (either stuffed or completely artificial birds). Alternatively,
the researcher may use a caged bird (Slagsvold 1993). This approach has been used for several
species (Table 3.2). Results of studies that have used presentations of models or live birds have
been more conclusive than manipulations of birds in groups, with test birds avoiding models
with enlarged badges of status, on their first encounter (Fig. 3.4). This strongly suggests that
these traits are recognized as signals of social rank.
Fig. 3.4 about here
The third approach that has been used to test for status signaling is choice experiments
(Table 3.2), in which individuals were tested to see if they could recognize dominant competitors
by color alone. Senar & Camerino (1998) recorded the active choice between feeding close to a
cage containing a live dominant bird or close to another cage containing a live subordinate (Fig.
3.5). This approach has the advantage that, when working with flocking species, results cannot
be biased by whether the bird under study prefers to feed socially or not. The use of live birds is
useful in providing more natural stimuli. The method has the additional advantage that, because
they are caged, potential companions cannot reveal their status by interacting with other birds
(Maynard Smith & Harper 2003), although birds could still use cues other than color (e.g.
postures) to infer aggressive potential. In any case, color manipulations reveal whether the traits
act as signals on their own. Such choice experiments have only been carried out with Eurasian
Siskins (Carduelis spinus) (Senar & Camerino 1998a). In this experiment, birds avoided
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individuals with either naturally large badges or experimentally enlarged badges, but did not
avoid individuals whose badge had been removed. These observations suggest that the black bib
of the Eurasian Siskin worked as a true signal of social status (Fig. 3.5).
Fig. 3.5 about here
Taken together, manipulation experiments confirm that, in several species, coloration is
not only correlated with dominance but is readily used by conspecifics as a signal of social
status. In the case of territorial species, earlier descriptions had suggested that signaling of
fighting ability could not be reliable (Rohwer 1982). However, both early and more recent
experiments with models or color manipulations, which resulted in effects on the acquisition and
maintenance of resources, clearly suggest that honest signals of territorial fighting ability can
evolve (Peek 1972; Smith 1972; Pärt & Qvarnström 1997; Pryke et al. 2001; Pryke & Andersson
2003).
Table 3.3 about here
Signaling between (but not within) sex and age classes
Another old controversy regarding the signaling of fighting ability is whether signaling
between, but not within, sex and age classes should still be regarded as true status signaling. The
original description of the status-signaling hypothesis assumed that it should work both between
and within sex and age classes (Rohwer 1975), although in fact the species under study only
exhibited signaling between age and sex classes (Watt 1986a; (Table 3.3). The most common
reasoning that was given to support the original formulation was that plumage variability among
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birds of different ages and sex may have evolved for reasons completely unrelated to status
signaling and that if a plumage trait is a true signal of social status it should also be used within
classes (Balph et al. 1979; Whitfield 1987a; Maynard Smith & Harper 1988). Some other
investigators, however, claim that if a trait is used to signal dominance between classes, it is still
a badge of status because individuals use it to avoid unnecessary and risky confrontations
(Ketterson 1979; Watt 1986b; Jones 1990). The controversy, therefore, is in fact a debate
between present versus original functions. My own view is that a true badge of status should
work both between and within classes and that cases in which the system only works between
classes have likely evolved under selection pressures other than status signaling (see Booth
(1990) for a discussion between adaptation and current utility in relation to coloration.)
There are cases in which juvenile birds signal their lower competitive ability to avoid
heightened aggression from adult birds (Lyon & Montgomerie 1986; Muehter et al. 1997; Senar
et al. 1998b; VanderWerf & Freed 2003) –so-called delayed plumage maturation (Rohwer et al.
1980; see below). For these birds, it is enough to signal juvenile-subordinate status (Studd &
Robertson 1985a), so that a graded signal that works within and between age classes might not
be needed. In some cases, however, plumage coloration may be graded within age classes (e.g.
Hill 1989; Senar et al. 1998b), but there is still a significant difference in plumage coloration
between ages. Cases such as the White-crowned Sparrow (Zonotrichia leucophrys) or the
Harris’ Sparrow (Z. querula) (Table 3.3), in which badges of status only work between (but not
within) juvenile and adult birds, could be better related to delayed plumage maturation than to
status signaling theory. A similar argument could be used to discuss intersexual plumage
differences (see Balph et al. 1979).
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Birds with the greater badges do not always win
Typically, birds with larger or more colorful patches of color are dominant over birds
with smaller or less colorful traits (Table 3.1). There are cases, however, in which the
relationship may be reversed. Lemel & Wallin (1993a) showed in the Great Tit (Parus major)
that changes in motivation could allow hungry, small-badged birds to dominate larger-badged
ones. This is equivalent to other data on general dominance relationships not directly related to
status signaling, in which hungry subordinates are able to beat otherwise dominant individuals
(Popp 1987; Andersson & Åhlund 1991), and these observations agree with the theoretical view
that, when the value of the contested resource is high relative to the cost of fighting, contests
should not be settled by plumage (i.e. non-costly traits; Maynard Smith & Harper 1988; Maynard
Smith & Harper 2003).
Similarly, in territorial species, a prior-ownership advantage (Hammerstein 1981; Leimar
& Enquist 1984; Hughes 1986; Austad 1989) may override any badge-of-status advantage
(Rohwer 1982; Wilson 1992). In these territorial species, badges of status may therefore be
more efficiently used during the juvenile-dispersal period (Wilson 1992; Lemel & Wallin 1993a)
or in migratory species during the period of territory establishment (Pärt & Qvarnström 1997, but
see Studd & Robertson 1985b). Given the similarity between prior-ownership in territorial
species and prior-residency in flocking species (Oberski & Wilson 1991), we should also expect
that individuals with smaller or less colorful patches of color may sometimes dominate
individuals with bigger or brighter badges when entering a flock.
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Finally, badge size or color seems to have no impact on the outcome of agonistic
interactions between individuals with prior experience with each other (Lemel & Wallin 1993a,
Brotons 1998). In fact, the theory of status signaling was originally conceived as a means of
reducing agonistic confrontations between individuals unaware of the resource-holding potential
of opponents (i.e. strangers; Rohwer 1975; Rohwer 1982). As a consequence, status signaling
should be especially relevant in nomadic species (e.g. Eurasian Siskins), because an individual,
even if living in a group of relatively stable membership, can interact with thousands of different
individuals in a single winter (Senar et al. 1992). In fact, Eurasion Siskins have been recently
recognized as a model species in studies of status signaling (Maynard Smith & Harper 2003).
Does the type of color matter?
Recent research has shown how different kinds of colors in birds respond differently to
environmental stress and may have different production costs (see Hill 2005) and as a
consequence it has been suggested that the different signal types may have completely different
information contents (Badyaev & Hill 2000; Fitze & Richner 2002; Senar & Escobar 2002;
Senar et al. 2003). Most descriptions of status signaling refer to species displaying melaninbased plumage coloration (Table 3.1). This widespread and generalized relationship of melanin
to dominance suggests that social status is signaled primarily by melanin (see also Senar 1999;
Jawor & Breitwisch 2003, for reviews). The fact that hormones such as testosterone and
luteinizing-hormone are related both to melanin deposition in the feathers (i.e.: badge size;
Poiani et al. 2000; Peters et al. 2000; Evans et al. 2000a; Buchanan et al. 2001; González et al.
2001; McGraw et al. 2003b) and to aggressive behavior and dominance (Hegner & Wingfield
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1987; Wingfield et al. 1987; Collis & Borgia 1992; Poiani et al. 2000) perhaps explains why
melanin seems to be such a good signal of dominance and aggressiveness (McGraw et al.
2003b).
The link between dominance signaling and melanin-based coloration is far from
universal, however. Structural coloration has been linked to dominance in a few cases, most of
them related to white patches that result from incoherent scattering of light (Balph et al. 1979;
Jones 1990; Pärt & Qvarnström 1997), and some recent work has found a relationship between
social status and UV coloration (Alonso-Alvarez et al. 2004). Although some work has falsified
the role of carotenoid-based colored patches as status signals in some species (Wolfenbarger
1999b; McGraw & Hill 2000a; McGraw & Hill 2000c), studies of other bird species have
demonstrated the status-signaling role of color traits known to contain carotenoids (Pryke &
Andersson 2003; Pryke et al. 2002a). Hence, although social status and fighting ability is
typically signaled by melanin-based pigmentation, they can also be signaled by carotenoid and
structural coloration. Unfortunately, the status signaling function of carotenoid or structural
coloration is poorly studied.
Another topic of interest is whether the signal of dominance is related to the size of the
color ornament or to the intensity of coloration per se. Although, in mate choice, both
components are important, with higher emphasis on the color quality of carotenoid displays and
the patch size of melanin displays (Chapter 4), fighting ability is normally signaled by the size of
the colored region (Table 3.1), and there are only a few examples in which color intensity is of
known importance (Pryke et al. 2001; Pryke et al. 2002a; Mennill et al. 2003).
Traditionally
the focus has been on the size of melanin-based ornaments (Jawor & Breitwisch 2003), however,
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with only a few recent papers emphasizing the achromatic spectral variation in melanin patches
(e.g. Mennill et al. 2003). More research is needed on the role of patch size versus color quality
in signaling status.
Signal reliability
In a group of Mountain Sheep (Ovis canadensis), the males with the largest horns are
dominant because large horns confer a direct fighting advantage on their possessor (Geist 1966).
However, it is hard to see how the color of plumage could physically enhance competitive
ability. This is why it is said that plumage signals of status are arbitrary (Roper 1986; Maynard
Smith & Harper 1988). The problem with such an arbitrary signal is that subordinates could
easily pretend to be dominants simply by adopting the appropriate badge of status, in which case
status signaling would not be evolutionarily stable. The situation is further complicated by the
fact that, to be useful, true signals of status should be recognized before any real fights takes
place (Watt 1986a). To solve this evolutionary puzzle, several hypothesis have been proposed.
Cost related to behavior: The incongruency and the social-control hypotheses
Theoretical studies suggested that honest signaling of status could be stable whenever cheaters
pay a high cost against highly dominant opponents (Maynard Smith & Harper 1988; Maynard
Smith & Harper 2003). Rohwer (1977), Rohwer & Rohwer (1978), and Järvi et al. (1987b)
proposed that birds should be attentive to behavior in addition to plumage cues, and that
dominants would persecute any cheaters because of the perceived incongruity between their
behavior and their status signals (the incongruence hypothesis). The reason why dominants
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should act despotically would not be because cheats are cheats, but because such incongruent
individuals are usually sick birds (e.g. a dominant individual that has become ill), and thus easy
to chase away from limited food resources (Rohwer & Rohwer 1978). In its original form,
however, the incongruence hypothesis did not explain why behavioral cues should be disbelieved
in one context and morphological cues disbelieved in another. Additionally, the described
tendency to punish cheats was difficult to explain in terms of an advantage to the individual
(Caryl 1982). The hypothesis was therefore modified and re-named the skeptical-recipient
hypothesis by Caryl (1982), who suggested that, in agonistic encounters, animals should do the
following: where cues to dominance are inconsistent, it is better to believe the least impressive
information that the opponent provides, basically because no one lies to devalue oneself. The
hypothesis was supported by a series of experiments in which subordinate birds were either
painted to look as dominants, injected with testosterone to behave aggressively as dominants, or
both painted and injected (Rohwer 1977; Rohwer & Rohwer 1978; Järvi et al. 1987b).
Subordinates were able to rise in the dominance hierarchy and to beat dominants only in the last
experiment, in which birds both appeared and behaved as dominants. It seems, therefore, that a
dominant plumage signal must be backed by dominant behavior. Holberton et al. (1989)
challenged this view, proposing that by injecting testosterone in winter, authors might have
forced the birds to enter breeding condition and to behave as territorial birds rather than as
dominants. This criticism is likely incorrect because, although some authors have found that
there is no evidence that winter aggression in flocking birds is mediated by testosterone (Belthoff
et al. 1994), others have shown that levels of testosterone in the spring are correlated with levels
in other seasons (Buchanan et al. 2001) and that the very subtle differences in testosterone levels
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during the post-breeding period between individuals are enough to determine differences in
badge size (Buchanan et al. 2001) and aggression levels. Nevertheless, the incongruence
hypothesis predicts that birds should be tested or attacked when behavior and signal are
incongruent, and this prediction is thus not supported by studies of several species of birds in
which individuals are able to increase dominance just by having their plumage dyed (Table 3.2).
As an alternative to the incongruence hypothesis, Rohwer (1977) and Rohwer & Rohwer
(1978) proposed the social-control hypothesis, which suggests that a subordinate will encounter
relatively more aggression from true dominants as a cheater than as a honest signaler, simply
because dominants are normally fighting each other. As the intrinsic fighting abilities of
subordinates are lower on average than those of true dominants, the heightened aggression that
cheaters receive is a cost that would outweigh any benefits arising from increased dominance
status. For this strategy to be evolutionarily stable, heightened aggression should not result from
the 'persecution' of cheaters by true dominants in the population, but should be the result of
dominant individuals interacting more with other dominant birds than with subordinates (so
called "like-versus-like aggression" between dominant individuals; Rohwer & Rohwer 1978;
Møller 1987a; Slotow et al. 1993b).
The social-control hypothesis has been tested in several species ((Harris sparrow: Rohwer
1977; House sparrow: Moller 1987a, González et al. 2002b; White-crowned Sparrow: Slotow et
al. 1993b).). The results, however, are ambiguous (see Slotow et al. 1993b for a review). The
social control of cheating requires like-versus-like aggression between dominant individuals, and
although theoretical analyses stress the need for this aggression for the evolutionary stability of
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the status signaling system (Ripoll et al. 2004; Box 3.1), this like-versus-like aggression has been
shown not to be always the case (see Table 3.4 and Slotow et al. 1993b). Nevertheless, the test
species, White-crowned Sparrows, used by Slotow et al. (1993b) to demonstrate that like-versuslike aggression does not always occur, and hence falsify the social control hypothesis, is also a
species for which status signaling does not work within age and sex classes (Fugle et al. 1984a;
Fugle & Rothstein 1987). Without true status signaling, the White-crowened Sparrow is not a
suitable species on which to test this hypothesis. Data on this topic from studies of the House
Sparrow (Passer domesticus), the other model species, is contradictory (Møller 1987a; Solberg
& Ringsby 1997; González et al. 2002b; Table 3.4). Hence, given the suggestive results from
recent theoretical models (Ripoll et al. 2004; Box 3.1), more experimental tests of the social
control hypothesis are needed.
Like the incongruence hypothesis, the social-control hypothesis predicts that birds with a
dominant appearance should be tested and attacked. The fact that, in several species, individuals
are able to increase dominance just by having their plumage dyed (Table 3.2) is inconsistent with
the hypothesis (Slotow et al. 1993b; González et al. 2002b; Fig. 3.6). Additionally, theoretical
analyses have shown that social control is not enough to maintain the evolutionary stability of
the status-signaling system, because small-badged dominant individuals could invade the honest
population (Owens & Hartley 1991; Johnstone & Norris 1993). Nevertheless, and as Caryl
(1982) has pointed out, the presence of individuals lying to devaluate themselves is doubtful.
The use in these models of only two dominance classes has also been used to discredit them,
because an essential feature of badges of status is the possibility of continuous variation
(Maynard Smith & Harper 2003). Additionally, model species used to test this point either do
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not show a true signaling system or results published by different authors are contradictory (see
above; but see González et al. 2002b for a convincing study falsifying social control).
Fig. 3.6 about here
There is an additional problem with previous tests of these two hypotheses. Observers
have focused on the response of dominant birds (i.e. whether or not they attacked cheats), but
different interpretations can be drawn from such data. For instance, the fact that subordinates
that are dyed to look like dominants (cheats) do not incur increased aggression from true
dominants does not necessarily mean that they have deceived their flock companions; instead the
dyed birds may be actively avoiding confrontations, or dominants may actually recognise them
as subordinates by their behavior and not attack them because they are not a real threat. This
makes it harder to distinguish between the incongruence and the social-control hypotheses. I
have also previously mentioned how important familiarity between birds may be to resolving
agonistic encounters, so familiarity should be taken into account in any test of the incongruence
or social control hypothesis (Grasso et al. 1996).
Behavioral costs of dominance, unrelated to direct aggressive behavior, have also been
recognized (Számado 2000). Senar & Camerino (1998) showed that Eurasian Siskins are able to
recognize dominant individuals by the size of their black bib and that they actively avoid
dominants, preferring to feed in the company of subordinate birds. Given the importance of
flocking to find food and avoid predators (Pulliam & Millikan 1982; Pulliam & Caraco 1984;
Lima & Dill 1990; Krebs & Davies 1993; Senar 1994), the risk of isolation may be an additional
important cost for dominance (Senar & Camerino 1998a). It is unclear, however, how this cost
could relate to the production of badges of status or to the reliability of the system.
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Predation risk as a signaling cost
Alternatively, predation risk has been suggested to be the selective force controlling
cheating (Balph et al. 1979; Fugle et al. 1984a; Fugle & Rothstein 1987; Slotow et al. 1993b).
This hypothesis assumes that individuals displaying large or more colorful badges of status are
more easily detected by predators. Truly dominant birds, however, can compensate for the
handicap of higher conspicuousness with greater experience and ability to escape predators. A
higher capacity of large badged House Sparrows to escape predators has in fact been recently
reported (Moreno-Rueda 2003). A higher predation risk associated with larger badges of status
was also reported by Møller (1989) for the same species, but the tendency was far from clear
because it was only significant for a part of the population and only in autumn. It is hard to
believe, however, that an additional one centimeter of black color in the breast plumage will
make a bird more easily detected by a predator. Additionally, highly conspicuous colors, as for
instance black-and-white, may be disruptively cryptic in contrasting backgrounds (Götmark &
Hohlfält 1995). Alternatively, it could be as Veiga (1993c) has suggested, that dominant birds
(with the larger or most colorful badges) are more active (Møller 1990; Reyer et al. 1998) or
more exposed than subordinates and hence are more easily located and preyed upon (Götmark et
al. 1997). However, convincing empirical data to support (or reject) the differential predation
hypothesis is lacking. Perhaps experiments with mounts may be useful in future tests of this
hypothesis (Götmark & Unger 1994).
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Physiological costs
As outlined before, the main evolutionary problem with badges of status is their arbitrary
nature. The identification of a (physiological) production cost of production, however, would
solve part of the problem (Owens & Hartley 1991; Johnstone & Norris 1993; Számado 2000). It
has been suggested that, because testosterone plays a role in badge production (Poiani et al.
2000; Peters et al. 2000; Evans et al. 2000a; Buchanan et al. 2001; González et al. 2001;
McGraw et al. 2003b), its immunodepressive effects (Folstad & Karter 1992; Poiani et al. 2000;
Evans et al. 2000a; Buchanan et al. 2003 and references therein; see however Hasselquist et al.
1999) would dictate that large badges of status would be maintained only by individuals able to
bear this cost. A possible critique on this view is that most color badges are produced during the
pre-basic molt, in late summer or early autumn, when gonadal activity is low (Veiga 1993c).
Recent data, however, has shown that, although levels of testosterone during the post-breeding
period are lower than levels during breeding, these are enough to determine bib size after molt
(Buchanan et al. 2001). Recent work has also shown how testosterone interacts with other
hormones (e.g. corticosterone) and that these in turn can affect immunocompetence (“integrated
immunocompetence model”; Poiani et al. 2000). This latter study particularly supports the view
of immunosupression as the handicap that may maintain the reliability of the social status
signals, at least for those badges colored with melanin (Evans et al. 2000a; Buchanan et al.
2001).
Other handicaps of bearing elaborate badges of status have also been suggested.
McGraw (2003a) has recently suggested a biochemical mechanism related to the fact that
minerals (e.g. Ca, Zn, Cu, Fe) used as critical regulatory factors in the biosynthesis of melanin
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pigments can also be toxic to the body when accumulated in high concentration. Because
melanin granules bind these metals and store them in pigmented cells, animals might directly
reveal dietary access to these rare elements and the physiological protection they have afforded
themselves by displaying large deposits of melanin in feathers (McGraw 2003a). There is still
no empirical support for this biochemical handicap, however, and it should only apply to
melanin-based coloration.
Another of the proposed physiological costs of badges of status is a higher metabolic rate
of dominant individuals (Hogstad 1987; Johnstone & Norris 1993; Cristol 1995a; Buchanan et
al. 2001). In status signaling species, however, we would predict just the reverse: a higher
metabolic rate for subordinate individuals than for dominants. Subordinates have to be
continuously attentive to and actively avoid large-badged flock companions while dominants
enjoy preferential access to resources just by signaling their higher fighting ability (Senar &
Camerino 1998a). Data on Eurasian Siskins support this prediction (Senar et al. 2000) and
falsifies the view of metabolic rate as a generalized cost of badges of status.
The mixed ESS hypothesis
A totally different hypothesis to account for the control of deception is that social
hierarchies are examples of mixed evolutionarily stable strategies (mixed ESS; Maynard Smith
1982b; Számado 2000). Here, individuals of different status are presumed to pursue different but
equally fit strategies, so that the existence of a social hierarchy is to the direct advantage of each
individual (Rohwer 1982; Maynard Smith 1982b; Roper 1986). By abandoning the assumption
that dominants are at an advantage and that subordinates strive to become dominants (“hopeful
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dominants”, West Eberhard 1975; Ekman 1989; Hogstad 1989), the evolutionary puzzle about
deception is solved (Rohwer 1982; Számado 2000). Species displaying a feudal social system
(Rohwer & Ewald 1981; Wiley 1990; Senar et al. 1990a; Cristol 1995b; Senar et al. 1997)
conform nicely to this view. Data on reproductive success in Yellow Warblers (Dendroica
petechia) suggests that dominant and subordinate birds may follow different equally successful
strategies (Studd & Robertson 1985c; but see Yezerinac & Weatherhead 1997). House Sparrows
(Vaclav & Hoi 2002) and Collared Flycatchers (Ficedula albicollis; Qvarnström 1999) of
different badge-size classes and Ruffs (Philomachus pugnax; Lank et al. 1995) with different
plumage coloration also seem to develop different but equally successful strategies. In fact, the
existence of alternative tactics and strategies leading to different but equally successful
phenotypes is widely recognized for different taxa and systems (Gadgil 1972; Emlen 1997;
Moczek & Emlen 2000; Tuttle 2003). There are many other reports, however, that suggest that
dominants are at a clear advantage in many different respects (for a review see Senar 1994), so
that an idea of a mixed ESS for dominance hierarchies may not be general.
Recapitulating
How signals of fighting ability and social status can be evolutionarily stable is highly
controversial, and alternative hypotheses have proven difficult to test. Nevertheless, available
data suggest that three of the hypotheses may be especially relevant to explain the evolutionary
stability of badges of status. It is generally recognised that the presence of a physiological cost to
the production of badges of status would be enough to explain the evolutionary stability of the
system, and the “immunocompetence handicap” (Folstad & Karter 1992; Poiani et al. 2000;
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Evans et al. 2000a; Buchanan et al. 2001) appears nicely applicable to melanin-based signals.
There is still, however, some doubt as to whether this would also be applicable to species in
which melanin-based patches are quite small (e.g. the Eurasian Siskin), and by definition, this
cost should not be applicable to badges signaled by carotenoid or structural colorations. The
view of badges of fighting ability as a mixed evolutionarily stable strategy (Maynard Smith
1982b; Számado 2000) is another highly credible way by which the reliability of the system
could be maintained. However, we urgently need data on the fitness of individuals with badges
of status of different sizes to better appraise this hypothesis. This hypothesis should be most
applicable to social flocking species, and in territorial birds it should be only applicable when
alternative reproductive strategies are displayed. Finally, although recent tests seem to falsify
the social-control hypothesis (González et al. 2002b), theoretical data suggests this hypothesis to
be possible (and even probable) (Lachmann et al. 2001; Ripoll et al. 2004). A recent paper by
McGraw et al. (2003b) supports this view in that individuals experiencing higher rates of
aggression during molt (i.e. dominant individuals), grew larger badges than subordinates (Fig.
3.7); these data could nicely link like-versus-like aggression and the social control hypothesis
with the physiological costs relating hormones, immunocompetence, and badge production.
Hence, it is clear that additional careful tests of the predictions of the social control hypothesis in
a broad and integrative sense are still needed.
Fig. 3.7 here
Nevertheless, it is probable that there is no single route to the evolution of badges of
status and therefore there is no unique mechanism to maintain the honesty of the signals— none
of the current hypothesis is fully supported by the data and hypotheses that fit one species are
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falsified in others. The kind of social organization displayed by the species (e.g. feudal versus
despotic; Senar et al. 1997; Hagelin 2002) may be highly relevant. In a feudal social system,
both dominants and subordinates may be equally fit (mixed ESS, see above), allowing for a
stable system. In a despotic social system, in which only dominants are at advantage, other
mechanisms should be at work. For some species, sexual selection may well explain the
evolution of some armaments including color displays (Berglund et al. 1996), while in other
species the display traits may only have evolved by social selection (Tanaka 1996; Wolf et al.
1999). For instance, displaying a trait that developed by social selection may favor both
dominants and subordinates and this may be enough to explain the stability of the signal. If the
trait is additionally selected by females in mate choice, however, subordinates may be at
disadvantage and the stability of the trait may need to be explained in another way (Ripoll et al.
2004). It should be stressed here that although an evolutionary explanation for armaments that
become ornaments has been proposed (i.e. traits of dual utility) (Berglund et al. 1996), this is not
(nor needs to be) always the case (Jones 1990). For instance, some traits may evolve solely
under social selection, and females may not use the trait for mate (Qvarnström & Forsgren
1998). This is for instance the case of the Eurasian Siskin, in which females select a mate by the
size of the carotenoid-based wing patch rather than by the size of the black bib, which is a signal
of dominance (Senar et al. 2004) or the Red-collared Widowbird, in which females select mates
by the length of the tail rather than by the color and size of the dominance-related throat patch
(Pryke et al. 2002a). However, it is not clear which may be the key variables that modulate the
interaction or independence between social and sexual selection (Qvarnström & Forsgren 1998),
and this is obviously a field that also needs further investigation.
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Summarising, available data clearly show that honest status signals are possible
(Maynard Smith & Harper 1988; Grafen 1990; Maynard Smith & Harper 2003; see Tables 3.1
and 3.2) and that there are different ways of controlling cheating. Competing hypotheses for
maintaining signal honesty are not mutually exclusive, and it is likely that different mechanisms
or combinations of mechanisms work in different contexts.
The frequency distribution of badges of status
Central to the discussion of the evolution of status signaling is how badge sizes are
distributed within and among sex and age groups. Rohwer and Ewald (1981) proposed that there
should be bimodal distributions, with many birds either having large or small badges, but fewer
individuals with intermediate badge sizes. Such a frequency distribution of badge sizes could be
maintained by negative frequency-dependent selection, whereby individuals of different
appearance and status either play mutually beneficial roles or employ alternate competitive
tactics (Rohwer 1982). Analyses of the frequency distributions of badge sizes from most
species, however, reveal that normality is the rule (Rohwer 1982; Jones & Hunter 1999; Fig.
3.8). Only the Eurasian Siskin has been found to display a bimodal distribution of status
signaling badge sizes (Senar et al. 1993d).
Fig. 3.8 about here
A recent hierarchical nonlinear matrix model, taking as evolutionary variables the (vector
of) probabilities of moving to other bib-size classes (Ripoll et al. 2004), has predicted the
conditions that favor bimodal versus normal distributions in status signaling characters at
equilibrium (evolutionary stability; Boxes 3.1 and 3.2). This model takes into account
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population parameters such as survival, reproduction, and rates of aggression. The first
conclusion of the model is that the prerequisite for a status-signaling system to be evolutionarily
stable is like-versus-like aggression between dominant individuals (Box 3.1), which, as outlined
before, lends support to the social-control hypothesis. A second result is the distinction between
potential (or inherent) survival and reproductive rates, which are values in a virgin environment
without competition or aggression among members of the population, and the values that these
rates reach at equilibrium, when competition effects among members of the dominance classes
are present. For example, when different dominance classes do not differ in pairing success, as
is the case with Eurasian Siskins (Senar et al. 2004), our model predicts that the survival rates at
the equilibrium for different badge size classes should not differ. Preliminary observations
suggest that, in fact, this is what happens in the Eurasian Siskin (pers. obs.). Finally, the model
allows one to predict under which circumstances the frequency distribution of different badge
sizes can become normal or bimodal (Box 3.2). The model states that, for bimodality to be
stable, the sum of potential survival and fecundity rates of dominant individuals should be higher
than that of subdominant birds, and subordinates should not be engaged in much intra-class
aggression. For instance, bimodality can be expected when large-badged individuals
(dominants) do not enjoy a pairing advantage but do experience higher potential survival than
smaller-badged birds. Again, this is what is observed in the Eurasian Siskin, in which birds
display a bimodal distribution of badge sizes (see above).
Bimodality can also appear in species in which badges of social status raise the potential
reproductive success of dominant individuals such as by female choice (i.e.: ambivalent
characters, Berglund et al. 1996). In this case, potential survival of dominant individuals is of
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minor importance. When potential survival for those dominant ornamented individuals is low,
however, the frequency distribution of the ornament may shift to a normal shape. This is in fact
what seems to happen to most ornamented species, for which the ornament may act as a
handicap that reduces potential survival (Grafen 1990; Johnstone 1995). Similarly, when
fecundity is independent of the size of the badge of dominance, a lower survival for individuals
displaying larger badges of status, for instance because of predation (Balph et al. 1979; Fugle et
al. 1984a; Fugle & Rothstein 1987; Møller 1989; Slotow et al. 1993b), could also select for
normal distributions.
Advertising youth and low competitive ability
Birds usually achieve adult plumage coloration at the end of the post-juvenile molt (Jenni
& Winkler 1994). In many bird species, however, full adult plumage coloration is only achieved
after a delay of one or more years. This delay has been termed “delayed plumage maturation”
(DPM; Selander 1965; Rohwer 1978a). DPM is most common in species (1) in which adults
have a higher competitive ability than yearlings species, (2) with a long life span but high
mortality rate during the breeding season (Studd & Robertson 1985a), and (3) that forage in
flocks rather than solitarily during winter (Beauchamp 2003). More importantly, DPM is more
common in dichromatic species (Beauchamp 2003) and in species in which females select a mate
on the basis of ornamental plumage coloration rather than on the basis of territory quality
(Montgomerie & Lyon 1986; Weggler 1997). Under these circumstances, male competition is
increased, and it may be advantageous for yearling birds to signal to adults their youth and their
lower competitive ability to obtain females, avoiding in this way aggressions from the adult
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class. DPM is hence currently (mostly) interpreted as a signal advertising youth, inexperience,
and poor competitive ability (Senar 2004).
Two key points distinguish DPM from true social status signaling. First, as discussed
before, DPM traits work to signal competitive ability between age classes (Senar 1999). Second,
DPM traits do not seem to signal fighting ability per se. Because of their inexperience, immature
birds have lower fighting ability than adults and they display colors that are unattractive to
females, thus avoiding competition with adults (Lawton & Lawton 1986; Lyon & Montgomerie
1986). In other words, it could be argued that the presence of ornamental plumage traits signals
dominance, whereas the presence of DPM traits signals subordinance. Several well-designed
experiments with bird models and detailed behavioral observations have shown how birds in
immature plumage (DPM) succeed in eliciting less aggression from adult birds (Table 3.5).
Hence, I stress that DPM signals have their own selection pressures and can be treated as signals
that are distinct from signals of social status.
Alternative hypothesis on DPM
Although the more general view of DPM is that the trait signals a low competitive ability,
other hypotheses have been proposed to explain DPM. The female-mimicry hypothesis proposes
that the aim of DPM is to allow males to mimic females, avoiding in this way attacks from adult
males (Rohwer 1978a; Rohwer et al. 1980). Work on Pied Flycatchers (Ficedula hypoleuca;
Slagsvold & Saetre 1991) and Eurasian Kestrels (Falco tinnunculus; Hakkarainen et al. 1993), in
which adult males do not distinguish females from immatures, supports this view (see also Table
3.5). The juvenile-mimicry hypothesis proposes that immature birds with DPM mimic non-
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reproductive juveniles, in this way avoiding aggression from the adult class (Lawton & Lawton
1986; Foster 1987; Table 3.5). Both hypotheses assume that the reduced aggression that
immatures receive from adults is through deception rather than signaling. It is very difficult,
however, to ascertain this intention (Semple & Mccomb 1996), and because the aim underlying
all of these hypotheses is the same, I think it is more parsimonious to take all of these hypothesis
as equivalent, irrespective of the plumage that immatures are wearing (female-like, juvenile-like
or immature per se) to reduce the aggression they receive from adults (see also Lawton and
Lawton 1986; Thompson 1991).
The remaining alternative hypotheses to explain DPM assume a non-signaling function of
the trait. The cryptic hypothesis proposes that immature plumage allows birds to avoid the attack
of predators (Selander 1965; Procter-Gray & Holmes 1981; Hill 1988; Stutchbury 1991; Table
3.5). Some work has found that the more cryptic plumage of immature birds makes them less
vulnerable to predation (de Vries 1976; Slagsvold et al. 1995; Götmark et al. 1997; Götmark
1997). However, although DPM may reduce predation, this is probably not the evolutionary
force selecting for this plumage. There are many species for which the difference between
immatures and adult birds appears as just a few feathers (e.g. greater coverts; Jenni & Winkler
1994), and although these feathers do not confer to immatures a cryptic appearance, they are
enough to reduce the aggression they may receive from adult birds (Lyon & Montgomerie 1986;
Senar et al. 1998b). Additional discredit for the hypothesis comes from the fact that, if crypsis
was the main selective pressure, immatures should behave cryptically and should retain the
cryptic brown and streaked plumage of most juvenile birds, and this is not the case (Rohwer et
al. 1980). The non-adaptive hypothesis suggests that DPM is the result of an energetic constraint
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that prevents an additional feather molt (Rohwer 1986; Rohwer & Butcher 1988). The fact that
some birds undertake a complete molt to obtain again an immature appearance, however,
falsifies this hypothesis (Rohwer & Butcher 1988).
Adult plumaged immatures
Although DPM refers to birds with a distinctive immature appearance, immature plumage
can be highly variable and some individuals may highly resemble adults (Rohwer et al. 1980;
Lyon and Montgomerie 1986). Detailed behavioral observations have shown how these birds
with an “advanced plumage maturation” (APM) enjoy a higher mating and breeding success than
individuals with DPM (Ralph & Pearson 1971; Rohwer & Niles 1979; Payne 1982; Price 1984;
Hill 1988; Grant 1990). Analyses of patterns of aggression show that adult-plumaged immatures
are distinguished by the adult class from adults and immature plumaged birds, and are the target
of aggressive interactions from the adult class, probably because these APM individuals are
really highly competitive in attracting females (Table 3.5; Hill 1989; Smith 1992; Gosler 1993;
Senar et al. 1998b). The fact that, under harsh environmental conditions, APM birds lose body
condition and have higher mortality rates compared to DPM birds (Grant 1990; Senar et al.
1998b) emphasizes the trade off between sexual signaling and survival.
Adaptation to the winter or to the spring?
It has been debated whether DPM is an adaptation to winter or to spring conditions
(Rohwer 1983; Rohwer & Butcher 1988). Earlier hypothesis on DPM assumed that the trait had
evolved as an adaptation to spring, when competition with adult birds is thought to be more
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intense. However, it could be that DPM had appeared as an adaptation to winter, to aid
immatures in avoiding aggressions from adult birds. Winter adaptation could cause birds to be
less competitive in mate attraction in the spring (Rohwer & Butcher 1988). The fact that several
bird species may pair during winter (Senar & Borras 2004) additionally complicates the
situation.
A way to resolve this controversy is to focus on species that develop a spring molt and to
compare plumages in winter and spring. Immature Indigo Buntings (Passerina cyanea), for
instance, display a female-like plumage during autumn and winter, but molt in spring to an adultlike plumage, supporting the view that DPM is functional during the wintering period (Rohwer
1986). In contrast, Painted Buntings (Passerina ciris) molt into a female-like plumage in spring,
which suggests that DPM is functional in both periods (Thompson 1991). In spite of
interspecific variation, however, most species with spring molt change from a delayed to an
adult-like plumage, while species that display DPM throughout the year do not show spring molt
(Rohwer & Butcher 1988). This led Rohwer & Butcher (1988) to suggest that DPM was an
adaptation for the winter (when aggression is probably more costly), and that most species
displayed DPM during the breeding season because of a molt constraint that prevented these
species from molting in spring to a more colorful plumage. Comparative analyses support this
view (Beauchamp 2003).
The evolutionary history of DPM
A key point to the understanding of DPM is whether this is an ancestral or derived trait.
Comparative analyses on House Finches have shown that DPM in this group has evolved
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recently (Hill 1996). Data from gulls, fulmars, and waders, however, suggests that DPM in this
group is the result of collateral selection on reduced molt, suggesting that DPM per se has no
function (Chu 1994). Comparative analyses from nine-primared oscines suggested that DPM in
these birds is an ancestral character, and that the evolutionary novelty had been the appearance of
immatures with an adult-like plumage (Björklund 1991); this is why Björklund (1991) proposed
that it would be more suitable to refer to a process of “advanced plumage maturation” rather than
DPM. In any case, until we get more data from a broader range of taxa, comparative data shows
that DPM may have evolved several times and probably for different reasons in different groups
(Weggler 1997).
Intrasexual signaling not related to fighting ability
Bird colors may function as signals in other intrasexual social contexts not related to
aggression and dominance (Chapter 4). Some early work proposed that white patches in wings
and on other body parts could function as signals to recruit conspecific individuals at feeding
patches (Armstrong 1971; Kushlan 1977). The increased size of the flock would then improve
vigilance and the probability of detecting predators (Hinde 1961). Recent comparative data
supports this function for white patches (Beauchamp & Heeb 2001).
Conversely, it has been suggested that white patches in rump feathers, tails, or wings
could act as warning flashes, signaling to flock companions the presense of a predator (Brooke
1998). Such a signal could be beneficial to the signaler by getting flock companions to take
flight, creating a dilution effect. Some detailed work (Alvarez 1993; Alvarez 1989) however,
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suggests that other alternatives, such as startling predators, better explain the appearance of these
flashes (e.g. (Brooke 1998).
Summary
Nearly three decades after the original description of fighting-ability and status-signaling
hypotheses, and after several reviews, the role of color displays in intrasexual signaling remains
controversial. Nevertheless, we can now safely state that, at least for several species, there exists
a true signaling of fighting ability and social status. This may be particularly relevant for species
in which many unfamiliar individuals interact, so that individual recognition is unlikely.
Signaling between but not within age and sex classes should not be regarded as true status
signaling. Most descriptions of status signaling refer to species displaying melanin-based
plumage coloration, but carotenoid and structural color displays can also signal status. Fighting
ability is normally signaled by the size of the trait, and there are only a few examples in which
color quality is of importance. I identify cases where the relationship between fighting ability
and plumage badges may reverse.
Different hypotheses have been proposed to explain the reliability of badges of status.
Three of them may be especially relevant: 1) the social-control hypothesis, which proposes that
only high quality dominant individuals can afford the aggression rate in which high status
individuals are generally involved, 2) the “immunocompetence handicap”, which proposes that
only high quality dominant birds can afford the immune depression of hormones necessary to
produce melanine, and 3) the mixed evolutionarily stable strategy hypothesis, which views large
badged dominants and small badged subordinates as displaying different but equally fit
strategies, so that there is no reason for subordinates to pretend to increase their rank. Recent
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theoretical and empirical data links social and physiological costs, which could nicely explain
signal reliability for melanin based signals. I additionally discuss drawbacks of some of the
experiments used up to now to test the reliability of the status signaling system. Nevertheless, it
is probable that there is no single route to badges of status and therefore there is no unique
mechanism to maintain the honestity of the signals. Finally, I present a model that explains why
the frequency distribution of badges of status generally follows a normal distribution, but also
provide instances in which it should be bimodal, as it is in fact the case in a few species.
Although fighting ability is the most common information provided by color patches,
other social scenes can also be of importance. Delayed plumage maturation, in which immature
birds display a plumage different from that of adult birds, is used by immature birds to signal to
adults their youth and lower competitive ability to obtain females, avoiding in this way
aggressions from the adult class. Color patches can also be used to attract conspecifics,
increasing in this way the size of the flock and hence the possibilities to detect predators.
Acknowledgements
I am most grateful to Geoffrey Hill, Kevin McGraw, Lluïsa Arroyo, and Joan Saldaña for
critically reading the manuscript. I also thank Joan Saldaña for writing the text of the model
displayed in the boxes and Olaf Leimar for his comments on its content. Pedro Cordero
provided the House Sparrow data in Fig. 3.8. This work was supported by research project
BOS2003-09589 from the Spanish Research Council, Ministerio de Ciencia y Tecnología.
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186
Hill & McGraw - 187
BOX 1 . A matrix model for the dynamics of n dominance classes
A recent hierarchical nonlinear matrix model by Ripoll et al. (2004), predicts that one of
the conditions for the evolutionary stability of status signaling systems is the presence of
like-versus-like aggression between the individuals of a dominant class. The model also
predicts under which circumstances badges of status will show a normal or a bimodal
frequency distribution (Box 3.2), which additionally allows a better understanding of the
interaction between sexual and social selection in shaping signals of fighting ability. The
model takes as evolutionary variables the (vector of) probabilities of moving to other bibsize classes. The mathematical development of the model follows:
A matrix model for the dynamics of n dominance classes is given by
N (t + 1) = (TS ( N (t )) + F ( N (t )) N (t ) ,
where T = (! ij ) is a transition matrix with 0 ! " ij ! 1 and
n
!"
ij
= 1 for all j, S = ( sij ) is a
i =1
survival matrix with sij = 0 for i ! j , and sii = si > 0 ( i = 1,K, n ), and F = ( f ij ) is a
fertility matrix such that f ij = 0 for all i ! 2 (we assume that all the newborns belong to
the subordinate dominance class). Finally, N (t ) is a vector with the number of individuals
in each class at time t as components.
The ranking or dominance hierarchy is introduced through the dependence of
the survival probabilities ( si ) and fertilities ( f i ) on a weighted average of the population
accounting for the mean number aggressive encounters per time interval. This number, of
course, is different for each dominance class and is computed from !ij , the probability
that an i-class individual suffers an aggressive encounter from a j-class individual per
time interval ( 0 ! "ij ! 1 ), regardless of the result of each encounter. These probabilities
are used to define the biotic environment experienced by the individuals in each class, in
such a way that the higher is the average number of these encounters in a given class, the
higher are the stressing conditions suffered by individuals in this class. In particular, if
187
Hill & McGraw - 188
W = (!ij ) , the per capita mean number of aggressive encounters in each class is given by
the vector ! (t ) = WN (t ) . In this context, !ij > ! ji means that individuals of the j-class
dominate individuals of the i-class.
According to this measure of the competition effects on each dominance class, we
can assume that si and f i are strictly decreasing functions of !i (t ) , the i-th component of
! (t ) . In particular, for each class, we assume that
si (!i ) = si0 Fi (!i (t )) and
f i (!i ) = f i 0 Fi (!i (t )) with si0 + f i 0 > 1 and Fi ! 0 as #i " ! . These hypotheses
guarantee the existence of a positive equilibrium N * of the model THAT is locally stable
for, at least, values of si0 + f i 0 > 1 but close to 1 for i = 1,K, n (see Ripoll et al., 2004, for
details).
Evolutionarily stable strategies. Let us consider a strategy defined by a vector !
containing as components a given subset of the transition probabilities ! ij . This will be a
suitable choice for a strategy if, for instance, one accepts that it is possible to change the
value of some ! ij behaviorally in order to maximize fitness. The evolutionarily stable
values of the transition probabilities ! ij appearing in ! , using the net reproductive
number R0 (! , N * ) as a fitness measure, are those values ! ess of ! that render an
equilibrium N * such that
si (!i* ) + f i (!i* ) = 1 for i = 1,K, n,
where "i* = "i ( N * (! ess )) . Note that these equalities says that, at the equilibrium
determined by ! ess , all dominance classes have the same fitness (measured by the sum
survival plus fertility) and, in fact, all of them have the same reproductive value. In other
words, there exists a sort of “ideal free distribution” of individuals among dominance
classes.
On the other hand, it is easy to see that any strategy ! ess is evolutionary neutral in
the sense that, in a resident equilibrium population adopting ! ess , any mutant population
with a different strategy ! mut will be also at equilibrium, i.e., that R0 (! mut ; N * (! ess )) = 1
for all " mut ! [0,1]. That is, the function ! " R0 (! , N * (! ess )) does not have a strict
maximum at ! = ! ess . However, using a 2x2 matrix model, it is easy to show that a
necessary condition for ! ess to be the limit of trait substitution sequences (TSSs) in the
trait space # = {($1 ,$ 2 ) " [0,1]! [0,1]}, i.e., like-versus-like aggression among individuals
of the dominant class is a neccessary condition for the mathematical convergence to be
stable.
Consider, for instance, the model with the following transition and aggression
matrices
188
Hill & McGraw - 189
)2 #
1 ' (1 #
&1 ' ) 1
& (
!! , W = $$ 1
!,
T = $$
1 ')2 "
( 2 !"
% )1
%1 ' ( 2
with 0 ! # i , "i ! 1 (i = 1,2) . In order to have a unique equilibrium N * = W !1C defined by
! ess , det(W ) = #1# 2 " (1 " #1 )(1 " # 2 ) = #1 + # 2 " 1 ! 0 . Note that this expression is, in
fact, a measure of the balance of an average of aggression within ( !1! 2 ) and between
( (1 " !1 )(1 " ! 2 ) ) dominance classes. So, when !1 + ! 2 > 1 , we talk about like-versus-like
aggression because then !1! 2 > (1 " !1 )(1 " ! 2 ) . The simplest way to check the necessity
of this sort of aggression for the convergence stability of ! ess is by computing the fitness
gradient ("R0 / "!1 , "R0 / "! 2 ) at the boundary of trait space ! given by
{(0," 2 ) : 0 ! " 2 ! 1}. Then it follows that, at any point of this boundary, !R0 / !" 2 = 0 and
!R0 / !"1 > (<) 0 when !1 + ! 2 > (<) 1 . That is, only when !1 + ! 2 > 1 , TSSs escape
from the boundary {(0," 2 ) : 0 ! " 2 ! 1}, which is a necessary condition for the
convergence of TSSs towards a ! ess since such an strategy never has the form (0,! 2 ) for
any 0 ! " 2 ! 1 .
189
Hill & McGraw - 190
BOX 2
Bimodality of the equilibrium. Even though the model in Box 1 is nonlinear, an explicit
expression of N * (! ess ) is easily obtained under the hypotheses on si and f i , and
assuming that W is an invertible matrix. This fact allows one to establish precise
conditions for the bimodality of N * under evolutionarily stable transition rates among
dominant classes. Precisely, from the condition si (!i* ) + f i (!i* ) = 1 , it immediately
follows that the equilibrium is given by
N * (" ess ) = W !1C
with C a constant vector with components ci = Fi !1 (1 /( si0 + f i 0 )) . In particular, for a 3x3
matrix model with
& (1 (1 ' (1 ) / 2 (1 ' (1 ) / 2 #
$
!
W =$ 0
(2
1 ' (2 ! ,
$0
!
1 ' (3
(3
%
"
and Fi (! ) = F (! ) for i = 1,2,3 , it immediately follows that N 2* < N 3* is equivalent to
c3 > c 2 as long as !1 > 0 and ! 2 + ! 3 > 1 (i.e., under like-vs-like aggression), which
implies that the sum of potential survival and fertility rates of dominant individuals
( s30 + f 30 ) has to be higher than that of subdominats ( s 20 + f 20 ). On the other hand, the
second condition for bimodality, namely, N 1* > N 2* , is satisfied for a wide range of values
of si0 , f i 0 , and ! i for any N * (! ess ) > 0 as long as the probability of aggressive
encounters among subordinates, !1 , is small enough (for details see Ripoll et al., 2004).
190
Hill & McGraw - 191
Fig. 3.1. The relationship between bib size and dominance score in captive European
Siskins. Note that the correlation is independent of the age of the birds. The presence of
this correlation, however, is not sufficient as evidence for signaling, and manipulation
experiments are needed (see Figs 21.8 and 3.5). Redrawn from Senar et al. (1993d).
Fig. 3.2. The proportion of interactions (mean ±SE) won by previously dominant Darkeyed Juncos before and after a plumage manipulation in which the size of status badges
was reduced. Redrawn from Grasso et al. (1996).
Fig. 3.3. The effects of manipulations of the red plumage patches of the Red-collared
Widowbirds on the mean (± SD) territory size (bottom) and number of aggressive
interactions (top) for males establishing territories. Redrawn from Pryke et al. (2002a).
Fig. 3.4. Left: Histogram of the closeness of approach (left) and behavior toward (right)
a Great Tit dummy by live Great Tits with breast stripes that were either wider or
narrower than the dummy’s. Live birds with wide breast stripes approached significantly
closer to the dummy, and more aggressively, than did birds with narrow stripes.
Redrawn from Järvi & Bakken (1984b).
Fig. 3.5. An experiment to test whether individual European Siskins recognize dominants
by the size of the bib. Choice was measured (upper panel) as willingness to feed close to
a cage containing a live Eurasian Siskin with a large bib or close to another cage
containing a live Siskin with a small bib (bibs either natural or manipulated). The six
191
Hill & McGraw - 192
graphs show the results from experiments in which male Eurasian Siskins were presented
with a choice between two food patches that differed only in the identity (and relative
dominance) of the adjacent stimulus flock companion. In Expt 1, neither stimulus cage
contained a bird, whereas in Expt 2 both contained a bird with a smaller badge than the
test bird (i.e. subordinates). In Expt 3, the released bird had to choose between a female
(a clearly subordinate individual) and an empty small cage. In Expt 4, the stimulus birds
were two male siskins differing in bib size, so that one was clearly dominant and the
other clearly subordinate. In Expt 5, two birds with small badges were used, but one of
the individuals had its black bib experimentally enlarged. In Expt 6, a bird with a small
badge and a bird with a large badge were used, but both badges had been experimentally
removed. Results are expressed as the mean (±SE) percent of time that the test bird
stayed close to one or another stimulus bird during a 3-min trial. The outcome of
Wilcoxon signed-rank tests and number of trials are shown. Redrawn from Senar &
Camerino (1998a).
Fig. 3.6. Proportion of total fights (+SE) won for experimental and control House
Sparrows before and after badge-size manipulation. Redrawn from Gonzalez et al.
(2002b).
Fig. 3.7. Scatterplots of the relationships between the group rate of aggressive
interactions during molt and both mean post-molt badge size and mean change in badge
size of caged male House Sparrows. Males that had held a higher social status tended to
grow larger black patches. Redrawn from McGraw et al. (2003b).
192
Hill & McGraw - 193
Fig. 3.8. Distributions of male bib sizes in three species of birds for which the bib
functions as a signal of social status. House sparrow (Møller 1987c); bib size measured
according to Møller (1987c); Shapiro Wilk W= 0.99, p = 0.91, N=80, 1983-1986. Great
Tit (Järvi & Bakken 1984b); bib size measured according to Figuerola and Senar
(2000b); Shapiro Wilk W= 0.99, p = 0.18, N=160, 1997-2000. European Siskin (Senar &
Camerino 1998a); bib size measured according Senar and Camerino (Senar & Camerino
1998a); Shapiro Wilk W= 0.93, p < 0.001, N=3454, 1990-2000. Based on Ripoll et al.
(2004).
193
adult
young
Dominance score
100
50
0
-50
r = 0.71
p < 0.01
-100
0
20
Bib size
40
(mm2)
Figure 15-1
Senar
Proportion of wins by original dominant
experimental manipulation (n = 7)
sham control (n = 7)
1.0
0.8
0.6
0.4
0.2
0
Before
treatment
After
treatment
Figure 15-2
Senar
Mean encounter rate (min-1)
Mean territory size (ha)
enlarged
reduced
0.3
0.2
0.1
0
1.5
1
0.5
0
red
orange
control
Figure 10-3
Senar
Test bird’s tie width:
> dummy’s
> dummy’s
Number of trials
10
8
6
4
2
0
5
10
15
20
25
Closest approach to dummy (cm)
aggressive
submissive
Behavior
Figure 15-4
Senar
releasing cage
food
food
?
left
test
cage
perch
right
test
cage
one-way window
100
Expt 2 (n = 20)
Expt 1 (n = 25)
50
NS
NS
0
Mean percent of time
Empty A
Empty B
Small bib
Small bib
100
Expt 4 (n = 25)
Expt 3 (n = 24)
50
p < 0.05
p < 0.05
0
Empty
Female
Large bib
Small bib
100
Expt 5 (n = 40)
Expt 6 (n = 24)
50
p < 0.05
NS
0
Enlarged bib
Small bib
Reduced bib
Small bib
Figure 15-6new
Senar
control
badge increased
Proportion of fights won
1.0
0.5
0
before
after
Badge manipulation
Figure 15-7
Senar
Change in bib area (mm2)
200
100
0
intact
castrated
+
empty implant
high
low
testosterone
Figure 15-8
Senar
House Sparrow
20
10
0
Number of individuals
300
380
460
Great Tit
40
20
0
300
700
1100
600
Siskin
400
200
0
0
20
40
60
Bib size (mm2)
Figure 15-9
Senar
Post-molt
badge size (cm2)
7
6
Change in
badge size (cm2)
1.0
0
-1.0
0
20
40
Aggressive interactions
during molt (h–1)
Figure 15-10
Senar
Table 15.1. The relationship between plumage color and dominance. In all cases, the relationship between the two variables is positive, except in the House Finch. Data on
the Northern Cardinal (Cardinalis cardinalis) and the House Finch is surprising in that although natural plumage color is correlated to dominance, the relationship disappears
in manipulated birds.
_____________________________________________________________________________________________________________________________________________________
Nature of
plumage
Species
plumage variability
Trait
Type
manipulation
prop won author
_____________________________________________________________________________________________________________________________________________________
Spheniscus demersus
Phasianus colchicus
Aethia pusilla
Charadrius alexandrinus
Cinclus cinclus
Agelaius phoeniceus
black & white contrast on head
general body surface
white underpart
black lateral breast band
area of the chesnut lower breast
red epaulets
size
color
size
size
color
size
(Ryan et al. 1987)
(Mateos & Carranza 1997)
75%
(Jones 1990)
(Lendvai et al. 2004)
(Bryant & Newton 1994)
(Peek 1972; Smith 1972; Roskaft & Rohwer 1987;
Eckert & Weatherhead 1987b)
Euplectes axillaris
red epaulets
size
Carotenoid
Yes
93%
(Pryke & Andersson 2003)
Euplectes ardens
red throat patch
color/size
Carotenoid
Yes
(Pryke et al. 2001; Pryke et al. 2002a)
Nectarinia johnstoni
scarlet pectoral tuft
size
(Evans & Hatchwell 1992)
Dendroica petechia
brown streaking in breast
size
Melanin
Yes
(Studd & Robertson 1985b)
Ficedula albicollis
frontal white patch
size
Structural
Yes
(Pärt & Qvarnström 1997)
Poecile atricapilla
black cap and bib
color
Melanin
No
94%
(Mennill et al. 2003)
(Järvi & Bakken 1984b; Maynard Smith & Harper 1988;
Parus major
black breast stripe
size
Melanin
Yes
r2= 74%
Wilson 1992; Lemel & Wallin 1993a)
Parus caeruleus
UV of crown
presence
UV
Yes
(Alonso-Alvarez et al. 2004)
2
(Hogstad & Kroglund 1993)
Parus montanus
black breast stripe
size
Melanin
Yes
r = 92-96%
Parus ater
black breast stripe
size
Melanin
Yes
(Brotons 1998)
Fringilla coelebs
red breast
color
Carotenoid
No
(Marler 1955)
Carpodacus mexicanus
red breast
color
Carotenoid
Yes
(McGraw & Hill 2000a; McGraw & Hill 2000c)
Carduelis chloris
general plumage yellowness
color
Carotenoid
No
(Maynard Smith & Harper 1988)
(Senar et al. 1993d)
Carduelis spinus
black bib
size
Melanin
Yes
r2= 50-70%
(Møller 1987c; Maynard Smith & Harper 1988;
Passer domesticus
black bib
size
Melanin
Yes
r2 s= 27-79%
Solberg & Ringsby 1997; Liker & Barta 2001;
González et al. 2002b; McGraw et al. 2003b)
Emberiza calandra
black bib
size
Melanin
No
(Maynard Smith & Harper 1988)
Cardinalis cardinalis
red general body
color
Carotenoid
Yes
(Wolfenbarger 1999b)
Junco hyemalis
head and bib blackness
size
Melanin
No
69%
(Balph et al. 1979; Ketterson 1979)
white in tail
size
Structural
No
72%
(Balph et al. 1979)
Zonotrichia querula
head and bib blackness
size
Melanin
Yes
75%
(Rohwer 1975)
Zonotrichia leucophrys
black and white in head
size
Melanin
Yes
87-96%
(Parsons & Baptista 1980; Fugle et al. 1984a)
____________________________________________________________________________________________________________________________________________
1
Melanin
Mixed
Structural
Melanin
Melanin
Carotenoid
No
Yes
Yes
Yes
No
Yes
size = area of colored feathers; color = hue, saturation, or brightness of colored patch
r2=percentage of dominance explained by the size of the plumage trait (according to a regression); when only a percentage is provided it refers to the proportion of contests in
which the bird with the larger badge won agonistic encounters.
2
1
Table 15.2. Overview of the different experiments carried out to test for the status-signaling role of plumage traits. In the experiments, the
stimulus birds were manipulated by enlarging the badge of status (dyeing subordinates) or reducing it (dyeing dominants).
_________________________________________________________________________________________________________________________________
Experiment
Species
Effect
Author
_________________________________________________________________________________________________________________________________
dyeing
Euplectes ardens
raising dominance
(Pryke et al. 2002a)
subordinates
improved territory defense
(Pryke et al. 2002a)
Euplectes axillaris
raising dominance
(Pryke & Andersson 2003)
improved territory defense
(Pryke et al. 2002a)
Phylloscopus inornatus increase territory size
(Marchetti 1998)
Parus major
raising dominance
(Lemel & Wallin 1993a)
no effect
(Järvi et al. 1987b)
Zonotrichia querula
raising dominance
(Rohwer 1985)
no effect
(Rohwer 1977)
Zonotrichia leucophrys raising dominance
(Parsons & Baptista 1980; Fugle et al. 1984a; Fugle & Rothstein 1987)
Junco hyemalis
raising dominance
(Holberton et al. 1989; Grasso et al. 1996)
Cardinalis cardinalis
no effect
(Wolfenbarger 1999b)
Fringilla coelebs
raising dominance
(Marler 1955)
Carpodacus mexicanus no effect
(McGraw & Hill 2000a)
Passer domesticus
raising dominance
(González et al. 2002b)
dyeing
dominants
Geothlypis trichas
Agelaius phoeniceus
increased aggression
loosing territory
(Lewis 1972)
(Peek 1972; Smith 1972; Roskaft & Rohwer 1987)
model
presentation
Aethia pusilla
Dendroica petechia
Setophaga ruticilla
Euplectes ardens
Parus major
Parus montanus
Passer domesticus
model avoidance
heightened aggression
no effect
reduced aggression
model avoidance
model avoidance
model avoidance
(Jones 1990)
(Studd & Robertson 1985b)
(Procter-Gray 1991)
(Pryke et al. 2001)
(Järvi & Bakken 1984b)
(Hogstad & Kroglund 1993)
(Møller 1987c)
choice tests
Carduelis spinus
large badges avoided
(Senar & Camerino 1998a)
_________________________________________________________________________________________________________________________________
2
Table 15.3. Species showing a relationship between plumage color display and dominance, Relationships are broken down for status signaling
that occurs between the sexes, different age classes, or individuals (i.e. within ages and sexes).
--------------------------------------------------------------------------------------------------------------------------------------------------Groups differing in plumage color display
________________________________
Species
sexes ages
individuals
author
--------------------------------------------------------------------------------------------------------------------------------------------------Aethia pusilla
Y
Y
Y
(Jones 1990)
Parus major
Y
Y
Y
(Järvi & Bakken 1984b) but see (Pöysä 1988; Wilson 1992)
Parus montanus
--Y
(Hogstad & Kroglund 1993)
Poecile atricapilla
-Y
Y
(Mennill et al. 2003)
Junco hyemalis
Y
Y
N
(Balph et al. 1979)
Zonotrichia leucophrys Y
Y
N
(Parsons & Baptista 1980; Fugle et al. 1984a)
Zonotrichia querula
Y
Y
N
(Watt 1986a; Watt 1986b; Jackson et al. 1988)
Fringilla coelebs
Y
--(Marler 1956)
Carduelis spinus
-Y
Y
(Senar et al. 1993d)
Passer domesticus
-Y
Y
(Møller 1987c) but see (Ritchison 1985)
------------------------------------------------------------------------------------------------------------------------------------------------------
3
Table 15.4. Direction of agonistic aggressions related to plumage coloration or dominance status. In some cases the dominance status of the
individuals has been estimated from their sex and/or age, according to the assumption that males dominate females and adults dominate young
birds.
_____________________________________________________________________________________________________________________________________
Direction of aggressions
_____________________________________________________________________________________________________________________________________
Like-vs-like (from dominant to dominant)
From dominant to subordinate
-------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------Parus major
(Järvi & Bakken 1984b; Wilson 1992)
Zonotrichia leucophrys (Fugle & Rothstein 1987; Keys & Rothstein 1991; Slotow et al. 1993b)
Parus atricapillus
(Ficken et al. 1990)
Serinus serinus
(pers.obs.)
Zonotrichia querula
(Rohwer & Ewald 1981)
Loxia leucoptera
(Benkman 1997)
Junco hyemalis
(Balph et al. 1979; Ketterson 1979)
Hesperiphona vespertina (Balph et al. 1979; Fellenberg 1986)
Carpodacus mexicanus (Belthoff & Gowaty 1996)
Carduelis sinica
(Nakamura 1982)
Carduelis chloris
(Flytström 1985)
Carduelis tristis
(Coutlee 1967)
Carduelis spinus
(Senar et al. 1990a; Senar et al. 1990b)
Carduelis flammea
(Dilger 1960)
Passer domesticus
(Møller 1987a; but see Hegner & Wingfield 1987; Solberg & Ringsby 1997; González et al. 2002b)
______________________________________________________________________________________________________________
4
Table 15.5. Studies of delayed plumage maturation and the different hypotheses they seem to support. The method used to test the different
hypotheses is also provided (see text). When available, information on whether data supports DPM as a winter or a spring adaptation is also
provided.
------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------Winter
Spring
----------------------------------------------------Species
CA
FM
C
CA
FM
C
JM
MC
Method
Author
----------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------Falco tinnunculus
Cygnus olor
Passerina cyanea
Passerina leclancherii
Passerina ciris
Passerina amoena
Passerina amoena
Icterus galbula
Icterus galbula
Icterus spurius
Chiroxiphia linearis
Chiroxiphia linearis
Progne subis
Progne subis
Tachycineta bicolor
Tachycineta bicolor
S
S
I
S
Chasiempis sandwichensis I
Pheucticus melanocephalus Pheucticus melanocephalus Setophaga ruticilla
Setophaga ruticilla
Setophaga ruticilla
S
I
S
S
I
-
I
S
I
S
S
I
I
I
I
S
S
S
I
S
S
I
S
S
S
S
S
I
I
5
S
I
I
I
S
I
S
I
I
I
I
S
I
I
I
I
I
I
I
I
I
I
I
I
S
S
S
I
I
I
I
I
S
I
I
I
I
I
I
I
S
I
-
Decoy presentation
Behavioral obs.
Molt phenology
Molt phenology
Molt phenology
Model presentation
Behavioral obs.
Molt phenology
Model presentation
Model presentation
Model presentation
Behavioral obs.
Model presentation
Behavioral obs.
Model presentation
Behavioral obs.
Model presentation
Model presentation
Behavioral obs.
Model presentation
Behavioral obs.
Molt phenology
(Hakkarainen et al. 1993)
(Conover et al. 2000)
(Rohwer 1986)
(Thompson & Leu 1995)
(Thompson 1991)
(Muehter et al. 1997)
(Greene et al. 2000)
(Rohwer & Manning 1990)
(Flood 1984)
(Enstrom 1992)
(McDonald 1993)
(Foster 1987)
(Stutchbury 1991)
(Brown 1984)
(Stutchbury & Robertson 1987)
(Lozano & Handford 1995)
(VanderWerf & Freed 2003)
(Hill 1989)
(Hill 1988; Hill 1994)
(Procter-Gray 1991)
(Procter-Gray & Holmes 1981)
(Rohwer et al. 1983)
Geospiza fortis
Malurus melanocephalus Ficedula hypoleuca
-
(Grant 1990)
(Karubian 2002)
(Slagsvold & Saetre 1991;
Saetre & Slagsvold 1996)
Phoenicurus ochruros
S
I
Behavioral obs.
(Weggler 1997)
Phoenicurus ochruros
I
I
I
I
S
Behavioral obs.
(Landmann & Kollinsky 1995a)
Phoenicurus ochruros
I
I
I
S
Model presentation
(Landmann & Kollinsky 1995b)
Phoenicurus ochruros
I
I
I
Behavioral obs.
(Cuadrado 1995)
Bombycilla cedrorum
S
I
I
Behavioral obs.
(Mountjoy & Robertson 1988)
Carpodacus mexicanus S
Behavioral obs.
(Brown & Brown 1988)
Carduelis spinus
S
I
I
Behavioral obs.
(Senar et al. 1998b)
----------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------------1
2
-
-
S
S
I
I
S
I
-
-
-
Behavioral obs.
Behavioral obs.
Decoy presentation
CA: competitive-ability-signaling hypothesis, FM: female-mimicry hypothesis, C: cryptic hypothesis, JM: juvenile-mimicry hypothesis, MC: molt-constraint hypothesis.
S: the hypothesis is supported; I: available data is inconsistent with the hypothesi
6