Chapter 3. Bird colors as intrasexual signals of aggression and. dominance. Juan Carlos Senar Unidad Asociada CSIC, Museu Ciències Naturals Barcelona

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1 Hill & McGraw 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 125

2 Hill & McGraw 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. 126

3 Hill & McGraw 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 127

4 Hill & McGraw 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 128

5 Hill & McGraw 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). 129

6 Hill & McGraw 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 130

7 Hill & McGraw 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 131

8 Hill & McGraw 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). 132

9 Hill & McGraw 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. 133

10 Hill & McGraw 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 134

11 Hill & McGraw ; 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, 135

12 Hill & McGraw 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 136

13 Hill & McGraw 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 137

14 Hill & McGraw 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 138

15 Hill & McGraw 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 139

16 Hill & McGraw 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. 140

17 Hill & McGraw 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). 141

18 Hill & McGraw 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 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 142

19 Hill & McGraw 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 143

20 Hill & McGraw 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; 144

21 Hill & McGraw 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 145

22 Hill & McGraw 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. 146

23 Hill & McGraw 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 147

24 Hill & McGraw 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 148

25 Hill & McGraw 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 149

26 Hill & McGraw 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- 150

27 Hill & McGraw 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 151

28 Hill & McGraw 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 152

29 Hill & McGraw 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 153

30 Hill & McGraw 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, 154

31 Hill & McGraw 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 155

32 Hill & McGraw 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 This work was supported by research project BOS from the Spanish Research Council, Ministerio de Ciencia y Tecnología. 156

33 Hill & McGraw Literature Cited Alonso-Alvarez, C., C. Doutrelant, and G. Sorci Ultraviolet reflectance affects male-male interactions in the Blue Tit (Parus caeruleus ultramarinus). Behav Ecol 15: Alvarez, F Uso del escudo anal por Gallinula chloropus en situaciones de peligro por predación. Etología 1: Alvarez, F Alertness signalling in two rail species. Anim Behav 46: Andersson, M Sexual selection. Princeton, NJ: Princeton University Press. Andersson, S., and M. Åhlund Hunger affects dominance among strangers in House Sparrows. Anim Behav 41: Armstrong, E. A Social signalling and white plumage. Ibis 113: 534. Austad, S. N Game theory and the evolution of animal contests. Trend Ecol Evol 4: 2-3. Badyaev, A. V., and G. E. Hill Evolution of sexual dichromatism: contribution of carotenoid-versus melanin-based coloration. Biol J Linn Soc 69:

34 Hill & McGraw Balph, M. H., D. F. Balph, and H. C. Romesburg Social status signalling in winter flocking birds: an examination of a current hypothesis. Auk 96: Beauchamp, G Delayed maturation in birds in relation to social foraging and breeding competition. Evol Ecol Res 5: Beauchamp, G. and P. Heeb Social foraging and the evolution of white plumage. Evol Ecol Res 3: Belthoff, J. R., A. M. Dufty Jr., and S. A. Gauthreaux Plumage variation, plasma steroids and social dominance in male House Finches. Condor 96: Belthoff, J. R., and P. A. Gowaty Male plumage coloration affects dominance and aggression in female House Finches. Bird Behav 11: 1-7. Benkman, C. W Feeding behavior, flock-size dynamics, and variation in sexual selection in crossbills. Auk 114: Berglund, A., A. Bisazza, and A. Pilastro Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58: Björklund, M Coming of age in fringillid birds: heterochrony in the ontogeny of secondary sexual characters. J Evol Biol 4: Booth, C. L Evolutionary significance of ontogenetic colour change in animals. Biol J Linn Soc 40:

35 Hill & McGraw Bradbury, J. W. and N. B. Davies Relative roles of intra- and intersexual selection. In Bradbury, J. W. and M. B. Andersson eds., Sexual selection: testing the alternatives, Wiley: Chichester, U.K. Breiehagen, T., and G. P. Saetre Territorial defence and plumage colour in Pied Flycatchers Ficedula hypoleuca. Anim Behav 44: Brooke, M. D. L Ecological factors influencing the occurrence of 'flash marks' in wading birds. Funct Ecol 12: Brotons, L Status signalling in the Coal Tit (Parus ater): the role of previous knowledge of individuals. Etología 6: Brown, C. R Light-breasted Purple Martins dominate dark-breasted birds in a roost: implications for female mimicry. Auk 101: Brown, M. B.. and C. R. Brown Access to winter food resources by bright- versus dull-colored House Finches. Condor 90: Bryant, D. M., and A. V. Newton Metabolic costs of dominance in dippers, Cinclus cinclus. Anim Behav 48: Buchanan, K. L., M. R. Evans, and A. R. Goldsmith Testosterone, dominance signalling and immunosuppression in the House Sparrow, Passer domesticus. Behav Ecol Sociobiol 55:

36 Hill & McGraw Buchanan, K. L., M. R. Evans, A. R. Goldsmith, D. M. Bryant, and L. V. Rowe Testosterone influences basal metabolic rate in male House Sparrows: a new cost of dominance signalling? Proc R Soc Lond B 268: Caryl, P. G Telling the truth about intentions. J theor Biol 97: Chu, P. C Historical examination of delayed plumage maturation in the shorebirds (Aves: Charadriiformes). Evolution 48: Collis, K., and G. Borgia Age-related effects of testosterone, plumage, and experience on aggression and social dominance in juvenile male Satin Bowerbirds (Ptilonorhynchus violaceus). Auk 109: Conover, M. R., J. G. Reese, and A. D. Brown Costs and benefits of subadult plumage in mute swans: testing hypothesis for the evolution of delayed plumage maturation. Am Nat 156: Coutlee, E. L Agonistic behavior in the American Goldfinch. Wilson Bull 79: Cristol, D. A. 1995a. Costs of switching social groups for dominant and subordinate Dark-eyed Juncos (Junco hyemalis). Behav Ecol Sociobiol 37: Cristol, D. A. 1995b. The coat-tail effect in merged flocks of Dark-eyed Juncos: social status depends on familiarity. Anim Behav 50: Cuadrado, M Female-like plumage does not reduce aggression from adult male Black Redstarts Phoenicurus ochrurus in winter. Ardea 83:

37 Hill & McGraw Darwin, C The descent of man and selection in relation to sex. London: John Murray. de Vries, T Prey selection and hunting methods of the Galápagos Hawk, Buteo galapagoensis. Gerfaut 66: Dilger, W. C Agonistic and social behavior of captive Redpolls. Wilson Bull 72: Eckert, C. G., and P. J. Weatherhead. 1987a. Competition for territories in red-winged blackbirds: Is resource-holding potential realized? Behav Ecol Sociobiol 20: Eckert, C. G., and P. J. Weatherhead. 1987b. Ideal dominance distributions: a test using red-winged blackbirds (Agelaius phoeniceus). Behav Ecol Sociobiol 20: Ekman, J. B Ecology on non-breeding social systems of Parus. Wilson Bull 101: Emlen, D. J Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Behav Ecol Sociobiol 41: Ens, B. J., and J. D. Goss-Custard Piping as a display of dominance by wintering Oystercatchers Haematopus ostralegus. Ibis 128:

38 Hill & McGraw Enstrom, D. A Breeding season communications hypotheses for delayed plumage maturation in passerines: tests in the Orchard Oriole, Icterus spurius. Anim Behav 43: Evans, M. R., A. R. Goldsmith, and R. A. Norris. 2000a. The effects of testosterone on antibody production and plumage coloration in male House Sparrows (Passer domesticus). Behav Ecol Sociobiol 47: Evans, M. R., and B. J. Hatchwell An experimental study of male adornment in the Scarlet-tufted Malachite Sunbird: I. The role of pectoral tufts in territorial defense. Behav Ecol Sociobiol 29: Fellenberg, W Die Invasion des Fichtenkreuzschnabels (Loxia curvirostra) 1983 in Westfalen und die weitere Bestandsentwicklung bis Ende Charadrius 22: Ficken, M. S., C. M. Weise, and J. W. Popp Dominance rank and resource access in winter flocks of Black-capped Chickadees. Wilson Bull 102: Figuerola, J., and J. C. Senar. 2000b. Measurement of plumage badges: an evaluation of methods used in the Great Tit Parus major. Ibis 142: Fitze, P. S., and H. Richner Differential effects of a parasite on ornamental structures based on melanins and carotenoids. Behav Ecol 13: Flood, N The adaptive significance of delayed plumage maturation in male Northern Orioles. Evolution 32:

39 Hill & McGraw Flytström, I Plumage variability and social rank in Greenfinch flocks. Honours thesis: University of Göteborg, Sweden. Folstad, I., and A. J. Karter Parasites, bright males, and the immunocompetence handicap. Am Nat 139: Foster, M. S Delayed maturation, neoteny, and social system differences in two Manakins of the genus Chiroxiphia. Evolution 41: Fugle, G. N., and S. I. Rothstein Experiments on the control of deceptive signals of status in White-crowned Sparrows. Auk 104: Fugle, G. N., S. I. Rothstein, C. W. Osenberg, and M. A. McGinley. 1984a. Signals of status in wintering White-crowned Sparrows, Zonotrichia leucophrys gambelii. Anim Behav 32: Gadgil, M Male dimorphism as a consequence of sexual selection. Am Nat 106: Geist, V The evolutionary significance of mountain sheep horns. Evolution 20: González, G., G. Sorci, and L. C. Smith Testosterone and sexual signalling in male House Sparrows (Passer domesticus). Behav Ecol Sociobiol 50: González, G., G. Sorci, L. C. Smith, and F. De Lope. 2002b. Social control and physiological cost of cheating in status signalling male House Sparrows (Passer domesticus). Ethology 108:

40 Hill & McGraw Gosler, A. G The Great Tit. London: Hamlyn. Götmark, F Bright plumage in the magpie: does it increase or reduce the risk of predation? Behav Ecol Sociobiol 40: Götmark, F., and A. Hohlfält Bright male plumage and predation risk in passerine birds: are males easier to detect than females? Oikos 74: Götmark, F., P. Post, J. Olsson and D. Himmelmann Natural selection and sexual dimorphism: sex-biased sparrowhawk predation favours crypsis in female chaffinches. Oikos 80: Götmark, F., and U. Unger Are conspicuous birds unprofitable prey? Field experiments with Hawks and stuffed prey species. Auk 111: Grafen, A Biological signals as handicaps. J theor Biol 144: Grant, B. R The significance of subadult plumage in Darwin's Finches, Geospiza fortis. Behav Ecol 1: Grasso, M. J., U. M. Savalli, and R. L. Mumme Status signalling in Dark-eyed Juncos: perceived status of other birds affects dominance interactions. Condor 98: Greene, E., B. E. Lyon, V. R. Muehter, L. Ratcliffe, S. J. Oliver, and P. T. Boag Disruptive sexual selection for plumage coloration in a passerine bird. Nature 407:

41 Hill & McGraw Gross, M. R Alternative reproductive strategies and tactics: diversity within sexes. Trend Ecol Evol 11: Hagelin, J. C The kinds of traits involved in male-male competition: comparison of plumage, behavior, and body size in quail. Behav Ecol 13: Hakkarainen, H., E. Korpimäki, E. Huhta, and P. Palokangas Delayed maturation in plumage colour: evidence for the female-mimicry hypothesis in the kestrel. Behav Ecol Sociobiol 33: Hammerstein, P The role of asymmetries in animal contests. Anim Behav 29: Hasselquist, D., J. A. Marsh, P. W. Sherman, and J. C. Wingfield Is avian humoral immunocompetence supressed by testosterone? Behav Ecol Sociobiol 45: Hegner, R. E., and J. C. Wingfield Social status and circulating levels of hormones in flocks of House Sparrows (Passer domesticus). Ethology 76: Hill, G. E The function of delayed plumage maturation in male Black-headed Grosbeaks. Auk 105: Hill, G. E Late spring arrival and dull plumage: aggression avoidance by yearling males? Anim Behav 37: Hill, G. E Testis mass and subadult plumage in Black-Headed Grosbeaks. Condor 96:

42 Hill & McGraw Hill, G. E Subadult plumage in the House Finch and tests of models for the evolution of delayed plumage maturation. Auk 113: Hill, G. E Environmental regulation of ornamental coloration in birds. In G. E. Hill and K. J. McGraw, eds. Bird Coloration, Volume 1: Mechanisms and Measurements. Cambridge Mass: Harvard University Press. Hill, G. E. and W. R. Brawner Melanin-based plumage coloration in the House Finch in unafected by coccidial infection. Proc R Soc Lond B 265: Hill, G. E. and K. J. McGraw Bird Coloration, Volume 1: Mechanisms and Measurements. Cambridge Mass: Harvard University Press. Hinde, R. A Behaviour. In Marshall, A. J. ed., Biology and comparative physiology of birds, Academic Press: London. Hogstad, O It is expensive to be dominant. Auk 104: Hogstad, O Social organization and dominance behavior in some Parus species. Wilson Bull 254: 262. Hogstad, O., and R. T. Kroglund The throat badge as a status signal in juvenile male Willow Tits Parus montanus. J Orn 134: Holberton, R. L., K. P. Able, and J. C. Wingfield Status signalling in Dark-eyed Juncos, Junco hyemalis: plumage manipulations and hormonal correlates of dominance. Anim Behav 37: Hughes, A. L Picking winners in animal contests. Trend Ecol Evol 1:

43 Hill & McGraw Jablonski, P. G., and P. Matyjasiak Male wing-patch asymmetry and aggressive response to intruders in the Common Chaffinch (Fringilla coelebs). Auk 119: Jackson, W. M., S. A. Rohwer, and R. L. Winnegrad Status signaling is absent within age-and-sex classes of Harris' Sparrows. Auk 105: Jawor, J. M., and R. Breitwisch Melanin ornaments, honesty, and sexual selection. Auk 120: Järvi, T., and M. Bakken. 1984b. The function of the variation in the breast stripe of the Great Tit (Parus major). Anim Behav 32: Järvi, T., O. Walso, and M. Bakken. 1987b. Status signalling by Parus major: an experiment in deception. Ethology 76: Jenni, L., and R. Winkler Moult and ageing of European Passerines. London: Academic Press. Johnstone, R. A Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol Rev 70: Johnstone, R. A., and K. J. Norris Badges of status and the cost of aggression. Behav Ecol Sociobiol 32: Jones, I. L Plumage variability functions for status signalling in least auklets. Anim Behav 39:

44 Hill & McGraw Jones, I. L., and F. M. Hunter Experimental evidence for mutual inter- and intrasexual selection favouring a crested auklet ornament. Anim Behav 57: Karubian, J Costs and benefits of variable breeding plumage in the Red-backed Fairy-wren. Evolution 56: Ketterson, E. D Status signaling in Dark-eyed Juncos. Auk 96: Keys, G. C., and S. I. Rothstein Benefits and costs of dominance and subordinance in White-crowned Sparrows and the paradox of status signalling. Anim Behav 42: Keyser, A. J., and G. E. Hill Structurally based plumage coloration is an honest signal of quality in male Blue Grosbeaks. Behav Ecol 10: Krebs, J. R., and N. B. Davies An introduction to behavioural ecology. Oxford: Blackwell Scientific Publications. Kushlan, J. A The significance of plumage colour in the formation of feeding aggregations of ciconiiforms. Ibis 119: Lachmann, M., S. Számado, and C. T. Bergstrom Cost and conflict in animal signals and human language. Proc Natl Acad Sci USA 98: Lack, D The natural regulation of animal numbers. Oxford: Clarendon. Lack, D Ecological adaptations for breeding in birds. London: Methuen. 168

45 Hill & McGraw Landmann, A., and C. Kollinsky. 1995a. Age and plumage related territory differences in male Black Redstarts: The (non)-adaptive significance of delayed plumage maturation. Ethol Ecol Evol 7: Landmann, A., and C. Kollinsky. 1995b. Territory defence in Black Redstarts, Phoenicurus ochruros: Effects of intruder and owner age? Ethology 101: Lank, D. B., C. M. Smith, O. Hanotte, T. Burke, and F. Cooke Genetic polymorphism for alternative mating behaviour in lekking male Ruff Philomachus pugnax. Nature 378: Lawton, M. F., and R. O. Lawton Heterochrony, deferred breeding, and avian sociality. Curr Ornithol 3: Leimar, O., and M. Enquist Effect of asymmetries in owner-intruder conflicts. J theor Biol 111: Lemel, J., and K. Wallin. 1993a. Status signalling, motivational condition and dominance: an experimental study in the Great Tit, Parus major L. Anim Behav 45: Lendvai, A. Z., J. Kis, T. Szekely, and I. C. Cuthill An investigation of mate choice based on manipulation of multiple ornaments in Kentish Plovers. Anim Behav 67:

46 Hill & McGraw Lewis, D. M Importance of face mask in sexual recognition and territorial behavior in the Yellowthroat. Jack-Pine Warbler 50: Liker, A., and Z. Barta Male badge size predicts dominance againsts females in House Sparrows. Condor 103: Lima, S. L., and L. M. Dill Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68: Lozano, G. A., and P. T. Handford A test of an assumption of delayed plumage maturation hypothesis using female Tree Swallows. Wilson Bull 107: Lyon, B. E., and R. D. Montgomerie Delayed plumage maturation in passerine birds: reliable signaling by subordinate males? Evolution 40: Marchetti, K The evolution of multiple male traits in the Yellow-browed Leaf Warbler. Anim Behav 55: Marler, P Studies of fighting in Chaffinches. (2) the effect on dominance relations of disguising females as males. Brit J Anim Behav 3: Marler, P Studies of fighting in Chaffinches. (3) Proximity as a cause of aggression. Brit J Anim Behav 4: Mateos, C., and J. Carranza The role of bright plumage in male-male interactions in the ring-necked pheasant. Anim Behav 54:

47 Hill & McGraw Maynard Smith, J. 1982a. Do animals convey information about their intentions? J theor Biol 97: 1-5. Maynard Smith, J. 1982b. Evolution and the theory of games. Cambridge: Cambridge Univ. Press. Maynard Smith, J., and D. Harper Animal signals. Oxford: Oxford Univ. Press. Maynard Smith, J., and D. G. C. Harper The evolution of aggression: can selection generate variability? Phil Trans R Soc Lond B 319: McDonald, D. B Delayed plumage maturation and orderly queues for status: a manakin mannequin experiment. Ethology 94: McGraw, K. J. 2003a. Melanins, metals, and mate quality. Oikos 102: McGraw, K. J., J. Dale, and E. A. Mackillop. 2003b. Social environment during molt and the expression of melanin-based plumage pigmentation in male House Sparrows (Passer domesticus). Behav Ecol Sociobiol 53: McGraw, K. J., and G. E. Hill. 2000a. Carotenoid-based ornamentation and status signaling in the House Finch. Behav Ecol 11: McGraw, K. J., and G. E. Hill. 2000b. Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B 267:

48 Hill & McGraw McGraw, K. J., and G. E. Hill. 2000c. Plumage brightness and breeding-season dominance in the House Finch: a negatively correlated handicap? Condor 102: Mennill, D. J., S. M. Doucet, R. Montgomerie, and L. M. Ratcliffe Achromatic color variation in Black-capped Chickadees, Poecile atricapilla: black and white signals of sex and rank. Behav Ecol Sociobiol 53: Moczek, A. P., and D. J. Emlen Male horn dimorphism in the scarab beetle, Onthophagus taurus: do alternative reproductive tactics favour alternative phenotypes? Anim Behav 59: Montgomerie, R. D., and B. E. Lyon Does longevity influence the evolution of delayed plumage maturation in passerine birds? Am Nat 128: Moran, N. A The evolutionary maintenance of alternative phenotypes. Am Nat 139: Moreno-Rueda, G The capacity to escape from predators in Passer domesticus: an experimental study. J Orn 144: Mountjoy, D. J., and R. J. Robertson Why are Waxwings "waxy"? Delayed plumage maturation in the Cedar Waxwing. Auk 105: Møller, A. P. 1987a. Social control of deception among status signalling House sparrows Passer domesticus. Behav Ecol Sociobiol 20:

49 Hill & McGraw Møller, A. P. 1987b. Variation in badge size in male House Sparrows Passer domesticus: evidence for status signalling. Anim Behav 35: Møller, A. P Natural and sexual selection on a plumage signal of status and on morphology in House Sparrows, Passer domesticus. J Evol Biol 2: Møller, A. P Sexual behaviour is related to badge size in the House Sparrow Passer domesticus. Behav Ecol Sociobiol 27: Muehter, V. R., E. Greene, and L. Ratcliffe Delayed plumage maturation in Lazuli Buntings: tests of the female mimicry and status signalling hypotheses. Behav Ecol Sociobiol 41: Nakamura, H Pair-formation and territory establishment of the Oriental Greenfinch Carduelis sinica in autumn (Aves: Fringillidae). Physiol Ecol Japan 19: Oberski, I. M., and J. D. Wilson Territoriality and site-related dominance: on two related concepts in avian social organization. Ethology 87: Owens, I. P. F., and I. R. Hartley "Trojan sparrows": evolutionary consequences of dishonest invasion for the badges-of-status model. Am Nat 138: Parsons, J., and L. F. Baptista Crown coloration and dominance in the Whitecrowned Sparrow. Auk 97: Payne, R. B Ecological consequences of song matching: breeding success and intraspecific song mimicry in Indigo Buntings. Ecology 63:

50 Hill & McGraw Pärt, T., and A. Qvarnström Badge size in Collared Flycatchers predicts outcome of male competition over territories. Anim Behav 54: Peek, F. W An experimental study of the territorial function of vocal and visual displays in the male Red-winged Blackbird (Agelaius phoeniceus). Anim Behav 20: Peters, A., L. B. Astheimer, C. R. J. Boland, and A. Cockburn Testosterone is involved in acquisition and maintenance of sexually selected male plumage in Superb Fairy-wrens, Malurus cyaneus. Behav Ecol Sociobiol 47: Poiani, A., A. R. Goldsmith, and M. R. Evans Ectoparasites of House Sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis and a new model. Behav Ecol Sociobiol 47: Popp, J. W Resource value and dominance among American goldfinches. Bird Behav 7: Pöysä, H Feeding consequences of the dominance status in Great Tit Parus major groups. Ornis Fenn 65: Price, T. D Sexual selection on body size, territory and plumage variables in a population of Darwin's finches. Evolution 38: Procter-Gray, E Female-like plumage of subadult male American Redstarts does not reduce aggression from other males. Auk 108:

51 Hill & McGraw Procter-Gray, E., and R. T. Holmes Adaptive significance of delayed attainment of plumage in male American Redstarts: tests of two hypotheses. Evolution 35: Pryke, S. R., and S. Andersson Carotenoid-based status signalling in Redshouldered Widowbirds (Euplectes axillaris): epaulet size and redness affect captive and territorial competition. Behav Ecol Sociobiol 53: Pryke, S. R., S. Andersson, M. J. Lawes, and S. E. Piper. 2002a. Carotenoid status signaling in captive and wild Red-collared Widowbirds: independent effects of badge size and color. Behav Ecol 13: Pryke, S. R., M. J. Lawes, and S. Andersson Agonistic carotenoid signalling in male red-collared widowbirds: aggression related to the colour signal of both the territory owner and model intruder. Anim Behav 62: Pulliam, H. R., and T. Caraco Living in groups: is there an optimal group size? In Krebs, J. R. and N. B. Davies eds., Behavioural ecology. An evolutionary approach, Blackwell Scientific Publications: Oxford. Pulliam, H. R., and G. C. Millikan Social organization in the nonreproductive season. In Farner, D. S., J. R. King and K. C. Parkes eds., Avian Biology. Vol. 6, Academic Press: New York. Qvarnström, A Different reproductive tactics in male Collared Flycatchers signalled by size of secondary sexual character. Proc R Soc Lond B 266:

52 Hill & McGraw Qvarnström, A., and E. Forsgren Should females prefer dominant males? Trend Ecol Evol 13: Ralph, C. J., and C. A. Pearson Correlation of age, size of territory, plumage and breeding success in White-crowned Sparrows. Condor 73: Reinertsen, R. E., and O. Hogstad Influence of social status on the nocturnal energy expenditure of the Willow Tit Parus montanus. Fauna norv Ser C, Cinclus 17: Reyer, H. U., W. Fischer, and P. Steck Sex-specific nest defense in House Sparrows (Passer domesticus) varies with badge size of males. Behav Ecol Sociobiol 42: Rhijn, J. G. V Communication by agonistic displays: a discussion. Behaviour 74: Rhijn, J. G. V., and R. Vodegel Being honest about one's intentions: an evolutionary stable strategy for animal conflicts. J theor Biol 85: Ripoll, J., J. Saldaña, and J. C. Senar Evolutionary stable transition rates in a stage-structured model. An application to the analysis of size distributions of badges of social status. Math Biosci 190: Ritchison, G Plumage variability and social status in captive male House Sparrows. Kentucky Warbler 61:

53 Hill & McGraw Rohwer, S. 1978a. Passerine subadult plumages and the deceptive acquisition of resources: Test of a critical assumption. Condor 80: Rohwer, S., and D. M. Niles The subadult plumage of Purple Martins: variability, female mimicry and recent evolution. Z Tierpsychol 51: Rohwer, S. A The social significance of avian winter plumage variability. Evolution 29: Rohwer, S. A Status signaling in Harris Sparrows: some experiments in deception. Behaviour 61: Rohwer, S. A. 1978b. Reply to Shields on avian winter plumage variability. Evolution 32: Rohwer, S. A The evolution of reliable and unreliable badges of fighting ability. Am Zool 22: Rohwer, S. A Testing the female mimicry hypothesis of delayed plumage maturation: a comment on Procter-Gray and Holmes. Evolution 37: Rohwer, S. A Dyed birds achieve higher social status than controls in Harris' Sparrows. Anim Behav 33: Rohwer, S. A A previously unknown plumage of first-year Indigo Buntings and theories of delayed plumage maturation. Auk 103:

54 Hill & McGraw Rohwer, S. A., and G. S. Butcher Winter versus summer explanations of delayed plumage maturation in temperate passerine birds. Am Nat 131: Rohwer, S. A., and P. W. Ewald The cost of dominance and advantage of subordination in a badge signaling system. Evolution 35: Rohwer, S. A., S. D. Fretwell, and D. M. Niles Delayed maturation in passerine plumages and the deceptive acquisition of resources. Am Nat 115: Rohwer, S. A., W. P. Klein, and S. Herad Delayed plumage maturation and the presumed prealternate molt in American Redstarts. Wilson Bull 95: Rohwer, S. A., and J. Manning Differences in timing and number of molts for Baltimore and Bullock's Orioles: implications to hybrid fitness and theories of delayed plumage maturation. Condor 92: Rohwer, S. A., and F. C. Rohwer Status signalling in Harris Sparrows: experimental deceptions achieved. Anim Behav 26: Rohwer, S. A., and E. Roskaft Results of dyeing male Yellow-headed Blackbirds solid black: implications for the arbitrary identity badge hypothesis. Behav Ecol Sociobiol 25: Roper, T. J Badges of status in avian societies. New Sci 109: Roskaft, E., T. Järvi, M. Bakken, C. Bech, and R. E. Reinertsen The relationship between social status and resting metabolic rate in Great Tits (Parus major) and Pied Flycatchers (Ficedula hypoleuca). Anim Behav 34:

55 Hill & McGraw Roskaft, E., and S. Rohwer An experimental study of the function of the red epaulettes and the black body colour of the male red-winged blackbirds. Anim Behav 35: Ryan, P. G., R. P. Wilson, and J. Cooper Intraspecific mimicry and status signals in juvenile African penguins. Behav Ecol Sociobiol 20: Saetre, G. P., and T. Slagsvold The significance of female mimicry in male contests. Am Nat 147: Savalli, U. M The evolution of bird coloration and plumage elaboration. A review of hypotheses. Curr Ornithol 12: Selander, R. K On mating systems and sexual selection. Am Nat 99: Selander, R. K Sexual selection and dimorphism in birds. In Campbell, B. G. ed., Sexual selection and the descent of man, Aldine: Chicago. Semple, S. and K. Mccomb Behavioural deception. Trends Ecol Evol 11: Senar, J. C Agonistic communication in social species: what is communicated? Behaviour 112: Senar, J. C Vivir y convivir: la vida en grupos sociales. In Carranza, J. ed., Etología: Introducción a la ciéncia del comportamiento, Univ. of Extremadura: Cáceres. 179

56 Hill & McGraw Senar, J. C Plumage coloration as a signal of social status. In Adams, N. and R. Slotow eds., Proc. 22 Int. Ornithol. Congr., Durban, BirdLife South Africa: Johannesburg. Senar, J. C Mucho más que plumas. Monografies del Museu de Ciències Naturals, vol. 2: Barcelona. Senar, J. C., and A. Borras Sobrevivir al invierno: estratégias de las aves invernantes en la Península Ibérica. Ardeola 51: Senar, J. C., P. J. K. Burton, and N. B. Metcalfe Variation in the nomadic tendency of a wintering finch Carduelis spinus and its relationship with body condition. Ornis Scand 23: Senar, J. C., and M. Camerino. 1998a. Status signalling and the ability to recognize dominants: an experiment with siskins (Carduelis spinus). Proc R Soc Lond B 265: Senar, J. C., M. Camerino, J. L. Copete, and N. B. Metcalfe. 1993d. Variation in black bib of the Eurasian Siskin (Carduelis spinus) and its role as a reliable badge of dominance. Auk 110: Senar, J. C., M. Camerino, and N. B. Metcalfe Agonistic interactions in siskin flocks: why are dominants sometimes subordinate? Behav Ecol Sociobiol 25:

57 Hill & McGraw Senar, J. C., M. Camerino, and N. B. Metcalfe. 1990a. Familiarity breeds tolerance: the development of social stability in flocking Siskins (Carduelis spinus). Ethology 85: Senar, J. C., M. Camerino, and N. B. Metcalfe A comparison of agonistic behaviour in two Cardueline finches: feudal species are more tolerant than despotic ones. Etología 5: Senar, J. C., J. L. Copete, and A. J. Martin. 1998b. Behavioural and morphological correlates of variation in the extent of postjuvenile moult in the Siskin Carduelis spinus. Ibis 140: Senar, J. C., J. L. Copete, and N. B. Metcalfe. 1990b. Dominance relationships between resident and transient wintering Siskins. Ornis Scand 21: Senar, J. C., J. Domènech, and M. Camerino Female Siskins choose mate by the size of the yellow wing stripe. Behav Ecol Sociobiol (in press). Senar, J. C., and D. Escobar Carotenoid derived plumage coloration in the siskin Carduelis spinus is related to foraging ability. Avian Sci 2: Senar, J. C., J. Figuerola, and J. Domènech Plumage coloration and nutritional condition in the Great Tit Parus major: the roles of carotenoids and melanins differ. Naturwiss 90:

58 Hill & McGraw Senar, J. C., V. Polo, F. Uribe, and M. Camerino Status signalling, metabolic rate and body mass in the siskin: the cost of being a subordinate. Anim Behav 59: Shields, W. M The social significance of avian winter plumage variability: a comment. Evolution 31: Simmons, L. W., J. L. Tomkins, and J. Hunt Sperm competition games played by dimorphic male beetles. Proc R Soc Lond B 266: Sinervo, B., and C. M. Lively The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380: Slagsvold, T Sex recognition and breast stripe size in Great Tits. Ardea 81: Slagsvold, T., S. Dale, and A. Kruszewicz Predation favours cryptic coloration in breeding male Pied Flycatchers. Anim Behav 50: Slagsvold, T., and G. P. Saetre Evolution of plumage color in male Pied Flycatchers (Ficedula hypoleuca): evidence for female mimicry. Evolution 45: Slotow, R., J. Alcock, and S. I. Rothstein. 1993b. Social status signalling in Whitecrowned Sparrows: an experimental test of the social control hypothesis. Anim Behav 46: Smith, D. G The role of the epaulets in the Red-winged Blackbird (Agelaius phoeniceus) social system. Behaviour 41:

59 Hill & McGraw Smith, R. D Age determination, wing-feather colour and wing-length change in Snow Buntings Plectrophenax nivalis. Ringing and Migration 13: Solberg, E. J., and T. H. Ringsby Does male badge size signal status in small island populations of House Sparrows, Passer domesticus? Ethology 103: Studd, M. V., and R. J. Robertson. 1985b. Evidence for reliable badges of status in territorial Yellow Warblers (Dendroica petechia). Anim Behav 33: Studd, M. V., and R. J. Robertson. 1985a. Life span, competition, and delayed plumage maturation in male passerines: the breeding threshold hypothesis. Am Nat 126: Studd, M. V., and R. J. Robertson. 1985c. Sexual selection and variation in reproductive strategy in male Yellow Warblers (Dendroica petechia). Behav Ecol Sociobiol 17: Studd, M. V., and R. J. Robertson Differential allocation of reproductive effort to territorial establishment and maintenance by male Yellow Warblers (Dendroica petechia). Behav Ecol Sociobiol 23: Stutchbury, B. J The adaptive significance of male subadult plumage in Purple Martins: plumage dyeing experiments. Behav Ecol Sociobiol 29:

60 Hill & McGraw Stutchbury, B. J., and R. J. Robertson Signaling subordinate and female status: two hypothesis for the adaptive significance of subadult plumage in female Tree Swallows. Auk 104: Számado, S Cheating as a mixed strategy in a simple model of aggressive communication. Anim Behav 59: Tanaka, Y Social selection and the evolution of animal signals. Evolution 50: Thompson, C. W The sequence of molts and plumages in Painted Buntings and implications for theories of delayed plumage maturation. Condor 93: Thompson, C. W., and M. Leu Molts and plumages of Orange-breasted Buntings (Passerina leclancherii): Implications for theories of delayed plumage maturation. Auk 112: Tuttle, E. M Alternative reproductive strategies in the White-throated Sparrow: behavioral and genetic evidence. Behav Ecol 14: Vaclav, R., and H. Hoi Different reproductive tactics in House Sparrows signalled by badge size: Is there a benefit to being average? Ethology 108: VanderWerf, E. A., and L. A. Freed 'Elepaio subadult plumages reduce aggression through graded status-signaling, not mimicry. J Field Ornithol 74: Veiga, J. P. 1993c. Badge size, phenotypic quality, and reproductive success in the House Sparrow: a study on honest advertisement. Evolution 47:

61 Hill & McGraw Verhulst, S., S. L. Dieleman, and H. K. Parmentier A tradeoff between immunocompetence and sexual ornamentation in domestic fowl. Proc Natl Acad Sci USA 96: Watt, D. J. 1986a. A comparative study of status signalling in sparrows (genus Zonotrichia). Anim Behav 34: Watt, D. J. 1986b. Relationship of plumage variability, size and sex to social dominance in Harris' Sparrows. Anim Behav 34: Weggler, M. B Age-related reproductive success and the function of delayed plumage maturation in male Black Redstarts Phoenicurus ochruros. Ph.D. diss., Universität Zürich. West Eberhard, M. J The evolution of social behaviour by kin selection. Q Rev Biol 50: Whitfield, D. P Plumage variability and territoriality in breeding turnstone Arenaria interpres: status signalling or individual recognition? Anim Behav 34: Whitfield, D. P. 1987a. Plumage variability, status signalling and individual recognition in avian flocks. Trend Ecol Evol 2: Wiley, R. H Prior-residency and coat-tail effects in dominance relationships of male Dark-eyed Juncos Junco hyemalis. Anim Behav 40:

62 Hill & McGraw Wilson, J. D A re-assessment of the significance of status signalling in populations of wild Great Tits, Parus major. Anim Behav 43: Wingfield, J. C., G. F. Ball, A. M. Jr. Dufty, R. E. Hegner, and M. Ramenofsky Testosterone and aggression in birds. Am Sci 75: Wolf, J. B., E. D. Brodie III, and A. J. Moore Interacting phenotypes and the evolutionary process.ii.selection resulting from social interactions. Am Nat 153: Wolfenbarger, L. L. 1999b. Is red coloration of male Northern Cardinals beneficial during the nonbreeding season?: a test of status signaling. Condor 101: Wolfenbarger, L. L. 1999a. Red coloration of male northern cardinals correlates with mate quality and territory quality. Behav Ecol 10: Yezerinac, S. M., and P. J. Weatherhead Extra-pair mating, male plumage coloration and sexual selection in Yellow Warblers (Dendroica petechia). Proc R Soc Lond B 264:

63 Hill & McGraw 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 =! ) is a transition matrix with 0 "! 1 and " = 1 for all j, S = s ) is a ( ij! ij survival matrix with s = 0 for i! j, and s s > 0 ( i = 1, K, n ), and F = f ) is a ij ii = i fertility matrix such that f = 0 for all i! 2 (we assume that all the newborns belong to ij 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 ( s i ) 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!, the probability that an i-class individual suffers an aggressive encounter from a j-class individual per time interval ( 0 "! 1), regardless of the result of each encounter. These probabilities! ij 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 n! i= 1 ij ij ( ij ( ij 187

64 Hill & McGraw 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 s i and f i are strictly decreasing functions of! i (t), the i-th component of 0!(t). In particular, for each class, we assume that s (! ) = s F ( ( t)) and i i i i! i f (! ) = f F ( ( t)) with s f > 1 and F! 0 as # "!. These hypotheses i i i i! i i + i * guarantee the existence of a positive equilibrium N of the model THAT is locally stable 0 0 for, at least, values of s i + f i > 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 R 0 (!, N ) as a fitness measure, are those values equilibrium * N such that * * s (! ) f (! ) = 1 for i = 1, K, n, i i + i i i i ess! of! that render an * * ess where " i = " i ( N (! )). Note that these equalities says that, at the equilibrium ess determined by!, 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 the sense that, in a resident equilibrium population adopting ess! is evolutionary neutral in ess!, any mutant population mut mut * ess with a different strategy! will be also at equilibrium, i.e., that R (! ; N (! )) 1 mut for all![ 0,1] maximum at 0 = * ess ". That is, the function! " R (!, N (! )) does not have a strict 0 ess! =!. However, using a 2x2 matrix model, it is easy to show that a ess necessary condition for! 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

65 Hill & McGraw & 1' ) 1 ) 2 # & ( 1 1' ( 1 # T = $, =, 1 1! W $ 2 1! % ) ') " % ' ( 2 ( 2 " with 0 #,! 1 ( i =1,2). In order to have a unique equilibrium N = W C defined by! i " i 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"! )(1 " ). The simplest way to check the necessity 1 2 ( 1! 2 ess of this sort of aggression for the convergence stability of! is by computing the fitness gradient " R / "!, " R / " ) at the boundary of trait space! given by ( 0 1 0! 2 ( 0, 2 ) : 0! " 2! 1 0 /! 1 > ( < ) 0 1 +! 2 > ( < ) ( 0, 2 ): 0!" 2! ess { } ". Then it follows that, at any point of this boundary,! R!" 0 and 0 / 2 =! R " when! 1. That is, only when! +! 1, TSSs escape 1 2 > from the boundary { 1} convergence of TSSs towards a! since such an strategy never has the form (, ) any 0! " 2! 1. ", which is a necessary condition for the 0! for 2 189

66 Hill & McGraw 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 s i (! i ) + fi (! i ) = 1, it immediately follows that the equilibrium is given by * ess! 1 N (" ) = W C with C a constant vector with components c i = F! i (1/( si + f i )). 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 F i (! ) = F(!) for i = 1,2, 3, it immediately follows that N < is equivalent to 2 N 3 c 3 > c 2 as long as! > 1 0 and! 1 2 +! 3 > (i.e., under like-vs-like aggression), which implies that the sum of potential survival and fertility rates of dominant individuals ( s + ) has to be higher than that of subdominats ( s + ). On the other hand, the 3 f 3 second condition for bimodality, namely, * * 1 N 2 2 f 2 N >, is satisfied for a wide range of values 0 0 * ess of s i, f i, and! i for any N (! ) > 0 as long as the probability of aggressive encounters among subordinates,! 1, is small enough (for details see Ripoll et al., 2004). 190

67 Hill & McGraw Fig 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 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 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 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 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

68 Hill & McGraw 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 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 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

69 Hill & McGraw Fig 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, Great Tit (Järvi & Bakken 1984b); bib size measured according to Figuerola and Senar (2000b); Shapiro Wilk W= 0.99, p = 0.18, N=160, 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, Based on Ripoll et al. (2004). 193

70 100 adult young Dominance score r = 0.71 p < Bib size (mm 2 ) Figure 15-1 Senar

71 experimental manipulation (n = 7) sham control (n = 7) Proportion of wins by original dominant Before treatment After treatment Figure 15-2 Senar

72 Mean territory size (ha) Mean encounter rate (min -1 ) enlarged red reduced orange control Figure 10-3 Senar

73 Test bird s tie width: > dummy s > dummy s 10 Number of trials Closest approach to dummy (cm) aggressive submissive Behavior Figure 15-4 Senar

74 releasing cage food food? left test cage one-way window perch right test cage 100 Expt 1 (n = 25) Expt 2 (n = 20) 50 NS NS 0 Empty A Empty B Small bib Small bib Mean percent of time Expt 3 (n = 24) p < 0.05 Empty Female Expt 4 (n = 25) p < 0.05 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

75 1.0 control badge increased Proportion of fights won before after Badge manipulation Figure 15-7 Senar

76 200 Change in bib area (mm 2 ) intact castrated + empty implant high low testosterone Figure 15-8 Senar

77 20 House Sparrow Number of individuals Great Tit 600 Siskin Bib size (mm 2 ) Figure 15-9 Senar