Blue as indicator of quality
The purity of an individual's colour is often a product of several factors including the ability to sequester pigments from the environment, nutrition and stability during development, or heredity. If a colour patch reflects the true condition of an individual, it may be an honest signal (Guilford & Dawkins, 1991); however, individuals that have preferred colouration without being good quality may be displaying dishonestly or may be colourful as a result of Fisherian runaway selection (Prum, 2010). Because blue colours often require precise development or expensive pigments, honest signalling hypotheses (Dawkins & Guilford, 1991; Maynard Smith, 1991) are commonly invoked to explain their function.
The role of feather colouration in signalling is well studied. In some species, bright plumage correlates with reproductive success and thus may be an honest signal of an individual's quality (Keyser & Hill, 1999). There are several examples in which blue plumage indicates the quality of a potential mate. In eastern bluebirds Sialia sialis, males with brighter blue and ultraviolet colouration are more successful in winning nest hollows, pair earlier in the season, provision nestlings more often (Siefferman & Hill, 2003, 2005a, 2007) and bright blue female colouration has been linked to a good quality diet and thus may indicate her quality (Siefferman & Hill, 2005a). The amount of blue on the body of male grosbeak Guiraca caerulea correlates with larger body size, lower bacterial load, larger territories with more prey and that they feed their first nestlings more frequently than males with less blue plumage (Keyser & Hill, 1999; Shawkey et al., 2007). Thus, in grosbeaks, we may expect that females should pay attention to the blueness of males. Ballentine & Hill (2003), however, reported that male grosbeak blueness is unlikely to be used by females as a mate-choice cue and that its correlation with large territory and body size indicates a role in intrasexual signalling and male–male competition. Also, in blue tits Cyanistes caeruleus blue and ultraviolet crown colouration is not effected by the nutritional quality of the diet (Peters et al., 2011), but is negatively correlated with the fluctuating asymmetry of feathers (Galvan, 2011); the more asymmetrical the bird, the less blue and ultraviolet the crown.
In some systems, blue is used in signals outside of the body. Blue items may be collected from the environment, such as blue ornaments or blue may be produced by an individual, but expressed as blue eggs. Male satin bowerbirds P. violaceus (Fig. 1) collect blue items from the environment (both natural and artificial) and place them in a bower made of dry vegetation, used in courtship displays (Endler & Day, 2006). Females assess this display separately to the chroma of the male's blue plumage, which correlates with mating success (Endler et al., 2005; Savard, Keagy & Borgia, 2011). The number and attractiveness of the bower ornaments (bower quality) may provide females information about the parasite load of the male that owns the bower (Doucet & Montgomerie, 2002). Males often steal items from the bowers of others and bluer items are more likely to be stolen (Wojcieszek et al., 2006; Wojcieszek, Nicholls & Goldzein, 2007a). Exactly what information about a male is portrayed by his bower is not clear, but constraints on building the most attractive bower may keep the owner honest. It is intriguing to imagine how this system evolved, perhaps blue items exploit a pre-existing bias in females where bluer bowers are more attractive. However, why blue in particular is the favoured colour, is unclear. One suggestion is that blue items are naturally rare in forests (Borgia, Kaatz & Condit, 1987; Hunter & Dwyer, 1997; Wojcieszek et al., 2006; Wojcieszek, Nicholls & Goldizen, 2007b).
Blue eggshell colouration is widespread in birds but its adaptive significance is still elusive (Kilner, 2006; English & Montgomerie, 2011). Three major non-exclusive hypotheses have been invoked to explain why some birds' eggs are blue: sexual signalling, mimicry and crypsis (in low light) (Moreno & Osorio, 2003; Soler et al., 2005). There have also been a variety of other hypotheses put forward including filtration of sunlight, enhancing the physical strength of the shell and warning colouration. Little evidence supports these hypotheses (Moreno & Osorio, 2003); however, it is difficult to know whether researcher bias has emphasized this lack of support. Evidence for the sexual selection hypothesis is founded in that, as an antioxidant, biliverdin is beneficial to developing embryos. Thus, males should pay attention to the antioxidant investment a female has made in her eggs and he should provision young according to which ones she has invested in the most (Navarro et al., 2011). Modelling egg colour with various life history traits of 152 species, Soler et al. (2005) found a positive correlation between bluer eggs and increased polygyny and suggested that females advertise their maternal investment to males via egg colour to entice them to feed her young preferentially. Cassey et al. (2008) considered egg colours in the context of an appropriate avian visual system and found only a weak link between maternal reproductive investment and blue eggshell colouration and thus no support for Soler et al. (2005)'s hypothesis. Navarro et al. (2011), however showed in spotless starlings Sturnus unicolor that egg shell colour intensity and the yolk's carotenoid concentration were positively correlated suggesting that colour may be a useful indicator of female investment. However, the intensity of the blue colour alone may be enhanced by an achromatic component that is more easily detectable in low-light nest environments (Avilés, Soler & Pérez-Contreras, 2006; Avilés et al., 2008) Further, in a test of the effect of eggshell colour on paternal provisioning, English & Montgomerie (2011) found that male American robins Turdus migratorius provisioned young nestlings (3 days old) from vivid blue eggs more than those from pale eggs, but this difference did not hold for older (6 or 9 days old) nestlings. Moreover, in the great reed warbler Acrocephalus arundinaceus, Honza et al. (2011) report no association between the blue-green chroma of egg shells and measures of female quality, and also that males did not adjust their investment (in parasite defence) in relation to egg shell chroma.
In Kilner's (2006) review of bird egg colouration, she reported that blue eggs were unusual among cavity nesters, and more often found in some (not all) species that build exposed nests. Kilner (2006) highlighted that if blue eggs are cryptic in exposed nests this adaptation has only been selectively advantageous in some species. Wegrzyn et al. (2011) argued that in cavity-nesting European starlings Sturnus vulgaris the ultraviolet and blue-green eggshell colour does not reflect female condition, but instead suggest that more intensely blue-green egg colouration makes eggs more easily visible in dark cavities. This is an intriguing hypothesis, but clearly, more empirical evidence is needed. Also, studies should be aware of the age of the eggs measured to avoid any confounding effects of fading (Moreno, Lobato & Morales, 2011).
A classic example of blue colour change as a signal is the diet-dependent foot colouration of the blue-footed booby Sula nebouxii. Velando, Beamonte-Barrientos & Torres (2006) showed that the intensity of the blue of a male's feet is a strong indication of his current condition, with the foot colour of nutrient-deprived males fading in less than two days. They also showed that maternal investment reduced when the feet of a male were experimentally dulled using cosmetics (Velando et al. 2006). These results indicate that females adjust their behaviour according to the foot colour of their mate and thus that females receive information on a male's recent foraging success by assessing foot colour. Even though, foot colour fades, it is likely to be a good indicator of recent foraging success and in older birds, an indication of their levels of oxidative stress (Torres & Velando, 2007).
Individual quality may be signalled by blue in inveretebrates. The evidence is sparse, but two examples that involve colour change have emerged. In the damselfly, Calopteryx maculata males with abdomens that are more blue than green are in better condition (Fitzstephens & Getty, 2000). Males that are better foragers increase their girth and in so doing the lamellae (microscopic ridges) in the epicuticle responsible for their blue-green colour are pushed closer together. This results in bluer-looking males because as the ridges get closer together, the shorter (bluer) wavelengths are preferentially reflected. Poorer-condition males, however, look green because the ridges are further apart (Fitzstephens & Getty, 2000). This colour change correlates with the territorial status of a male, but whether blueness translates into fitness benefit via female preference or male–male competition is not yet clear (Fitzstephens & Getty, 2000). Also, recently, Barnard et al. (2012) reported on a blue streak on the anterio–dorsal part of the carapace of sexually mature mud fiddler crabs Uca pugnax, They observed that the streak became darker in colour with decreased ambient light, but did not change with temperature and suggest that its reflectance or rate of change may encode information useful in courtship (Barnard et al., 2012).
Blue for sex identification
In most gonochorist species, there are fitness advantages in displaying one's sex [notable exceptions include: beta male cuttlefish masquerading as females (Hanlon et al., 2005) and andromorphic female dragonflies (Forbes, Richardson & Baker, 1995)]. Some studies assess whether species use colour as a sex cue through manipulative behavioural assays. For example, in many Odonata, a proportion of females don bluer, male colouration (Fincke, 1994; Van Gossum, Stoks & De Bruyn, 2001; Iserbyt et al., 2009) While some studies have found support for the hypothesis that andromorph females endure less harassment by males (Cordero, Carbone & Utzeri, 1998; Van Gossum et al., 2001) or may actually be mimicking males (Robertson, 1985), others have shown that males can learn to recognize andromorphs as females (Miller & Fincke, 1999). Cooper & Burns (1987) found that the blue venter of fence lizards Sceloporus undulatus is used by males to recognize the sex of conspecifics. When presented with females that were painted with male colours, male fence lizards displayed aggression. When presented with males painted with female colours, male fence lizards displayed courtship behaviours. How females react to painted males in this species would be of great interest to determine if colour is used in recognition by both sexes. Also, testing for further functions may reveal that this colour conveys multiple signals, not only sex but something about the quality of the individual.
Male Balkan moor frogs Rana arvalis wolterstorffi change colour from brown to blue and ultraviolet during the mating season (Ries et al., 2008; Hettyey et al., 2009). Ries et al. (2008) suggest that this is so male frogs can ensure they are recognized as such during scramble competition. However, Sheldon et al. (2003) propose that blue male colouration signals genetic quality that helps tadpoles avoid predation. Hettyey et al. (2009) found that the bluest of the small males enjoy greater mating success while blueness of the larger males does not predict mating success. They also reported that bluer individuals had higher body temperatures, but the mechanism of colour change and how it relates to body temperature is unknown. If selectively advantageous, it is unclear as to why males turn blue for only a brief period rather than maintaining their blue and ultraviolet colouration all the time and perhaps suggests a trade off with crypsis. Investigating costs of maintaining their blue colour may be the key to understanding the function of this colour change.
Signalling sex may be particularly important in sequentially hermaphroditic species such as the western Achoerodus gouldii and eastern blue gropers A. viridis and the blue-throated wrasse Notolabrus tetricus. In these species, females turn blue as they become male through a shift in the biliverdin (a blue pigment) concentration in their blood (Gagnon, 2006; Coulson, Hesp & Potter, 2009). If a male is removed from the population the largest female will change sex and in doing so, change the colour to blue (Coulson et al., 2009). The cues for this change and how it affects the behaviour of conspecifics, however, remain unexplored.
Sex identification seems to be given as the function of colouration when a study yields no evidence to support sexual signalling. In this way, sex identification is used like a null hypothesis or default explanation for sexual dichromatism. If the function of colouration is sex identification, it may only be a small evolutionary step away from providing more information than just sex such as information about the individual's quality. Variation in such signals could be co-opted as indicators of quality for preference or in aggressive interactions.