Plumage colour in nestling blue tits: sexual dichromatism,condition dependence and genetic effects

Sexual-selection theory assumes that there are costs associated with ornamental plumage coloration. While pigment-based ornaments have repeatedly been shown to be condition dependent, this has been more difficult to demonstrate for structural colours. We present evidence for condition dependence of both types of plumage colour in nestling blue tits (Parus caeruleus). Using reflectance spectrometry, we show that blue tit nestlings are sexually dichromatic, with males having more chromatic (more 'saturated') and ultraviolet (UV)-shifted tail coloration and more chromatic yellow breast coloration. The sexual dimorphism in nestling tail coloration is qualitatively similar to that of chick-feeding adults from the same population. By contrast, the breast plumage of adult birds is not sexually dichromatic in terms of chroma. In nestlings, the chroma of both tail and breast feathers is positively associated with condition (body mass on day 14). The UV/blue hue of the tail feathers is influenced by paternally inherited genes, as indicated by a maternal half-sibling comparison. We conclude that the expression of both carotenoid-based and structural coloration seems to be condition dependent in blue tit nestlings, and that there are additional genetic effects on the hue of the UV/blue tail feathers. The signalling or other functions of sexual dichromatism in nestlings remain obscure. Our study shows that nestling blue tits are suitable model organisms for the study of ontogenetic costs and heritability of both carotenoid-based and structural colour in birds.     

Ultraviolet sexual dimorphism and assortative mating in blue tits

In spite of strong evidence for viability-based sexual selection and sex ratio adjustments, the blue tit, Parus caeruleus, is regarded as nearly sexually monomorphic and no epigamic signals have been found. The plumage coloration has not, however, been studied in relation to bird vision, which extends to the UV-A waveband (320 to 400 nm). Using molecular sex determination and UV/VIS spectrometry, we report here that blue tits are sexually dichromatic in UV/blue spectral purity (chroma) of the brilliant crown patch. It is displayed in courtship by horizontal posturing and erected nape feathers. A previously undescribed sexual dimorphism in crown size (controlling for body size) further supports its role as an epigamic ornament. Against grey-brown leaf litter and bark during pair formation in early spring, but also against green vegetation, UV contributes strongly to conspicuousness and sexual dimorphism. This should be further enhanced by the UV/bluish early morning skylight (''woodland shade'') in which blue tits display. Among 18 breeding pairs, there was strong assortative mating with respect to UV chroma, but not size, of the crown ornament. We conclude that blue tits are markedly sex dimorphic in their own visual world, and that UV/violet coloration probably plays a role in blue tit mate acquisition.     

Seasonal changes in a ultraviolet structural colour signal in blue tits, Parus caeruleus

Recent studies of blue tits, Parus caeruleus , have found sexual selection and a viability-indicating function of the structural ultraviolet and blue crown plumage, but the reasons for this signal variation are not understood. Furthermore, studies in England and Sweden have yielded somewhat different results (particularly with regard to the spectral position of the reflectance peak). Here we investigate whether the blue tit UV/blue ornament varies with time of year since such variation might be relevant to the signalling function as well as the apparent difference between populations. From 400 blue tits captured at two different localities in Sweden, we found that objective measures of 'hue' (spectral location), 'chroma' (spectral purity) and 'brightness' (spectral intensity), varied substantially with season. Just after moult (October), crown 'hue' is maximally UV-shifted (359 nm for males and 373 nm for females). Thereafter the peak drifts upwards and by the time of nestling feeding (June) male reflectance peaks at 404 nm and female at 413 nm. This change is probably due to feather wear as well as fat and dirt accumulation, which might constitute an additional male quality cue. Our results suggest that it is important to consider plumage age when exploring variation in structural plumage coloration, and that it can largely explain the difference between the British and Swedish studies. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 237–245.     

Ultraviolet plumage does not signal social status in free-living blue tits; an experimental test

Ultraviolet (UV) signals are suggested to be sexually selectedin a wide range of taxa. Most research, however, has focusedon the role of UV signals in mate choice, whereas possible functionsin intraspecific competition remain largely untested. Studieson other colors indicate that ornaments preferred by femalescan also function as signals of social status in competitiveinteractions between individuals. Whereas these colors are mainlypigment based, UV reflectance is generally caused by selectivereflectance of light from surface structures. Here we test experimentallywhether the structurally based UV-reflective crown plumage inthe blue tit (Cyanistes caeruleus) serves as a signal of statusin interindividual competition. We reduced the crown UV reflectanceof free-living blue tits in winter and compared their probabilityof winning conflicts over food at a feeding table with control-treatedand untreated individuals. Although we controlled for effectsof sex, age, and distance from territory, we found no effectof reduced UV reflectance on the probability of winning norwere conflicts involving UV-reduced individuals more likelyto escalate. Therefore, we conclude that the UV reflectanceof the blue tit's crown does not serve as a signal of statusin competition over food in winter. We suggest that the observedsite-dependent dominance structure may constrain the opportunityfor a status signal to evolve and that enhancing attractivenessin mate choice may be the sole function of the crown's UV reflectance.     

Blue,not UV,plumage color is important in satin bowerbird Ptilonorhynchus violaceus display

Several studies have suggested that peak plumage reflectance in birds matches color preferences used in mate choice. We tested this hypothesis in adult satin bowerbird males that have a short‐wavelength saturated blue‐black plumage with a peak reflectance in the UV. We found that the chroma of the blue (405–480 nm), but not the peak reflecting UV (320–400 nm) portion of the male plumage spectrum was significantly correlated with male mating success. A plot of correlation coefficients between male mating success and plumage saturation showed a well‐defined peak in the blue. This suggests that: 1) blue plumage coloration is more important in mate choice than UV or other colors, and 2) that there is a mismatch between the peak reflectance of the plumage of male satin bowerbirds and the range of plumage wavelengths that are correlated with male mating success. This indicates that it is not safe to infer a role of UV or other colors in mate choice simply because of a peak in plumage reflectance.     

Variation in ultraviolet reflectance by carotenoid-bearing feathers of tanagers (Thraupini: Emberizinae: Passeriformes)

Avian visual sensitivity encompasses both the human visible range (400–700 nm) and also near‐ultraviolet (UV) wavelengths (320–400 nm) invisible to normal humans. I used reflectance spectrophotometry to assess variation in UV reflectance for yellow, orange and red plumage in 67 species of tanager (Passeriformes). Previous chemical studies, and my analysis of reflectance minima, suggest that carotenoids are the dominant pigments in yellow, orange and red tanager plumage. Spectra recorded over the range of wavelengths to which birds are sensitive (320–700 nm) were invariably bimodal, with both a plateau of high reflectance at longer (> 500 nm) wavelengths and a distinct secondary peak at UV (< 400 nm) wavelengths. Within this overall framework, variation in UV reflectance was expressed within well‐defined quantitative limits: (1) peak reflectance was always lower than the corresponding plateau of reflectance at longer visible wavelengths; (2) the intensity of peak reflectance declined steadily below 350 nm; (3) wavelengths of peak reflectance clustered between 350 and 370 nm. Significant correlations were detected between various measures of total reflectance in the UV and visible wavebands, but not between various measures of spectral location of UV and visible reflectance. I propose that the strong absorption band at short visible wavelengths (～ 380–550 nm) responsible for bimodal spectra of carotenoids in vitro is also responsible for bimodal reflectance by carotenoid‐based plumage colours. The construction of the UV and visible reflectance bands from different sides of this same absorbance band provides a mechanism for the observed covariation between UV and visible wavelengths. Lack of an association between the spectral locations of the UV and visible reflectance bands may result from the limited variation in spectral location of the UV band. These patterns suggest that plumage colours are subject to constraints, just as are more traditional morphological characters. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84 , 243–257.     

Seasonal Changes in Colour: A Comparison of Structural,Melanin- and Carotenoid-Based Plumage Colours

Background

Plumage coloration is important for bird communication, most notably in sexual signalling. Colour is often considered a good quality indicator, and the expression of exaggerated colours may depend on individual condition during moult. After moult, plumage coloration has been deemed fixed due to the fact that feathers are dead structures. Still, many plumage colours change after moult, although whether this affects signalling has not been sufficiently assessed.

Methodology/Principal Findings

We studied changes in coloration after moult in four passerine birds (robin, Erithacus rubecula; blackbird, Turdus merula; blue tit, Cyanistes caeruleus; and great tit, Parus major) displaying various coloration types (melanin-, carotenoid-based and structural). Birds were caught regularly during three years to measure plumage reflectance. We used models of avian colour vision to derive two variables, one describing chromatic and the other achromatic variation over the year that can be compared in magnitude among different colour types. All studied plumage patches but one (yellow breast of the blue tit) showed significant chromatic changes over the year, although these were smaller than for a typical dynamic trait (bill colour). Overall, structural colours showed a reduction in relative reflectance at shorter wavelengths, carotenoid-based colours the opposite pattern, while no general pattern was found for melanin-based colours. Achromatic changes were also common, but there were no consistent patterns of change for the different types of colours.

Conclusions/Significance

Changes of plumage coloration independent of moult are probably widespread; they should be perceivable by birds and have the potential to affect colour signalling.     

No evidence for general condition-dependence of structural plumage colour in blue tits: an experiment

Condition-dependence is a central but contentious tenet of evolutionary theories on the maintenance of ornamental traits, and this is particularly true for structural plumage colour. By providing diets of different nutritional quality to moulting male and female blue tits, we experimentally manipulated general condition within the natural range, avoiding deprivation or stressful treatments. We measured reflectance of the structural-coloured UV/blue crown, a sexually selected trait in males, and the white cheek, a nonpigmented structural colour, directly after moult and again during the following spring mating season. We employed a variety of colour indices, based on spectral shape and avian visual models but, despite significant variation in condition and coloration, found no evidence for condition-dependence of UV/blue or white plumage colour during either season. These and previously published results suggest that structural colour might be sensitive to stress, rather than reduced body condition, during moult.     

Effectiveness of a commonly-used technique for experimentally reducing plumage UV reflectance

Ultraviolet (UV) plumage is thought to be sexually selected through intra-sexual competition, female choice and differential allocation. Experimental manipulations of plumage UV reflectance are essential to demonstrate that mate choice or intra-sexual competition are causally related to UV coloration. The most widely-used technique for manipulating UV reflectance in wild birds is the application of a mixture of UV-absorbing chemicals and preen gland fat. However, although this UV reduction technique is commonly used, little is known about the persistence of the treatment and the temporal variation in UV reflectance that it causes. We manipulated the UV crown plumage of wild and captive blue tits Parus caeruleus , and took repeated photospectrometric measurements of both UV-reduced and control-treated individuals. Our results show that the UV reduction lasts for at least five days and that the treatment has no negative effects on the survival of wild birds.     

Ultraviolet reflectance affects male-male interactions in the blue tit (Parus caeruleus ultramarinus)

Several animal species have been shown to use phenotypic traitsto assess the competitive ability of opponents and adjust theiraggressiveness depending on the likelihood to win the contest.In birds, these phenotypic traits usually involve patches ofcolored feathers. The benefit to harbor honest signals of malequality is the avoidance of wasteful aggressive interactions.Recent work has shown that ultraviolet (UV) plumage reflectanceis an important signal used by females during mate choice. Surprisingly,however, the role of UV signaling on intrasexual selection hasbeen neglected. In the present study, we aimed to test whetherUV reflectance of crown feathers was used as a signal of malecompetitive ability during male-male interactions. Breedingmale blue tits (Parus caeruleus ultramarinus) were exposed duringthe female egg-laying period to blue tit taxidermic mounts witheither control or reduced UV reflectance of crown feathers.In agreement with the prediction that UV reflectance advertisesmale quality, we found that breeding blue tits behaved lessaggressively toward the UV-reduced decoy. To our knowledge,this is the first experimental evidence suggesting a role forUV signaling on intrasexual selection.     

Effects of nestling condition on UV plumage traits in blue tits: an experimental approach

Intraspecific sexual and social communications are among themost important factors shaping costly color traits in birds.Condition capture models assume that only animals in superiorcondition can develop and maintain a colorful plumage. Althoughthere is good evidence that carotenoid-based components of plumagecolors show condition dependence, the situation is more controversialwith the underlying UV-reflecting structural component. We conducteda brood size manipulation in blue tits (Parus caeruleus) toinvestigate condition-dependent effects on plumage colorationin male and female offspring. Carotenoid chroma and UV reflectanceof the yellow breast plumage showed condition-dependent expressionin male and female fledglings. However, only males that wereraised in reduced broods had higher UV reflectance in the UV/bluetail feathers, whereas female tail coloration did not differbetween treatments. Our data suggest that there is a sex-specificeffect on the blue but not the yellow plumage and that thisis related to differences in the signaling function of bothplumage traits. Although sexual selection may already act onmale nestlings to develop colorful tail feathers for the nextbreeding season, the UV/yellow breast feathers are molted duringthe postjuvenile molt, and their signaling value is likely tobe important for both sexes during the extended postfledglingphase.     

Territorial responses of male blue tits, Cyanistes caeruleus , to UV-manipulated neighbours

Multiple phenotypic traits can affect the outcome of interactions among territorial animals. Individuals may use current and previously acquired information on phenotypic traits to assess the competitive ability of opponents and adjust the strength of their response depending on the threat the opponent poses. In birds, colourful plumage and song are widespread phenotypic traits. Recent work has shown that ultraviolet (UV) plumage reflectance may be used by males in assessing an opponent’s strength and by females in mate choice. In the present study, we investigated whether and how territorial male blue tits, Cyanistes caeruleus, use previously acquired information from UV reflectance of the crown feathers of neighbours to adjust their response to playback of song of these neighbours simulated to intrude their territory. We compared responses to neighbours with those to unfamiliar strangers with unknown plumage features. We found that subject males with UV-enhanced neighbours responded more strongly to these neighbours than to strangers, i.e. showed more flights, used songs without trill and tended to overlap more songs. Subject males with UV-reduced neighbours gave a lower or similar response to neighbours compared to strangers. This indicates that male blue tits combine previously acquired information about an intruder’s plumage with familiarity of its song, and that their response depends on the perceived quality of the neighbour. This study provides evidence that familiarity in combination with multiple signals of quality may influence territorial relations among neighbours.     

The relationship between plumage colouration,problem‐solving and learning performance in great tits Parus major

Recent studies suggest that individuals with better problem‐solving and/or learning performance have greater reproductive success, and that individuals may thus benefit from choosing mates based on these performances. However, directly assessing these performances in candidate mates could be difficult. Instead, the use of indirect cues related to problem‐solving and/or learning performance, such as condition‐dependent phenotypic traits, might be favored. We investigated whether problem‐solving and learning performance on a novel non‐foraging task correlated with sexually selected plumage colouration in a natural population of great tits Parus major. We found that males successful in solving the task had darker blue‐black crowns than non‐solvers, and that males solving the task more rapidly over multiple attempts (i.e. learners) exhibited blue‐black crowns with higher UV chroma and shorter‐wavelength hues than non‐learners. In contrast, we found no link between behavioural performance on the task and the yellow breast colouration in either sex. Our findings suggest that blue‐black crown colouration could serve as a signal of problem‐solving and learning performance in wild great tit males. Further research remains necessary to determine whether different sexually selected traits are used to signal cognitive performance for mate choice, either directly (i.e. cognitive performance influencing individual's health and ornamentation through diet for example) or indirectly (i.e. due to a correlation with a third factor such as individual quality or condition).     

Juvenile coloration of Florida Scrub-Jays ( Aphelocoma coerulescens ) is sexually dichromatic and correlated with condition

The Florida Scrub-Jay is a monogamous cooperative breeder in which both males and females display extensive structurally based blue plumage. Juveniles of this species exhibit blue tail and wing feathers that they begin growing as nestlings, and some of these feathers are retained throughout their first year. Although the birds appear to be sexually monochromatic, we assessed whether cryptic dichromatism exists in both the magnitude and pattern of coloration in tail feathers of juvenile Florida Scrub-Jays. We then determined whether variation in plumage coloration is associated with nutritional condition during molt. Tails of juvenile male Florida Scrub-Jays exhibit a greater proportion of UV reflectance than those of females. Mass at age 11 days and ptilochronology of the juvenile tail feathers were used as measures of individual nutritional condition during feather growth, and the latter was found to be positively associated with UV chroma. These data demonstrate that Florida Scrub-Jays are sexually dichromatic and suggest that variation in plumage color may be condition dependent, although we cannot rule out alternative explanations. Juvenile plumage coloration, therefore, has the potential to function as a signal of individual quality in both males and females.     

Condition-dependent variation in the blue-ultraviolet coloration of a structurally based plumage ornament

After years of investigation into the function of sexually dimorphic ornamental traits, researchers are beginning to understand how bright plumage colour in birds acts as an intraspecific signal. This work has focused primarily on pigment-based ornaments because they are highly variable in patch size, hue and brightness for some species. In contrast, structurally based ornaments have been little studied, in part because they do not appear to be as variable as pigment-based ornaments. We investigated a structurally based plumage ornament in a wild population of blue grosbeaks (Guiraca caerulea), a sexually dimorphic passerine. We report plumage variation that extends into the ultraviolet region of the spectrum. The pattern of covariation between four out of five elements of plumage variation suggests that structurally based ornamentation is pushed towards extreme expression of the trait as predicted by the sexual selection theory. The ''bluest'' birds have the highest percentage of blue feathers on the body. These ornamental feathers reflect light maximally at the shortest wavelengths (ultraviolet), with the greatest intensity and the greatest contrast. Age may have some effect on expression of blueness. In addition, plumage variables are correlated with growth bars in tail feathers (a record of nutritional condition during moult in a non-ornamental trait). This suggests that the ornament is partially condition dependent. Thus, blue plumage in male grosbeaks may serve as an honest indicator of age and quality.     

Optimizing the colour and fabric of targets for the control of the tsetse fly Glossina fuscipes fuscipes

Background

Most cases of human African trypanosomiasis (HAT) start with a bite from one of the subspecies of Glossina fuscipes. Tsetse use a range of olfactory and visual stimuli to locate their hosts and this response can be exploited to lure tsetse to insecticide-treated targets thereby reducing transmission. To provide a rational basis for cost-effective designs of target, we undertook studies to identify the optimal target colour.

Methodology/Principal Findings

On the Chamaunga islands of Lake Victoria , Kenya, studies were made of the numbers of G. fuscipes fuscipes attracted to targets consisting of a panel (25 cm square) of various coloured fabrics flanked by a panel (also 25 cm square) of fine black netting. Both panels were covered with an electrocuting grid to catch tsetse as they contacted the target. The reflectances of the 37 different-coloured cloth panels utilised in the study were measured spectrophotometrically. Catch was positively correlated with percentage reflectance at the blue (460 nm) wavelength and negatively correlated with reflectance at UV (360 nm) and green (520 nm) wavelengths. The best target was subjectively blue, with percentage reflectances of 3%, 29%, and 20% at 360 nm, 460 nm and 520 nm respectively. The worst target was also, subjectively, blue, but with high reflectances at UV (35% reflectance at 360 nm) wavelengths as well as blue (36% reflectance at 460 nm); the best low UV-reflecting blue caught 3× more tsetse than the high UV-reflecting blue.

Conclusions/Significance

Insecticide-treated targets to control G. f. fuscipes should be blue with low reflectance in both the UV and green bands of the spectrum. Targets that are subjectively blue will perform poorly if they also reflect UV strongly. The selection of fabrics for targets should be guided by spectral analysis of the cloth across both the spectrum visible to humans and the UV region.     

Novel chromatic and structural biomarkers of diet in carotenoid-bearing plumage

Previous attempts to establish a link between carotenoid-based plumage reflectance and diet have focused on spectral features within the human visible range (400-700 nm), particularly on the longer wavelengths (550-700 nm) that make these plumages appear yellow, orange or red. However, carotenoid reflectance spectra are intrinsically bimodal, with a less prominent but highly variable secondary reflectance peak at near-ultraviolet (UV; 320-400 nm) wavelengths visible to most birds but not to normal humans. Analysis of physical reflectance spectra of carotenoid-bearing plumages among trophically diverse tanagers (Thraupini, Emberizinae, Passeriformes) indicated that both the absolute and relative (to long visible wavelengths) amounts of short waveband (including UV) reflectance were lower in more frugivorous species. Striking modifications to the branched structure of feathers increased with frugivory. These associations were independent of phylogenetic relatedness, or other physical (specimen age, number of carotenoid-bearing patches) or ecological (body size, elevation) variables. By comparison, reflectance at longer visible wavelengths ('redness') was not consistently associated with diet. The reflectance patterns that distinguished frugivores should be more apparent to UV-sensitive birds than to UV-blind humans, but humans can perceive the higher plumage gloss produced by modified gross feather structure. Basic aspects of carotenoid chemistry suggest that increases in pigment concentration and feather dimensions reduce short waveband reflectance by the plumages of frugivores.     

Sexual dichromatism,size dimorphism,and microscale anatomy of white wing stripe in blue tits

Achromatic patches are a common element of plumage patterns in many bird species and there is growing body of evidence that in many avian taxa they can play a signaling role in mate choice. Although the blue tit Cyanistes caeruleus is a well-established model species in the studies on coloration, its white wing patch has never been examined in the context of sex-specific trait expression. In this exploratory study, we examined sexual size dimorphism and dichromatism of greater covert’s dots creating white wing patch and analyzed its correlations with current body condition and crown coloration—a trait with established role in sexual selection. Further, we qualitatively analyzed microstructural barb morphology underlying covert’s coloration. We found significant sexual dimorphism in the dot size independent of covert size and sexual dichromatism in both white dot and blue outer covert’s vane spectral characteristics. Internal structure of covert barbs within the white dot was similar to the one found in barbs from the blue part that is, with a medullary area consisting of dead keratinocytes containing channel-type ß-keratin spongy nanostructure and centrally located air cavities. However, it lacked melanosomes which was the main observed difference. Importantly, UV chroma of covert’s blue vane was positively correlated with crown UV chroma and current condition (the latter only in males), which should be a premise for further research on the signal function of the wing stripe.     

Seasonality of carotenoid‐based plumage coloration: modelling wavelength‐specific change through spectral reconstruction

Plumage coloration has provided important model systems for research on signal expression. Whilst it had previously been assumed that moulting provided the only mechanism to change plumage coloration, recent studies have shown plumage colours to be seasonally dynamic, with implications both for the quantification of expression and for any signalling role. However, the mechanistic processes underlying such change remain uncertain. Here, we describe within‐moult shifts in expression of a carotenoid‐based colour trait – the yellow ventral plumage of the great tit Parus major – over a nine‐month timespan. We report that plumage chromaticity (‘colour’) – but not achromaticity (‘brightness’) – exhibits a marked seasonal decline, independent of sex, age or body condition, and at a constant rate across twelve environmentally heterogeneous plots within our study site. To gain a greater understanding of the mechanisms underlying this change we employed a spectral reconstruction approach, that generates predicted spectra for any timepoint within the sampling period. By comparing spectra for both early and late in the moult we show that the seasonal decline in chromaticity is driven by both a marked reduction in ultraviolet (UV) reflectance and, to a lesser extent, loss of active carotenoid pigments. Thus, our study shows that seasonal loss of chromaticity in the great tit is driven by altered reflectance primarily in the UV section of the spectrum, a finding made possible by the use of spectral compartmentalisation and multi‐parallel modelling to produce reconstructed spectra. Whether change in plumage coloration influences signal function will depend on the dynamics of the signalling system but it could clearly inflate patterns such as assortative mating and should be considered in studies of colour expression.     

Brighter yellow blue tits make better parents

Whether or not bird ornaments are a signal for direct (e.g. good parents) or indirect (e.g. good genes) benefits to prospective partners in sexual selection is controversial. Carotene coloration in Parus species is directly related to the ingestion of caterpillars, so that a brightly carotene-coloured tit may be signalling its ability to find caterpillars, a main high-quality food source for good fledgling development, and hence its parental abilities. If carotene-based plumage coloration is related to the good-parent hypothesis, we predict that yellow plumage brightness of tit fathers should be positively correlated to their investment in offspring provisioning. Here, we use cross-fostering experiments in blue tits (Parus caeruleus) to show that chick development (as measured by tarsus length) is related to yellowness of the foster father, but not to that of the genetic parents. Using these data, we were able to measure, for the first time to our knowledge, the separate contribution of genetic and environmental factors (i.e. parental plumage coloration) to chick development, and hence parental investment. Our data, which relate carotenoid coloration to models of good parents, and data from other authors, which relate ultraviolet coloration to good-genes models, stress that different kinds of coloration within an individual may provide different units of information to prospective females.