Ornamental comb colour predicts T-cell-mediated immunity in male red grouse <Emphasis Type="Italic">Lagopus lagopus scoticus</Emphasis>

Sexual ornaments might reliably indicate the ability to cope with parasites and diseases, and a better ability to mount a primary inflammatory response to a novel challenge. Carotenoid-based ornaments are amongst the commonest sexual signals of birds and often influence mate choice. Because carotenoids are immuno-stimulants, signallers may trade-off allocating these to ornamental colouration or using them for immune responses, so carotenoid-based ornaments might be particularly useful as honest indicators of immuno-compentence. Tetraonid birds, such as the red grouse Lagopus lagopus scoticus, exhibit supra-orbital yellow-red combs, a conspicuous ornament which functions in intra- and inter-sexual selection. The colour of combs is due to epidermal pigmentation by carotenoids, while their size is testosterone-dependent. In this study, I investigated whether comb characteristics, and in particular, comb colour, indicated immuno-competence in free-living male red grouse. I assessed T-cell-mediated immunity using a standardised challenge with phytohaemagglutinin. Red grouse combs reflect in the red and in the ultraviolet spectrum of light, which is not visible to humans but that grouse most likely see, so I measured comb colour across the whole bird visible spectrum (300-700 nm) using a reflectance spectrometer. I found that males with bigger and redder combs, but with less ultraviolet reflectance, had greater T-cell-mediated immune response. Comb colour predicted T-cell-mediated immune response better than comb size, indicating that the carotenoid-based colouration of this ornament might reliably signal this aspect of male quality.     

Dietary antioxidants, lipid peroxidation and plumage colouration in nestling blue tits Cyanistes caeruleus

Carotenoid pigments are responsible for many of the red, yellow and orange plumage and integument traits seen in birds. One idea suggests that since carotenoids can act as antioxidants, carotenoid-mediated colouration may reveal an individual's ability to resist oxidative damage. In fact, there is currently very little information on the effects of most dietary-acquired antioxidants on oxidative stress in wild birds. Here, we assessed the impacts on oxidative damage, plasma antioxidants, growth and plumage colouration after supplementing nestling blue tits Cyanistes caeruleus with one of three diets; control, carotenoid treatment or α-tocopherol treatment. Oxidative damage was assessed by HPLC analysis of plasma levels of malondialdehyde (MDA), a by-product of lipid peroxidation. Contrary to predictions, we found no differences in oxidative damage, plumage colouration or growth rate between treatment groups. Although plasma lutein concentrations were significantly raised in carotenoid-fed chicks, α-tocopherol treatment had no effect on concentrations of plasma α-tocopherol compared with controls. Interestingly, we found that faster growing chicks had higher levels of oxidative damage than slower growing birds, independent of treatment, body mass and condition at fledging. Moreover, the chromatic signal of the chest plumage of birds was positively correlated with levels of MDA but not plasma antioxidant concentrations: more colourful nestlings had higher oxidative damage than less colourful individuals. Thus, increased carotenoid-mediated plumage does not reveal resistance to oxidative damage for nestling blue tits, but may indicate costs paid, in terms of oxidative damage. Our results indicate that the trade-offs between competing physiological systems for dietary antioxidants are likely to be complex in rapidly developing birds. Moreover, interpreting the biological relevance of different biomarkers of antioxidant status represents a challenge for evolutionary ecology.     

The fractal dimension of a conspicuous ornament varies with mating status and shows assortative mating in wild red-legged partridges (<Emphasis Type="Italic">Alectoris rufa</Emphasis>)

Complex body designs, such as plumage ornaments in birds, can be described by fractal geometry. These complex patterns could have a role as visual signals during courtship and social interactions, but an empirical validation in the wild is currently lacking. Here, we investigated whether the fractal dimension (FD) of a complex plumage pattern displayed by red-legged partridges Alectoris rufa could function as a potential sexual signal. We captured wild birds early in the breeding season and tested if mated and unmated birds differed in the FD of their conspicuous melanin-based black bib. We also tested if the FD of the black bib was correlated within the pair, looking for evidence of assortative mating based on the expression of this trait. We simultaneously assessed similar effects in other ornamental traits (black bib size, white throat patch and black flank band surface, redness of the eye rings and bill). Mated birds showed higher black bib FD values than unmated ones. Mated males, but not females, also displayed a larger black bib. Moreover, the black bib FD (but not the trait size) and the white throat patch surface showed assortative mating. Finally, females with higher black bib FD showed smaller black flank band surface, suggesting a trade-off in the expression of the two melanin-pigmented plumage traits. This provides unique and novel indication for the shape complexity of a pigmented trait, here described by its fractal dimension, to be potentially under sexual selection in a wild animal.     

Do feather-degrading bacteria actually degrade feather colour? No significant effects of plumage microbiome modifications on feather colouration in wild great tits

Parasites are known to exert selective pressures on host life history traits since the energy and nutrients needed to mount an immune response are no longer available to invest in other functions. Bird feathers harbour numerous microorganisms, some of which are able to degrade feather keratin (keratinolytic microorganisms) and affect feather integrity and colouration in vitro. Although named “feather-degrading” microorganisms, experimental evidence for their effects on feathers of free-living birds is still lacking. Here, we tested whether (i) keratinolytic microorganisms can degrade feathers in vivo and thus modify the colour of feathers during the nesting period and (ii) whether feather microorganisms have a long-term effect on the investment in colouration of newly moulted feathers. We designed treatments to either favour or inhibit bacterial growth, thus experimentally modifying plumage bacterial communities, in a wild breeding population of great tits (Parus major). Our analyses revealed no significant effects of the treatments on feather colours. Moreover, we found that differences in bacterial exposure during nesting did not significantly affect the colouration of newly moulted feathers. Our results suggest that significant feather degradation obtained during in vitro studies could have led to an overestimation of the potential of keratinolytic microorganisms to shape feather colouration in free-living birds.     

Do feather-degrading bacteria affect sexually selected plumage color?

Models of parasite-mediated sexual selection propose that males with more elaborate sexual traits will have fewer parasites. These models have generally been tested using metazoan or protozoan parasites of the blood, gut, or integument. Fewer studies have examined sexual ornaments in relation to bacterial infections. While most surface bacteria are harmless or beneficial, feather-degrading bacteria may have detrimental effects. In this study, we examined the relationships between overall bacterial load, feather-degrading bacterial load, and sexually selected carotenoid-based plumage color in a wild population of house finches (Carpodacus mexicanus). We found that males with the redder plumage preferred by females had similar overall bacterial loads, but lower feather-degrading bacterial loads, than males with less red plumage. These data suggest that plumage color can signal abundance of feather-degrading bacteria to potential mates. It remains unclear whether feather-degrading bacteria directly or indirectly affect plumage color, but the observed correlations suggest that feather-degrading bacteria may play some role in sexual selection.     

Assortative mating by carotenoid-based plumage colour: a quality indicator in American goldfinches,<Emphasis Type="Italic"> Carduelis tristis</Emphasis>

We investigated the mating patterns in 22 breeding pairs of wild American goldfinches (Carduelis tristis) with respect to their body size, condition, and carotenoid-based, yellow plumage colour. Using reflectance spectrometry, we objectively quantified plumage colours across the bird-visible wavelengths, revealing a unexpected UV peak in the reflectance spectrum from yellow feathers. We summarized our colour measurements using a principal components analysis to create a single variable, carotenoid PC1, that represents the intensity of this carotenoid-based yellow colour, a measure of phenotypic quality in this species. We found no evidence of assortative mating with respect to measures of body size or condition but there was positive assortative mating by carotenoid PC1, such that the yellow plumage colours of males and females were significantly correlated within pairs. We argue that the yellow carotenoid coloration of goldfinches may be important in mutual mate choice and, thus, that sexual selection in this species may act upon female ornamentation, as well as the more obvious plumage signals of males. Because assortative mating results in an increase in genetic variance, we suggest that this might be a mechanism that maintains variance in ornamental traits in spite of the variance-eroding effects of sexual selection.     

Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (<Emphasis Type="Italic">Alectoris rufa</Emphasis>)

Carotenoid pigments cannot be synthesized by vertebrates but must be ingested through the diet. As they seem to be a limited resource, carotenoid-based ornaments are particularly interesting as possible honest signals of individual quality, in particular of foraging efficiency and nutritional status. Some studies have demonstrated the condition dependence of carotenoid-based plumage in birds. However, many other carotenoid-pigmented bare parts (i.e. skin, caruncles, bills, cere, and tarsi) are present in birds but, in comparison with plumage, little is known about these traits as indicators of individual quality. Here, we show that the eye ring pigmentation and bill redness of the red-legged partridge (Alectoris rufa) are positively associated to body condition and recent changes in body mass. Also, we found a negative relationship between these two traits and heterophil-to-lymphocyte ratio, an indicator of physiological stress (the relationship with bill redness being significant only for males). In an experiment, we found that after a period of reduction in food intake (with the consequent loss of body mass), food-restricted birds showed lower eye ring pigmentation than ad-libitum-fed birds. Therefore, different ornaments seem to reflect changes in body condition but at different speeds or intensities (eye ring, a fleshy ornament, appears to respond more rapidly to changes in the nutritional status than a keratinized structure as the bill). These results indicate that carotenoid-based ornaments are condition-dependent traits in the red-legged partridge, being therefore susceptible to be employed as honest signals of quality in sexual selection.     

Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch

The Hamilton-Zuk hypothesis proposes that the bright colours displayed by many species of birds serve as signals of individual resistance to parasites. Despite the popularity of this hypothesis, only one previous study has tested whether plumage coloration predicts how individuals respond to a disease challenge. We inoculated 24 male house finches (Carpodacus mexicanus) of variable plumage hue with a novel bacterial pathogen, Mycoplasma gallicepticum (MG). We found no relationship between plumage hue and time to first symptoms following inoculation, but we found a significant negative relationship between plumage hue and clearance of disease: males with redder plumage cleared MG infection significantly better than did males with yellower plumage. The hue of carotenoid-based plumage coloration has been shown to be a primary criterion in female mate choice in the house finch. These observations suggest that one benefit to females for choosing redder males is obtaining mates with better resistance to parasites.     

Integrated plumage colour variation in relation to body condition, reproductive investment and laying date in the collared flycatcher

The possible integration of different sexual ornaments into a composite system, and especially the information content of such ornament complexes, is poorly investigated. Many bird species display complex plumage coloration, but whether this represents one integrated or several independent sexual traits can be unclear. Collared flycatchers (Ficedula albicollis) display melanised and depigmented plumage areas, and the spectral features (brightness and UV chroma) of these are correlated with each other across the plumage. In a 5-year dataset of male and female plumage reflectance, we examined some of the potential information content of integrated, plumage-level colour attributes by estimating their relationships to previous and current year body condition, laying date and clutch size. Females were in better condition the year before they became darker pigmented, and males in better current year condition were also darker pigmented. Female pigment-based brightness was positively, while male structurally based brightness was negatively related to current laying date. Finally, the overall UV chroma of white plumage areas in males was positively associated with current clutch size. Our results show that higher degree of pigmentation is related to better condition, while the structural colour component is associated with some aspects of reproductive investment. These results highlight the possibility that correlated aspects of a multiple plumage ornamentation system may reflect together some aspects of individual quality, thereby functioning as a composite signal.     

The effect of growth rate and ageing on colour variation of European pond turtles

Many chelonians have colourful dots, patches and stripes throughout their body that are made up, at least in part, of carotenoids. Therefore, turtles are very suitable models to study the evolution and functionality of carotenoid-based colouration. Recent studies suggested a close link between colouration and immune system in these taxa. However, more research is needed to understand the role of these colourful stripes and patches in turtle visual signalling. The purpose of this study was to explore the relationship between growth rate and colouration in European pond turtles. In particular, we wanted to answer the question of whether there is a trade-off between growth and colour expression. We also aimed to explore the effect of body size and age on colour variation. Turtles from a reintroduction-breeding program were recaptured, weighed and measured over an 8-year period to estimate their growth rates and age. We also measured with a spectrometer the reflectance of colour patches in two different body parts: shell and forelimb. We found that turtles with a faster growth rate had brighter limb stripes independently of their age. On the other hand, shell colouration was related to body size with larger turtles having brighter shell stripes and higher values of carotenoid chroma. Our results suggest that fast-growers may afford to express intense colourful limb stripes likely due to their higher intake of carotenoids that would modulate both growth and colour expression. However, shell colouration was related to body size probably due to ontogenetic differences in the diet, as juveniles are strictly carnivorous while adults are omnivorous. Alternatively, shell colouration might be involved in crypsis as the shell is visually exposed to predators.     

One trait, many signals: different information on male quality is enclosed within the same trait in a blenny fish

Colourful ornaments are traditionally evaluated as one trait. However, they could consist of several components, such as total size, colour intensity and extension, each possibly bearing its own message about one aspect of quality. Males of the blenny Salaria pavo exhibit a colourful head crest and solely care for eggs. During the breeding season, the head crest shows a yellow colouration, the intensity and relative extension of which are independent of crest size. Here, we show that: (1) carotenoids are responsible for the head crest yellow patch; (2) activating the immune system by injecting the bacterial antigen lipopolysaccharides affects both the intensity and extent of the yellow colouration; and (3) females assess males on the basis of colour patch expression. However, the response of the yellow patch to the immune challenge was dependent on head crest size. Indeed, males with a larger head crest reacted better to the simulated infection, sustaining a level of yellow patch close to pre-challenge size.     

Multimodal sexual signals in male ocellated lizards Lacerta lepida: vitamin E in scent and green coloration may signal male quality in different sensory channels

The mechanisms that confer honesty to multiple sexual signals of vertebrates remain less known. We suggest that vitamin E in the scent (femoral secretions) and carotenoids in coloration of Lacerta lepida lizards might advertise quality because they are relevant in metabolism as major antioxidants and have a dietary origin. Results showed that there may be similar trade-offs between immunity and both chemical and visual signaling, as males with more vitamin E in secretions and those with more greenish, darker, and saturated carotenoid-dependent colorations had a higher immune response. This suggests that only high-quality males can divert from metabolism and allocate enough vitamin E to secretions and enough carotenoids to coloration. Therefore, information provided by visual and chemical signals is congruent. The use of multiple sensory channels may allow signaling a male quality under different circumstances or reinforce the reliability of the signal when both signals are perceived simultaneously. However, we also found that characteristics of carotenoid-dependent coloration mirror the amounts of vitamin E in secretions. This might support that carotenoids, which are not true antioxidants in the organism, would just reflect and “inform” on the actual contents of metabolic antioxidant vitamin E, which is part of the true system that prevent oxidation. We suggest that the metabolic roles of vitamins might be the actual basis of honesty of many sexual displays, and that carotenoid-based signals might be just the visible part of the whole system.     

Carotenoid-dependent coloration of male American kestrels predicts ability to reduce parasitic infections

The signaling function of sexually selected traits, such as carotenoid-dependent avian plumage coloration, has received a great deal of recent attention especially with respect to parasitism and immunocompetence. We argue that parasite-mediated models of sexual selection may have an implicit temporal component that many researchers have ignored. For example, previous studies have demonstrated that carotenoid-dependent traits can signal past parasite exposure, current levels of parasitism, or the ability of individuals to manage parasitic infections in the future. We examined repeated measures of carotenoid-dependent skin color and blood parasitism in American kestrels (Falco sparverius) to distinguish whether coloration might signal current parasitism or the potential to deal with infections in the future. We found no evidence that coloration was related to current levels of parasitism in either sex. However, coloration of males significantly predicted their response to parasitism; males with bright orange coloration during prelaying, when mate choice is occurring, were more likely than dull yellow males to reduce their levels of infection by the time incubation began. Coloration during prelaying may advertise a male’s health later in the breeding season. For kestrels, the ability to predict future health would be highly beneficial given the male’s role in providing food to his mate and offspring. Coloration of females was not a significant predictor of parasitism in the future, and we provide several possible explanations for this result.     

Integument coloration signals reproductive success,heterozygosity, and antioxidant levels in chick-rearing black-legged kittiwakes

Carotenoid pigments are important for immunity and as antioxidants, and carotenoid-based colors are believed to provide honest signals of individual quality. Other colorless but more efficient antioxidants such as vitamins A and E may protect carotenoids from bleaching. Carotenoid-based colors have thus recently been suggested to reflect the concentration of such colorless antioxidants, but this has rarely been tested. Furthermore, although evidence is accruing for multiple genetic criteria for mate choice, carotenoid-based colors have rarely been shown to reflect both phenotypic and genetic quality. In this study, we investigated whether gape, tongue, eye-ring, and bill coloration of chick-rearing black-legged kittiwakes Rissa tridactyla reflected circulating levels of carotenoids and vitamins A and E. We further investigated whether integument coloration reflected phenotypic (body condition and fledging success) and genetic quality (heterozygosity). We found that the coloration of fleshy integuments was correlated with carotenoid and vitamin A levels and fledging success but only in males. Furthermore, the coloration of tongue and eye-ring was correlated with heterozygosity in both males and females. Integument colors might therefore be reliable signals of individual quality used by birds to adjust their parental care during the chick-rearing period.     

Habitat structure is associated with the expression of carotenoid-based coloration in nestling blue tits Parus caeruleus

We investigated how the expression of carotenoid-based plumage coloration (lightness and chroma) in nestling blue tits Parus caeruleus is associated with forest structure in oak forests of central Spain. We found evidence of a reduced expression of carotenoid-based coloration in nestlings growing up in successionally young and structurally simple forest territories. Our results suggest that breast feather coloration can be used as an indicator of nestling quality because nestlings with more intense yellow plumage coloration had larger body size and stronger immune responses to the injection of phytohemagglutinin (PHA). Given the association of forest structural complexity with carotenoid-based plumage coloration, our findings suggest that variation in habitat structure may have a significant impact on forest birds in their first stages of life which has implications for forest management practices.     

Sexually dichromatic coloration reflects size and immunocompetence in female Spanish terrapins, Mauremys leprosa

Many studies have shown the importance of colorful ornamentation in mate choosiness or intrasexual conflict. However, research on color ornaments has focused mainly on birds, lizards or fish, but remains practically unknown in other animal groups such as turtles. In addition, female ornaments and their relation with sexual selection also remain almost unknown. Here, we measured the coloration of the shell and the limb stripes of male and female Spanish terrapins Mauremys leprosa and explored the existence of sexual dichromatism and the relation of color characteristics with body size and health state estimated from the immune response to the injection of an antigen (phytohaemagglutinin test). Our results showed that shell coloration, which could be constrained by natural selection to be cryptic, changed with body size, but did not differ between sexes. In contrast, females had brighter and less ultraviolet-saturated and more orange-saturated limb stripes than males. In females, interindividual variation in limb stripe coloration was related with body size and immune response suggesting that this coloration may inform honestly about multiple traits that could be important in sexual selection. In contrast, coloration of limb stripes of males was duller than in females, and was not related with any trait suggesting that coloration is not important in sexual selection for males.     

Carotenoid-based bill colour is an integrative signal of multiple parasite infection in blackbird

In the study of parasite-mediated sexual selection, there has been controversial evidence for the prediction that brighter males should have fewer parasites. Most of these studies have focused on one parasite species. Our aim was to investigate the expression of carotenoid-based coloured signals in relation to patterns of multiple parasite infections, to determine whether colour reflects parasite load of all parasite species, or whether different relationships might be found when looking at each parasite species independently. We investigated the relationship between bill colour, body mass and plasma carotenoids and parasite load (feather chewing lice, blood parasite Plasmodium sp., intestinal parasites cestodes and coccidia) in the blackbird (Turdus merula). Bill colour on its own appeared to be a poor predictor of parasite load when investigating its relationships with individual parasite species. Variation in parasite intensities at the community level was summarised using principal component analysis to derive synthetic indexes of relative parasite species abundance and absolute parasite load. The relative abundance of parasite species was strongly related to bill colour, plasma carotenoid levels and body mass: birds with relatively more cestodes and chewing lice and relatively less Plasmodium and coccidia had a more colourful bill, circulated more carotenoids and were heavier. These results suggest that bill colour more accurately reflects the relative intensities of parasite infection, rather than one-by-one relationships with parasites or absolute parasite burden. Investigating patterns of multiple parasite infection would thus improve our understanding of the information conveyed by coloured signals on parasite load.     

Optical properties of the uropygial gland secretion: no evidence for UV cosmetics in birds

Ultraviolet (UV) reflectance of the plumage is common in birds and plays an important role in sexual signalling. Recently, it has been proposed that birds are able to modify plumage UV reflectance by the application of uropygial gland secretion. Based on a survey of the optical properties of this secretion from 51 species belonging to 12 avian orders, we show that two main types of uropygial secretions exist, one predominantly found in passerines and one in non-passerines, both reducing relative UV reflectance of a white background (Teflon™ tape). We quantified how each type of secretion (exemplified by blue tit and mallard) affected feather UV reflectance. Both secretions reduced overall brightness and relative UV reflectance of white mallard feathers but hardly affected the reflectance of UV/blue blue tit crown feathers. According to models of avian colour vision, changes in reflectance due to application of the secretion were at or below the discrimination threshold of most birds. We conclude that the uropygial secretion is unlikely to play a major role in modifying plumage UV reflectance. However, the optical properties of the uropygial secretion may have been selected to interfere as little as possible with visual signaling through plumage reflectance. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Detrimental effects of carotenoid pigments: the dark side of bright coloration

Carotenoid pigments produce yellow, orange, and red integumentary color displays that can serve as reliable signals of health and condition. In many birds and fish, individuals gain competitive or mating advantages by ingesting and utilizing large quantities of carotenoid pigments. Carotenoid pigments serve as antioxidants, performing important functions as free-radical scavengers. The beneficial effects of carotenoid pigments are well documented, but rarely have researchers considered potential detrimental effects of high-level accumulation of carotenoids. We maintained American goldfinches (Carduelis tristis) on high- or low-carotenoid diets through molt and tested for damage to the liver and skeletal muscle. High intake of carotenoids had no measurable effect on liver enzymes but caused an increase in creatine kinase, an indicator of skeletal muscle breakdown, and a reduction in vertical flight performance, a measure of skeletal muscle integrity. The detrimental effects of high-level carotenoid accumulation were approximately equivalent to the negative effects of removing carotenoids from the diet. The adverse effects observed in this study have important implications for theories of the function and evolution of colorful plumage.