Environmental Pollution Affects the Plumage Color of Great Tit Nestlings through Carotenoid Availability

Birds need to acquire carotenoids for their feather pigmentation from their diet, which means that their plumage color may change as a consequence of human impact on their environment. For example, the carotenoid-based plumage coloration of Great tit, Parus major, nestlings is associated with the degree of environmental pollution. Breast feathers of birds in territories exposed to heavy metals are less yellow than those in unpolluted environments. Here we tested two hypotheses that could explain the observed pattern: (I) deficiency of carotenoids in diet, and (II) pollution-related changes in transfer of carotenoids to feathers. We manipulated dietary carotenoid levels of nestlings and measured the responses in plumage color and tissue concentrations. Our carotenoid supplementation produced the same response in tissue carotenoid concentrations and plumage color in polluted and unpolluted environments. Variation in heavy metal levels did not explain the variation in tissue (yolk, plasma, and feathers) carotenoid concentrations and was not related to plumage coloration. Instead, the variation in plumage yellowness was associated with the availability of carotenoid-rich caterpillars in territories. Our results support the hypothesis that the primary reason for pollution-related variation in plumage color is carotenoid deficiency in the diet.     

Synchronizing feather-based measures of corticosterone and carotenoid-dependent signals: what relationships do we expect?

Carotenoids produce many of the red, orange and yellow signal traits of birds, and individuals must trade off utilizing carotenoids for physiological processes versus ornamentation. Proximate mechanisms regulating this trade-off are poorly understood, despite their importance for expression of color signals. Corticosterone (CORT) may play a significant mechanistic role in signal expression because it mobilizes energy substrates and influences foraging behavior. We used a unique feather-based approach to test whether CORT mediates expression of carotenoid-based coloration. First, we investigated relationships between levels of CORT from feathers (CORT_f) and carotenoid-based plumage signals in common redpolls (Acanthis flammea). Then, we determined how the width of growth bars and probability of having fault bars on feathers varied with CORT_f, specifically whether these metrics reflected developmental costs of elevated CORT (“stress” hypothesis) or represented an individual’s quality (“quality” hypothesis). CORT_f correlated positively with the strength of carotenoid signals, but only in adult males. However, also in adult males, CORT_f was positively related to width of feather growth bars and negatively with probability of having fault bars, providing support for the quality hypothesis. Overall, CORT_f was lower in adult males than in females or young males, possibly due to dominance patterns. Our results indicate that CORT may indirectly benefit feather quality, potentially by mediating the expression of carotenoid signals. We place our sex-specific findings into a novel framework that proposes that the influences of CORT in mediating carotenoid-based plumage traits will depend on the extent to which carotenoids are traded off between competing functions.     

Melanin-based plumage coloration in the house finch is unaffected by coccidial infection

For most species of birds, ornamental plumage coloration may result from two types of pigments: carotenoids and melanins. Despite the fact that melanin pigments can be synthesized by birds from basic, amino acid precursors, while carotenoids cannot be synthesized by birds and must be ingested, melanin-based plumage coloration and carotenoid-based plumage coloration have often been treated as a single trait in investigations of the function and evolution of plumage coloration. Expression of carotenoid-based coloration is known to be dependent on condition, while the effects of individual condition have not been well-tested for expression of melanin-based coloration. In this study, we experimentally tested the effect of coccidial infection of the intestinal tract of male house finches during moult on expression of melanin-based plumage coloration. Coccidial infection had a significant negative effect on carotenoid-based coloration, but it had no significant effect on melanin-based feather coloration. Unlike carotenoid-based coloration, melanin-based coloration may be cheap to produce, and honesty of melanin-based coloration my require social mediation.     

Plumage yellowness predicts foraging ability in the blue tit Cyanistes caeruleus

Carotenoid‐based coloration in adult birds has been often regarded as an honest signal of individual quality. However, few studies have demonstrated a link between carotenoid display and the quantity or quality of resources provided to the offspring. The present study investigated the expression of a carotenoid‐based ornament, the breast plumage yellowness of the blue tit Cyanistes caeruleus, in relation to the level of parental provisioning effort and the amount of carotenoid‐rich prey provided to the young. The study was conducted in two forest types (evergreen and deciduous), which also allowed an exploration of the possible existence of habitat effects on the coloration of breeding birds. It was found that plumage colour intensity (carotenoid chroma) correlated positively with nestling provisioning rates of both males and females, supporting the good parent hypothesis. In addition, carotenoid chroma was positively related with the proportion of Lepidoptera larvae brought to the nest in both sexes. Female but not male coloration was positively linked to breeding success (proportion of fledged young). Nestling coloration did not correlate with that of their parents, nor the frequency with which they were fed. Hue and lightness of nestling's plumage correlated positively with body mass and tarsus length, respectively. The results obtained in the present study indicate that ventral plumage coloration in blue tits may advertise the ingested carotenoids (carotenoid foraging ability) and also their overall parental quality in terms of nestling provisioning rates. This suggests that plumage yellowness can be used as an indicator of foraging ability in this species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 418–429.     

Dietary carotenoids predict plumage coloration in wild house finches

Carotenoid pigments are a widespread source of ornamental coloration in vertebrates and expression of carotenoid-based colour displays has been shown to serve as an important criterion in female mate choice in birds and fishes. Unlike other integumentary pigments, carotenoids cannot be synthesized; they must be ingested. Carotenoid-based coloration is condition-dependent and has been shown to be affected by both parasites and nutritional condition. A controversial hypothesis is that the expression of carotenoid-based coloration in wild vertebrates is also affected by the amount and types of carotenoid pigments that are ingested. We tested this carotenoid-limitation hypothesis by sampling the gut contents of moulting house finches and comparing the concentration of carotenoid pigments in their gut contents with the colour of growing feathers. We found a positive association: males that ingested food with a higher concentration of carotenoid pigments grew brighter ornamental plumage. We also compared the concentration of carotenoids in the gut contents of males from two subspecies of house finches with small and large patches of carotenoid-based coloration. Consistent with the hypothesis that carotenoid access drives the evolution of carotenoid-based colour displays, males from the population with limited ornamentation had much lower concentrations of carotenoids in their gut contents than males from the population with extensive ornamentation. These observations support the idea that carotenoid intake plays a part in determining the plumage brightness of male house finches.     

The influence of carotenoid acquisition and utilization on the maintenance of species-typical plumage pigmentation in male American goldfinches (Carduelis tristis) and northern cardinals (Cardinalis cardinalis).

Birds display a tremendous variety of carotenoid-based colors in their plumage, but the mechanisms underlying interspecific variability in carotenoid pigmentation remain poorly understood. Because vertebrates cannot synthesize carotenoids de novo, access to pigments in the diet is one proximate factor that may shape species differences in carotenoid-based plumage coloration. However, some birds metabolize ingested carotenoids and deposit pigments that differ in color from their dietary precursors, indicating that metabolic capabilities may also contribute to the diversity of plumage colors we see in nature. In this study, we investigated how the acquisition and utilization of carotenoids influence the maintenance of species-typical plumage pigmentation in male American goldfinches (Carduelis tristis) and northern cardinals (Cardinalis cardinalis). We supplemented the diet of captive goldfinches with red carotenoids to determine whether males, which are typically yellow in color, were capable of growing red plumage. We also deprived cardinals of red dietary pigments to determine whether they could manufacture red carotenoids from yellow precursors to grow species-typical red plumage. We found that American goldfinches were able to deposit novel pigments in their plumage and develop a striking orange appearance. Thus, dietary access to pigments plays a role in determining the degree to which goldfinches express carotenoid-based plumage coloration. We also found that northern cardinals grew pale red feathers in the absence of red dietary pigments, indicating that their ability to metabolize yellow carotenoids in the diet contributes to the bright red plumage that they display.     

Changes in carotenoid‐based plumage colour in relation to age in European Serins Serinus serinus

Yearling birds generally display duller colours than adults. This may be due to selection favouring birds with more intensely coloured plumage or to an increase in colour after the first complete moult. Most research to date on the topic has been carried out on species with structural plumage coloration or with carotenoid‐based coloration that is produced by the unmodified deposition of pigments. However, no study has been carried out on species whose carotenoids are metabolically modified before deposition. In this study, we assess age‐related changes in the carotenoid‐based coloration of European Serins, a species that metabolically processes carotenoids before they can be deposited into feathers. Birds were captured over consecutive years and we carried out both cross‐sectional and longitudinal analysis. Adults had significantly greater values of lightness and chroma than yearling birds. However, there were no changes in plumage colour when analysing the same individuals captured in subsequent seasons. Plumage lightness and chroma of adult males after moult were related to body mass, suggesting a role of body condition on plumage coloration. Our results suggest that changes in plumage coloration with age in European Serins are due to a selection process that favours more intensely coloured individuals.     

Carotenoid-based coloration correlates with the hatching date of Blue Tit Cyanistes caeruleus nestlings

Carotenoid-based coloration occurs predominantly in adult birds, yet in some species from the family Paridae, this trait is also present at the nestling stage. One of the factors proposed to affect the expression of this trait in immature birds is hatching date. Here, using the avian tetrahedral colour space model, we examined the influence of hatching date on the breast carotenoid-based plumage coloration of the Blue Tit Cyanistes caeruleus nestlings. Because Blue Tits are sexually dichromatic, we also investigated the potential interaction between hatching date and sex that could arise from differences in condition dependence of this trait between males and females. We found a positive relationship between UV chroma of breast feathers and hatching date. The amount of UV reflectance is thought to be negatively related to carotenoid content in feathers. The observed increase of UV chroma through the breeding season might therefore be caused by a seasonal decline in the availability and quality of Lepidoptera larvae – the main source of carotenoids in food of the Tits. We also observed a sex difference in the relationship between brightness of breast feathers (achromatic, structural component) and hatching date, which in males was negative and in females not significant. Our study provides further evidence that the timing of breeding is related to the expression of nestling carotenoid-based coloration, a potentially meaningful element of offspring–parent communication, and suggests a sex-specific effect of hatching date on its structural component.     

Preen waxes do not protect carotenoid plumage from bleaching by sunlight

The plumage coloration of wild birds often changes during the breeding season. One of the possible reasons for this is that sunlight, and particularly ultraviolet (UV) wavelengths, degrades the pigments responsible for plumage coloration. It has been suggested that birds may apply preen wax to feathers to protect feathers from bleaching. This hypothesis is tested by exposing carotenoid-based breast feathers of Great Tits to ambient light, light filtered to exclude UV and darkness. Preen waxes were experimentally removed from feather samples and the effect of light on coloration of treatment and control feathers compared. Ambient light had an effect on feather colour but preen wax did not. Feathers exposed to sun gradually became less saturated and hues shifted towards shorter wavelengths. This was not apparent in control feathers kept in darkness. Feathers exposed to full-spectra sunlight faded more than those that were kept in light with UV wavelengths removed. There was a decrease in brightness of feathers in both experimental and control groups, which was assumed to be an effect of dirt accumulation. This experiment confirmed earlier suspicions regarding the detrimental effects of UV irradiation on carotenoid-based coloration of avian feathers but failed to show any protective function of preen waxes. The possible consequences of these mechanisms of colour change for birds with regard to mating strategies are discussed.     

Color expression in experimentally regrown feathers of an overwintering migratory bird: implications for signaling and seasonal interactions

Plumage coloration in birds plays a critical role in communication and can be under selection throughout the annual cycle as a sexual and social signal. However, for migratory birds, little is known about the acquisition and maintenance of colorful plumage during the nonbreeding period. Winter habitat could influence the quality of colorful plumage, ultimately carrying over to influence sexual selection and social interactions during the breeding period. In addition to the annual growth of colorful feathers, feather loss from agonistic interactions or predator avoidance could require birds to replace colorful feathers in winter or experience plumage degradation. We hypothesized that conditions on the wintering grounds of migratory birds influence the quality of colorful plumage. We predicted that the quality of American redstart (Setophaga ruticilla) tail feathers regrown after experimental removal in Jamaica, West Indies, would be positively associated with habitat quality, body condition, and testosterone. Both yearling (SY) and adult (ASY) males regrew feathers with lower red chroma, suggesting reduced carotenoid content. While we did not observe a change in hue in ASY males, SY males shifted from yellow to orange plumage resembling experimentally regrown ASY feathers. We did not observe any effects of habitat, testosterone, or mass change. Our results demonstrate that redstarts are limited in their ability to adequately replace colorful plumage, regardless of habitat, in winter. Thus, feather loss on the nonbreeding grounds can affect social signals, potentially negatively carrying over to the breeding period.     

Habitat structure and prey composition generate contrasting effects on carotenoid‐based coloration of great tit Parus major nestlings

Carotenoid‐based coloration of nestling plumage is generally considered a reliable signal of quality and has consistently been related to habitat structure. The main hypothesis proposed to explain this correlation is that high quality habitats contain high quality food, which in return affects the expression of carotenoid‐based plumage. It therefore assumes that, at the population level, the link between habitat structure and food composition is consistent and more relevant than inter‐individual differences in foraging ability or parental investment. In addition, it is assumed by default that food and habitat produce concordant effects on nestling coloration. In this work we evaluated habitat structure and prey composition in addition to several measures of parental investment. We investigated their relative effect on carotenoid‐based plumage coloration (lightness, chroma and hue) of great tit Parus major nestlings. We found a low correlation between carotenoid‐based coloration of nestlings and that of their parents. Nestling coloration, especially lightness and chroma, increased with the intake of more spiders. The time of breeding was positively correlated with lightness and chroma and negatively correlated with hue. Finally, the maturity of oak trees surrounding nest‐boxes correlated negatively with lightness, and the size of all tree species surrounding nest‐boxes correlated positively with hue of chick plumage. Our findings support the view that habitat structure and prey composition may produce divergent effects on feather pigmentation, and that prey proportions and variables related to parental investment should be assessed when considering carotenoid‐based coloration of chicks. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 547–555.     

Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny

Birds show striking interspecific variation in their use of carotenoid-based coloration. Theory predicts that the use of carotenoids for coloration is closely associated with the availability of carotenoids in the diet but, although this prediction has been supported in single-species studies and those using small numbers of closely related species, there have been no broad-scale quantitative tests of the link between carotenoid coloration and diet. Here we test for such a link using modern comparative methods, a database on 140 families of birds and two alternative avian phylogenies. We show that carotenoid pigmentation is more common in the bare parts (legs, bill and skin) than in plumage, and that yellow coloration is more common than red. We also show that there is no simple, general association between the availability of carotenoids in the diet and the overall use of carotenoid-based coloration. However, when we look at plumage coloration separately from bare part coloration, we find there is a robust and significant association between diet and plumage coloration, but not between diet and bare part coloration. Similarly, when we look at yellow and red plumage colours separately, we find that the association between diet and coloration is typically stronger for red coloration than it is for yellow coloration. Finally, when we build multivariate models to explain variation in each type of carotenoid-based coloration we find that a variety of life history and ecological factors are associated with different aspects of coloration, with dietary carotenoids only being a consistent significant factor in the case of variation in plumage. All of these results remain qualitatively unchanged irrespective of the phylogeny used in the analyses, although in some cases the precise life history and ecological variables included in the multivariate models do vary. Taken together, these results indicate that the predicted link between carotenoid coloration and diet is idiosyncratic rather than general, being strongest with respect to plumage colours and weakest for bare part coloration. We therefore suggest that, although the carotenoid-based bird plumage may a good model for diet-mediated signalling, the use of carotenoids in bare part pigmentation may have a very different functional basis and may be more strongly influenced by genetic and physiological mechanisms, which currently remain relatively understudied.     

Energetic constraints on expression of carotenoid-based plumage coloration

Carotenoid pigments are used by many bird species as feather colorants, creating brilliant yellow, orange, and red plumage displays. Such carotenoid-based plumage coloration has been shown to function as an honest signal that is used in female mate choice. Despite recent interest in carotenoid-based ornamental traits, the basis for individual variation in expression of carotenoid-based plumage coloration remains incompletely understood. I tested the hypothesis that, independent of carotenoid access, food stress during molt would cause reduced expression of carotenoid pigmentation. I fed molting male House Finches Carpodacus mexicanus seed diets supplemented with either the red carotenoid pigment canthaxanthin or the yellow/orange carotenoid pigment β-cryptoxanthin (in the form of tangerine juice). Within each diet treatment, one group of males was given restricted food access and the other group was given unrestricted food access. Carotenoid supplements were placed in water so carotenoid access was controlled independent of food access. The results indicated a strong effect of both carotenoid access and food access on color display. Some males in the β-cryptoxanthin-supplemented group grew red plumage, suggesting that they can metabolically modify yellow pigments into red pigments, but no bird supplemented with β-cryptoxanthin grew plumage as red as birds supplemented with canthaxanthin. Males in the unrestricted food groups grew redder and more intensely pigmented plumage than males in the restricted food groups. These observations provide the best evidence to date of an energetic cost of carotenoid utilization in the generation of colorful plumage.     

Season-, sex-, and age-specific accumulation of plasma carotenoid pigments in free-ranging white-winged crossbills Loxia leucoptera

Many birds acquire carotenoid pigments from foods and deposit these pigments into feathers and bare‐parts to become sexually attractive, but little work has been done on the interindividual and temporal variability in the types and amounts of carotenoids that free‐ranging individuals have available for use in coloration or other functions (e.g., in immunomodulation). To address this issue, we studied intra‐annual variation in plasma carotenoid profiles of juvenile and adult white‐winged crossbills Loxia leucoptera of both sexes. Adult male crossbills exhibit bright red carotenoid‐based plumage pigmentation, whereas females uniformly display drab yellow feather coloration and juvenile males only occasionally display some orange or pink color. Yellow xanthophylls (e.g., lutein, zeaxanthin) were predominant in plasma of birds from both sexes and age classes throughout the year. Plasma xanthophylls levels tended to be highest in the summer, when crossbills increase seed consumption for breeding as well as supplement their diet with insects. Blood accumulation of three other, less common plasma carotenoids‐β‐cryptoxanthin, rubixanthin, and gazaniaxanthin‐varied in a highly season‐, sex‐, and age‐dependent fashion. These carotenoids were virtually absent in juvenile or adult female plasma at all times of year and were only present in male plasma, at higher concentrations in adults than juveniles, during the period of feather growth (Sept.–Nov.). These pigments have been reported as valuable precursors of the metabolically derived red pigments (e.g., 3‐hydroxy‐echinenone, 4‐oxo‐rubixanthin, and 4‐oxo‐gazaniaxanthin, respectively) that appear in the plumage of male crossbills. These findings suggest that male crossbills either adopt a season‐specific foraging strategy to acquire foods rich in these pigments at the time they are needed to develop red coloration, or have a unique physiological ability to metabolically produce these pigments or absorb them from food during molt, in order to maximize color production.     

The effect of dietary carotenoid access on sexual dichromatism and plumage pigment composition in the American goldfinch

We investigated potential dietary and biochemical bases for carotenoid-based sexual dichromatism in American goldfinches (Carduelis tristis). Captive male and female finches were given access to the same type and amount of carotenoid pigments in the diet during their nuptial molt to assess differences in the degree to which the two sexes incorporated ingested pigments into their plumage. When birds were fed a uniform, plain-seed diet, or one that was supplemented with the red carotenoid canthaxanthin, we found that males grew more colorful plumage than females. HPLC analyses of feather pigments revealed that male finches incorporated a higher concentration of carotenoids into their pigmented feathers than females. Compared to females, males also deposited significantly more canary xanthophyll B into feathers when fed a plain-seed diet and a greater concentration and proportion of canthaxanthin when fed a carotenoid-supplemented diet. These results indicate that sex-specific expression of carotenoid pigmentation in American goldfinches may be affected by the means by which males and females physiologically utilize (e.g. absorb, transport, metabolize, deposit) carotenoid pigments available to them in the diet.     

The effects of diet quality and quantity on plumage colour and growth of great tit Parus major nestlings: a food manipulation experiment along a pollution gradient

The yellow carotenoid-based plumage coloration of great tit Parus major nestlings is found to be paler in polluted and urban environments. Because carotenoid pigmentation is often considered to be a condition dependent trait in birds we wanted to find out whether food-limitation and poor nestling condition could explain the pale plumage colour in a polluted area. P. major nestlings were supplemented with variable diets along a well known heavy metal pollution gradient around a copper smelter: two food treatments with carotenoids, one food treatment with little carotenoid and one unsupplemented control. Our field experiment showed that nestlings in the polluted area grew better with carotenoid rich diets, while such effect was not found in the unpolluted area. Nestlings showed higher plasma carotenoid (lutein) levels and higher plumage carotenoid chroma values in the unpolluted area than in the polluted area. However, plasma lutein levels or plumage colour were not associated with heavy metal levels in nestling faeces (a proxy for dietary exposure). Our results provide only weak evidence for carotenoid-based colouration to be condition-dependent in great tit nestlings as we found a positive relationship between body mass and carotenoid chroma in the non-supplemented control group only. The positive relationship between body mass and plumage colour intensity is more likely to be produced by the fact that good availability of caterpillars, an important food source for P. major, also means a good availability of carotenoids to nestlings. Our results suggest that main reason for pale nestling plumage in the polluted area is lower quality invertebrate food, and not nutrition-related oxidative stress.     

Variation in melanin pigmentation of a sexually selected plumage trait and its adaptive value in the Common Snipe Gallinago gallinago

There is increasing evidence that melanin‐based plumage coloration correlates with different components of fitness and that it may act as a social or sexual signal of individual quality. We analysed variation in melanin pigmentation in the outermost tail feathers of the Common Snipe Gallinago gallinago. During courtship flights, male Snipe use their outermost tail feathers to generate a drumming sound, which plays a role in territory establishment and mate choice. As the outermost tail feathers are displayed to females during these flights, we predicted that conspicuous variation in their rusty‐brown (pheomelanin‐based) coloration may act as an honest signal of individual quality. To test this prediction, we spectrophotometrically measured brightness (an indicator of total melanin content) and red chroma (an indicator of pheomelanin content) of the outermost tail feathers in 180 juvenile and adult Common Snipe. An age‐related decline in feather brightness was found exclusively in females, suggesting that melanization could have evolved by natural selection to camouflage incubating birds. In both sexes, brightness of the tail feathers was inversely correlated with their structural quality (as measured with mass–length residuals), suggesting that melanization could increase mechanical properties of feathers and, in males, enhance the quality of courtship sonation. Red chroma positively correlated with total plasma protein concentration, supporting our prediction that pheomelanin pigmentation of tail feathers may act as an honest signal of condition. Our study indicated that variation in the melanin‐based coloration of the outermost tail feathers in the Common Snipe could have evolved as a result of several different selection pressures and it emphasizes the complexity of the processes that underlie the evolution of melanin‐based plumage coloration in birds.     

The color of greater flamingo feathers fades when no cosmetics are applied

Greater flamingos use cosmetic coloration by spreading uropygial secretions pigmented with carotenoids over their feathers, which makes the plumage redder. Because flamingos inhabit open environments that receive direct solar radiation during daytime, and carotenoids bleach when exposed to solar radiation, we expected that the plumage color would fade if there is no maintenance for cosmetic purposes. Here, we show that the concentrations of pigments inside feathers and on the surface of feathers were correlated, as well as that there was a correlation between the concentrations of pigments in the uropygial secretions and on the surface of feathers. There was fading in color (becoming less red) in feathers that received direct solar radiation when there was no plumage maintenance, but not so in others maintained in darkness. When we controlled for the initial color of feathers, the feathers of those individuals with higher concentration of pigments on the feather surfaces were those that lost less coloration after experimental exposure of feathers to sunny conditions. These results indicate that exposure to sunlight is correlated with the fading of feather color, which suggests that individuals need to regularly apply makeup to be more colorful. These results also reinforce the view that these birds use cosmetic coloration as a signal amplifier of plumage color. This may be important in species using highly variable habitats, such as wetlands, since the conditions experienced when molting may differ from those when the signal should be functional, usually months after molting.     

Astaxanthin is responsible for the pink plumage flush in Franklin's and Ring-billed gulls

ABSTRACT.   Carotenoid pigments produce the red, orange, and yellow plumage of many birds. Carotenoid-containing feathers are typically rich in color and displayed by all adult members of the species. In many gulls and terns, however, an unusual light pink coloring (or flush) to the normally white plumage can be found in highly variable proportions within and across populations. The carotenoid basis of plumage flush was determined in an Elegant Tern ( Sterna elegans ; Hudon and Brush 1990 ), but it is not clear if all larids use this same mechanism for pink plumage coloration. We examined the carotenoid content of pink feathers in Franklin's ( Larus pipixcan ) and Ring-billed ( Larus delawarensis ) gulls and found that a single carotenoid—astaxanthin—was present. Astaxanthin was primarily responsible for the flush in Elegant Terns as well, but was accompanied by other carotenoids (e.g., canthaxanthin and zeaxanthin), as is typical of most astaxanthin-containing bird feathers. In both gull and tern species, carotenoids were contained within feathers and did not occur on the plumage surface in preen oil, as some have previously speculated. We hypothesize that some gulls turn pink because they acquire unusually high amounts of astaxanthin in their diets at the time of feather growth. It is tempting to link the increase in sightings of pink Ring-billed Gulls since the late 1990s with the introduction of pure, synthetic astaxanthin to the diets of hatchery-raised salmon.     

Ancient origins and multiple appearances of carotenoid-pigmented feathers in birds

The broad palette of feather colours displayed by birds serves diverse biological functions, including communication and camouflage. Fossil feathers provide evidence that some avian colours, like black and brown melanins, have existed for at least 160 million years (Myr), but no traces of bright carotenoid pigments in ancient feathers have been reported. Insight into the evolutionary history of plumage carotenoids may instead be gained from living species. We visually surveyed modern birds for carotenoid-consistent plumage colours (present in 2956 of 9993 species). We then used high-performance liquid chromatography and Raman spectroscopy to chemically assess the family-level distribution of plumage carotenoids, confirming their presence in 95 of 236 extant bird families (only 36 family-level occurrences had been confirmed previously). Using our data for all modern birds, we modelled the evolutionary history of carotenoid-consistent plumage colours on recent supertrees. Results support multiple independent origins of carotenoid plumage pigmentation in 13 orders, including six orders without previous reports of plumage carotenoids. Based on time calibrations from the supertree, the number of avian families displaying plumage carotenoids increased throughout the Cenozoic, and most plumage carotenoid originations occurred after the Miocene Epoch (23 Myr). The earliest origination of plumage carotenoids was reconstructed within Passeriformes, during the Palaeocene Epoch (66–56 Myr), and not at the base of crown-lineage birds.