Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test

Many male birds use carotenoid pigments to acquire brilliant colors that advertise their health and condition to prospective mates. The direct means by which the most colorful males achieve superior health has been debated, however. One hypothesis, based on studies of carotenoids as antioxidants in humans and other animals, is that carotenoids directly boost the immune system of colorful birds. We studied the relationship between carotenoid pigments, immune function, and sexual coloration in zebra finches (Taeniopygia guttata), a species in which males incorporate carotenoid pigments into their beak to attract mates. We tested the hypotheses that increased dietary carotenoid intake enhances immunocompetence in male zebra finches and that levels of carotenoids circulating in blood, which also determine beak coloration, directly predict the immune response of individuals. We experimentally supplemented captive finches with two common dietary carotenoid pigments (lutein and zeaxanthin) and measured cell-mediated and humoral immunity a month later. Supplemented males showed elevated blood-carotenoid levels, brighter beak coloration, and increased cell-mediated and humoral immune responses than did controls. Cell-mediated responses were predicted directly by changes in beak color and plasma carotenoid concentration of individual birds. These experimental findings suggest that carotenoid-based color signals in birds may directly signal male health via the immunostimulatory action of ingested and circulated carotenoid pigments.     

Carotenoids bolster immunity during moult in a wild songbird with sexually selected plumage coloration

Carotenoid‐based colours in animals are valuable models for testing theories of sexual selection and life‐history trade‐offs because the pigments used in coloration are chemically tractable in the diet and in the body, where they serve multiple purposes (e.g. health enhancement, photoprotection). An important assumption underlying the hypothesized signalling value of carotenoid coloration is that there is a trade‐off in carotenoid pigment allocation, such that not all individuals can meet the physiological/morphological demands for carotenoids (i.e. carotenoids are limited) and that only those who have abundant supplies or fewer demands become the most colourful. Studies of carotenoid trade‐offs in colourful animals have been limited largely to domesticated species, which may have undergone artificial selection that changed the historical/natural immunomodulatory roles of carotenoids, to young animals lacking carotenoid‐based signals or to species displaying carotenoid‐based skin and bare parts. We studied the health benefits of carotenoids during moult in house finches (Carpodacus mexicanus), which display sexually selected, carotenoid‐based plumage coloration. We manipulated dietary carotenoid availability during both winter (nonmoult) and autumn (moult) in captive males and females and found that carotenoid‐supplemented birds mounted stronger immune responses (to phytohemagglutinin injection and to a bacterial inoculation in blood) than control birds only during moult. This study provides experimental, seasonal support for a fundamental tenet of Lozano's ‘carotenoid trade‐off’ hypothesis and adds to a growing list of animal species that benefit immunologically from ingesting higher dietary carotenoid levels. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 560–572.     

Interspecific variation in dietary carotenoid assimilation in birds: links to phylogeny and color ornamentation

Many birds use carotenoid pigments to acquire rich red, orange, and yellow coloration in feathers and bare parts that is used as a signal of mate quality. Because carotenoids are derived from foods, much attention has been paid to the role of diet in generating color variation both within and among avian species. Less consideration has been given to physiological underpinnings of color variability, especially among species. Here, I surveyed published literature (e.g. captive feeding studies) on carotenoid assimilation in six bird species and completed additional controlled carotenoid-supplementation experiments in two others to consider the ability of different taxa to extract carotenoids from the diet in relation to phylogeny and coloration. I found that, for a given level of carotenoids in the diet, passerine birds (zebra finch, Taeniopygia guttata; house finch, Carpodacus mexicanus; American goldfinch, Carduelis tristis; society finch, Lonchura domestica) exhibit higher levels of carotenoids in circulation than non-passerines like gamebirds (domestic chicken, Gallus domesticus; red junglefowl, Gallus gallus; Japanese quail, Coturnix coturnix; red-legged partridge, Alectoris rufa). This difference in carotenoid accumulation is likely due to interspecific variation in micelle, chylomicron, or lipoprotein concentrations or affinities for xanthophyll carotenoids. Passerine birds more commonly develop carotenoid-based colors than do birds from ancient avian lineages such as Galliformes, and the physiological differences I uncover may explain why songbirds especially capitalize on carotenoid pigments for color production. Ultimately, because we can deconstruct color traits into component biochemical, physical, and physiological parts, avian color signals may serve as a valuable model for illuminating the proximate mechanisms behind interspecific variation in signal use in animals.     

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.     

Carotenoid limitation and allocation priorities in asynchronous raptor nestlings

The evolution and maintenance of conspicuous animal traits and communication signals have long fascinated biologists. Many yellow–red conspicuous traits are coloured by carotenoid pigments, and in some species they are displayed at a very young age. In nestling birds, the functions and proximate mechanisms of carotenoid‐pigmented traits are probably different and not as well known as those of adults. Here we investigated how Montagu's harrier (Circus pygargus) nestlings within structured families used a limited resource, carotenoid pigments, and whether they used these for increasing coloration (deposition in integuments) or for mounting a response to a phytohaemagglutinin (PHA) challenge, which measures pro‐inflammatory potential and aspects of cellular immune responsiveness. We manipulated carotenoid availability, using dietary carotenoid supplementations, and show that when supplemented, nestlings primarily allocated supplemental carotenoids to increase their coloration, irrespective of their sex, but depending of their position within the brood. Responses to PHA challenge were condition‐dependent, but depending on carotenoid availability. Moreover, how nestlings allocated carotenoids depended on their rank within the brood, which in turn influenced their level of carotenoid limitation (first‐hatched nestlings being less constrained than later‐hatched nestlings). We discuss why nestlings would use supplemental carotenoids for increasing bare parts coloration rather than for responding to a PHA challenge, and the potential benefits for doing so in a parent–offspring communication context. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 13–24.     

Do carotenoids buffer testosterone-induced immunosuppression? An experimental test in a colourful songbird

Testosterone (T) is hypothesized to be an important honesty reinforcer of animal sexual signals. Owing to its immunosuppressive effects, only those individuals that can immunologically withstand high T levels can develop the most exaggerated traits. To date, few studies have isolated phenotypic or genotypic buffers that provide 'high-quality' animals with such an advantage. Dietary carotenoid pigments may in fact confer such a benefit because when in high supply carotenoids boost immunocompetence and coloration in animals like birds and fishes. We examined the experimental effect of T elevation on carotenoid and immune status in male and female zebra finches (Taeniopygia guttata) and found that T was immunostimulatory in a generalized cell-mediated challenge. We also detected a significant interaction between T treatment and the change in plasma carotenoids that occurred during the immune challenge; the relationship between blood carotenoid change and immunity was positive in controls and negative in T-implanted birds. This suggests that, while correlationally birds with high carotenoid stores were inherently better at mounting strong immune responses, experimentally administered T induced birds to deplete carotenoids for maximizing their health. Our findings highlight a nutrient-specific mechanism by which animals escape high immune costs of T elevation and thus can still elevate ornamentation.     

Anhydrolutein in the zebra finch: a new,metabolically derived carotenoid in birds

Many birds acquire carotenoid pigments from the diet that they deposit into feathers and bare parts to develop extravagant sexual coloration. Although biologists have shown interest in both the mechanisms and function of these colorful displays, the carotenoids ingested and processed by these birds are poorly described. Here we document the carotenoid-pigment profile in the diet, blood and tissue of captive male and female zebra finches (Taeniopygia guttata). Dietary carotenoids including: lutein; zeaxanthin; and β-cryptoxanthin were also present in the plasma, liver, adipose tissue and egg-yolk. These were accompanied in the blood and tissues by a fourth pigment, 2′,3′-anhydrolutein, that was absent from the diet. To our knowledge, this is the first reported documentation of anhydrolutein in any avian species; among animals, it has been previously described only in human skin and serum and in fish liver. We also identified anhydrolutein in the plasma of two closely related estrildid finch species (Estrilda astrild and Sporaeginthus subflavus). Anhydrolutein was the major carotenoid found in zebra finch serum and liver, but did not exceed the concentration of lutein and zeaxanthin in adipose tissue or egg yolk. Whereas the percent composition of zeaxanthin and β-cryptoxanthin were similar between diet and plasma, lutein was comparatively less abundant in plasma than in the diet. Lutein also was proportionally deficient in plasma from birds that circulated a higher percentage of anhydrolutein. These results suggest that zebra finches metabolically derive anhydrolutein from dietary sources of lutein. The production site and physiological function of anhydrolutein have yet to be determined.     

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.     

Food Color Preferences of Molting House Finches (Carpodacus mexicanus) in Relation to Sex and Plumage Coloration

Food color can be indicative of specific nutrients, and thus discrimination based on color can be a valuable foraging behavior. Several bird and fish species with carotenoid-based body ornamentation show color preferences for presumably carotenoid-rich red and orange foods. However, little is known within species about whether or not individuals with (or growing) more colorful ornaments show stronger food-color preferences than those with drabber coloration. Here, we examine food color preferences in house finches ( Carpodacus mexicanus ) – a species with sexually dichromatic and selected carotenoid coloration – as a function of sex and plumage coloration during molt. We captured wild, molting juvenile house finches over 4 wk in late summer/early fall, quantified the color and size of plumage ornaments being developed in males, and determined food color preference in captivity by presenting individuals with dyed sunflower chips (red, orange, yellow, and green). On average, finches showed an aversion to yellow-dyed chips and a preference for red- and green-colored chips. We found no significant difference between male and female preferences for specific food colors, and food color preference was not significantly related to male plumage ornamentation. However, we did find that redder birds demonstrated a higher degree of food selectivity, measured as the proportion of their preferred food color consumed. These results suggest that food color is not a major factor determining food choice in molting house finches, but that there still may be aspects of foraging behavior that are linked to the development of colorful plumage.     

Differential accumulation and pigmenting ability of dietary carotenoids in colorful finches

Many animals develop bright red, orange, or yellow carotenoid pigmentation that they use to attract mates. Colorful carotenoid pigments are acquired from the diet and are either directly incorporated as integumentary colorants or metabolized into other forms before deposition. Because animals often obtain several different carotenoids from plant and animal food sources, it is possible that these pigments are accumulated at different levels in the body and may play unique roles in shaping the ultimate color expression of individuals. We studied patterns of carotenoid accumulation and integumentary pigmentation in two colorful finch species--the American goldfinch (Carduelis tristis) and the zebra finch (Taeniopygia guttata). Both species acquire two main hydroxycarotenoids, lutein and zeaxanthin, from their seed diet but transform these into a series of metabolites that are used as colorful pigments in the plumage (goldfinches only) and beak (both species). We conducted a series of carotenoid-supplementation experiments to investigate the relative extent to which lutein and zeaxanthin are accumulated in blood and increase carotenoid coloration in feathers and bare parts. First, we supplemented the diets of both species with either lutein or zeaxanthin and measured plasma pigment status, feather carotenoid concentration (goldfinches only), and integumentary color. Zeaxanthin-supplemented males grew more colorful feathers and beaks than lutein-supplemented males, and in goldfinches incorporated a different ratio of carotenoids in feathers (favoring the accumulation of canary xanthophyll B). We also fed goldfinches different concentrations of a standard lutein-zeaxanthin mix and found that at physiologically normal and high concentrations, birds circulated proportionally more zeaxanthin over lutein than occurred in the diet. Collectively, these results demonstrate that zeaxanthin is preferentially accumulated in the body and serves as a more potent substrate for pigmentation than lutein in these finches.     

Ketocarotenoid circulation,but not retinal carotenoid accumulation,is linked to eye disease status in a wild songbird

Pathogenic or parasitic infections pose numerous physiological challenges to organisms. Carotenoid pigments have often been used as biomarkers of disease state and impact because they integrate multiple aspects of an individual’s condition and nutritional and health state. Some diseases are known to influence carotenoid uptake from food (e.g. coccidiosis) and carotenoid use (e.g. as antioxidants/immunostimulants in the body, or for sexually attractive coloration), but there is relatively little information in animals about how different types of carotenoids from different tissue sources may be affected by disease. Here we tracked carotenoid accumulation in two body pools (retina and plasma) as a function of disease state in free-ranging house finches (Haemorhous mexicanus). House finches in eastern North America can contract mycoplasmal conjunctivitis (Mycoplasma gallisepticum, or MG), which can progress from eye swelling to eye closure and death. Previous work showed that systemic immune challenges in house finches lower carotenoid levels in retina, where they act as photoprotectors and visual filters. We assessed carotenoid levels during the molt period, a time of year when finches uniquely metabolize ketocarotenoids (e.g. 3-hydroxy-echinenone) for acquisition of sexually selected red plumage coloration, and found that males infected with MG circulated significantly lower levels of 3-hydroxy-echinenone, but no other plasma carotenoid types, than birds exhibiting no MG symptoms. This result uncovers a key biochemical mechanism for the documented detrimental effect of MG on plumage redness in H. mexicanus. In contrast, we failed to find a relationship between MG infection status and retinal carotenoid concentrations. Thus, we reveal differential effects of an infectious eye disease on carotenoid types and tissue pools in a wild songbird. At least compared to retinal sources (which appear somewhat more temporally stable than other body carotenoid pools, even to diseases of the eye evidently), our results point to either a high physiological cost of ketocarotenoid synthesis (as is argued in models of sexually selected carotenoid coloration) or high benefit of using this ketocarotenoid to combat infection.     

Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi-factorial study

Carotenoid-based skin colorations vary seasonally in many bird species and are thought to be honest sexually selected signals. In order to provide more insight in the potential signal function and underlying mechanisms of such colorations we here quantified patterns of variation of leg coloration in adult male and female Eurasian kestrels (Falco tinnunculus tinnunculus) over the breeding season, and evaluated the relationship between coloration and levels of carotenoids, androgens and estrogens, oxidative damage and plasma non-enzymatic antioxidant capacity. We studied both reproducing wild and non-reproducing captive birds to test for the effect of diet and breeding effort. Males were more colored than females only during mating, and independently of diet, suggesting that leg-color is a sexually selected trait. Seasonal variation in leg color was associated with circulating carotenoids, but concentrations of these molecules were not related to antioxidant capacity, body condition or oxidative damage. These results indicate that carotenoid-based colorations may not be an honest signal of health status in this species. Production of carotenoid rich eggs coincided with low levels of circulating carotenoids in females, indicating that carotenoids might be a limited resource for laying female kestrels. Finally, young rearing males had higher levels of oxidative damage than females, and wild birds of both sexes had higher levels of these parameters than captive birds. These results may indicate that parental effort and physical activity are costly, independently from hormonal status. Since androgens did not explain carotenoid variation we suggest that multiple interacting factors can regulate carotenoid levels along the season.     

Carotenoid and protein supplementation have differential effects on pheasant ornamentation and immunity

A currently popular hypothesis states that the expression of carotenoid-dependent sexual ornaments and immune function may be correlated because both traits are positively affected by carotenoids. However, such a correlation may arise for another reason: it is well known that immune function is dependent on nutritional condition. A recent study has suggested that the expression of ornaments may too depend on nutritional condition, as males in good nutritional condition are better at assimilating and/or modulating carotenoids. Thus, carotenoid-dependent ornaments and immune function may be correlated because both are dependent on nutritional condition. To elucidate if, and how, ornamentation and immune function are linked, pheasant diets were supplemented with carotenoid and/or protein in a fully factorial experiment. Carotenoid treatment affected wattle coloration and tail growth, but not cellular or humoral immunity. Immunity was unrelated to males' initial ornamentation including wattle colour. Males in better body condition, measured as residual mass, increased their wattle coloration more when carotenoid supplemented. Protein positively affected humoral but not cellular immunity, but had no effect on ornaments. Cellular, but not humoral, immunity increased with male body condition. Thus, there was no evidence that an immune-stimulatory effect of carotenoids resulted in wattle coloration honestly signalling immune function, but wattle coloration may still signal male body condition.     

Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata).

Carotenoid-based sexual coloration is the classic example of an honest signal of mate quality. Animals cannot synthesize carotenoid pigments and ultimately depend on dietary sources. Thus, in carotenoid-poor environments, carotenoid coloration may be a direct indicator of foraging ability and an indirect indicator of health and vigour. Carotenoid coloration may also be affected, more directly, by parasites in some species. Carotenoids are not, however, the only conspicuous pigments available to animals. Pteridine pigments, with similar spectral properties, are displayed in the exoskeletons and wings of insects, the irides of birds and the skins of fishes, lizards and amphibians. Unlike carotenoids, pteridines are synthesized de novo by animals. We report that the orange spots that male guppies (Poecilia reticulata) display to females contain red pteridine pigments (drosopterins) in addition to carotenoids. We also examined the relationship between drosopterin production by males and carotenoid availability in the field. The results contrasted sharply with the hypothesis that males use drosopterins to compensate for carotenoid scarcity: males used more, not less, drosopterins in streams with higher carotenoid availability. The positive association between drosopterin use and carotenoid availability could reflect the costs of drosopterin synthesis or it could be a consequence of females preferring a particular pigment ratio or hue. Male guppies appear to use drosopterin pigments in a manner that dilutes, but does not eliminate, the indicator value of carotenoid coloration.     

Carotenoid coloration in greenfinches is individually consistent irrespective of foraging ability

Carotenoid-based plumage coloration of birds has been hypothesized to honestly reflect individual quality, either because carotenoids are difficult to acquire via food or because of a trade-off in allocation of carotenoids between maintenance and signaling functions. We tested whether differential foraging ability is a necessary precondition for maintaining individual differences in carotenoid-based plumage coloration in male greenfinches (Carduelis chloris). Wild-caught birds were brought into captivity, where half of them were supplemented with carotenoids while the other half was maintained on a carotenoid-poor diet. Color of the yellow parts of tail feathers, grown under natural conditions, was compared with that of the replacement feathers, grown in captivity. Carotenoid supplementation increased feather chroma (saturation). Color of wild-grown feathers significantly correlated with the color of lab-grown feathers. This result demonstrates the existence of a significant component of variation in carotenoid coloration, which reflects physiological qualities or genetic differences among individuals independent of foraging ability. Among both experimental groups, plasma carotenoid concentration during feather growth strongly correlated with chroma of the feathers grown in captivity. This indicates that carotenoid-based plumage coloration can reveal circulating carotenoid levels over a very wide range of concentrations, suggesting the ample signaling potential of such a mechanism.     

Age-Related Relationships between Innate Immunity and Plasma Carotenoids in an Obligate Avian Scavenger

Variation in immunity is influenced by allocation trade-offs that are expected to change between age-classes as a result of the different environmental and physiological conditions that individuals encounter over their lifetime. One such trade-off occurs with carotenoids, which must be acquired with food and are involved in a variety of physiological functions. Nonetheless, relationships between immunity and carotenoids in species where these micronutrients are scarce due to diet are poorly studied. Among birds, vultures show the lowest concentrations of plasma carotenoids due to a diet based on carrion. Here, we investigated variations in the relationships between innate immunity (hemagglutination by natural antibodies and hemolysis by complement proteins), pathogen infection and plasma carotenoids in nestling and adult griffon vultures (Gyps fulvus) in the wild. Nestlings showed lower hemolysis, higher total carotenoid concentration and higher pathogen infection than adults. Hemolysis was negatively related to carotenoid concentration only in nestlings. A differential carotenoid allocation to immunity due to the incomplete development of the immune system of nestlings compared with adults is suggested linked to, or regardless of, potential differences in parasite infection, which requires experimental testing. We also found that individuals with more severe pathogen infections showed lower hemagglutination than those with a lower intensity infection irrespective of their age and carotenoid level. These results are consistent with the idea that intraspecific relationships between innate immunity and carotenoids may change across ontogeny, even in species lacking carotenoid-based coloration. Thus, even low concentrations of plasma carotenoids due to a scavenger diet can be essential to the development and activation of the immune system in growing birds.     

The evolution of carotenoid coloration in estrildid finches: a biochemical analysis

The estrildid finches (Aves: Passeriformes: Estrildidae) of Africa, Asia, and Australia have been the focus of several recent tests of sexual selection theory. Many estrildids display bright red, orange, or yellow colors in the beak or plumage, which typically are generated by the presence of carotenoid pigments. In this study, we used high-performance liquid chromatography to investigate the carotenoid content of feathers and other colorful tissues in seven species of estrildids. Star finches (Neochmia ruficauda) and diamond firetails (Stagonopleura guttata) circulated two main dietary carotenoids (lutein and zeaxanthin) through the blood and liver and used both to acquire a yellow plumage color. However, five other estrildids (common waxbill, Estrilda astrild; black-rumped waxbill, Estrilda troglodytes; zebra waxbill, Amandava subflava; red avadavat, Amandava amandava; and zebra finch, Taeniopygia guttata) circulated these same dietary carotenoids along with two metabolites (dehydrolutein and anhydrolutein) through the blood and/or liver and used all four as yellow plumage colorants. We subsequently tracked the distribution of these pigments using a published phylogeny of estrildid finches to determine the evolutionary pattern of carotenoid metabolism in these birds. We found that finches from the most ancient tribe of estrildids (Estrildini) possessed the ability to metabolize dietary carotenoids. Although carotenoids from the most ancestral extant estrildid species have yet to be analyzed, we hypothesize (based on their relationships with other songbirds known to have such metabolic capabilities) that these finches inherited from their ancestors the capability to metabolize carotenoids. Interestingly, later in estrildid evolution, certain taxa lost the ability to metabolize dietary carotenoids (e.g., in the Poephilini), suggesting that the occurrence of carotenoid metabolism can be labile and is likely shaped by the relative costs and benefits of color signaling across different species.     

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.     

An Ultrastructural and Carotenoid Analysis of the Red Ventrum of the Japanese Newt,Cynops pyrrhogaster

The ventral skin of the wild Japanese newt Cynops pyrrhogaster is creamy at metamorphosis, but turns red when mature. The color of the ventral skin of laboratory (lab)‐reared newts stays yellow throughout their life. However, the mechanism for the red coloration of this animal still remains unknown. In this study, we have performed ultrastructural and carotenoid analyses of the red ventrum of wild and lab‐reared Japanese newts. Using electron microscopy, we observed a number of xanthophores having ring carotenoid vesicles (rcv) and homogenous carotenoid granules (hcg) in the ventral red skin of the wild newt. In the skin, β‐carotene and five other kinds of carotenoids were detected by thin‐layer chromatography (TLC). In the ventral yellow skin of lab‐reared newts, however, only β‐carotene and three other kinds of carotenoids were found. The total amount of carotenoids in the red skin of the wild adult newt was six times more than that of the yellow skin of the lab‐reared newt. Moreover, rcv were more abundant in xanthophores in red skin, but hcg were more abundant in yellow skin. These results, taken together, suggest that the presence of carotenoids in rcv in xanthophores is one of the critical factors for producing the red ventral coloration of the Japanese newt C. pyrrhogaster.     

Carotenoid pigments in male American goldfinches: what is the optimal biochemical strategy for becoming colourful?

Studies of brilliant carotenoid‐based coloration in birds have traditionally centred on the role that these colours play in attracting mates. More recently, biologists have begun to take a biochemical approach to understanding the types of pigments found in feathers and how these relate to the expression of ornamental coloration. Nevertheless, surprisingly few studies have assessed the types and amounts of carotenoids present in the diet or blood of animals in relation to season, sex, condition or sexually attractive colour traits, particularly for wild birds. It is conceivable not only that the total concentration of pigments available is an important predictor of sexual attractiveness and mate quality, but also that specific pigments vary among individuals and play more important physiological and pigmenting roles than others. We investigated the carotenoid content of blood and feathers in wild‐caught, yellow‐pigmented male American goldfinches (Carduelis tristis) throughout the year to determine the optimal biochemical strategy for becoming colourful. We found that birds acquired two main yellow hydroxycarotenoids (lutein and zeaxanthin) from the diet during both moulting and non‐moulting periods. Blood concentrations of both pigments changed significantly over time, with moulting birds accumulating higher levels of both lutein and zeaxanthin, but proportionally more zeaxanthin, than non‐moulting birds. Moulting birds that acquired more lutein and more zeaxanthin in blood deposited a higher concentration of carotenoid pigments (canary xanthophylls A and B) into plumage and acquired more colourful feathers. In sum, these results indicate that (a) the types of dietary carotenoids available across seasons do not change in American goldfinches, (b) seasonal fluctuations in plasma‐carotenoid signatures may result from differences in dietary access or pigment processing, and (c) the best biochemical strategy for becoming a colourful, wild male goldfinch is to accumulate as many dietary/blood pigments as possible during moult. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83 , 273–280.