Carotenoid Chroma Research Articles

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.

Deleterious effects of light exposure on immunity and sexual coloration in birds

Summary1. Sunlight ultraviolet (UV) exposure can be highly damaging to biological tissues, being known to cause cellular damage and immunosuppression in humans and rodents, and depletion of carotenoid‐based sexual plumage coloration in birds (i.e. photobleaching). However, it remains unknown whether sunlight may cause photobleaching in living tissues that comprise sexual signals such as bare parts in birds. It seems possible that any carotenoids depleted from bare parts by sunlight could be replenished, but if so, this could impact the availability of carotenoids for other functions such as immunity and antioxidant defence. Such trade‐offs seem particularly likely in individuals that have a low dietary intake of carotenoids, or small amounts of carotenoids in body storage.2. We investigated the effects of exposure to simulated sunlight UV (UV+) on bill coloration, blood plasma and liver (i.e. body storage) carotenoids and pro‐inflammatory immune responses in male zebra finches (Taeniopygia guttata) in vivo, compared with individuals maintained in an identical environment but with the UV wavelengths removed by a filter (UV−). We also investigated whether any deleterious effects of UV exposure were mitigated by dietary carotenoid supplementation (UV+ Car+).3. Exposure to simulated sunlight UV was associated with low levels of carotenoids in liver, and elevated levels of carotenoids in blood plasma, suggesting the mobilisation of stored carotenoids. Simulated sunlight UV also caused impaired pro‐inflammatory immune responses, whereas this was not seen in carotenoid‐supplemented birds. We found no effects of simulated sunlight UV or carotenoid supplementation on oxidative damage in blood plasma or bill.4. Bill ‘carotenoid chroma’ diminished, and bill ‘UV chroma’ correspondingly increased, in all groups during the experiment (i.e. even in UV+ Car+ birds, and in UV− birds). This likely arose because the illuminance in the experimental cages was far higher than in standard laboratory housing conditions and suggests that carotenoid pigmentation is highly susceptible to photobleaching even under exposure to human‐visible wavelengths.5. These results highlight the potential for sunlight exposure to invoke a range of deleterious consequences for birds, including photobleaching and depression of immunity via pathways mediated by carotenoid allocation trade‐offs. The expression of carotenoid‐based sexual signals may therefore reveal an individual’s history of sunlight exposure and its deleterious effects on immunity.

Yolk androgens in great tit eggs are related to male attractiveness, breeding density and territory quality

Females can adaptively adjust phenotype of their offspring via deposition of various compounds into eggs, including androgens and other hormones. Here, I investigated how egg yolk androgens (testosterone and androstenedione) related to environmental conditions and parental traits in the great tit (Parus major) across three breeding seasons. Male and female traits studied included age, condition and multiple feather ornaments, both carotenoid- and melanin-based (carotenoid and UV chroma of yellow breast feathers, area of black breast band and white cheek immaculateness). Yolk mass increased with laying temperature, laying date and area of male black breast band. Concentration of androgens increased with breeding density, territory quality and carotenoid chroma of male yellow breast feathers and was higher in mates of 1 year old as compared to older males. Yolk androgens were not related to any of the female traits analysed. These patterns were thus consistent with (1) social and environmental effects on yolk mass and composition and (2) both positive and negative differential allocation strategies of resource allocation in females. Overall, male traits were the most important predictors of egg yolk characteristics in this socially monogamous songbird.

Dissecting Carotenoid from Structural Components of Carotenoid‐Based Coloration: A Field Experiment with Great Tits (Parus major)

Carotenoid-based yellowish to red plumage colors are widespread visual signals used in sexual and social communication. To understand their ultimate signaling functions, it is important to identify the proximate mechanism promoting variation in coloration. Carotenoid-based colors combine structural and pigmentary components, but the importance of the contribution of structural components to variation in pigment-based colors (i.e., carotenoid-based colors) has been undervalued. In a field experiment with great tits (Parus major), we combined a brood size manipulation with a simultaneous carotenoid supplementation in order to disentangle the effects of carotenoid availability and early growth condition on different components of the yellow breast feathers. By defining independent measures of feather carotenoid content (absolute carotenoid chroma) and background structure (background reflectance), we demonstrate that environmental factors experienced during the nestling period, namely, early growth conditions and carotenoid availability, contribute independently to variation in yellow plumage coloration. While early growth conditions affected the background reflectance of the plumage, the availability of carotenoids affected the absolute carotenoid chroma, the peak of maximum ultraviolet reflectance, and the overall shape, that is, chromatic information of the reflectance curves. These findings demonstrate that environment-induced variation in background structure contributes significantly to intraspecific variation in yellow carotenoid-based plumage coloration.

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.

Sex and age differences in reflectance and biochemistry of carotenoid-based colour variation in the great tit Parus major

The plumage coloration in great tits (Parus major) is the subject of much behavioural and ecophysiological research, yet there is a lack of analyses of the natural colour variation and its mechanisms. We used reflectance spectrometry and high-performance liquid chromatography to explore individual, sexual and age-related variation in carotenoid coloration and pigmentation, paramount to the often presumed, but rarely substantiated, costs and 'honesty' of carotenoid displays. In adults, we found that sex was the strongest predictor of 'brightness' (higher in males) and of 'hue' (longer wavelength in females). There was no sex difference in 'carotenoid chroma' or carotenoid content of feathers which also was unrelated to adult age (1 or 2+ years) and condition. Similar patterns were revealed for nestlings. Regarding the biochemical 'signal content', 'carotenoid chroma', but not 'hue', was significantly related to the carotenoid content (lutein and zeaxanthin) of feathers. These results refute the previously assumed exaggeration of carotenoid pigmentation in male great tits, and question the condition-dependence of carotenoid coloration in this species. However, the sexual dimorphism in total reflectance or 'brightness', most likely due to melanins rather than carotenoids, may have implications for signalling or other adaptive explanations that need to be explored.

Carotenoid pigmentation does not reflect total non‐enzymatic antioxidant activity in plasma of adult and nestling great tits, Parus major

Summary Based on carotenoids’ antioxidant and pro‐vitamin functions, carotenoid pigmentation, particularly in birds, has been hypothesized to honestly advertize condition and health. As antioxidants, carotenoids protect the body from oxidative damage caused by internal or external stressors (e.g. growth, infection and anthropogenic pollution). However, the relative importance of carotenoids in the avian antioxidant defence has been questioned, and the positive relationship between colouration and health may be a ‘red herring’. In the present study, we investigate carotenoid‐based plumage colouration and circulating carotenoids in relation to plasma non‐enzymatic total antioxidant activity (TAA) in adult and nestling great tits (Parus major). The study was conducted in urban vs. rural populations, with documented differences in oxidative stress level and plumage pigmentation. First, we found that there was no relationship between TAA and plumage pigmentation (carotenoid chroma) or plasma carotenoids. Second, urban environment significantly influenced TAA; old (2+ years) urban birds had higher activity than old rural birds, and also compared to younger (1 year) urban adults. This is likely to be due to the increased demand for plasma antioxidants as a consequence of urban environmental stress. Third, nestlings’ TAA showed no difference between urban and rural environments. However, it was highly influenced by brood, but not related to parental levels, therefore most likely due to differences in the nestling environment. We suggest that carotenoids are not significant contributors to extra‐cellular antioxidant defence in great tits, and that carotenoid pigmentation may be an overrated health indicator in this respect. Honest carotenoid signalling, when present, is thus likely to be mediated by some other constraint, such as nutrition or uptake, or other health‐modulating mechanisms.

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

Intraspecific sexual and social communications are among the most important factors shaping costly color traits in birds. Condition capture models assume that only animals in superior condition can develop and maintain a colorful plumage. Although there is good evidence that carotenoid-based components of plumage colors show condition dependence, the situation is more controversial with the underlying UV-reflecting structural component. We conducted a brood size manipulation in blue tits (Parus caeruleus) to investigate condition-dependent effects on plumage coloration in male and female offspring. Carotenoid chroma and UV reflectance of the yellow breast plumage showed condition-dependent expression in male and female fledglings. However, only males that were raised in reduced broods had higher UV reflectance in the UV/blue tail feathers, whereas female tail coloration did not differ between treatments. Our data suggest that there is a sex-specific effect on the blue but not the yellow plumage and that this is related to differences in the signaling function of both plumage traits. Although sexual selection may already act on male nestlings to develop colorful tail feathers for the next breeding season, the UV/yellow breast feathers are molted during the postjuvenile molt, and their signaling value is likely to be important for both sexes during the extended postfledgling phase.