Seasonal changes in colour: a comparison of structural, melanin- and carotenoid-based plumage colours

Abstract

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

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

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

Figure 1. Graphical representation of the procedure used to compute chromatic variation.

Principal component analysis of the xyz coordinates reveals that most of the chromatic variation (>80%) can be described by a single principal component (PC1). By selecting the data point with the lowest PC1 value (marked here by the asterisk) and computing discriminability (ΔS) between this point and all other points in the sample (black arrows, only a few arrows are depicted for clarity) we obtain a measurement of chromatic variation that takes into account the different signal-to-noise ratios of the four single cone types in the avian retina and can be directly compared between different colour types. The data represented in the figure corresponds to the yellow breast of the blue tit. Inset shows the position of the vertices of the tetrahedral visual space of birds. In this representation larger values of x represent higher stimulation of the L cone and lower stimulation of the M cone, larger values of y correspond to higher stimulation of the S cone and larger values of z increased stimulation of the VS cone.

Figure 2. Seasonal variation in robin coloration.

The left panel depicts chromatic changes (ΔS), and the right panel achromatic changes (ΔL) for males (open circles) and females (closed circles) during the year (monthly means +/− SE). Higher values of ΔS correspond to higher relative reflectance in the shorter wavelengths (UV, blue) and lower values higher relative reflectance in the longer wavelengths (red). Higher values of ΔL correspond to higher achromatic brightness relative to the darkest individual in that plumage patch. Lines for males (grey) and females (black) are derived from the final models in Tables 1 and 2. The centre panel shows average reflectance spectra for males (open symbols) and females (closed symbols) for the months of Nov-Dec (circles) and Apr-May (triangles). These months were selected because they were the first (Nov-Dec) months without moulting birds and the last (Apr-May) months before moult. Note that reflectance spectra are not to scale to highlight the differences in spectral shape.

Figure 3. Seasonal variation in blackbird coloration.

See legend of Figure 2 for more details. Note that the ΔS and ΔL graphs for the bill have not been drawn to the same scale as the plumage patches.

Figure 4. Seasonal variation in blue tit coloration.

See legend of Figure 2 for more details.

Figure 5. Seasonal variation in great tit coloration.

See legend of Figure 2 for more details.

Figure 6. Total chromatic (A) and achromatic (B) changes over the year.

Based on the final models in Tables 1 and 2 and discriminated by the main colour-producing mechanism (note that while the great tit crown has been included among melanin-based colours, its UV reflectance hints at an additional structural component, see Discussion). One value is depicted for linear changes and two (united by the arrows) for curvilinear patterns of change (the first corresponds to the minimum or maximum and the second to the final value). Positive values of chromatic changes indicate an increase in the reflectance at shorter wavelengths while positive values of achromatic changes indicate increased achromatic brightness over the year. When males and females presented different patterns of change they were depicted separately.