Abstract

Reflectance by yellow to red carotenoid-based plumages in birds with ultraviolet-sensitive (UVS) color vision typically shifts to redder (longer) wavelengths as carotenoid consumption (Dietc) increases. This apparent asymmetric red-shift response implies an overall bias against conceivable shifts to bluer (shorter) wavelengths. However, recent studies among species of Piciformes–Coraciiformes (e.g., woodpeckers, barbets, toucans, bee-eaters, and allies) with violet-sensitive (VS) color vision discovered two kinds of blue shifts between the same plumage and dietary traits. Compared to UVS absolute red shifts (positive slopes at higher Dietc), VS express absolute (negative slopes at higher Dietc for yellow and orange plumages) or relative (zero slope for red plumages) blue shifts. These contrasting patterns for different color vision systems suggest that generalized symmetry concepts of opposite (plumage shift) patterns that maintain invariant (Dietc, perception) processes can be abstracted from physical to biological systems, with positive versus negative responses formalized as “antisymmetries” and relative responses formalized as “broken symmetries”. A subset of VS “true woodpecker” (Picinae) species with known yellow and red plumage-carotenoid chemistries demonstrated similar blue shifts for the main reflectance bands and their independence from phylogeny, sex, and specimen collection year, thus providing key chemical details to further test generalized plumage symmetries. Juxtapositions were facilitated because both yellow and red plumages in true woodpeckers contained comparatively blue- and red-shifted carotenoid types. Despite this parallel, each plumage deployed chemical variations in radically different ways. Yellow plumage contained only chemically defined yellow carotenoids, including intrinsically more red-shifted natives (i.e., hydroxy-xanthophylls) widespread among birds through their diets, and intrinsically more blue-shifted picofulvins (i.e., 7,8-di- and tetra-hydro-carotenoids) probably characteristic of and metabolized by VS birds. Higher absolute and relative (to natives) picofulvin concentrations were significant predictors of absolute blue shifts in yellow plumage reflectance, and were significantly predicted by higher Dietc. Transitivity implied Dietc ⟶ native ⟶ picofulvin ⟶ reflectance, such that picofulvins caused absolute blue shifts at higher Dietc, and natives caused absolute red shifts at lower Dietc. Moreover, opposite trends for picofulvin and native concentrations in feathers were consistent with the proposed endogenous synthesis of picofulvins from natives. Yellow plumages comprised mainly of picofulvins at very low (from very low Dietc from ants and termites) or high (from very high Dietc from fruits) concentrations were especially distinctive for some of these and other interrelationships, suggesting some heterogeneity in yellow pigmentation strategies from dietary idiosyncrasies. Red plumages contained only relatively low concentrations of yellow dietary natives (hydroxy-xanthophylls), but varied widely in the concentration of metabolites of comparatively intermediate (4-oxo-keto-carotenoids) or extreme (4,4′-oxo-keto-carotenoids) redness. However, different red chemistries lacked any corresponding significant relationships with variations in reflectance or Dietc. Variations in reflectance based on chemical compositions were more visible to humans for yellow than red plumage types, setting minimum salience levels for the more discriminating diurnal avian color visions. Therefore, VS yellow plumage chemistries that emphasize deposition of easily obtained (cheaper) dietary natives at low Dietc, and of more deliberately synthesized (costly) picofulvin metabolites at higher Dietc were consistent with several forms of honest signaling in UVS from resource limitations based on Dietc, including through potential costs and benefits and their trade-offs. Conversely, the diverse chemical compositions and costs of red plumages of similar physical reflectance properties, and evidence that intrinsically orange carotenoids intermediate between red and yellow ones were actively excluded from plumage, suggested that true woodpecker reds were under selection for a convergent appearance. In light of true woodpecker biology, sensory bias, and social and aposematic mimicry are likely mechanisms promoting resemblance. These results extend to the chemical level earlier interpretations of opposite shift patterns as antisymmetries of invariant processes and relative shift patterns as broken symmetries of altered processes for VS vis-à-vis UVS carotenoid-based systems.

IPC Classification

Keywords