Stéphanie M. Doucet

pavo: an R package for the analysis, visualization and organization of spectral data

Summary Recent technical and methodological advances have led to a dramatic increase in the use of spectrometry to quantify reflectance properties of biological materials, as well as models to determine how these colours are perceived by animals, providing important insights into ecological and evolutionary aspects of animal visual communication. Despite this growing interest, a unified cross-platform framework for analysing and visualizing spectral data has not been available. We introduce pavo, an R package that facilitates the organization, visualization and analysis of spectral data in a cohesive framework. pavo is highly flexible, allowing users to (a) organize and manipulate data from a variety of sources, (b) visualize data using Rs state-of-the-art graphics capabilities and (c) analyse data using spectral curve shape properties and visual system modelling for a broad range of taxa. In this paper, we present a summary of the functions implemented in pavo and how they integrate in a workflow to explore and analyse spectral data. We also present an exact solution for the calculation of colour volume overlap in colourspace, thus expanding previously published methodologies. As an example of pavos capabilities, we compare the colour patterns of three African glossy starling species, two of which have diverged very recently. We demonstrate how both colour vision models and direct spectral measurement analysis can be used to describe colour attributes and differences between these species. Different approaches to visual models and several plotting capabilities exemplify the packages versatility and streamlined workflow. pavo provides a cohesive environment for handling spectral data and addressing complex sensory ecology questions, while integrating with Rs modular core for a broader and comprehensive analytical framework, automated management of spectral data and reproducible workflows for colour analysis.

Iridescence: a functional perspective

In animals, iridescence is generated by the interaction of light with biological tissues that are nanostructured to produce thin films or diffraction gratings. Uniquely among animal visual signals, the study of iridescent coloration contributes to biological and physical sciences by enhancing our understanding of the evolution of communication strategies, and by providing insights into physical optics and inspiring biomimetic technologies useful to humans. Iridescent colours are found in a broad diversity of animal taxa ranging from diminutive marine copepods to terrestrial insects and birds. Iridescent coloration has received a surge of research interest of late, and studies have focused on both characterizing the nanostructures responsible for producing iridescence and identifying the behavioural functions of iridescent colours. In this paper, we begin with a brief description of colour production mechanisms in animals and provide a general overview of the taxonomic distribution of iridescent colours. We then highlight unique properties of iridescent signals and review the proposed functions of iridescent coloration, focusing, in particular, on the ways in which iridescent colours allow animals to communicate with conspecifics and avoid predators. We conclude with a brief overview of non-communicative functions of iridescence in animals. Despite the vast amount of recent work on animal iridescence, our review reveals that many proposed functions of iridescent coloration remain virtually unexplored, and this area is clearly ripe for future research.

STRUCTURAL PLUMAGE COLORATION, MALE BODY SIZE, AND CONDITION IN THE BLUE-BLACK GRASSQUIT

Abstract In birds, the colors ultraviolet, blue, and green originate from feather microstructure rather than pigmentation. Structural plumage coloration may be maintained by sexual selection, yet there exists only limited evidence that structural colors can honestly signal individual quality. In this study, I found considerable individual variation in the blue-black to ultraviolet coloration of the wing coverts and rump of male Blue-black Grassquits (Volatinia jacarina), thereby revealing the potential for sexual selection on structural plumage coloration in this species. I used a principal components analysis (PCA) of four color characteristics to combine reflectance data into a single color score. Birds with high color scores have brighter, more intensely colored, and more saturated blue-black feathers. There was a significant positive relationship between color scores for both body regions and male condition. There was also a positive trend between the color score of the rump region and male body size. These results support recent findings that structural plumage coloration is condition-dependent, and this type of coloration may be an honest signal of male quality in the Blue-black Grassquit. Coloración Estructural del Plumaje, Tamaño Corporal y Condición Física en Machos de Volatinia jacarina Resumen. En las aves, los colores ultravioleta, azul y verde están dados por la microestructura de las plumas y no por la pigmentación. La coloración estructural del plumaje puede ser mantenida por selección sexual, aunque existe poca evidencia que indique que los colores estructurales son un indicador confiable de la calidad de un individuo. En este estudio encontré variación individual considerable en la coloración negro-azulada a ultravioleta de las cobertoras alares y la rabadilla de machos de Volatinia jacarina, revelando que la coloración estructural del plumaje en esta especie podría estar sujeta a selección sexual. Utilicé un análisis de componentes principales (PCA) de cuatro características de color para combinar datos de reflectancia en un solo valor de color. Las aves con altos valores de color tienen plumas más brillantes e intensamente coloreadas y más saturadas de color negro-azulado. Existió una relación positiva significativa entre los valores de color para ambas regiones del cuerpo y la condición física de los machos. También hubo una tendencia positiva entre el valor del color de la región de la rabadilla y el tamaño corporal de los machos. Estos resultados apoyan descubrimientos recientes que demuestran que la coloración estructural del plumaje depende de la condición física, y que este tipo de coloración puede ser una señal confiable de la calidad de los machos de V. jacarina.

Achromatic color variation in black-capped chickadees, Poecile atricapilla : black and white signals of sex and rank

Sexual dichromatism and phenotypic variation in elaborate male traits are common products of sexual selection. The spectral properties of carotenoid and structurally-based plumage colors and the patch sizes of melanin-based plumage colors have received considerable attention as sexual signals in birds. However, the importance of variation in achromatic plumage colors (white, gray and black) remains virtually unexplored, despite their widespread occurrence. We investigated a potential signal function of the achromatic black and white plumage of black-capped chickadees (Poecile atricapilla). We captured and color-banded 178 free-living chickadees and assessed winter flock dominance hierarchies by tabulating pairwise interactions at feeders. We recaptured 73 of these birds and measured plumage coloration for six body regions using a reflectance spectrometer and the area of melanin-based plumage patches from standardized photographs. We found extensive individual variation in chickadee plumage traits and considerable sexual dichromatism. Male black-capped chickadees have significantly brighter white plumage than females, larger black patches, and greater plumage contrast between adjacent white and black plumage regions. We also found rank differences in the plumage reflectance of males; high-ranking males, who are preferred by females as both social and extra-pair partners, exhibit significantly darker black plumage and grow their feathers more rapidly than low-ranking males. This variation among individuals reveals a potential signal function for achromatic plumage coloration in birds.

Iridescent plumage in satin bowerbirds: structure, mechanisms and nanostructural predictors of individual variation in colour

SUMMARY Iridescence is produced by coherent scattering of light waves from alternating layers of materials of different refractive indices. In birds, iridescent colours are produced by feather barbules when light is scattered from alternating layers of keratin, melanin and air. The structure and organization of these layers, and hence the appearance of bird species with different types of plumage iridescence, varies extensively. One principal distinction between different types of iridescent colours is whether they are produced by a single pair of layers or by multiple pairs of layers. Multi-layer iridescence, such as that displayed by hummingbirds, has been relatively well characterized, but single-layer iridescence has only recently been modeled successfully. Here we use electron microscopy, spectrometry and thin-film optical modeling to investigate the glossy, ultraviolet-blue iridescent plumage colouration of adult male satin bowerbirds Ptilonorhynchus violaceus minor. The flattened barbules of adult males are composed of a superficial keratin layer overlying a melanin layer that is several granules thick. A thin-film model based on the thickness of the keratin layer and its two associated interfaces (air/keratin and keratin/melanin) generates predicted reflectance spectra that closely match measured spectra. In addition, hues predicted from this model are positively correlated with measured hues. As predicted from our thin-film model, measured hues shifted to shorter wavelengths at increasing angles of incidence and reflectance. Moreover, we found that individual variation in barbule nanostructure can predict measured variation in both hue and UV-chroma. Thus, we have characterized the microstructure of satin bowerbird barbules, uncovered the mechanisms responsible for producing ultraviolet iridescence in these barbules, and provided the first evidence of a nanostructural basis for individual variation in iridescent plumage colour.

The effect of coccidial infection on iridescent plumage coloration in wild turkeys

Wild turkeys, Meleagris gallopavo, are among the most ornamented birds in North America, displaying vividly coloured fleshy ornaments on their heads and bright, iridescent structural coloration in their plumage. We investigated the effect of experimental inoculation with coccidian parasites on the expression of iridescent structural coloration in yearling male turkeys. Prior to moult of ornamental feathers, we assigned turkeys to three experimental groups: we maintained six turkeys free of coccidial infection, inoculated four turkeys with a single species of coccidial oocysts, and inoculated six turkeys with multiple species of coccidial oocysts. We used reflectance spectrometry to quantify the plumage coloration of wing covert and breast feathers in the breeding plumage of males in each treatment protocol. We found significant treatment-based variation in the iridescent plumage coloration of yearling male turkeys such that infected males showed proportionately less UV reflectance in their wing covert and breast feathers and had duller breast feathers. This is the first experimental evidence that parasites can suppress the expression of structural plumage coloration, and our findings suggest that, in wild turkeys, iridescent coloration could serve as a condition-dependent signal of male health.

Concordant evolution of plumage colour, feather microstructure and a melanocortin receptor gene between mainland and island populations of a fairy–wren

Studies of the patterns of diversification of birds on islands have contributed a great deal to the development of evolutionary theory. In white–winged fairy–wrens, Malurus leucopterus, mainland males develop a striking blue nuptial plumage whereas those on nearby islands develop black nuptial plumage. We explore the proximate basis for this divergence by combining microstructural feather analysis with an investigation of genetic variation at the melanocortin–1 receptor locus (MC1R). Fourier analysis revealed that the medullary keratin matrix (spongy layer) of the feather barbs of blue males was ordered at the appropriate nanoscale to produce the observed blue colour by coherent light scattering. Surprisingly, the feather barbs of black males also contained a spongy layer that could produce a similar blue colour. However, black males had more melanin in their barbs than blue males, and this melanin may effectively mask any structural colour produced by the spongy layer. Moreover, the presence of this spongy layer suggests that black island males evolved from a blue–plumaged ancestor. We also document concordant patterns of variation at the MC1R locus, as five amino acid substitutions were perfectly associated with the divergent blue and black plumage phenotypes. Thus, with the possible involvement of a melanocortin receptor locus, increased melanin density may mask the blue–producing microstructure in black island males, resulting in the divergence of plumage coloration between mainland and island white–winged fairy–wrens. Such mechanisms may also be responsible for plumage colour diversity across broader geographical and evolutionary scales.

Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch

A study was undertaken to examine secondary sexual characters (spawning colouration and overall body size) in relation to sperm metrics in one alternative reproductive tactic of coho salmon Oncorhynchus kisutch: large hooknose males that spawn in dominance-based hierarchies. Males with less intense red spawning colouration had higher sperm velocities than males with darker red spawning colouration. There was no relationship between male body size and sperm metrics. These results suggest that within an alternative reproductive tactic, variation in sperm competition intensity may select for a trade-off between investment in sexual colouration and sperm quality.

The Evolution of Signal Design in Manakin Plumage Ornaments

Animal signals are characterized by two design components: efficacy (detectability) and content (message being conveyed). Selection for efficient signal perception should favor the evolution of traits that exhibit an optimal balance between these two design components. We examined the evolution of signal design in the colorful plumage ornaments of manakins (Aves: Pipridae). We used a model of avian color space to quantify how differences in plumage coloration would be perceived by a typical passerine bird and examined patterns of coloration across 50 species of manakin. Using phylogenetically independent contrasts, we show that plumage contrast against the background increases with sexual dichromatism in males but not females, suggesting that sexual selection has favored the evolution of male plumage ornaments that enhance signal efficacy. Plumage contrast within individuals also increased with dichromatism in males but not females. Finally, plumage colors produced by different mechanisms, which may reveal different aspects of quality, resulted in different degrees of contrast against the background. Our findings suggest that selection for signal efficacy and content may sometimes be opposing, creating a trade‐off between these two components of signal design. Manakins may mediate this trade‐off by combining multiple plumage ornaments that differ in efficacy and content.

Egg coloration in ring-billed gulls (Larus delawarensis): a test of the sexual signaling hypothesis

Although many avian eggs appear to be cryptically colored, many species also lay vibrant blue green eggs. This seemingly conspicuous coloration has puzzled biologists since Wallace, as natural selection should favor reduced egg visibility to minimize predation pressure. The sexual signaling hypothesis posits that blue green egg coloration serves as a signal of female quality and that males exert post-mating sexual selection on this trait by investing more in the nests of females laying more intensely blue green eggs. This hypothesis has received mixed support to date, and most previous studies have been conducted in cavity-nesting species where male evaluation of his partner’s egg coloration, relative to that of other females, may be somewhat limited. In this study, we test the sexual signaling hypothesis in colonially nesting ring-billed gulls (Larus delawarensis) where males have ample opportunity to assess their mate’s egg coloration relative to that of other females. We used correlational data and an experimental manipulation to test four assumptions and predictions of the sexual signaling hypothesis: (1) blue green pigmentation should be limiting to females; (2) extent of blue green egg coloration should relate to female quality; (3) extent of blue green egg coloration should relate to offspring quality; and (4) males should provide more care to clutches with higher blue green chroma. Our data provide little support for these predictions of the sexual signaling hypothesis in ring-billed gulls. In light of this and other empirical data, we encourage future studies to consider additional hypotheses for the evolution of blue green egg coloration.