(Erik Iverson 24 May 2017; Photo K Tarvin)
Birds are well-known for being among the most colorful of all animals, with many species displaying striking, brightly-colored feathers. Scientists have long wondered why color is so important to fitness, and hundreds of studies have been published on the relationships between plumage and traits such as age, physiological condition, reproductive success, and attractiveness to mates. However, there is a growing awareness that plumage is not the only important site of coloration among birds; there is also considerable variation within and between species in the color of bills and in bare skin such as legs, feet, ceres, or wattles. Yet compared to plumage, these ‘bare part’ ornaments have received relatively little attention; a 2006 review of carotenoid coloration in birds, for instance, identified only 14 studies of bare parts versus 130 studies of plumage.
Unlike plumage, bare part color has the potential to be highly flexible. For example, carotenoid-based bare parts can lose their color within days of food deprivation or within hours of stress. Amidst growing suggestions that changes in bare part color could have important implications for signaling, one of the authors, Jordan Karubian, was studying Red-Backed Fairywrens (Malurus melanocephalus) in Australia. In this species, males either acquire a territory and display black breeding plumage and bills, or stay dull and serve as helpers at the nest. Jordan noticed that when a breeding male died and a dull male took over its vacancy, the dull male’s bill would darken within several weeks. Experiments confirmed this effect and showed that dull males with newly black bills also had testosterone levels comparable to birds with black plumage. I joined Jordan’s lab as an undergraduate and studied fairywrens as well, and when I was looking for a topic for an honors thesis Jordan suggested that bare parts were an expanding area in need of a review. That thesis grew and grew, eventually becoming my master’s work and encompassing 321 published studies of bare-part coloration and signaling.
Our review shows that despite the research focus on plumage, bare part signals might be more common than plumage-based ones and are an important visual signal in many species that lack bright plumage altogether. Carotenoids, melanin, and structural colors are all flexible in bare parts, and rapid blood flushing through skin can change color even more rapidly. Bare part color provides up-to-date information about a signaler, allowing competitors, mates, and offspring to adjust their strategies and maximize their fitness. Carotenoid-signaling with bare parts may also be less costly than with plumage, allowing signaling by females and non-breeding males. In species where both plumage and bare parts of the same color exist, the two are likely to be ‘multiple messages,’ conveying different aspects of condition or targeting different audiences. We believe that more careful and extensive characterization of bare part coloration will contribute greatly to our understanding of this underappreciated dynamic signal, and help inform a more inclusive theory of animal communication.