Date Published: April 24, 2019
Publisher: Public Library of Science
Author(s): Suzanne Amador Kane, Yuchao Wang, Rui Fang, Yabin Lu, Roslyn Dakin, Matthew Shawkey.
Colorful feathers have long been assumed to be conspicuous to predators, and hence likely to incur costs due to enhanced predation risk. However, many mammals that prey on birds have dichromatic visual systems with only two types of color-sensitive visual receptors, rather than the three and four photoreceptors characteristic of humans and most birds, respectively. Here, we use a combination of multispectral imaging, reflectance spectroscopy, color vision modelling and visual texture analysis to compare the visual signals available to conspecifics and to mammalian predators from multicolored feathers from the Indian peacock (Pavo cristatus), as well as red and yellow parrot feathers. We also model the effects of distance-dependent blurring due to visual acuity. When viewed by birds against green vegetation, most of the feathers studied are estimated to have color and brightness contrasts similar to values previously found for ripe fruit. On the other hand, for dichromat mammalian predators, visual contrasts for these feathers were only weakly detectable and often below detection thresholds for typical viewing distances. We also show that for dichromat mammal vision models, the peacock’s train has below-detection threshold color and brightness contrasts and visual textures that match various foliage backgrounds. These findings are consistent with many feathers of similar hue to those studied here being inconspicuous, and in some cases potentially cryptic, in the eyes of common mammalian predators of adult birds. Given that birds perform many conspicuous motions and behaviors, this study suggests that mammalian predators are more likely to use other sensory modalities (e.g., motion detection, hearing, and olfaction), rather than color vision, to detect avian prey. This suggests new directions for future behavioral studies and emphasizes the importance of understanding the influence of the sensory ecology of predators in the evolution of animal coloration.
Ever since Darwin, colorful feathers have been assumed to present salient visual signals readily detectable by their natural predators [1,2]. For this reason, sexually-selected ornaments like the iridescent eyespot feathers of the Indian peacock (Pavo cristatus) (Fig 1A) have been proposed to incur a cost due to increased predation [2–4]. As Zahavi argued in his paper introducing the handicap principle: “The more brilliant the plumes, the more conspicuous the male to predators” . Evidence for such opposing selection pressures has been found in ornamented guppies preyed upon by fish . On the contrary, susceptibility to cat predation was not found to correlate significantly with sexual dichromatism in birds , and a recent experimental study found that conspicuous plumage does not enhance predation by avian predators ( and references therein). Conspicuously-colored plumage also has been proposed to function as warning coloration for aposematism [9,10]. However, while these hypotheses are predicated on the predator being able to detect prey visual signals , no studies have tested whether this is true for the mammalian predators that prey on many birds. For example, the primary predators of adult peafowl are carnivorans (felids and canids, S1 Appendix), and cats are a major threat to bird populations world-wide . These predators all have dichromatic visual systems; i.e., they have only two types of cone visual receptors with distinct spectral sensitivities, not the four characteristic of most birds or the three found in most humans . Because dichromatic mammals lack red-green color discrimination, they are unlikely to detect many of the chromatic visual cues evident to birds and humans [13–15]. Studies of visual ecology have considered how prey appear to various types of predators (birds, insects and fish) for many types of prey, including insects and birds [16,17], fish , cuttlefish , crustaceans , primates  and lizards . Two previous studies also have studied the iridescence reflectance spectra of peacock eyespots and how they are perceived by peahens (females) [22,23]. So far, no studies have compared how visual signals from peacocks and other birds appear in the vision of their mammalian predators.
All data and software required in order to replicate all of our results are archived either in the supplemental materials or at https://figshare.com/s/688fb19dad98b6273324.
The results of our study show that sexually-selected color signals readily detectable by conspecifics are not necessarily conspicuous to mammalian predators. Instead, for all distances considered, the color and brightness contrasts for all feather samples studied here relative to green foliage were much greater for birds than for dichromatic mammals. For all viewing distances modeled here, most feather samples had color contrasts in dichromatic predator vision that were perceptually indistinguishable from background vegetation; two exceptions were in the low detectable range: the peafowl’s blue plumage (color contrast range [1.6, 1.8] JND) and the yellow scarlet macaw feather patches (color contrasts [1.6, 1.7] for ≤ 2 m). Unsurprisingly, the same feathers were highly conspicuous to conspecifics: their color contrasts were comparable to values found for avian visual modeling for fruit viewed against green foliage [118,143]. The brightness contrasts for these feathers vs background foliage in dichromatic predator vision were on the whole greater than the corresponding color signals, although only values for yellow exceeded the weakly detectable 1–3 JND range. This suggests that patterns with high brightness contrast, such as those created by white and dark melanin-pigmented plumage, might be more readily detectable by dichromat predators than color signals, and thus represent a greater detection risk ; such brightness-based visual signals also would presumably be more readily detectable for low light conditions. While the interpretation of supra-threshold color and brightness contrasts is still debated , our results show that such supranormal stimuli remain detectable by conspecifics and other birds even at large distances where carnivores cannot perceive them.