The Physical Basis of Extreme Animal Coloration

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2022

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Animals use color to hide from predators, signal to mates, and communicate, among other functions. Some animals, such as birds, butterflies, and spiders, have evolved extreme forms of coloration that push the limits of absorption and reflectance. In these animals, pigments and structural elements are combined to produce high absorption or high reflectance. Compared to more typical pigmentary or structural colors, relatively little work has been done to examine the physical basis of extreme coloration across taxa. In this dissertation, I use butterflies, deep-sea fishes, and cleaner shrimp to further explore the presence of extreme coloration in different taxa and the underlying color production mechanisms. In Chapter 2 I began my investigation of extreme coloration with butterflies. First, I identified several species of butterflies from four subfamilies that all have a reflectance < 0.5%. After identifying a set of particularly black butterflies, I used scanning electron microscopy (SEM) to visualize the morphology of the black scales for each species. I found that hole shape and size varied dramatically across species, with no correlation to reflectance. However, two structural features were consistently found in all species - steep ridges and expanded trabeculae compared to dark brown butterflies. Using finite-difference time-domain (FDTD) modeling, I discovered that those two conserved features reduce reflectance from the scales by up to 16-fold. Furthermore, additional modeling demonstrated that the ridges and trabeculae create more scattering, leading to more absorption by melanin embedded within the scales. Given that ultra-black scales in butterflies are often found adjacent to bright, colored scales, ultra-black may be used to increase the contrast of color signals. After analyzing the underlying basis of ultra-black coloration in butterflies, I turned to deep-sea fishes. Many deep-sea fishes exist in a world where the primary source of light is bioluminescence. Predators with sensitive eyes can detect even dim reflections from potential prey. I hypothesized that deep-sea fishes have evolved structural features or pigments to minimize reflectance from the skin. Similar to my approach in Chapter 1, I began by identifying 16 species of fishes with exceptionally low reflectance. I found that in all 16 species there was a continuous layer of melanosomes in the skin. My FDTD modeling showed that the melanosomes in the skin had the optimal size and shape to minimize reflectance. Furthermore, the melanosomes in deep-sea fishes are larger and more elongated for a given size than what is typical in other ectothermic vertebrates. In this case, unlike other ultra-black animals, where scattering is created by a keratin or chitin matrix, fish melanosomes provide both scattering and absorption. Ultra-black skin reduces sighting distance by predators by more than 6-fold compared to typical black fishes, making it a highly effective form of camouflage in the deep-sea. Between birds, butterflies, fishes, and spiders, the mechanisms underlying ultra-black coloration are relatively well understood. However, less attention has been paid to bright white coloration. In Chapter 4, I used similar methods to Chapters 2 and 3 to explore the physical basis of bright white coloration in cleaner shrimp antennae. Cleaner shrimp engage in a mutualistic relationship with client fishes. Some species of cleaner shrimp use long white body parts to signal to these client fish and advertise their services. Two such species are Ancylomenes pedersoni and Lysmata amboinensis, which signal to client fish using their white antennae. Using SEM, I found that the antennae in both species contain a 1-3µm thick layer of non-pigmented nanospheres. With FDTD modeling, I showed that these nanospheres are the optimal size to maximize reflectance and that they can increase reflectance by up to 19-fold compared to antennae without these nanospheres. Similar to what I found in deep-sea fishes, the nanoparticles create a highly scattering structure that, in the absence of absorption from melanin, forms a bright white color instead of ultra-black. Collectively, the three chapters presented here build upon a small, but growing, body of research into the physical basis of extreme animal coloration. This work provides a foundation for new investigations into the functional effects and the evolution of extreme coloration and has the potential to inspire novel man-made materials.

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Davis, Alexander (2022). The Physical Basis of Extreme Animal Coloration. Dissertation, Duke University. Retrieved from https://hdl.handle.net/10161/25149.

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