Vision and Bioluminescence in Cephalopods

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2018

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Abstract

In the deep pelagic ocean, there are no structures to serve as hiding spots, and visual interactions among animals are potentially continuous. The light environment in the midwater habitat is highly structured due to light scattering and absorption. Downwelling sunlight becomes exponentially dimmer, bluer, and more diffuse with depth. This optical structure means that an animal’s depth and viewing direction greatly affect the distances at which it can see visual targets such as potential prey or approaching predators. Additionally, this light environment mediates the visibility of bioluminescent camouflage and signals. My dissertation examines how the midwater light environment affects the ecology and evolution of vision and bioluminescence through an examination of cephalopods, a highly visual group that exhibits a broad diversity of eye adaptations and multiple evolutions of bioluminescence. My research investigates (1) vision and behavior in a deep-sea squid with dimorphic eyes, (2) depth-dependent patterns in cephalopod eye size and visual range, and (3) evolutionary dynamics in bioluminescent cephalopods.

First, I examined the function of differently sized and shaped left and right eyes in midwater “cockeyed” squids (Histioteuthis and Stigmatoteuthis) by using in-situ video footage from remotely operated vehicles at the Monterey Bay Aquarium Research Institute to quantify eye and body orientations. I found evidence that the larger left eye orients upward toward downwelling sunlight and may be useful for spotting silhouettes of potential prey, while the smaller right eye orients slightly downward into darkness, where it may be specialized for detecting bioluminescent flashes. I also found that 65% of adult squids had a yellow pigment in the lens of the larger left eye, which may be used to break the counterillumination camouflage of their prey. Visual modeling showed that the visual gains provided by increasing eye size were much higher for an upward-oriented eye than for a downward-oriented eye, which may explain the evolution of this unique visual strategy.

Second, I examined the effects of depth and optical habitat on eye scaling across cephalopod species by collecting morphological measurements from 120 species at the Smithsonian National Museum of Natural History and constructing a corresponding database of species depth distributions and light habitats from the literature. I then compared absolute eye sizes and relative eye scaling to species light habitats, and found that cephalopods occupying dim light habitats had significantly larger eyes than those occupying bright or dark (abyssal) habitats. My results provide evidence for increased investment in eye size with depth through the midwater habitat until dim, downwelling sunlight disappears.

Finally, I examined the potential effects of the midwater light habitat on evolutionary dynamics among bioluminescent cephalopods using comparative evolutionary methods. I constructed a database of cephalopod daytime depths (as a proxy for light level), body sizes, eye investment, and bioluminescence from published records, then used a published phylogeny and Brownian Motion and Ornstein-Uhlenbeck likelihood models of continuous character evolution in discrete selective categories to determine a best-fit model of evolution. I found evidence that bioluminescence and non-bioluminescent cephalopods are under different selective regimes with different trait optima for depth, body size, and eye investment. Together, this work shows that the structured, directional light environment of the pelagic midwater realm has implications at organismal, macroecological, and macroevolutionary levels.

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Thomas, Kate Nicole (2018). Vision and Bioluminescence in Cephalopods. Dissertation, Duke University. Retrieved from https://hdl.handle.net/10161/16964.

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