Structural and functional assessments of vision and touch in sea otters, Enhydra lutris

The proximate mechanisms underlying foraging behavior in sea otters (Enhydra lutris) are relatively unknown despite decades of research focused on the biology and ecology of this top predator. Sea otters prey on infaunal or visually cryptic benthic invertebrates, but maintain a high rate of capture to consume a quarter of their body mass each day. Consequently, sea otter sensory systems have been shaped by selective pressures for accurate and efficient detection of prey location and assessment of prey quality. This dissertation describes a series of behavioral experiments with trained sea otters and anatomical studies from post-mortem sea otters to assess the visual and tactile capabilities of this species in the context of underwater foraging behavior. Chapter 1 focuses on the visual sense and potential adaptations for foraging in marine environments and low light. This material comprises quantitative and qualitative descriptions of pupil mobility, retinal photoreceptor distribution, and tapetal morphology to assess low-light sensitivity relative to previously demonstrated amphibious acuity. We find that sea otter pupils adjust in size to variable light levels and sea otter retinas retain features that enhance sensitivity in low light. However, pupillary dynamic size range and visual acuity in low light are limited relative to other marine carnivores, likely due to a smaller absolute eye size, non-specialized circular pupil shape, and a reliance on a narrow range of pupil sizes to adequately deform the lens to retain visual acuity under water. Given that sea otters forage successfully across a wide range of light levels and for buried prey, the conclusions from Chapter 1 motivated subsequent investigations of whether sea otter touch abilities are sensitive enough to compensate for the loss of visual focus in low light. The results presented in Chapters 2 are drawn from a comprehensive series of four experiments with a trained sea otter to directly measure in-air and underwater tactile sensitivity for paws and facial vibrissae. These studies provide a behavioral means to evaluate predictions based on previous research of sea otter brain and vibrissal morphology. We find that sea otter paw and vibrissal sensitivities are comparable to other tactile specialists, but paw-based touch is especially acute and comparable to human hands. Additionally, sea otter decision times were reliably less than 250 ms for paw and 500 ms for vibrissae, which suggests that sea otters can make fast and accurate decisions based on information received through touch. Chapter 3 builds on the behavioral results from Chapter 2 to investigate the density and distribution of sensory receptors and associated circulatory structures in sea otter glabrous (i.e., hairless) skin—paw pads, flipper digit pads, lips, and the rhinarium—and to link the degree of neural investment to differential sensitivity and use of these regions in observed sea otter behavior. We confirm the presence of two mammalian mechanoreceptor types—Merkel cells and Pacinian corpuscles—and find that their densities, as well as corresponding neural and blood supply, were highest in the paw digit tips and substantially lower in other glabrous skin. This pattern of increased neural investment is consistent with the areas of the paw primarily used for texture discrimination in Chapter 2, which suggests that the distal paw serves as a tactile fovea in sea otters. As a body of work, this dissertation combines structural and functional approaches to provide a more comprehensive assessment of the visual and tactile systems in sea otters. The findings from these studies not only contribute foundational knowledge about the sensory biology of sea otters, but also offer a mechanistic framework to interpret behavioral patterns and energy expenditure observed in wild sea otters across variable environmental conditions