Abstract
Sea otters (Enhydra lutris) are amphibious mammals that maintain equal in-air and underwater visual acuity. However, their lens-based underwater accommodative mechanism presumably requires a small pupil that may limit sensitivity across light levels. In this study, we consider adaptations for amphibious living by assessing the tapetum lucidum, retina, and pupil dynamics in sea otters. The sea otter tapetum lucidum resembles that of terrestrial carnivores in thickness and fundic coverage. A heavily rod-dominated retina appears qualitatively similar to the ferret and domestic cat, and a thick outer nuclear layer relative to a thinner inner nuclear layer is consistent with nocturnal vertebrates and other amphibious carnivores. Pupil size range in two living sea otters is smaller relative to other amphibious marine carnivores (pinnipeds) when accounting for test conditions. The pupillary light response seems slower than other aquatic and terrestrial species tested in comparable brightness, although direct comparisons require further assessment. Our results suggest that sea otters have retained features for low-light vision but rapid adjustments and acute underwater vision may be constrained across varying light levels by a combination of pupil shape, absolute eye size, and the presumed coupling between anterior lens curvature and pupil size during accommodation.
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Abbreviations
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- H&E:
-
Hematoxylin and eosin
- IHC:
-
Immunohistochemistry
- INL:
-
Inner nuclear layer
- IOP:
-
Intraocular pressure
- IR:
-
Infrared
- LED:
-
Light-emitting diode
- M/L:
-
Middle- to long-wavelength sensitive
- ONL:
-
Outer nuclear layer
- ONL/INL:
-
Ratio of outer nuclear layer thickness to inner nuclear layer thickness
- PBS:
-
Phosphate-buffered saline
- PNA:
-
Biotinylated peanut agglutinin
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Acknowledgements
We thank the volunteers and staff at the Pinniped Cognition and Sensory Systems Lab, especially C. Casey, K. Cunningham, A. Ghoul, T. Grant, J. Lofstrom, J. Mihok, R. Nichols, A. Rouse, J. Sills, and C. Whalen for their assistance with research. D. Levenson provided experimental support, equipment, and advice. We thank A. Johnson, E. Lenihan, K. Mayer, and M. Young at Monterey Bay Aquarium for sample collection, logistical support, and access to sea otters. L. Carswell at US Fish and Wildlife Service provided assistance in the permitting procedure. A. Friedlaender and P. Robinson provided photographic assistance during pilot testing for this study, and E.J. Ehrhardt provided gross anatomical assessments of two sea otter eyes that contributed to planning for this study. We also thank the many people who guided the authors in eye dissection and histology in stages of this research, including C. Beier and S. Sher at University of California Santa Cruz, M. Glössman at University of Vienna, Austria, and M. Miller, L. Henkel, F. Batac, E. Dodd, C. Young and A. Reed at California Department of Fish and Wildlife’s Marine Wildlife Veterinary Care and Research Center, and A. Minella and A. Moshiri at the University of California Davis. T. Tinker, P. Raimondi, B. Lyon, and J. Estes at the University of California Santa Cruz contributed to the interpretation of this research. N. Castañeda, K. Dale, S. Kienle, C. Law, R. Mehta, and K. Voss provided helpful suggestions on earlier versions of this manuscript.
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This work was supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. NSF DGE 1339067 and the Department of Education Graduate Assistance in Areas of National Need Fellowship P200A150100. Research costs were supported in part by Monterey Bay Aquarium, the Friends of Long Marine Lab, and the Pinniped Cognition and Sensory Systems Lab.
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SMS and CR contributed to conceptualization; SMS, BM, KF, and CR contributed to methodology; BM, KF, and MM contributed to resources; SMS, BM, and CR contributed to validation; SMS contributed to formal analysis; SMS, BM, KF, and CR contributed to investigation; SMS curated the data; SMS wrote the original draft; all authors contributed to review and editing of subsequent drafts; SMS and BM contributed to visualization; CR contributed to supervision; SMS and CR administered the project; SMS and CR contributed to funding acquisition.
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All procedures performed in studies involving animals were in accordance with the ethical standards of the University of California Santa Cruz. All applicable international, national, and institutional guidelines for the care and use of animals were followed under authorization from the United States Fish and Wildlife Services Permits MA186914-1 and MA186914-2 and the Institutional Care and Use Committees at University of California Santa Cruz (Reicc1304, Reicc1603, and Reicc1701) and Monterey Bay Aquarium (13-02). Post-mortem samples were collected under Letters of Authorization from the United States Fish and Wildlife Service (08EVEN00-2016-B-0187 and 08EVEN00-2017-B-0045). This article does not contain any studies of human participants.
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Strobel, S.M., Moore, B.A., Freeman, K.S. et al. Adaptations for amphibious vision in sea otters (Enhydra lutris): structural and functional observations. J Comp Physiol A 206, 767–782 (2020). https://doi.org/10.1007/s00359-020-01436-4
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DOI: https://doi.org/10.1007/s00359-020-01436-4