Adaptations for amphibious vision in sea otters (Enhydra lutris): structural and functional observations.

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.

Active touch in sea otters: in-air and underwater texture discrimination thresholds and behavioral strategies for paws and vibrissae.

Sea otters (Enhydra lutris) are marine predators that forage on a wide array of cryptic, benthic invertebrates. Observational studies and anatomical investigations of the sea otter somatosensory cortex suggest that touch is an important sense for detecting and capturing prey. Sea otters have two well-developed tactile structures: front paws and facial vibrissae. In this study, we use a two-alternative forced choice paradigm to investigate tactile sensitivity of a sea otter subject's paws and vibrissae, both in air and under water. We corroborate these measurements by testing human subjects with the same experimental paradigm. The sea otter showed good sensitivity with both tactile structures, but better paw sensitivity (Weber fraction, c=0.14) than vibrissal sensitivity (c=0.24). The sea otter's sensitivity was similar in air and under water for paw (cair=0.12, cwater=0.15) and for vibrissae (cair=0.24, cwater=0.25). Relative to the human subjects we tested, the sea otter achieved similar sensitivity when using her paw and responded approximately 30-fold faster regardless of difficulty level. Relative to non-human mammalian tactile specialists, the sea otter achieved similar or better sensitivity when using either her paw or vibrissae and responded 1.5- to 15-fold faster near threshold. Our findings suggest that sea otters have sensitive, rapid tactile processing capabilities. This functional test of anatomy-based hypotheses provides a mechanistic framework to interpret adaptations and behavioral strategies used by predators to detect and capture cryptic prey in aquatic habitats.

Developmental Plasticity in Anurans: Meta-analysis Reveals Effects of Larval Environments on Size at Metamorphosis And Timing of Metamorphosis.

Many anuran amphibians (frogs and toads) rely on aquatic habitats during their larval stage. The quality of this environment can significantly impact lifetime fitness and population dynamics. Over 450 studies have been published on environmental impacts on anuran developmental plasticity, yet we lack a synthesis of these effects across different environments. We conducted a meta-analysis and used a comparative approach to understand whether developmental plasticity in response to different larval environments produces predictable changes in metamorphic phenotypes. We analyzed data from 124 studies spanning 80 anuran species and six larval environments and showed that intraspecific variation in mass at metamorphosis and the duration of the larval period is partly explained by the type of environment experienced during the larval period. Changes in larval environments tended to reduce mass at metamorphosis relative to control conditions, with the degree of change depending on the identity and severity of environmental change. Higher temperatures and lower water levels shortened the duration of the larval period, whereas less food and higher densities increased the duration of the larval period. Phylogenetic relationships among species were not associated with interspecific variation in mass at metamorphosis plasticity or duration of the larval period plasticity. Our results provide a foundation for future studies on developmental plasticity, especially in response to global changes. This study provides motivation for additional work that links developmental plasticity with fitness consequences within and across life stages, as well as how the outcomes described here are altered in compounding environments.

We conducted a meta-analysis to identify how six different environments affect mass at metamorphosis and time to metamorphosis in larval anurans. We find that some, but not all, environmental conditions triggered predictable changes in size and timing of metamorphosis, and phylogenetic relatedness rarely explains developmental plasticity variation among species.

Anatomy of the sense of touch in sea otters: Cutaneous mechanoreceptors and structural features of glabrous skin.

Sea otters (Enhydra lutris) demonstrate rapid, accurate tactile abilities using their paws and facial vibrissae. Anatomical investigations of neural organization in the vibrissal bed and somatosensory cortex coincide with measured sensitivity, but no studies describe sensory receptors in the paws or other regions of glabrous (i.e., hairless) skin. In this study, we use histology to assess the presence, density, and distribution of mechanoreceptors in the glabrous skin of sea otters: paws, rhinarium, lips, and flipper digits, and we use scanning electron microscopy to describe skin-surface texture and its potential effect on the transduction of mechanical stimuli. Our results confirm the presence of Merkel cells and Pacinian corpuscles, but not Meissner corpuscles, in all sea otter glabrous skin. The paws showed the highest density of Merkel cells and Pacinian corpuscles. Within the paw, relative densities of mechanoreceptor types were highest in the distal metacarpal pad and digits, which suggests that the distal paw is a tactile fovea for sea otters. In addition to the highest receptor density, the paw displayed the thickest epidermis. Rete ridges (epidermal projections into the dermis) and dermal papillae (dermal projections into the epidermis) were developed across all glabrous skin. These quantitative and qualitative descriptions of neural organization and physical features, combined with previous behavioral results, contribute to our understanding of how structure relates to function in the tactile modality. Our findings coincide with behavioral observations of sea otters, which use touch to maintain thermoregulatory integrity of their fur, explore objects, and capture visually cryptic prey.

Specializations of somatosensory innervation in the skin of humpback whales (Megaptera novaeangliae).

Cetacean behavior and life history imply a role for somatosensory detection of critical signals unique to their marine environment. As the sensory anatomy of cetacean glabrous skin has not been fully explored, skin biopsy samples of the flank skin of humpback whales were prepared for general histological and immunohistochemical (IHC) analyses of innervation in this study. Histology revealed an exceptionally thick epidermis interdigitated by numerous, closely spaced long, thin diameter penicillate dermal papillae (PDP). The dermis had a stratified organization including a deep neural plexus (DNP) stratum intermingled with small arteries that was the source of intermingled nerves and arterioles forming a more superficial subepidermal neural plexus (SNP) stratum. The patterns of nerves branching through the DNP and SNP that distribute extensive innervation to arteries and arterioles and to the upper dermis and PDP provide a dense innervation associated through the whole epidermis. Some NF-H+ fibers terminated at the base of the epidermis and as encapsulated endings in dermal papillae similar to Merkel innervation and encapsulated endings seen in terrestrial mammals. However, unlike in all mammalian species assessed to date, an unusual acellular gap was present between the perineural sheaths and the central core of axons in all the cutaneous nerves perhaps as mechanism to prevent high hydrostatic pressure from compressing and interfering with axonal conductance. Altogether the whale skin has an exceptionally dense low-threshold mechanosensory system innervation most likely adapted for sensing hydrodynamic stimuli, as well as nerves that can likely withstand high pressure experienced during deep dives.