Abstract
Innervation in the glabrous skin of cetaceans (baleen mysticetes and toothed odontocetes) has evolved over 50 million years in the marine realm. The obligate marine lifestyle and behaviors of these 89 extant species suggest a role for cutaneous detection of hydrodynamic signals of flow and pressure waves, tactile contact, hydrostatic pressure, and temperature. This report presents the first study of somatosensory anatomy in a mysticete, the flank skin of Megaptera novaeangliae (humpback whales). Biopsy collection, handling and immunohistochemical methods were optimized tovisualize sensory nerves in whale skin, and resolve research problems associated with the lipid-dense tissue. The biopsy tip was modified to preserve sample integrity for histological research. To improve penetration of immunolabeling antibodies, a pretreatment method was developed to remove lipids and melanin pigment, resulting in reduced background noise, autofluorescence, and non-specific binding.Cetacean skin and innervation are more elaborate than that of land mammals. Their distinct pencillate evaginations of dermis (papillae) interdigitate with cellularly dense epidermal pegs. Unlike the thin stratified skin of land mammals, with its individual branching axons and a few discreet end-organs, the whale's axons persist in tight, parallel multi-afferent bundles from the deep dermis to distal papillae. Bundles divide, but axons do not branch. Immunolabeling revealed a variety of novel, complex three-dimensional structures, bifurcations, and contact patterns with the dermal-epidermal junction. Specializations in the papillae include bridges, tangled and simple loops, and rarely, endbulbs or a Meissner's-like corpuscle. Each dermal stratum has a neurovascular plexus, which were imaged transporting dense matrices of low-threshold mechanosensory fibers. From the neural matrixes, bundled fibers travel in fascicles ensheathed by a perineurium. Morphometric analyses compared innervation factors between dermal strata. Fascicle size, axon diameter, and axons per bundle decreased in superficial regions. Axon density in the flank was 53/mm², similar to human thigh skin. Neural fascicles containeda large unoccupied space, which has not been described in other species. Fascicles of terrestrial mammals have small inter-axonal spaces filled with endoneurial fluid thatcreates a positive oncotic pressure. The whale's increased volume of endoneurial fluid may be a mechanism of increasing pressure in the fascicle, protecting the nerve bundlefrom extreme external pressures of deep foraging dives. The mysticete somatosensory system is elegant in its economical use of the fundamental sensory element, axons, to form mechanosensory structures that are diverse, pleomorphic, and scalable. The elongate papillae that encapsulate and house nerve termini, functioning as sensory end-organs, focus and filter physical force stimuli withinthis pressure-transducing tissue. In summary: this immunohistochemical study describes the structures and organization of innervation in the flank skin of humpback whales.Comparative projects using skin from specialized body regions, and other species, will begin to unravel the phylogeny and abilities of cetacean somatosensory innervation.