Second Harmonic Generation Imaging Reveals Entanglement of Collagen Fibers in the Elephant Trunk Skin Dermis

Abstract

Form-function relationships often have tradeoffs: if a material is tough, it is often inflexible, and vice versa. This is particularly relevant for the elephant trunk, where the skin should be protective yet elastic. To investigate how this is achieved, we used classical histochemical staining and second harmonic generation microscopy to describe the morphology and composition of elephant trunk skin. We report structure at the macro and micro scales, from the thickness of the dermis to the interaction of 10 µm thick collagen fibers. We analyzed several sites along the length of the trunk, to compare and contrast the dorsal-ventral and proximal-distal skin morphologies and compositions. We find the dorsal skin of the elephant trunk can have keratin armor layers over 2mm thick, which is nearly 100 times the thickness of the equivalent layer in human skin. We also found that the structural support layer (the dermis) of elephant trunk contains a distribution of collagen-I (COL1) fibers in both perpendicular and parallel arrangement. The bimodal distribution of collagen is seen across all portions of the trunk, and is dissimilar from that of human skin where one orientation dominates within a body site. We hypothesize that this distribution of COL1 in the elephant trunk allows both flexibility and load-bearing capabilities. Additionally, when viewing individual fiber interaction of 10 µm thick collagen, we find the fiber crossings per unit volume are five times more common than in human skin, suggesting that the fibers are entangled. We surmise that these intriguing structures permit both flexibility and strength in the elephant trunk. The complex nature of the elephant skin may inspire the design of materials that can combine strength and flexibility.

Elephants develop wrinkles through both form and function

“…It has been shown that the distal dorsal part of the trunk contributes the most to trunk stretching and that the ventral side stretches comparably little when the trunk is extended 1 . The distal ventral trunk has been described to be used in sweeping food together 9 and most trunk manipulation movements are accomplished with gripping and grabbing on the ventral side 54 . Specifically, the trunk section just before the trunk tip is used in holding food or other objects, often between the lateral skin ridges that go along the ventral trunk and that have a very high density of whiskers in this distinct trunk part 49 .…”

“…This skin has a protective function, but elephants also utilize it to assist in gripping objects when they wrap 6 or sweep food using the wrinkled ventral portion at the tip of the trunk 7 . Elephant skin is known for some simple gross mechanical properties, such as a cracked epidermis for thermoregulation 8 in African elephants and entangled collagen in the dermis of the trunk for added protection and extension 9 . The trunk's mobility and flexibility are enabled by a highly complex musculature [10][11][12] , controlled by a very elaborate motor nucleus 13 .…”

“…The tough and dense skin protecting the body of the elephant from exposure to the elements is cracked for thermoregulation 15 . This tough skin has flexibility by having collagen fiber arranged in all directions allowing for a combination of strength and flexibility 16 .The integumentum (outer layer) of the trunk, however, is densely packed with wrinkles that eventually transition to folds as you approach the proximal portion 17 . The formation and function of these wrinkles are thought to be for extension on the dorsal side 17 and grip on the ventral side 18 .…”