Groovy and Gnarly: Surface Wrinkles as a Multifunctional Motif for Terrestrial and Marine Environments

Abstract

Synopsis From large ventral pleats of humpback whales to nanoscale ridges on flower petals, wrinkled structures are omnipresent, multifunctional, and found at hugely diverse scales. Depending on the particulars of the biological system—its environment, morphology, and mechanical properties—wrinkles may control adhesion, friction, wetting, or drag; promote interfacial exchange; act as flow channels; or contribute to stretching, mechanical integrity, or structural color. Undulations on natural surfaces primarily arise from stress-induced instabilities of surface layers (e.g., buckling) during growth or aging. Variation in the material properties of surface layers and in the magnitude and orientation of intrinsic stresses during growth lead to a variety of wrinkling morphologies and patterns which, in turn, reflect the wide range of biophysical challenges wrinkled surfaces can solve. Therefore, investigating how surface wrinkles vary and are implemented across biological systems is key to understanding their structure–function relationships. In this work, we synthesize the literature in a metadata analysis of surface wrinkling in various terrestrial and marine organisms to review important morphological parameters and classify functional aspects of surface wrinkles in relation to the size and ecology of organisms. Building on our previous and current experimental studies, we explore case studies on nano/micro-scale wrinkles in biofilms, plant surfaces, and basking shark filter structures to compare developmental and structure-vs-function aspects of wrinkles with vastly different size scales and environmental demands. In doing this and by contrasting wrinkle development in soft and hard biological systems, we provide a template of structure–function relationships of biological surface wrinkles and an outlook for functionalized wrinkled biomimetic surfaces.

Curvature in Biological Systems: Its Quantification, Emergence, and Implications across the Scales

“…[ 76 ] The similarities in physical models and biological wrinkle patterns suggest a common role of mechanical instabilities being an important driving force for the development of form in biology. [ 82 ] A similar wrinkling mechanism is found in the hibiscus petal that modulates its optical properties (Figure 7f). [ 40 ] Even earlier in embryonic development, compressive mechanical stress due to differential tissue growth is suggested to induce the very first buckling events in forming cranial flexure (bending of the neuronal tube prior to brain development) which then eventually twists rightward.…”

Wrinkle nanostructures generate a novel form of blue structural color in great argus flight feathers

“…These shared features of surface keratin nanostructures among archosaurs ( Figure 3 ) hint at a possible homology of their underlying developmental mechanisms. While wrinkle structures are widely found in living organisms, 32 , 33 and are actively under consideration for biomimetic applications, 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 this is the first example of a biophotonic (i.e., color-producing) wrinkle nanostructure in birds.…”

Biomimetic models of fish gill rakers as lateral displacement arrays for particle separation

“…While the morphometrics of American shad were used to represent ram suspension-feeding fish dimensions, our biomimetic model is applicable to multiple species with a comparable rib-and-slot arrangement of steps. For example, suspension-feeding species that, like American shad, have gill rakers forming d-type ribs with a slot aspect ratio of less than 3-4 include Atlantic herring (Clupea harengus, Clupeidae) [46], European anchovy (Engraulis encrasicolus, Engraulidae) [46] and basking sharks (Cetorhinus maximus, Cetorhinidae) [47]. Therefore, the generalized gill rakers and oral cavity configurations used in our physical and computational models are broadly applicable and can be readily modified to reflect the specific dimensions of many species that have gill rakers with a d-type rib-and-slot arrangement of steps.…”

“…Both mucus and protuberances have been hypothesized or demonstrated in experiments with a diverse variety of live suspension-feeding fish to play key roles in particle retention and fluid dynamics [46,63]. Microridges detected on the leading edge of basking shark gill rakers have recently been demonstrated in CFD simulations to have the potential for profound effects on flow patterns during filtration [47]. Given the extensive interactions reported here between particles and the gill raker walls, modifications of the wall surface properties and microstructures by mucus, tissue layers and/or protuberances will alter particle trajectories within the slots.…”