Skin Denticles Research Articles

An Application of the Shark Skin Denticle Geometry for Windbreak Fence Design and Fabrication

Windbreak fences in open and urban areas can be used to effectively reduce the wind velocity. In this paper we examine how the geometrical shape of the windbreak fence can optimally mitigate wind velocity. We propose an approach for windbreak fence design based on a bionic parametric model of the shark skin denticle geometry, which improves the reduction of the wind velocity around and behind the windbreak fences. The generative model was used to estimate improvements by variations in the parameters of the fence panel's geometrical shape, inspired by shark skin denticles. The results of the Computational Fluid Dynamics (CFD) analysis indicates that the fence surface inspired by shark skin performs much better than both flat and corrugated surfaces. Taking into account the complex geometry of the surface inspired by shark skin denticles, we propose a fabrication process using an expanded polystyrene foam (EPS) material, created using an industrial robot arm with a hot-wire tool. Creating EPS moulds for the shark skin denticle panels allows for a richer variety material to be used in the final design, leading both to higher efficiency and a more attractive design.

Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles

Teeth and denticles belong to a specialized class of mineralizing epithelial appendages called odontodes. Although homology of oral teeth in jawed vertebrates is well supported, the evolutionary origin of teeth and their relationship with other odontode types is less clear. We compared the cellular and molecular mechanisms directing development of teeth and skin denticles in sharks, where both odontode types are retained. We show that teeth and denticles are deeply homologous developmental modules with equivalent underlying odontode gene regulatory networks (GRNs). Notably, the expression of the epithelial progenitor and stem cell marker sex-determining region Y-related box 2 (sox2) was tooth-specific and this correlates with notable differences in odontode regenerative ability. Whereas shark teeth retain the ancestral gnathostome character of continuous successional regeneration, new denticles arise only asynchronously with growth or after wounding. Sox2+ putative stem cells associated with the shark dental lamina (DL) emerge from a field of epithelial progenitors shared with anteriormost taste buds, before establishing within slow-cycling cell niches at the (i) superficial taste/tooth junction (T/TJ), and (ii) deep successional lamina (SL) where tooth regeneration initiates. Furthermore, during regeneration, cells from the superficial T/TJ migrate into the SL and contribute to new teeth, demonstrating persistent contribution of taste-associated progenitors to tooth regeneration in vivo. This data suggests a trajectory for tooth evolution involving cooption of the odontode GRN from nonregenerating denticles by sox2+ progenitors native to the oral taste epithelium, facilitating the evolution of a novel regenerative module of odontodes in the mouth of early jawed vertebrates: the teeth.

Hydrodynamic function of biomimetic shark skin: effect of denticle pattern and spacing

The structure of shark skin has been the subject of numerous studies and recently biomimetic shark skin has been fabricated with rigid denticles (scales) on a flexible substrate. This artificial skin can bend and generate thrust when attached to a mechanical controller. The ability to control the manufacture of biomimetic shark skin facilitates manipulation of surface parameters and understanding the effects of changing denticle patterns on locomotion. In this paper we investigate the effect of changing the spacing and arrangement of denticles on the surface of biomimetic shark skin on both static and dynamic locomotor performance. We designed 3D-printed flexible membranes with different denticle patterns and spacings: (1) staggered-overlapped, (2) linear-overlapped, and (3) linear-non-overlapped, and compared these to a 3D-printed smooth-surfaced control. These 3D printed shark skin models were then tested in a flow tank with a mechanical flapping device that allowed us to either hold the models in a stationary position or move them dynamically. We swam the membranes at a frequency of 1 Hz with different heave amplitudes (from ±1 cm to ±3 cm) while measuring forces, torques, self-propelled swimming speed, and cost of transport (COT). Static tests revealed drag reduction of denticle patterns compared to a smooth control at low speeds, but increased drag at speeds above 25 cm s−1. However, during dynamic (swimming) tests, the staggered-overlapped pattern produced the fastest swimming speeds with no significant increase in the COT at lower heave values. For instance, at a heave frequency of 1 Hz and amplitude of ±1 cm, swimming speed of the staggered-overlapped pattern increased by 25.2% over the smooth control. At higher heave amplitudes, significantly faster self-propelled swimming speeds were achieved by the staggered-overlapped pattern, but with higher COT. Only the staggered-overlapped pattern provides a significant swimming performance advantage over the smooth control and the other two denticle patterns. Quantitative hydrodynamic comparisons among skin models where control over manufacture allows alteration of design parameters provides a useful experimental tool for future work on the considerable natural diversity of shark skin denticles both among species and on different body locations.

Early development of rostrum saw-teeth in a fossil ray tests classical theories of the evolution of vertebrate dentitions.

In classical theory, teeth of vertebrate dentitions evolved from co-option of external skin denticles into the oral cavity. This hypothesis predicts that ordered tooth arrangement and regulated replacement in the oral dentition were also derived from skin denticles. The fossil batoid ray Schizorhiza stromeri (Chondrichthyes; Cretaceous) provides a test of this theory. Schizorhiza preserves an extended cartilaginous rostrum with closely spaced, alternating saw-teeth, different from sawfish and sawsharks today. Multiple replacement teeth reveal unique new data from micro-CT scanning, showing how the ‘cone-in-cone’ series of ordered saw-teeth sets arrange themselves developmentally, to become enclosed by the roots of pre-existing saw-teeth. At the rostrum tip, newly developing saw-teeth are present, as mineralized crown tips within a vascular, cartilaginous furrow; these reorient via two 90° rotations then relocate laterally between previously formed roots. Saw-tooth replacement slows mid-rostrum where fewer saw-teeth are regenerated. These exceptional developmental data reveal regulated order for serial self-renewal, maintaining the saw edge with ever-increasing saw-tooth size. This mimics tooth replacement in chondrichthyans, but differs in the crown reorientation and their enclosure directly between roots of predecessor saw-teeth. Schizorhiza saw-tooth development is decoupled from the jaw teeth and their replacement, dependent on a dental lamina. This highly specialized rostral saw, derived from diversification of skin denticles, is distinct from the dentition and demonstrates the potential developmental plasticity of skin denticles.

Evolutionary origins and development of saw-teeth on the sawfish and sawshark rostrum (Elasmobranchii; Chondrichthyes).

A well-known characteristic of chondrichthyans (e.g. sharks, rays) is their covering of external skin denticles (placoid scales), but less well understood is the wide morphological diversity that these skin denticles can show. Some of the more unusual of these are the tooth-like structures associated with the elongate cartilaginous rostrum ‘saw’ in three chondrichthyan groups: Pristiophoridae (sawsharks; Selachii), Pristidae (sawfish; Batoidea) and the fossil Sclerorhynchoidea (Batoidea). Comparative topographic and developmental studies of the ‘saw-teeth’ were undertaken in adults and embryos of these groups, by means of three-dimensional-rendered volumes from X-ray computed tomography. This provided data on development and relative arrangement in embryos, with regenerative replacement in adults. Saw-teeth are morphologically similar on the rostra of the Pristiophoridae and the Sclerorhynchoidea, with the same replacement modes, despite the lack of a close phylogenetic relationship. In both, tooth-like structures develop under the skin of the embryos, aligned with the rostrum surface, before rotating into lateral position and then attaching through a pedicel to the rostrum cartilage. As well, saw-teeth are replaced and added to as space becomes available. By contrast, saw-teeth in Pristidae insert into sockets in the rostrum cartilage, growing continuously and are not replaced. Despite superficial similarity to oral tooth developmental organization, saw-tooth spatial initiation arrangement is associated with rostrum growth. Replacement is space-dependent and more comparable to that of dermal skin denticles. We suggest these saw-teeth represent modified dermal denticles and lack the ‘many-for-one’ replacement characteristic of elasmobranch oral dentitions.

Elevated carbon dioxide alters the plasma composition and behaviour of a shark.

Increased carbon emissions from fossil fuels are increasing the pCO2 of the ocean surface waters in a process called ocean acidification. Elevated water pCO2 can induce physiological and behavioural effects in teleost fishes, although there appear to be large differences in sensitivity between species. There is currently no information available on the possible responses to future ocean acidification in elasmobranch fishes. We exposed small-spotted catsharks (Scyliorhinus canicula) to either control conditions or a year 2100 scenario of 990 μatm pCO2 for four weeks. We did not detect treatment effects on growth, resting metabolic rate, aerobic scope, skin denticle ultrastructure or skin denticle morphology. However, we found that the elevated pCO2 group buffered internal acidosis via [Formula: see text] accumulation with an associated increase in Na(+), indicating that the blood chemistry remained altered despite the long acclimation period. The elevated pCO2 group also exhibited a shift in their nocturnal swimming pattern from a pattern of many starts and stops to more continuous swimming. Although CO2-exposed teleost fishes can display reduced behavioural asymmetry (lateralization), the CO2-exposed sharks showed increased lateralization. These behavioural effects may suggest that elasmobranch neurophysiology is affected by CO2, as in some teleosts, or that the sharks detect CO2 as a constant stressor, which leads to altered behaviour. The potential direct effects of ocean acidification should henceforth be considered when assessing future anthropogenic effects on sharks.

Biomimetic shark skin: design, fabrication and hydrodynamic function.

Although the functional properties of shark skin have been of considerable interest to both biologists and engineers because of the complex hydrodynamic effects of surface roughness, no study to date has successfully fabricated a flexible biomimetic shark skin that allows detailed study of hydrodynamic function. We present the first study of the design, fabrication and hydrodynamic testing of a synthetic, flexible, shark skin membrane. A three-dimensional (3D) model of shark skin denticles was constructed using micro-CT imaging of the skin of the shortfin mako (Isurus oxyrinchus). Using 3D printing, thousands of rigid synthetic shark denticles were placed on flexible membranes in a controlled, linear-arrayed pattern. This flexible 3D printed shark skin model was then tested in water using a robotic flapping device that allowed us to either hold the models in a stationary position or move them dynamically at their self-propelled swimming speed. Compared with a smooth control model without denticles, the 3D printed shark skin showed increased swimming speed with reduced energy consumption under certain motion programs. For example, at a heave frequency of 1.5 Hz and an amplitude of ± 1 cm, swimming speed increased by 6.6% and the energy cost-of-transport was reduced by 5.9%. In addition, a leading-edge vortex with greater vorticity than the smooth control was generated by the 3D printed shark skin, which may explain the increased swimming speeds. The ability to fabricate synthetic biomimetic shark skin opens up a wide array of possible manipulations of surface roughness parameters, and the ability to examine the hydrodynamic consequences of diverse skin denticle shapes present in different shark species.

The hydrodynamic function of shark skin and two biomimetic applications

It has long been suspected that the denticles on shark skin reduce hydrodynamic drag during locomotion, and a number of man-made materials have been produced that purport to use shark-skin-like surface roughness to reduce drag during swimming. But no studies to date have tested these claims of drag reduction under dynamic and controlled conditions in which the swimming speed and hydrodynamics of shark skin and skin-like materials can be quantitatively compared with those of controls lacking surface ornamentation or with surfaces in different orientations. We use a flapping foil robotic device that allows accurate determination of the self-propelled swimming (SPS) speed of both rigid and flexible membrane-like foils made of shark skin and two biomimetic models of shark skin to measure locomotor performance. We studied the SPS speed of real shark skin, a silicone riblet material with evenly spaced ridges and a Speedo® 'shark skin-like' swimsuit fabric attached to rigid flat-plate foils and when made into flexible membrane-like foils. We found no consistent increase in swimming speed with Speedo® fabric, a 7.2% increase with riblet material, whereas shark skin membranes (but not rigid shark skin plates) showed a mean 12.3% increase in swimming speed compared with the same skin foils after removing the denticles. Deformation of the shark skin membrane is thus crucial to the drag-reducing effect of surface denticles. Digital particle image velocimetry (DPIV) of the flow field surrounding moving shark skin foils shows that skin denticles promote enhanced leading-edge suction, which might have contributed to the observed increase in swimming speed. Shark skin denticles might thus enhance thrust, as well as reduce drag.

By the Teeth of Their Skin, Cavefish Find Their Way

Event Abstract Back to Event By the Teeth of Their Skin, Cavefish Find Their Way Gal Haspel1*, Adina Schwartz2, Amy Streets2, Daniel E. Camacho3 and Daphne Soares2 1 National Institute of Neural Disorder and Stroke, United States 2 University of Maryland, Biology department, United States 3 Pontificia Universidad Católica del Ecuador, Facultad de Ciencias Exactas y Naturales, Ecuador We describe a mechanosensory system in which skin-teeth are used as sensory organs. Mechanosensation is a vital sensory modality for fishes. These animals usually create hydrodynamic images of their environments through specialized skin organs called neuromasts. The Ecuadorian cavefish, Astroblepus pholeter, lives in a fast current cave and shows relatively few neuromasts but a hypertrophy of skin denticles along the dorsal surface of its head and trunk. Here we show that A. pholeter uses its skin denticles for mechanosensation in the perpetually dark cave. We examine the anatomy, physiology and behaviour related to the mechanosensory role of skin denticles and demonstrate that this sensory system may present a case of adaptation that highlights an ancestral sensory organ. Figure 1 Figure 2 Keywords: Astroblepus pholeter, cavefish, denticles, mechanosensory, odontodes, skin-teeth Conference: Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012. Presentation Type: Poster Presentation (see alternatives below as well) Topic: Sensory: Mechanosensation Citation: Haspel G, Schwartz A, Streets A, Camacho DE and Soares D (2012). By the Teeth of Their Skin, Cavefish Find Their Way. Conference Abstract: Tenth International Congress of Neuroethology. doi: 10.3389/conf.fnbeh.2012.27.00312 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 30 Apr 2012; Published Online: 07 Jul 2012. * Correspondence: Dr. Gal Haspel, National Institute of Neural Disorder and Stroke, Bethesda, MD, 20892, United States, haspel@njit.edu Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Gal Haspel Adina Schwartz Amy Streets Daniel E Camacho Daphne Soares Google Gal Haspel Adina Schwartz Amy Streets Daniel E Camacho Daphne Soares Google Scholar Gal Haspel Adina Schwartz Amy Streets Daniel E Camacho Daphne Soares PubMed Gal Haspel Adina Schwartz Amy Streets Daniel E Camacho Daphne Soares Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Evolution of developmental pattern for vertebrate dentitions: an oro‐pharyngeal specific mechanism

Classically the oral dentition with teeth regulated into a successional iterative order was thought to have evolved from the superficial skin denticles migrating into the mouth at the stage when jaws evolved. The canonical view is that the initiation of a pattern order for teeth at the mouth margin required development of a sub-epithelial, permanent dental lamina. This provided regulated tooth production in advance of functional need, as exemplified by the Chondrichthyes. It had been assumed that teeth in the Osteichthyes form in this way as in tetrapods. However, this has been shown not to be true for many osteichthyan fish where a dental lamina of this kind does not form, but teeth are regularly patterned and replaced. We question the evolutionary origin of pattern information for the dentition driven by new morphological data on spatial initiation of skin denticles in the catshark. We review recent gene expression data for spatio-temporal order of tooth initiation for Scyliorhinus canicula, selected teleosts in both oral and pharyngeal dentitions, and Neoceratodus forsteri. Although denticles in the chondrichthyan skin appear not to follow a strict pattern order in space and time, tooth replacement in a functional system occurs with precise timing and spatial order. We suggest that the patterning mechanism observed for the oral and pharyngeal dentition is unique to the vertebrate oro-pharynx and independent of the skin system. Therefore, co-option of a successional iterative pattern occurred in evolution not from the skin but from mechanisms existing in the oro-pharynx of now extinct agnathans.

The odontode explosion: The origin of tooth‐like structures in vertebrates

Essentially we show recent data to shed new light on the thorny controversy of how teeth arose in evolution. Essentially we show (a) how teeth can form equally from any epithelium, be it endoderm, ectoderm or a combination of the two and (b) that the gene expression programs of oral versus pharyngeal teeth are remarkably similar. Classic theories suggest that (i) skin denticles evolved first and odontode-inductive surface ectoderm merged inside the oral cavity to form teeth (the 'outside-in' hypothesis) or that (ii) patterned odontodes evolved first from endoderm deep inside the pharyngeal cavity (the 'inside-out' hypothesis). We propose a new perspective that views odontodes as structures sharing a deep molecular homology, united by sets of co-expressed genes defining a competent thickened epithelium and a collaborative neural crest-derived ectomesenchyme. Simply put, odontodes develop 'inside and out', wherever and whenever these co-expressed gene sets signal to one another. Our perspective complements the classic theories and highlights an agenda for specific experimental manipulations in model and non-model organisms.

A revised hypothesis on the evolutionary origin of the vertebrate dentition

Despite claims to the contrary, the evolutionary origin of teeth has not been definitely established. The classical 'outside in' theory stating that teeth derive from odontodes that invaded the oral cavity in conjunction with the origin of jaws has been challenged by an alternative, 'inside out', hypothesis suggesting that teeth evolved from pharyngeal denticles, as endodermal derivatives, prior to the origin of jaws. We propose a third scenario, a revised 'outside in' hypothesis (Huysseune et al., 2009). Our hypothesis is consistent with the current data and avoids speculations about convergent tooth evolution. We suggest that teeth may indeed have arisen before the origin of jaws, a pillar of the 'inside out' hypothesis, but not from the endodermally lined posterior pharynx. Rather, teeth would have been the result of competent, odontode-forming ectoderm invading the oropharyngeal cavity through the mouth as well as through the gill slits, interacting with neural-crest derived mesenchyme. Arguments in support of this hypothesis are: (i) the observation that pharyngeal teeth are present only in species known to possess gill slits, and disappear from the pharyngeal region in early tetrapods concomitant with the closure of gill slits; (ii) the assumption that endoderm alone, together with neural crest, cannot form teeth; (iii) observations on pharyngeal tooth and gill slit formation in extant species; (iv) the observation that the dental lamina (sensu Reif, 1982) is not a prerequisite for tooth formation; (v) evidence that patterning does not distinguish pharyngeal from skin denticles, and (vi) the observation on zebrafish mutants affected in the dermal skeleton. This 'modified outside in' hypothesis can be tested both on paleontological data (it predicts a correlation of the presence of pharyngeal teeth and of gill slits), and on developmental data in extant species (it predicts the necessity of an ectodermal signal to make [pharyngeal] teeth).

Evolutionary and developmental origins of the vertebrate dentition

According to the classical theory, teeth derive from odontodes that invaded the oral cavity in conjunction with the origin of jaws (the 'outside in' theory). A recent alternative hypothesis suggests that teeth evolved prior to the origin of jaws as endodermal derivatives (the 'inside out' hypothesis). We compare the two theories in the light of current data and propose a third scenario, a revised 'outside in' hypothesis. We suggest that teeth may have arisen before the origin of jaws, as a result of competent, odontode-forming ectoderm invading the oropharyngeal cavity through the mouth as well as through the gill slits, interacting with neural crest-derived mesenchyme. This hypothesis revives the homology between skin denticles (odontodes) and teeth. Our hypothesis is based on (1) the assumption that endoderm alone, together with neural crest, cannot form teeth; (2) the observation that pharyngeal teeth are present only in species known to possess gill slits, and disappear from the pharyngeal region in early tetrapods concomitant with the closure of gill slits, and (3) the observation that the dental lamina (sensu Reif, 1982) is not a prerequisite for teeth to form. We next discuss the progress that has been made to understand the spatially restricted loss of teeth from certain arches, and the many questions that remain regarding the ontogenetic loss of teeth in specific taxa. The recent advances that have been made in our knowledge on the molecular control of tooth formation in non-mammalians (mostly in some teleost model species) will undoubtedly contribute to answering these questions in the coming years.

A possible Late Cambrian vertebrate from Australia

THE fossil record of early vertebrates starts with certainty with the dermal armour of agnathan fish from the Early–Middle Ordovician of Australia1,2. Recent controversial acceptance that conodonts3 and the fragments called Anatolepis4,5 may be vertebrate remains6, extends their fossil record back to the Late Cambrian. Now a new type of phosphatic skeleton from Australia shows a three-layered structure that indicates vertebrate affinity, but with several unique features not known in other vertebrates. The new evidence challenges the most widely accepted current theory for the development of the vertebrate skeleton7–11, which assumes the odontode (skin denticle) to be the primitive patterning component. The Australian material provides an alternative model for early vertebrate dermal armour with which to assess the vertebrate-like hard tissues in conodonts12,13 and the dermal armour of Anatolepis4–6,14.