Diversity of dermal denticle structure in sharks: Skin surface roughness and three‐dimensional morphology

Shark skin is covered with numerous placoid scales or dermal denticles. While previous research has used scanning electron microscopy and histology to demonstrate that denticles vary both around the body of a shark and among species, no previous study has quantified three‐dimensional (3D) denticle structure and surface roughness to provide a quantitative analysis of skin surface texture. We quantified differences in denticle shape and size on the skin of three individual smooth dogfish sharks (Mustelus canis) using micro‐CT scanning, gel‐based surface profilometry, and histology. On each smooth dogfish, we imaged between 8 and 20 distinct areas on the body and fins, and obtained further comparative skin surface data from leopard, Atlantic sharpnose, shortfin mako, spiny dogfish, gulper, angel, and white sharks. We generated 3D images of individual denticles and measured denticle volume, surface area, and crown angle from the micro‐CT scans. Surface profilometry was used to quantify metrology variables such as roughness, skew, kurtosis, and the height and spacing of surface features. These measurements confirmed that denticles on different body areas of smooth dogfish varied widely in size, shape, and spacing. Denticles near the snout are smooth, paver‐like, and large relative to denticles on the body. Body denticles on smooth dogfish generally have between one and three distinct ridges, a diamond‐like surface shape, and a dorsoventral gradient in spacing and roughness. Ridges were spaced on average 56 µm apart, and had a mean height of 6.5 µm, comparable to denticles from shortfin mako sharks, and with narrower spacing and lower heights than other species measured. We observed considerable variation in denticle structure among regions on the pectoral, dorsal, and caudal fins, including a leading‐to‐trailing edge gradient in roughness for each region. Surface roughness in smooth dogfish varied around the body from 3 to 42 microns.     

Scale morphology and flexibility in the shortfin mako Isurus oxyrinchus and the blacktip shark Carcharhinus limbatus

We quantified placoid scale morphology and flexibility in the shortfin mako Isurus oxyrinchus and the blacktip shark Carcharhinus limbatus. The shortfin mako shark has shorter scales than the blacktip shark. The majority of the shortfin mako shark scales have three longitudinal riblets with narrow spacing and shallow grooves. In comparison, the blacktip shark scales have five to seven longitudinal riblets with wider spacing and deeper grooves. Manual manipulation of the scales at 16 regions on the body and fins revealed a range of scale flexibility, from regions of nonerectable scales such as on the leading edge of the fins to highly erectable scales along the flank of the shortfin mako shark body. The flank scales of the shortfin mako shark can be erected to a greater angle than the flank scales of the blacktip shark. The shortfin mako shark has a region of highly flexible scales on the lateral flank that can be erected to at least 50°. The scales of the two species are anchored in the stratum laxum of the dermis. The attachment fibers of the scales in both species appear to be almost exclusively collagen, with elastin fibers visible in the stratum laxum of both species. The most erectable scales of the shortfin mako shark have long crowns and relatively short bases that are wider than long. The combination of a long crown length to short base length facilitates pivoting of the scales. Erection of flank scales and resulting drag reduction is hypothesized to be passively driven by localized flow patterns over the skin. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Sexual Dimorphisms in the Dermal Denticles of the Lesser-Spotted Catshark,Scyliorhinus canicula (Linnaeus, 1758)

The dermal layers of several elasmobranch species have been shown to be sexually dimorphic. Generally, when this occurs the females have thicker dermal layers compared to those of males. This sexual dimorphism has been suggested to occur as a response to male biting during mating. Although male biting as a copulatory behaviour in Scyliorhinus canicula has been widely speculated to occur, only relatively recently has this behaviour been observed. Male S. canicula use their mouths to bite the female’s pectoral and caudal fins as part of their pre-copulatory behaviour and to grasp females during copulation. Previous work has shown that female S. canicula have a thicker epidermis compared to that of males. The structure of the dermal denticles in females may also differ from that of males in order to protect against male biting or to provide a greater degree of friction in order to allow the male more purchase. This study reveals that the length, width and density of the dermal denticles of mature male and female S. canicula are sexually dimorphic across the integument in areas where males have been observed to bite and wrap themselves around females (pectoral fin, area posterior to the pectoral fin, caudal fin, and pelvic girdle). No significant differences in the dermal denticle dimensions were found in other body areas examined (head, dorsal skin and caudal peduncle). Sexually dimorphic dermal denticles in mature S. canicula could be a response to male biting/wrapping as part of the copulatory process.     

The characterization, replication and testing of dermal denticles of Scyliorhinus canicula for physical mechanisms of biofouling prevention

There is a current need to develop novel non-toxic antifouling materials. The mechanisms utilized by marine organisms to prevent fouling of external surfaces are of interest in this regard. Biomimicry of these mechanisms and the ability to transfer the antifouling characteristics of these surfaces to artificial surfaces are a highly attractive prospect to those developing antifouling technologies. In order to achieve this, the mechanisms responsible for any antifouling ability must be elucidated from the study of the natural organism and the critical surface parameters responsible for fouling reduction. Dermal denticles of members of the shark family have been speculated to possess some natural, as yet unidentified antifouling mechanism related to the physical presence of denticles. In this study, the dermal denticles of one particular member of the slow-swimming sharks, Scyliorhinus canicula were characterized and it was found that a significant natural variation in denticle dimensions exists in this species. The degree of denticle surface contamination was quantified on denticles at various locations and it was determined that the degree of contamination of the dorsal surface of denticles varies with the position on the shark body. In addition, we successfully produced synthetic sharkskin samples using the real skin as a template. Testing of the produced synthetic skin in field conditions resulted in significant differences in material attachment on surfaces exhibiting denticles of different dimensions.     

Whole-body lift and ground effect during pectoral fin locomotion in the northern spearnose poacher (Agonopsis vulsa)

The northern spearnose poacher, Agonopsis vulsa, is a benthic, heavily armored fish that swims primarily using pectoral fins. High-speed kinematics, whole-body lift measurements, and flow visualization were used to study how A. vulsa overcomes substantial negative buoyancy while generating forward thrust. Kinematics for five freely swimming poachers indicate that individuals tend to swim near the bottom (within 1 cm) with a consistently small (less than 1°) pitch angle of the body. When the poachers swam more than 1 cm above the bottom, however, body pitch angles were higher and varied inversely with speed, suggesting that lift may help overcome negative buoyancy. To determine the contribution of the body to total lift, fins were removed from euthanized fish (n=3) and the lift and drag from the body were measured in a flume. Lift and drag were found to increase with increasing flow velocity and angle of attack (ANCOVA, p<0.0001 for both effects). Lift force from the body was found to supply approximately half of the force necessary to overcome negative buoyancy when the fish were swimming more than 1 cm above the bottom. Lastly, flow visualization experiments were performed to examine the mechanism of lift generation for near-bottom swimming. A vortex in the wake of the pectoral fins was observed to interact strongly with the substratum when the animals approached the bottom. These flow patterns suggest that, when swimming within 1 cm of the bottom, poachers may use hydrodynamic ground effect to augment lift, thereby counteracting negative buoyancy.     

Reduction of barnacle recruitment on micro‐textured surfaces: Analysis of effective topographic characteristics and evaluation of skin friction

This study investigates five designed micro‐textured surfaces and their effects on barnacle fouling and hydrodynamic drag. Three of the micro‐textures were developed in the present study and evaluated together with two commercial riblet films. All micro‐structures were arranged as longitudinal grooves with different profile depths, widths and angles of inclination. In field tests the recruitment of the barnacle Balanus improvisus on micro‐textured surfaces and smooth controls was evaluated. All micro‐textured surfaces reduced recruitment, and the most efficient texture reduced recruitment by 98%. For some micro‐textures the reduction of recruitment declined as settlement intensity increased. In a correlative analysis, the trigonometric inclination of the micro‐structures explained most of the recruitment reduction. The steepest angle of inclination caused a massive reduction in barnacle settlement. Surface micro‐structures may affect the boundary‐layer flow and the hydrodynamic drag (skin friction) of the surface. The skin friction was empirically measured in a flow channel using a sub‐set of the tested micro‐textures. The measurements of skin friction showed that the orientation of the microstructures is important, with a minimum friction when the grooves are parallel to the flow. For one of the micro‐textures the skin friction was ca 10% lower compared to a hydraulically smooth surface. It is concluded that, depending on the flow speed, micro‐textures will not significantly increase skin friction when arranged parallel to the flow, even at moderate protrusion through the viscous sub‐layer.     

Male secondary sexual traits are hydrodynamic devices for enhancing swimming performance in a monogamous filefish Paramonacanthus japonicus

The Japanese filefish Paramonacanthus japonicus has extreme sexual dimorphism in its overall shape, even though its mating system is monogamy with biparental care. This sexual dimorphism is mainly due to the development of secondary sexual traits in males. Males become more slender in body with elevated soft dorsal and anal fins as they mature. We examined the function of such male secondary sexual traits by field research and fluid-dynamic analysis. Underwater observations showed that movement rate and steady swimming speed of males were higher than those of females. Male and female P. japonicus showed similar feeding habits and egg-tending behavior, although males attacked potential egg predators more frequently. A wind-tunnel experiment using the air bearing and spring system showed that the drag coefficient of males was significantly lower than that of females, indicating a lower male hydrodynamic drag performance. Also, male elevated soft dorsal and anal fins are considered to give rise to higher thrust performance in monacanthids. Thus, these results suggest that male secondary sexual traits are hydrodynamic devices for enhancing swimming performance that seem to be actually functional under natural conditions. We discuss the evolution of such conspicuous male sexual traits in P. japonicus. Electronic Publication     

Characterization of the pelagic shark‐fin trade in north‐central Chile by genetic identification and trader surveys

Shark fins have become a highly valued commodity with the major Asian fin‐trade centres supplied from global sources, including Chile. With growing concerns about the resilience of shark populations to heavy fishing pressure, there is a need for better information on shark landings to aid management efforts. In the widespread absence of shark landing records especially by species, monitoring the fin trade has been proposed as a way to assess species exploitation levels. Here, the first species assessment of the Chilean shark‐fin trade was provided. The goals of this study were to (1) determine the species composition and relative species proportion of sharks utilized in the fin trade, (2) determine the relationship between fin trader market names and species and (3) assess trader accuracy in identifying shark fin species based on fin photographs. Fins were analysed from two different fin drying facilities (n = 654) (secaderos) and two fin‐storage warehouses (n = 251). In contrast to official government landing records that only document four species in the landings, molecular species identification of the fins demonstrated that at least 10 pelagic shark species are present in the north‐central Chilean shark fin trade: Alopias superciliosus, Alopias vulpinus, Carcharhinus obscurus, Galeorhinus galeus, Isurus oxyrinchus, Isurus paucus, Lamna nasus, Prionace glauca, Sphyrna lewini, Sphyrna zygaena. The species composition of the fins from the secaderos was P. glauca (83·9%), I. oxyrinchus (13·6%), L. nasus (1·7%) and A. superciliosus (0·2%). There was generally good agreement between market names and single shark species for the trade categories ‘Azulejo’, ‘Tiburon’, ‘Tintorera’, ‘Cola de zorro’ and ‘Martillo’. In contrast, the market category ‘Carcharhinus’ consisted of a mixture of at least five species. The molecular results also identified two species (S. lewini and I. paucus) not previously recorded in Chilean waters. The fin identification survey given to nine regional traders demonstrated that they were highly accurate in recognizing pictures of fins from P. glauca and I. oxyrinchus. The overall strong concordance between market categories and fins from single species and the trader accuracy in survey fin identification suggests that monitoring the Chilean fin trade by market names will provide a reasonably accurate picture of the volume of sharks landed by species.     

Structure and topographic distribution of oral denticles in elasmobranch fishes

The placoid scales, or denticles, of the external epidermis of elasmobranchs are well known as a hard protective coat over the skin to reduce abrasion or as elements to reduce hydrodynamic drag. However, the structure and function of denticles within the oral cavity is uncertain. Using stereological and scanning electron microscopy, this study examines the structure and distribution of oral denticles in a range of elasmobranchs. Of the batoids analyzed, only members of the Rhinobatidae possessed oral denticles, with no denticles found in the members sampled in the Gymnuridae or Dasyatidae. In contrast, oral denticles were located in all the selachians examined, except for members of the Orectolobidae. Within the selachians, the denticles of the Carcharhinidae have a grooved surface and a central spine, which is angled toward the posterior of the mouth. These denticular adaptations are beneficial to reduce hydrodynamic drag, an advantage for these free-swimming species with ram ventilation. Alternatively, members of the Hemiscyllidae have broad bulbous denticles that often overlap, providing a hard surface to protect the epithelium from abrasion during the consumption of hard-bodied prey. The distribution and high number of oral denticles appears to spatially compromise the capacity for oral (taste) papillae to populate the oropharyngeal cavity but provides increased friction and grip on prey items as they are manipulated within the mouth.     

Occipital spine of Orthacanthus (Xenacanthidae,Elasmobranchii): Structure and growth

The morphology of 16 occipital spines of the xenacanthid Orthacanthus from Upper Carboniferous deposits of Robinson (Kansas, USA), Nýřan (Czech Republic) and Puertollano (Spain) is described. The nonreplaced spines reveal the growth pattern of the shark. Moreover, the relationship between growth and paleoenvironmental conditions can be used to determine paleoecological conditions. Both external and internal morphology indicate that the spine was superficially inserted in the skin. During growth, the spine moved from a deep position in the dermis, in which trabecular dentine is formed, to a more superficial location in which centrifugally growing lamellar dentine was formed. Centripetally growing lamellar dentine was deposited more slowly than the centrifugally growing dentine; it obliterated the pulp cavity. The denticles are independent dermal elements formed by a dermal papilla and secondarily attached by dentine to the spine proper. The number of denticles per annual cycle and the density of denticulation vary with the growth rate. Moreover, the ratio of length of denticulated region to total length of the spine changes throughout ontogeny. In consequence, those features cannot be used for systematic purposes without a careful analysis of the variability. Centrifugally growing lamellar dentine in spines from Robinson shows a regular alternation of layers, suggesting tidal conditions in the environment in which the sharks lived. Monthly and seasonal cycles also occur. Tidal (lunar) cyclicity is also observed in the denticles: size and distance between denticles increase and decrease gradually, forming waves that are considered seasonal and yearly cycles. The observed regularity could be related to the variation in calcium phosphate deposition following the cyclical changes in water temperature produced in the tidal zone. Monthly and seasonal cycles are the result of the interaction of the solar and tidal (lunar) cycles. The cyclical pattern of growth is used to determine the age and growth rates. Orthacanthus was a fast‐growing shark like the Recent sharks Isurus, Mustelus, and Negaprion. J. Morphol. 242:1–45, 1999. © 1999 Wiley‐Liss, Inc.     

General descriptions of the dermis structure of a juvenile whale shark Rhincodon typus from the Gulf of California

The aim of this study is to provide preliminary observations on the microanatomy of Rhincodon typus skin using histology and electron microscopy analyses. Skin biopsies were obtained from a deceased juvenile male shark (548 cm total length) stranded in La Paz, Mexico, during February 2018. The results of this study evidenced the basic structure of the dermal denticles in the epidermis of the trunk of the shark, as well as the composition of the connective tissue in the hypodermis. Histological images of the hypodermis showed a high concentration of collagen fibres, formed by a large number of fine and wavy fibres of compact shape and little intercellular substance.     

Trigonognathus kabeyai,a new genus and species of the squalid sharks from Japan

Two specimens of the peculiar squalid shark,Trigonognathus kabeyai gen. et sp. nov., were collected from the coastal waters of Wakayama and Tokushima, Japan, by bottom trawl at depths of 330 and 360 meters. Shape of teeth similar in both jaws; slender, unicuspid, canine-like, without any cusplets or serrations, with weak thin fold on both lingual and labial sides in anterior teeth on both jaws; tooth at symphysis of each jaw longest. Interspace between teeth very wide. Both jaws triangular in shape. Most of dermal denticles on body and head roughly rhombic, swollen very much near central part, with about 10–40 facets on the dorsal surface of its crown. Preoral snout length very short. Many small organs considered to be photophores present mainly on ventral surfaces of head and body.     

The denticle surface of thresher shark tails: Three-dimensional structure and comparison to other pelagic species

Shark skin denticles (scales) are diverse in morphology both among species and across the body of single individuals, although the function of this diversity is poorly understood. The extremely elongate and highly flexible tail of thresher sharks provides an opportunity to characterize gradients in denticle surface characteristics along the length of the tail and assess correlations between denticle morphology and tail kinematics. We measured denticle morphology on the caudal fin of three mature and two embryo common thresher sharks (Alopias vulpinus), and we compared thresher tail denticles to those of eleven other shark species. Using surface profilometry, we quantified 3D-denticle patterning and texture along the tail of threshers (27 regions in adults, and 16 regions in embryos). We report that tails of thresher embryos have a membrane that covers the denticles and reduces surface roughness. In mature thresher tails, surfaces have an average roughness of 5.6 μm which is smoother than some other pelagic shark species, but similar in roughness to blacktip, porbeagle, and bonnethead shark tails. There is no gradient down the tail in roughness for the middle or trailing edge regions and hence no correlation with kinematic amplitude or inferred magnitude of flow separation along the tail during locomotion. Along the length of the tail there is a leading-to-trailing-edge gradient with larger leading edge denticles that lack ridges (average roughness = 9.6 μm), and smaller trailing edge denticles with 5 ridges (average roughness = 5.7 μm). Thresher shark tails have many missing denticles visible as gaps in the surface, and we present evidence that these denticles are being replaced by new denticles that emerge from the skin below.     

Teeth outside the mouth: The evolution and development of shark denticles

Vertebrate skin appendages are incredibly diverse. This diversity, which includes structures such as scales, feathers, and hair, likely evolved from a shared anatomical placode, suggesting broad conservation of the early development of these organs. Some of the earliest known skin appendages are dentine and enamel-rich tooth-like structures, collectively known as odontodes. These appendages evolved over 450 million years ago. Elasmobranchs (sharks, skates, and rays) have retained these ancient skin appendages in the form of both dermal denticles (scales) and oral teeth. Despite our knowledge of denticle function in adult sharks, our understanding of their development and morphogenesis is less advanced. Even though denticles in sharks appear structurally similar to oral teeth, there has been limited data directly comparing the molecular development of these distinct elements. Here, we chart the development of denticles in the embryonic small-spotted catshark (Scyliorhinus canicula) and characterize the expression of conserved genes known to mediate dental development. We find that shark denticle development shares a vast gene expression signature with developing teeth. However, denticles have restricted regenerative potential, as they lack a sox2+ stem cell niche associated with the maintenance of a dental lamina, an essential requirement for continuous tooth replacement. We compare developing denticles to other skin appendages, including both sensory skin appendages and avian feathers. This reveals that denticles are not only tooth-like in structure, but that they also share an ancient developmental gene set that is likely common to all epidermal appendages.     

Comparative squamation of the lateral line canal pores in sharks

The current study collected the first quantitative data on lateral line pore squamation patterns in sharks and assessed whether divergent squamation patterns are similar to experimental models that cause reduction in boundary layer turbulence. In addition, the hypothesis that divergent orientation angles are exclusively found in fast‐swimming shark species was tested. The posterior lateral line and supraorbital lateral line pore squamation of the fast‐swimming pelagic shortfin mako shark Isurus oxyrinchus and the slow‐swimming epi‐benthic spiny dogfish shark Squalus acanthias was examined. Pore scale morphology and pore coverage were qualitatively analysed and compared. In addition, pore squamation orientation patterns were quantified for four regions along the posterior lateral line and compared for both species. Isurus oxyrinchus possessed consistent pore scale coverage among sampled regions and had a divergent squamation pattern with multiple scale rows directed dorsally and ventrally away from the anterior margin of the pore with an average divergent angle of 13° for the first row of scales. Squalus acanthias possessed variable amounts of scale coverage among the sampled regions and had a divergent squamation pattern with multiple scale rows directed ventrally away from the anterior margin of the pore with an average angle of 19° for the first row of scales. Overall, the squamation pattern measured in I. oxyrinchus fell within the parameters used in the fluid flow analysis, which suggests that this pattern may reduce boundary layer turbulence and affect lateral line sensitivity. The exclusively ventral oriented scale pattern seen in S. acanthias possessed a high degree of divergence but the pattern did not match that of the fluid flow models. Given current knowledge, it is unclear how this would affect boundary layer flow. By studying the relationship between squamation patterns and the lateral line, new insights are provided into sensory biology that warrant future investigation due to the implications for the ecology, morphology and sensory evolution of sharks.     

Insights into the life history and ecology of a large shortfin mako shark Isurus oxyrinchus captured in southern California

In June 2013, a record‐breaking female Isurus oxyrinchus (total length 373 cm, mass 600 kg) was captured by rod and reel off Huntington Beach, California, where it was subsequently donated to research and provided a rare opportunity to collect the first data for a female I. oxyrinchus of this size. Counts of vertebral band pairs estimate the shark to have been c. 22 years old, depending upon assumptions of band‐pair deposition rates, and the distended uteri and spent ovaries indicated that this shark had recently given birth. The stomach contained a c. 4 year‐old female California sea lion Zalophus californianus that confirmed the high trophic position of this large I. oxyrinchus, which was corroborated with the high levels of measured contaminants and tissue isotope analyses.     

A non‐invasive dolphin telemetry tag: Computer design and numerical flow simulation

The impact of devices attached to animals remains a challenge in telemetry studies of dolphins. It was hypothesized that the hydrodynamic design of a tag could provide stable attachment to the dorsal fin by means of resultant hydrodynamic force appearing when a dolphin is swimming. To verify this hypothesis the computer fluid dynamics (CFD) study of tag performance was carried out. A virtual model presenting authentic geometry of a dolphin with tag attached to the dorsal fin was constructed. The same model without tag was used as a reference object to calculate tag impact as regards drag, lift, and moments coefficients. Flow around the models was simulated for the range of velocities as well as the ranges of pitch and yaw angles. It was shown that in 33 of 35 CFD scenarios the streamlined shape of a tag generates the lift force that facilitates keeping a tag attached to the fin. Throughout the set of calculations the tag‐associated drag coefficient does not exceed 4%, which indicates low impact. Data obtained present a baseline for the further development of non‐invasive dolphin telemetry tags.     

Control of posture, depth, and swimming trajectories of fishes

Perturbations vary in period and amplitude, and responses tounavoidable perturbations depend on response time and scale.Disturbances due to unavoidable perturbations occur in threetranslational planes and three rotational axes during forwardsand backwards swimming. Stability depends on hydrodynamic dampingand correcting forces, which may be generated by propulsors(powered) or by control surfaces moving with the body (trimming).Hydrostatic forces affecting body orientation (posture) resultin negative metacentric heights amplifying rolling disturbances.The ability to counteract perturbations and correct disturbancesis greater for fishes with more slender bodies, which appearsto affect habitat choices. Postural control problems are greatestat low speeds, and are avoided by some fishes by sitting onthe bottom. In currents, body form and behavior affect lift,drag, weight, and friction and hence speeds to which posturecan be controlled. Self-correcting and regulated damping andtrimming mechanisms are most important in stabilizing swimmingtrajectories. Body resistance, fin trajectory, multiple propulsors,and long-based fins damp self-generated locomotor disturbances.Powered control using the tail evolved early in chordates, andis retained by most groups, although fishes, especially acanthopterygians,make greater use of appendages. As with most areas of stability,little is known of control costs. Costs and benefits of low-densityinclusions and hydrodynamic mechanisms for depth control varywith habits and habitats. Control may make substantial contributionsto energy budgets.     

The role of the pectoral fins in body trim of sharks

In a large aquarium the leopard shark Triakis semifasciata , sand tiger shark Odontaspis taurus , sandbar shark Carcharhinus plumbeus , and spiny dogfish Squalus acanthias cruised steadily at 0·1-0·7 body lengths s^-1. Relative to the trajectory of the shark, the pectoral fins were maintained at a positive angle of ttack regardless of vertical direction. For level swimming the mean angle of attack for the pectoral fin was 11±1·7, 10·1±1·3°, 9·3±1·3°, and 15·0±0·0 for T. semifasciata , C. plumbeus , O. taurus , and S. acanthias , respectively. The long axis of the body was canted at an angle of attack for T. semifasciata and S. acanthias , but trim was maintained during level swimming for C. plumbeus and O. taurus . Hydrodynamic analysis of the body and fin design of T. semifasciata indicated that the pectoral fins could develop suffcient pitching moment to maintain depth and keep the body in trim. Demonstration of positive angles of attack support the hypothesis that lift is generated in the anterior body to counterbalance the lift produced by the heterocercal tail.