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.     

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.     

Bomb dating and age validation using the spines of spiny dogfish (Squalus acanthias)

Bomb radiocarbon has previously been used to validate the age of large pelagic sharks based on incorporation into vertebrae. However, not all sharks produce interpretable vertebral growth bands. Here we report the first application of bomb radiocarbon as an age validation method based on date-specific incorporation into spine enamel. Our results indicate that the dorsal spines of spiny dogfish, Squalus acanthias, recorded and preserved a bomb radiocarbon pulse in growth bands formed during the 1960s with a timing which was very similar to that of marine carbonates. Using radiocarbon assays of spine growth bands known to have formed in the 1960s and 1970s as a dated marker, we confirm the validity of spine enamel growth band counts as accurate annual age indicators to an age of at least 45 year. Radiocarbon incorporation into northeast Atlantic dogfish spines occurred in similar years as those in the northwest Atlantic and northeast Pacific, although the amount of radiocarbon differed in keeping with the radiocarbon content of the different water masses. Published reports suggesting that Pacific dogfish are longer lived and slower growing than their Atlantic counterparts appear to be correct, and are not due to errors in interpreting the spine growth bands. Radiocarbon assays of fin spine enamel appears to be well suited to the age validation of sharks with fin spines which inhabit the upper 200 m of the ocean.     

Revision der GattungOrthacanthus Agassiz 1843 (Chondrichthyes: Xenacanthida)

The genusOrthacanthus Agassiz 1843 is subdivided on the basis of different development and insertion of the dorsal spine into the subgeneraOrthacanthus (Orthacanthus)Agassiz 1843 andOrthacanthus (Lebachachanthus) Soler-Gijon 1997.Orthacanthus (Lebachacanthus) possesses a short dorsal spine situated dorsally of the shoulder girdle with broad and rounded cross section and with two short rows of denticles situated postero-laterally. This type of spine limits the dorsal fin anteriorly.Orthacanthus (Orthacanthus) possesses a long and slender spine with rounded cross section and long rows of denticles postero-laterally, inserted at the postero-dorsally edge of the neurocranium in the occipital region. This kind of insertion is similar to that of the generaTriodus andXenacanthus but not to that ofOrthacanthus (Lebachacanthus).     

Elasmobranchs from the Lower Triassic Sulphur Mountain Formation near Wapiti Lake (BC, Canada)

Hybodontoid and nonhybodontoid sharks are described from the Lower Triassic Vega‐Phroso Siltstone Member of Sulphur Mountain Formation on the basis of newly discovered material. The age of the classic fossil site ‘Wapiti Lake’ in the Canadian Rocky Mountains is discussed on the basis of new field data and one conodont found in association. Preliminary results suggest that these elasmobranch remains are between early Smithian and Spathian in age. Apart from the enigmatic genus Listracanthus and previously reported edestoids, the shark fauna consists of at least one hybodont, at least two questionable hybodontoid genera and an elasmobranch of enigmatic affinities, represented by peculiar denticles only and described as ‘genus A’incertae sedis. The presence of the only previously reported hybodont genus, cf. Palaeobates, is erroneous. The largest specimen represents the most complete Early Mesozoic shark known. The heterodonty of its dentition, fin spine morphology and the short, robust body shape imply it represents a member of a new family of shark, Wapitiodidae fam. nov. , and is described here as Wapitiodus aplopagus gen. et sp. nov. The unique dental morphology shows affinities to Polyacrodus but clearly differs in the complete lack of side cusps. Wapitiodus gen. nov. possesses a primitive fin spine structure. The tooth crowns are entirely blunt in the distal (posterior) tooth files, and are acuminate‐unicuspid in several anterior files. Tooth morphology, the shape of the basal cartilages, the proximal insertion of the fin spines and the pectoral fin structure are interpreted as diagnostic characters for this new genus, and possibly for the Wapitiodidae fam. nov. The majority of observed characters appear to be primitive and are reminiscent of Palaeozoic sharks, however, and these features include dorsal fin spine morphology and gross skull anatomy. A second species, provisionally placed in the same genus, is described as Wapitiodus homalorhizo sp. nov. Wapitiodus homalorhizo sp. nov. can be distinguished from W. aplopagus gen. et sp. nov. by the proportions of the fin spines, tooth morphology and possibly the body shape. Several isolated teeth and other fragmentary material are referred to either Wapitiodus gen. nov. sp. indet. or to ?Polyacrodus sp. (Polyacrodontidae gen. et sp. indet.). A third genus of elasmobranch (incertae sedis) is described as ‘Genus A’ and is recognized by its peculiar scales. © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149 , 309–337.     

Seasonal variation in occurrence of the sevengill shark,Notorynchus cepedianus,in two inshore habitats of southern New Zealand

Despite being a large, relatively abundant predator, the distribution and seasonal occurrence of the broadnose sevengill shark, Notorynchus cepedianus, in New Zealand is poorly understood. During 71 sampling trips conducted from July 2013 to May 2015, sharks were attracted to coastal sampling sites in southern New Zealand at ōtākou/Otago Harbour and Te Whaka ā Te Wera/Paterson Inlet, Stewart Island, using chum. Using a logistic regression model, water temperature was identified as a key predictor of encountering sevengill sharks. In addition, location, cloud cover and sea state were also identified as influential predictors. At ōtākou, a clear seasonal pattern of sevengill shark sightings emerged. Sharks were detected on 86% of survey trips in summer, whilst no sharks were detected in winter or spring. At Te Whaka ā Te Wera, sharks were sighted throughout all seasons, but a decline in shark encounters occurred during winter. This study represents the first systematic data on seasonal habitat use by sevengill sharks in New Zealand.     

Comparing external and internal dorsal-spine bands to interpret the age and growth of the giant lantern shark, Etmopterus baxteri (Squaliformes: Etmopteridae)

The giant lantern shark, Etmopterus baxteri, is taken as bycatch of commercial fisheries that operate in deepwater off southeastern Australia. Bands on the second dorsal spine were used to obtain age estimates. The number of bands on the external surface of the spine and within the inner dentine layer increased with animal length. Most spines had more bands on the external surface, and the rate of band formation was significantly different between the external surface and the inner dentine layer. Females had a maximum of 57 external bands and 26 internal bands, while males had up to 48 external bands and 22 internal bands. Age estimates from external bands suggest maturity (A ₅₀) at 20 years for males and 30 years for females. Internal band age estimates suggest maturity at 10.5 years for males and 11.5 years for females. Although there is a large discrepancy between these two preliminary (i.e., unvalidated) age estimates, they both suggest that E. baxteri is a long-lived and late maturing species that is likely to be susceptible to over fishing.     

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.     

Spatial ecology of juvenile lemon sharks (<Emphasis Type="Italic">Negaprion brevirostris</Emphasis>) in tidal creeks and coastal waters of Eleuthera,The Bahamas

Fisheries exploitation and habitat alteration are threatening lemon shark (Negaprion bevirostris) populations because they use nearshore regions as nursery sites. As such, there is a need for information on the spatial ecology of juvenile lemon sharks to identify critical habitats that require protection, as well as to understand their basic ecology. The purpose of this study was to determine the habitat preferences and movement patterns of juvenile lemon sharks along a sub-section of coastline characterized by coastal flats and tidal creeks of Eleuthera, The Bahamas. Eleven juvenile lemon sharks (766 ± 127 mm total length; mean±SD) were captured from various tidal creeks within the 23 km study area and were surgically implanted with acoustic transmitters. A series of 27 hydrophone receivers acted as a passive monitoring array to detect tagged individuals as they moved among habitats. Findings suggest that juvenile lemon sharks tagged in this study prefer shallow water habitats within tidal creeks, and typically display high site fidelity with occasional forays to alternate habitats or creeks. In fact, more than 90% of tagged lemon sharks had the greatest percentage of detections located at a receiver at or close to the location where they were tagged. There was no evidence of differences in diel or seasonal movement and habitat use. Knowledge gained from this study will be useful for directing future conservation and management strategies including coastal development plans and marine protected areas.     

Finspine morphogenesis in squalid and heterodontid sharks

Modern selachian finspines develop within a single, enlarged dermal papilla much earlier than any other papillary derived structure, and rapidly enlarge beyond the confines of the papilla. Within this, the spine primordium differentiates into two parts (mantle and trunk). Both components elongate basally and become mineralized by odontoblasts, but only the mantle has an enameloid layer. Mantle and trunk are reunited secondarily by dentine. The finspine vascular supply becomes blocked in adults, possibly to avoid loss of body fluids should the finspine (which is not shed) be damaged. Finspines probably have both defensive (perhaps mainly in juveniles) and locomotory (unctions. Odontocytes sometimes occur in the finspine base of Squalus , although the rest of the spine consists of acellular metadentine. The innermost dentine layers are centripetally deposited, resembling lamellar orthodentine of a tooth pulp. Over this is a continuous layer of centrifugally deposited lamellar dentine. Apically there is another centripetal layer (the mantle), which occurs only on certain parts of the spine. Enamelled tubercles can occur in Squalus , as a result of scleroblast disorganization, not as a result of secondary coalescence.     

Age estimation of the exploited deepwater shark Centrophorus squamosus from the continental slopes of the Rockall Trough and Porcupine Bank

Dorsal spine sections of the deepwater squalid shark Centrophorus squamosus provided age estimates of 21–70 years. Small specimens were not recorded in the study area. It was not possible to obtain estimates from vertebral centra. The estimates are discussed in the context of other studies using dorsal spines of squalid sharks. Sexual maturity was achieved at large size, >75% of maximum length. Total length at 50% maturity was calculated as 101 cm (males) and 128 cm (females).     

Non‐trophic impacts from white sharks complicate population recovery for sea otters

Complex interactions between protected populations may challenge the recovery of whole ecosystems. In California, white sharks (Carcharodon carcharias) mistargeting southern sea otters (Enhydra lutris nereis) are an emergent impact to sea otter recovery, inhibiting the broader ecosystem restoration sea otters might provide. Here, we integrate and analyze tracking and stranding data to compare the phenology of interactions between white sharks and their targeted prey (elephant seals, Mirounga angustirostris) with those of mistargeted prey (sea otters, humans). Pronounced seasonal peaks in shark bites to otters and humans overlap in the late boreal summer, immediately before the annual adult white shark migration to elephant seal rookeries. From 1997 to 2017, the seasonal period when sharks bite otters expanded from 2 to 8 months of the year and occurred primarily in regions where kelp cover declined. Immature and male otters, demographics most associated with range expansion, were disproportionately impacted. While sea otters are understood to play a keystone role in kelp forests, recent ecosystem shifts are revealing unprecedented bottom‐up and top‐down interactions. Such shifts challenge ecosystem management programs that rely on static models of species interactions.     

Essential waters: Young bull sharks in Fiji's largest riverine system

Coastal and estuarine systems provide critical shark habitats due to their relatively high productivity and shallow, protected waters. The young (neonates, young‐of‐the‐year, and juveniles) of many coastal shark species occupy a diverse range of habitats and areas where they experience environmental variability, including acute and seasonal shifts in local salinities and temperatures. Although the location and functioning of essential shark habitats has been a focus in recent shark research, there is a paucity of data from the South Pacific. In this study, we document the temporal and spatial distribution, age class composition, and environmental parameters of young bull sharks (Carcharhinus leucas) in the Rewa, Sigatoka, and Navua Rivers, Fiji's three largest riverine systems. One hundred and seventy‐two young bull sharks were captured in fisheries‐independent surveys from January 2016 to April 2018. The vast majority of the captures were neonates. Seasonality in patterns of occurrence of neonate individuals suggests a defined parturition period during summer. Environmental parameters between the Rewa and the Sigatoka River differed significantly, as did the recorded young bull sharks abundance. According to the surveys, young bull sharks occur in all three rivers with the Rewa River likely representing essential habitat for newly born bull sharks. These results enhance the understanding of bull shark ecology in Fiji and provide a scientific basis for the implementation of local conservation strategies that contribute to the protection of critical habitats.     

Habitat use,seasonality and demography of the broadnose sevengill shark Notorynchus cepedianus in central Patagonia: Another piece of the puzzle

The habitat use, seasonality and demography of the broadnose sevengill shark Notorynchus cepedianus were investigated in central Patagonia, where a data gap exists for the species. Catch and effort and video‐derived indices indicated high relative abundance of sharks during warm months. Video stations revealed differences in the spatial use by sharks, being more frequently observed in the inner section of the bay. Complementary tagging efforts evidenced both a seasonal residence pattern and site fidelity between consecutive warm seasons. Juveniles outnumbered adults, which suggests that they may use the study area as a secondary nursing ground. Evidence from spontaneous regurgitation further suggests that prey abundance may be driving the seasonal occurrence of sharks in the region. This study allows for a more comprehensive understanding of the population structure and dynamics of sevengill sharks in the Southwest Atlantic. Abstract in Spanish is available with online material.     

Functional morphology of the gills of the shortfin mako,Isurus oxyrinchus,a lamnid shark

This study examines the functional gill morphology of the shortfin mako, Isurus oxyrinchus, to determine the extent to which its gill structure is convergent with that of tunas for specializations required to increase gas exchange and withstand the forceful branchial flow induced by ram ventilation. Mako gill structure is also compared to that of the blue shark, Prionace glauca, an epipelagic species with lower metabolic requirements and a reduced dependence on fast, continuous swimming to ventilate the gills. The gill surface area of the mako is about one‐half that of a comparably sized tuna, but more than twice that of the blue shark and other nonlamnid shark species. Mako gills are also distinguished from those of other sharks by shorter diffusion distances and a more fully developed diagonal blood‐flow pattern through the gill lamellae, which is similar to that found in tunas. Although the mako lacks the filament and lamellar fusions of tunas and other ram‐ventilating teleosts, its gill filaments are stiffened by the elasmobranch interbranchial septum, and the lamellae appear to be stabilized by one to two vascular sacs that protrude from the lamellar surface and abut sacs of adjacent lamellae. Vasoactive agents and changes in vascular pressure potentially influence sac size, consequently effecting lamellar rigidity and both the volume and speed of water through the interlamellar channels. However, vascular sacs also occur in the blue shark, and no other structural elements of the mako gill appear specialized for ram ventilation. Rather, the basic elasmobranch gill design and pattern of branchial circulation are both conserved. Despite specializations that increase mako gill area and efficacy relative to other sharks, the basic features of the elasmobranch gill design appear to have limited selection for a larger gill surface area, and this may ultimately constrain mako aerobic performance in comparison to tunas. J. Morphol. 271:937–948, 2010. © 2010 Wiley‐Liss, Inc.     

Assessment of multiple paternity in single litters from three species of carcharhinid sharks in Hawaii

We tested for presence or absence of multiple paternity in single litters from each of three congeneric shark species in Hawaii: the sandbar shark, Carcharhinus plumbeus, bignose shark, Carcharhinus altimus, and Galapagos shark, Carcharhinus galapagensis. Based on eight polymorphic microsatellite loci, we excluded paternity by a single sire in sandbar and bignose sharks, but could not exclude a single sire for the litter from the Galapagos shark. This study doubles the number of shark species tested for multiple paternity, and is the first demonstration of multiple paternity in sandbar and bignose sharks.     

Growth and Maximum Size of Tiger Sharks (Galeocerdo cuvier) in Hawaii

Tiger sharks (Galecerdo cuvier) are apex predators characterized by their broad diet, large size and rapid growth. Tiger shark maximum size is typically between 380 & 450 cm Total Length (TL), with a few individuals reaching 550 cm TL, but the maximum size of tiger sharks in Hawaii waters remains uncertain. A previous study suggested tiger sharks grow rather slowly in Hawaii compared to other regions, but this may have been an artifact of the method used to estimate growth (unvalidated vertebral ring counts) compounded by small sample size and narrow size range. Since 1993, the University of Hawaii has conducted a research program aimed at elucidating tiger shark biology, and to date 420 tiger sharks have been tagged and 50 recaptured. All recaptures were from Hawaii except a single shark recaptured off Isla Jacques Cousteau (24°13′17″N 109°52′14″W), in the southern Gulf of California (minimum distance between tag and recapture sites  =  approximately 5,000 km), after 366 days at liberty (DAL). We used these empirical mark-recapture data to estimate growth rates and maximum size for tiger sharks in Hawaii. We found that tiger sharks in Hawaii grow twice as fast as previously thought, on average reaching 340 cm TL by age 5, and attaining a maximum size of 403 cm TL. Our model indicates the fastest growing individuals attain 400 cm TL by age 5, and the largest reach a maximum size of 444 cm TL. The largest shark captured during our study was 464 cm TL but individuals >450 cm TL were extremely rare (0.005% of sharks captured). We conclude that tiger shark growth rates and maximum sizes in Hawaii are generally consistent with those in other regions, and hypothesize that a broad diet may help them to achieve this rapid growth by maximizing prey consumption rates.     

Histological and morphological aspects of reproduction in the sandbar shark Carcharhinus plumbeus in the U.S. south‐eastern Atlantic Ocean and Gulf of Mexico

The reproduction of the sandbar shark Carcharhinus plumbeus in the U.S. south‐eastern Atlantic Ocean including the Gulf of Mexico was examined using a combination of histological and morphological characteristics of C. plumbeus collected through fishery‐dependent and ‐independent sampling programmes (n = 1,567). Indices of maturity were constructed using measurements of gonads, reproductive tracts and claspers, and sandbar sharks exhibited 50% maturity sizes of 140 and 148 cm fork length for males and females respectively. Gonado‐somatic indices and variation in reproductive tract condition were used to determine seasonal trends in reproduction of mature C. plumbeus. Sandbar sharks have discrete seasonal reproductive cycles in which males produce sperm from January to May with a peak in May and females develop eggs from January to May with ovulation occurring in June. Females were shown to exhibit a >2 year reproductive cycle. Embryonic development was assessed through measurements of masses and lengths of uterine contents. Gestation was 12 months, from July to the following June, with parturition in late June. This research highlights a difference from previously reported data on the periodicity of female reproduction in C. plumbeus in the U.S. south‐eastern Atlantic Ocean and Gulf of Mexico, which may have major effects on future C. plumbeus stock management.     

Dramatic increase in sea otter mortality from white sharks in California

Although southern sea otters (Enhydra lutris nereis) are not considered prey for white sharks (Carcharodon carcharias), sharks do nonetheless bite sea otters. We analyzed spatial and temporal trends in shark bites on sea otters in California, assessing the frequency of shark bite wounds in 1,870 carcasses collected since 1985. The proportion of stranded sea otters having shark bites has increased sharply since 2003, and white shark bites now account for >50% of recovered carcasses. The trend was most pronounced in the southern part of the range, from Estero Bay to Point Conception, where shark bite frequency has increased eightfold. Seasonal trends were also evident: most shark‐bitten carcasses are recovered in late summer and fall; however, the period of elevated shark bite frequency has lengthened. The causes of these trends are unclear, but possible contributing factors include increased white shark abundance and/or changes in white shark behavior and distribution. In particular, the spatiotemporal patterns of shark‐bitten sea otters match increases in pinniped populations, and the increased availability of marine mammal prey for white sharks may have led to more sharks spending more time in nearshore waters utilized by both sea otters and pinnipeds.     

Angel sharks (Squatinidae): A review of biological knowledge and exploitation

Angel sharks (Squatina spp.) are distributed in warm temperate to tropical waters around the world. Many species occur in shelf seas and exhibit seasonal inshore–offshore migrations, moving inshore to give birth. Consequently, there can be high spatial overlap of angel shark populations with fisheries and other human activities. Their dorso-ventrally flattened body shape, large size (most species attain >100 cm total length, L_T) and demersal nature means that they may be taken in a variety of demersal fishing gears from birth. Available data indicate that angel sharks typically have a biennial reproductive cycle, with litter sizes generally <20 and the young born at c. 20–30 cm. The biological characteristics of angel sharks render them susceptible to overexploitation, as exemplified by the decline of Squatina squatina from many parts of its former range in the north-east Atlantic and Mediterranean Sea. Currently, half of the 22 recognized extant species of angel shark are classed as Threatened on the International Union for Conservation of Nature (IUCN) Red List (with a further three classified as Data Deficient). Given the biological vulnerability of angel sharks, and that many species are data-limited, the current paper provides a review of available biological information and fisheries data pertaining to this family.