Vertebral morphology in the tail-whipping common thresher shark, Alopias vulpinus.

Thresher sharks (Alopias spp.) are characterized by an elongated, scythe-like caudal fin that is used in tail-whipping, a behaviour where the tail is thrown overhead to stun prey. Tail-whipping is performed via extreme dorsoventral bending of the vertebral column, and is dramatically different from lateral oscillatory motion used for swimming. Previous work has examined thresher shark vertebral morphology and mechanical properties, but in the context of swimming loads. Our goal was to assess centra morphometrics and microarchitecture for variations that may support extreme dorsoventral bending. We examined anterior and posterior body vertebrae from an embryo, five juvenile, and four adult thresher sharks using micro-computed tomography. We used principal component and landmark analyses to examine variables influencing vertebral morphology and mineral arrangement, respectively. We found that morphology and microstructure significantly varied across body regions and ontogeny. We hypothesize that anterior body vertebrae increase stability, while posterior body vertebrae support the caudal fin. Vertebral size and quantity of mineral structures (lamellae and nodes) increased across ontogeny, suggesting vertebrae adapt over development to support a larger body and tail. Based on our results, we hypothesize that thresher shark vertebrae vary in morphometrics and mineralization (amount and arrangement) supporting the mechanical needs for tail-whipping.

Microstructure and energy dispersive diffraction reconstruction of 3D patterns of crystallographic texture in a shark centrum.

Purpose: Tomography using diffracted x-rays produces reconstructions mapping quantities such as crystal lattice parameter(s), crystallite size, and crystallographic texture, information quite different from that obtained with absorption or phase contrast. Diffraction tomography is used to map an entire blue shark centrum with its double cone structure (corpora calcerea) and intermedialia (four wedges). Approach: Energy dispersive diffraction (EDD) and polychromatic synchrotron x-radiation at 6-BM-B, the Advanced Photon Source, were used. Different, properly oriented Bragg planes diffract different x-ray energies; these intensities are measured by one of ten energy-sensitive detectors. A pencil beam defines the irradiated volume, and a collimator before each energy-sensitive detector selects which portion of the irradiated column is sampled at any one time. Translating the specimen along X , Y , and Z axes produces a 3D map. Results: We report 3D maps of the integrated intensity of several bioapatite reflections from the mineralized cartilage centrum of a blue shark. The c axis reflection's integrated intensities and those of a reflection with no c axis component reveal that the cone wall's bioapatite is oriented with its c axes lateral, i.e., perpendicular to the backbone's axis, and that the wedges' bioapatite is oriented with its c axes axial. Absorption microcomputed tomography (laboratory and synchrotron) and x-ray excited x-ray fluorescence maps provide higher resolution views. Conclusion: The bioapatite in the cone walls and wedges is oriented to resist lateral and axial deflections, respectively. Mineralized tissue samples can be mapped in 3D with EDD tomography and subsequently studied by destructive methods.

Ocean warming alters the distributional range, migratory timing, and spatial protections of an apex predator, the tiger shark (Galeocerdo cuvier).

Given climate change threats to ecosystems, it is critical to understand the responses of species to warming. This is especially important in the case of apex predators since they exhibit relatively high extinction risk, and changes to their distribution could impact predator-prey interactions that can initiate trophic cascades. Here we used a combined analysis of animal tracking, remotely sensed environmental data, habitat modeling, and capture data to evaluate the effects of climate variability and change on the distributional range and migratory phenology of an ectothermic apex predator, the tiger shark (Galeocerdo cuvier). Tiger sharks satellite tracked in the western North Atlantic between 2010 and 2019 revealed significant annual variability in the geographic extent and timing of their migrations to northern latitudes from ocean warming. Specifically, tiger shark migrations have extended farther poleward and arrival times to northern latitudes have occurred earlier in the year during periods with anomalously high sea-surface temperatures. A complementary analysis of nearly 40 years of tiger shark captures in the region revealed decadal-scale changes in the distribution and timing of shark captures in parallel with long-term ocean warming. Specifically, areas of highest catch densities have progressively increased poleward and catches have occurred earlier in the year off the North American shelf. During periods of anomalously high sea-surface temperatures, movements of tracked sharks shifted beyond spatial management zones that had been affording them protection from commercial fishing and bycatch. Taken together, these study results have implications for fisheries management, human-wildlife conflict, and ecosystem functioning.

Shark centra microanatomy and mineral density variation studied with laboratory microComputed Tomography.

Centra of shark vertebrae from three species of Lamniformes (Alopias vulpinus, Carcharodon carcharias and Isurus oxyrinchus) and three species of Carcharhiniformes (Carcharhinus plumbeus, Carcharhinus obscurus and Prionace glauca) were imaged with laboratory microcomputed Tomography (microCT) using volume element (voxel) sizes between 16 and 24 µm. Linear attenuation coefficients were the same in the corpus calcarea (hour-glass-shaped cone) and intermedialia of the lamniforms but were smaller in the intermedialia than in the corpus calcarea of the carcharhiniforms. All centra contained growth bands which were visible as small changes in linear attenuation coefficient. In all six cases, the cross-sections of the cones were close to circular, and the cone angles matched those reported in the literature. Cartilage canals were a prominent structure in the intermedialia of all species, 3D renderings of centra of C. obscurus and I. oxyrinchus diameters showed these canals ran radially outward from the cone walls, and canal diameters were consistent with the limited numerical values in the literature. Somewhat higher calcification levels around the periphery of cartilage canals and of outer surfaces of the intermedialia and corpus calcerea suggest microstructural variation exists at scale below that which can be resolved in the present data sets.

Mechanical behavior of shark vertebral centra at biologically relevant strains.

Cartilaginous shark skeletons experience axial deformation at the intervertebral joints, but also within the mineralized cartilaginous centrum, which can compress to between 3% and 8% of its original length in a free-swimming shark. Previous studies have focused on shark centra mechanical properties when loaded to failure; our goal was to determine properties when compressed to a biologically relevant strain. We selected vertebrae from six shark species and from the anterior and posterior regions of the vertebral column. Centra were X-radiographed to measure double cone proportion and apex angles, and were mechanically tested at three displacement rates to 4% strain. We determined the variation in toughness and stiffness of vertebral centra among shark species and ontogenetic stages, testing strain rates, and compared anterior and posterior regions of the vertebral column. Our results suggest that toughness and stiffness, which are positively correlated, may be operating in concert to support lateral body undulations, while providing efficient energy transmission and return in these swift-swimming apex predators. We analyzed the contribution of double cone proportion and apex angle to centra mechanical behavior. We found that the greatest stiffness and toughness were in the youngest sharks and from the posterior body, and there was significant interspecific variation. Significant inverse correlations were found between mechanical properties and double cone apex angle suggesting that properties can be partially attributed to the angle forming the double cone apex. These comparative data highlight the importance of understanding cartilaginous skeleton mechanics under a wide variety of loading conditions representative of swimming behaviors seen in the wild.

Genetic Diversity of White Sharks, Carcharodon carcharias, in the Northwest Atlantic and Southern Africa.

The white shark, Carcharodon carcharias, is both one of the largest apex predators in the world and among the most heavily protected marine fish. Population genetic diversity is in part shaped by recent demographic history and can thus provide information complementary to more traditional population assessments, which are difficult to obtain for white sharks and have at times been controversial. Here, we use the mitochondrial control region and 14 nuclear-encoded microsatellite loci to assess white shark genetic diversity in 2 regions: the Northwest Atlantic (NWA, N = 35) and southern Africa (SA, N = 131). We find that these 2 regions harbor genetically distinct white shark populations (Φ ST = 0.10, P < 0.00001; microsatellite F ST = 0.1057, P < 0.021). M-ratios were low and indicative of a genetic bottleneck in the NWA (M-ratio = 0.71, P < 0.004) but not SA (M-ratio = 0.85, P = 0.39). This is consistent with other evidence showing a steep population decline occurring in the mid to late 20th century in the NWA, whereas the SA population appears to have been relatively stable. Estimates of effective population size ranged from 22.6 to 66.3 (NWA) and 188 to 1998.3 (SA) and evidence of inbreeding was found (primarily in NWA). Overall, our findings indicate that white population dynamics within NWA and SA are determined more by intrinsic reproduction than immigration and there is genetic evidence of a population decline in the NWA, further justifying the strong domestic protective measures that have been taken for this species in this region. Our study also highlights how assessment of genetic diversity can complement other sources of information to better understand the status of threatened marine fish populations.

Seasonal distribution and historic trends in abundance of white sharks, Carcharodon carcharias, in the western North Atlantic Ocean.

Despite recent advances in field research on white sharks (Carcharodon carcharias) in several regions around the world, opportunistic capture and sighting records remain the primary source of information on this species in the northwest Atlantic Ocean (NWA). Previous studies using limited datasets have suggested a precipitous decline in the abundance of white sharks from this region, but considerable uncertainty in these studies warrants additional investigation. This study builds upon previously published data combined with recent unpublished records and presents a synthesis of 649 confirmed white shark records from the NWA compiled over a 210-year period (1800-2010), resulting in the largest white shark dataset yet compiled from this region. These comprehensive records were used to update our understanding of their seasonal distribution, relative abundance trends, habitat use, and fisheries interactions. All life stages were present in continental shelf waters year-round, but median latitude of white shark occurrence varied seasonally. White sharks primarily occurred between Massachusetts and New Jersey during summer and off Florida during winter, with broad distribution along the coast during spring and fall. The majority of fishing gear interactions occurred with rod and reel, longline, and gillnet gears. Historic abundance trends from multiple sources support a significant decline in white shark abundance in the 1970s and 1980s, but there have been apparent increases in abundance since the 1990s when a variety of conservation measures were implemented. Though the white shark's inherent vulnerability to exploitation warrants continued protections, our results suggest a more optimistic outlook for the recovery of this iconic predator in the Atlantic.

Vertebral bomb radiocarbon suggests extreme longevity in white sharks.

Conservation and management efforts for white sharks (Carcharodon carcharias) remain hampered by a lack of basic demographic information including age and growth rates. Sharks are typically aged by counting growth bands sequentially deposited in their vertebrae, but the assumption of annual deposition of these band pairs requires testing. We compared radiocarbon (Δ(14)C) values in vertebrae from four female and four male white sharks from the northwestern Atlantic Ocean (NWA) with reference chronologies documenting the marine uptake of (14)C produced by atmospheric testing of thermonuclear devices to generate the first radiocarbon age estimates for adult white sharks. Age estimates were up to 40 years old for the largest female (fork length [FL]: 526 cm) and 73 years old for the largest male (FL: 493 cm). Our results dramatically extend the maximum age and longevity of white sharks compared to earlier studies, hint at possible sexual dimorphism in growth rates, and raise concerns that white shark populations are considerably more sensitive to human-induced mortality than previously thought.

Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks.

We conducted stable 13C and 15N analysis on white shark vertebrae and demonstrated that incremental analysis of isotopes along the radius of a vertebral centrum produces a chronological record of dietary information, allowing for reconstruction of an individual's trophic history. Isotopic data showed significant enrichments in 15N with increasing sampling distance from the centrum center, indicating a correlation between body size and trophic level. Additionally, isotopic values verified two distinct ontogenetic trophic shifts in the white shark: one following parturition, marking a dietary switch from yolk to fish; and one at a total length of >341 cm, representing a known diet shift from fish to marine mammals. Retrospective trophic-level reconstruction using vertebral tissue will have broad applications in future studies on the ecology of threatened, endangered, or extinct species to determine life-long feeding patterns, which would be impossible through other methods.