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1. Revealing chemistry-structure-function relationships in shark vertebrae across length scales

   https://doi.org/10.1016/j.actbio.2024.09.041  

   Raja_Somu, Dawn ; Fuentes, Malena ; Lou, Lihua ; Agarwal, Arvind ; Porter, Marianne ; Merk, Vivian ( September 2024 , Acta Biomaterialia)

   Wagner, R William (Ed.)

   Shark cartilage presents a complex material composed of collagen, proteoglycans, and bioapatite. In the present study, we explored the link between microstructure, chemical composition, and biomechanical function of shark vertebral cartilage using Polarized Light Microscopy (PLM), Atomic Force Microscopy (AFM), Confocal Raman Microspectroscopy, and Nanoindentation. Our investigation focused on vertebrae from Blacktip and Shortfin Mako sharks. As typical representatives of the orders Carcharhiniformes and Lamniformes, these species differ in preferred habitat, ecological role, and swimming style. We observed structural variations in mineral organization and collagen fiber arrangement using PLM and AFM. In both sharks, the highly calcified corpus calcarea shows a ridged morphology, while a chain-like network is present in the less mineralized intermedialia. Raman spectromicroscopy demonstrates a relative increase of glucosaminocycans (GAGs) with respect to collagen and a decrease in mineral-rich zones, underlining the role of GAGs in modulating bioapatite mineralization. Region-specific testing confirmed that intravertebral variations in mineral content and arrangement result in distinct nanomechanical properties. Local Young's moduli from mineralized regions exceeded bulk values by a factor of 10. Overall, this work provides profound insights into a flexible yet strong biocomposite, which is crucial for the extraordinary speed of cartilaginous fish in the worlds’ oceans. 

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2. Internal vertebral morphology of bony fishes matches the mechanical demands of different environments

   https://doi.org/10.1002/ece3.9499  

   Baxter, Dana ; Cohen, Karly_E ; Donatelli, Cassandra_M ; Tytell, Eric_D ( November 2022 , Ecology and Evolution)

   Fishes have repeatedly evolved characteristic body shapes depending on how close they live to the substrate. Pelagic fishes live in open water and typically have narrow, streamlined body shapes; benthic and demersal fishes live close to the substrate; and demersal fishes often have deeper bodies. These shape differences are often associated with behavioral differences: pelagic fishes swim nearly constantly, demersal fishes tend to maneuver near the substrate, and benthic fishes often lie in wait on the substrate. We hypothesized that these morphological and behavioral differences would be reflected in the mechanical properties of the body, and specifically in vertebral column stiffness, because it is an attachment point for the locomotor musculature and a central axis for body bending. The vertebrae of bony fishes are composed of two cones connected by a foramen, which is filled by the notochord. Since the notochord is more flexible than bony vertebral centra, we predicted that pelagic fishes would have narrower foramina or shallower cones, leading to less notochordal material and a stiffer vertebral column which might support continuous swimming. In contrast, we predicted that benthic and demersal fishes would have more notochordal material, making the vertebral column more flexible for diverse behaviors in these species. We therefore examined vertebral morphology in 79 species using micro‐computed tomography scans. Six vertebral features were measured including notochordal foramen diameter, centrum body length, and the cone angles and diameters for the anterior and posterior vertebral cones, along with body fineness. Using phylogenetic generalized least squares analyses, we found that benthic and pelagic species differed significantly, with larger foramina, shorter centra, and larger cones in benthic species. Thus, morphological differences in the internal shape of the vertebrae of fishes are consistent with a stiffer vertebral column in pelagic fishes and with a more flexible vertebral column in benthic species.

    

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3. Volitional Swimming Kinematics of Blacktip Sharks, Carcharhinus limbatus, in the Wild

   https://doi.org/10.3390/drones4040078  

   Porter, Marianne E. ; Ruddy, Braden T. ; Kajiura, Stephen M. ( December 2020 , Drones)

   null (Ed.)

   Recent work showed that two species of hammerhead sharks operated as a double oscillating system, where frequency and amplitude differed in the anterior and posterior parts of the body. We hypothesized that a double oscillating system would be present in a large, volitionally swimming, conventionally shaped carcharhinid shark. Swimming kinematics analyses provide quantification to mechanistically examine swimming within and among species. Here, we quantify blacktip shark (Carcharhinus limbatus) volitional swimming kinematics under natural conditions to assess variation between anterior and posterior body regions and demonstrate the presence of a double oscillating system. We captured footage of 80 individual blacktips swimming in the wild using a DJI Phantom 4 Pro aerial drone. The widespread accessibility of aerial drone technology has allowed for greater observation of wild marine megafauna. We used Loggerpro motion tracking software to track five anatomical landmarks frame by frame to calculate tailbeat frequency, tailbeat amplitude, speed, and anterior/posterior variables: amplitude and frequency of the head and tail, and the body curvature measured as anterior and posterior flexion. We found significant increases in tailbeat frequency and amplitude with increasing swimming speed. Tailbeat frequency decreased and tailbeat amplitude increased as posterior flexion amplitude increased. We found significant differences between anterior and posterior amplitudes and frequencies, suggesting a double oscillating modality of wave propagation. These data support previous work that hypothesized the importance of a double oscillating system for increased sensory perception. These methods demonstrate the utility of quantifying swimming kinematics of wild animals through direct observation, with the potential to apply a biomechanical perspective to movement ecology paradigms. 

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4. Beam theory predicts muscle deformation and vertebral curvature during feeding in rainbow trout ( Oncorhynchus mykiss )

   https://doi.org/10.1242/jeb.245788  

   Jimenez, Yordano E ; Camp, Ariel L ( October 2023 , Journal of Experimental Biology)

   Muscle shortening underpins most skeletal motion and ultimately animal performance. Most animal muscle generates its greatest mechanical output over a small, homogeneous range of shortening magnitudes and speeds. However, homogeneous muscle shortening is difficult to achieve for swimming fish because the whole body deforms like a bending beam: as the vertebral column flexes laterally, longitudinal muscle strain increases along a medio-lateral gradient. Similar dorsoventral strain gradients have been identified as the vertebral column flexes dorsally during feeding in at least one body location in one fish. If fish bodies also deform like beams during dorsoventral feeding motions, this would suggest the dorsal body (epaxial) muscles must homogenize both dorsoventral and mediolateral strain gradients. We tested this hypothesis by measuring curvature of the anterior vertebral column with XROMM and muscle shortening in 14 epaxial subregions with fluoromicrometry during feeding in rainbow trout (Oncorhynchus mykiss). We compared measured strain with the predicted strain based on beam theory's curvature–strain relationship. Trout flexed the vertebrae dorsally and laterally during feeding strikes, yet when flexion in both planes was included, the strain predicted by beam theory was strongly and significantly correlated with measured strain (P<0.01, R2=0.60). Beam theory accurately predicted strain (slope=1.15, compared with ideal slope=1) across most muscle subregions, confirming that epaxial muscles experience dorsoventral and mediolateral gradients in longitudinal strain. Establishing this deformation–curvature relationship is a crucial step to understanding how these muscles overcome orthogonal strain gradients to produce powerful feeding and swimming behaviours.

    

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5. Erratum To: Foretelling the Flex—Vertebral Shape Predicts Behavior and Ecology of Fishes

   https://doi.org/10.1093/icb/icab177  

   Cassandra M Donatelli ; Alexus S Roberts ; Eric Scott ; Kylene DeSmith ; Dexter Summers ; Layanne Abu-Bader ; Dana Baxter ; Emily M Standen ; Marianne E Porter ; Adam P Summers ; et al ( September 2021 , Integrative and Comparative Biology)

   One key evolutionary innovation that separates vertebrates from invertebrates is the notochord, a central element that provides the stiffness needed for powerful movements. Later, the notochord was further stiffened by the vertebrae, cartilaginous, and bony elements, surrounding the notochord. The ancestral notochord is retained in modern vertebrates as intervertebral material, but we know little about its mechanical interactions with surrounding vertebrae. In this study, the internal shape of the vertebrae—where this material is found—was quantified in 16 species of fishes with various body shapes, swimming modes, and habitats. We used micro-computed tomography to measure the internal shape. We then created and mechanically tested physical models of intervertebral joints. We also mechanically tested actual vertebrae of five species. Material testing shows that internal morphology of the centrum significantly affects bending and torsional stiffness. Finally, we performed swimming trials to gather kinematic data. Combining these data, we created a model that uses internal vertebral morphology to make predictions about swimming kinematics and mechanics. We used linear discriminant analysis (LDA) to assess the relationship between vertebral shape and our categorical traits. The analysis revealed that internal vertebral morphology is sufficient to predict habitat, body shape, and swimming mode in our fishes. This model can also be used to make predictions about swimming in fishes not easily studied in the laboratory, such as deep sea and extinct species, allowing the development of hypotheses about their natural behavior. 

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