Durophagous predators consume hard‐shelled prey such as bivalves, gastropods, and large crustaceans, typically by crushing the mineralized exoskeleton. This is costly from the point of view of the ...bite forces involved, handling times, and the stresses inflicted on the predator's skeleton. It is not uncommon for durophagous taxa to display an ontogenetic shift from softer to harder prey items, implying that it is relatively difficult for smaller animals to consume shelled prey. Batoid fishes (rays, skates, sawfishes, and guitarfishes) have independently evolved durophagy multiple times, despite the challenges associated with crushing prey harder than their own cartilaginous skeleton. Potamotrygon leopoldi is a durophagous freshwater ray endemic to the Xingu River in Brazil, with a jaw morphology superficially similar to its distant durophagous marine relatives, eagle rays (e.g., Aetomylaeus, Aetobatus). We used second moment of area as a proxy for the ability to resist bending and analyzed the arrangement of the mineralized skeleton of the jaw of P. leopoldi over ontogeny using data from computed tomography (CT) scans. The jaws of P. leopoldi do not resist bending nearly as well as other durophagous elasmobranchs, and the jaws are stiffest nearest the joints rather than beneath the dentition. While second moment has similar material distribution over ontogeny, mineralization of the jaws under the teeth increases with age. Neonate rays have low jaw stiffness and poor mineralization, suggesting that P. leopoldi may not feed on hard‐shelled prey early in life. These differences in the shape, stiffness and mineralization of the jaws of P. leopoldi compared to its durophagous relatives show there are several solutions to the problem of crushing shelled prey with a compliant skeleton.
Changes to jaw stiffness over ontogeny suggest durophagous freshwater rays cannot consume shelled prey as juveniles. Contrary to other molluscivorous batoids, jaws are more robust and internally supported at the joints than under the teeth.
A large brain can offer several cognitive advantages. However, brain tissue has an especially high metabolic rate. Thus, evolving an enlarged brain requires either a decrease in other energetic ...requirements, or an increase in overall energy consumption. Previous studies have found conflicting evidence for these hypotheses, leaving the metabolic costs and constraints in the evolution of increased encephalization unclear. Mormyrid electric fishes have extreme encephalization comparable to that of primates. Here, we show that brain size varies widely among mormyrid species, and that there is little evidence for a trade-off with organ size, but instead a correlation between brain size and resting oxygen consumption rate. Additionally, we show that increased brain size correlates with decreased hypoxia tolerance. Our data thus provide a non-mammalian example of extreme encephalization that is accommodated by an increase in overall energy consumption. Previous studies have found energetic trade-offs with variation in brain size in taxa that have not experienced extreme encephalization comparable with that of primates and mormyrids. Therefore, we suggest that energetic trade-offs can only explain the evolution of moderate increases in brain size, and that the energetic requirements of extreme encephalization may necessitate increased overall energy investment.
The anatomy of sharks, rays, and chimaeras (chondrichthyans) is crucial to understanding the evolution of the cranial system in vertebrates due to their position as the sister group to bony fishes ...(osteichthyans). Strikingly different arrangements of the head in the two constituent chondrichthyan groups—holocephalans and elasmobranchs—have played a pivotal role in the formation of evolutionary hypotheses targeting major cranial structures such as the jaws and pharynx. However, despite the advent of digital dissections as a means of easily visualizing and sharing the results of anatomical studies in three dimensions, information on the musculoskeletal systems of the chondrichthyan head remains largely limited to traditional accounts, many of which are at least a century old. Here, we use synchrotron tomographic data to carry out a digital dissection of a holocephalan and an elasmobranch widely used as model species: the elephantfish, Callorhinchus milii, and the small‐spotted catshark, Scyliorhinus canicula. We describe and figure the skeletal anatomy of the head, labial, mandibular, hyoid, and branchial cartilages in both taxa as well as the muscles of the head and pharynx. In Callorhinchus, we make several new observations regarding the branchial musculature, revealing several previously unreported or ambiguously characterized muscles, likely homologous to their counterparts in the elasmobranch pharynx. We also identify a previously unreported structure linking the pharyngohyal of Callorhinchus to the neurocranium. Finally, we review what is known about the evolution of chondrichthyan cranial muscles from their fossil record and discuss the implications for muscle homology and evolution, broadly concluding that the holocephalan pharynx is likely derived from a more elasmobranch‐like form which is plesiomorphic for the chondrichthyan crown group. This dataset has great potential as a resource, particularly for researchers using these model species for zoological research, functional morphologists requiring models of musculature and skeletons, as well as for palaeontologists seeking comparative models for extinct taxa.
We use synchrotron tomography to image the heads of two chondrichthyan model species—the holocephalan Callorhinchus milii, and the elasmobranch Scyliorhinus canicula—generating detailed 3D models of the cranial skeleton and muscles. We redescribe these structures, and identify previously unknown, elasmobranch‐like features in the gill musculature of Callorhinchus. Using this new information and evidence from the fossil record, we reevaluate chondrichthyan cranial muscle evolution.
The present study analysed aspects of reproductive biology based on macroscopic and microscopic structures of whitespotted eagle ray Aetobatus narinari captured by artisanal fishing off the coast of ...Paraíba and Pernambuco (7° 30′ S, 34° 49′ W; 7° 47′ S, 34° 51′ W), northeast Brazil. Of the 71 individuals in the sample, 55% were female (disc width – WD: 532–1698 mm) and 45% were male (WD: 442–1410 mm). The body size at which 50% of the individuals are mature (WD50) for males was 1155.8 mm; the clasper length varied between 24 and 184 mm. The WD50 for females was 1293.9 mm; the diameter of the largest vitellogenic follicle varied between 11 and 31 mm; and only the left ovary and uterus were functional. The microanatomy of the reproductive tract of males and females agrees with that of other elasmobranch species. In males, the highest hepato‐somatic index (IH) average and gonado‐somatic index (IG) average occurred in the third bimester of the year, whereas in females the highest values (average IH and IG, respectively) were in the second bimester of the year. Based on the information on reproduction of A. narinari from this study, it will be possible to contribute to the correct management and protection of this species.
Weakly electric knifefish have intrigued both biologists and engineers for decades with their unique electrosensory system and agile swimming mechanics. Study of these fish has resulted in models ...that illuminate the principles behind their electrosensory system and unique swimming abilities. These models have uncovered the mechanisms by which knifefish generate thrust for swimming forward and backward, hovering, and heaving dorsally using a ventral elongated median fin. Engineered active electrosensory models inspired by electric fish allow for close-range sensing in turbid waters where other sensing modalities fail. Artificial electrosense is capable of aiding navigation, detection and discrimination of objects, and mapping the environment, all tasks for which the fish use electrosense extensively. While robotic ribbon fin and artificial electrosense research has been pursued separately to reduce complications that arise when they are combined, electric fish have succeeded in their ecological niche through close coupling of their sensing and mechanical systems. Future integration of electrosense and ribbon fin technology into a knifefish robot should likewise result in a vehicle capable of navigating complex 3D geometries unreachable with current underwater vehicles, as well as provide insights into how to design mobile robots that integrate high bandwidth sensing with highly responsive multidirectional movement.
The primary skeletal tissue in elasmobranchs –sharks, rays and relatives– is cartilage, forming both embryonic and adult endoskeletons. Only the skeletal surface calcifies, exhibiting mineralized ...tiles (tesserae) sandwiched between a cartilage core and overlying fibrous perichondrium. These two tissues are based on different collagens (Coll II and I, respectively), fueling a long-standing debate as to whether tesserae are more like calcified cartilage or bone (Coll 1-based) in their matrix composition. We demonstrate that stingray (Urobatis halleri) tesserae are bipartite, having an upper Coll I-based ‘cap’ that merges into a lower Coll II-based ‘body’ zone, although tesserae are surrounded by cartilage. We identify a ‘supratesseral’ unmineralized cartilage layer, between tesserae and perichondrium, distinguished from the cartilage core in containing Coll I and X (a common marker for mammalian mineralization), in addition to Coll II. Chondrocytes within tesserae appear intact and sit in lacunae filled with Coll II-based matrix, suggesting tesserae originate in cartilage, despite comprising a diversity of collagens. Intertesseral joints are also complex in their collagenous composition, being similar to supratesseral cartilage closer to the perichondrium, but containing unidentified fibrils nearer the cartilage core. Our results indicate a unique potential for tessellated cartilage in skeletal biology research, since it lacks features believed diagnostic for vertebrate cartilage mineralization (e.g. hypertrophic and apoptotic chondrocytes), while offering morphologies amenable for investigating the regulation of complex mineralized ultrastructure and tissues patterned on multiple collagens.
The relationship between cartilage growth – mineralization patterns were studied in adult Rajidae with X‐ray morphology/morphometry, undecalcified resin‐embedded, heat‐deproteinated histology and ...scanning electron microscopy. Morphometry of the wing‐fins, nine central rays of the youngest and oldest specimens documented a significant decrement of radials mean length between inner, middle and outer zones, but without a regular progression along the ray. This suggests that single radial length growth is regulated in such a way to align inter‐radial joints parallel to the wing metapterygia curvature. Trans‐illumination and heat‐deproteination techniques showed polygonal and cylindrical morphotypes of tesserae, whose aligned pattern ranged from mono‐columnar, bi‐columnar, and multi‐columnar up to the crustal‐like layout. Histology of tessellated cartilage allowed to identify of zones of the incoming mineral deposition characterized by enhanced duplication rate of chondrocytes with the formation of isogenic groups, whose morphology and topography suggested a relationship with the impending formation of the radials calcified column. The morphotype and layout of radial tesserae were related to mechanical demands (stiffening) and the size/mass of the radial cartilage body. The cartilage calcification pattern of the batoids model shares several morphological features with tetrapods' endochondral ossification, that is, (chondrocytes' high duplication rate, alignment in rows, increased volume of chondrocyte lacunae), but without the typical geometry of the metaphyseal growth plates.
Research Highlights
1. The wing‐fins system consists of stiff radials, mobile inter‐radial joints and a flat inter‐radial membrane adapted to the mechanical demand of wing wave movement.
2. Growth occurs by forming a mixed calcified‐uncalcified cartilage texture, developing intrinsic tensional stresses documented by morphoanatomical data.
(a) Bright field and (b) Phase‐contrast image. The cartilage growth pattern forms a mixed texture of calcified‐uncalcified matrix (not undergoing remodeling) which develops intrinsic, tensional stresses inside the tissue, histologically documented by elongation of chondrocyte lacunae and collagen fibers in the resilient uncalcified zones and by fractures in the neighboring calcified matrix.
Regionalization of the vertebral column occurred early during vertebrate evolution and has been extensively investigated in mammals. However, less data are available on vertebral regions of crown ...gnathostomes. This is particularly true for batoids (skates, sawfishes, guitarfishes, and rays) whose vertebral column has long been considered to be composed of the same two regions as in teleost fishes despite the presence of a synarcual. However, the numerous vertebral units in chondrichthyans may display a more complex regionalization pattern than previously assumed and the intraspecific variation of such pattern deserves a thorough investigation. In this study, we use micro‐computed tomography (µCT) scans of vertebral columns of a growth series of thorny skates Amblyraja radiata to provide the first fine‐scale morphological description of vertebral units in a batoids species. We further investigate axial regionalization using a replicable clustering analysis on presence/absence of vertebral elements to decipher the regionalization of the vertebral column of A. radiata. We identify four vertebral regions in this species. The two anteriormost regions, named synarcual and thoracic, may undergo strong developmental or functional constraints because they display stable patterns of shapes and numbers of vertebral units across all growth stages. The third region, named hemal transitional, is characterized by high inter‐individual morphological variation and displays a transition between the monospondylous (one centrum per somite) to diplospondylous (two centra per somite) conditions. The posteriormost region, named caudal, is subdivided into three sub‐regions with shapes changing gradually along the anteroposterior axis. These regionalized patterns are discussed in light of ecological habits of skates.
The vertebral column of a skate species is described in details for different ontogenetic stages. Four regions are recognized: the synarcual and the thoracic regions display few inter‐individual variability, as opposed to the hemal transitional and caudal regions. The importance of describing transitional vertebrae is highlighted to better understand functional and developmental aspects of the vertebral column.
The vertebral skeleton is a defining feature of vertebrate animals. However, the mode of vertebral segmentation varies considerably between major lineages. In tetrapods, adjacent somite halves ...recombine to form a single vertebra through the process of 'resegmentation'. In teleost fishes, there is considerable mixing between cells of the anterior and posterior somite halves, without clear resegmentation. To determine whether resegmentation is a tetrapod novelty, or an ancestral feature of jawed vertebrates, we tested the relationship between somites and vertebrae in a cartilaginous fish, the skate (
). Using cell lineage tracing, we show that skate trunk vertebrae arise through tetrapod-like resegmentation, with anterior and posterior halves of each vertebra deriving from adjacent somites. We further show that tail vertebrae also arise through resegmentation, though with a duplication of the number of vertebrae per body segment. These findings resolve axial resegmentation as an ancestral feature of the jawed vertebrate body plan.
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