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.
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 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.
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.
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.
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.
Mochokid catfish offer a distinct opportunity to study a communication system transitioning to a new signaling channel because some produce sounds and others electric discharges. Both signals are ...generated using an elastic spring system (ESS), which includes a protractor muscle innervated by motoneurons within the protractor nucleus that also has a motoneuron afferent population. Synodontis grandiops and S. nigriventris produce sounds and electric discharges, respectively, and their ESSs show several morphological and physiological differences. The extent to which these differences explain different signal types remains unclear. Here, we compare ESS morphologies and behavioral phenotypes among five mochokids. S. grandiops and S. nigriventris were compared with Synodontis eupterus that is known to produce both signal types, and representative members of two sister genera, Microsynodontis cf. batesii and Mochokiella paynei, for which no data were available. We provide support for the hypothesis that peripheral and central components of the ESS are conserved among mochokids. We also show that the two nonsynodontids are only sonic, consistent with sound production being an ancestral character for mochokids. Even though the three sound producing‐only species differ in some ESS characters, several are similar and likely associated with only sound production. We propose that the ability of S. eupterus to generate both electric discharges and sounds may depend on a protractor muscle intermediate in morphology between sound producing‐only and electric discharge‐only species, and two separate populations of protractor motoneurons. Our results further suggest that an electrogenic ESS in synodontids is an exaptation of a sound producing ESS.
This study provides an anatomical characterization of motor and premotor neurons associated with the muscle producing swim bladder sounds and/or electric discharges in five mochokid catfish. Even though the same muscle and neuronal populations are associated with these behaviors across all species, our results suggest that behavioral differences are associated with quantitative differences, mainly in the size of the protractor muscle and associated skeletal elements, and the number, size and location of motoneurons.
All stingrays in the family Myliobatidae are durophagous, consuming bivalves and gastropods, as well as decapod crustaceans. Durophagous rays have rigid jaws, flat teeth that interlock to form ...pavement-like tooth plates, and large muscles that generate bite forces capable of fracturing stiff biological composites (e.g. mollusk shell). The relative proportion of different prey types in the diet of durophagous rays varies between genera, with some stingray species specializing on particular mollusk taxa, while others are generalists. The tooth plate module provides a curved occlusal surface on which prey is crushed, and this curvature differs significantly among myliobatids. We measured the effect of jaw curvature on prey-crushing success in durophagous stingrays. We milled aluminum replica jaws rendered from computed tomography scans, and crushed live mollusks, three-dimensionally printed gastropod shells, and ceramic tubes with these fabricated jaws. Our analysis of prey items indicate that gastropods were consistently more difficult to crush than bivalves (i.e. were stiffer), but that mussels require the greatest work-to-fracture. We found that replica shells can provide an important proxy for investigations of failure mechanics. We also found little difference in crushing performance between jaw shapes, suggesting that disparate jaws are equally suited for processing different types of shelled prey. Thus, durophagous stingrays exhibit a many-to-one mapping of jaw morphology to mollusk crushing performance.
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.