The world’s oceans are home to many fantastic creatures, including about 16,000 species of actinopterygian, or ray-finned, fishes. Notably, 85% of marine fish species come from a single ...actinopterygian subgroup, the acanthomorph or spiny-rayed fishes. Here, we review eight functional innovations found in marine acanthomorphs that have been instrumental in the adaptive radiation of this group in the marine realm. Jaw protrusion substantially enhances the suction feeding mechanism found in all fish. Fin spines serve as a major deterrent to predators and enhance the locomotor function of fins. Pharyngognathy, a specialization of the second pair of jaws in the pharynx, enhances the ability of fishes to process hard and tough prey. Endothermy allows fishes to function at high levels of physiological performance in cold waters and facilitates frequent movement across strong thermal gradients found in the open ocean. Intramandibular joints enhance feeding for fishes that bite and scrape prey attached to hard surfaces. Antifreeze proteins prevent ice crystal growth in extracellular fluids, allowing fish to function in cold waters that would otherwise freeze them. Air-breathing allowed fishes at the water’s edge to exploit terrestrial habitats. Finally, bioluminescence functions in communication, attracting prey and in hiding from predators, particularly for fishes of the deep ocean. All of these innovations have evolved multiple times in fishes. The frequent occurrence of convergent evolution of these complex functional novelties speaks to the persistence and potency of the selective forces in marine environments that challenge fishes and stimulate innovation.
Wainwright and Longo review eight biological innovations that enabled acanthomorphs to become the dominant group of fish in the modern ocean.
Among over 30 000 species of ray-finned fishes, seahorses and pipefishes have a unique feeding mechanism whereby the elastic recoil of tendons allows them to rotate their long snouts extremely ...rapidly in order to capture small elusive prey. To understand the evolutionary origins of this feeding mechanism, its phylogenetic distribution among closely related lineages must be assessed. We present evidence for elastic recoil-powered feeding in snipefish (Macroramphosus scolopax) from kinematics, dynamics and morphology. High-speed videos of strikes show they achieve extremely fast head and hyoid rotational velocities, resulting in rapid prey capture in as short a duration as 2 ms. The maximum instantaneous muscle-mass-specific power requirement for head rotation in snipefish was above the known vertebrate maximum, which is evidence that strikes are not the result of direct muscle power. Finally, we show that the over-centre conformation of the four-bar linkage mechanism coupling head elevation to hyoid rotation in snipefish can function as a torque reversal latch, preventing the head from rotating and providing the opportunity for elastic energy storage. The presence of elastic recoil feeding in snipefish means that this high-performance mechanism is not restricted to the Syngnathidae (seahorses and pipefish) and may have evolved in parallel.
The smallest, fastest, repeated-use movements are propelled by power-dense elastic mechanisms, yet the key to their energetic control may be found in the latch-like mechanisms that mediate ...transformation from elastic potential energy to kinetic energy. Here, we tested how geometric latches enable consistent or variable outputs in ultrafast, spring-propelled systems. We constructed a reduced-order mathematical model of a spring-propelled system that uses a torque reversal (over-center) geometric latch. The model was parameterized to match the scales and mechanisms of ultrafast systems, specifically snapping shrimp. We simulated geometric and energetic configurations that enabled or reduced variation of strike durations and dactyl rotations given variation of stored elastic energy and latch mediation. Then, we collected an experimental dataset of the energy storage mechanism and ultrafast snaps of live snapping shrimp (Alpheus heterochaelis) and compared our simulations with their configuration. We discovered that snapping shrimp deform the propodus exoskeleton prior to the strike, which may contribute to elastic energy storage. Regardless of the amount of variation in spring loading duration, strike durations were far less variable than spring loading durations. When we simulated this species' morphological configuration in our mathematical model, we found that the low variability of strike duration is consistent with their torque reversal geometry. Even so, our simulations indicate that torque reversal systems can achieve either variable or invariant outputs through small adjustments to geometry. Our combined experiments and mathematical simulations reveal the capacity of geometric latches to enable, reduce or enhance variation of ultrafast movements in biological and synthetic systems.
Jumping microrobots and insects power their impressive leaps through systems of springs and latches. Using springs and latches, rather than motors or muscles, as actuators to power jumps imposes new ...challenges on controlling the performance of the jump. In this paper, we show how tuning the motor and spring relative to one another in a torque reversal latch can lead to an ability to control jump output, producing either tuneable (variable) or stereotyped jumps. We develop and utilize a simple mathematical model to explore the underlying design, dynamics, and control of a torque reversal mechanism, provides the opportunity to achieve different outcomes through the interaction between geometry, spring properties, and motor voltage. We relate system design and control parameters to performance to guide the design of torque reversal mechanisms for either variable or stereotyped jump performance. We then build a small (356 mg) microrobot and characterize the constituent components (e.g. motor and spring). Through tuning the actuator and spring relative to the geometry of the torque reversal mechanism, we demonstrate that we can achieve jumping microrobots that both jump with different take-off velocities given the actuator input (variable jumping), and those that jump with nearly the same take-off velocity with actuator input (stereotyped jumping). The coupling between spring characteristics and geometry in this system has benefits for resource-limited microrobots, and our work highlights design combinations that have synergistic impacts on output, compared to others that constrain it. This work will guide new design principles for enabling control in resource-limited jumping microrobots.
The extraordinary snaps of snapping shrimp evolved through simple morphological transitions with remarkable mechanical results.
The extraordinary snaps of snapping shrimp evolved through simple ...morphological transitions with remarkable mechanical results.
We review the origins, prominent innovations, and major patterns of diversification in suction feeding by vertebrates. Non-vertebrate chordates and larval lamprey suspension-feed by capturing small ...particles in pharyngeal mucous. In most of these lineages the gentle flows that transport particles are generated by buccal cilia, although larval lamprey and thaliacean urochordates have independently evolved a weak buccal pump to generate an oscillating flow of water that is powered by elastic recovery of the pharynx following compression by buccal muscles. The evolution of jaws and the hyoid facilitated powerful buccal expansion and high-performance suction feeding as found today throughout aquatic vertebrates. We highlight three major innovations in suction feeding. Most vertebrate suction feeders have mechanisms that occlude the corners of the open mouth during feeding. This produces a planar opening that is often nearly circular in shape. Both features contribute to efficient flow of water into the mouth and help direct the flow to the area directly in front of the mouth’s aperture. Among several functions that have been identified for protrusion of the upper jaw, is an increase in the hydrodynamic forces that suction feeders exert on their prey. Protrusion of the upper jaw has evolved five times in ray-finned fishes, including in two of the most successful teleost radiations, cypriniforms and acanthomorphs, and is found in about 60% of living teleost species. Diversification of the mechanisms of suction feeding and of feeding behavior reveals that suction feeders with high capacity for suction rarely approach their prey rapidly, while slender-bodied predators with low capacity for suction show the full range of attack speeds. We hypothesize that a dominant axis of diversification among suction feeders involves a trade-off between the forces that are exerted on prey and the volume of water that is ingested.
Abstract
As animals get smaller, their ability to generate usable work from muscle contraction is decreased by the muscle’s force–velocity properties, thereby reducing their effective jump height. ...Very small animals use a spring-actuated system, which prevents velocity effects from reducing available energy. Since force–velocity properties reduce the usable work in even larger animals, why don’t larger animals use spring-actuated jumping systems as well? We will show that muscle length–tension properties limit spring-actuated systems to generating a maximum one-third of the possible work that a muscle could produce—greatly restricting the jumping height of spring-actuated jumpers. Thus a spring-actuated jumping animal has a jumping height that is one-third of the maximum possible jump height achievable were 100% of the possible muscle work available. Larger animals, which could theoretically use all of the available muscle energy, have a maximum jumping height that asymptotically approaches a value that is about three times higher than that of spring-actuated jumpers. Furthermore, a size related “crossover point” is evident for these two jumping mechanisms: animals smaller than this point can jump higher with a spring-actuated mechanism, while animals larger than this point can jump higher with a muscle-actuated mechanism. We demonstrate how this limit on energy storage is a consequence of the interaction between length–tension properties of muscles and spring stiffness. We indicate where this crossover point occurs based on modeling and then use jumping data from the literature to validate that larger jumping animals generate greater jump heights with muscle-actuated systems than spring-actuated systems.
Physical principles and laws determine the set of possible organismal phenotypes. Constraints arising from development, the environment, and evolutionary history then yield workable, integrated ...phenotypes. We propose a theoretical and practical framework that considers the role of changing environments. This ‘ecomechanical approach’ integrates functional organismal traits with the ecological variables. This approach informs our ability to predict species shifts in survival and distribution and provides critical insights into phenotypic diversity. We outline how to use the ecomechanical paradigm using drag-induced bending in trees as an example. Our approach can be incorporated into existing research and help build interdisciplinary bridges. Finally, we identify key factors needed for mass data collection, analysis, and the dissemination of models relevant to this framework.
All organisms must comply with physical laws, which place rigid or hard constraints on survival and reproduction. Ecomechanics is the expression of that interplay, and assumes a central role when considering organismal development, ecology, and evolution.How organisms will respond to changes in the environment, such as human-mediated climate change, will depend strongly on ecomechanics.Functional traits are commonly used to investigate the consequences of ecological variation. Ecomechanical models that incorporate functional traits and environmental variables are key to deciphering the rules of life and expand upon functional trait studies.The use of the ecomechanical framework is illustrated using multiple examples (e.g., wind-induced bending mechanics in trees and gecko adhesion in the real world). We emphasize safety factors as a key metric when assessing the evolution of form and performance. Biologists can apply our framework to many other systems.We offer suggestions for constructing and tailoring the data pipeline for future ecomechanical models to enhance their availability and utility for various disciplines.
Seahorses, seadragons, pygmy pipehorses, and pipefishes (Syngnathidae, Syngnathiformes) are among the most recognizable groups of fishes because of their derived morphology, unusual life history, and ...worldwide distribution. Despite previous phylogenetic studies and recent new species descriptions of syngnathids, the evolutionary relationships among several major groups within this family remain unresolved.
Here, we provide a reconstruction of syngnathid phylogeny based on genome-wide sampling of 1314 ultraconserved elements (UCEs) and expanded taxon sampling to assess the current taxonomy and as a basis for macroevolutionary insights. We sequenced a total of 244 new specimens across 117 species and combined with published UCE data for a total of 183 species of Syngnathidae, about 62% of the described species diversity, to compile the most data-rich phylogeny to date. We estimated divergence times using 14 syngnathiform fossils, including nine fossils with newly proposed phylogenetic affinities, to better characterize current and historical biogeographical patterns, and to reconstruct diversification through time. We present a phylogenetic hypothesis that is well-supported and provides several notable insights into syngnathid evolution. We found nine non-monophyletic genera, evidence for seven cryptic species, five potentially invalid synonyms, and identified a novel sister group to the seahorses, the Indo-Pacific pipefishes Halicampus macrorhynchus and H. punctatus. In addition, the morphologically distinct southwest Pacific seahorse Hippocampus jugumus was recovered as the sister to all other non-pygmy seahorses. As found in many other groups, a high proportion of syngnathid lineages appear to have originated in the Central Indo-Pacific and subsequently dispersed to adjoining regions. Conversely, we also found an unusually high subsequent return of lineages from southern Australasia to the Central Indo-Pacific. Diversification rates rose abruptly during the Middle Miocene Climate Transition and peaked after the closure of the Tethys Sea.
Our results reveal a previously underappreciated diversity of syngnathid lineages. The observed biogeographic patterns suggest a significant role of the southern Australasian region as a source and sink of lineages. Shifts in diversification rates imply possible links to declining global temperatures, the separation of the Atlantic and Pacific faunas, and the environmental changes associated with these events.
Suction-feeding fishes exhibit diverse prey-capture strategies that vary in their relative use of suction and predator approach (ram), which is often referred to as the ram-suction continuum. ...Previous research has found that ram varies more than suction distance among species, such that ram accounts for most differences in prey-capture behaviors. To determine whether these findings hold at broad evolutionary scales, we collected high-speed videos of 40 species of spiny-rayed fishes (Acanthomorpha) feeding on live prey. For each strike, we calculated the contributions of suction, body ram (swimming) and jaw ram (mouth movement relative to the body) to closing the distance between predator and prey. We confirm that the contribution of suction distance is limited even in this phylogenetically and ecologically broad sample of species, with the extreme suction area of prey-capture space conspicuously unoccupied. Instead of a continuum from suction to ram, we find that variation in body ram is the major factor underlying the diversity of prey-capture strategies among suction-feeding fishes. Independent measurement of the contribution of jaw ram revealed that it is an important component of diversity among spiny-rayed fishes, with a number of ecomorphologies relying heavily on jaw ram, including pivot feeding in syngnathiforms, extreme jaw protruders and benthic sit-and-wait ambush predators. A combination of morphological and behavioral innovations has allowed fish to invade the extreme jaw ram area of prey-capture space. We caution that while two-species comparisons may support a ram-suction trade-off, these patterns do not speak to broader patterns across spiny-rayed fishes.
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