A power amplification dyad in seahorses.

Throughout evolution, organisms repeatedly developed elastic elements to power explosive body motions, overcoming ubiquitous limits on the power capacity of fast-contracting muscles. Seahorses evolved such a latch-mediated spring-actuated (LaMSA) mechanism; however, it is unclear how this mechanism powers the two complementary functions necessary for feeding: rapidly swinging the head towards the prey, and sucking water into the mouth to entrain it. Here, we combine flow visualization and hydrodynamic modelling to estimate the net power required for accelerating the suction feeding flows in 13 fish species. We show that the mass-specific power of suction feeding in seahorses is approximately three times higher than the maximum recorded from any vertebrate muscle, resulting in suction flows that are approximately eight times faster than similar-sized fishes. Using material testing, we reveal that the rapid contraction of the sternohyoideus tendons can release approximately 72% of the power needed to accelerate the water into the mouth. We conclude that the LaMSA system in seahorses is powered by two elastic elements, the sternohyoideus and epaxial tendons. These elements jointly actuate the coordinated acceleration of the head and the fluid in front of the mouth. These findings extend the known function, capacity and design of LaMSA systems.

Multiple performance peaks for scale-biting in an adaptive radiation of pupfishes.

The physical interactions between organisms and their environment ultimately shape their rate of speciation and adaptive radiation, but the contributions of biomechanics to evolutionary divergence are frequently overlooked. Here we investigated an adaptive radiation of Cyprinodon pupfishes to measure the relationship between feeding kinematics and performance during adaptation to a novel trophic niche, lepidophagy, in which a predator removes only the scales, mucus, and sometimes tissue from their prey using scraping and biting attacks. We used high-speed video to film scale-biting strikes on gelatin cubes by scale-eater, molluscivore, generalist, and hybrid pupfishes and subsequently measured the dimensions of each bite. We then trained the SLEAP machine-learning animal tracking model to measure kinematic landmarks and automatically scored over 100,000 frames from 227 recorded strikes. Scale-eaters exhibited increased peak gape and greater bite length; however, substantial within-individual kinematic variation resulted in poor discrimination of strikes by species or strike type. Nonetheless, a complex performance landscape with two distinct peaks best predicted gel-biting performance, corresponding to a significant nonlinear interaction between peak gape and peak jaw protrusion in which scale-eaters and their hybrids occupied a second performance peak requiring larger peak gape and greater jaw protrusion. A bite performance valley separating scale-eaters from other species may have contributed to their rapid evolution and is consistent with multiple estimates of a multi-peak fitness landscape in the wild. We thus present an efficient deep-learning automated pipeline for kinematic analyses of feeding strikes and a new biomechanical model for understanding the performance and rapid evolution of a rare trophic niche.

A new theoretical performance landscape for suction feeding reveals adaptive kinematics in a natural population of reef damselfish.

Understanding how organismal traits determine performance and, ultimately, fitness is a fundamental goal of evolutionary eco-morphology. However, multiple traits can interact in non-linear and context-dependent ways to affect performance, hindering efforts to place natural populations with respect to performance peaks or valleys. Here, we used an established mechanistic model of suction-feeding performance (SIFF) derived from hydrodynamic principles to estimate a theoretical performance landscape for zooplankton prey capture. This performance space can be used to predict prey capture performance for any combination of six morphological and kinematic trait values. We then mapped in situ high-speed video observations of suction feeding in a natural population of a coral reef zooplanktivore, Chromis viridis, onto the performance space to estimate the population's location with respect to the topography of the performance landscape. Although the kinematics of the natural population closely matched regions of high performance in the landscape, the population was not located on a performance peak. Individuals were furthest from performance peaks on the peak gape, ram speed and mouth opening speed trait axes. Moreover, we found that the trait combinations in the observed population were associated with higher performance than expected by chance, suggesting that these combinations are under selection. Our results provide a framework for assessing whether natural populations occupy performance optima.

Trophic guilds of suction-feeding fishes are distinguished by their characteristic hydrodynamics of swimming and feeding.

Suction-feeding in fishes is a ubiquitous form of prey capture whose outcome depends both on the movements of the predator and the prey, and on the dynamics of the surrounding fluid, which exerts forces on the two organisms. The inherent complexity of suction-feeding has challenged previous efforts to understand how the feeding strikes are modified when species evolve to feed on different prey types. Here, we use the concept of dynamic similarity, commonly applied to understanding the mechanisms of swimming, flying, walking and aquatic feeding. We characterize the hydrodynamic regimes pertaining to (i) the forward movement of the fish (ram), and (ii) the suction flows for feeding strikes of 71 species of acanthomorph fishes. A discriminant function analysis revealed that feeding strikes of zooplanktivores, generalists and piscivores could be distinguished based on their hydrodynamic regimes. Furthermore, a phylogenetic comparative analysis revealed that there are distinctive hydrodynamic adaptive peaks associated with zooplanktivores, generalists and piscivores. The scaling of dynamic similarity across species, body sizes and feeding guilds in fishes indicates that elementary hydrodynamic principles govern the trophic evolution of suction-feeding in fishes.

Treatment-level impacts of microplastic exposure may be confounded by variation in individual-level responses in juvenile fish.

Microplastic (MP) pollution is a key global environmental issue and laboratory exposure studies on aquatic biota are proliferating at an exponential rate. However, most research is limited to treatment-level effects, ignoring that there may be substantial within-population variation in responses to anthropogenic stressors. MP exposure experiments often reveal considerable, yet largely overlooked, inter-individual variation in particle uptake within concentration treatments. Here, we investigated to what degree treatment-level responses to MP exposure may be affected by variation in MP ingestion rates in the early life stages of a marine fish, the Gilt-head seabream, Sparus aurata. First, we tested whether MP ingestion variation is repeatable. Second, we assessed to what degree this variation may determine individual-level effects of MP exposure on fitness-related behavioural performance (i.e., escape response). We found that consistent inter-individual variation in MP ingestion was prevalent and led to differential impacts within exposure treatments. Individuals with high MP ingestion rates exhibited markedly inferior escape responses, a result that was partially concealed in treatment-level analyses. Our findings show that the measured response of populations to environmental perturbations could be confounded by variation in individual-level responses and that the explicit integration of MP ingestion variation can reveal cryptic patterns during exposure experiments.

Elastic energy storage in seahorses leads to a unique suction flow dynamics compared with other actinopterygians.

Suction feeding is a dominant prey-capture strategy across actinopterygians, consisting of a rapid expansion of the mouth cavity that drives a flow of water containing the prey into the mouth. Suction feeding is a power-hungry behavior, involving the actuation of cranial muscles as well as the anterior third of the fish's swimming muscles. Seahorses, which have reduced swimming muscles, evolved a unique mechanism for elastic energy storage that powers their suction flows. This mechanism allows seahorses to achieve head rotation speeds that are 50 times faster than those of fish lacking such a mechanism. However, it is unclear how the dynamics of suction flows in seahorses differ from the conserved pattern observed across other actinopterygians, or how differences in snout length across seahorses affect these flows. Using flow visualization experiments, we show that seahorses generate suction flows that are 8 times faster than those of similar-sized fish, and that the temporal patterns of cranial kinematics and suction flows in seahorses differ from the conserved pattern observed across other actinopterygians. However, the spatial patterns retain the conserved actinopterygian characteristics, where suction flows impact a radially symmetric region of ∼1 gape diameter outside the mouth. Within seahorses, increases in snout length were associated with slower suction flows and faster head rotation speeds, resulting in a trade-off between pivot feeding and suction feeding. Overall, this study shows how the unique cranial kinematics in seahorses are manifested in their suction-feeding performance, and highlights the trade-offs associated with their unique morphology and mechanics.

Work that body: fin and body movements determine herbivore feeding performance within the natural reef environment.

Herbivorous fishes form a keystone component of reef ecosystems, yet the functional mechanisms underlying their feeding performance are poorly understood. In water, gravity is counter-balanced by buoyancy, hence fish are recoiled backwards after every bite they take from the substrate. To overcome this recoil and maintain contact with the algae covered substrate, fish need to generate thrust while feeding. However, the locomotory performance of reef herbivores in the context of feeding has hitherto been ignored. We used a three-dimensional high-speed video system to track mouth and body kinematics during in situ feeding strikes of fishes in the genus Zebrasoma, while synchronously recording the forces exerted on the substrate. These herbivores committed stereotypic and coordinated body and fin movements when feeding off the substrate and these movements determined algal biomass removed. Specifically, the speed of rapidly backing away from the substrate was associated with the magnitude of the pull force and the biomass of algae removed from the substrate per feeding bout. Our new framework for measuring biting performance in situ demonstrates that coordinated movements of the body and fins play a crucial role in herbivore foraging performance and may explain major axes of body and fin shape diversification across reef herbivore guilds.

Suction Feeding by Small Organisms: Performance Limits in Larval Vertebrates and Carnivorous Plants.

Suction feeding has evolved independently in two highly disparate animal and plant systems, aquatic vertebrates and carnivorous bladderworts. We review the suction performance of animal and plant suction feeders to explore biomechanical performance limits for aquatic feeders based on morphology and kinematics, in the context of current knowledge of suction feeding. While vertebrates have the greatest diversity and size range of suction feeders, bladderworts are the smallest and fastest known suction feeders. Body size has profound effects on aquatic organismal function, including suction feeding, particularly in the intermediate flow regime that tiny organisms can experience. A minority of tiny organisms suction feed, consistent with model predictions that generating effective suction flow is less energetically efficient and also requires more flow-rate specific power at small size. Although the speed of suction flows generally increases with body and gape size, some specialized tiny plant and animal predators generate suction flows greater than those of suction feeders 100 times larger. Bladderworts generate rapid flow via high-energy and high-power elastic recoil and suction feed for nutrients (relying on photosynthesis for energy). Small animals may be limited by available muscle energy and power, although mouth protrusion can offset the performance cost of not generating high suction pressure. We hypothesize that both the high energetic costs and high power requirements of generating rapid suction flow shape the biomechanics of small suction feeders, and that plants and animals have arrived at different solutions due in part to their different energy budgets.

Coral tentacle elasticity promotes an out-of-phase motion that improves mass transfer.

Corals rely almost exclusively on the ambient flow of water to support their respiration, photosynthesis, prey capture, heat exchange and reproduction. Coral tentacles extend to the flow, interact with it and oscillate under the influence of waves. Such oscillating motions of flexible appendages are considered adaptive for reducing the drag force on flexible animals in wave-swept environments, but their significance under slower flows is unclear. Using in situ and laboratory measurements of the motion of coral tentacles under wave-induced flow, we investigated the dynamics of the tentacle motion and its impact on mass transfer. We found that tentacle velocity preceded the water velocity by approximately one-quarter of a period. This out-of-phase behaviour enhanced mass transfer at the tentacle tip by up to 25% as compared with an in-phase motion. The enhancement was most pronounced under flows slower than 3.2 cm s-1, which are prevalent in many coral-reef environments. We found that the out-of-phase motion results from the tentacles' elasticity, which can presumably be modified by the animal. Our results suggest that the mechanical properties of coral tentacles may represent an adaptive advantage that improves mass transfer under the limiting conditions of slow ambient flows. Because the mechanism we describe operates by enhancing convective processes, it is expected to enhance other fitness-determining transport phenomena such as heat exchange and particle capture.

Hydrodynamic Simulations of the Performance Landscape for Suction-Feeding Fishes Reveal Multiple Peaks for Different Prey Types.

The complex interplay between form and function forms the basis for generating and maintaining organismal diversity. Fishes that rely on suction-feeding for prey capture exhibit remarkable phenotypic and trophic diversity. Yet the relationships between fish phenotypes and feeding performance on different prey types are unclear, partly because the morphological, biomechanical, and hydrodynamic mechanisms that underlie suction-feeding are complex. Here we demonstrate a general framework to investigate the mapping of multiple phenotypic traits to performance by mapping kinematic variables to suction-feeding capacity. Using a mechanistic model of suction-feeding that is based on core physical principles, we predict prey capture performance across a broad range of phenotypic trait values, for three general prey types: mollusk-like prey, copepod-like prey, and fish-like prey. Mollusk-like prey attach to surfaces, copepod-like prey attempt to escape upon detecting the hydrodynamic disturbance produced by the predator, and fish-like prey attempt to escape when the predator comes within a threshold distance. This approach allowed us to evaluate suction-feeding performance for any combination of six key kinematic traits, irrespective of whether these trait combinations were observed in an extant species, and to generate a multivariate mapping of phenotype to performance. We used gradient ascent methods to explore the complex topography of the performance landscape for each prey type, and found evidence for multiple peaks. Characterization of phenotypes associated with performance peaks indicates that the optimal kinematic parameter range for suction-feeding on different prey types are narrow and distinct from each other, suggesting different functional constraints for the three prey types. These performance landscapes can be used to generate hypotheses regarding the distribution of extant species in trait space and their evolutionary trajectories toward adaptive peaks on macroevolutionary fitness landscapes.

Pelagic fish predation is stronger at temperate latitudes than near the equator.

Species interactions are widely thought to be strongest in the tropics, potentially contributing to the greater number of species at lower latitudes. Yet, empirical tests of this "biotic interactions" hypothesis remain limited and often provide mixed results. Here, we analyze 55 years of catch per unit effort data from pelagic longline fisheries to estimate the strength of predation exerted by large predatory fish in the world's oceans. We test two central tenets of the biotic interactions hypothesis: that predation is (1) strongest near the equator, and (2) positively correlated with species richness. Counter to these predictions, we find that predation is (1) strongest in or near the temperate zone and (2) negatively correlated with oceanic fish species richness. These patterns suggest that, at least for pelagic fish predation, common assumptions about the latitudinal distribution of species interactions do not apply, thereby challenging a leading explanation for the latitudinal gradient in species diversity.

The hydrodynamic regime drives flow reversals in suction-feeding larval fishes during early ontogeny.

Fish larvae are the smallest self-sustaining vertebrates. As such, they face multiple challenges that stem from their minute size, and from the hydrodynamic regime in which they dwell. This regime, of intermediate Reynolds numbers, was shown to affect the swimming of larval fish and impede their ability to capture prey. Prey capture is impeded because smaller larvae produce weaker suction flows, exerting weaker forces on the prey. Previous observations on feeding larvae also showed prey exiting the mouth after initially entering it (hereafter 'in-and-out'), although the mechanism causing such failures had been unclear. In this study, we used numerical simulations to investigate the hydrodynamic mechanisms responsible for the failure to feed caused by this in-and-out prey movement. Detailed kinematics of the expanding mouth during prey capture by larval Sparus aurata were used to parameterize age-specific numerical models of the flows inside the mouth. These models revealed that for small larvae which expand their mouth slowly, fluid entering the mouth cavity is expelled through the mouth before it is closed, resulting in flow reversal at the orifice. This relative efflux of water through the mouth was >8% of the influx through the mouth for younger ages. However, similar effluxes were found when we simulated slow strikes by larger fish. The simulations can explain the observations of larval fish failing to feed because of the in-and-out movement of the prey. These results further highlight the importance of transporting the prey from the gape deeper into the mouth cavity in determining suction-feeding success.

Rapid adaptive evolution of scale-eating kinematics to a novel ecological niche.

The origins of novel trophic specialization, in which organisms begin to exploit resources for the first time, may be explained by shifts in behavior such as foraging preferences or feeding kinematics. One way to investigate behavioral mechanisms underlying ecological novelty is by comparing prey capture kinematics among species. We investigated the contribution of kinematics to the origins of a novel ecological niche for scale-eating within a microendemic adaptive radiation of pupfishes on San Salvador Island, Bahamas. We compared prey capture kinematics across three species of pupfish while they consumed shrimp and scales in the lab, and found that scale-eating pupfish exhibited peak gape sizes twice as large as in other species, but also attacked prey with a more obtuse angle between their lower jaw and suspensorium. We then investigated how this variation in feeding kinematics could explain scale-biting performance by measuring bite size (surface area removed) from standardized gelatin cubes. We found that a combination of larger peak gape and more obtuse lower jaw and suspensorium angles resulted in approximately 40% more surface area removed per strike, indicating that scale-eaters may reside on a performance optimum for scale biting. To test whether feeding performance could contribute to reproductive isolation between species, we also measured F1 hybrids and found that their kinematics and performance more closely resembled generalists, suggesting that F1 hybrids may have low fitness in the scale-eating niche. Ultimately, our results suggest that the evolution of strike kinematics in this radiation is an adaptation to the novel niche of scale eating.

The interaction between suction feeding performance and prey escape response determines feeding success in larval fish.

The survival of larval marine fishes during early development depends on their ability to feed before depleting their yolk reserves. Most larval fish capture prey by expanding their mouth, generating a 'suction flow' that draws the prey into it. These larvae dwell in a hydrodynamic environment that impedes their ability to capture even non-evasive prey; however, the marine environment is characterized by an abundance of evasive prey, predominantly copepods. Copepods sense the hydrodynamic disturbance created by approaching predators and perform high-acceleration escape maneuvers. Using a 3D high-speed video system, we characterized the interaction between Sparus aurata larvae and prey from a natural zooplankton assemblage that contained evasive prey, and assessed the factors that determine the outcome of these interactions. At 8-33 days post hatching, larvae preferentially attacked large prey that was moving prior to the initialization of the strike; however, feeding success was lower for larger, more evasive prey. Thus, larvae were challenged in capturing their preferred prey. Larval feeding success increased with increasing Reynolds numbers, but decreased sharply when the prey performed an escape maneuver. The kinematics of successful strikes resulted in a shorter response time but higher hydrodynamic signature available for the prey, suggesting that strike success in our experiments was determined by brevity rather than stealth: executing a fast strike eliminated a potential escape response by the prey. Our observations of prey selectivity reveal that larval performance, rather than preferences, determines their diet during early development.

A novel mechanism of mixing by pulsing corals.

The dynamic pulsation of xeniid corals is one of the most fascinating phenomena observed in coral reefs. We quantify for the first time the flow near the tentacles of these soft corals, the active pulsations of which are thought to enhance their symbionts' photosynthetic rates by up to an order of magnitude. These polyps are approximately 1 cm in diameter and pulse at frequencies between approximately 0.5 and 1 Hz. As a result, the frequency-based Reynolds number calculated using the tentacle length and pulse frequency is on the order of 10 and rapidly decays as with distance from the polyp. This introduces the question of how these corals minimize the reversibility of the flow and bring in new volumes of fluid during each pulse. We estimate the Péclet number of the bulk flow generated by the coral as being on the order of 100-1000 whereas the flow between the bristles of the tentacles is on the order of 10. This illustrates the importance of advective transport in removing oxygen waste. Flow measurements using particle image velocimetry reveal that the individual polyps generate a jet of water with positive vertical velocities that do not go below 0.1 cm s-1 and with average volumetric flow rates of approximately 0.71 cm3 s-1 Our results show that there is nearly continual flow in the radial direction towards the polyp with only approximately 3.3% back flow. 3D numerical simulations uncover a region of slow mixing between the tentacles during expansion. We estimate that the average flow that moves through the bristles of the tentacles is approximately 0.03 cm s-1 The combination of nearly continual flow towards the polyp, slow mixing between the bristles, and the subsequent ejection of this fluid volume into an upward jet ensures the polyp continually samples new water with sufficient time for exchange to occur.

Pleiotropic jaw morphology links the evolution of mechanical modularity and functional feeding convergence in Lake Malawi cichlids.

Complexity in how mechanistic variation translates into ecological novelty could be critical to organismal diversification. For instance, when multiple distinct morphologies can generate the same mechanical or functional phenotype, this could mitigate trade-offs and/or provide alternative ways to meet the same ecological challenge. To investigate how this type of complexity shapes diversity in a classic adaptive radiation, we tested several evolutionary consequences of the anterior jaw four-bar linkage for Lake Malawi cichlid trophic diversification. Using a novel phylogenetic framework, we demonstrated that different mechanical outputs of the same four jaw elements are evolutionarily associated with both jaw protrusion distance and jaw protrusion angle. However, these two functional aspects of jaw protrusion have evolved independently. Additionally, although four-bar morphology showed little evidence for attraction to optima, there was substantial evidence of adaptive peaks for emergent four-bar linkage mechanics and jaw protrusion abilities among Malawi feeding guilds. Finally, we highlighted a clear case of two cichlid species that have -independently evolved to graze algae in less than 2 Myr and have converged on similar jaw protrusion abilities as well as four-bar linkage mechanics, but have evolved these similarities via non-convergent four-bar morphologies.

Prepared for the future: A strong signal of evolution toward the adult benthic niche during the pelagic stage in Labrid fishes.

The morphology of organisms reflects a balance between their evolutionary history, functional demands, and biomechanical constraints imposed by the immediate environment. In many fish species, a marked shift in the selection regime is evident when pelagic larvae, which swim and feed in the open ocean, settle in their adult benthic habitat. This shift is particularly dramatic in coral-reef fishes, where the adult habitat is immensely complex. However, whether the adult trophic ecotype affects the morphology of early-life stages is unclear. We measured a suite of 26 functional-morphological traits in the head and body of larvae from an ontogenetic series of 16 labrid species. Using phylogenetic comparative methods, we reconstructed the location of adaptive peaks of larvae whose adults are associated with different trophic ecotypes. We found that the morphospace occupation in these larvae is largely driven by divergent adaptations to the adult benthic habitats. The disparity between adaptive peaks is achieved early and does not monotonically increase with size. Our findings thus refute the notion that larvae rapidly acquire the trophic-specific traits during a metamorphic period immediately prior to settlement. This early specialization might be due to the highly complex musculoskeletal system of the head that cannot be rapidly modified.

The Levantine jellyfish Rhopilema nomadica and Rhizostoma pulmo swim faster against the flow than with the flow.

Jellyfish locomotion and orientation have been studied in the past both in the laboratory, testing mostly small jellyfish, and in the field, where it was impossible to control the seawater currents. Utilizing an outdoor water flume, we tested the locomotion of jellyfish when swimming against and with currents of up to 4.5 cm s-1. We used adult jellyfish from two of the most abundant species in the eastern Mediterranean, Rhopilema nomadica and Rhizostoma pulmo, and measured their pulsation frequency and swimming speed relative to the water. While pulsation frequency was not affected by the water velocity, jellyfish swam faster against the current than with it. This finding suggests that jellyfish possess a sensory ability, whose mechanism is currently unknown, enabling them to gauge the flow and react to it, possibly in order to reduce the risk of stranding.

Phylogenomics of a putatively convergent novelty: did hypertrophied lips evolve once or repeatedly in Lake Malawi cichlid fishes?

BACKGROUND: Phylogenies provide critical information about convergence during adaptive radiation. To test whether there have been multiple origins of a distinctive trophic phenotype in one of the most rapidly radiating groups known, we used ultra-conserved elements (UCEs) to examine the evolutionary affinities of Lake Malawi cichlids lineages exhibiting greatly hypertrophied lips. RESULTS: The hypertrophied lip cichlids Cheilochromis euchilus, Eclectochromis ornatus, Placidochromis "Mbenji fatlip", and Placidochromis milomo are all nested within the non-mbuna clade of Malawi cichlids based on both concatenated sequence and single nucleotide polymorphism (SNP) inferred phylogenies. Lichnochromis acuticeps that exhibits slightly hypertrophied lips also appears to have evolutionary affinities to this group. However, Chilotilapia rhoadesii that lacks hypertrophied lips was recovered as nested within the species Cheilochromis euchilus. Species tree reconstructions and analyses of introgression provided largely ambiguous patterns of Malawi cichlid evolution. CONCLUSIONS: Contrary to mitochondrial DNA phylogenies, bifurcating trees based on our 1024 UCE loci supported close affinities of Lake Malawi lineages with hypertrophied lips. However, incomplete lineage sorting in Malawi tends to render these inferences more tenuous. Phylogenomic analyses will continue to provide powerful inferences about whether phenotypic novelties arose once or multiple times during adaptive radiation.