Twist and chew: three-dimensional tongue kinematics during chewing in macaque primates.

Three-dimensional (3D) tongue movements are central to performance of feeding functions by mammals and other tetrapods, but 3D tongue kinematics during feeding are poorly understood. Tongue kinematics were recorded during grape chewing by macaque primates using biplanar videoradiography. Complex shape changes in the tongue during chewing are dominated by a combination of flexion in the tongue's sagittal planes and roll about its long axis. As hypothesized for humans, in macaques during tongue retraction, the middle (molar region) of the tongue rolls to the chewing (working) side simultaneous with sagittal flexion, while the tongue tip flexes to the other (balancing) side. Twisting and flexion reach their maxima early in the fast close phase of chewing cycles, positioning the food bolus between the approaching teeth prior to the power stroke. Although 3D tongue kinematics undoubtedly vary with food type, the mechanical role of this movement-placing the food bolus on the post-canine teeth for breakdown-is likely to be a powerful constraint on tongue kinematics during this phase of the chewing cycle. The muscular drivers of these movements are likely to include a combination of intrinsic and extrinsic tongue muscles.

Linking ecomechanical models and functional traits to understand phenotypic diversity.

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.

A phylogenomic framework for pelagiarian fishes (Acanthomorpha: Percomorpha) highlights mosaic radiation in the open ocean.

The fish clade Pelagiaria, which includes tunas as its most famous members, evolved remarkable morphological and ecological variety in a setting not generally considered conducive to diversification: the open ocean. Relationships within Pelagiaria have proven elusive due to short internodes subtending major lineages suggestive of rapid early divergences. Using a novel sequence dataset of over 1000 ultraconserved DNA elements (UCEs) for 94 of the 286 species of Pelagiaria (more than 70% of genera), we provide a time-calibrated phylogeny for this widely distributed clade. Some inferred relationships have clear precedents (e.g. the monophyly of 'core' Stromateoidei, and a clade comprising 'Gempylidae' and Trichiuridae), but others are unexpected despite strong support (e.g. Chiasmodontidae + Tetragonurus). Relaxed molecular clock analysis using node-based fossil calibrations estimates a latest Cretaceous origin for Pelagiaria, with crown-group families restricted to the Cenozoic. Estimated mean speciation rates decline from the origin of the group in the latest Cretaceous, although credible intervals for root and tip rates are broad and overlap in most cases, and there is higher-than-expected partitioning of body shape diversity (measured as fineness ratio) between clades concentrated during the Palaeocene-Eocene. By contrast, more direct measures of ecology show either no substantial deviation from a null model of diversification (diet) or patterns consistent with evolutionary constraint or high rates of recent change (depth habitat). Collectively, these results indicate a mosaic model of diversification. Pelagiarians show high morphological disparity and modest species richness compared to better-studied fish radiations in contrasting environments. However, this pattern is also apparent in other clades in open-ocean or deep-sea habitats, and suggests that comparative study of such groups might provide a more inclusive model of the evolution of diversity in fishes.

When Does Form Reflect Function? Acknowledging and Supporting Ecomorphological Assumptions.

Ecomorphology is the study of relationships between organismal morphology and ecology. As such, it is the only way to determine if morphometric data can be used as an informative proxy for ecological variables of interest. To achieve this goal, ecomorphology often depends on, or directly tests, assumptions about the nature of the relationships among morphology, performance, and ecology. We discuss three approaches to the study of ecomorphology: morphometry-driven, function-driven, and ecology-driven and study design choices inherent to each approach. We also identify 10 assumptions that underlie ecomorphological research: 4 of these are central to all ecomorphological studies and the remaining 6 are variably applicable to some of the specific approaches described above. We discuss how these assumptions may impact ecomorphological studies and affect the interpretation of their findings. We also point out some limitations of ecomorphological studies, and highlight some ways by which we can strengthen, validate, or eliminate systematic assumptions.

Structure of supporting elements in the dorsal fin of percid fishes.

The dorsal fin is one of the most varied swimming structures in Acanthomorpha, the spiny-finned fishes. This fin can be present as a single contiguous structure supported by bony spines and soft lepidotrichia, or it may be divided into an anterior, spiny dorsal fin and a posterior, soft dorsal fin. The freshwater fish family Percidae exhibits especially great variation in dorsal fin spacing, including fishes with separated fins of varying gap length and fishes with contiguous fins. We hypothesized that fishes with separated dorsal fins, especially those with large gaps between fins, would have stiffened fin elements at the leading edge of the soft dorsal fin to resist hydrodynamic loading during locomotion. For 10 percid species, we measured the spacing between dorsal fins and calculated the second moment of area of selected spines and lepidotrichia from museum specimens. There was no significant relationship between the spacing between dorsal fins and the second moment of area of the leading edge of the soft dorsal fin.

Swimming with multiple propulsors: measurement and comparison of swimming gaits in three species of neotropical cichlids.

Comparative studies of fish swimming have been limited by the lack of quantitative definitions of fish gaits. Traditionally, steady swimming gaits have been defined categorically by the fin or region of the body that is used as the main propulsor and named after major fish clades (e.g. carangiform, anguilliform, balistiform, labriform). This method of categorization is limited by the lack of explicit measurements, the inability to incorporate contributions of multiple propulsors and the inability to compare gaits across different categories. I propose an alternative framework for the definition and comparison of fish gaits based on the propulsive contribution of each structure (body and/or fin) being used as a propulsor relative to locomotor output, and demonstrate the effectiveness of this framework by comparing three species of neotropical cichlids with different body shapes. This approach is modular with respect to the number of propulsors considered, flexible with respect to the definition of the propulsive inputs and the locomotor output of interest, and designed explicitly to handle combinations of propulsors. Using this approach, gait can be defined as a trajectory through propulsive space, and gait transitions can be defined as discontinuities in the gait trajectory. By measuring and defining gait in this way, patterns of clustering corresponding to existing categorical definitions of gait may emerge, and gaits can be rigorously compared across categories.

Performance variation due to stiffness in a tuna-inspired flexible foil model.

Tuna are fast, economical swimmers in part due to their stiff, high aspect ratio caudal fins and streamlined bodies. Previous studies using passive caudal fin models have suggested that while high aspect ratio tail shapes such as a tuna's generally perform well, tail performance cannot be determined from shape alone. In this study, we analyzed the swimming performance of tuna-tail-shaped hydrofoils of a wide range of stiffnesses, heave amplitudes, and frequencies to determine how stiffness and kinematics affect multiple swimming performance parameters for a single foil shape. We then compared the foil models' kinematics with published data from a live swimming tuna to determine how well the hydrofoil models could mimic fish kinematics. Foil kinematics over a wide range of motion programs generally showed a minimum lateral displacement at the narrowest part of the foil, and, immediately anterior to that, a local area of large lateral body displacement. These two kinematic patterns may enhance thrust in foils of intermediate stiffness. Stiffness and kinematics exhibited subtle interacting effects on hydrodynamic efficiency, with no one stiffness maximizing both thrust and efficiency. Foils of intermediate stiffnesses typically had the greatest coefficients of thrust at the highest heave amplitudes and frequencies. The comparison of foil kinematics with tuna kinematics showed that tuna motion is better approximated by a zero angle of attack foil motion program than by programs that do not incorporate pitch. These results indicate that open questions in biomechanics may be well served by foil models, given appropriate choice of model characteristics and control programs. Accurate replication of biological movements will require refinement of motion control programs and physical models, including the creation of models of variable stiffness.

Correlated evolution of body and fin morphology in the cichlid fishes.

Body and fin shapes are chief determinants of swimming performance in fishes. Different configurations of body and fin shapes can suit different locomotor specializations. The success of any configuration is dependent upon the hydrodynamic interactions between body and fins. Despite the importance of body-fin interactions for swimming, there are few data indicating whether body and fin configurations evolve in concert, or whether these structures vary independently. The cichlid fishes are a diverse family whose well-studied phylogenetic relationships make them ideal for the study of macroevolution of ecomorphology. This study measured body, and caudal and median fin morphology from radiographs of 131 cichlid genera, using morphometrics and phylogenetic comparative methods to determine whether these traits exhibit correlated evolution. Partial least squares canonical analysis revealed that body, caudal fin, dorsal fin, and anal fin shapes all exhibited strong correlated evolution consistent with locomotor ecomorphology. Major patterns included the evolution of deep body profiles with long fins, suggestive of maneuvering specialization; and the evolution of narrow, elongate caudal peduncles with concave tails, a combination that characterizes economical cruisers. These results demonstrate that body shape evolution does not occur independently of other traits, but among a suite of other morphological changes that augment locomotor specialization.

Passive mechanical models of fish caudal fins: effects of shape and stiffness on self-propulsion.

Fishes are found in a great variety of body forms with tail shapes that vary from forked tuna-like tails to the square-shaped tails found in some deep-bodied species. Hydrodynamic theory suggests that a fish's body and tail shape affects undulatory swimming performance. For example, a narrow caudal peduncle is believed to reduce drag, and a tuna-like tail to increase thrust. Despite the prevalence of these assertions, there is no experimental verification of the hydrodynamic mechanisms that may confer advantages on specific forms. Here, we use a mechanically-actuated flapping foil model to study how two aspects of shape, caudal peduncle depth and presence or absence of a forked caudal fin, may affect different aspects of swimming performance. Four different foil shapes were each made of plastics of three different flexural stiffnesses, permitting us to study how shape might interact with stiffness to produce swimming performance. For each foil, we measured the self-propelling swimming speed. In addition, we measured the forces, torques, cost of transport and power coefficient of each foil swimming at its self-propelling speed. There was no single 'optimal' foil exhibiting the highest performance in all metrics, and for almost all measures of swimming performance, foil shape and flexural stiffness interacted in complicated ways. Particle image velocimetry of several foils suggested that stiffness might affect the relative phasing of the body trailing edge and the caudal fin leading edge, changing the flow incident to the tail, and affecting hydrodynamics of the entire foil. The results of this study of a simplified model of fish body and tail morphology suggest that considerable caution should be used when inferring a swimming performance advantage from body and tail shape alone.

Serotonin as an integrator of leech behavior and muscle mechanical performance.

The obliquely striated muscle in the leech body wall has a broad functional repertoire; it provides power for both locomotion and suction feeding. It also operates over an unusually high strain range, undergoing up to threefold changes in length. Serotonin (5-HT) may support this functional flexibility, integrating behavior and biomechanics. It can act centrally, promoting motor outputs that drive body wall movements, and peripherally, modulating the mechanical properties of body wall muscle. During isometric contractions 5-HT enhances active force production and reduces resting muscle tone. We therefore hypothesized that 5-HT would increase net work output during the cyclical contractions associated with locomotion and feeding. Longitudinal strains measured during swimming, crawling and feeding were applied to body wall muscle in vitro with the timing and duration of stimulation selected to maximize net work output. The net work output during all simulated behaviors significantly increased in the presence of 100µM 5-HT relative to the 5-HT-free control condition. Without 5-HT the muscle strips could not achieve a net positive work output during simulated swimming. The decrease in passive tension associated with 5-HT may also be important in reducing muscle antagonist work during longitudinal muscle lengthening. The behavioral and mechanical effects of 5-HT during locomotion are clearly complementary, promoting particular behaviors and enhancing muscle performance during those behaviors. Although 5-HT can enhance muscle mechanical performance during simulated feeding, low in vivo activity in serotonergic neurons during feeding may mean that its mechanical role during this behavior is less important than during locomotion.

Leeches run cold, then hot.

Food processing is costly, potentially limiting the energy and time devoted to other essential functions such as locomotion or reproduction. In ectotherms, post-prandial thermophily, the selection of a warm environmental temperature after feeding, may be advantageous in minimizing the duration of this elevated cost. Although present in many vertebrate taxa, this behaviour had not previously been observed in invertebrates. Sanguivorous leeches ingest large blood meals that are costly to process and limit mobility until excess fluid can actively be expelled to reduce body volume. When presented with a temperature gradient from 10°C to 30°C, leeches select a temperature that is significantly warmer (24.3 ± 0.9°C, n = 6) than their acclimation temperature (T(a), 21°C). Unfed leeches preferred temperatures that were significantly cooler than ambient (12.8 ± 0.9°C, n = 6). This behavioural strategy is consistent with minimizing the time course of elevated post-feeding energy costs and reducing energy expenditure during fasting. Our observations raise the possibility that thermoregulatory behaviour of this type is an unrecognized feature of other invertebrate taxa.

The mechanics of explosive seed dispersal in orange jewelweed (Impatiens capensis).

Explosive dehiscence ballistically disperses seeds in a number of plant species. During dehiscence, mechanical energy stored in specialized tissues is transferred to the seeds to increase their kinetic and potential energies. The resulting seed dispersal patterns have been investigated in some ballistic dispersers, but the mechanical performance of a launch mechanism of this type has not been measured. The properties of the energy storage tissue and the energy transfer efficiency of the launch mechanism were quantified in Impatiens capensis. In this species the valves forming the seed pod wall store mechanical energy. Their mass specific energy storage capacity (124 J kg(-1)) was comparable with that of elastin and spring steel. The energy storage capacity of the pod tissues was determined by their level of hydration, suggesting a role for turgor pressure in the energy storage mechanism. During dehiscence the valves coiled inwards, collapsing the pod and ejecting the seeds. Dehiscence took 4.2+/-0.4 ms (mean +/-SEM, n=13). The estimated efficiency with which energy was transferred to the seeds was low (0.51+/-0.26%, mean +/-SEM, n=13). The mean seed launch angle (17.4+/-5.2, mean +/-SEM, n=45) fell within the range predicted by a ballistic model to maximize dispersal distance. Low ballistic dispersal efficiency or effectiveness may be characteristic of species that also utilize secondary seed dispersal mechanisms.