Muscle power production during intermittent swimming in bluegill sunfish.

Locomotion is essential for the survival and fitness of animals. Fishes have evolved a variety of mechanisms to minimize the cost of transport. For instance, bluegill sunfish have recently been shown to employ intermittent swimming in nature and in laboratory conditions. We focused on the functional properties of the power-producing muscles that generate propulsive forces in bluegill to understand the implications of intermittent activity. We used in vivo aerobic or red muscle activity parameters (e.g., oscillation frequency and onset time and duration of activation) in muscle physiology experiments to examine muscle power output during intermittent versus steady swimming in these fish. Intermittent propulsion involves swimming at relatively slow speeds with short propulsive bursts alternating with gliding episodes. The propulsive bursts are at higher oscillation frequencies than would be predicted for a given average swimming speed with constant propulsion. The work-loop muscle physiology experiments with red muscle demonstrated that intermittent activity allows muscle to produce sufficient power for swimming compared with imposed steady swimming conditions. Further, the intermittent muscle activity in vitro reduces fatigue relative to steady or continuous activity. This work supports the fixed-gear hypothesis that suggests that there are preferred oscillation frequencies that optimize efficiency in muscle use and minimize cost of transport.

Drag coefficient estimates from coasting bluegill sunfish Lepomis macrochirus.

The drag coefficient bluegill sunfish Lepomis macrochirus was estimated from coasting deceleration as (mean ± SD) 0.0154 ± 0.0070 at a Reynolds number of 41,000 ± 14,000. This was within the coasting range in other species and lower than values obtained from dead drag measurements in this species and others. Low momentum losses during coasting may allow its use during intermittent propulsion to modulate power output or maximize energy economy.

Linking muscle metabolism and functional variation to field swimming performance in bluegill sunfish (Lepomis macrochirus).

Skeletal muscle has diverse mechanical roles during locomotion. In swimming fish, power-producing muscles work in concert with the accessory muscles of the fins which augment and control power transfer to the water. Although fin muscles represent a significant proportion of the locomotor muscle mass, their physiological properties are poorly characterized. To examine the relationship between muscle metabolism and the differing mechanical demands placed on distinct muscle groups, we quantified the aerobic and glycolytic capacities of the myotomal, pectoral and caudal muscles of bluegill sunfish. These were indicated by the activities of citrate synthase and lactate dehydrogenase, rate-limiting enzymes for aerobic respiration and glycolysis, respectively. The well-established roles of slow and fast myotomal muscle types in sustained and transient propulsive movements allows their use as benchmarks to which other muscles can be compared to assess their function. Slow myotomal muscle had the highest CS activity, consistent with meeting the high metabolic and mechanical power demands of body-caudal fin (BCF) swimming at the upper end of the aerobically supported speed range. The largest pectoral adductors and abductors had CS activities lower than the slow myotomal muscle, in line with their role supplying thrust for low-speed, low-power swimming. The metabolic capacities of the caudal muscles were surprisingly low and inconsistent with their activity during steady-state BCF swimming at high speeds. This may reflect adaptation to the observed swimming behavior in the field, which typically involved short bouts of BCF-propulsive cycles rather than sustained propulsive activity.

Field swimming behavior in largemouth bass deviates from predictions based on economy and propulsive efficiency.

Locomotion is energetically expensive. This may create selection pressures that favor economical locomotor strategies, such as the adoption of low-cost speeds and efficient propulsive movements. For swimming fish, the energy expended to travel a unit distance, or cost of transport (COT), has a U-shaped relationship to speed. The relationship between propulsive kinematics and speed, summarized by the Strouhal number (St=fA/U, where f is tail beat frequency, A is tail tip amplitude in m and U is swimming speed in m s-1), allows for maximal propulsive efficiency where 0.2

Locomotor and energetic consequences of behavioral thermoregulation in the sanguivorous leech Hirudo verbana.

Medicinal leeches (Hirudo verbana) thermoregulate with respect to their sanguivorous feeding behavior. Immediate postprandial preferences are for warmer than their initial acclimation temperature (Ta, 21°C, Petersen et al. 2011), while unfed leeches have a lower preferred temperature (Tpref, 12.5°C). This may reduce energy expenditure and defer starvation if feeding opportunities are limited. Energetic benefits may have an associated cost if low temperatures reduce mobility and the ability to locate further hosts. These costs could be limited if mobility is unimpaired at low temperatures, or if acclimation can restore locomotor performance to the levels at Ta. The transition from Ta to the unfed Tpref significantly reduced speed and propulsive cycle frequency during swimming, and extension and retraction rates during crawling. Aerobic metabolic rate was also reduced from 0.20±0.03Wkg-1 at Ta to 0.10±0.03Wkg-1 at Tpref. The Q10 values of 1.7-2.9 for energetic and swimming parameters indicate a substantial temperature effect, although part of the decline in swimming performance can be attributed to temperature-related changes in water viscosity. 6 weeks at Ta resulted in no detectable acclimation in locomotor performance or aerobic metabolism. The energetic savings associated with a lower Tpref in unfed leeches effectively doubled the estimated time until depletion of energy reserves. Given that some mobility is still retained at Tpref, and that acclimation is in itself costly, the energetic benefits of selecting cooler temperatures between feedings may outweigh the costs associated with reduced locomotor performance.

Scaling of the fast-start escape response of juvenile bluegills.

Morphology, size and physiological properties change markedly across fish ontogeny. This impacts locomotor performance and organismal fitness, although the effects are unpredictable due to the complexity of phenotype-function relationships. Morphological and behavioral changes with growth are often paralleled by changes in habitat use, diet and vulnerability to predators. Our goal was to quantify the changes in external morphology and escape performance throughout post-larval development in bluegill sunfish (Lepomis macrochirus), and place these changes in context with known changes in habitat use in the field. Development into adult ecomorphs is associated with phenotypic plasticity in response to habitat-specific differences in diet. On this basis, we hypothesized that variation in morphology and performance would increase during bluegill ontogeny as diversification of adult ecomorphs occurred. However, we found that variation in phenotype and escape performance decreased during early ontogeny. Phenotypic variation expanded later in development, after fish gained access to the variety of habitats and food types that may favor phenotypic plasticity. Performance is predicted to decline with growth due to the differential scaling of inertia and cross-sectional area, a major determinant of muscle force. In contrast, acceleration increased with size, and velocity and acceleration increased more rapidly with size than predicted. Post-larval maturation in bluegill featured a shift to a deeper body shape, and an increase in the relative size of the anal and caudal fins. This was a likely factor in the deviation of escape performance scaling relationships from predictions based on geometric similarity.

The effects of steady swimming on fish escape performance.

Escape maneuvers are essential to the survival and fitness of many animals. Escapes are frequently initiated when an animal is already in motion. This may introduce constraints that alter the escape performance. In fish, escape maneuvers and steady, body caudal fin (BCF) swimming are driven by distinct patterns of curvature of the body axis. Pre-existing muscle activity may therefore delay or diminish a response. To quantify the performance consequences of escaping in flow, escape behavior was examined in bluegill sunfish (Lepomis macrochirus) in both still-water and during steady swimming. Escapes executed during swimming were kinematically less variable than those made in still-water. Swimming escapes also had increased response latencies and lower peak velocities and accelerations than those made in still-water. Performance was also lower for escapes made up rather than down-stream, and a preference for down-stream escapes may be associated with maximizing performance. The constraints imposed by pre-existing motion and flow, therefore, have the potential to shape predator-prey interactions under field conditions by shifting the optimal strategies for both predators and prey.

Trade-offs between performance and variability in the escape responses of bluegill sunfish (Lepomis macrochirus).

Successful predator evasion is essential to the fitness of many animals. Variation in escape behaviour may be adaptive as it reduces predictability, enhancing escape success. High escape velocities and accelerations also increase escape success, but biomechanical factors likely constrain the behavioural range over which performance can be maximized. There may therefore be a trade-off between variation and performance during escape responses. We have used bluegill sunfish (Lepomis macrochirus) escape responses to examine this potential trade-off, determining the full repertoire of escape behaviour for individual bluegill sunfish and linking this to performance as indicated by escape velocity and acceleration. Fish escapes involve an initial C-bend of the body axis, followed by variable steering movements. These generate thrust and establish the escape direction. Directional changes during the initial C-bend were less variable than the final escape angle, and the most frequent directions were associated with high escape velocity. Significant inter-individual differences in escape angles magnified the overall variation, maintaining unpredictability from a predator perspective. Steering in the latter stages of the escape to establish the final escape trajectory also affected performance, with turns away from the stimulus associated with reduced velocity. This suggests that modulation of escape behaviour by steering may also have an associated performance cost. This has important implications for understanding the scope and control of intra- and inter-individual variation in escape behaviour and the associated costs and benefits.

Resolving shifting patterns of muscle energy use in swimming fish.

Muscle metabolism dominates the energy costs of locomotion. Although in vivo measures of muscle strain, activity and force can indicate mechanical function, similar muscle-level measures of energy use are challenging to obtain. Without this information locomotor systems are essentially a black box in terms of the distribution of metabolic energy. Although in situ measurements of muscle metabolism are not practical in multiple muscles, the rate of blood flow to skeletal muscle tissue can be used as a proxy for aerobic metabolism, allowing the cost of particular muscle functions to be estimated. Axial, undulatory swimming is one of the most common modes of vertebrate locomotion. In fish, segmented myotomal muscles are the primary power source, driving undulations of the body axis that transfer momentum to the water. Multiple fins and the associated fin muscles also contribute to thrust production, and stabilization and control of the swimming trajectory. We have used blood flow tracers in swimming rainbow trout (Oncorhynchus mykiss) to estimate the regional distribution of energy use across the myotomal and fin muscle groups to reveal the functional distribution of metabolic energy use within a swimming animal for the first time. Energy use by the myotomal muscle increased with speed to meet thrust requirements, particularly in posterior myotomes where muscle power outputs are greatest. At low speeds, there was high fin muscle energy use, consistent with active stability control. As speed increased, and fins were adducted, overall fin muscle energy use declined, except in the caudal fin muscles where active fin stiffening is required to maintain power transfer to the wake. The present data were obtained under steady-state conditions which rarely apply in natural, physical environments. This approach also has potential to reveal the mechanical factors that underlie changes in locomotor cost associated with movement through unsteady flow regimes.

Variation in fast-start performance within a population of polyphenic bluegill (Lepomis macrochirus).

Bluegill sunfish Lepomis macrochirus exhibit intraspecific variation in their morphology and swimming performance based on habitat. The pelagic form has a relatively streamlined, fusiform body shape associated with greater steady-state swimming speed and energy economy. In contrast, littoral bluegill have deeper bodies with fins located farther from their center of mass to enhance maneuverability among littoral vegetation. Deeper body shapes have been associated with increased fast-start performance to escape predators or capture prey. We hypothesized that littoral bluegill, which have a deeper body shape, would exhibit greater fast-start performance than pelagic bluegill. A total of 29 bluegill (16 littoral, 13 pelagic) were caught by hook and line, and their fast-start performance was analyzed from high-speed video recordings. Body shape appears to be a poor predictor of fast-start performance. Contrary to our expectations, pelagic bluegill had a significantly higher peak velocity, peak acceleration, and angular velocity compared to littoral bluegill. Pelagic bluegill living among larger predators and foraging on mobile prey may be exposed to selection pressures that favor increased fast-start performance. Integrated studies of internal morphology and physiology are needed to fully understand the relationship between morphology and performance in this population.

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.

Differential segmental strain during active lengthening in a large biarticular thigh muscle during running.

The iliotibialis lateralis pars postacetabularis (ILPO) is the largest muscle in the hindlimb of the guinea fowl and is thought to play an important role during the stance phase of running, both absorbing and producing work. Using sonomicrometry and electromyography, we examined whether the ILPO experiences differential strain between proximal, central and distal portions of the posterior fascicles. When the ILPO is being lengthened while active, the distal portion was found to lengthen significantly more than either the proximal or central portions of the muscle. Our data support the hypothesis that the distal segment lengthened farther and faster because it began activity at shorter sarcomere lengths on the ascending limb of the length-tension curve. Probably because of the self-stabilizing effects of operating on the ascending limb of the length-tension curve, all segments reached the end of lengthening and started shortening at the same sarcomere length. During shortening, this similarity in sarcomere length among the segments was maintained, as predicted from force-velocity effects, and shortening strain was similar in all segments. The differential active strain during active lengthening is thus ultimately determined by differences in strain during the passive portion of the cycle. The sarcomere lengths of all segments of the fascicles were similar at the end of active shortening, but after the passive portion of the cycle the distal segment was shorter. Differential strain in the segments during the passive portion of the cycle may be caused by differential joint excursions at the knee and hip acting on the ends of the muscle and being transmitted differentially by the passive visco-elastic properties of the muscle. Alternatively, the differential passive strain could be due to the action of active or passive muscles in the thigh that transmit force to the IPLO in shear. Based on basic sarcomere dynamics we predict that differential strain is more likely to occur in muscles undergoing active lengthening at the beginning of contraction than those undergoing only shortening.

Mechanisms producing coordinated function across the breadth of a large biarticular thigh muscle.

We examined the hypothesis that structural features of the iliotibialis lateralis pars postacetabularis (ILPO) in guinea fowl allow this large muscle to maintain equivalent function along its anterior-posterior axis. The ILPO, the largest muscle in the hindlimb of the guinea fowl, is a hip and knee extensor. The fascicles of the ILPO originate across a broad region of the ilium and ischium posterior to the hip. Its long posterior fascicles span the length of the thigh and insert directly on the patellar tendon complex. However, its anterior fascicles are shorter and insert on a narrow aponeurosis that forms a tendinous band along the anterior edge of the muscle and is connected distally to the patellar tendon. The biarticular ILPO is actively lengthened and then actively shortened during stance. The moment arm of the fascicles at the hip increases along the anterior to posterior axis, whereas the moment arm at the knee is constant for all fascicles. Using electromyography and sonomicrometry, we examined the activity and strain of posterior and anterior fascicles of the ILPO. The activation was not significantly different in the anterior and posterior fascicles. Although we found significant differences in active lengthening and shortening strain between the anterior and posterior fascicles, the differences were small. The majority of shortening strain is caused by hip extension and the inverse relationship between hip moment arm and fascicle length along the anterior-posterior axis was found to have a major role in ensuring similar shortening strain. However, because the knee moment arm is the same for all fascicles, knee flexion in early stance was predicted to produce much larger lengthening strains in the short anterior fascicles than our measured values at this location. We propose that active lengthening of the anterior fascicles was lower than predicted because the aponeurotic tendon of insertion of the anterior fascicles was stretched and only a portion of the lengthening had to be accommodated by the active muscle fascicles.

Function of a large biarticular hip and knee extensor during walking and running in guinea fowl (Numida meleagris).

Physiological and anatomical evidence suggests that in birds the iliotibialis lateralis pars postacetabularis (ILPO) is functionally important for running. Incorporating regional information, we estimated the mean sarcomere strain trajectory and electromyographic (EMG) amplitude of the ILPO during level and incline walking and running. Using these data and data in the literature of muscle energy use, we examined three hypotheses: (1) active lengthening will occur on the ascending limb of the length-tension curve to avoid potential damage caused by stretch on the descending limb; (2) the active strain cycle will shift to favor active shortening when the birds run uphill and shortening will occur on the plateau and shallow ascending limb of the length-tension curve; and (3) measures of EMG intensity will correlate with energy use when the mechanical function of the muscle is similar. Supporting the first hypothesis, we found that the mean sarcomere lengths at the end of active lengthening during level locomotion were smaller than the predicted length at the start of the plateau of the length-tension curve. Supporting the second hypothesis, the magnitude of active lengthening decreased with increasing slope, whereas active shortening increased. In evaluating the relationship between EMG amplitude and energy use (hypothesis 3), we found that although increases in EMG intensity with speed, slope and loading were positively correlated with muscle energy use, the quantitative relationships between these variables differed greatly under different conditions. The relative changes in EMG intensity and energy use by the muscle probably varied because of changes in the mechanical function of the muscle that altered the ratio of muscle energy use to active muscle volume. Considering the overall function of the cycle of active lengthening and shortening of the fascicles of the ILPO, we conclude that the function of active lengthening is unlikely to be energy conservation and may instead be related to promoting stability at the knee. The work required to lengthen the ILPO during stance is provided by co-contracting knee flexors. We suggest that this potentially energetically expensive co-contraction serves to stabilize the knee in early stance by increasing the mechanical impedance of the joint.

Serotonin modulates muscle function in the medicinal leech Hirudo verbana.

The body wall muscles of sanguivorous leeches power mechanically diverse behaviours: suction feeding, crawling and swimming. These require longitudinal muscle to exert force over an extremely large length range, from 145 to 46 per cent of the mean segmental swimming length. Previous data, however, suggest that leech body wall muscle has limited capacity for force production when elongated. Serotonin (5-HT) alters the passive properties of the body wall and stimulates feeding. We hypothesized that 5-HT may also have a role in allowing force production in elongated muscle by changing the shape of the length-tension relationship (LTR). LTRs were measured from longitudinal muscle strips in vitro in physiological saline with and without the presence of 10 µM 5-HT. The LTR was much broader than previously measured for leech muscle. Rather than shifting the LTR, 5-HT reduced passive muscle tonus and increased active stress at all lengths. In addition to modulating leech behaviour and passive mechanical properties, 5-HT probably enhances muscle force and work production during locomotion and feeding.

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 mechanical function of linked muscles in the guinea fowl hind limb.

Although mechanical linkages between the proximal and distal limb are present in a range of species, their functional significance is unknown. We have investigated the mechanical function of the flexor cruris lateralis pars pelvica (FCLP), flexor cruris lateralis pars accessoria (FCLA) and gastrocnemius intermedia (GI), a system of linked muscles spanning proximal and distal limb segments in the guinea fowl (Numida meleagris) hind limb. The FCLP, which is in the anatomical position of a hamstring muscle, is the primary component of the linkage. It is connected to the distal femur via the FCLA, the tarsometatarsus via the tendon of insertion of the GI and the common Achilles tendon, and the tibiotarsus via a distal tendon of insertion. The FCLP may, therefore, potentially exert moments at the hip, knee and ankle joints depending on the joint angles and the relative states of activation in the three muscles. Evidence presented here suggests that the GI and FCLA act as actively controlled links that alter distal action of the FCLP. The FCLP and GI are coactive in the late swing and early stance phases of the stride, forming a triarticular complex, and likely act together to resist and control ankle flexion immediately after foot-down in addition to providing hip extension and knee flexion moments. The FCLP and FCLA are coactive from mid-through to late stance, acting together as a uniarticular hip extensor. Available evidence suggests that this role of the FCLP and FCLA is of increased importance in inclined running and accelerations. This linkage between a proximal muscle and alternate distal connections allows for functional flexibility, both in terms of the site at which the muscle exerts force and the nature of the muscle's mechanical function. The interactions generated between the proximal and distal limb by linkages of this type suggest that less emphasis should be placed on the distinct functional roles of specific anatomical classes of muscle within proximal and distal limb segments.

The seed dispersal catapult of Cardamine parviflora (Brassicaceae) is efficient but unreliable.

PREMISE OF THE STUDY: Seed dispersal performance is an essential component of plant fitness. Despite their significance in shaping performance, the mechanical processes that drive dispersal are poorly understood. We have quantified seed dispersal mechanics in Cardamine parviflora (Brassicaceae), a ballistic disperser that launches seeds with specialized catapult-like structures. To determine which aspects of catapult function dictate interspecific dispersal differences, we compared this disperser with other ballistic dispersers. Comparison with brassicas that lack ballistic dispersal may also provide insight into the evolution of this mechanism. • METHODS: Catapult performance was quantified using high-speed video analysis of dehiscence, ballistic modeling of seed trajectories, and measuring the mechanical energy storage capacity of the spring-like siliqua valve tissue that launched the seeds. • KEY RESULTS: The siliquae valves coiled rapidly outward, launching the seeds in 4.7 ± 1.3 ms (mean ± SD, N = 11). Coiling was likely driven by the bilayered valve structure. The catapult was 21.3 ± 10.3% efficient (mean ± SD, N = 11) at transferring stored elastic energy to the seeds as kinetic energy. The majority of seeds (71.4%) were not launched effectively. • CONCLUSIONS: The efficiency of the C. parviflora catapult was high in comparison to that of a ballistic diplochore, a dispersal mode associated with poor ballistic performance, although the unreliability of the launch mechanism limited dispersal distance. Effective launching requires temporary seed-valve adhesion. The adhesion mechanism may be the source of the unreliability. Valve curvature is likely driven by the bilayered valve structure, a feature absent in nonballistic brassicas.

The physiology and mechanics of undulatory swimming: a student laboratory exercise using medicinal leeches.

The medicinal leech is a useful animal model for investigating undulatory swimming in the classroom. Unlike many swimming organisms, its swimming performance can be quantified without specialized equipment. A large blood meal alters swimming behavior in a way that can be used to generate a discussion of the hydrodynamics of swimming, muscle mechanics, hydrostatic skeletons, and the physiological features that allow leeches to deal with the volume increase and osmotic load imposed by the meal. Analyses can be carried out at a range of levels tailored to suit a particular class.