Slow and sustainable intermittent swimming has recently been described in several Centrarchid fishes, such as bluegill and largemouth bass. This swimming behavior involves short periods of body‐caudal fin undulation alternating with variable periods of coasting. This aerobic muscle powered swimming appears to reduce energetic costs for slow, sustainable swimming, with fish employing a “fixed‐gear” or constant tailbeat frequency and modulating swimming speed by altering the length of the coasting period. We asked if this swimming behavior was found in other fish species by examining volitional swimming by brook trout in a static swimming tank. Further, we employed muscle mechanics experiments to explore how intermittent swimming affects muscle power output in comparison to steady swimming behavior. Brook trout regularly employ an intermittent swimming form when allowed to swim volitionally, and consistently showed a tailbeat frequency of ~2 Hz. Coasting duration had a significant, inverse relationship to swimming speed. Across a range of slow, sustainable swimming speeds, tailbeat frequency increased modestly with speed. The duration of periods of coasting decreased significantly with increasing speed. Workloop experiments suggest that intermittent swimming reduces fatigue, allowing fish to maintain high power output for longer compared to continuous activity. This study expands the list of species that employ intermittent swimming, suggesting this behavior is a general feature of fishes.
Intermittent propulsion in largemouth bass, Micropterus salmoides , increases power production at low swimming speeds
Locomotion dominates animal energy budgets, and selection should favour behaviours that minimize transportation costs. Recent fieldwork has altered our understanding of the preferred modes of locomotion in fishes. For instance, bluegill employ a sustainable intermittent swimming form with 2–3 tail beats alternating with short glides. Volitional swimming studies in the laboratory with bluegill suggest that the propulsive phase reflects a fixed-gear constraint on body–caudal-fin activity. Largemouth bass ( Micropterus salmoides ) also reportedly display intermittent swimming in the field. We examined swimming by bass in a static tank to quantify the parameters of volitional locomotion, including tailbeat frequency and glide duration, across a range of swimming speeds. We found that tailbeat frequency was not related to speed at low swimming speeds. Instead, speed was a function of glide duration between propulsive events, with glide duration decreasing as speed increased. The propulsive Strouhal number remained within the range that maximizes propulsive efficiency. We used muscle mechanics experiments to simulate power production by muscle operating under intermittent versus steady conditions. Workloop data suggest that intermittent activity allows fish to swim efficiently and avoid the drag-induced greater energetic cost of continuous swimming. The results offer support for a new perspective on fish locomotion: intermittent swimming is crucial to aerobic swimming energetics.
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- Award ID(s):
- 1754567
- PAR ID:
- 10443743
- Date Published:
- Journal Name:
- Biology Letters
- Volume:
- 18
- Issue:
- 5
- ISSN:
- 1744-957X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
Locomotion that is driven by muscle activity dominates the daily energetic expenditure in most animals. In fish, routine propulsion when swimming at low, steady speeds and at various gaits is powered primarily by red, oxidative muscle. In Bluegill Sunfish (Lepomis macrochirus), swimming speed is thought to reflect the most energetically efficient gait type. Since field observations of Bluegill suggest that intermittent swimming is the preferred gait, we hypothesized that intermittent locomotion would be more energetically efficient than steady swimming. To test this hypothesis, we used electromyography to analyze muscle activation intensity of Bluegill swimming steadily in a flume and volitionally intermittently in a pool. In the flume, muscle activation intensity and tailbeat frequency increased as a function of speed. However, when swimming volitionally in the pool, muscle activation intensity varied relative to average velocity and tailbeat frequency was lower than in the flume at the same velocities. Although we expected muscle activation intensity to be higher when steady swimming at a given speed, ~48% of fish (n=11) had higher muscle activation intensities when swimming volitionally when compared at the same speed in the flume. Also, there was a positive relationship between speed and glide duration, but there was no relationship between speed and muscle activation intensity when swimming intermittently. Instead, intermittent swimming may lower fatigue and enhance maneuverability, rather than increase energetic efficiency.more » « less
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Locomotion is an important behavior in the life history of animals and is characterized by discrete gaits, which may be adopted for optimal energetic efficiency, fatigue resistance, or maneuverability. We evaluated the kinematics and electromyography of Bluegill Sunfish (Lepomis macrochirus) swimming at different gaits to evaluate which factors might influence gait choice. When placed in the flume, Bluegill adopted a steady swimming gait until speeds reached 2.0 BL/s. When swimming volitionally, either in a laboratory pool or the field, Bluegill adopted an intermittent swimming gait (burst phase followed by a glide phase) and swam at average speeds of 1.0-1.3 BL/s. No statistical relationship was found between the kinematics of the burst and glide phases in either the lab or the field, so the phases were considered uncoupled. Furthermore, since the kinematics (tailbeat frequency, glide-duty factor) of lab and field volitional swimming were statistically identical, the EMGs of volition swimming in the lab likely reflect field effort. When relativized to volitional swimming speeds, the EMG intensities for both gaits were statistically identical. These results suggest that intermittent swimming may not reflect a strategy for energetic efficiency. Instead, the decoupling between the burst and glide phase may improve maneuverability, since 75% of 3D tracked intermittent swimming bouts (n=129) in the field involved a directional change. Although previous research suggests that intermittent swimming may also provide fatigue resistance, we hypothesize that intermittent swimming evolved in Bluegill as an adaptive gait for navigating their densely vegetated habitat.more » « less
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Locomotion is vital to the survival and fitness of animals and dominates daily energy budgets. The main energy consuming process of locomotion is the muscle activity needed to maintain stability or generate propulsive forces. In fish, the speed of swimming is thought to depend on the gait type, which may reflect an energetically efficient locomotory behavior. Bluegill Sunfish (Lepomis macrochirus) exhibit either steady or intermittent (burst-coast) gaits when swimming in the field, but whether these gaits differ in their energetic efficiency is unknown. We analyzed the electromyography (EMG) of oxidative muscle in Bluegill swimming at low velocities to determine if steady swimming is more or less energetically efficient than intermittent swimming. EMG data were acquired using bipolar fine wire electrodes implanted into oxidative musculature at 2/3 tail length. Steady swimming EMGs were recorded in a flume (fish treadmill) at incrementally increasing speeds relative to body length, until nonoxidative muscle was recruited. As speed increased, EMG intensity increased, which corresponds to increased muscle recruitment. Fish reached maximum EMG intensity (100% oxidative muscle capacity) between 1.75 - 2.25 BL/s. Intermittent swimming EMGs were recorded while the fish swam volitionally in a pool. The burst phase consisted of 2-3 tailbeats, followed by a coast phase duration of 1 second or less. Based on preliminary results, fish in the pool swam at an average of 62.1% (n = 10) of their maximum oxidative capacity. When intermittently swimming, muscle activity was 37.9% more efficient than steady swimming at similar speeds. This demonstrates that when swimming volitionally Bluegill choose the most energetically effective gait. However, further analysis is needed to determine how individual variation affects swimming performance. Continued comparison of these methods of locomotion will broaden the understanding of energy decisions that fish make. These results suggest that intermittent swimming is the more energetically efficient form of aquatic locomotion. This work is supported by NSF grant award number 2135851.more » « less
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Fish maintain high swimming efficiencies over a wide range of speeds. A key to this achievement is their flexibility, yet even flexible robotic fish trail real fish in terms of performance. Here, we explore how fish leverage tunable flexibility by using their muscles to modulate the stiffness of their tails to achieve efficient swimming. We derived a model that explains how and why tuning stiffness affects performance. We show that to maximize efficiency, muscle tension should scale with swimming speed squared, offering a simple tuning strategy for fish-like robots. Tuning stiffness can double swimming efficiency at tuna-like frequencies and speeds (0 to 6 hertz; 0 to 2 body lengths per second). Energy savings increase with frequency, suggesting that high-frequency fish-like robots have the most to gain from tuning stiffness.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rsbl.2021.0658
