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1. Electromyography of Bluegill Sunfish at Different Gaits: Steady Versus Intermittent Swimming

   Morris, C ; Coughlin DJ ; Pfister, AHL ; Reynolds, ZT ; Parker, J ; Ellerby, DJ ; Wood, BM ( January 2023 , Society of Integrative and Comparative Biology)

   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. 

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2. Intermittent Swimming Kinematics of Bluegill Sunfish (Lepomis macrochirus): Energetics versus Maneuverability

   Morris, C ; Coughlin, D ; Pfister, A ; Reynolds, Z ; Ellerby, D ; Wood, BM ( July 2023 , Society of Experimental Biology)

   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. 

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3. Field Observations Provide Biological Context for Interpreting Laboratory Data: The Locomotory Performance of Bluegill Sunfish (Lepomis macrochirus) as an Example

   Wood, BM ; Le, E ; Postupaka, D ; Svensson, K ; Uhm, C ; Pfister, A ; Ellerby, DJ ( February 2021 , Integrative and comparative biology)

   Field observations of animal behavior are essential for guiding the interpretations of laboratory data in order to ensure that they coincide with biological reality. Knowing how an organism behaves in its natural environment is a necessary first step in bridging the gap between experimental data collected in the controlled, artificial environment of the lab and explaining the adaptive significance of measured traits. Field observations also challenge assumptions about behavioral definitions and the apparent discreteness of behaviors measured in the lab. As part of an ongoing study in the locomotor performance of Bluegill Sunfish (Lepomis macrochirus), we illustrate the role field observations play in contextualizing and expanding interpretations of experimental data and standard assumptions about Bluegill behavior. A comprehensive field study of Lake Waban (Wellesley, MA) and its inhabitants was carried out using underwater cameras, fish finding sonar, and temperature/luminosity loggers to develop a behavioral profile of Bluegill relative to their habitat and interspecific interactions. Although previous experimental work assumed Bluegill adopted locomotor strategies that maximized energy efficiency, field observations demonstrate that swimming performance is driven by a myriad of abiotic and biotic factors. These factors include the need to navigate complex habitats, to flee from predators, to adopt context-specific foraging strategies, to ward off rivals, and to coordinate social interactions. These observations add an extra dimension for understanding why Bluegill adopt particular swimming behaviors and how those behaviors might be adaptively significant at each stage of their life history. 

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4. Bluegill Sunfish Kinematics: How Gaits Affect Swimming Efficiency

   Parker, J. ; Morris, C. ; Duncan, M. ; Wood, B.M. ( April 2022 , The University of Montana Western 15th Annual Research Symposium)

   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. 

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5. A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature

   https://doi.org/10.1038/s41598-021-88828-x  

   Jimenez, Yordano E. ; Marsh, Richard L. ; Brainerd, Elizabeth L. ( May 2021 , Scientific Reports)

   The axial musculature of fishes has historically been characterized as the powerhouse for explosive swimming behaviors. However, recent studies show that some fish also use their ‘swimming’ muscles to generate over 90% of the power for suction feeding. Can the axial musculature achieve high power output for these two mechanically distinct behaviors? Muscle power output is enhanced when all of the fibers within a muscle shorten at optimal velocity. Yet, axial locomotion produces a mediolateral gradient of muscle strain that should force some fibers to shorten too slowly and others too fast. This mechanical problem prompted research into the gearing of fish axial muscle and led to the discovery of helical fiber orientations that homogenize fiber velocities during swimming, but does such a strain gradient also exist and pose a problem for suction feeding? We measured muscle strain in bluegill sunfish,Lepomis macrochirus,and found that suction feeding produces a gradient of longitudinal strain that, unlike the mediolateral gradient for locomotion, occurs along the dorsoventral axis. A dorsoventral strain gradient within a muscle with fiber architecture shown to counteract a mediolateral gradient suggests that bluegill sunfish should not be able to generate high power outputs from the axial muscle during suction feeding—yet prior work shows that they do, up to 438 W kg⁻¹. Solving this biomechanical paradox may be critical to understanding how many fishes have co-opted ‘swimming’ muscles into a suction feeding powerhouse.

    

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