skip to main content


Title: Distributed propulsion enables fast and efficient swimming modes in physonect siphonophores
Many fishes employ distinct swimming modes for routine swimming and predator escape. These steady and escape swimming modes are characterized by dramatically differing body kinematics that lead to context-adaptive differences in swimming performance. Physonect siphonophores, such as Nanomia bijuga , are colonial cnidarians that produce multiple jets for propulsion using swimming subunits called nectophores. Physonect siphonophores employ distinct routine and steady escape behaviors but–in contrast to fishes–do so using a decentralized propulsion system that allows them to alter the timing of thrust production, producing thrust either synchronously (simultaneously) for escape swimming or asynchronously (in sequence) for routine swimming. The swimming performance of these two swimming modes has not been investigated in siphonophores. In this study, we compare the performances of asynchronous and synchronous swimming in N. bijuga over a range of colony lengths (i.e., numbers of nectophores) by combining experimentally derived swimming parameters with a mechanistic swimming model. We show that synchronous swimming produces higher mean swimming speeds and greater accelerations at the expense of higher costs of transport. High speeds and accelerations during synchronous swimming aid in escaping predators, whereas low energy consumption during asynchronous swimming may benefit N. bijuga during vertical migrations over hundreds of meters depth. Our results also suggest that when designing underwater vehicles with multiple propulsors, varying the timing of thrust production could provide distinct modes directed toward speed, efficiency, or acceleration.  more » « less
Award ID(s):
2100705 2100156 2100703 2114169 2114171
PAR ID:
10410366
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
119
Issue:
49
ISSN:
0027-8424
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Siphonophores are ubiquitous and often highly abundant members of pelagic ecosystems throughout the open ocean. They are unique among animal taxa in that many species use multiple jets for propulsion. Little is known about kinematics of the individual jets produced by nectophores or whether the jets are coordinated during normal swimming behavior. Using remotely operated vehicles and SCUBA, we video recorded the swimming behavior of several physonect species in their natural environment. The pulsed kinematics of the individual nectophores that comprise the siphonophore nectosome were quantified and, based on these kinematics, we examined the coordination of adjacent nectophores. We found that, for the 5 species considered, nectophores located along same side of the nectosomal axis (i.e.; axially aligned) were coordinated and their timing was offset such that they pulsed metachronally. However, this level of coordination did not extend across the nectosome and no coordination was evident between nectophores on opposite sides of the nectosomal axis. For most species, the metachronal contraction waves of nectophores were initiated by the apical nectophores and traveled dorsally. However, the metachronal wave of Apolemia rubriversa traveled in the opposite direction. Although nectophore groups on opposite sides of the nectosome were not coordinated, they pulsed with similar frequencies. This enabled siphonophores to maintain relatively linear trajectories during swimming. The timing and characteristics of the metachronal coordination of pulsed jets affects how the jet wakes interact and may provide important insight into how interacting jets may be optimized for efficient propulsion.

     
    more » « less
  2. ABSTRACT Many fishes use their tail as the main thrust producer during swimming. This fin's diversity in shape and size influences its physical interactions with water as well as its ecological functions. Two distinct tail morphologies are common in bony fishes: flat, truncate tails which are best suited for fast accelerations via drag forces, and forked tails that promote economical, fast cruising by generating lift-based thrust. This assumption is based primarily on studies of the lunate caudal fin of Scombrids (i.e. tuna, mackerel), which is comparatively stiff and exhibits an airfoil-type cross-section. However, this is not representative of the more commonly observed and taxonomically widespread flexible forked tail, yet similar assumptions about economical cruising are widely accepted. Here, we present the first comparative experimental study of forked versus truncate tail shape and compare the fluid mechanical properties and energetics of two common nearshore fish species. We examined the hypothesis that forked tails provide a hydrodynamic advantage over truncate tails at typical cruising speeds. Using experimentally derived pressure fields, we show that the forked tail produces thrust via acceleration reaction forces like the truncate tail during cruising but at increased energetic costs. This reduced efficiency corresponds to differences in the performance of the two tail geometries and body kinematics to maintain similar overall thrust outputs. Our results offer insights into the benefits and tradeoffs of two common fish tail morphologies and shed light on the functional morphology of fish swimming to guide the development of bio-inspired underwater technologies. 
    more » « less
  3. 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. 
    more » « less
  4. 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
  5. Eel-like fish can exhibit efficient swimming with comparatively low metabolic cost by utilizing sub-ambient pressure areas in the trough of body waves to generate thrust, effectively pulling themselves through the surrounding water. While this is understood at the fish’s preferred swimming speed, little is known about the mechanism over a full range of natural swimming speeds. We compared the swimming kinematics, hydrodynamics, and metabolic activity of juvenile coral catfish (Plotosus lineatus) across relative swimming speeds spanning two orders of magnitude from 0.2 to 2.0 body lengths (BL) per second. We used experimentally derived velocity fields to compute pressure fields and components of thrust along the body. At low speeds, thrust was primarily generated through positive pressure pushing forces. In contrast, increasing swimming speeds caused a shift in the recruitment of push and pull propulsive forces whereby sub-ambient pressure gradients contributed up to 87% of the total thrust produced during one tail-beat cycle past 0.5 BL s−1. This shift in thrust production corresponded to a sharp decline in the overall cost of transport and suggests that pull-dominated thrust in anguilliform swimmers is subject to a minimum threshold below which drag-based mechanisms are less effective. 
    more » « less