Skating by: low energetic costs of swimming in a batoid fish (original) (raw)
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Swimming performance is considered a key trait determining the ability of fish to survive. Hydrodynamic theory predicts that the energetic costs required for fishes to swim should vary with speed according to a U-shaped curve, with an expected energetic minimum at intermediate cruising speeds and increasing expenditure at low and high speeds. However, to date no complete datasets have shown an energetic minimum for swimming fish at intermediate speeds rather than low speeds. To address this knowledge gap, we used a negatively buoyant fish, the clearnose skate Raja eglanteria, and took two approaches: a classic critical swimming speed protocol and a single-speed exercise and recovery procedure. We found an anaerobic component at each velocity tested. The two approaches showed U-shaped, though significantly different, speed-metabolic relationships. These results suggest that (i) postural costs, especially at low speeds, may result in J-or U-shaped metabolism-speed curves; (ii) anaerobic metabolism is involved at all swimming speeds in the clearnose skate; and (iii) critical swimming protocols might misrepresent the true costs of locomotion across speeds, at least in negatively buoyant fish. aerobic performance | critical swimming speed | elasmobranch | EPOC | swimming metabolic rate S wimming ability has no doubt contributed to the astonishing diversity and evolutionary success of fishes (1, 2), and efficiency of locomotion is a key measure of performance that influences reproduction, competition, foraging, and survival outcomes (3, 4). In fact, daily and seasonal movements allow fish to forage, reproduce, and find refuge from predators or abiotic stressors (5, 6). It comes as no surprise, therefore, that fish lo-comotion has been a productive research area for both evolutionary biologists and physiologists (4, 7-10). All fishes are capable of varying locomotor speed to some degree, and both the hydrodynamic mechanisms and energetic consequences of the species-specific use of propulsors (i.e., fins) have been investigated theoretically and experimentally (11-13). Vertebrate locomotor theory predicts that the total energetic requirements (or metabolic rate, _ MO 2) for steady swimming should vary with velocity, with the greatest expenditure at the lowest and highest sustainable speeds and minimum expenditure at intermediate speeds (4). This hypothesis is based on the assumption that during swimming, fish face perturbing forces and must stabilize their body posture to maintain direction (4, 14). As speed decreases, controlling stability becomes more difficult (15), and thus instability costs increase below optimal cruising speeds (14). For negatively buoyant fish, such a process involves a significant energy loss, because they also need to counteract gravity by accelerating water downward to create hydrodynamic lift (7, 16). At higher swimming speeds, energy expenditure increases significantly, as body drag is a function of velocity squared (17). Consequently, there is a range of intermediate velocities at which fish are expected to swim relatively economically , and these are typically identified as cruising speeds (4). Taken together, these different hydrodynamic forces acting on fishes during locomotion should result in the hypothetical nonlinear relationship (as either a J-shaped or a U-shaped curve) between speed and _ MO 2 (Fig. 1A). However, to date, we lack experimental measurements of energetic cost over a range of speeds sufficiently broad and in sufficient detail to support this theoretical model. This is especially surprising because the energetic cost of swimming has been assessed in many species of fish across a range of speeds. Instead, virtually all studies show that _ MO 2 increases with speed, with a minimum energetic cost at the lowest velocity tested (Fig. 1A). Testing swimming fish at very low speeds can be challenging, and thus fish energetic analyses have not generally provided data at low enough speeds to demonstrate increased energetic costs. One exception to this is recent work with a batoid fish, the little skate Leucoraja erinacea, which has demonstrated a unique relationship between speed and _ MO 2 (18). In that study, skates exhibited a decreasing _ MO 2 with increasing speed up to a relatively low optimal cruising velocity, but were unable to swim steadily beyond the optimal speed. In that case, locomotor performance was limited to the descending portion of a single metabolism speed relationship (18). Batoid fishes lack an expansive caudal fin and are unable to transition from paired fin to body and caudal fin locomotion, i.e., cannot switch gait, as is the case with many other aquatic vertebrates (16-18). Instead, they must rely on modified pectoral fins fused to the head, forming a disk to propel themselves at varying speeds (17, 19). Even though this extreme body plan is well adapted for a benthic life history, batoids are also able to swim up in the water column, and some species can even undertake large-scale migrations (20). Another notable conclusion of the previous study was the detection of a significant postexercise oxygen debt-a proxy for Significance Hydrodynamic theory predicts that the energetic costs required for fishes to swim should vary with speed according to a U-shaped curve, with an expected energetic minimum at intermediate cruising speeds. Empirical studies to date do not support this view. Here we report a complete dataset on a swimming batoid fish that shows a clear energetic minimum at intermediate swimming speeds. We also demonstrate that this species uses a combination of aerobic and anaerobic metabolism to fuel steady swimming at each speed, including the slowest speeds tested. This contradicts the widespread assumption that fish use only aerobic metabolism at low speeds. Kinematic data support this nonlinear relationship by also showing a U-shaped pattern to body angle during steady swimming.
Gait transition and oxygen consumption in swimming striped surfperch Embiotoca lateralis Agassiz
Journal of Fish Biology, 2006
A flow-through respirometer and swim tunnel was used to estimate the gait transition speed (U p-c ) of striped surfperch Embiotoca lateralis, a labriform swimmer, and to investigate metabolic costs associated with gait transition. The U p-c was defined as the lowest speed at which fish decrease the use of pectoral fins significantly. While the tail was first recruited for manoeuvring at relatively low swimming speeds, the use of the tail at these low speeds [as low as 0Á75 body (fork) lengths s À1 , L F s À1 ) was rare (<10% of the total time). Tail movements at these low speeds appeared to be associated with occasional slow manoeuvres rather than providing power. As speed was increased beyond U p-c , pectoral fin (PF) frequencies kept increasing when the tail was not used, while they did not when PF locomotion was aided by the tail. At these high speeds, the tail was employed for 40-50% of the time, either in addition to pectoral fins or during burstand-coast mode. Oxygen consumption increased exponentially with swimming speeds up to gait transition, and then levelled off. Similarly, cost of transport (C T ) decreased with increasing speed, and then levelled off near U p-c . When speeds !U p-c are considered, C T is higher than the theoretical curve extrapolated for PF swimming, suggesting that PF swimming appears to be higher energetically less costly than undulatory swimming using the tail.
Swimming efficiency and the influence of morphology on swimming costs in fishes
Journal of Comparative Physiology B, 2006
Swimming performance is considered a main character determining survival in many aquatic animals. Body morphology highly influences the energetic costs and efficiency of swimming and sets general limits on a species capacity to use habitats and foods. For two cyprinid fishes with different morphological characteristics, carp (Cyprinus carpio L.) and roach (Rutilus rutilus (L.)), optimum swimming speeds (U mc) as well as total and net costs of transport (COT, NCOT) were determined to evaluate differences in their swimming efficiency. Costs of transport and optimum speeds proved to be allometric functions of fish mass. NCOT was higher but U mc was lower in carp, indicating a lower swimming efficiency compared to roach. The differences in swimming costs are attributed to the different ecological demands of the species and could partly be explained by their morphological characteristics. Body fineness ratios were used to quantify the influence of body shape on activity costs. This factor proved to be significantly different between the species, indicating a better streamlining in roach with values closer to the optimum body form for efficient swimming. Net swimming costs were directly related to fish morphology. Keywords Energetic costs AE Fish AE Morphology AE Optimum speed AE Swimming efficiency Abbreviations AMR: Active metabolic rate (W) AE COT: Total cost of transport when swimming at U mc AE COT•W: COT times body weight (N) AE M: Fish mass (kg) AE NCOT: Net cost of transport AE SMR: Standard metabolic rate (W) AE U: Swimming speed (m s À1) AE U mc : Swimming speed associated with minimum costs (m s À1)
Modelling energetic costs of fish swimming
2005
The oxygen consumption rates of two cyprinid fishes, carp (Cyprinus carpio L.) and roach (Rutilus rutilus (L.)), were analysed for a wide range of body mass and swimming speed by computerized intermittent-flow respirometry. Bioenergetic models were derived, based on fish mass (M) and swimming speed (U), to predict the minimal speed and mass-specific active metabolic rate (AMR) in these fishes (AMR 5 aM b U c). Mass and speed together explained more than 90% of the variance in total swimming costs in both cases. The derived models show that carp consume far more oxygen at a specific speed and body mass, thus being less efficient in energy use during swimming than roach. It was further found that in carp (AMR 5 0.02M 0.8 U 0.95) the metabolic increment during swimming is more strongly effected by speed, whereas in roach (AMR 5 0.02M 0.93 U 0.6) it is more strongly effected by body mass. The different swimming traits of carp and roach are suitable for their respective lifestyles and ecological demands.
Journal of Experimental Biology
To determine the energetic costs of rigid-body, median or paired-fin (MPF) swimming versus undulatory, body-caudal fin (BCF) swimming, we measured oxygen consumption as a function of swimming speed in two MPF swimming specialists, Schlegel's parrotfish and Picasso triggerfish. The parrotfish swam exclusively with the pectoral fins at prolonged swimming speeds up to 3.2 total lengths per second (L s(-1); 30 min critical swimming speed, U(crit)). At higher speeds, gait transferred to a burst-and-coast BCF swimming mode that resulted in rapid fatigue. The triggerfish swam using undulations of the soft dorsal and anal fins up to 1.5 L s(-1), beyond which BCF undulations were recruited intermittently. BCF swimming was used continuously above 3.5 L s(-1), and was accompanied by synchronous undulations of the dorsal and anal fins. The triggerfish were capable of high, prolonged swimming speeds of up to 4.1 L s(-1) (30 min U(crit)). In both species, the rates of increase in oxygen consu...
Energetic Extremes in Aquatic Locomotion by Coral Reef Fishes
PLoS ONE, 2013
Underwater locomotion is challenging due to the high friction and resistance imposed on a body moving through water and energy lost in the wake during undulatory propulsion. While aquatic organisms have evolved streamlined shapes to overcome such resistance, underwater locomotion has long been considered a costly exercise. Recent evidence for a range of swimming vertebrates, however, has suggested that flapping paired appendages around a rigid body may be an extremely efficient means of aquatic locomotion. Using intermittent flow-through respirometry, we found exceptional energetic performance in the Bluelined wrasse Stethojulis bandanensis, which maintains tuna-like optimum cruising speeds (up to 1 metre s 21 ) while using 40% less energy than expected for their body size. Displaying an exceptional aerobic scope (22-fold above resting), streamlined rigid-body posture, and wing-like fins that generate lift-based thrust, S. bandanensis literally flies underwater to efficiently maintain high optimum swimming speeds. Extreme energetic performance may be key to the colonization of highly variable environments, such as the wave-swept habitats where S. bandanensis and other wing-finned species tend to occur. Challenging preconceived notions of how best to power aquatic locomotion, biomimicry of such lift-based fin movements could yield dramatic reductions in the power needed to propel underwater vehicles at high speed.
Unsteady flow affects swimming energetics in a labriform fish (Cymatogaster aggregata)
Journal of Experimental Biology, 2014
Unsteady water flows are common in nature, yet the swimming performance of fishes is typically evaluated at constant, steady speeds in the laboratory. We examined how cyclic changes in water flow velocity affect the swimming performance and energetics of a labriform swimmer, the shiner surfperch, Cymatogaster aggregata, during station holding. Using intermittent-flow respirometry, we measured critical swimming speed (U crit ), oxygen consumption rates (Ṁ O2 ) and pectoral fin use in steady flow versus unsteady flows with either low-[0.5 body lengths (BL) s −1 ] or high-amplitude (1.0 BL s −1 ) velocity fluctuations, with a 5 s period. Individuals in low-amplitude unsteady flow performed as well as fish in steady flow. However, swimming costs in high-amplitude unsteady flow were on average 25.3% higher than in steady flow and 14.2% higher than estimated values obtained from simulations based on the non-linear relationship between swimming speed and oxygen consumption rate in steady flow. Time-averaged pectoral fin use (fin-beat frequency measured over 300 s) was similar among treatments. However, measures of instantaneous fin use (fin-beat period) and body movement in highamplitude unsteady flow indicate that individuals with greater variation in the duration of their fin beats were better at holding station and consumed less oxygen than fish with low variation in fin-beat period. These results suggest that the costs of swimming in unsteady flows are context dependent in labriform swimmers, and may be influenced by individual differences in the ability of fishes to adjust their fin beats to the flow environment.