Biomedical subjects

R V Baudinette

Publications and source records attributed to R V Baudinette.

At least 19 recordsLinked to original sources

PubMed2006

Routine metabolic rate of southern bluefin tuna (Thunnus maccoyii).

Routine metabolic rate (RMR) was measured in fasting southern bluefin tuna, Thunnus maccoyii, the largest tuna species studied so far (body mass=19.6 kg (+/-1.9 SE)). Mean mass-specific RMR was 460 mg kg(-1) h(-1) (+/-34.9) at a mean water temperature of 19 degrees C. When evaluated southern bluefin tuna standard metabolic rate (SMR) is added to published values of other tuna species, there is a strong allometeric relationship with body mass (423 M(0.86), R(2)=0.97). This demonstrates that tuna interspecific SMR scale with respect to body mass similar to that of other active teleosts, but is approximately 4-fold higher. However, RMR (not SMR) is most appropriate in ram-ventilating species that are physiologically unable to achieve complete rest. Respiration was measured in a large (250,000 l) flexible polypropylene respirometer (mesocosm respirometer) that was deployed within a marine-farm sea cage for 29 days. Fasted fish were maintained within the respirometer up to 42 h while dissolved oxygen dropped by 0.056 (+/-0.004) mg l(-1) h(-1). Fish showed no obvious signs of stress. They swam at 1.1 (+/-0.1) fork lengths per second and several fed within the respirometer immediately after measurements.

Animals↗

PubMed2006

Differential design for hopping in two species of wallabies.

Hindlimb musculoskeletal anatomy and steady speed over ground hopping mechanics were compared in two species of macropod marsupials, tammar wallabies and yellow-footed rock wallabies (YFRW). These two species are relatively closely related and are of similar size and general body plan, yet they inhabit different environments with presumably different musculoskeletal demands. Tammar wallabies live in relatively flat, open habitat whereas yellow-footed rock wallabies inhabit steep cliff faces. The goal of this study was to explore musculoskeletal differences between tammar wallabies and yellow-footed rock wallabies and determine how these differences influence each species' hopping mechanics. We found the cross-sectional area of the combined ankle extensor tendons of yellow-footed rock wallabies was 13% greater than that of tammar wallabies. Both species experienced similar ankle joint moments during steady-speed hopping, however due to a lower mechanical advantage at this joint, tammar wallabies produced 26% more muscle force. Thus, during moderate speed hopping, yellow-footed rock wallabies operated with 38% higher tendon safety factors, while tammar wallabies were able to store 73% more elastic strain energy (2.18 J per leg vs. 1.26 J in YFRW). This likely reflects the differing demands of the environments inhabited by these two species, where selection for non-steady locomotor performance in rocky terrain likely requires trade-offs in locomotor economy.

Animals↗

PubMed2005

An allometric study of lung morphology during development in the Australian pelican, Pelicanus conspicillatus, from embryo to adult.

Pelicans produce altricial chicks that develop into some of the largest birds capable of sustained flight. We traced pulmonary morphological development in the Australian pelican, Pelicanus conspicillatus, from third trimester embryos to adults. We described growth and development with allometric relationships between lung components and body mass or lung volume, according to the equation y = ax(b). Pelican lung volume increased faster than body mass (b = 1.07). Relative to lung volume, the airways and vascular spaces increased allometrically (b > 1) in embryos, but isometrically (b approximately 1) after hatching. Parabronchial mantle volume decreased (b < 1) prior to hatching and increased isometrically thereafter. Surface area of air capillaries, blood capillaries and the blood-gas barrier increased relative to lung volume (b > 0.67) before and after hatching. Barrier thickness decreased before hatching, remained constant in juveniles and decreased by adulthood. The anatomical diffusing capacity significantly increased before hatching (b = 4.44) and after hatching (b = 1.26). Although altricial pelicans developed pulmonary complexity later than precocial turkeys, the volume-specific characteristics were similar. However, lungs of volant adult pelicans became significantly larger, with a greater capacity for gas exchange, than lungs of terrestrial turkeys. Exchange characteristics of growing pelican lungs were inferior to those of adult birds of 26 other species, but converged with them at maturity.

Animals↗

PubMed2005

Joint work and power associated with acceleration and deceleration in tammar wallabies (Macropus eugenii).

Measurements of joint work and power were determined using inverse dynamics analysis based on ground reaction force and high-speed video recordings of tammar wallabies as they decelerated and accelerated while hopping over a force platform on level ground. Measurements were obtained over a range of accelerations ranging from -6 m s(-2) to 8 m s(-2). The goal of our study was to determine which joints are used to modulate mechanical power when tammar wallabies change speed. From these measurements, we also sought to determine which hind limb muscle groups are the most important for producing changes in mechanical work. Because our previous in vivo analyses of wallaby distal muscle function indicated that these muscle-tendon units favor elastic energy savings and perform little work during steady level and incline hopping, we hypothesized that proximal muscle groups operating at the hip and knee joint are most important for the modulation of mechanical work and power. Of the four hind limb joints examined, the ankle joint had the greatest influence on the total limb work, accounting for 89% of the variation observed with changing speed. The hip and metatarsophalageal (MP) joints also contributed to modulating whole limb work, but to a lesser degree than the ankle, accounting for 28% (energy production) and -24% (energy absorption) of the change in whole limb work versus acceleration, respectively. In contrast, the work produced at the knee joint was independent of acceleration. Based on the results of our previous in vivo studies and given that the magnitude of power produced at the ankle exceeds that which these muscles alone could produce, we conclude that the majority of power produced at the ankle joint is likely transferred from the hip and knee joints via proximal bi-articular muscles, operating in tandem with bi-articular ankle extensors, to power changes in hopping speed of tammar wallabies. Additionally, over the observed range of performance, peak joint moments at the ankle (and resulting tendon strains) did not increase significantly with acceleration, indicating that having thin tendons favoring elastic energy storage does not necessarily limit a tammar wallaby's ability to accelerate or decelerate.

Acceleration↗

PubMed2005

The mechanics of jumping versus steady hopping in yellow-footed rock wallabies.

The goal of our study was to explore the mechanical power requirements associated with jumping in yellow-footed rock wallabies and to determine how these requirements are achieved relative to steady-speed hopping mechanics. Whole body power output and limb mechanics were measured in yellow-footed rock wallabies during steady-speed hopping and moving jumps up to a landing ledge 1.0 m high (approximately 3 times the animals' hip height). High-speed video recordings and ground reaction force measurements from a runway-mounted force platform were used to calculate whole body power output and to construct a limb stiffness model to determine whole limb mechanics. The combined mass of the hind limb extensor muscles was used to estimate muscle mass-specific power output. Previous work suggested that a musculoskeletal design that favors elastic energy recovery, like that found in tammar wallabies and kangaroos, may impose constraints on mechanical power generation. Yet rock wallabies regularly make large jumps while maneuvering through their environment. As jumping often requires high power, we hypothesized that yellow-footed rock wallabies would be able to generate substantial amounts of mechanical power. This was confirmed, as we found net extensor muscle power outputs averaged 155 W kg(-1) during steady hopping and 495 W kg(-1) during jumping. The highest net power measured reached nearly 640 W kg(-1). As these values exceed the maximum power-producing capability of vertebrate skeletal muscle, we suggest that back, trunk and tail musculature likely play a substantial role in contributing power during jumping. Inclusion of this musculature yields a maximum power output estimate of 452 W kg(-1) muscle. Similar to human high-jumpers, rock wallabies use a moderate approach speed and relatively shallow leg angle of attack (45-55 degrees) during jumps. Additionally, initial leg stiffness increases nearly twofold from steady hopping to jumping, facilitating the transfer of horizontal kinetic energy into vertical kinetic energy. Time of contact is maintained during jumping by a substantial extension of the leg, which keeps the foot in contact with the ground.

Analysis of Variance↗

PubMed2004

Dynamics of leg muscle function in tammar wallabies (M. eugenii) during level versus incline hopping.

The goal of our study was to examine whether the in vivo force-length behavior, work and elastic energy savings of distal muscle-tendon units in the legs of tammar wallabies (Macropus eugenii) change during level versus incline hopping. To address this question, we obtained measurements of muscle activation (via electromyography), fascicle strain (via sonomicrometry) and muscle-tendon force (via tendon buckles) from the lateral gastrocnemius (LG) and plantaris (PL) muscles of tammar wallabies trained to hop on a level and an inclined (10 degrees, 17.4% grade) treadmill at two speeds (3.3 m s(-1) and 4.2 m s(-1)). Similar patterns of muscle activation, force and fascicle strain were observed under both level and incline conditions. This also corresponded to similar patterns of limb timing and movement (duty factor, limb contact time and hopping frequency). During both level and incline hopping, the LG and PL exhibited patterns of fascicle stretch and shortening that yielded low levels of net fascicle strain [LG: level, -1.0+/-4.6% (mean +/- S.E.M.) vs incline, 0.6+/-4.5%; PL: level, 0.1+/-1.0% vs incline, 0.4+/-1.6%] and muscle work (LG: level, -8.4+/-8.4 J kg(-1) muscle vs incline, -6.8+/-7.5 J kg(-1) muscle; PL: level, -2.0+/-0.6 J kg(-1) muscle vs incline, -1.4+/-0.7 J kg(-1) muscle). Consequently, neither muscle significantly altered its contractile dynamics to do more work during incline hopping. Whereas electromyographic (EMG) phase, duration and intensity did not differ for the LG, the PL exhibited shorter but more intense periods of activation, together with reduced EMG phase (P<0.01), during incline versus level hopping. Our results indicate that design for spring-like tendon energy savings and economical muscle force generation is key for these two distal muscle-tendon units of the tammar wallaby, and the need to accommodate changes in work associated with level versus incline locomotion is achieved by more proximal muscles of the limb.

Animals↗

PubMed2003

Oxygen transport capacity in the air-breathing fish, Megalops cyprinoides: compensations for strenuous exercise.

Tarpon have high resting or routine hematocrits (Hct) (37.6+/-3.4%) and hemoglobin concentrations (120.6+/-7.3 gl(-1)) that increased significantly following bouts of angling-induced exercise (51.9+/-3.7% and 142.8+/-13.5 gl(-1), respectively). Strenuous exercise was accompanied by an approximately tenfold increase in blood lactate and a muscle metabolite profile indicative of a high energy demand teleost. Routine blood values were quickly restored only when this facultative air-breathing fish was given access to atmospheric air. In vitro studies of oxygen transport capacity, a function of carrying capacity and viscosity, revealed that the optimal Hct range corresponded to that observed in fish under routine behaviour. During strenuous exercise however, further increase in viscosity was largely offset by a pronounced reduction in the shear-dependence of blood which conformed closely to an ideal Newtonian fluid. The mechanism for this behaviour of the erythrocytes appears to involve the activation of surface adrenergic receptors because pre-treatment with propranolol abolished the response. High levels of activity in tarpon living in hypoxic habitats are therefore supported by an elevated Hct with adrenergically mediated viscosity reduction, and air-breathing behaviour that enables rapid metabolic recovery.

Adaptation, Physiological↗

PubMed2001

The influence of locomotion on air-sac pressures in little penguins.

Air-sac pressures have been reported to oscillate with wing beat in flying magpies and with foot paddling in diving ducks. We sought to determine the impact on air-sac pressure of wing beats during swimming and of the step cycle during walking in little penguins (Eudyptula minor). Fluctuations averaged 0.16+/-0.06 kPa in the interclavicular air sacs, but only 0.06+/-0.04 kPa in the posterior thoracic sac, generating a small differential pressure between sacs of 0.06+/-0.02 kPa (means +/- S.E.M., N=4). These fluctuations occurred at approximately 3 Hz and corresponded to wing beats during swimming, indicated by electromyograms from the pectoralis and supracoracoideus muscles. There was no abdominal muscle activity associated with swimming or exhalation, but the abdominal muscles were active with the step cycle in walking penguins, and oscillations in posterior air-sac pressure (0.08+/-0.038 kPa) occurred with steps. We conclude that high-frequency oscillations in differential air-sac pressure enhance access to and utilization of the O(2) stores in the air sacs during a dive.

Abdominal Muscles↗

PubMed2001

Postnatal development and control of the pulmonary surfactant system in the tammar wallaby Macropus eugenii.

Marsupials are born at an early stage of development and are adapted for future development inside the pouch. Whether the pulmonary surfactant system is fully established at this altricial stage is unknown. This study correlates the presence of surfactant proteins (SP-A, SP-B and SP-D), using immunohistochemistry, with the ex-utero development of the lung in the tammar wallaby Macropus eugenii and also investigates the control of phosphatidylcholine (PC) secretion from developing alveolar type II cells. All three surfactant proteins were found at the site of gas exchange in the lungs of joeys at all ages, even at birth when the lungs are in the early stages of the terminal air-sac phase. Co-cultures of alveolar type II cells and fibroblasts were isolated from the lungs of 30- and 70-day-old joeys and incubated with the hormones dexamethasone (10 micromol l(-1)), prolactin (1 micromol l(-1)) or triiodothyronine (100 micromol l(-1)) or with the autonomic secretagogues isoproterenol (100 micromol l(-1)) or carbamylcholine chloride (100 micromol l(-1)). Basal secretion of PC was greater at 30 days of age than at 70 days. Co-cultures responded to all five agonists at 30 days of age, but only the autonomic secretagogues caused a significant increase in PC secretion at 70 days of age. This demonstrates that, as the cells mature, their activity and responsiveness are reduced. The presence of the surfactant proteins at the site of gas exchange at birth suggests that the system is fully functional. It appears that surfactant development is coupled with the terminal air-sac phase of lung development rather than with birth, the length of gestation or the onset of air-breathing.

Animals↗

PubMed2001

Energetics of terrestrial locomotion of the platypus Ornithorhynchus anatinus.

The platypus Ornithorhynchus anatinus Shaw displays specializations in its limb structure for swimming that could negatively affect its terrestrial locomotion. Platypuses walked on a treadmill at speeds of 0.19-1.08 m x s(-1). Video recordings were used for gait analysis, and the metabolic rate of terrestrial locomotion was studied by measuring oxygen consumption. Platypuses used walking gaits (duty factor >0.50) with a sprawled stance. To limit any potential interference from the extensive webbing on the forefeet, platypuses walk on their knuckles. Metabolic rate increased linearly over a 2.4-fold range with increasing walking speed in a manner similar to that of terrestrial mammals, but was low as a result of the relatively low standard metabolic rate of this monotreme. The dimensionless cost of transport decreased with increasing speed to a minimum of 0.79. Compared with the cost of transport for swimming, the metabolic cost for terrestrial locomotion was 2.1 times greater. This difference suggests that the platypus may pay a price in terrestrial locomotion by being more aquatically adapted than other semi-aquatic or terrestrial mammals.

Adaptation, Biological↗

PubMed2000

Energy, water balance and the roost microenvironment in three Australian cave-dwelling bats (Microchiroptera).

The ghost bat, Macroderma gigas, and the orange leaf-nosed bat, Rhinonycteris aurantius, occupy similar ranges across northern Australia and are often found in the same roost caves. Both species are considered rare and vulnerable to further population decline. A third small species, the large bent-wing bat, Miniopterus schreibersii, has a similar body mass to R. aurantius, but has one of the largest ranges of any Australian mammal. In the present study we examine the effect and sensitivity of the animals' roosting microclimates on their energy and water balance. M. schreibersii exhibits a basal metabolic rate about 40% greater than other bats of similar body mass, whereas the other two species are close to predicted levels. R. aurantius shows a decrease in body temperatures below thermoneutrality. R. aurantius has levels of pulmocutaneous water loss among the highest seen for a mammal, and calculations based on nasal tip temperatures suggest that most of this loss is across the skin. Calculated ambient temperatures at which metabolic water production is equal to pulmocutaneous water loss in dry air are -14.7 degrees C for R. aurantius, 9.8 degrees C for M. schreibersii and -0.3 degrees C for M. gigas. Exposing the animals to relative humidities of between 80% and 90% shifted these calculated temperatures to 5.6 degrees C, 25.2 degrees C, and 2.9 degrees C, respectively. For each species the ratio of metabolic water production to evaporative water loss has been treated as a joint function of humidity and ambient temperature. The resulting surface plot shows that under known roosting conditions in caves R. aurantius and M. schreibersii remain in positive water balance, whereas M. gigas does not.

Animals↗

PubMed1999

Morphometric analysis of postnatal lung development in a marsupial: transmission electron microscopy.

Postnatal lung development in the tammar wallaby was investigated using transmission electron microscopy and stereological morphometry. Volume densities of interstitial, epithelial and endothelial tissue and capillaries in the parenchymal septa were measured as were surface densities of the airspaces and gas exchange capillaries. Absolute changes in these parameters were related to body mass. Three phases of development were identified. During the ectothermic period, in the first 70 days after birth when the lung was in the terminal air sac phase, the most marked change was an increase in volume density of septal interstitium. The transitional period between ectothermy and endothermy, between 70 and 180 days after birth, corresponded to the alveolar phase and was characterised by accelerated increase in air space surface area. Maturation of the parenchymal septa and establishment of the mature capillary system occurred largely after 180 days when endothermy was established. The anatomical diffusion factor in the tammar wallaby adult is similar to that for eutherians.

Aging↗

PubMed1999

Oxygen transport and acid-base balance during exercise in the tammar wallaby.

Rates of oxygen consumption (V(O)2), body temperatures and pulmonary blood temperatures, blood gases and blood pH were measured for seven 4.9+/-0.8 (SE) kg tammar wallabies (Macropus eugenii) during rest and during treadmill hopping. For animals resting on the treadmill V(O)2 averaged 0.030+/-0.003 L min(-1). During hopping V(O)2 increased linearly with speed up to 2.5 m sec(-1). Above 2.5 m sec(-1) V(O)2 was independent of hopping speed and averaged 0.340+/-0.004 L min(-1). At rest, rectal temperatures and pulmonary blood temperatures averaged 36 degrees C. During treadmill hopping, rectal temperatures and pulmonary blood temperatures increased similarly, to 39 degrees C. The Pv(CO)2 increased and pHv decreased in proportion to the increased V(O)2. The Pa(CO)2 and pHa were not significantly changed from values for animals resting on the treadmill. Cardiac output (Vb) averaged 0.97+/-0.04 L min(-1) when the wallabies were at rest on the treadmill and increased linearly with treadmill speeds up to 2.5 m sec(-1). Above 2.5 m sec(-1) Vb was independent of hopping speed and averaged 2.9+/-0.04 L min(-1). When data for all speeds were combined, Vb increased linearly with V(O)2. Thus, in spite of their unique mode of locomotion wallabies have maintained relationships between pulmonary ventilation and V(O)2 and between Vb and V(O)2 that are similar to those reported for eutherian mammals.

Acid-Base Equilibrium↗

PubMed1999

Energetics of locomotion by the Australian water rat (Hydromys chrysogaster): a comparison of swimming and running in a semi-aquatic mammal.

Semi-aquatic mammals occupy a precarious evolutionary position, having to function in both aquatic and terrestrial environments without specializing in locomotor performance in either environment. To examine possible energetic constraints on semi-aquatic mammals, we compared rates of oxygen consumption for the Australian water rat (Hydromys chrysogaster) using different locomotor behaviors: swimming and running. Aquatic locomotion was investigated as animals swam in a water flume at several speeds, whereas water rats were run on a treadmill to measure metabolic effort during terrestrial locomotion. Water rats swam at the surface using alternate pelvic paddling and locomoted on the treadmill using gaits that included walk, trot and half-bound. Water rats were able to run at twice their maximum swimming velocity. Swimming metabolic rate increased with velocity in a pattern similar to the 'humps' and 'hollows' for wave drag experienced by bodies moving at the water surface. Metabolic rate increased linearly during running. Over equivalent velocities, the metabolic rate for running was 13-40 % greater than for swimming. The minimum cost of transport for swimming (2.61 J N-1 m-1) was equivalent to values for other semi-aquatic mammals. The lowest cost for running (2.08 J N-1 m-1) was 20 % lower than for swimming. When compared with specialists at the extremes of the terrestrial-aquatic continuum, the energetic costs of locomoting either in water or on land were high for the semi-aquatic Hydromys chrysogaster. However, the relative costs for H. chrysogaster were lower than when an aquatic specialist attempts to move on land or a terrestrial specialist attempts to swim.

Animals↗

PubMed1998

Morphometric estimate of gas-exchange tissue in the new-born tammar wallaby, Macropus eugenii.

The lung of the new-born marsupial is at the terminal air sac stage of development. The maturational status of the lung of new-born tammar wallaby was assessed using established morphometric techniques and the results were compared with data from a morphometric study of the lung of the rat. Volume densities of the parenchyma and non-parenchyma, conducting airways and blood vessels, the relative volumes of airspace and tissue, the thickness and the composition of the septa differed between the two species. In addition the volume of capillaries and the surface area of the effective gas-exchange tissue was greater in the new-born rat than in the new-born tammar pouch young. The lung of the new-born tammar appears to be at an earlier phase of the terminal air sac stage than that of the new-born rat. Lung development up to birth appears to be commensurate to the metabolic needs of the organism at birth.

Animals↗

PubMed1998

Morphometric analysis of postnatal lung development in the tammar wallaby: light microscopy.

Postnatal growth of the lung in the tammar wallaby, Macropus eugenii, was investigated using morphometric techniques with light microscopy. Lung volume, parenchymal and non-parenchymal volume densities were measured. Volume densities of parenchymal airspace and tissue and non-parenchymal conducting airways and large blood vessels were determined. Lung volume and all the other parameters that were measured showed a biphasic increase in relation to increase in body mass. All parameters, with the exception of airway volume, increased relatively slowly in relation to increase in mass in the first 70 days after birth, when the pouch young are ectothermic. Between 70 and 180 days, during the period of transition from ectothermy to endothermy, the parameters increased more rapidly, suggesting accelerated lung growth in preparation for the extra metabolic demands associated with the establishment of thermoregulatory control in the pouch young. Specific lung volume in the adult tammar is lower than that of eutherians of equivalent mass, however, the parenchymal volume is relatively high.

Aging↗

PubMed1998

In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies.

Moderate to large macropodids can increase their speed while hopping with little or no increase in energy expenditure. This has been interpreted by some workers as resulting from elastic energy savings in their hindlimb tendons. For this to occur, the muscle fibers must transmit force to their tendons with little or no length change. To test whether this is the case, we made in vivo measurements of muscle fiber length change and tendon force in the lateral gastrocnemius (LG) and plantaris (PL) muscles of tammar wallabies Macropus eugenii as they hopped at different speeds on a treadmill. Muscle fiber length changes were less than +/-0.5 mm in the plantaris and +/-2.2 mm in the lateral gastrocnemius, representing less than 2 % of total fiber length in the plantaris and less than 6 % in the lateral gastrocnemius, with respect to resting length. The length changes of the plantaris fibers suggest that this occurred by means of elastic extension of attached cross-bridges. Much of the length change in the lateral gastrocnemius fibers occurred at low force early in the stance phase, with generally isometric behavior at higher forces. Fiber length changes did not vary significantly with increased hopping speed in either muscle (P>0.05), despite a 1. 6-fold increase in muscle-tendon force between speeds of 2.5 and 6.0 m s-1. Length changes of the PL fibers were only 7+/-4 % and of the LG fibers 34+/-12 % (mean +/- S.D., N=170) of the stretch calculated for their tendons, resulting in little net work by either muscle (plantaris 0.01+/-0.03 J; gastrocnemius -0.04+/-0.30 J; mean +/- s.d. ). In contrast, elastic strain energy stored in the tendons increased with increasing speed and averaged 20-fold greater than the shortening work performed by the two muscles. These results show that an increasing amount of strain energy stored within the hindlimb tendons is usefully recovered at faster steady hopping speeds, without being dissipated by increased stretch of the muscles' fibers. This finding supports the view that tendon elastic saving of energy is an important mechanism by which this species is able to hop at faster speeds with little or no increase in metabolic energy expenditure.

Animals↗

PubMed1997

Energetics of swimming by the platypus Ornithorhynchus anatinus: metabolic effort associated with rowing.

The metabolism of swimming in the platypus Ornithorhynchus anatinus Shaw was studied by measurement of oxygen consumption in a recirculating water flume. Platypuses swam against a constant water current of 0.45-1.0 ms-1. Animals used a rowing stroke and alternated bouts of surface and submerged swimming. Metabolic rate remained constant over the range of swimming speeds tested. The cost of transport decreased with increasing velocity to a minimum of 0.51 at 1.0 ms-1. Metabolic rate and cost of transport for the platypus were lower than values for semiaquatic mammals that swim at the water surface using a paddling mode. However, relative to transport costs for fish, the platypus utilized energy at a similar level to highly derived aquatic mammals that use submerged swimming modes. The efficient aquatic locomotion of the platypus results from its specialised rowing mode in conjunction with enlarged and flexible forefeet for high thrust generation and a behavioral strategy that reduces drag and energy cost by submerged swimming.

Animals↗