Energetics of locomotion by the Australian Water Rat (Hydromys Chrysogaster): A comparison of swimming and running in a semi-aquatic mammal

© The Company of BiologistsSemi-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.F.E. Fish and R.V. Baudinett

Modulation of proximal muscle function during level versus incline hopping in tammar wallabies (Macropus eugenii)

Copyright © 2007 The Company of Biologists LtdWe examined the functional role of two major proximal leg extensor muscles of tammar wallabies during level and inclined hopping (12°, 21.3% grade). Previous in vivo studies of hopping wallabies have revealed that, unlike certain avian bipeds, distal hindlimb muscles do not alter their force–length behavior to contribute positive work during incline hopping. This suggests that proximal muscles produce the increased mechanical work associated with moving up an incline. Based on relative size and architectural anatomy, we hypothesized that the biceps femoris (BF), primarily a hip extensor, and the vastus lateralis (VL), the main knee extensor, would exhibit changes in muscle strain and activation patterns consistent with increased work production during incline versus level hopping. Our results clearly support this hypothesis. The BF experienced similar activation patterns during level and incline hopping but net fascicle shortening increased (–0.5% for level hopping versus –4.2% for incline hopping) during stance when the muscle likely generated force. Unlike the BF, the VL experienced active net lengthening during stance, indicating that it absorbs energy during both level and incline hopping. However, during incline hopping, net lengthening was reduced (8.3% for level hopping versus 3.9% for incline hopping), suggesting that the amount of energy absorbed by the VL was reduced. Consequently, the changes in contractile behavior of these two muscles are consistent with a net production of work by the whole limb. A subsidiary aim of our study was to explore possible regional variation within the VL. Although there was slightly higher fascicle strain in the proximal VL compared with the distal VL, regional differences in strain were not significant, suggesting that the overall pattern of in vivo strain is fairly uniform throughout the muscle. Estimates of muscle work based on inverse dynamics calculations support the conclusion that both the BF and VL contribute to the additional work required for incline hopping. However, on a muscle mass-specific basis, these two muscles appear to contribute less than their share. This indicates that other hindlimb muscles, or possibly trunk and back muscles, must contribute substantial work during incline hopping.C. P. McGowan, R. V. Baudinette and A. A. Biewene

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

© The Company of BiologistsModerate 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.Andrew A. Biewener, David D. Konieczynski and Russell V. Baudinett

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

Copyright © 2005 The Company of BiologistsMeasurements 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.C.P. McGowan, R.V. Baudinette and A.A. Biewene

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

© The Company of BiologistsMarsupials 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 µmol l–1), prolactin (1 µmol l–1) or triiodothyronine (100 µmol l–1) or with the autonomic secretagogues isoproterenol (100 µmol l–1) or carbamylcholine chloride (100 µmol 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.Natalie J. Miller, Sandra Orgeig, Christopher B. Daniels and Russell V. Baudinett

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

© The Company of BiologistsAir-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 O2 stores in the air sacs during a dive.D.F. Boggs, R.V. Baudinette, P.B. Frappell and P.J. Butle

Energetics of terrestrial locomotion of the platypus Ornithorhynchus anatinus

© Company of BiologistsThe 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.F.E. Fish, P.B. Frappell, R.V. Baudinette and P.M. MacFarlan

Exercise training enhances aerobic capacity in juvenile estuarine crocodiles (Crocodylus porosus)

Copyright © 2008 Elsevier Inc. All rights reserved.Tomasz Owerkowicz and Russell V. Baudinettehttp://www.elsevier.com/wps/find/journaldescription.cws_home/525464/description#descriptio

Energetics of swimming by the ferret: Consequences of forelimb paddling

Copyright © 2006 Elsevier Inc. All rights reserved.Frank E. Fish and Russell V. Baudinettehttp://www.elsevier.com/wps/find/journaldescription.cws_home/525464/description#descriptio