Exercising with and Without Lungs: I. The Effects of Metabolic Cost, Maximal Oxygen Transport and Body Size on Terrestrial Locomotion in Salamander Species

1988 ◽  
Vol 138 (1) ◽  
pp. 471-485 ◽  
Author(s):  
ROBERT J. FULL ◽  
BRUCE D. ANDERSON ◽  
CASEY M. FINNERTY ◽  
MARTIN E. FEDER

To whom offprint reprints should be addressed. Metabolic cost, oxygen consumption (MO2, respiratory structure and body size interact to determine the capacity of salamanders for terrestrial locomotion. Salamanders respiring via both lungs and skin, Ambystoma laterale and A. tigrinum, or with skin alone, Desmognathus ochrophaeus and D. quadramaculatus, attained a steady-state MO2 during exercise in a treadmill respirometer. Endurance was correlated with the speed at which maximal MO2, was attained (VMO2.max). Low aerobic costs of transport (60–80% lower than reptiles of similar mass) increased VMO2.max. However, in lungless salamanders a low maximum MO2 decreased VMO2.max significantly. MO2 increased only 1.6- to 3.0-fold above resting rates in active lungless salamanders, whereas it could increase 3.5- to 7.0-fold in active lunged salamanders. Lungless salamanders attained maximal MO2 at half to one-tenth the speed of lunged animals. Lungless salamanders fatigued in 20 min or less at speeds that lunged salamanders could sustain for 1–2 h. Body size also affected the capacity for oxygen uptake during activity and locomotor performance. The large lungless salamander D. quadramaculatus attained maximum MO2 even at its lowest rate of travel. Cutaneous gas exchange does not provide lungless salamanders with gas transport capacities found in lunged animals. However, only small increases in MO2 may be required for modest levels of activity.

1983 ◽  
Vol 104 (1) ◽  
pp. 79-95 ◽  
Author(s):  
MARTIN E. FEDER

The oxygen consumption of larvae of the frog Rana berlandieri Baird was reduced during exposure to aquatic hypoxia at 25°C, and under severe hypoxia the larvae lost oxygen to the water. The larvae responded to aquatic hypoxia by increasing aerial oxygen consumption and lung ventilatory frequency, and also by altering their heart rate and gill ventilation frequency. Under severe or prolonged aquatic hypoxia without access to air, Rana larvae accumulated lactate. When prevented from breathing air, the larvae were unable to compensate fully by increasing their aquatic oxygen consumption. Body size or the interaction of body size and oxygen partial pressure significantly affected the aerial oxygen consumption, the total oxygen consumption and gill ventilation frequency, but did not affect other aspects of larval gas exchange. Anuran larvae resemble air-breathing fishes in some responses to aquatic hypoxia (e.g. increased dependence upon aerial oxygen uptake and changes in ventilatory frequencies), but are unusual in some ways (e.g. oxygen loss to the water). The interactions of body size and hypoxia are not sufficient to explain why so many anuran larvae without lungs are small.


1993 ◽  
Vol 71 (7) ◽  
pp. 1372-1378 ◽  
Author(s):  
Barbara E. Taylor ◽  
Thomas H. Carefoot

Survival and oxygen uptake in air and water were investigated in four species of terrestrial isopods, Armadillidium vulgare Latreille, 1804, Porcellio scaber Latreille, 1804, Oniscus asellus Linné, 1758, and Ligia pallasii Brandt, 1833, to compare the degree of vestigial adaptation to aquatic existence versus adaptation to terrestrial existence. Most submerged A. vulgare, P. scaber, and O. asellus died by 18 h, whether in fresh water or isosmotic seawater. Ligia pallasii lived for almost 2 d in fresh water and for at least 25 d in seawater (none died during this time). Oxygen uptake in water was 44 – 66% that in air for the three fully terrestrial species, and 160% that in air for the semiterrestrial L. pallasii. Oxygen consumption of submerged A. vulgare (representative of fully terrestrial forms) declined to 50% after 14 h and to 17% by 24 h, by which time the animals were clinically dead. In comparison, L. pallasii's aquatic oxygen consumption was maintained at normal or higher levels for at least 3 d. All species could survive several hours of immersion in fresh water, sufficient to withstand temporary rain deluge. Ligia pallasii's superior capabilities to survive and respire in seawater reflect its greater similarity to aquatic ancestors, and an evolutionary series showing progressive decline in survival and gas-exchange capability in water would be as follows: L. pallasii > O. asellus > P. scaber ≥ A. vulgare.


1990 ◽  
Vol 149 (1) ◽  
pp. 395-406
Author(s):  
DONALD W. THOMAS ◽  
DANIELLE CLOUTIER ◽  
DANIEL GAGNÉ

We measured the breathing pattern and oxygen consumption of hibernating little brown bats {Myotis lucifugus) in open- and closed-circuit metabolic chambers. At 5°C, hibernating M. lucifugus showed bouts of ventilation lasting on average 1.24min and separated by periods of apnea lasting on average 47.59min. The bats consumed 0.014 ml O2g−1 during ventilation bouts and 0.002 ml g−1 during apnea. The total O2 uptake was 0.016 ml g−1 for a complete ventilationapnea cycle, giving a Vo2 of 0.020 ml g−1 h−11. This value is considerably lower than most values previously published for Myotis spp. and we suggest that studies using open-circuit systems that did not account for the intermittent nature of gas exchange during hibernation may be in error. Based on the dimensions of the respiratory tract, we estimate that 0.026 ml O2g−1h−1 and 0.009mlCO2g−1h−1 could diffuse down the tract if the glottis was open. The low O2 uptake during apnea indicates that the glottis was closed. If CO2 retention acts to depress metabolism in hibernators, a closed glottis and arrhythmic breathing may be adaptive strategies in hibernation.


Author(s):  
Islay D. Marsden ◽  
Sandra E. Shumway ◽  
Dianna K. Padilla

Metabolic rate is one of the most frequently measured physiological variables and the relationship between oxygen uptake and body mass is one of the most controversial issues in biology. The present study used closed chamber respirometry to compare the oxygen uptake of 32 species of benthic British gastropod molluscs of a wide size-range (from less than 0.001 g to greater than 10 g dry tissue weight). We investigated the effects of body size on the respiratory rate at 10°C to explore the evolutionary and phylogenetically determined patterns of metabolic scaling both among different gastropods groups, and within siphonate and asiphonate caenogastropods. Resting oxygen uptake (O2) increased with body mass (W) with a slope value of 0.6 using both ordinary least squares (OLS) and standard major axis (SMA) where N = 488, over a 6 fold range of body mass. The slopes b of the regression lines relating oxygen uptake to body mass were similar for all heterobranch molluscs and most caenogastropods. Highest mass-specific rates for oxygen consumption were found for the smallest littorinid species. Trophic mode significantly affected the amount of oxygen consumed with higher oxygen uptake in herbivores than other groups, including detritivores and predators. All of the gastropods reduced their oxygen consumption when exposed to declining oxygen conditions; however, about a third of the species exhibited partial regulation at higher oxygen partial pressures. When exposed to 20% normal saturation levels, smaller gastropods respired at approximately 25% of their rates in fully saturated seawater whereas larger species (above 0.1 g dry tissue weight) respired at approximately 35% of the values recorded at full saturation. Our study suggests that a scaling exponent relating O2 to body mass of 0.6 is typical and may be ‘universal’ for gastropods. It is below the 0.75 scaling exponent which has been proposed for ectothermic invertebrates. It is concluded that size does matter in determining the metabolic patterns of gastropods and that the quantity of oxygen consumed and the energy balance of gastropods is affected by activity, food type and exposure to declining oxygen conditions.


1982 ◽  
Vol 97 (1) ◽  
pp. 1-21 ◽  
Author(s):  
C. R. Taylor ◽  
N. C. Heglund ◽  
G. M. Maloiy

This series of four papers investigates the link between the energetics and the mechanics of terrestrial locomotion. Two experimental variables are used throughout the study: speed and body size. Mass-specific metabolic rates of running animals can be varied by about tenfold using either variable. This first paper considers metabolic energy consumed during terrestrial locomotion. New data relating rate of oxygen consumption and speed are reported for: eight species of wild and domestic artiodactyls; seven species of carnivores; four species of primates; and one species of rodent. These are combined with previously published data to formulate a new allometric equation relating mass-specific rates of oxygen consumed (VO2/Mb) during locomotion at a constant speed to speed and body mass (based on data from 62 avian and mammalian species): VO2/Mb = 0.533 Mb-0.316.vg + 0.300 Mb-0.303 where VO2/Mb has the units ml O2 s-1 kg-1; Mb is in kg; and vg is in m s-1. This equation can be expressed in terms of mass-specific rates of energy consumption (Emetab/Mb) using the energetic equivalent of 1 ml O2 = 20.1 J because the contribution of anaerobic glycolysis was negligible: Emetab/Mb = 10.7 Mb-0.316.vg + 6.03 Mb-0.303 where Emetab/Mb has the units watts/kg. This new relationship applies equally well to bipeds and quadrupeds and differs little from the allometric equation reported 12 years ago by Taylor, Schmid-Nielsen & Raab (1970). Ninety per cent of the values calculated from this genera equation for the diverse assortment of avian and mammalian species included in this regression fall within 25% of the observed values at the middle of the speed range where measurements were made. This agreement is impressive when one considers that mass-specific rates of oxygen consumption differed by more than 1400% over this size range of animals.


1990 ◽  
Vol 154 (1) ◽  
pp. 397-405
Author(s):  
HEGE JOHANNESEN ◽  
STEWART C. NICOL

Oxygen consumption (VO2), tidal volume, respiratory frequency and the composition of the gas in the interclavicular air sac were measured in the little penguin Eudyptula minor (Forster) at ambient temperatures (Ta) of 5 and 20 °C. VO2 increased from 14.60 ml O2 kg−1 at 20°C to 18.29 ml O2 kg−1 min−1 at 5 °C. However, the elevated atVO2 the low Ta was not matched by a similar rise in total inspiratory ventilation (Vi). The ventilatory requirement (Vi/VO2) thus decreased from 0.5751 mmol−11 at 20°C to 0.4401 mmol−1 at 5°C. An increased gas exchange efficiency during cold exposure was also shown by the composition of the gas in the interclavicular air sac. PO2 decreased from 11.95 kPa at 20°C to 10.24kPa at 5°C, while the corresponding increase in PCO2 was from 6.61 to 7.50 kPa. Oxygen extraction, calculated from VO2, Vi and O2 content of the inspired air, increased from 24.60% at 20°C to 31.04% at 5°C. Oxygen extraction calculated from the O2 contents of inspired air and interclavicular air—sac gas was 38.73 % at 20°C and 47.18% at 5°C. The results confirm previous findings for the little penguin which showed a decrease in the ventilatory requirement with increasing oxygen uptake. However, the improved gas exchange efficiency during cold exposure and the strong correlation found between oxygen extraction and oxygen consumption have not been demonstrated previously for this species.


1976 ◽  
Vol 230 (1) ◽  
pp. 158-162 ◽  
Author(s):  
EA Kroeger

The present studies were designed to measure the metabolic cost, in terms of oxygen consumption (QO2) and lactate production, of membrane ion transport, and activation of the contractile apparatus of rat myometrium. The normal QO2 of 16.98 +/- 0.84 mumol/g wet tissue per h was reduced to 15.42 +/- 0.66 in the presence of high-K (127 mM) solution. This was further reduced to 14.05 +/- 0.77 and 13.53 +/- 0.76 by the addition of D-600 (10(-5) M), which inhibits Ca influx or in the presence of Ca-deficient high-K solutions, respectively. Ouabain (10(-3) M) reduced QO2 by an amount similar to that produced by high K. Addition of K+ to Na-rich preparations produced an immediate ouabain-sensitive increase of QO2 whose rate was a linear function of [K+]o up to 30 mM in Ca-deficient solution. In all of the above conditions, changes in lactate release paralleled those in QO2. Isoproterenol (10(-6) M), which causes mechanical inhibition of myometrium, had no effect on the QO2 of muscles in normal solution but reduced the QO2 of muscles in Ca-deficient solution. Lactate release was increased by isoproterenol in both normal and Ca-deficient solutions. These results show that the Na pump is an important site of energy utilization in myometrium. Components which can be interpreted in terms of energy utilization for Ca pumping and the contractile apparatus were also demonstrated.


1990 ◽  
Vol 150 (1) ◽  
pp. 233-246 ◽  
Author(s):  
R. J. Full ◽  
D. A. Zuccarello ◽  
A. Tullis

The mass-specific minimum cost of terrestrial locomotion (Cmin) decreases with an increase in body mass. This generalization spans nearly eight orders of magnitude in body mass and includes two phyla. The general relationship between metabolic cost and mass is striking. However, a significant amount of unexplained interspecific variation in Cmin exists at any given body mass. To determine how variation in morphology and physiology affects metabolic energy cost, we measured the oxygen consumption of three comparably sized insects running on a miniature treadmill; the American cockroach Periplaneta americana, the caterpillar hunting beetle Calosoma affine and the Australian field cricket Teleogryllus commodus. Steady-state oxygen consumption (VO2ss) increased linearly with speed. Cmin was similar for crickets and cockroaches (8.0 and 8.5 ml O2 g-1km-1, respectively), but was substantially lower for beetles (4.6 ml O2 g-1km-1). The predicted value of Cmin for all three insects was within the 95% confidence intervals of the Cmin versus body mass function. However, the 95% confidence intervals extend approximately 2.5-fold above and 40% below the regression line, making the variation at any given body mass nearly sixfold. Normalizing for the rate of muscle force production by determining the metabolic cost per stride failed to account for the interspecific variation in the cost of locomotion observed in the three insects. Ground contact costs (i.e. VO2ss multiplied by leg contact time during a stride) in insects were similar to those measured in mammals (1.5-3.1 J kg-1) and were independent of speed, but did not explain the interspecific variation in the cost of locomotion. Muscles of the caterpillar hunting beetle may have a greater mechanical advantage than muscles of the Australian field cricket and American cockroach. Variation in musculo-skeletal arrangement, apart from variation in body mass, could translate into significant differences in the minimum cost of terrestrial locomotion.


1997 ◽  
Vol 21 (1) ◽  
pp. 9-16 ◽  
Author(s):  
R. S. Gailey ◽  
M. S. Nash ◽  
T. A. Atchley ◽  
R. M. Zilmer ◽  
G. R. Moline-Little ◽  
...  

The effect of prosthesis mass on the metabolic cost of steady-state walking was studied in ten male non-vascular trans-tibial amputees (TTAs) and ten non-amputee controls. The subjects underwent four trials of treadmill ambulation, with each trial performed for nine minutes at level grade and 76 m/min. Twenty minutes of seated rest followed each trial. During trials numbers one and two, TTAs ambulated without mass added to their prosthesis. During the third and fourth trials, either 454 or 907 grammes mass (1 or 2lbs mass respectively) were randomly assigned and added to eithier the prosthesis or the leg of the non-amputee control. Subjects were blinded to the amount of mass added to their limb. Within-group comparisons across the four trials showed significant differences in oxygen consumption (VO2) and heart rate (HR) between the two non “mass added” trials, but no effect for addition of mass. The VO2 of TTAs was only 0.6ml/kg/min (4.7 percent) greater during walking following the addition of 907 grammes to the prosthesis than without mass addition at all, while HR averaged only 1.4 beats/min. higher under the same testing condition. Pearson-product moment correlations echoed these findings, as moderate, but in all cases, negative correlations were observed for associations among the factors of subject age, stump length, and prosthesis-shoe weight, and both VO2 and HR. It was concluded that adding up to 907 grammes mass to a non-vascular TTA's prosthesis will not significantly increase the energy expenditure or HR at a normal walking speed, and that elevated energy cost of ambulation in repeated measures testing without mass added may reflect task familiarisation and not an added burden of prosthesis mass.


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