Ventilation and Metabolism in a Large Semifossorial Marsupial:The                     Effect of Graded Hypoxia and Hypercapnia

Frappell, Peter B.; Baudinette, R. V.; MacFarlane, Peter M.; Wiggins, Paul R.; Shimmin, Glenn

doi:10.1086/324769

Cited by 20 publications

(9 citation statements)

References 14 publications

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“…Thus, it is not clear whether it is the capacity for heterothermy or the chronic hypoxia of a fossorial life that results in hypoxia tolerance. A number of semi-fossorial, as well as nonfossorial, heterotherms exhibit tolerance to hypoxia comparable with fossorial species (Hiestand et al, 1950; Biörck et al, 1956; Burlington et al, 1971;Davies and Schadt, 1989;Mortola, 1991;Walsh et al, 1996; Boggs et al, 1999;Frappell et al, 2002). Such tolerance does not necessarily depend on exposure to chronic hypoxia, as it is also expressed in adults not exposed to hypoxia during development (Mortola, 1991).…”

Section: Hypoxia Tolerance As An Adaptation To Heterothermy Per Sementioning

confidence: 99%

Hypoxia tolerance in mammalian heterotherms

Drew

Harris

LaManna

et al. 2004

Journal of Experimental Biology

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Heterothermic mammals tolerate severe hypoxia, as well as a variety of central nervous system insults, better than homeothermic mammals. Tolerance to hypoxia may stem from adaptations associated with the ability to survive hibernation and periodic arousal thermogenesis. Here, we review evidence and mechanisms of hypoxia tolerance during hibernation, euthermy and arousal in heterothermic mammals and consider potential mechanisms for regenerative-like processes, such as synaptogenesis, observed within hours of hypoxic stress associated with arousal thermogenesis. 3156hypothermia and metabolic suppression in ground squirrels as it does in hypoxia-tolerant turtles and fish (Bullard et al., 1960). Additional adaptations in heterothermic mammals may synergize with hypothermia and metabolic suppression to attenuate the cytotoxic cascade. Because many of these protective mechanisms such as hypothermia, metabolic suppression, immunosuppression/leukocytopenia and increased antioxidant defenses differ between hibernating (torpid) and euthermic animals, we will discuss hypoxia tolerance in hibernating animals separately from hypoxia tolerance in euthermic animals (Fig.·1; reviewed in Drew et al., 2001).Hypoxia tolerance in the hibernating state: evidence and mechanisms Reports dating back to the early 1800s describe hypoxia tolerance in the hibernating state in bats, marmots and ground squirrels and show that tolerance displayed during hibernation exceeds tolerance observed during euthermy (Spallanzani et al., 1803; Carlisle, 1805; cited in Biörck et al., 1956; reviewed in Bullard et al., 1960). Biörck et al. (1956) confirmed these initial observations and reported that hibernating hedgehogs (Erinaceus europaeus) survive 50-120·min of 100% N2, in most cases without apparent damage.Interestingly, many hibernating species in steady-state torpor are not hypoxic despite 10-fold or greater decreases in respiratory rates. During torpor, Arctic ground squirrels (Spermophilus parryii), as well as other species of ground squirrel, are well oxygenated with normal to above normal arterial oxygen pressures (Frerichs et al., 1994; Y. L. Ma, X. Zhu, P. M. Rivera, O. Toien, B. M. Barnes, J. C. LaManna, M. A. Smith and K. L. Drew, manuscript submitted for publication). By contrast, other heterothermic species, such as golden-mantled ground squirrels (Spermophilus lateralis) and hedgehogs (E. europaeus), may become hypoxic during torpor owing to long periods of apnea. These species often breathe intermittently during hibernation, waiting up to 30·min or longer between breaths. In hedgehogs, arterial oxygen partial pressure (PaO∑), sampled from chronic aorta cannula, is higher in torpor than in the active state (120 vs 105·mmHg; 160 vs 14.0·kPa) but K. L. Drew and others Release of neurotransmitters, including the excitotoxin glutamate, and activation of NMDA and AMPA receptors contribute to the flood of Ca 2+ from extra-and intracellular stores, which leads to calcium overload (4). Activated microglia release inflammatory cytokines and ni...

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Section: Hypoxia Tolerance As An Adaptation To Heterothermy Per Sementioning

confidence: 99%

Hypoxia tolerance in mammalian heterotherms

Drew

Harris

LaManna

et al. 2004

Journal of Experimental Biology

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“…Effects of hypoxia on vertebrate physiology have received a lot of attention from different groups of researchers: clinicians studying pathologic conditions (Giffard et al, 2004;Graham et al, 2004;Fan et al, 2005), environmental physiologists interested in human acclimation (or lack thereof) to high altitude (Hochachka, 1998;Hoppeler and Vogt, 2001;Erzurum et al, 2007), and comparative physiologists interested in animal adaptation to oxygen-poor environments (Frappell et al, 2002;Bickler and Buck, 2007;Ramirez et al, 2007). Less attention has been paid to hyperoxia, which is only encountered by air-breathing vertebrates at hatching or birth (Mortola, 2001).…”

Section: Introductionmentioning

confidence: 99%

Atmospheric oxygen level affects growth trajectory, cardiopulmonary allometry and metabolic rate in the American alligator (Alligator mississippiensis)

Owerkowicz

Elsey

Hicks

2009

Journal of Experimental Biology

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SUMMARYRecent palaeoatmospheric models suggest large-scale fluctuations in ambient oxygen level over the past 550 million years. To better understand how global hypoxia and hyperoxia might have affected the growth and physiology of contemporary vertebrates, we incubated eggs and raised hatchlings of the American alligator. Crocodilians are one of few vertebrate taxa that survived these global changes with distinctly conservative morphology. We maintained animals at 30°C under chronic hypoxia (12% O 2 ), normoxia (21% O 2 ) or hyperoxia (30% O 2 ). At hatching, hypoxic animals were significantly smaller than their normoxic and hyperoxic siblings. Over the course of 3 months, post-hatching growth was fastest under hyperoxia and slowest under hypoxia. Hypoxia, but not hyperoxia, caused distinct scaling of major visceral organs -reduction of liver mass, enlargement of the heart and accelerated growth of lungs. When absorptive and post-absorptive metabolic rates were measured in juvenile alligators, the increase in oxygen consumption rate due to digestion/absorption of food was greatest in hyperoxic alligators and smallest in hypoxic ones. Hyperoxic alligators exhibited the lowest breathing rate and highest oxygen consumption per breath. We suggest that, despite compensatory cardiopulmonary remodelling, growth of hypoxic alligators is constrained by low atmospheric oxygen supply, which may limit their food utilisation capacity. Conversely, the combination of elevated metabolism and low cost of breathing in hyperoxic alligators allows for a greater proportion of metabolised energy to be available for growth. This suggests that growth and metabolic patterns of extinct vertebrates would have been significantly affected by changes in the atmospheric oxygen level.

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“…In fact we (Hahn 1990;Young et al, 1992;Nassar et al, 2002). The lower curve (~) illustrates resting ventilation rate as a function of size based on data for 32 species (Morrison et al 1959;Kleinman and Radford 1964;Mortola and Nororaj 1985;Nagel 1991;Worthington et al 1991;Frappell et al 1992;Jürgens et al 1996;Frappell et al 2002;Frappell 2003;Elvert and Heldmaier 2005;Self 2007). Note that Didelphis ( ) and rat (Rattus), hedgehog (Atelerix) and 4-eyed opossum (Philander) are able to increase their 1:1 ventilatory/step rates up to their natural frequencies at their maximum speeds (mean resting to maximum data points indicated by arrows), while the smaller Monodelphis ( ) has no locomotor scope -it is at its natural frequency at rest and at its preferred speed but must drop below its natural frequency when forced to higher speeds.…”

Section: Discussionmentioning

confidence: 99%