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

Abstract

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.

Testing Metabolic Theories

“…Some experimental studies of growth under manipulated O 2 are consistent with the WBE expectations; exposure to chronic hypoxia results in a decrease in adult size in some insects (Klok and Harrison 2009;Harrison et al 2010) as well as reduced growth rates in fish (Wang et al 2009), American alligators Alligator mississippiensis (Owerkowicz et al 2009), and embryonic mammals and birds (de Grauw et al 1986;Giussani et al 2007). For many species, processes like growth respond to hypoxia in a threshold manner and only under extreme conditions (Chabot and Dutil 1999;McNatt and Rice 2004).…”

The evolutionary consequences of oxygenic photosynthesis: a body size perspective

“…Size distributions among species within higher taxa are widely thought to be determined by energetic considerations and mortality schedules (Brown et al 1993;Hallock 1985;Sebens 2002). As oxygen availability can affect both efficiency and rate of growth (Owerkowicz et al 2009), variation in oxygen availability should affect selection across the size spectrum, not simply at the maximum. For example, time-dependent risk of death due to predation or disease tends to select against large size because of the time required to grow larger prior to reproduction.…”

“…The most pronounced acceleration of growth under experimental hyperoxia occurred in the domestic chicken (Metcalfe et al 1981;Stock et al 1983), a species which has been bred specifically for rapid growth. In studies finding size effects associated with both hypoxia and hyperoxia, the magnitude of change in body size under hyperoxia has been much less than that observed under hypoxia (Frazier et al 2001;Owerkowicz et al 2009). Several other studies have found size decrease under hypoxia but no increase under hyperoxia (Andrews 2002;Greenberg and Ar 1996;Herman and Ingermann 1996;).…”

Reduced egg shell permeability affects embryonic development and hatchling traits in Lycodon rufozonatum and Pelodiscus sinensis

“…Unlike previous studies applying low-concentration O 2 to eggs (e.g. Kam 1993;Owerkowicz et al 2009), we used external regional hypoxia with half of the egg surface left for gas exchange, suggesting that reptile embryos may be able to survive losing half of the respiratory egg surface with the help of physiological adjustment like compensatory responses of cardiovascular functions (Kam 1993;Miller et al 2002;Du et al 2010b). In addition, gaseous O 2 could circulate from uncovered egg regions to covered regions, which may reduce the hypoxia stress imposed on embryos.…”

“…1). Instead, it is a response to hypoxia, because hypoxia reduces energy metabolism of embryos and yields small hatchlings with large residual yolk sac (Owerkowicz et al 2009). The difference in embryonic yolk utilization between the upper-half and bottom-half hypoxia indicated that O 2 deficiency in early development may impose a significant effect on embryonic development, although O 2 consumption increases dramatically only in later developmental stage when embryos grow fast (Vleck & Hoyt 1991;Andrews 2004).…”