Vertebrate Respiration and Circulation in Extreme Conditions

Abstract

The, acquisition and internal transport of respiratory gases and metabolic fuels depend on linked processes, with design and function related to energetic demands and attributes of the environment. Environmental challenges to these processes reflect variation in the density of gases, temperature and the pressures that prevail in the environmental medium. The limits of vertebrate survival and performance are tested in environments of low oxygen such as soil, mud or water in which animals overwinter sometimes at freezing temperatures; high altitude where the atmospheric density of oxygen is low; and the deeper reaches of ocean where pressure and distance challenge the physiology of air‐breathing vertebrates. Cardiorespiratory functions are also limited by the metabolic demands of animals related to body size, temperature, activity and gravity, which also impacts features of morphology and behaviour. Responses of vertebrates to physical environmental challenges are related to phylogenetic evolutionary changes and include both plasticity of adjustments and genetic/genomic changes influencing form and function, including molecular underpinnings. Key Concepts Aerobic cellular respiration requires internal transport of fuels, oxygen and carbon dioxide, which are exchanged with the external environment and at greater rates during exercise or activity involving muscles. The rate of energy expenditure, or metabolism, per unit of body mass decreases with increasing body size, while increasing with temperature and level of activity. The functional capacities of each step in oxygen transport are matched to each other, and the upper limits to aerobic capacity depend on the integrated function of the linked steps in oxygen transport, rather than any single factor. Saving of energy is related to lowering of body temperature, suppression of metabolism, behavioural reduction of activity and molecular adjustments in fuel usage, among other factors. Countermeasures to gravity's ‘pull’ on blood circulation include tight tissues, relatively nondistending blood vessels, effective neurogenic control of heart and blood vessels and anatomical or behavioural reduction in the vertical length of blood vessels. Increasing altitude reduces the density of oxygen, reduces temperature, increases the diffusion of gases and increases evaporative water loss. The pressure in a fluid column increases with depth as a result of gravity, and increasing pressures in deep water columns compress air spaces, alter the structure of proteins and function of enzymes and decrease the fluidity of membranes. Atmospheric hypoxia limits the distributional range and performance of vertebrates at higher altitudes. Responses to hypoxia may increase the cardiac output and blood flow to tissues, increase the growth of blood vessels, increase blood oxygen capacity and circulating blood volume and adjust metabolic pathways to favour increased efficiency of ATP production. Compared with mammals, birds have superior ability to acquire O 2 and to maintain blood flow to the brain during hypoxia when levels of CO 2 in the blood are reduced. The survival of overwintering ectothermic vertebrates at subzero temperatures is aided by behavioural, physiological and biochemical adaptations that enable animals either to avoid freezing or to tolerate some portion of their body fluids being converted to ice, which is managed by cryoprotectants and antifreeze proteins. Routine dives of diving vertebrates are aerobic, but glycolysis supplements the energy requirements during prolonged submergence or repetitive dives of some species, as well as the low metabolic needs of turtles and frogs hibernating at low temperatures. Vertebrate adaptations for diving deeply include enhanced oxygen reserves primarily in blood, circulation of blood principally to brain and heart, smaller volumes and collapse of the lung to minimize problems associated with buoyancy and the entry into blood of pressurized pulmonary nitrogen, which leads to embolism and the debilitating condition known as the bends. In sea snakes, cardiovascular shunts ‘meter’ the lung oxygen store, lower the partial pressure of oxygen in blood and enable the loss of nitrogen while minimizing the loss of oxygen across the skin.