Common to all terrestrial air breathers and their bimodal and aquatic antecedents is the need to achieve a balance between O2 consumption–CO2 excretion in the tissues and the rate of delivery or removal of these gases via the gills, bladder, skin, or lungs. This balance between “supply” and “demand” normally is very finely controlled in some groups of vertebrates, whereas in others it may be achieved only in the relatively long term.

Continuous water breathers

Almost all water breathers respond to hypoxic exposure with an increase in the frequency and amplitude of branchial pumping (see Shelton 1970b for review). The extraction of O2 from the water in aquatic breathers is usually low, but the oxygen stores of the body, intervening between the respiratory membranes and the mitochondria, are limited to comparatively small amounts bound to hemoglobin and myoglobin. Thus, overall there is not a high oxygen-store-to-oxygen-utilization ratio (Chapter 3), a situation that severely restricts the short-term ability of aquatic fish to protect the tissues from the effects of environmental hypoxia or changes in metabolic rate. This low store-to-utilization ratio has necessitated a sensitive control over both ventilation and perfusion to maintain oxygen supplies to the tissues. Such a control system has to (1) provide monitoring of respiratory gas levels, particularly O2, at one or more sites between the respiratory membranes and the mitochondria, and (2) mediate active behavioral (avoidance) and physiological (hyperventilation, lamellar recruitment) responses, such that even brief imbalances in O2 supply and demand are obviated.

Very different modes of ventilation exist for lungs and gills. In fish a pressure gradient drives a unidirectional flow of water across the gills from the buccal cavity to the opercular cavities (Figure 4.1a). The synchronized action of a buccal pump and an opercular pump generates the pressure gradient. Mammalian lungs, however, are tidally ventilated by aspiration. Below-ambient pressures are developed within the lung through expansion of the thoracic cage to draw air into the lung (Figure 4.1b). Thus the evolution of air breathing in vertebrates has been associated with a change from a unidirectional mode of ventilation of a respiratory surface with water to one with a tidal mode of ventilation with air using aspiration. Clearly these changes are dictated by the marked differences in density and viscosity between air and water (see Chapter 2).

Most bimodally breathing vertebrates use a modified buccal force pump to ventilate their air-breathing organ. The modified buccal force pump is analogous to, if not homologous to, the buccal pump used to ventilate the gills. The positive-pressure phase of the buccal pump is utilized to force-ventilate the air-breathing organ. These three major forms of vertebrate ventilation are shown schematically in Figure 4.2 and Table 4.1.

To examine the evolution of air-breathing mechanisms, we must first consider gill ventilation in fish breathing water, particularly the nature of the buccal force pump.

We envisage that air-breathing vertebrates have evolved several times from water-breathing, bony fish belonging to the group Osteichthyes. These fish have within their body an enclosed chamber of air, which may function in buoyancy or as a source for oxygen. It is difficult to ascertain the evolutionary relationships between lungs and swim bladders, but they probably evolved independently, with lungs appearing before swim bladders. Because of their ventral location lungs have probably always functioned only in oxygen transfer, whereas dorsal swim bladders could function in either gas transfer or buoyancy control. These two functions are not mutually exclusive in swim bladders because the removal of oxygen without a simultaneous addition of an equal amount of CO2 to the gas chamber will reduce its size and result in an increase in the overall density of the fish. In all probability this dorsal gas bladder initially served both as an oxygen source during aquatic hypoxia, and for buoyancy regulation, depending on the nature of the environment and the requirements of the animal. Subsequent evolution in fish resulted in the development of some forms specialized for buoyancy control and others in which modifications for more efficient gas transfer were selected. The latter would have involved the elaboration of a large, thin respiratory epithelium and some means of ventilation and perfusion of this epithelium.

Modern-day bimodal breathers may use a modified gill, the buccal or pharyngeal cavity, a region of the gut, or a lung or gas bladder for gas exchange.

Air versus water as a respiratory medium

Air-saturated water contains about one-thirtieth of the oxygen found in an equal volume of air; even so, most vertebrates, including water-breathing fish, can maintain oxygen delivery to the tissues in the face of changes in both oxygen supply and demand. There is an ultimate level of hypoxia, however, at which an animal is unable to maintain oxygen delivery, and aerobic metabolism falls. The exact level at which this occurs varies widely with the species. When environmental oxygen levels become limiting, behavioral, physiological, and/or biochemical mechanisms are invoked which enable some animals to survive hypoxic conditions. In general, the behavioral mechanisms are to escape from the hypoxic conditions. Many fish avoid hypoxic waters by moving to skim the surface waters where the oxygen content is usually higher. Some fish species breathe air and tap the generally stable and large oxygen supply in the atmosphere. Some of these air-breathing fish, particularly those that inhabit waters that are nearly always hypoxic, are obligate air breathers. For example, the pirarucu, Arapaima gigas, relies on air breathing for most of its oxygen supply, and will die if not allowed access to the surface (Stevens and Holeton 1978).

Carbon dioxide levels in lakes and oceans vary considerably, unlike atmospheric levels, which remain very low and stable. These oscillations in CO2 levels create problems for aquatic animals, affecting CO2 excretion and therefore hydrogen ion regulation.