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Respiration: an Introduction JJ Cech Jr., University of California, Davis, CA, USA CJ Brauner, University of British Columbia, Vancouver, BC, Canada

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Respiration: an Introduction JJ Cech Jr., University of California, Davis, CA, USA CJ Brauner, University of British Columbia, Vancouver, BC, Canada GAS EXCHANGE Respiration: An Introduction JJ Cech Jr., University of California, Davis, CA, USA CJ Brauner, University of British Columbia, Vancouver, BC, Canada ª 2011 Elsevier Inc. All rights reserved. Introduction Tissue Respiration The Environment: Water and Air as Respiratory Media Whole Animal and Techniques in Respiratory Ventilation and Gas-Exchange Organs Physiology Gas Transport and Exchange Further Reading Glossary Mitochondria Organelles that produce most of the Bohr effect Effect of the proton concentration (pH) aerobic energy required by the cell. on the oxygen affinity of hemoglobin. P50 The oxygen partial pressure at half-maximal oxygen Carbonic anhydrase A zinc metalloenzyme that saturation of blood or hemoglobin. reversibly catalyzes the reaction of CO2 and H2O to form Partial pressure The atmospheric pressure exerted + � H and HCO3 . by O2 alone proportional to the total concentration of Diffusion Net movement of a solute from an area of this gas. It is typically measured in either mmHg (torr) higher concentration to an area of lower concentration. or kPa. Equilibrium Pertaining to the situation when all forces Respiratory cascade A model of gas exchange in acting are balanced by others resulting in a stable which gas is viewed as flowing through a series of unchanging system. resistances from the environment to the tissues or vice Haldane effect Proton binding to hemoglobin (as a versa. The model is based on the analogy of water function of oxygenation). flowing down a series of cascades with the difference Hypoxia Low partial pressures of oxygen in external or being that gas flow is driven by differences in partial internal environments. pressure rather than gravity. Interlamellar cell mass (ILCM) A mass made up of Rete Structure consisting of blood vessels arranged to undifferentiated cells and ionocytes, and possibly other facilitate the exchange of heat or oxygen. cell types, filling up a variable part of the space between Root effect A property of fish hemoglobin in which the lamellae of fish gills. protons decrease the maximal oxygen saturation of Lamellae Also known as secondary lamellae, these are hemoglobin. For practical purposes, it is defined as a attached in rows to the gill filaments. They are the reduction of oxygen saturation at atmospheric oxygen primary sites for gas exchange in fish gills. Each lamella tension. is made up of two epithelial layers separated by pillar Ventilation The movement of the respiratory cells. Oxygen is taken up by erythrocytes flowing inside medium (air or water) over the surface of the gas the lamellae from water flowing between the lamellae. exchanger. Introduction Models: Bioenergetics in Aquaculture Settings and Bioenergetics in Ecosystems), all of which are important Respiration and gas exchange is an essential process to determinants of fitness. maintain an aerobic existence in all vertebrates, including The complex process of respiration in fish is discussed fishes. The uptake of oxygen (O2), along with metabolism in detail in this section. It starts with the environment of organic substrates such as glucose and lipids, is needed where O2 and CO2 move into and out of the animal, to power the biochemical machinery (e.g., in the mito­ respectively, by simple diffusion. Gases diffuse across a chondria) in cells for body maintenance, as well as for gas-exchange organ which represents the interface other aerobic functions such as growth, movement, repro­ between the organism and the environment and may duction, and disease resistance (see also Energetic consist of skin, gills, and in some cases an air-breathing 791 792 Gas Exchange | Respiration: An Introduction organ. Ventilation of the respective media (water and in The Environment: Water and Air some cases air if an air-breathing organ is present) in as Respiratory Media conjunction with blood perfusion across the gas-exchange organ, both of which can be altered proportionally Characteristics of the environment can have a profound depending upon the animal’s metabolic state, ensures effect on respiration. Respiratory gas exchange in aquatic sufficient gas exchange to meet the demands of the environments presents different problems when com­ animal. pared with respiration in air. Water is a dense, viscous The circulatory system provides the conduit through medium, which also has a high heat capacity and 20–30­ which the blood is ultimately delivered to the tissues; fold lower oxygen concentration (due to low gas solubi­ hemoglobin (Hb), maintained within the red blood cell, lity) relative to air. Increases in temperature or salinity plays a vital role in the transport of both O2 and CO2 in all further decrease oxygen solubility in water, and therefore fishes, except icefishes, which represent the only verte­ oxygen content for a given gas pressure as indicated in brate that lacks Hb. Hemoglobin is a remarkable molecule Figure 1. and is one of the best-understood proteins in terms of how The PO2 and PCO2 of water can vary dramatically changes in the environment of the red blood cell alter the compared to those of atmospheric air. This is because tertiary and quaternary structure of Hb to influence the the gases contained in air do not necessarily exchange nature in which Hb binds and releases ligands such as O2, readily with water. The PO2 of aquatic environments can + CO2, and H ’s in particular. These changes optimize be zero (anoxia), low (hypoxic), normoxic, or high conditions for gas exchange to tissues in general, as well (hyperoxic), depending on the photosynthetic and as specifically to the eye and swimbladder allowing for respiratory rates of the biotic community and on water acute vision and buoyancy control respectively in many circulation characteristics. Some shallow, freshwater habi­ teleosts. tats may vary between 20 and 40 mmHg PO2 just before Finally, blood reaches the tissues where waste dawn to 200–400 mmHg at mid-day. Thus, water can be products are removed and substrates supplied to less saturated and more saturated with oxygen, even on a cells and mitochondria providing the basics for cellu­ diel basis. Many fishes, especially those that spend at least lar and mitochondrial respiration, and thus life. The part of their lives in shallow habitats, have evolved struc­ following describes these various steps in respiration tural and functional abilities to deal with variable water in more detail, providing background information and PO2 values. introducing each article that appears within the Fish in boreal, subpolar, or polar lakes may experi­ section. ence a seasonal challenge of oxygen availability – a 12 350 8 FW 10 °C 300 10 SW 10 °C 6 250 8 FW 30 °C –1 –1 l l 2 200 2 SW 30 °C M 6 µ 4 ml-O 150 mg-O 4 100 2 50 2 0 0 0 0 20 806040 100 120 % Air saturation 0 50 100 150 200 P O2 (torr or mmHg) 0 5 1015 20 25 P O2 (kPa) Figure 1 The relationship between partial pressure of oxygen (x-axis) and total oxygen content (y-axis) at 10 and 30 �C in either freshwater (FW) or seawater (SW). The three legends for each of the axes represent the different units that are used to describe both partial pressure and content in water. Reproduced from Diaz RJ and Breitburg DL (2009) The hypoxic environment. In: Richards JG, Farrell AP, and Brauner CJ (eds.) Fish Physiology, Volume 27 Hypoxia, pp. 1–23. Academic Press, with permission from Elsevier. Gas Exchange | Respiration: An Introduction 793 gradually deepening hypoxia (lowered PO2,s)duringthe relatively novel finding is discussed in Ventilation and winter as ice cover seals off gas exchange with the atmo­ Animal Respiration: Plasticity in Gill Morphology. sphere and snow cover, along with shortened While the gills are usually the predominant site for gas photoperiods, attenuate incoming light decreasing exchange in adult fish, this is not the case early in develop­ photosynthetic production of O2.Extreme wintersmay ment when the total body surface area:volume ratio in larval prolong these conditions leading to a total consumption and juvenile fish is high and gill secondary lamellae in of the remaining dissolved O2 (anoxia) by the lake’s particular have yet to be fully developed. At this point, all biota, leading to a winter fish kill (see also Hypoxia: gas exchange is across the skin. The fundamental principles The Expanding Hypoxic Environment). associated with gas exchange in aquatic media and their Fishes living in high-altitude environments must also implications for larval fishes are discussed in Ventilation cope with low-PO2 water. In this case, it is due to the lower and Animal Respiration: Respiratory Gas Exchange total barometric pressure (and the correspondingly low­ During Development: Models and Mechanisms. This arti­ ered partial pressures of the atmospheric gases). Finally, cle lays the foundations for a discussion of when the gills certain types of pollution, including those that introduce become important for gas exchange during development excessive nutrients into waterways (eutrophication), typi­ whichisdiscussedinVentilation and Animal Respiration: cally lead to wider, diel dissolved-O2 ranges, often Respiratory Gas Exchange During Development: including quite hypoxic PO2, s. Thus, fish living and Respiratory Transitions. Interestingly, the gills may take respiring aquatic media are subjected to large and routine on a more significant role for ionoregulation than for gas changes in O2 availability relative to air-breathing exchange early in development, based upon the time that + animals and many are adapted to these potentially 50% of whole body unidirectional Na uptake and O2 extreme conditions. uptake transitions to the gills. This ontogeny has interesting implications for the evolution of gill function. Ventilation and Gas-Exchange Organs Gas Transport and Exchange The physical and chemical characteristics of aquatic envir­ onments, specifically low oxygen solubility of water, Once O2 has diffused across the gill lamellae, about 98% is probably contributed to the evolutionary development of reversibly bound to Hb (oxyhemoglobin) contained within gill structure and function, and to the many mechanisms the red blood cell.
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