Fish Physiology: Primitive Fishes

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• Publisher: Academic Press
• Year: 2011
• eBook ISBN: 9780080549521
• Topic: Biological Sciences
• Subtopic: Physiology
• Index: Biological Sciences

Primitive fishes are a relatively untapped resource in the scientific search for insights into the evolution of physiological systems in fishes and higher vertebrates. Volume 26 in the Fish Physiology series presents what is known about the physiology of these fish in comparison with the two fish groups that dominate today, the modern elasmobranchs and the teleosts. Chapters include reviews on what is known about cardiovascular, nervous and ventilatory systems, gas exchange, ion and nitrogenous waste regulation, muscles and locomotion, endocrine systems, and reproduction. Editors provide a thorough understanding of how these systems have evolved through piscine and vertebrate evolutionary history.Primitive Fishes includes ground-breaking information in the field, including highlighs of the most unusual characteristics amongst the various species, which might have allowed these fishes to persist virtually unchanged through evolutionary time. This volume is essential for all comparative physiologists, fish biologists, and paleontologists.- Provides an analysis of the evolutionary significance of physiological adaptations in "ancient fishes"- Offers insights on the evolution of higher vertebrates- The only single source that presents an in-depth discussion of topics related to the physiology of ancient fishes

Gas Transport and Exchange

C.J. Brauner, M. Berenbrink

Abstract

Gas exchange is a prerequisite of vertebrate life. In terms of structural and functional diversity and habitats occupied, extant teleosts clearly outcompete extant primitive fishes; however, there are a few aspects related to gas exchange that may have contributed to the survival of these primitive fishes. Most of the primitive fishes either have the ability to breath air, have the ability to tolerate aerial exposure (and in some cases estivate), or are tolerant to aquatic hypoxia. Many of the bimodal breathers retain fully functional gills, which at times allow strictly aquatic breathing over prolonged periods which may be important for aerial predator avoidance or surviving ice cover in temperate climates. While air breathing is important for surviving aquatic hypoxia, it is also important in enhancing O₂ uptake during exercise. Living primitive fishes occupy strategic positions in the evolutionary tree of vertebrates and may shed light on the evolution of blood O₂ and CO₂ transport characteristics. Evolutionary reconstruction indicates that the increase in the Bohr–Haldane effect in primitive ray‐finned fishes was followed first by a gradual increase in the magnitude of the Root effect and then a gradual reduction in specific Hb buffer value. This was followed by the evolution of a choroid rete mirabile and ocular O₂ secretion in the last common ancestor of Amia calva and teleosts. Finally, the adrenergic red blood cell Na⁺/H⁺ exchanger was never present in primitive ray‐finned fishes or primitive teleosts and only evolved in advanced teleosts. No such evolutionary trends are observed in primitive lobe‐finned fishes.

1 Introduction

The uptake of O₂ from the environment and elimination of metabolically produced CO₂ are prerequisites of vertebrate life. A great deal is known about the differences in O₂ and CO₂ transport and exchange between water and air‐breathing vertebrates; however, this stems largely from studies on teleost fishes in the former, and mammals in particular in the latter. Fishes possess great diversity in gas exchange strategy, ranging from completely water breathing to obligate air breathing, and thus occupy a crucial phylogenetic position in the transition of life from water to land which has large implications for gas exchange (Dejours, 1988; Graham, 1997). Relatively little in relation to O₂ and CO₂ transport and exchange is preserved within the fossil record, and consequently, reconstruction of the evolution of gas exchange is limited largely to studies on extant species. In the following sections, primitive fishes will be discussed going backward in time from the closest living relatives of teleosts to successively more distantly related groups of primitive fishes. We first discuss the relative roles of the respective gas‐exchange surfaces [gills, skin, and air‐breathing organs (ABOs)] to O₂ and CO₂ exchange in each primitive fish group. We then discuss general aspects of O₂ and CO₂ exchange, largely on the basis of what is known in teleosts and then what is known for primitive fishes. Finally, we discuss how this information on primitive fishes helps to identify some general trends in the evolution of vertebrate blood gas transport characteristics.

2 Partitioning of O₂ and CO₂ Exchange Across the Respiratory Surfaces

In typical water‐breathing teleosts, the gills are the predominant surface for both O₂ and CO₂ exchange; but in some cases, there can be appreciable O₂ uptake across the skin. Many of the primitive fish groups discussed in this chapter contain species that are facultative or obligate air‐breathers. Thus, the gills, skin, and ABOs are all potential sites for gas exchange in many primitive fishes. There has been considerable interest and research conducted on the morphologies of the respective gas exchange structures (see Chapter 4, this volume) and a great number of direct measurements of the relative role and efficiency of each structure to both O₂ and CO₂ exchange, which are briefly summarized below. In most air‐breathing fishes studied to date, there appears to be a spatial separation of O₂ and CO₂ exchange. That is, the majority of O₂ uptake may occur across the ABO, and the majority of CO₂ excreted across the gills and/or skin. This is largely related to the fact that the capacitance coefficient for CO₂ does not change much between water and air, while that for O₂ is 20‐ to 30‐fold higher (depending on the temperature) in air than water (Dejours, 1988). Because ventilation‐rate volume (ventilation frequency × volume) of gas exchangers in fish is largely regulated to secure adequate O₂ uptake, ventilation‐rate volume of the ABO in an air‐breather is greatly reduced relative to that of the gills in a water‐breather. The reduced ventilation‐rate volume is sufficient for O₂ uptake, but insufficient for CO₂ elimination across the ABO, and consequently CO₂ diffuses out across the gills and/or skin (Dejours, 1988; Graham, 1997). The spatial uncoupling of O₂ and CO₂ transport has interesting implications for gas exchange in fish, given that at least in most teleost fishes there is a tight interaction between O₂ and CO₂ exchange that resides at the level of Hb in the red blood cell (RBC) (Jensen, 1989; Brauner and Randall, 1996, 1998; Brauner and Val, 1996; Nikinmaa, 2001).

Air breathing not only permits fishes to survive exposure to aquatic hypoxia but also allows them to maintain normal levels of metabolism and activity in aquatic hypoxia, provided O₂ taken up in the ABO is not subsequently lost across the gills. Consequently, many air‐breathing fishes possess circulatory adaptations in the gills. Of the four gill arches, efferent vessels from the third and fourth arches give rise to the pulmonary artery leading to the ABO, and venous return from the ABO is direct to the heart. The first and second gill arches lead exclusively to the dorsal aorta. The creation of a double circulatory loop is most developed in the obligate air‐breathing lungfishes but present to some degree in some of the other groups described below (reviewed in Graham, 1997). Those primitive fishes that are not air‐breathers tend to be tolerant of aerial exposure and/or aquatic hypoxia and thus are very tolerant of adverse environments. The following sections review the limited information that ex...

Table of contents

• Cover image
• Title page
• Table of Contents
• Living Primitive Fishes and Fishes From Deep Time
• Cardiovascular Systems in Primitive Fishes
• Nervous and Sensory Systems
• Ventilatory Systems
• Gas Transport and Exchange
• Ionic, Osmotic, and Nitrogenous Waste Regulation
• Locomotion in Primitive Fishes
• Peripheral Endocrine Glands. I. The Gastroenteropancreatic Endocrine System and the Thyroid Gland
• Peripheral Endocrine Glands. II. The Adrenal Glands and the Corpuscles of Stannius
• Why Have Primitive Fishes Survived?
• Series Editors
• Contributors to Volume 26
• Preface
• Index
• Contents of Previous Volumes