Physiology of Elasmobranch Fishes: Internal Processes

Robert E. Shadwick, Anthony Farrell, Colin Brauner, Anthony P. Farrell, Colin J. Brauner

• Publisher: Academic Press
• Year: 2015
• Print ISBN: 9780128012864
• eBook ISBN: 9780128014370
• Topic: Biological Sciences
• Subtopic: Marine Biology
• Index: Biological Sciences

Fish Physiology: Physiology of Elasmobranch Fishes, Volume 34B is a useful reference for fish physiologists, biologists, ecologists, and conservation biologists. Following an increase in research on elasmobranchs due to the plight of sharks in today's oceans, this volume compares elasmobranchs to other groups of fish, highlights areas of interest for future research, and offers perspective on future problems. Covering measurements and lab-and-field based studies of large pelagic sharks, this volume is a natural addition to the renowned Fish Physiology series.- Provides needed comprehensive content on the physiology of elasmobranchs- Offers a systems approach between structure and interaction with the environment and internal physiology- Contains contributions by leading experts in their respective fields, under the guidance of internationally recognized and highly respected editors- Highlights areas of interest for future research, including perspective on future problems

1

Elasmobranch Cardiovascular System

Richard W. Brill and N. Chin Lai

1. Introduction

2. Cardiovascular Function and Energetics

2.1. Oxygen Transport by the Cardiovascular System

2.2. Responses to Hypoxia

2.3. Elasmobranch Cardiac Anatomy

2.4. Cardiac Metabolic Biochemistry

3. Factors Controlling and Effecting Cardiovascular Function

3.1. Heart Rate and Stroke Volume

3.2. Body Fluid Volume and Blood Pressure Regulation

4. Signaling Mechanisms Effecting Blood Vessel Diameter

4.1. Gasotransmitters

4.2. Endothelins and Prostaglandins (Prostacyclin)

4.3. Autonomic Nervous System Signaling Mechanisms (Adrenaline and Noradrenaline)

4.4. Other Vascular Signaling Mechanisms (Acetylcholine, Adenosine, CNP, Serotonin, Vasoactive Intestinal Polypeptide, Bombesin, and Neuropeptide Y)

4.5. Substances Affecting Gill Blood Flow Patterns

5. The Action Potential and Excitation–Contraction (EC) Coupling in Elasmobranch Hearts: The Influences of Environmental, Biochemical, and Molecular Factors

5.1. The Action Potential

5.2. EC Coupling

5.3. Effects of Catecholamines and Acetylcholine

5.4. Effects of Temperature and Acidosis

6. Practical Applications: Physiology in the Service of Elasmobranch Conservation

6.1. Global Climate Change and Ocean Acidification

6.2. Surviving Interactions with Fishing Gear

7. Summary

The functional characteristics of elasmobranch and teleost cardiovascular systems are similar at routine metabolic rates. Differences do become apparent, however, in cardiovascular function of high-energy-demand species (e.g., mako shark and yellowfin or skipjack tunas) at maximum metabolic rates. Elasmobranchs have an autonomic nervous system separable into parasympathetic and sympathetic components. The vagus nerve has a major role in controlling heart rate, although sympathetic innervation of the heart and blood vessels is absent. Elasmobranchs increase cardiac output primarily by increasing stroke volume which, in turn, is primarily determined by ventricular end diastolic volume. End diastolic volume is determined by filling time and venous filling pressure; with the latter being effected by venous tone and venous capacitance. Blood volume and pressure in elasmobranchs are controlled by endocrine (e.g., renin-angiotensin, kallikrein-kinin, and natriuretic peptides) and paracrine (e.g., endothelins, prostaglandins, the gasotransmitters NO and H₂S,) mechanisms. Excitation-contraction (EC) coupling in elasmobranch hearts largely fits the accepted model for vertebrates, although the rise in cytoplasmic calcium is primarily from trans-sarcolemmal sources, which includes Na⁺-Ca²⁺ exchanger (NCX).

Some elasmobranchs populations are severely depleted due to the intersection of life history characteristics, unsustainable rates of fisheries-associated mortality, and environmental degradation. To address these issues effectively will require a better understanding of the elasmobranch cardiovascular physiology – including the ability of various species to withstand the physiological consequences of the increasing temperature and expanding hypoxic zones accompanying global climate change, and the severe acidosis and the plasma ionic imbalances resulting from interactions with fishing gear.

Keywords

Cardiac; heart; myocardium; shark

The functional characteristics of elasmobranch and teleost cardiovascular systems are similar at routine metabolic rates. Differences do become apparent, however, in cardiovascular function of high-energy-demand species (e.g., mako shark and yellowfin or skipjack tunas) at maximum metabolic rates. Elasmobranchs have an autonomic nervous system separable into parasympathetic and sympathetic components. The vagus nerve has a major role in controlling heart rate, although sympathetic innervation of the heart and blood vessels is absent. Elasmobranchs increase cardiac output primarily by increasing stroke volume which, in turn, is primarily determined by ventricular end diastolic volume. End diastolic volume is determined by filling time and venous filling pressure; with the latter being effected by venous tone and venous capacitance. Blood volume and pressure in elasmobranchs are controlled by endocrine (e.g., renin-angiotensin, kallikrein-kinin, and natriuretic peptides) and paracrine (e.g., endothelins, prostaglandins, the gasotransmitters NO and H₂S,) mechanisms. Excitation-contraction (EC) coupling in elasmobranch hearts largely fits the accepted model for vertebrates, although the rise in cytoplasmic calcium is primarily from trans-sarcolemmal sources, which includes Na⁺-Ca²⁺ exchanger (NCX).

Some elasmobranchs populations are severely depleted due to the intersection of life history characteristics, unsustainable rates of fisheries-associated mortality, and environmental degradation. To address these issues effectively will require a better understanding of the elasmobranch cardiovascular physiology – including the ability of various species to withstand the physiological consequences of the increasing temperature and expanding hypoxic zones accompanying global climate change, and the severe acidosis and the plasma ionic imbalances resulting from interactions with fishing gear.

1 Introduction

In this chapter we review recent advances in our understanding of cardiovascular physiology of elasmobranchs, but we specifically forego an extensive narrative on basic cardiovascular anatomy as detailed descriptions are available in earlier reviews (e.g., Butler and Metcalfe, 1988; Muñoz-Chápuli, 1999; Satchell, 1999; Tota, 1999). Rather this chapter centers on factors and mechanism affecting and controlling cardiovascular function, as well as the relationship of cardiovascular function to energetics, life style, and habitat. We also briefly review recent work that is applicable to elasmobranch conservation; specifically the relationship of cardiovascular function to the ability of various species to tolerate hypoxia and the effects of directional climate change, and to survive following capture and release from fishing gear.

The phylogenies of the cartilaginous fishes (class Chondrichthyes), and the subclasses Elasmobranchii (sharks and rays) and Holocephali (chimeras), are explained in detail by Klimley (2013) and Janvier and Pradel, (2015). In brief, the Elasmobranchii is separated into subgroups Selachii (sharks) and Batoidea (skates and rays), which show extraordinarily different body morphologies (e.g., the latter are dorso-ventrally flattened, have ventral gill slit openings, and pectoral fins fused to the side of the head forming wings). The modern sharks, in turn, are considered to have derived from two separate lineages: the squalomorphs (superorder Squalomorphi) and galeomorphs (superorder Galeomorphi), with the former considered the more primitive (Klimley, 2013). Since their major diversification in the Permian (∼250×10⁶ years ago), members of the Elasmobranchii have come to occupy almost all aquatic environments – from the surf zone of the continental shelves, to the brightly lighted surface water of the pelagic zone far from the continents, to abyssal depths (>3000 m), and even into freshwaters – and to occupy latitudes from the tropics to high Arctic (Klimley, 2013). Elasmobranchs also show a great diversity in life styles, life-histories, feeding strategies, energetics, etc. (Compagno, 1990). Given this great heterogeneity in gross body morphologies and ecologies, we contend that the cardiovascular systems of the ∼900–1000 extant species of cartilaginous fishes undoubtedly have a significant range in functional characteristics. Unfortunately, the functional properties of only a few elasmobranch species have been investigated, and these have largely been small, inshore, demersal species (e.g., catsharks, Scyliorhinus stellaris and S. canicula; epaulette shark, Hemiscyllium ocellatum; Port Jackson shark, Heterodontus portusjacksoni; eastern shovelnose ray, Aptychotrema rostrata; and spiny dogfish, Squalus acanthias and S. suckleyi). This situation occurs, in large measure, because studies on cardiovascular function generally require access to live specimens held in captivity, and species which are small enough to be easily and safely instrumented. As a result, our summary of cardiovascular function in elasmobranchs will largely rely on data from a relatively small number of generally inshore species that are primarily from temperate, and more occasionally from tropical, areas. We readily admit, therefore, that many of our conclusions may not be universally true for all extant elasmobranch species, but rather be applicable primarily to species sharing a recent common phylogeny, or those belonging to one of the ecomorphotype categories to which they can be assigned (Compagno, 1990).

2 Cardiovascular Function and Energetics

The rate at which the cardiovascular system d...

Table of contents

• Cover image
• Title page
• Table of Contents
• Copyright
• Contents of Physiology of Elasmobranch Fishes: Structure and Interaction with Environment, Volume 34A
• Contributors
• Preface
• List of Abbreviations
• 1. Elasmobranch Cardiovascular System
• 2. Control of Breathing in Elasmobranchs
• 3. Oxygen and Carbon Dioxide Transport in Elasmobranchs
• 4. Organic Osmolytes in Elasmobranchs
• 5. Regulation of Ions, Acid–Base, and Nitrogenous Wastes in Elasmobranchs
• 6. Feeding and Digestion in Elasmobranchs: Tying Diet and Physiology Together
• 7. Metabolism of Elasmobranchs (Jaws II)
• 8. Endocrine Systems in Elasmobranchs
• Index
• Other Volumes in the Fish Physiology Series