Locomotion, Volume 7: Locomotion (Fish Physiology)

FISH PHYSIOLOGY Volume VII Locomotion CONTRIBUTORS F. W. H. BEAMISH QUENTIN BONE C. C. LINDSEY WILLIAM R. DRIEDZIC ...

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FISH PHYSIOLOGY Volume VII Locomotion

CONTRIBUTORS F. W. H. BEAMISH QUENTIN BONE

C. C. LINDSEY

WILLIAM R. DRIEDZIC

WILLIAM H. NEILL

JOHN J. MAGNUSON

P. W. HOCHACHKA

DAVID J. RANDALL

DAVID R. JONES

E. DON STEVENS PAUL W. WEBB

FISH PHYSIOLOGY Edited by W. S. HOAR DEPARTMENT OF ZOOLOGY UNIVERSITY OF BRlTISH COLUMBIA VANCOUVER, CANADA

and

D. J. RANDALL DEPARTMENT OF ZOOLOGY UNIVERSITY OF BRlTJSH COLUMBIA VANCOUVER, CANADA

Volume VII

Locomotion

ACADEMIC PRESS New York San Francisco London 1978 A Subsidiary of Harcourt Brace Jovanovich, Publishers

COPYRIGHT 6 1978, BY ACADEMIC PRESS, INC. ALL RIGHTS RESERVED. NO PART OF THIS PUBLICATION MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM OR BY ANY MEANS. ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING, O R ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITING FROM THE PUBLISHER.

ACADEMIC PRESS, INC.

111 Fifth Avenue, New York. New York 10003

United Kingdom Edition published by ACADEMIC PRESS, INC. (LONDON) LTD.

24/28 Oval Road, London NW1

7DX

Library of Congress Cataloging in Publication Data Hoar, William Stewart, Date Fish physiology. Includes bibliographies. CONTENTS: v. 1. Excretion, ionic regulation, and metabolism.--v. 2. The endocrine system.--v. 3. Reproduction and growth, bioluminescence, pigments, and poisons. [etc.] 1. Fishes--Physiology. I. Randall, D. J., joint author. 11. Conte, Frank P., Date 111. Title. QL639.1.H6 597’.01 76-84233 ISBN 0-12-350407-4 ( V. 7 )

PRINTED IN THE UNITED STATES OF AMERICA

8182

9 8 7 6 5 4 3 2

CONTENTS ix

LIST OF CONTRIBUTORS

xi

PREFACE

TERMINOLOGY TO DESCRIBE

SWIMMING ACTIVITYIN

FISH

xiii xv

CONTENTS O F OTHER VOLUMES

1. Form, Function, and Locomotory Habits in Fish C. C . Lindsey I. Introduction 11. Early History of Studies on Fish Locomotion 111. Modes of Swimming IV. Nonswimming Locomotion V. Propulsive Anatomy VI. Locomotory Habits of Wild Fish References

1 5 8 39 46 75 88

2. Swimming Capacity F. W. H . Beamish I. Introduction 11. Field Measurements of Performance 111. Laboratory Measurements of Performance IV. Energetics of Swimming V. Application to Management Practices References

101 103 117 163 168 172

3. Hydrodynamics: Nonscombroid Fish Paul W. Webb 1. Introduction Steady Swimming Unsteady Propulsion Unsteady versus Steady Propulsion Mechanics of Median and Paired Fin Propulsion References

11. 111. IV. V.

V

190 191 22 1 228 230 232

CONTENTS

vi 4. Locomotion by Scombrid Fishes: Hydromechanics, Morphology, and Behavior John J . Magnuson 11. Observed Swimming Speeds 111. General Considerations of Swimming Equilibria

240 24 1 250

IV. height, Buoyancy, Hydrodynamic Lift, and Prediction of Sustained Speeds V. Resistance to Forward Movement VI. Thrust Production References

25 1 267 288 308

I. Introduction

5. Body Temperature Relations of Tunas, Especially Skipjack E . Don Stevens and William H. Neil1 I. Introduction 11. His tory 111. What Is the Real (i.e,,Typical) Excess Body Temperature of Tunas? IV. What Is the Heat Source Responsible for Large Excess Body Temperatures in Tunas? V. Anatomical Basis oif Warm-Bodiedness in Tunas VI . Exchange of Heat between Tunas and Their Environment VII. Do Tunas Regulate Their Body Temperature? VIII. Adaptive Values of Warm-Bodiedness and Large Thermal Inertia IX. Physiological Insights into the Natural History of Tunas X. Conclusion: A Thermocentric Overview of Tuna Evolution References

3 16 317 319 32 1 325 334 340 348 353 354 356

6. Locomotor Muscle Quentin Bone I. Introduction 11. The Organization of the Myotomes

111. IV. V. VI.

Fin Muscles Fiber Types Proprioception Fish Muscle and the Muscles of Higher Forms References

36 1 363 368 368 4 10 416 417

CONTENTS

vii

7. The Respiratory and Circulatory Systems during Exercise David R . Jones and David J . Randall I. General Introduction 11. Assessment of Exercise Performance 111. The Respiratory System during Exercise

IV. The Circulatory System during Exercise References

425 426 442 466 492

8. Metabolism in Fish during Exercise William R . Driedzic and P. W. Hochachku I. Introduction 11. Biochemical Insights from Respiratory Physiology

111. Red-White Muscle Differences I v. Metabolism of Adenylates and Related Compounds V. Carbohydrate Metabolism VI . Lipid Metabolism VII. Protein Metabolism VIII. Citric Acid Cycle References

503 504 505

507 517 525 530 533 536

AUTHOR INDEX

545

SYSTEMATICINDEX

56 1

SUBJECTINDEX

570

This Page Intentionally Left Blank

LIST OF CONTRIBUTORS Numbers in parentheses indicate the pages on which the authors’ contributions begin.

F. W. H. BEAMISH (101),Department of Zoology, University of Guelph, Guelph, Ontario N 1 G 2W1, Canada QUENTINBONE(361),The Marine Laboratory, Citadel Hill, Plymouth PLl 2PB, United Kingdom WILLIAMR. DRIEDZIC* (503),Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1W5, Canada

P. W. HOCHACHKA (503), Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1W5, Canada DAVIDR. JONES (425),Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1W5, Canada C. C. LINDSEY(11, The University of Manitoba, Department of Zoology, Dufi Roblin Building, Winnipeg, Manitoba R3T 2N2, Canada J. MAGNUSON(239),Laboratory of Limnology, Department of Zoology, University of Wisconsin-Madison, Madison, Wisconsin 53706

JOHN

WILLIAMH. NEILL (315),Department of Wildlife and Fisheries Sciences, Texas A G M University, College Station, Texas 77843

DAVIDJ. RANDALL (425), Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1W5, Canada E. DON STEVENS (315), Department of Zoology, University of Guelph, Guelph, Ontario N1 G 2W1, Canada PAULW. WEBB(189),The School of Natural Resources, The University of Michigan, Ann Arbor, Michigan 48104 * Present address: Department of Biology, Mount Allison University, Sackville, New Brunswick EOA 3C0, Canada. ix


PREFACE Locomotion in fish varies considerably, both quantitatively and qualitatively, between species and within species with age and environment. Only a few swimming modes in a small number of species have been examined in detail by a relatively small number of investigators. However, these studies, drawing on expertise from a variety of disciplines, have greatly increased our understanding of how fish move, and the flurry of activity is throwing some light on a previously confused and confusing field. This volume attempts to detai'1 ourpresent stage of understanding of fish locomotion. In order to clarify discussions, we have attempted to categorize some swimming activities in fish and hope that these categories will gain general acceptance. Neither the terms nor the groupings are new, but are drawn from already published work referred to in the text. The limitations of such a classification are that it tends to obscure variability and to present swimming activity as a series of discrete categories rather than a continuum. The contents of this volume reflect areas of study rather than a balanced report on all aspects of fish locomotion. For instance, the first chapter describes the variety of locomotor patterns in fish, and then swimming modes in trout and tuna are discussed in detail in two further chapters. This is not to imply that there is something very different about tuna and trout locomotion compared with that of other fishes, only that these modes have been studied in detail, whereas other modes of locomotion in fish have not. The neural control and generation of locomotor patterns are poorly understood in any vertebrate. I n fish, we are still at the stage of describing the types of nerve and muscle fibers present, how they are arranged and function to initiate and generate movements. There are only a few studies of the control of the respiratory and cardiovascular systems in fish during exercise and there are huge gaps in our understanding of these fields. The same can be said of metabolic changes associated with exercise. Each of these subjects is reviewed in an attempt to indicate areas of knowledge and regions of ignorance. A relatively small number of fish, in particular, tunas and lamnid sharks, are able to maintain muscle temperatures above ambient xi

xii

PREFACE

levels. These animals swim continuously utilizing the hot trunk muscle. This subject is reviewed as a special aspect of fish locomotion. Finally, many people advised and helped us in editing this text; in particular, the chapters were reviewed by many people other than ourselves. We are grateful for all help given. The result is a better text, more useful we hope, to those interested in fish locomotion. W. S. HOAR D. J. RANDALL

TERMINOLOGY TO DESCRIBE SWIMMING ACTIVITY IN FISH

Sustained Swimming: A spectrum of swimming activities and speeds that can be maintained for an indefinite period-in operational does not involve fatigue. terms for longer than 200 min-and Metabolism is aerobic and the activities would include foraging, station holding, schooling, cruising at preferred speeds in negatively buoyant fish, and steady swimming at low speeds, including migration. Burst Swimming: Rapid movements of short duration and high speed, maintained for less than 15 sec. Energy is made available largely through anaerobic processes. Burst activity may be subdivided into an acceleration period and a sprint, when swimming speed is high but steady. Prolonged Swimming: Covers a spectrum of speeds between burst and sustained and is often categorized by steady swimming with more vigorous efforts periodically. The swimming period lasts between 15 sec and 200 min and if maintained will end in fatigue. Energy is supplied from either or both aerobic and anaerobic processes. Fatigue: A fish is fatigued when it collapses and can no longer maintain a given swimming speed. Critical Swimming Speed, Ucrit:This is a useful operational term for comparing swimming speeds of different fish. Swimming speeds of individual fish of the same species but different swimming abilities, because of differing physiological states, can be compared b y expressing the swimming speed as %UCrit.In order to measure Ucritrfish are subjected to stepwise increases in swimming speed (usually in a water tunnel) until fatigue occurs. The critical swimming speed is computed from the maximum speed achieved.prior to fatigue. For instance, if a fish can maintain a swimming speed of 10 cm/sec for 60 min (the most usual duration for each step) but fatigues after 30 min at a swimming xiii

xiv

TERMINOLOGY TO DESCRIBE SWIMMING ACTIVITY IN FISH

speed 12 cm/sec, then the critical swimming speed is between 10 and 12 cm/sec and is computed as follows:

10

+ [(12 - 10) x

30/60] = 11 cm/sec

where 10 is the speed at the last completed step, (12 - 10) is the size of each step, and 30/60 is the time to fatigue at the last step divided b y the step duration. The duration and velocity increment of each step will influence the critical swimming speed obtained, and thus the step duration and velocity increment should be stated; for example, the 60 min, 5 cm/sec Ucritwas 20 cm/sec.

Steady uersus Unsteady Swimming: In many experiments using water tunnels or fish wheels, fish are trained to swim at a constant speed in one direction (steady swimming), whereas in their normal environment fish usually accelerate and change direction continually (unsteady swimming). Steady swimming is clearly more easily quantified and analyzed than unsteady swimming and so is used in experiments; however, caution must be used in applying conclusions based on the analysis of steady swimming to fish swimming in an unsteady manner. It is important to note, therefore, if the swimming is steady or unsteady. Thus burst, prolonged, and sustained swimming may contain either steady or unsteady components. The critical swimming speed can only b e measured for steady swimming. Fry (1971, pp. 3 and 4) has discussed the terms “standard,” routine,” and “active” levels of metabolism and the term “scope for activity” in his article “The Effect of Environmental Factors on the Physiology of Fish” in Fish Physiology, Volume VI. Standard metabolism is an approximation of the minimum metabolic rate for the intact organism. Routine metabolism, usually referring to aerobic metabolism and measured as oxygen uptake, refers to the metabolic rate when movements are restricted and the fish is protected from outside stimuli but is free to move and does so occasionally. Active metabolic rate refers to the oxygen uptake at the maximum sustained rate for a fish swimming steadily and is equivalent to oxygen uptake at the critical swimming speed. “

CONTENTS OF OTHER VOLUMES Volume I

The Body Compartments and the Distribution of Electrolytes W. N . Holmes and Edward M . Doraldson The Kidney Ckvelund P . Hickman, Jr., and Benjamin F . Trump Salt Secretion Frank P . Conte

The Effects of Salinity on the Eggs and Larvae of Teleosts F . G . T . Holliday Formation of Excretory Products Roy P . Forster and Leon Goldstein Intermediary Metabolism in Fishes P. W. Hochachka Nutrition, Digestion, and Energy Utilization Arthur M . Phillips, Jr. AUTHOR INDEX-SYSTEMATICINDEX-SUBj ~ c rINDEX Volume I1

The Pituitary Gland: Anatomy and Histophysiology J. N . Ball and Bridget I . Baker The Neurohypophysis A. M . Perks Prolactin (Fish Prolactin or Paralactin) and Growth Hormone J. N . Ball Thyroid Function and Its Control in Fishes Aubrey Gorbmun xv

CONTENTS OF OTHER VOLUMES

xvi

The Endocrine Pancreas August Epple The Adrenocortical Steroids, Adrenocorticotropin and the Corpuscles of Stannius I . Chester Jones, D . K. 0 . Chan, 1. W. Henderson, and J . N . Ball The Ultimobranchial Glands and Calcium Regulation D. Harold Copp Urophysis and Caudal Neurosecretory System Howard A. Bern AUTHOR INDEX-SYSTEMATICINDEX-SUB JECT INDEX Volume 111

Reproduction William S . Hoar Hormones and Reproductive Behavior in Fishes N. R. Liley Sex Differentiation Toki-o Y a m m o t o Development: Eggs and Larvae J. H . S . Blader Fish Cell and Tissue Culture Ken Wolf and hl. C . Quimby Chromatophores and Pigments Ryozo Fujii Bioluminescence J . A. C . Nicol Poisons and Venoms Findluy E . Russell AUTHOR INDEX-sYSTEM.4TIC

INDEX-SUBJECT

INDEX

Volume IV

Anatomy and Physiology of the Central Nervous System Jerald 1. Bernstein


The Pineal Organ James Clarke Fenwick Autonomic Nervous Systems Graeme Campbell The Circulatory System D. 1. Randall Acid-Base Balance C. Albers Properties of Fish Hemoglobins Austen Riggs Gas Exchange in Fish D. J. Randull The Regulation of Breathing G . Shelton Air Breathing in Fishes Kiell Johallsen The Swim Bladder as a Hydrostatic Organ Johan B. Steen Hydrostatic Pressure Malcolm S. Gordon Immunology of Fish John E. Cushing

AUTHORINDEX-SYSTEMATIC INDEX-SUBJECT INDEX Volume V Vision: Visual Pigments F . W . Munz Vision: Electrophysiology of the Retina T . Tomita Vision: The Experimental Analysis of Visua1,Behavior David lngb Chemoreception Toshiaki J. Hara

xvii

xviii


Temperature Receptors R . W. hlurray Sound Production and Detection William N . Tavolga The Labyrinth 0. Lowenstein The Lateral Organ Mechanoreceptors Ake Flock The Mauthner Cell J. Diamond Electric Organs h1. V. L. Bennett Electroreception M . V . L. Bennett

AUTHOR INDEX-SYSTEMATIC INDEX-SUB JEGT INDEX Volume VI The Effect of Environmental Factors on the Physiology of Fish F. E . J. Fry Biochemical Adaptation to the Environment P. W. Hochachka and G . N . Somero Freezing Resistance in Fishes Arthur L. DeVries Learning and Memory Henry Gleitman and Paul Rozin The Ethological Analysis of Fish Behavior Gerard P. Baerends Biological Rhythms Horst 0. Schwassmann Orientation and Fish Migration Arthur D . Hasler Special Techniques D . J . Randall and W. S. Hoar AUTHORINDEX-SYSTEMATIC INDEX-SUB JECT INDEX

FISH PHYSIOLOGY Volume VII Locomotion


1 FORM. FUNCTION. AND LOCOMOTORY HABITS IN FISH

.

C . C LZNDSEY I . Introduction ................................................... I1 . Early History of Studies on Fish Locomotion .................... 111. Modes of Swimming ...........................................

A . Nomenclature of Modes ..................................... B . Propulsion by Body and/or Caudal Fin ....................... C Propulsion by Undulation of Median or Pectoral Fins ......... D. Propulsion by Oscillation of Median or Pectoral Fins .........

.

IV. Nonswimming Locomotion ...................................... A . Jet Propulsion ............ ........ ............... B . Terrestrial Locomotion . . . . ............................. C . Moving on the Bottom and Burrowing ... D . Jumping, Gliding, and Flying ................................ V. Propulsive Anatomy ......... ................................ A . Trunk ......................................................

...........................................

Wild Fish ................................. A . Records of Long Distance Movements ........................ B . Short-Term Components of Long-Term Movements . . . . . . . . . . . C Activity Cycles in Wild Fish ................................. D . Schooling .................................................. E . Some Pitfalls in Locomotory Studies ......................... References .......... ............................................

.

1 5

8 8 11 26 37 39 39 40

43 46 46 62 75 75 80 83 85 87 88

.

I INTRODUCTION A fish moving through water is constrained by physical forces quite different from those affecting an animal moving on land or through the air . Some of the problems facing fish may be appreciated by examining the favorable and unfavorable features of water. in contrast to those of land or air. as a medium for locomotion . Most fish swim by pushing back against the water with undulations of their body or their fins . Water is unfavorable in that it presents a 1 FISH PHYSIOLOGY. VOL. V1I Copyright @ 1978 by Academic Press. Inc . All rights of reproduction in any fonn reserved . ISBN 0-12-350407-4

2

C . C. LINDSEY

yielding medium against which to push, and much energy may be wasted in’making profitless eddies. Water is favorable in that it offers little drag from friction, but drag of another sort, d u e to inertial forces (“pressure drag”), is high, because water is so dense. At the same time, the density of water makes it a very favorable medium in which to live because it buoys up the body of an organism. Fish do not require strong internal structures to carry their weight, in contrast to land animals which are severely limited b y their need for structural support. Also because of the buoyancy of water, work to keep from failing is minimal. Compared with terrestrial life, fish need expend little energy to move vertically. Because liquids are almost incompressible, pressure is not usually a problem to fish, except that it constrains the rapid vertical movements of any species carrying a chamber of compressible gas. In contrast to animals underwater, those inhabiting the air live in an insubstantial medium even more yielding than water. Hence most terrestrial animals perform their locomotion by pushing against the earth rather than against the air. The ground is a medium with almost no “give,” so that little energy is lost by imparting waste motion to the soil, and all goes into forward momentum of the animal. But, because frictional drag is very great, few animals can glide rapidly over (or within) the earth‘s surface. (Despite the give of water, fish can swim faster in water than snakes can crawl over the ground.) Most terrestrial animals have abandoned fishlike techniques of propulsion; instead they “walk,” taking advantage of the frictional forces and resistance of the ground to provide thrust for the limbs, and of the negligible drag of the air to allow forward progression of the body and the individual limbs. Walking is an inappropriate technique for attaining speed underwater, as is apparent to a human who tries to run while partly immersed. Many aquatic invertebrates which are heavier than water do walk slowly on the bottom, but to attain speed they must leave the bottom and swim. Few species of fish walk on the bottom underwater with their paired limbs. On the other hand, those fish which make excursions out onto land usually have to resort to walking or skipping in some fashion, since the air provides so insubstantial a medium against which their usual body undulations can act. Proof of this is the observation that a live fish on a slippery deck flaps futilely without achieving forward progression, even though the same muscular undulations performed underwater would have propelled it swiftly forward. Eels can progress overland through grass or on rough ground, but here the body

1. FORM, FUNCTION,

AND LOCOMOTORY HABITS

3

undulations are thrusting against the ground, not the air; the eel is not swimming through the air, but is crawling like a snake. Just as the fastest aquatic animals abandon the bottom and swim through the water, so the fastest terrestrial animals leave the ground and fly through the air. Roughly half the living species of animals can fly. Most are small animals (insects),in which the surface area for lift is great relative to the weight. For them the viscosity of the medium is important relative to its inertia (i-e., they operate at low Reynolds numbers, as explained in Chapter 3). Their physical constraints are therefore in some ways comparable to those of larval fish and other small animals underwater. One feature of locomotion under such conditions is that stopping and starting are no problem; when viscosity is dominant a flying insect or swimming fish larva stops as soon as it ceases to propel itself, and begins to move at full speed with negligible time-lag as soon as the propulsive movements begin (Lighthill, 1969). The larger flying species (birds and bats) on the other hand, operate with speeds and dimensions where the viscous forces are less significant; to them, as to larger fish, the inertial forces of the medium are dominant (although the absolute values are very different in water and in air). To these animals, extra energy is required to accelerate the body from rest; conversely a moving bird or large fish, if well streamlined, can glide a long way after it ceases propulsive movements. Gravity, which is of minor concern underwater, is a major factor in air. To birds supporting themselves in the air, a severe constraint is weight. Extreme structural economies (such as hollow bones and feathers) are needed to minimize the effects of gravity in a large flying animal. Underwater, some of the midwater fishes which lack gas chambers display comparable weight economies (such as reduced skeleton, and substitution of light fatty tissues wherever possible). Fish can thereby achieve neutral buoyancy in water. But in air the density of the medium is so slight that even the most lightly built bird still weighs much more than the air it displaces. No animal has attained neutral buoyancy in air, although this should be theoretically possible through development of a large bladder of hydrogen or other light gas. In water, on the other hand, “weightlessness” is relatively easy to attain, by inclusion of a small gas chamber which displaces an equivalent volume (and 800 times the weight) of water. The majority of bony fish (but not sharks) have such a gas chamber; to them, structural weight economies are not necessary. Animals flying through air are like winged aircraft; they must divert part of their locomotory effort into lift to overcome gravity. Neutrally

4

C . C . LINDSEY

buoyant fish in water are like dirigibles; they can concentrate all their effort into forward thrust. Only in sharks, rays, tunas, and other fish which may lack a gas chamber does lift become important, and so their locomotion through water has some features in common with the flight of birds or aircraft. Most of the few fish which are capable of brief aerial locomotion progress through the air by passive gliding rather than by flying (and swim underwater by conventional body undulations). They are comparable to those restricted groups of mammals, amphibians, and reptiles which can glide but which are not primarily adapted to this mode of locomotion. Only very few fish (includingthe Gasteropelecidae, and Pantodon) can fly in air by beating their wings, and this they d o ineptly. The formidable problems of simultaneous adaptations for locomotion both in midair and underwater have been overcome, among the vertebrates, only by diving birds such as loons. Among the invertebrates a few types of insects (including water beetles and some bugs) can swim underwater and fly in air in the same life history stage. Most which can move effectively in both media do so at two radically different life history stages (e.g., dragonfly nymph and adult). Another set of locomotory constraints arising from properties of water are those factors determining the oxygen available to the propulsive system. Water contains only about one-thirtieth as much oxygen as does an equal volume of air. Water is also much heavier and more viscous to move. To meet these problems, fish have a flow-through respiratory system which extracts a high proportion of the available oxygen. This is achieved without undue expansion of the respiratory surface, which in tunas is about the same as that in terrestrial vertebrates of equivalent weight, and in other fish is smaller. A very large gill area would present too great a drag, apart from allowing excessive ion exchange (a nonexistent problem in terrestrial lungs). But even with its highly efficient countercurrent design and moderate gill area, the energy expenditure for gill ventilation in an active fish may amount to about one-tenth of its total metabolic output. In contrast, an active man probably uses no more than 3% of his total oxygen consumption for breathing. Some fish species move the water over the gills with their branchial muscles. Others simply swim with their mouths open, in which case their drag is increased and the energy for gill ventilation must come from additional work by the propulsive body muscles. The proportion of the total energy output used for ventilation is probably less in small than in large fish. This is just one of many ways in which

1. FORM, FUNCTION, AND LOCOMOTORY HABITS

5

physical constraints of the environment operate differently on small and on large fish. An elegant survey of aquatic animal propulsion (including many major groups omitted above) is given by Lighthill (1969),whose view is that of an aerodynamicist. Other insights into the locomotory problems in different media are to be found throughout the works of Alexander (1967, 1968, 1971), Gray (1968 and earlier), Schmidt-Nielsen ( 1972a,b), and Tucker (1975).

11. EARLY HISTORY OF STUDIES ON FISH LOCOMOTION Few of the features of fish locomotion are evident to the naked eye. The usual method of locomotion in fish is now thought to depend on passing alternating waves of contraction backward along the body muscles. Thrust against the water either is generated by the sides of the body pushing obliquely backward (as in a swimming eel), or else has become progressively more concentrated in the tail fin (as in fast swimmers such as the tuna). The paired fins seem to contribute little in conventional forward swimming, and are reserved for maneuvering. Not only are these points difficult to discern by direct observation; they also do not follow by logical extension from the locomotory habits of terrestrial animals. Consequently, the historical development of opinions on fish locomotion has been marked by contradictions and controversies. In the fourth century B.C., Aristotle referred to fish locomotion in various passages in his three works “Parts of Animals,” “Movement of Animals,” and “Progression of Animals.” H e wrote that fish with very long bodies and no paired fins, such as the moray, move along by an undulating motion of the body; “that is, they use the water just as serpents use the ground.” He made the acute observation that eels move in the same way in water and on land but with fewer bends in the former medium (a hydrodynamic explanation for which might only now be attempted). Aristotle anticipated Newton by 20 centuries in his statement that there must always be something “immovable” outside an animal “supported upon which that which moves moves. F i r if that which supports the animal is to be always giving way . . . there will be no progress, that is, no walking unless the ground were to remain still, and flying or swimming unless the air or sea were to offer resistance.” Aristotle fell short of an understanding of undulatory locomotion in that he did not perceive that the crests of the body waves pass backward, and he tried to draw an analogy between a

6

C . C. LINDSEY

snake’s motion and the walking of quadrupeds. He correctly described a ray as swimming by means of the edges of its flattened disc. He was apparently wrong with respect to the locomotion of most fishes, as he thought that the two pairs of fins were their principal means of propulsion. He suggested that the caudal fin was primarily for steering. The ancient Hindu medical work Susruta-samhita probably reached its final form in the early years A.D., but it may contain components which predate Aristotle. According to the free translation by Hora (1935), it suggests a correlation between body form, habitat, and locomotion in some freshwater fishes; river fish are said to be bulky in the middle because they move with their head and tail; pool fish, having little space to move about, are deep-bodied; torrent fish are flattened because they crawl with their chests on the bottom. The first attempts at mechanical analysis of fish locomotion were by Borelli, a disciple of Galileo, who in 1680 published a diagram of a fish swimming b y sweeping its caudal fin and peduncle side-to-side in an arc (reproduced in Gray, 1968). Borelli thought of the tail fin as operating like an oar sculled behind a boat. He dispelled the notion of Aristotle that the paired fins when present are the main locomotory organs, stating they are held at the sides during swimming; Borelli pointed out also that the muscles of the body, which provide power for the tail strokes, are large in proportion to those of the paired fins. He outlined the role of the gas bladder in controlling the specific gravity and hence the position of the fish in the water. He departed from observation, however, when he described the tail as operating like a frog’s foot, contracted during a “preparatory” outward sweep and expanded during a powerful inward propulsive sweep. Two fundamental points he made, which display the influence of Galileo, were: (1) the fish cannot move its tail without also moving its body, and (2) the force moving the fish forward is due to resistance of the water against the surface of the moving tail. Pettigrew ( 1874) challenged Borelli’s view that forward motion could result simply by lashing the tail from side to side. He argued that moving the tail from the midline outward during the “preparatory” sweep would produce a backward movement of the whole. Breder (1926) comments “His logic would seem to be correct, but that he was in error has been positively demonstrated by the construction of a model.” (Breder built a model boat, which did swim forward simply by means of an oscillating rigid tail vane.) What Pettigrew overlooked was that the outward sweep of the tail, on a fish or on a boat, does not move the whole backward; instead, it swings the main body (ahead of the joint) slightly in a sidewise arc opposite to that of the tail. The subsequent inward stroke moves the whole forward as

1. FORM, FUNCTION,

AND LOCOMOTORY HABITS

7

well as swinging the body back into line. Pettigrew invoked complex rolling motions of the fish to overcome his supposed difficulty. Breder ( 1926) attacked Pettigrew enthusiastically for these and other “absurdities,” and complained that uncritical paraphrasing of Pettigrew’s views by Bridge (1904) in the Cambridge Natural History has given them undeserved circulation. However, Pettigrew did observe that fish throw their bodies into a double or sigmoid curve rather than into the simple arc described by Borelli (although he believed this must occur in all fish, which it does not). Pettigrew correctly observed that the tail tip of a slowly moving sturgeon described a figure-8 when viewed from above. He implied that this was an adaptation for efficient propulsion; Gray (1933a) showed it to be the inevitable result of the propagation of a wave of curvature along any inextensible body. The possibility of precise observation on locomotion dates from Marey’s (1895) use of cinematography. He produced sequential photographs of swimming fish, a technique since widely emulated. His pictures demonstrated that waves of curvature pass along the length of the body. Unfortunately, his Fig. 199 of a swimming conger eel shows one in which the body undulations are either stationary or are slowly movingforward relative to the water, so that the fish must actually have been slowing down when it was photographed. Since Marey did not attempt to analyze the forces involved in swimming, he missed the fact that this was an unhappily chosen figure to illustrate swimming. Although Gray (1933b)drew attention in a footnote to the aberration, Marey’s figure has been widely copied. It still appears in the third edition of Norman and Greenwood’s (1975) otherwise admirable text. [Nikolsky’s (1963) text does not make this mistake, but it does use as an illustration of locomotion (his Fig. 32) a sequence from Gray (1933a) which actually shows an eel swimming backward.] Notwithstanding, Marey provided a strong incentive for studies on fish locomotion, and inspired later experimental studies in France by Houssay (1912), who tried to measure the thrust and drag of fish, and by Magnan (1929, 1930). Dean (1895) reproduced one of Marey’s illustrations showing the wave form in a swimming eel. Dean explicitly stated “It is the pressure of the fish’s body against the water enclosed in these incurved places which causes the forward movement.” In an outstanding synthesis called “The Locomotion of Fishes,” Breder (1926)gave an extensive treatment of the mechanical principles, as well as a systematic description of locomotion in different fish groups. Breder concluded that “All the movements of fishes when swimming (except exhalation) are fundamentally of an undulatory muscular nature even though obscured by various specializations, and are induced

8

C. C. LINDSEY

by the serial action of metameral muscles.” H e categorized the types of movement of the body and of the fins, and coined many of the terms (e.g., Anguilliform, Carangiform) now in use. Th dominant figure in marrying precise measurement of moving animals with mathematical analysis has been Sir James Gray. The wide-ranging curiosity of Gray and his colleagues, notably H. W. Lissmann, has been brought to bear dn the locomotion of large vertebrates, and of sperm, and of most groups in between. In a series of papers starting in 1933 Gray analyzed photographs to show how undulatory swimming movements generate thrust. Gray (1936b) compared the calculated drag of a swimming dolphin with the calculated power output of its muscles, and concluded that dolphins (and some fish) are observed to swim at speeds which according to theory are impossibly fast. This famous “Gray’s Paradox” has stimulated much research and controversy ever since. In trying to balance the equation, some have sought improved measures of the muscular power output. Some have recorded much more precise observations on swimming fish [notably Bainbridge (1958 and later) using an ingenious “fish wheel”]. Some have looked for drag-reducing mechanisms. Most important, some have questioned the assumption that drag of a swimming fish could be equated to that of a rigid body or model. Some tried to measure the drag on actual fish, but their measurements seemed only to add to the growing confusion. Sir Geoffrey Taylor (1952), and Sir James Lighthill (1960), proposed mathematical models which might allow calculation of the drag of a swimming fish. Newer “bulk momentum” models concentrate attention on the kinematics of the trailing edge of the tail throughout one propulsive cycle, from which they attempt to calculate the thrust and power which must have been generated. Their significance is described in Webb’s (1975) publication, which is itself an important bridge across the communication gap between biologists and physical scientists. Recently DuBois et al. (1974) implanted pressure sensors at various points on the surface of live and of dead fish in a water tunnel. Webb (1975; see also Chapter 3) brings up to date the developments in fish hydrodynamics and energetics. One might summarize that the gap between the swimming fish and the scientists is closing, but the fish is still well ahead.

111. MODES OF SWIMMING A. Nomenclature of Modes

The different types, or modes, of propulsive movements of fish were classified by Breder (1926), whose nomenclature, somewhat ex-

1. FORM, FUNCTION, AND LOCOMOTORY HABITS

9

panded,, is followed here. Examples of fish displaying these modes are shown in Fig. 1. As Breder stated, the suffix “-form” (e.g., in anguilliform) refers to the types of movement and not to the body forms, and is therefore not strictly parallel to words such as “fusiform.” Indeed,

Fig. 1. Modes of forward swimming in fish, arranged along the vertical axis according to the propulsive contributions of body and fins (indicated by density of shading), and along the horizontal axis according to a scale running from serpentine undulation (more than one wavelength present) to oscillation (a rigid wigwag or fanlike motion). Species illustrated are: (A) Anguilla anguilla, (B) Squalus acanthias, (C) Cadus morhua, (D) Salmo gairdneri, (E) Caranx hippos, (F) Clupea harengus, ( G ) Zsurus glaucus, (H) Thunnus albacares, (I) Ostracion tuberculatum, (J)Amia calua, (K) Gymnotus carapo, (L) Balistes capriscus, (M) Lagocephalus laeuigatus, (N) Raja undulata, (0)Diodon holocanthus, and (P) Cymatogaster aggregata.

10

C. C. LINDSEY

one fish may show more than one mode of swimming, as in the surfperch Cymatogaster aggregata, which usually swims with its pectoral fins (labriform mode) but switches to caudal fin locomotion (carangiform mode) at high speeds (Webb, 197313). Breder (1926), Bainbridge (1963), and Webb (1975)have stressed that these classifications refer to average types within an essentially continuous range of swimming modes, and should not be applied too rigorously. Use of Breder's nomenclature in the following discussion and in Fig. 1 is simply for convenience. The arrangement of swimming modes implies no evolutionary or taxonomic affinities; clearly there has often been functional convergence on one swimming mode by taxonomically remote groups (e.g., locomotion is anguilliform both in lampreys and in blennies). The rationale for a classification according to propulsive mode is that similar hydrodynamic analysis may be applicable to animals which swim in the same way, regardless of diverse phyletic origins. In a swimming eel, most of the body is bent into backward-moving waves, whose amplitude is quite wide over the whole body length (Fig. 2A). In progressively shorter, thicker fish, propulsive waves tend to be increasingly concentrated in the tail region, so that only about half a wavelength is visible, and its amplitude rises rapidly in the

\'

\\

'!\\\

Fig. 2. Gradation of swimming modes from (A) anguilliform, through (B) subcarangiform, and (C) carangiform, to (D) thunniform. The black silhouette (dorsal view) is superimposed on successive positions one-half tail beat earlier (broken outline) and one-half tail beat later (stippled). (A) Anguilla anguilla, 7 em long, about 1.5 beatskec. (B) Gadus rnerlangus, 24 cm long, about 1.7 beatdsec. (C) Scornber scombrus, 40 ern long, about 2.4 beatdsec. (D)Euthynnus ajinis, length unknown, perhaps about 40 em, about 2.4 beats/sec. A, B, and C based on Gray (1933a, 1968); D based on Fierstine and Walters (1968).

1.

FORM, FUNCTION, AND LOCOMOTORY HABITS

11

region of the tail base (Fig. 2B, C). This propulsive mode reaches its climax in the very swift mackerels and tunas that appear to the naked eye to swim by moving only the caudal fin (Fig. 2D). A few species like the boxfish Ostrucion have totally inflexible bodies which cannot be thrown into a wave; they swim by oscillating the caudal fin back and forth like a fan or pendulum. This gradation from multi-waved undulation, through progressive and eventually exclusive concentration of propulsive movement in a pendulumlike oscillation, can be seen not only in the body but also in the median and paired fins. The nomenclature “anguilliformcarangiform-ostraciiform” was used by Breder (1926) as a scale to refer to flexures in the dorsal, anal, and pectoral fins as well as in the whole body, although he coined additional names for the swimming modes which involve the fins. A comparable “undulation-oscillation” scale is used in Fig. 1. The modes of swimming dealt with in this section refer to straightforward horizontal motion in still water while free from contact with any solid. They therefore omit accelerating, turning, rising, stopping, and other maneuvers which may be vitally important components of locomotion. Nonswimming movements such as burrowing, creeping, jumping, and flying are dealt with in Section IV, as is jet propulsion. A somewhat different analysis of locomotion types was presented by Kramer (1960).He grouped fish into ten categories using combinations of the swimming characteristics: use of trunk versus median or paired fin muscles; straight versus curving path; adaptation for high sustained speed versus rapid acceleration; inclination of fin axes on the body. Fish were also categorized according to ecological types: fast swimmers, roamers, swimmers between obstacles, slow and precise maneuverers, and bottom resters. Kramer proposed no nomenclature for his swimming modes.

B. Propulsion by Body and/or Caudal Fin

1. CLASSIFICATION

The classification of modes of propulsion by the body or tail has since been somewhat expanded from that designed by Breder (1926), but nomenclature has not been uniform. Table I shows the apparent equivalence between terms used by different authors. The two extremes of the spectrum “anguilliform” and “ostraciiform” have been used consistently. Breder’s intermediate term “carangiform” covers a

C. C. LINDSEY

12 Table I

Classification by Various Authors of Methods of Fish Propulsion Involving the Body and/or Caudal Fin Breder (1926)

Bainbridge (1961)

Marshall (1971)”

Anguilliform Carangiform

Anguilliform More anguilliform carangiform Carangiform More ostraciiform carangiform Ostraciiform

Anguilliform Subanguilliform

Anguilliform Subcarangiform

Anguilliform Subcarangiform

Fusiform Thunniform

Carangiform Carangiform with lunate tail Ostraciform

Carangiform Thunnifom

Carangiform Carangiform Ostraciiform

Webb (1975)

Present

Ostraciiform

Marshall did not propose a formal classification, but used these terms in his text.

wide range of swimming patterns, which are now suspected to require more than one hydrodynamic model (Lighthill, 1969). Hence three “ terms, subcarangiform,” “carangiform,” and “thunniform,” will be used, the latter as a more convenient substitute for “carangiform with large lunate tail” (Lighthill, 1969) or “carangiform mode with semilunate taiI” (Webb, 1975). Some characteristics of each of these propulsive modes are given in Table 11, and examples of taxonomic groups in which some (but not necessarily all) members use that mode.

2. ANGUILLIFORMMODE Anguilliform is a purely undulatory mode of swimming, in which most or all of the length of the body participates. The side-to-side amplitude of the wave is relatively large along the whole body, and it increases toward the tail. The body is long and thin; in eels it may be nearly cylindrical anteriorly, and somewhat laterally compressed toward the posterior. The caudal fin is often small, or even absent. Figure 2A shows three successive positions of a swimming eel Anguilla, after which the mode is named. It must not be supposed from these outlines that there are fixed pivots of nodes around which the body sections oscillate. The manner in which the waves of contraction move smoothly backward is better illustrated in the successive outlines of a swimming herring larva in Fig. 3. Each wave is generated by contractions of the body muscles in a few anterior segments on one side of the vertebral column, while those on the opposite side are relaxed and are slightly stretched. The resultant bending of the body toward the contracted side passes backward as the wave of muscle

Table I1 Comparison of Swimming Modes Involving the Body and/or the Caudal Fin Anguilliform mode

Subcarangiform mode

Wave length Body length

Short, always 0.5, usually > 1.0 Large along whole body. Anguilla max. 0.36, Clupea larva max. 0.46 Long thin. Anterior cylindrical, posterior compressed

Uusually 15

10

15

Comments

References

Hook and line Hook and line Hook and line Timed over measured distance (swimming tunnel) Timed over measured distance (fishway) Timed over measured distance (swimming tunnel) Annular trough Annular trough Timed over measured distance (swimming tunnel) Timed over measured distance (fishway) Timed over measured distance (fishway) Distance covered by one tailbeat Annular trough Annular trough Timed over measured distance (fishway) Annular trough

Gero (1952) Gero ( 1952) Lane (1941) Blaxter and Dickson (1959) Weaver (1965) Blaxter and Dickson (1959) Boy= ( 1961) Boyar (1961) Blaxter and Dickson (1959) Dow ( 1962) Stringham (1924) Komarov (1971) Paulik and DeLacy (1957) Paulik and DeLacy (1957) Weaver (1963) Paulik and D e h c y (1957) Napier (1914)' Weaver ( 1963) Denil ( 1937) Lane (1941) Paulik and DeLacy (1957) Weaver (1963) Webb (personal communication) Webb (personal communication) Bainbridge (1960) Bainbridge (1960) Denil (1909) Lavollee ( 1902)' Denil ( 1937) Lane (1941) Blaxter and Dickson (1959) Peterson (1974) Neil1 et al. (personal communication) Lane (1941) Stringham (1924) Blaxter and Dickson (1959) Bainbridge (1960) Bainbridge ( 1960) Komarov (1971) Komarov (1971) Komarov (1971) Regnard (1893) Komarov (1971) Lane (1941) Bainbridge (1960) Bainbridge (1960) Lane (1941) Komarov (1971) Wales (1950) Blaxter and Dickson ( 1959) Blaxter and Dickson ( 1959) Blaxter and Dickson (1959) Blaxter and Dickson ( 1959) Komarov (1971)

Timed over measured distance (fishway)

7

Hook and line Annular trough Timed over measured distance (fishway)

14 14

Annular trough Annular trough

10-15 15 25

Timed Over measured distance (fishway) Timed over measured distance (swimming tunnel) Swimming tunnel Timed over measured distance (annular tank) Hook and line

< 10.0 14 14

14 14

11.5-17.0 9.5-12.0 9.0-17.0 9.0-12.0

Timed over measured distance (swimming tunnel) Annular trough Annular trough Distance covered by one tailbeat Distance covered by one tailbeat Distance covered by one tailbeat Annular trough Distance covered by one tailbeat Tank observation Annular trough Annular trough Tank observation Distance covered by one tailbeat Timed over measured distance (culvert) Timed over measured distance (swimming tunnel) Timed over measured distance (swimming tunnel) Timed over measured distance (swimming tunnel) Timed over measured distance (swimming tunnel) Distance covered by one tailbeat

(Continued) 119

120

F. W. H. BEAMISH Table IVVelocity Specie3

Zoarces uilii parous Gasterosteus spinarhiu Potnicrops itajora Serrunus seribo Gyintiocephalus cernua Lepomis cyanellus Leponiio cyanellus Micropterus Percu Perca fluoiatilis Pornatornus salatrir Trachura mediterraneus pontious Spicara smoris Mullus barbatus pontious Creilahrus tinca Mugil curatus Mugil saliens Sphyroena barracuda Pholis gunnelus Gobius minutus Acauthocybium solanderi Acanthocyhium solanderi Scomber scomhrus Thuuricis albacores Thunnus alhucures Thunnus thynnus Istiophorus Trigla ~ p p . Pleuronectes flesus Pleurouectes microcephalus Pleuronectes platesea Pleuronectes platesea "

Number 1

1 1

Length (cm)

6.4 10.0 -

18.5 10.5

x 8

2 1 2 3 13 I 5 1 1

2 1 14I 6

11.5 16.0 15.7 17.0 11.8 15.0 24.0 1R.5 121-130 10 6.5 92-113 113.1 33.0-38.0 53-98 98 147

IR.O 27.5 8.0 0.7-1.0 6.0-15.0

cni sec-'

la21 72 174 227 133 10-70 10-150

145 204 258 235 109 107 442 400 1220 30 27 1204-2 140

2082

P sec-'

2.u-3.3 7.2 -

2-5 2-5

-

12.3 12.7 1.3-8.8 1.3-18.8

3.0 10-20 2.,%3.0 10-20 Gradually to prescribed velocity Gradually to prescribed velocity

~~

Swimming time at iiiarimum velocity (min)

10 10 10 1 1-120 1-17

5 5 5 5

5

10 10 10

5 5 5 5 5

5

>300 2300 66 21 6 10

60 1

10 10

20

34.1

3 3 3 3 3 '3 3

Tunnel swimming chamber.

', Oval or iiiinular swimming chamber. *Towed .;winlining cage.

146

30 30 30 30 60 30 15

30 30 30 30 60 30 15

VI Speeds of Fish Temperature ("C)

Maximum velocity cm sec-'

t sec-I

16.633.6 16.F34.7 24.2-41.3 75 91-143 36.6 97.5 14.9-26.5 22.0-35.4 25..>37.5 30.5-41.2 28.4 :10-49 49-55 2.3-55 28-64 22.9-34.3 19.8-29.7 14.3 22.9 26.8-43.3 02.C46.4 27.1 21.7 46.4 51.1 53.6 55.4 66.2 40 23-67 29-53 2,3-53 19-73 30-70 48-70 25.1-43.3 13.7-34.3 170 70-100 50-76

0.9-1.2

82

34.7 37.4 47.6 49.5 48.2 48.9 55.9

0.!L1.2 1.1-1.7 2.5 5.4-6.0 2.3-5.3 4.8-7.6 3.0-3.2 3.9-4.5 4.2-4.4 4.65.4 4.5

3.S7.8

Acclimation

Experimental

5 10 15

5 10 15

3.6

4.0 4.4 4.8 10.5

Endurance Endurance

5-6

5-6

10

10 15 20 24 10 15 20 20

15 20 24 10 15 20 20

1 6

1 6

10 15 20 24 15 15 15 15 15

10 15 20 24 15 15 15 15 15 [221

11.5 15 1Y.5

11.5 15 19.5 ,!&I5 15

s 1.5 1.S3.5 55-6.4

15

3.90 4.67 4.82 4.6 4.8 5.I

1-14 15

1-14 15

15 15

15 15 15 15 15 15 15

15 15 15 15

15

Endurance. 20%; O,, .%I9 mglliter 3-19 mglliter Endurance, 20%; 0,. Endurance, 20%,0%. .>I9 muliter O,, 2-26 muliter; CO,, 1-120 mglliter Control Infected; Notiophyetus siilniincolo

Endurance, 50% fatigue Endurance, 50% fatigue Endurance, 50% fatigue Endurance, 50% fatigue Endurance, 50% htigue Endurance, 50% fatigue Endurance, 20% Fatigue; O,, 2-10 mgiliter Endurance. 20% fatigue; 4, 2-10 mglliter Endurance, 20% fatigue; O,, 2-10 mglliter Salinity, 0-30% 02,2.0-2.3 inyiliter

10

10

18-19 18-19

8.5 3-4 2.1-3.2 2.7 3.50

Endurance Endurance Endurance

12

1.4-5.6 1.45.6

18-19 18-19 2.3 3.5 4.3-2.8 3.3-4.6 3.7 2.9 3.2

Comments

Control Infected; Nanophyetus sulrniricola Photography Salinity, @GO% 0,. 3.8-5.0mgiliter Exposure to 1.5mglliter fenitrothion Exposure to 0.5 mglliter fenitrothion Exposure to 0.15 mglliter fenitrothion 0 fenitrothion Metabolism Metabolism Metabolism

Reference Beamish (1974)" Beamish ( 1974)" Beamish (1974)" Magnan (1929) Brawn (1960)' Boyer (196Ub Boyer ( 1961)b Brett et al. ( 1958)' Brett et al. (1958)' Brett et a/. ( 1958)' Brett et al. (1958Ib Brett et al. ( 1958)b Davis et ul. (1963)" Davis et al. (1963)" Davis et al. ( 1963)" Dahlberg et al. (19SaP Butler and Milleman (1971)" Butler and Milleman (1971)" Brett et al. ( 1958)' Brett et al. ( 1958)' Brett et al. (1958)' Brett et al. ( 1958Ib Brett et al. (1958)' Brett et al. (1958)' Brett et al. (1958)b Brett et a/. ( 1958)b Brett et ul. (1958)b Brett et al. (1958)' Brett et 01. (1958)' Kerr (1953)" Davis et a / . (1963)" Davis et al. (1963)" Davis et al. (1963)" Rao ( 1968)" Kutty ( 1968)" Fry and Cox ( 1970)' Butler and Millemail (1971)" Butler and Milleman (1971)" Gray (1953) Byrne et al. (1972)" Kutty and Saunders (1973)" Magnan (1929) Peterson (1974) Peterson (1974) Peterson (1974) Peterson ( 1974) Peterson ( 1974)" Peterson (1974)" Peterson (1974)"

(Continued)

147

Table VI-

Species

Saloelinus fontinalis Saloe!inus fontinults Saloelinus namaycush Saloelinus namaycush Esox lucius Esox lucius Carussius auratus Carassius auratus Carassius auratus Carassius auratus Carassius auratus Carussius auratus Curassius uuratus Carassius aurutus Carassius auratus Cyprinus carpi0 Leuciscus leuciscus Pimephales promelas Scardinius erythrophthalmus Scardinius erythrophthalmus Gadus luscus Gadus merlungus Gadus morhua Gadus morhua Merluccius vulgaris Macrozoarces americanus Morone saxotilis Morone saxotilis Lepomis macrochirus

Number

6 6

Weight (B)

Velocity increments (cm sec-I)

11.0

3

11.6

3 4-12 PI2

27.7 82.8 16.5 37.8 4.4 4.4 4.4 4.4 4.4 4.4 4.4

3 3 3

3 3 3 10 7

465

34 40 12 1090 340

18.2 15-17 13.5 18.2 4.8 19.0 18.2 16.7 17.7 35.5 35-37 22.6 33.6-38.4 2-14 8.9-11.4 4.5-5.7 5.1-5.4

30 105 65 45 53 51 51

45 30

30 32 45 45 48 51 38 137 181

1.5 0.5 2 2

Swimming time at maximum velocity (min) 15 15 2 2

17

3

Lepomis macrochirus Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus sulmoides Micrapterus salmoides Micropterus saltnoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus sulmoides Perca Jlaoescens Perca perca Stizostedion vitreum oitreurn Sdaena aguilu Mugil capita

Total length (cm)

Time between increments (min)

50-60

18.8 16.5 17.7 560 580-635 23.7 156237

1.9-3.7 2.9-3.4

21.3 5.7 8.0-8.5

4.a6.4 5.67.4

8.0-8.6 2.0-2.2 2.0-2.2 2.0-2.2 2.0-2.2 2.0-2.2 2.0-2.2 5.7 15-27 15-27 15-27 15-27 15-27 15-27 0.61.4 18.3 0.7-1.5 29.7 26.5

45-270 45-270 45-270 4S270 45-270 45-270

4-12 2 4-12 2 4-12 2 4-12 2 4-12 2 4-12 2 2 4-12 Gradually to prescribed velocity 110 40

Gradually until laps lost 13

Gradually to prescribed velocity Gradually to prescribed velocity 19 Gradually to prescribed velocity Gradually to prescribed velocity Gradually to prescribed velocity 2-3 2-5 2-3

2-5

2 2 2 2 2 2 2 40-300

3

>5.6240 >4.2-240 1.1-6.6 10 30 31-201 22-28

Gradually until laps lost 2.3 10 2.3 10 2.2 3 2.2 3 2.2 3 2.2 3 2.2 3 2.2 3 Gradually until laps lost 10 30 10 30 10 30 10 30 10 30 10 30 Gradually to prescribed velocity

3 3 30 30 30 30 30 30 60

Gradually to prescribed velocity

60

3 10

10 3 3 3 3 3

18.4 29.5 26.0

148

Continued Temperature ("C)

Maximum velocity cm sec-'

67.9 88.7 35-54 4a83 210 148 22.4-34.7 29. I 22.4-40.3 51 28-51 50 15.3-38.8 15-85 60-126 170 170 19.6 114 130 55 23 75-135 75-135 79 90-120 35-87 67 22.5

&'

sec-'

6.2 7.7

Acclimation

Experimental

15 15 a23 10-22

15 15 8-23 10-22

12.7 3.9

1-3.2 3.8-8.4 12.6 9.2 4.1 6.0 5.9 3.3

5 10 15 20 25 30 35 20 15-30

5-25 10

Acute exposure to temperature

5-25 20 15-35 30 20-38 20 15-30


15

15

Acute exposure to temperature O,, 0.8-1.9 mgiliter Thermal acclimated, metabolism Photography Photography

1.3

21

28.0

5.s5.5

21

21

88 18.8-30.7 20-41 24-43 4.8-14.6 5.S16.8 7.2-23.9 11.1-27.0 8.5-29.2 17.7-31.2 I8.X-30.7 24-55 32-3-58 4s-€3 47-64 48-66 40-60 0.64.6

4. I 3.2-5.4 2.45.0 2.8-7.8 2.2-6.5 2.b7.8 3.blO.l 5.1-12.4 3.6-13.0 7.8-13.6 33-5.4 1.6-2.0 2.2 2.0-3.0 2.43.1 2.43.2 2.2-2.7 1.0-3.3 3.6 0.7-3.3 3.8 2.3

20 25 25

20 25 25 5-20 5-25 10-30 10-30 10-30 20-30 20

0..>5.0


Photography

21

I13 61

Metabolism Metabolism

Photography

2.1-3.8 2.1-3.7 3.5 2.4-3.2 7.6-12.6 5.9-7.5 4.0-5.0

6fi

Comments

8 5 8

8 5

Endurance Endurance

8

Endurance Endurance, 50% fatigue Endurance, 50% fatigue Eudurance, O,, 6.5 mdliter; H2S, 0-0.15 mglliter Endurance, O,, 6.5 niglliter; H,S, 0-0.01 mglliter

22 22

5 10

15 20 25 30 20 10

15 20 25 .30

34 13 13

02,1-24 nig/liter 4, 1.2-8.1; CO, 3-54 mglliter Acute exposure to temperature Acute exposure to temperature Acute exposure to temperature Acute exposure to temperature Acute exposure to teniperature Acute exposure to temperature

10

15 20 25 30 34 13

Velocity, 50% fatigue

13

Velocity, 50% fntigue

Reference Peterson (1974)' Peterson (1974)' Gibson and Fry (1954)' Gibson and Fry ( 1954)' Gray (1953) Magnan (1929) Fry and Hart ( 1948)& Fry and Hart ( 1948)' Fry and Hart ( 1948)' Fry and Hart ( 1948)' Fry and Hart ( 1948)' Fry and Hart ( 1948)' Fry and Hart ( 1948)' Kutty ( 1 9 6 8 ) O Smitet al. (1971)' Gray (1953) Gray (1953) McLeod (1967)' Magnan ( 1929) Gray (1953) Magnan ( 1929) Magnan (1929) Beamish (1966h)" Beamish (1966b)' Magnan ( 1929) Beamish (1966b)" Kerr ( 1953)' Kerr ( 1953)" Oseid and Smith (1972)' Oseid and Smith (1972)' Mngnan (1929) MacLeod (1967)' Dahlberg et ul. (1968)' Dahlberg et ul. (1968)' Larimore and Duever ( 1968)b Larimore and Duever ( 1968)' Larimore and Duever (1968)' Larimore and Duever ( 1968)' Lwimore and Duever (1968)b Larimore and Duever ( 1968)' Larimore and Duever (I968)* Beamish (1970)" Beamish (1970)" Beamish (1970)" Beamish (1970)'' Beamish (1970)" Beamish (1970)" Houde (1969)" Maguan (1929) Houde (1969)" Magnan (1929) Magnan (1929)

(Continued) 149

150

F. W. H. BEAMISH

Table VI-

Species

iiumIher

Trirchurus symmetricus Truchunrs symmetricus Cobivs puuiotilus Gobius syrnisii Cohius nielonostoniu Scornber scornlnus Sehster dnctyloptenrs Sebostes morinus Sehos tes nu rinu,s Sebostes inarinus Hernilriptews uniericunus .Uyoxocephulus oclodecieispinosus Pseudul,leirrotiectes unmricunus Pseurlopleiironectes umericunus Pseudopleurmiectes omericonus Pseudopleuronectes oinericonrrs

Totnl length (cm)

15 8 13

14.6 11.2 8.8

I1 42

10.6 9.0 25.3

40 40 70 16 50 .30 30 30

20

26.8 17-19 1617 1617 18.8-22.7 19.8-21.3 19-21 19-21 19-20 22-23

Weight

(n)

2R.6 25.2 29.3

Velocity increments (cm sec-')

Time hetween increments (niin)

Gradually to prescribed Gradually to prescribed Gradually to prescribed Gradually to prescribed Gradually to prescrihed

velocity velocity velocity velocity velocity

Swimming time at inaximum velocity (inin) 3.4 4.5 1&15 R-10 ,>4

,MI 127-166 113-137 114-140 231-271 13C-162 135-193 149-190 130-171 215-219

Gradually to prescribed velocity Gradually to prescribed velocity Gradually to prescribed velocity Gradually to prescribed velocity Gradually to prescribed velocity Gradually to prescribed velocity Gr:idually to prescribed velocity Gradoally to prescribed velocity Gradually to preacribed velocity

0.7-14.2 0.R-13.2 0.612.7 0.4-0.7 0.5-6.7 1.%14.1 1.7-10.3 1.4-10.0 5.3-25.4

among the former species. When trout and salmon were exposed to 100 cercariae daily for 15 days, which more closely approximated the natural rate of infection than a single large dose, endurance was reduced by 51 and 34% in trout and salmon, respectively. Hemorrhagic areas developed in the infected fish but not in the controls, to which Butler and Milleman (1971) attributed impairment of relative swimming performance. The incidence of parasitism among fish used in swimming studies is seldom reported. The recent findings strongly suggest that closer attention to the species, stage, and abundance of parasites present in experimental fish would significantly reduce variability in measurements of performance, and better facilitate quantitative comparisons among the results of swimming speed studies.

D. Environmental Constraints on Performance

1. TEMPERATURE Swimming capacity is regulated by the metabolic capacity of fish to convert chemical energy into propulsive thrust through muscular contraction. Adenosine triphosphate (ATP) generated by the stepwise degradation of carbohydrate and lipid is an essential prerequisite for muscle contraction. In sustained swimming the formation of ATP by aerobic processes would be expected to be more important than that

2.

151

SWIMMING CAPACITY

Continued Temperature ("C) Maximum velocity c ~ nsec-' 160

139 48-50 44 34 HI 98 52- 135 52-135 52-135 105-120 6(!-120 75-13.5 75-135 7,5135 75-135

't

sec-I

10.8 12.4 5.5-5.7 4.2 3.8

Accliination

Experimental

18.5

18.5

18.5

18.5

Comments

Reference

Endurance, 50% fatigue Endurnnce, 50%ftitigue

Hunter (1971)" Hunter (1971)" Shazkiiia (197213)" Shazkina ( 197211)" Shazkina (197213)" Mngnan (1929) Magnan ( 1929) Beamish (196613)" Beamish (196611)" Beamish ( 196613)" Beninish (196613)" Beainish (196613)" Beamish (196611)" Beamish (1966h)" Beamish (196613)" Beainish (196613)"

19-21 19-21

19-21

:3.2 3.6 3.1-8.0 3.1-8.0 3.1-8.0 4.6-6.4 2.8-5.7 4.0-6.5

3.6-6.6 3.9-6.6 3.S6.1

5 8

5

8

8 11 8 8

5 8 11

5 8 11

14

14

11 8

Endurance Endurance Endurance Endurance Endurance Endurance Endurance Enduraiice Endurance

by anaerobiosis. The contribution by both aerobic and anaerobic reactions is important in prolonged swimming (Bilinski, 1974). Burst swimming relies heavily on the anaerobic mobilization of metabolites from carbohydrate sources (Drummond and Black, 1960; Black et al., 1961; Dean and Goodnight, 1964; Beamish, 1966c, 1968; Drummond, 1967, 1971; Dando, 1969).Since the physiological mechanisms associated with swimming vary with the category of locomotion, it is not surprising that they should differ in their response to temperature.

a . Sustained and Prolonged Swimming Speed. A t swimming speeds where aerobic processes contribute significantly to the production of ATP the influence of temperature can perhaps best be understood from its relationship with oxygen consumption (see Brett, 1970b; Fry, 1971, for comprehensive reviews). I n the metabolic processes oxygen serves as a final acceptor in the electron transport system rather than participating directly in the enzyme reactions involved in biological oxidation. Of the oxygen consumed, a portion serves to meet the basal metabolic requirements while the remainder provides for other activities including swimming, digestion, excretion, and growth. The amount of oxygen that can be extracted is, within limits, related to or dependent on the environmental conditions (Beamish and Dickie, 1967; Fry, 1967))each factor acting independently or interacting with others to alter the potential expression of maximum metabolic rate. The term "scope for activity" was employed by Fry (1947) to illustrate the effect of environmental identities on the oxygen available to verte-

152

F. W. H. BEAMISH

brate poikilotherms for activities excluding basal metabolism. Changes in scope for activity in relation to temperature are illustrated in Fig. 11 for brook trout (Graham, 1949), lake trout, Salvelinus namaycush (Gibson and Fry, 1954) and largemouth bass (Beamish,

1970).

Temperature, O C Fig. 11. Metabolic scope for activity of (A) brook trout, Salvelinus f o n t i n a h (Graham, 1949); (B) lake trout, Salvelinus namaycush (Gibson and Fry, 1954); (C) largemouth bass, M i c r o p t m s salmoides (Beamish, 1970), in relation to temperature.

153

2. SWIMMING CAPACITY

Within the thermal range of tolerance for a species, prolonged speeds typically increased with temperature to a maximum and thereafter decline. Examples of prolonged swimming speeds in relation to temperature of acclimation are presented in Fig. 12. Temperature compensation, customarily applied to adaptive evolution of metabolic performance (Bullock, 1955; Fry, 1958; Roberts, 1966; Brett, 1970b)

0

10

20

30

40

Temperature,O C Fig. 12. Prolonged swimming speed and temperature. (From Fry and Hart, 1948; Gibson and Fry, 1954; Brett et al. 1958; Wohlschlag, 1964; Larimore and Duever, 1968; Beamish, 1970; Brett and Glass, 1973.)

154

F. W. H. BEAMISH

applies also to prolonged swimming speeds. Among the eurythermal temperate species such as goldfish (Fry and Hart, 1948) and large and smallmouth bass (Beamish, 1970; Larimore and Duever, 1968) the temperature for maximum prolonged performance lies within the range of 25"-30°C (Table VI). Stenothermal temperate species such as the lake trout, Saluelinus namaycush (Gibson and Fry, 1954), display maximum prolonged speeds between 15"and 20°C.The prolonged performance of the antarctic stenothermal, Trematomus borchgreuinki (Wohlschlag, 1964), in contrast to the temperate species was highest at -0.8"C and fish were unable to swim at temperatures above 2°C. Prolonged performance may vary severalfold within the range of thermal tolerance for a species. The ( 3 min, 2.2 cm sec-l) prolonged speed for smallmouth bass (2.2cm) increased from 4.8 to 31.2 cm sec-' (2.2-14.2 e sec-') between 5" and 30°C (Larimore and Duever, 1968). The prolonged (60 min, 10 m sec-I) critical for sockeye salmon (20 cm) varied from just over 50-90 cm sec-l (2.5-4.5 6 sec-l) between 1" and

15°C. The response of prolonged swimming speed to thermal acclimation is presented for three species in Fig. 13. In each, maximum performance progressively shifts toward a higher exposure temperature as acclimation is increased. This, of course, suggests that the capacity for activity over much of the range of thermal tolerance for a species is greatest at environmental temperatures equal to or above those to which it is acclimated. For example, goldfish acclimated to 5" and 25°C performed best at 18" and 28"C, respectively (Fry and Hart, 1948). Similarly, the ( 3 min, 2.2 cm sec-*) prolonged speed of smallmouth bass, acclimated to lo" or 15°C occurred at 22" and 25"C, respectively (Larimore and Duever, 1968). Griffiths and Alderdice ( 1972) thoroughly investigated the influence of acute temperature exposure on the (60 min, one-eighth critical) critical speeds of young coho salmon (7.9-9.5 cm). Maximum critical speeds occurred at test temperatures above the acclimation, denoted in Fig. 13 by line A. At a given test temperature, maximum performance coincided closely with acclimation, in the figure described b y ridge B. Optimum performance occurred at a combination of acclimation and test temperatures near 20°C. Fry (1967) concluded, based on earlier evidence, that maximum swimming performance for a given temperature occurs when acclimation and exposure are identical which is generally concordant with the observations of Griffiths and Alderdice (1972).

b . Burst Swimming Speed. Temperature appears to exert little influence on burst speed although information at this level is particularly

2.

155

SWIMMING CAPACITY

B M i c r o ~ t e r u sdolomieu

,

,

,

,

,

,

,

,

l O

0

10

0

40

30

20

10

26

t

Oncorhynchus klsulch

0

2

,

1

1

8

20

90

40

Test Temperature,'C

Temperature, OC 1

1

14

1

1

1

1

C

20

26

Acclimation TemperaturePC Fig. 13. Prolonged swimming speed and temperature. Th e heavy lines in panels (A) and (B) denote prolonged for fish acclimated to the test temperatures. Light lines indicate the response between prolonged and test temperature for a particular acclimation temperature (Fry and Hart, 1948; Larimore and Duever, 1968). I n panel (C) the U critical speed isopleths (cm sec-l) for coho salmon, Oricorhynchus kisutch, are presented in relation to acclimation and test temperature (Griffiths and Alderdice, 1972).

156

F. W. H. BEAMISH

scarce. Blaxter and Dickson (1959) measured the burst speeds for a number of marine and freshwater teleosts (Table IV) and were unable to demonstrate any correlation between performances and temperature. Based on metabolic studies of sockeye salmon in relation to performance, Brett ( 1964) anticipated temperature independence for burst swimming. The swimming endurance of redfish, Atlantic cod, and winter flounder, Pseudopleuronectes americanus, at speeds approaching burst velocities did not vary appreciably over the ecological range of temperatures experienced throughout much of the year in the northwest Atlantic ( Beamish, 196613). More recently Groves (reported in Brett, 1970b) reported a temperature independence in the burst speed achieved but a dependence in terms of endurance by sockeye salmon.

2. OXYGEN In aquatic organisms which use oxygen for their respiration, the ambient oxygen consumption itself can limit swimming performance. There appears for most fish a threshold oxygen concentration below which swimming performance is reduced (Dizon, 1977).

a. Sustained and Prolonged Swimming Speed. Kutty (1968) and Kutty and Saunders (1973) introduced the term “critical oxygen concentration” to describe the concentration at which fish are unable to maintain sustained or prolonged speeds. Thus Atlantic salmon (23.4cm) sustained speeds of 50 and 70 cm sec-l (2.1and 3.0 C sec-l) for several hours until ambient oxygen was reduced to 4.0 and 4.8 mg O2 liter-’, respectively (Kutty and Saunders, 1973; see also Fig. 14). Critical oxygen concentrations of goldfish (18.5 cm) at 59.2 and 18.6 cm sec-’ (3.2 and 1.0 C sec-l) were 1.8 and 0.8 mg O2 l i t e r 1 , respectively (Kutty, 1968). Similar reductions in sustained and prolonged swimming performance in the presence of low oxygen have been demonstrated for a number of species (Graham, 1949; Katz et al., 1959; Davis et al., 1963; Whitworth and Irwin, 1964; McLeod and Smith, 1966; Dahlberg et al., 1968; see also Table VI; Fig. 14). Above air saturation, prolonged performance of coho salmon and largemouth bass was independent of oxygen (Dahlberg et al., 1968; see also Fig. 14). In contrast to the earlier observations by Prosser et al. (1957) on goldfish, Kutty (1968) found acclimation to low ambient oxygen did not alter the critical oxygen concentrations for a given sustained swimming speed. Failure to swim at low ambient oxygen was not attributed by Kutty (1968) to fatigue as fish began to swim as soon as oxygen levels were increased, but rather to an oxygen sensing mecha-

2.

157

SWIMMING CAPACITY

v I

0

Q

u)

E

0

'0 Q

Q

a v)

D

.-C

E

.-E

3

v)

407-M icropterus salmoides

20

0

1

1

1

1

1

1

1

1

1

1

,

1

,

Fig. 14. Swimming speed and ambient oxygen concentration. In the upper panel, critical oxygen concentrations at which fish are unable to maintain a sustained speed (Kutty, 1968; Kutty and Saunders, 1973). In the lower two panels, the relationship, between prolonged speed and oxygen (Dahlbery et ul., 1968).

nism such as the peripheral or central oxygen receptors reported by Saunders and Sutterlin (1971).

b. Burst Swimming Speed. The effect of dissolved oxygen on burst swimming has not been measured. However, burst speed depending as it does on anaerobic energy sources may be expected to be largely

158

F . W. H. BEAMISH

independent of ambient oxygen except that between swimming events the accumulated metabolic debt must be repaid before the next burst of swimming can realize its full potential. The mobilization of energy resources for repeated bursts and therefore the frequency of rapid swimming may well be restricted by moderate oxygen deficiency.

3. CARBONDIOXIDE Carbon dioxide has long been known to reduce the affinity of blood for oxygen (Root, 1931) and to influence the metabolic rate of fish (Basu, 1959; Beamish, 1964b). Particularly little information is available on the effect of carbon dioxide on swimming, a notable exception being the research of.Dahlberg et al. (1968). They measured the prolonged speed of largemouth bass and coho salmon in response to dissolved oxygen and free carbon dioxide. The prolonged speeds of largemouth bass did not change in response to concentrations of carbon dioxide to 48 mg liter-'. The performance of coho salmon in contrast to that observed for bass declined on exposure to concentrations of carbon dioxide between 2-61 mg liter-'. In low concentrations of oxygen the influence of carbon dioxide was less pronounced. For an oxygen concentration of 10 mg liter-l, the prolonged speed of salmon decreased from about 60 to fractionally above 50 cm sec-' when carbon dioxide increased from 2 to 61 mg liter-'. In contrast, when ambient oxygen was about 2 mg liter-I, prolonged speed did not change with increase in free carbon dioxide.

4. SALINITY Salt concentration in the blood of fish is less than that of seawater. In a marine environment water is lost at the gills and other body surfaces (Potts, 1954; Black, 1951). Conversely freshwater homeostasis is dependent on the elimination of absorbed water, the concentration of the body fluids being greater than that of the environment (Black, 1957).The mechanism by which osmoregulation is achieved may vary among species (Parry, 1958; Gordon, 1963; Threadgold and Houston, 1964) but each requires the expenditure of energy. Few measurements have been made on the relationship between salinity and swimming performance. A consistent pattern of change in the swimming speed of skipjack and yellow fin tuna did not occur in response to a salinity decrease from 34 to 2W/00 (Dizon, 1977).Critical speeds (60 min, one-eighth critical) of coho salmon in relation to salinities and temperatures between 0-20./, and 3"-23"C, respectively, were measured by Glow and McInerney (1977) (Fig. 15, Table

2.

159

SWIMMING CAPACITY

Oncorhynchus k isutc h

,

25

20

Fry, 8.9 crn

--_:--

'

40

44

i' \

Fig. 15. Critical swimming speed isopleths (cm sec-I) for coho salmon fry and smolts, Oncorhynchus kisutch, in relation to salinity and temperature (Glova and McInerney, 1977).

V). The combined effects of salinity and temperature indicated critical swimming performance of underyearling coho was predominantly a temperature-dependent response during the premigratory stages of development. Swimming performance of fry was almost independent of salinity as reflected by the flat configuration of the performance isopleths in Fig. 15. Coho smolts achieved maximum critical speeds at

160

F. W. H. BEAMISH

salinities ranging from just under 8 to about 190/,. Relative to this salinity optimum, critical, performance declined by about 6 and 4 cm sec-’ at 0 and 20”/,, respectively. Just prior to, or concurrent with smoltification, coho appear to lose their euryhaline capacity to function efficiently over a range of salinities which is concordant with observations on salinity tolerance for this species (Alderdice, 1963). Performance restrictions attributable to salinity have not been measured for other species. However, fluctuations in metabolic expenditure in association with prolonged speeds have been measured for rainbow trout (Rao, 1968) and Tilapia nilotica (Farmer and Beamish, 1969) in salinities of 0-30”/,. In both studies the energy actually expended in swimming was independent of salinity. Nevertheless, changes in metabolic rate did occur, suggesting that performance capacity would be reduced in proportion to the energy expended in osmotic regulation.

5. THEDISTURBED ENVIRONMENT The influence of those identities introduced into the environment either directly or indirectly by man or through his activities has received attention only in recent years with most of the effort expended in the determination of their lethal concentrations. Of particular concern to the swimming capacity of fish are those identities which influence the exchange of respiratory gases or the metabolic pathways involved in the mobilization of energy. From among the many factors that may contribute to the disturbed environment, only a few have been examined with respect to their influence on swimming performance. Conifer pulpwood fiber in suspension impairs the removal of oxygen from water by physically clogging the gill lamellae and interrupting the respiratory flow during gill cleaning reflexes (MacLeod and Smith, 1966). On exposure to suspensions of pulpwood fiber equivalent to 200 mg liter-’ the endurance of fathead minnows, Pimephales promelas, forced to swim at a low velocity was significantly less than that of fish in freshwater under comparable concentrations of dissolved oxygen (Fig. 16A). The influence of the pulpwood suspension was most pronounced at the higher temperatures (Fig. 16B) which is consistent with its impairment of gaseous exchange. In contrast to the influence on endurance at prolonged swimming, burst swimming speed was independent of the concentration of pulpwood fiber. Hydrogen sulfide is found not infrequently in the aquatic environment and results from the decomposition of material either naturally occurring or present through the activities of man. Endurance of bluegills (3.2 cm) forced to swim at 22.5 cm sec-’ increased from just

161

2. SWIMMING CAPACITY 80-

60

-

Q 40

-

E

Plmephales promelas

t

al 0

c

15OC

CI

rn

i 20-

0

-

40

A ,

Pulpwood Fiber 1

2

1

1

4

1

1

1

6

al

1

0

0

50 Saivelinus fontinails

u)

E

Pulpwood Filter

21°c

200

100

Fiber Concentration, mg liter"

Oxygen, mg liter''

I

0

-

t1

tI

Salmo galrdneri

t

0

Fenitrothion, mg Iihr-'

Copper, mg liter"

Fig. 16. (A) The influence of pulpwood fiber and dissolved oxygen on the distance swum by fathead minnows, Pimephales promelas (MacLeod and Smith, 1966). (B) Temperature, oxygen, and pulpwood fiber effect on swimming distance by fathead minnows (MacLeod and Smith, 1966): ( C ) Effect of fenitrothion on prolonged speed of brook trout, Saloelinus fontinalis (Peterson, 1974). (D) Effect of copper on critical speed of rainbow trout, Salmo gairdneri (Waiwood, personal communication).

over 200 min in the absence of hydrogen sulfide to 240 min at 0.4 pg liter-'H2S, and with further increases, decreased so that at 14.6 p g liter-' fish swam only for 30 min (Oseid and Smith, 1972). Coincident with the long term exposure to H2S was an increase in the rate of gill irrigation which undoubtedly lead to an appreciable reduction in the mobilization of energy through aerobic processes. Sodium pentachlorophenate (PCP), used as a defoliant or for the protection of timber from wood-boring insects and fungal infection, is considered a general metabolic poison for fish (Webb and Brett, 1973).

162

F. W. H. BEAMISH

However, the (60 min, 5 cm sec-l) critical speed of sockeye salmon (5.3-6.0 cm) did not change significantly from about 40 cm sec-I (7.3C sec-’) on exposure to concentrations of PCP between 0-50 pl-1 (Webb and Brett, 1973). Similarly, Krueuger et al. (1966) found that swimming performance of Cichlasoma bimaculatum was not reduced by pentachlorophenol until the concentration approached lethal levels. Webb and Brett (1973) proposed that a general metabolic poison such as PCP should not “preferentially” affect the gas exchange system particularly where excitement, as included in fish forced to swim, serves as a “stressor.” The influence of fenitrothion, an organophosphate insecticide used in the control of spruce budworm, on prolonged swimming speed of brook trout was determined by Peterson (1974). Prolonged swimming speed decreased from 5.0 C sec-’ for controls to 3.5 C sec-’ for trout exposed to 1.5 mg liter-’, the highest concentration applied (Fig. 16C). While the mechanism through which fenitrothion reduces swimming performance is unknown, Peterson (1974) suggested it may cause impairment of those areas of the nervous system concerned with muscle activity or alternately by causing indirect effects through “motivational” disturbances. In a comprehensive study on the influence of bleached kraft mill effluent (BKME), Howard (1975) measured the (60 min, 5 cm sec-l) critical speed of coho salmon to concentrations equivalent to 90% of the level at which 50% of the fish died within 96 hr (96 hr LC,,). Exposure for 18 hr to a concentration of 0.9 LCso resulted in a 72% reduction in swimming capacity. Further critical speed for a given concentration of BKME was independent of exposure time beyond 18 hr and returned to control levels within 6-12 hr after being placed in effluent-free water. In swimming fish, Howard (1975) suggests BKME retards gaseous exchange either by absorption of the effluent on the gill surface or through the formation of a weak chemical bond to the gill epithelium. In addition, Javaid ( 1973) observed ventilatory irregularities among sockeye salmon exposed to BKME. Effluents from mining operations discharged into waterways may also exert a pronounced influence on the capacity of fish to perform. Waiwood (personal communication) measured the influence of total copper and p H in relation to water hardness on the (60 min, 5 cm sec-l) critical swimming speed of rainbow trout (Fig. 16D). H e found that for a given hardness, critical speed was reduced by increasing concentrations of copper but that the effect diminished with time of exposure to about 10 days (Fig. 16D). Further, the influence of a given concentration of copper on performance decreased inversely with

2.

SWIMMING CAPACITY

163

water hardness. Copper is known to have a deleterious effect on the composition of blood (McKim et al., 1970) and to damage various tissues including the kidney, liver, intestine, and cephalic lateral canals (Baker, 1969; Gardner and Laroche, 1973). Tissue damage would undoubtedly cause an elevation in basal metabolism and a decline in the scope for activity. Swimming performance, depending as it does on the immediate recruitment of energy, has been recommended for use as a criterion in the determination of the sublethal effects of pollutants on fish (Brett, 1967; Sprague, 1971). However, the proper application of swimming speed, as well as the category of performance to be tested as a criterion of sublethal effect, requires a comprehensive prior knowledge of the pharmacological effects of the pollutants concerned. Impairment of the gaseous exchange of mechanism might, for example, be masked in burst swimming speeds which depend on anaerobic processes. Further, the capacity exhibited by some fish to acclimate in part or even fully to a given pollutant should be respected by the serious investigator.

IV. ENERGETICS OF SWIMMING

The expenditure of energy during swimming is reflected in gaseous exchange and should include measurements of both oxygen consumption and carbon dioxide production. However, due to limitations imposed by the techniques available, measurements of carbon dioxide production are infrequently made, the researches of Kutty (1968) being a notable exception. More generally, calculation of the energy expenditure for swimming is made from units of oxygen consumption and converted to units of energy on the basis of an oxycalorific coefficient derived for domestic homeothermic animals (Brody, 1945). This coefficient assumes not only the complete oxidation of catabolized substrates but also a normal balance of the sources such as is implied by an average respiratory quotient of 0.8. Winberg (1956) suggested that irrespective of the components oxidized, the oxycalorific coefficient will not vary more than 1.5%. It is generally agreed an oxycalorific coefficient of 3.363.44 is most applicable for teleosts (Warren and Davis, 1967; Brett, 1973; Beamish et al., 1975). In contrast, Krueger et al. (1968) reported that calorific loss based on lipid depletion in strenuously exercised salmon was substantially greater than that estimated from respiratory rates, and questioned the method of evaluation of energy production indirectly from oxygen consump-

164

F. W. H. BEAMISH

tion. Brett (1973) on the other hand, concluded an oxycalorific coefficient of 3.36 cal mg 0 2 - 1 consumed is acceptable for teleosts and that under carefully regulated experimental conditions, estimates of energy expenditure made from the oxygen consumed by sockeye salmon are not at variance with those based on the utilization of body components. In sustained swimming the mobilization of energy is achieved through aerobic processes so that the quantity of oxygen consumed is proportional to the amount of work performed. Fish swimming at prolonged speeds derive energy from both aerobic and anaerobic processes, the contribution from the latter increasing with the severity of exercise. At prolonged speeds, utilization of glycogen stores was reported by Pritchard et al. (1971) as the principal cause of swimming failure in the jack mackerel. The evolution of respiratory gases has not been measured for burst swimming because of the practical difficulties imposed by the short duration of muscular activity. It is presumed, however, that at burst swimming, fish consume some oxygen and that the remainder of the energy requirement is met through anaerobic processes. The latter results in an oxygen debt which is repaid subsequent to the termination of exercise. The allocation of aerobic and anaerobic processes in relation to the category of swimming is summarized in Fig. 17. Swimming energetics is the subject of several reviews which should be consulted (Fry, 1957; Fry and Hochachka, 1970; Brett, 1962, 1970a, 1972; Beamish and Dickie, 1967; Randall, 1970; Doudoroff and Shumway, 1970; Schmidt-Nielsen, 1972; Bilinski, 1974). Present evidence indicates that swimming may elevate the total metabolic rate by as much as 15-fold (Beamish, 1964a; Brett, 1964). The oxygen consumed at sustained and prolonged swimming speeds is presented for a number of species in Fig. 18. Subtraction of standard or basal metabolism from the total oxygen uptake has been used to approximate the expenditure of energy associated with a particular swimming speed. Where anaerobic processes do not contribute significantly this would appear a satisfactory procedure. The rate of increase in the logarithm of oxygen uptake with relative swimming speed in Fig. 18 is surprisingly similar among species despite obvious variation in methodology, size, and temperature and is reasonably well represented by a coefficient of 0.36. Thus for each increase in relative swimming speed of C sec-' there is a corresponding 2.3-fold elevation in metabolic rate. In severe prolonged and burst swimming, caution must be exercised in not accounting for energy expenditure by anaerobic processes. The anaerobic contribution is perhaps most conveniently as-

165

2. SWIMMING CAPACITY Resting Repayment

0

45

Reperfoman

90

Swimming Speed, cm sec-l

Recovery Time, h

Fig. 17. Oxygen consumption and debt for sockeye salmon, Oncohynchus nerka (18 cm), in relation to swimming speed and recovery at 15°C.(Redrawn from Brett, 1964, I. Fish. Res. Board Can.)

sessed by continued measurement of oxygen consumption on completion of swimming until it returns to preexercise levels at which time the 'oxygen debt is presumably repaid (Heath and Pritchard, 1962; Brett, 1964; Smit et al., 1971).This procedure assumes the products of anaerobic metabolism such as lactate are not excreted but subsequently oxidized during the recovery phase following exercise. Recently, Karuppannan (1972, reported in Kutty and Peer Mohamed, 1975) has shown that Tilapia mossambica excrete some lactate after strenuous exercise, corroborating the earlier observations by Blaika (1958) on the anaerobic metabolism of crucian carp, Carussius carassius. The maximum rate of oxygen consumption among fish species appears to vary at least Sfold with maximum values in excess of 2000 mg kg-l hr-I (Stevens, personal communication). The metabolic capacity of the higher vertebrates is generally one or two orders of magnitude above that demonstrated for teleosts (Bartholomew and Tucker, 1963, 1964; Bartholomew et al., 1965; Tucker, 1970; Brett, 1972). This discrepancy is compensated for, in part by a greater tolerance by teleosts to oxygen debt but from which recovery is slow. In sockeye salmon the rate of replacement of oxygen debt following fatigue was in excess of 3 hr and independent of temperature (Brett, 1964). The magnitude of the debt accumulated at the time of fatigue was influenced by temper-

mm 100

100

1.0

21)

Swimming Speed,

3)

4.0

0

1 sec-l

Fig. 18. Oxygen consumption, energy utilization, and swimming speed. Th e total oxygen consumed is presented in the upper panel. Subtraction of the basal from total metabolic rate provides a measure of the energy required for a given speed of swimming. Th e heavy line in the lower panel denotes the general rate of increase in net oxygen consumption and was fitted by eye. (From Basu, 1959; Beamish, 1964a, 1970; Brett, 1964; Brett and Sutherland, 1965; Farmer and Beamish, 1969; Kutty, 1969; Webb,

1971b.)

2.

167

SWIMMING CAPACITY

ature and increased 2-fold between 5” and 15°C. Similarly, Heath and Pritchard ( 1962) found that bluegill sunfish, after strenuous exercise, maintained a high consumption of oxygen followed after 1 hr by a gradual decline to preexercise levels 10-24 hr later. Schmidt-Nielson ( 1972) expressed the energy cost for locomotion independently of swimming speed as the caloric expenditure to transport 1 unit of body mass 1 km. A reanalysis of Brett’s data on prolonged swimming speeds of sockeye salmon b y Schmidt-Nielsen showed a logarithmic linear decrease in energy expenditure with increase in body weight over a range of three orders of magnitude (Fig. 19). The application of this expression of the energetic cost of locomotion to other species exercised at sustained and prolonged speeds under different environmental conditions shows a remarkable similarity to the relation described for salmon in Fig. 19. Closer examination of the comparative energy cost at low and high prolonged speeds based on measurements of oxygen uptake indicates a reduction as velocity is increased. Thus, the energy expenditure for mullet, Liza rnacrolepis, declined from 2.09 to 1.48 cal g-I km-’ between 10 and 22.5 cm sec-’ (Kutty, 1969),which presumably reflects a greater contribution of anaerobic metabolism at the higher speeds. Refinement in the measurement of total metabolism of swimming fish, while desirE ’Y

Swimming

1.0

Fish

-

Micropterus salrnoides

Lepornis gibbosus’

*

Coregonus

P

al C

w

0.1

I

1

I

10

I

I

I

100

1000

Weight, g Fig. 19. Energy cost of swimming relative to body size calculated by SchmidtNielsen (1972) from data collected by Brett (1964), Wohlschlag et al. (1968), Matyukhin and Stolbow (1970, reported in Schmidt-Nielsen, 1972), Rao (1971),and Smitet al. (1971). In addition, measurements made by Brett and Sutherland (1965), Farmer and Beamish (1969), Kutty (1969), Tytler (1969), and Beamish (1970) have been recalculated and added to the figure.

I

168

F. W. H. BEAMISH

able, is unlikely to alter significantly the linear relationship described by Schmidt-Nielsen. Following Schmidt-Nielsen’s interesting hypothesis, Gold (1973, 1974) and Calder (1974) expressed the energy cost of swimming one body length in terms of the mass of propulsive muscles relative to total weight and multiplied by the number of muscle contractions or tailbeats required to transport the animal one length. This assumed a constancy in the quantity of energy available per contraction per unit of muscle mass equal to 1 cal kg-l. Energy for muscular contraction is derived from the hydrolysis of adenosine triphosphate to adenosine diphosphate and inorganic phosphate. The evolution of adenosine triphosphate through the catabolism of organic compounds may occur under both aerobic and anaerobic conditions, the former being the more efficient in terms of yield but each offering distinct advantages to the swimming teleost. In sustained swimming where the amount of oxygen consumed is proportional to the work performed, the main source of energy is from long-chain fatty acids and to a lesser extent protein and glycogen (Greene, 1926; Idler and Tsuyuki, 1958; Drummond and Black, 1960). When the capacity for aerobic metabolism is exceeded as in severe prolonged or burst swimming, adenosine triphosphate is synthesized by anaerobic glycolysis of stored muscle glycogen. Lactic acid, the end product of glycolysis, diffuses from the muscle into the bloodstream (Nakatani, 1957; Black, Connor et al., 1962; Driedzic and Hochachka, 1975). Both swimming and the accumulation of lactic acid may continue until the glycogen deposits are depleted or the end product of anaerobic glycolysis exerts a detrimental effect on activity. Where exercise is extreme in its severity, death may result during the recovery period (Parker et al., 1959; Beamish, 1966c; Caillouet, 1967). The actual cause of death is uncertain but may result from interference with the acid base equilibrium, coupled with reduced affinity of hemoglobin for oxygen, and, in the presence of excess acid, lowered affinityfor carbon dioxide (Black, 1958a).When death does not follow strenuous exercise, the elevated rate of oxygen consumption serves not only to meet the routine metabolic requirements but also to replace muscle supplies of adenosine triphosphate, creatine phosphate, and glycogen (Bilinski, 1974).

V. APPLICATION TO MANAGEMENT PRACTICES Hatchery breeding programs have tended to select for qualities such as rapid growth, early maturity, high fecundity, and disease resis-

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tance which, of course, are of obvious benefit to the culturist. However, when the objective is to stock desirable waterways with the view of generating a sustainable population, selective breeding programs may have overlooked qualities essential to the continued well being of the population. Swimming performance is an important component of viability as it relates to a fish’s capacity to maintain station against current, avoid predators, and acquire food. Bams (1967) proposed that unless severe environmental conditions impose a serious constraint, the most important component of survival is stamina. Vibert (1956) used the ability of fish to swim against a current as a test of adaptability for stocking. The importance of swimming performance is reflected by the higher survival of fish which were conditioned to a stream habitat prior to stocking (Shuck and Kingsbury, 1948; Miller,

1957). The stamina of hatchery and stream-conditioned rainbow trout was investigated b y Reimers (1956). Hatchery rainbow trout were able to swim against a current of 90 cm sec-’ for 5-10 min before fatigued, considerably less than the 30 min recorded for stream-conditioned trout. The performance of wild stocks of brook trout, even though reared under hatchery conditions, was consistently superior to that recorded for domestic stocks of the same species (Vincent, 1960; Green, 1964). The size at which fish are stocked may also influence their success. Survival of planted chinook salmon suggest a greater success among fingerlings than fry (Junge and Phinney, 1963). Thomas et al. ( 1964) attributed the greater survival of fingerlings to a number of factors including performance capacity. The role of nutrition on swimming performance and the ultimate capacity of planted fish to cope with the environment has not been examined but represents a potentially profitable area of research. Hatchery procedure in the incubation of eggs may also iegulate the ultimate capacity of the species to perform. Bams (1967) examined different methods of incubating eggs of sockeye salmon on the ultimate relative performance of fry. Naturally propagated salmon demonstrated the best relative performance followed by fry reared in gravel from the time of hatching and held, prior to the advanced alevin stage, in baskets or trays without a substrate. The poorest stamina was registered by fish reared in hatchery troughs without gravel at any stage. Investigations aimed at determining size and structure of fish stocks can be influenced b y the species’ resistance to fatigue. This may result when fish are tagged and released subsequent to capture by any method which involves severe muscular exertion on the part of the

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fish. Fox example, marine demersal species are frequently captured for tagging purposes by otter trawls which are towed along the seabed at speeds of 140-200 cm sec-' for 30 min or more. Many fish are unable to swim at these speeds for long and fatigue. This imposes a severe metabolic load, manifested by an oxygen debt, a depletion of glycogen reserves, and elevation in lactate, as well as a number of other physiological changes. Mortalities following capture by otter trawl have been reported and attributed to muscular fatigue. Among haddock, Melanogrammus aeglefinus, mortalities ranged between 7 and 78% of those captured b y otter trawl (Beamish, 1966~).Fatigue deaths in ocean troll-caught chinook and coho salmon were observed by Milne and Ball (1956,1958),Parker and Black ( 1959) and Parker et al. (1959). Barrett and Connor (1962) attributed some of the deaths of hook and line-caught yellowfin and skipjack tuna during recovery to fatigue. The steadily increasing demand for greater utilization of waterways has resulted in the construction of dams on rivers and the location of electrical generating plants near rivers, lakes, and oceans (Kerr, 1953).One of the problems associated with the construction of dams is that of preserving fish populations indigenous to the waters. On the west coast of North America, particular concern has been expressed for the well being of valuable stocks and anadromous trout and salmon. This entails providing safe passage for fish through waterways and over obstacles. One of the considerations in the construction and operation of a fishway is to provide flows at the entrance which will attract the desired species. Weaver (1963) conducted a series of velocity preference studies at the site of the Bonneville Dam on the Columbia River. The experiments were conducted in large dual channels and compared the frequency of fish passing through each in relation to water velocity. The results suggested the proportion of rainbow trout and chinook and coho salmon selecting the channel with the highest current speed applied, 240 cm sec-', was appreciably greater than that at any other velocity, the lowest of which was 60 cm sec-'. Information on the critical length of the passageway was provided from performance studies designed to measure the distance salmonids could swim at velocities to 500 cm sec-'. Mean maximum speed which rainbow trout (68.5 cm) could maintain for 9.14 m (1.5 sec) was 642 cm sec-' (9.5 8 sec-l) with one individual (61 cm) achieving 817 cm sec-' (13.4e sec-I). Maximum speeds for chinook (75.3cm) and coho salmon (51.0cm) were 604 and 421 cm sec-' (8.2and 8.2 8 sec-l), respectively. Earlier, Paulik and DeLacy (1957) measured the swimming speed of rainbow trout, coho, and sockeye salmon to provide information needed in the design of fishways. They found, in laboratory studies,

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the maximum prolonged speed for rainbow trout (63.6cm) was 213 cm sec-1 (3.4e sec-I), well below that found by Weaver (1963). Similarly the maximum prolonged speed of coho (56.2 cm) 190 cm sec-l (3.5e sec-I) fell short of the subsequent measurements made by Weaver ( 1963).

Another of the basic problems in the design of fishways is the location, number, and size of resting pools. Recovery of coho salmon (65.6 cm) from an exhaustive swimming effort at 100 cm sec-' was found to be 31% complete after 1 hr rest and 67% after 3 hr. All fish recovered when allowed 18-24 hr (Paulik et al., 1957). From these data the investigators concluded the necessity for adequate resting facilities along a fishway when velocities exceeded 100 cm sec-' for more than a few minutes. Swimming performance of salmonids has been found to decline slightly as adult fish migrate upstream (Paulik and DeLacy, 1958). In Passamaquoddy Bay of the Bay of Fundy, a study was initiated to examine the possible effects of the construction of a series of dams on the fishery. Of major importance were the Atlantic herring which accounted for the vast majority of the total fish landings. Movements of herring indicated they entered the bay through narrow passages in which water velocity occasionally reached 300 cm sec-'. With the construction of the dams currents would have exceeded this speed. Laboratory measurements of swimming endurance at prescribed velocities indicated that had the dams been constructed, high currents together with the periods during which the dam gates were closed would have denied herring access to the bay for all but about 20 min every 24 hr. Observations on the swimming capacity of the western sucker, Catostornus occidentalis, as they moved upstream through a culvert prompted Wales (1950) to note the possibility of excluding undesirable species from portions of a river by regulating current speed. Swimming speed studies have been applied also in the design and assessment of fishing gear. The efficiency of otter trawls has received considerable attention as they supply much of the total annual harvest of fish from the marine environment. Reports from divers and from photographic observations (Blaxter and Parrish, 1966; Beamish, 1967) have indicated the orientation of fish swimming ahead of the trawl. With this information and the swimming capacity of the species the probability of escape can be estimated, assuming a straight line course and a fixed speed of swimming. Such estimates have been made for a number of demersal species in t h e northwest Atlantic by Beamish (1967) and the North Sea by Blaxter (1967; see also Fig. 20).

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I

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impossible

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Speed required to escape, m sec-‘ Fig. 20. Swimming speed required to avoid capture by otter ?awl at different angles

of escape when the fish is in the center of the path of the net and reacts 3 m away (Blaxter, 1967). Arrow at 2 m sec-I indicates maximum burst speed for adult clupeoids. Panel (A) illustrates the change when nets of 12, 18, and 24 m in width are employed at speeds of 1.2 ni sec-I. Panel (B) indicates change when towing speed is varied from 1.2 to 2.4 m sec-l and net width is held at 12 m.

ACKNOWLEDGMENTS 1 am most grateful to Dr. E. D. Stevens for his comments on the manuscript and to Mrs. E. Thomas for her assistance with the figures.

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Radakov, D. V., and Solovyev, B. S . (1959). First attempts to employ a submarine for observing the behaviour of herring. Rybn. Khoz. (Moscow) 35, 16-21. (Fish. Res. Board Can., Transl. Ser. No. 338.) Randall, D. J. (1970). Gas exhange in fish. Zn “Fish Physiology” (W. S. Hoar and D. J. Randall, eds.), Vol. 4, pp. 253-291. Academic Press. New York. Rao, C. M. M . (1968). Oxygen consumption gf rainbow trout (Salmo gairdneri) in relation to activity and salinity. Can. 1.Zool. 46, 781-786. Rao, C . M. M. (1971). Influence of activity and salinity on the weight-dependent oxygen consumption of the rainbow trout Salmo gairdneri. Mar. Biol. 8, 205-212. Rasmussen, B. (1959). On the migration pattern ofthe West Greenland stock of cod. Ann. Bfol. 4, 123-124. Regnard, M. P. (1893).Sur un dispositif qui permet d e mesurer la vitesse d e translation d’un Poisson se mouvant dans I’eau. C.R. SOC. Biol. 5, 81-83. Reimers, N . (1956).Trout stamina. Prog. Fish-Cult. 18, 112. Richardson, I . D., Cuihing, D. H., Harden-Jones, F. R., Beverton, R. J. H., and Blacker, R. W. (1959). Echo sounding experiment in the Barents Sea. Fish. Inuest. Minist. Agric., Fish. Food (G.B.)Ser. 11 Salmon Freshwater Fish. 22(9), 7-16. Ricker, W. E. (1975).Computation and interpretation ofbiological statistics of fish populations. Bull., Fish. Res. Board Can. 191, 1-382. Roberts, J. L. (1966). Systematic versus cellular acclimation to temperature by poikilotherms. Helgol. Wiss. Meeresunters. 14, 451-465. Root, R. W. (1931).The respiratory function of the blood of marine fishes. Biol. Bull. (Woods Hole, Mass.) 61, 427-456. Royce, W. F., Smith, L. S., and Hartt, A. C. (1968). Models of oceanic migrations’of Pacific salmon and comments on guidance mechanisms. U.S.Fish Wildl. Serv., Fish. Bull. 66, 441-462. Ruhland, M. L., and Heusner, A. (1959). Chambre respiratoire pour la determination simultane d e I’activitk et de la comsommation d’oxygene par une methode manom6trique chez des poissons de 3-log. C.R. SOC. Biol. 153, 161-164. Ryland, J. S. (1963). The swimming speeds of plaice larvae.]. E x p . Biol. 40, 285-299. Saetersdal, G. (1956). Fisheries research in northern waters-study items and results. Dep. Rep. No. 1. Deep Sea Research Inst., Fish. Directorate, Bergen. (Transl. by Cent. Off. Inf., London.) Saunders, R. L., and Sutterlin, A. M. (1971). Cardiac and respiratory responses to hypoxia in the sea raven, Hemitripterus americanus, and an investigation of possible control mechanisms. J . Fish. Res. Board Can. 28, 491-503. Scharfe, J. (1960). A new method for aimed one-boat trawling in midwater and on the bottom. Stud. Reu. Gen. Fish. Counc. Mediterr. 13, 1-38. Schmidt-Nielsen, K. ( 1972).Locomotion: Energy cost of swimming, flying, and running. Science 177,222-228. Schuyf, A., and DeGroot, S. J. (1971).An indictive locomotion detector for use in diurnal activity experiments in fish.]. Cons., Cons. Perm. Int. Explor. Mer 34, 126-131. Shaw, E. (1960). The development of schooling behaviour in fishes. Physiol. 2001.33, 79-86. Shazkina, E. P. (1972a). Energy metabolism and food rations of steelhead trout under conditions of the Chernaya Rachka trout industry. Tr. USES Nauchno. Issled. Znst. Morsk. Rubn. Khoz. Okeanogr. 76, 13CL134. (Transl. for Ref. Zh. Biol., No. 61203, pp. 138-144, 1972.) Shazkina, E. P. (197213).Active metabolism in Azov goby. Proc. All-Union Res. Znst. Mar. Fish. Oceanogr. 85, 138-144. (Transl. Ser. No. 3040. Fish. Mar. Serv. Can., 1974.)

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Shuck, H. A., and Kingsbury, 0. R. (1948). Survival and growth of fingerling brown trout (Salmofario) reared under different hatchery conditions and planted in fast and slow water. Trans. Am. Fish. SOC. 75, 147-156. Smit, H. (1965). Some experiments of the oxygen consumption of goldfish (Carassius auratus L.) in relation to swimming speed. Can. J. Zool. 43,623-633. Smit, H., Amelink-Koutstaal, J. M., Vijverberg, J., and von Vaupel-Klein, J. C. (1971). Oxygen consumption and efficiency of swimming goldfish. Comp. Biochem. Physiol. A 39, 1-28. Smith, H. D., and Margolis, L. (1970). Some effects ofEubothrium saluelini (Schrank, 1790) on sockeye salmon, Oncorhynchus nerka (Walbaum), in Babine Lake, British Columbia. J. Parasitol. 56, Sect. 11, 321-322. Smith, L. S., and Newcomb, T. W. (1970). A modified version of the Blazka respirameter and exercise chamber for large fish.J. Fish. Res. Board Can. 27, 1321-1324. Spoor, W. A. (1946). A quantitative study of the relationship between the activity and oxygen consumption of the goldfish, and its application to the measurement of respiratory metabolism in fishes. Biol. Bull. (Woods Hole, Mass.) 91, 312-325. Spoor, W. A., and Drummond, R. A. (1972). An electrode for detecting movement in gradient tanks. Trans, Am. Fish. SOC.101, 714-715. Spoor, W. A., Neiheisel, T.W., and Drummond, R. A. (1971). An electrode chamber for recording respiratory and other movements of free-swimming animals. Trans. Am. Fish. SOC. 100, 22-28. Sprague, J. B. (1971). Measurement of pollutant toxicity of fish. 111. Sublethal effects and “safe” concentrations. Water Res. 5, 245-266. Stasko, A. B. (t975). Progress of migrating Atlantic salmon (Salmo salar) along an estuary observed by ultrasonic tracking. J . Fish Biol. 7, 329-338. Stasko, A. B., and Rommel, S. A,, Jr. (1974). Swimming depth of adult American eels (Anguilla rostrata) in a saltwater bay as determined by ultrasonic tracking./. Fish. Aes. Board Can. 31, 1148-1150. Stasko, A. B., Horrall, R. M., Hasler, A. D., and Stasko, D. (1973). Coastal movements of mature Fraser River pink salmon (Oncorhynchus gorbuscha) as revealed by ultrasonic tracking.J. Fish. Res. Board Can. 30, 1309-1316. Stevens, E. D., and Fry, F. E. J. (-1971).Brain and muscle temperatures in ocean caught and captive skipjack tuna. Comp. Biochem. Physiol. A38, 203-211, Stevens, E. D., Lam, H. N., and Kendall, J. (1974). Vascular anatomy of the countercurrent heat exchanger in skipjack tuna. J. Exp. Biol. 61, 145-153. Stringham, E. (1924).The maximum speed of freshwater fishes. Am. Nut. 58,156-161. Sundnes, G. (1963).Swimming speed of fish as a factor in gear research. Fiskeridir. Skr., Ser. Havunders. 13, 126132. Tesch, F. W. (1974). Speed and direction of silver and yellow eels, Anguilla anguilla, released and tracked in the open North Sea. Ber. Dtsch. Wiss.Komm. Meeresforsch. 23, 181-197. Thomas, A. E., Burrows, R. E., and Chenoweth, H. H. (1964). A device for stamina measurement of fingerling salmonides. Bur. Sport Fish. WiZdZ. ( U . S . ) ,Res. Rep. No. 67, pp. 1-15. Thompson, D. W. (1917). “On Growth and Form,” 793 pp. Cambridge Univ. Press, London. Thorson, T. B. (1971). Movement of bull sharks, Carcharhinus leucas between Caribbean Sea and Lake Nicaragua demonstrated by tagging. Copeia No. 2, pp. 336338. Threadgold, L. T., and Houston, A. H. (1964). An electron microscope study of the “chloride cell” of Salmo salar L. E x p . Cell Res. 34, 1-23.

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Trefethen, P. S. (1956). Sonic equipment for tracking individual fish. U.S. Fish Wildl. Seru. Spec. Sci. Rep.-Fish. 179, 1-11. Trout, G . C. (1957). The Bear Island cod: Migrations and movements. Fish. Invest. Minist. Agric. Fish. Food (G.B.)Ser. I1 Salmon Freshwater Fish. 21, 1-51. Tucker, V. A. (1970).Energetic cost of locomotion in animals. Comp. Biochem. Physiol. A 34, 841-846. Tytler, P. (1969). Relationship between oxygen consumption and swimming speed in the haddock, Melanogrammus aeglefinus. Nature (London) 221,274-275. Verwey, J. (1960). Uber die Orienteir ung wandern der Meerestiere. Helgol. Wiss. Meeresunters. 7 , 51-58. Vibert, R. (1956). Methode pour I’btude et I’amelioration de la survie des alevins de repeuplement (triuites et saumons). Ann. Sta. Cent. Hydrobiol. Appl. 6, 347-439. Vincent, R. E. (1960).Some influences of domestication upon three stocks of brook trout (Saluelinusfontinalis Mitchill). Trans. Am. Fish. Soc. 89, 35-52. von Kausch, H. (1968). Der Einfluss der Spontanaktivitat auf die Stoffwechselrate junger Karpfen (Cyprinus carpio L.) im Hunger und bei Fiitterung. Arch. Hydrobiol., Suppl. 33,263-330. Wales, J. H. (1950). Swimming speed of the western sucker Catostomus occidentalis Ayres. Calif. Fish Game 36, 433-434. Walters, V., and Fierstine, H. L. (1964). Measurements of swimming speeds of yellow fin tuna and wahoo. Nature (London) 202,208-209. Wardle, C. S. (1975).Limit of fish swimming speed. Nature (London)255, 725-727. Warren, C. E., and Davis, G. E. (1967). Laboratory studies on the feeding, bioenergetics and growth of fish. In “The Biological Basis for Freshwater Fish Production” (S. Gerking, ed.), pp. 175-214. Blackwell, Oxford. Watanabe, N. (1942). Measurements on the bodily density, body temperature, and swimming velocity “katuwu”, Euthynnus vagans (Lesson). Nippon Suisan Gakkaishi 11, 146-148. Weaver, C. R. (1963). Influence of water velocity upon orientation and performance of adult migrating salmonids. U . S . Fish Wildl. Serv., Fish. Bull. 63,97-121. Weaver, C . R. (1965). Observations on the swimming ability of adult American shad (Alosa sapidissima). Trans. Am. Fish. SOC.94, 382-385. Webb, P. W. (1971a). The swimming energetics of trout. I. Thrust and power output at cruising speeds.]. Exp. B i d . 55, 489-520. Webb, P. W. (1971b). The swimming energetics of trout. 11. Oxygen consumption and swimming efficiency. J . E x p . Biol. 55,521-540. Webb, P. W., and Brett, J. R. (1973). Effects of sublethal concentrations of sodium pentachlorophenate on growth rate, food conversion efficiency, and swimming performance in underyearling sockeye salmon (Oncorhynchus nerka).]. Fish. Res. Board Can. 30, 49S507. Whitworth, W. R., and Irwin, W. H. (1964). Oxygen requirements of fishes in relation to exercise. Trans. Am. Fish. Soc. 93. 209-212. Wiehs, D. (1973a). Optimal fish cruising speeds. Nature (London) 245,48-50. Wiehs, D. (197313). Hydromechanics of fish schooling. Nature (London)241,290-291. Wiehs, D. (1974). Energetic advantages of burst swimming of fish. J. Theor. Biol. 48, 215-229. Winberg, G. G. (1956).“Rate of Metabolism and Food Requirements of Fishes,” 251 pp. Beloiussian State Univ., Minsk (In Russian). (Fish. Res. Board Can., Trans]. Ser. No. 194.) Wohlschlag, D. E. (1957). Differences in metabolic rates of migrating and resident freshwater forms of an arctic whitefish. Ecology 38, 502-510.

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Wohlschlag, D. E. ( 1964). Respiratory metabolism and ecological characteristics of some fishes in McMurdo Sound, Antarctica. Antarct. Res. Ser. 1, 33-62. Wohlschlag, D. E., Cameron, J. N., and Cech, J. J., Jr. (1968). Seasonal changes in the respiratory metabolism of the pinfish (Lagodon rhomboides).Contrib. Mar. Sci. 13, 89-104. Woodhead, P. M. J. (1964). Diurnal changes in trawl catches of fishes. Rupp. P.-V. Reun., Cons. Int. Erplor. Mer 155, 35-44. Yuen, H. S. H. (1966). Swimming speeds of yellowfin and skipjack tuna. Trans. Am. Fish. Soc. 95,203-209. Yuen, H. S. H. (1970). Behaviour of skipjack tuna, Katsuwonus pelamis, as determined by tracking with ultrasonic devices.J. Fish. Res. Board Can. 27, 2071-2079. Yuen, H. S. H., Dizon, A. E., and Uchiyama, J. H. (1974). Notes on the tracking of the Pacific blue marlin, Makaira nigricans. In “Proceedings of the International Billfish Symposium, Kailua-Kona, Hawaii, 9-12 August 1972” (R. S. Shomura and F. Williams, eds.), Part 2, Review and Contributed Papers, pp. 265-268 (NOAA Tech. Rep. NMFS SSRF-675). NOAA, Honolulu. Zaitsev, V. P., and Radakov, D. V. (1960). Submarines in fishery research. I n “Soviet Fisheries Investigations in North European Seas” (1. J . Marty et al., eds.), pp. 463-466. VNIRO and PINRO, Moscow.


3 HYDRODYNAMICS: NONSCOMBROID FISH PAUL W.WEBB

. . .. . . . . . .. . ..

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Steady Swimming . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Biological Approach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Hydromechanical Approach ......................... C. Drag Reducing Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Unsteady Propulsion . . . . . . . , . . . . . . . . . . . . . . . . . . , , . . . . . , . . . . . . . . A. Kinematics . . . . ..,... .. . .. .............................. B. Acceleration Performance . . . . , . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Mechanics ... . . .. .. .. .. . .. ......... ....... .... ... .. ......... ........................ D. Work Done in Acceleration E. Drae Reduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Unsteady versus Steady Propulsion.. . . . . . . . . . . , . . . . . . . . . . . . . . . . A. Mechanics and Structure . . , . . . .. , .. . . . .. . . .. .. ... . . ... B. Performance , . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , , , . , . . . . . . . . V. Mechanics of Median and Paired Fin Propulsion . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Y

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190 191 192 199 218 22 1 222 226 226 226 227 228 228 229 230 232

FISH PHYSIOLOGY, VOL. VII Copyright @ 1978 b y Academic Press, Inc. All rights oi reproduction in any form re5ewed. ISBN 0-12-350407-4

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Symbols

A CD Cf C f lam C f turb DF

d dT

f e

m P PK PT R L

S t

U V W W

6* 77P

K

A Y Pe

d

tailbeat amplitude drag coefficient frictional drag coefficient frictional drag coefficient for laminar boundary layer flow turbulent drag coefficient for turbulent boundary layer flow frictional drag body depth; mean of depth and width for equivalent rigid body trailing edge depth tailbeat frequency length virtual mass per unit length total rate of working rate of energy loss to wake thrust power Reynolds number wetted surface area time swimming speed velocity of propulsive wave lateral velocity of propulsive segments resultant velocity of water displaced by propulsive segments displacement thickness of boundary layer mechanical efficiency of caudal propeller angle subtended by plane normal to the trailing edge to transverse axis of motion of that edge propulsive wavelength kinematic viscosity of water density of environment phase difference

I. INTRODUCTION Modem studies of fish propulsion mechanics can be considered to have started with the use of cinematographic techniques by Marey (1895). Although many years have elapsed since Marey’s pioneer work, research is still concerned with the same problems: How do fish swim? What is the resistance to motion? How much power is expended in swimming? Significant advance toward answering these questions has largely been made between 1960 and the mid-1970’s. This advance can be attributed to a technological advance in the de-

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sign of efficient water tunnel respirometers (Marr, 1959; Blaika et al., 1960; Brett, 1963, 1964) and theoretical advances in hydrodynamic models, particularly by Lighthill (1969, 1970, 1971) and Wu (1971a,b,c,d). Fish propulsion patterns are extremely diverse (see Chapter 1). Although significant advances have been made in the understanding of some swimming modes, the majority have not progressed beyond the descriptions given in Breder’s (1926) collation of locomotory types. Emphasis has been placed on the relatively simple mechanics of body/caudal fin propulsion. Following Gray’s ( 1933a,b) classical discussion of propulsion in the eel, numerous quantitative observations have been made relating body and caudal fin movements to swimming speed (Bainbridge, 1958, 1963; Magnuson and Prescott, 1966; Yuen, 1966; Fierstine and Walters, 1968; Pyatetskiy, 1970a; Hunter and Zweifel, 1971; Smit et al., 1971; Webb, 1971a, 1973a); such observations have been encompassed by numerous theoretical models (Webb, 1975a). In contrast, the more complex locomotor patterns involving paired and noncaudal median fins have progressed little beyond qualitative descriptions of fin movements (Harris, 1937, 1953; Breder and Edgerton, 1943; Lissman, 1961; Nursall, 1962; Webb, 1973b). The rapid advance in understanding some swimming modes, contrasting with little advance in others, sets constraints on any discussion of propulsion mechanics. Only qualitative discussion, often speculative, is possible for swimming modes other than those involving body/ caudal fin movements. The latter are amenable to quantitative analysis. In addition to these constraints, others apply as a result of research emphasis on certain activity levels. These levels are steady swimming at cruising (sustained), prolonged, and sprint (burst) activities. Unsteady activities at acceleration (burst) and routine levels have been neglected. These constraints restrict the present discussion largely to bodykaudal fin propulsion in steady swimming activity.

11. STEADY SWIMMING Biologists and hydrodynamicists have taken different approaches to the problems of how fish swim and the calculation of thrust and power required. The traditional biological approach to the mechanics of fish swimming has not led to satisfactory quantitative solutions. The hydrodynamic approach has led to numerous models amenable to quantitative solution but these have largely been neglected by

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biologists. Recent hydromechanical models have led to generalizations on the mechanical importance of variation in body and fin morphology. Concerted efforts to rectify the two approaches have recently begun (Wu et al., 1975; Pedley, 1977; Alexander and Goldspink, 1977; this volume). A. Biological Approach

1. GENERATION OF THRUST

The mechanisms by which fish generate thrust have been described in terms of arbitrarily defined “segments” of the body and/or fins, regarded by Gray (1968) to be “the fundamental unit of aquatic undulatory propulsion.” Each segment is considered in a quasi-static time frame, i.e., at any instant the forces acting on a segment are the same as those for an identical segment moving steadily at the same speed and subtending the same angle to incident flow. The forces acting on the segment can be qualitatively described in terms of the. change in momentum of water deflected by the surface and by comparing a segment with a hydrofoil (Borelli, 1680; Pettigrew, 1873; Marey, 1874, 1895; Breder, 1926; Gray, 1933a, 1968; Bainbridge, 1963). Use of such quasi-static models was very effective in establishing the kinematic requirements for the generation of thrust (Gray, 1933a,b,c). Gray showed that thrust develops only when a propulsive segment subtends a positive angle of attack to the incident water flow. This occurs when a propulsive wave travels backward over the body at a velocity greater than the speed of forward swimming. The relationship between muscle shortening activity and the formation of propulsive movements has recently been described by Blight (1977). 2. THRUST,DRAG,AND POWER The quasi-static approach can be used to calculate net thrust and power. These are obtained by integrating instantaneous forces for each segment throughout a propulsive cycle (von Holste and Kuchemann, 1942; Parry, 1949; Gero, 1952; Taylor, 1952; Gray, 195313).Most models based on these principles are somewhat unsatisfactory because they usually involve too great an oversimplification of both body movements and body form and do not take into account interactions between segments (Webb, 1975a). Drag and power requirements for swimming fish have most commonly been calculated assuming a swimming fish can be compared with an equivalent manmade rigid body (the rigid-body analogy). The

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analogy apparently stems from classicial observations by Sir George Cayley (ca. 1809, see Gibbs-Smith, 1962) who noted the streamline profiles of trout and dolphin, two animals capable of impressive swimming performance. In using the rigid-body analogy, drag may be calculated from standard hydrodynamic equations or determined by drag measurements on dead, anesthetized, or model fish (Magnan, 1930; Kempf and Neu, 1932; Denil, 1936; Harris, 1936; Richardson, 1936; Parry, 1949; Gero, 1952; Gray, 1936, 1957; Bainbridge, 1961; Kent et al., 1961; Osborne, 1961; Brett, 1963, 1965; Sundnes, 1963; Smit, 1965; Smit et al., 1971; Brown and Muir, 1970; Pershin, 1970; Pyatetskiy, 1970a,b; Webb, 1975a).

3. THE RIGIDLBODYANALOGY Details of flow patterns and the origins of drag for rigid bodies are given in standard hydrodynamic texts (e.g., Prandtl and Tietjens, 1934a,b). The main concepts pertinent to a discussion of drag are summarized by Webb (1975a). Drag arises from frictional and inertial (pressure) forces. The former arises as a result of viscosity in areas of flow with large velocity gradients. Pressure drag results from distortion of flow around solid bodies and, since it depends on the shape of a body, is often referred to as form drag. The flow around a body is divisible into two regions (Fig. 1).At the body surface, there is no slip between the body and the water, and the velocity is equal to that of the body. The velocity increases rapidly to 1% of that of the undisturbed free stream over a very shprt distance from the body. This region of flow is defined as the boundary layer and is characterized by steep velocity gradients; consequently, frictional resistance arises in this region. Beyond the boundary layer is a region of outer flow where velocity gradients are negligible and viscosity can be neglected. The outer flow is deflected around the body, and this deflection can lead to pressure drag. The velocity of the water increases as it is deflected around the front surface of a body. A maximum velocity is attained at the shoulder, the point of maximum thickness. Velocity decreases downstream over the tapering portion of the body. The changes in velocity, resulting from distortion of the flow, are associated with pressure changes. From Bernoulli’s theorem:

where AP, pressure difference; U , velocity.

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PRESSURE adverse

GRADIENTS

OUTER FLOW

favorable

LAMINAR TRANSITIONAL TURBULENT

BOUNDARY-LAYER I AMINAR

ATTACHED

TRANSITIONAL (PARTLY LAMINAR, PARTLY TURBULENT

TURBULENT

Some causes of Transition and Turbulence I) poor body shape. 2) adverse pressure gradient. 3) turbulence in outer flow. 4)surface roughness. 5) large size and/or speed.

Separation is encouraged SEPARATED

by adverse pressure gradients.

Fig. 1. Diagrammatic representation of streamline flow about a streamline body. The body is shown at rest relative to the fluid. The flow can be divided into two regions, the outer flow and the boundary layer flow (shown stippled). The boundary layer is a thin skin ofwater surrounding the body across which the velocity of the water increases from zero at the surface to the velocity of the free stream or outer flow. Flow in either region may b e laminar, turbulent, or may be transitional, changing from laminar to turbulent flow. The boundary layer separates from a solid body near the downstream edge (trailing edge) as a result of backflow in the boundary layer. The separated boundary layer forms a wake downstream of the body. Adverse pressure gradients, with increasing pressure in the opposite direction to mean flow, occur downstream of the point of maximum thickness (shoulder) of the body. Adverse pressure gradients facilitate premature boundary layer separation. Transition is encouraged by poor body shape, adverse pressure gradients, turbulence in the outer flow, surface roughness, and high Reynolds numbers (large size and/or speed). (From Webb, 1975a, Bull. Fish. Res. Board Can. No. 190, 159 pp.)

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Consequently, the pressure in the water decreases up to the shoulder, and subsequently increases toward the trailing edge. The former pressure change results in a favorable pressure gradient increasing in the direction of mean flow. The increase in pressure downstream results in an unfavorable pressure gradient increasing in the opposite direction to mean flow. The unfavorable pressure gradient interacts with the boundary layer, and together with frictional forces reducing boundary layer velocities, eventually causes back flow in the boundary layer. As a result the boundary layer separates from the body and a wake is formed. This dissipates kinetic energy and conti-ibutes to form drag. In addition, the downstream flow remains distorted and the net pressure across the wake is lower than in the upstream undisturbed water. Therefore, there is also a net pressure force acting along the body resisting motion. The magnitude of the frictional drag force is readily calculated from the standard Newtonian equation:

1 Df = z p eSU2Cf

( 2)

where Df,frictional drag; pe, density of environment; S, wetted surface area; Cf, drag coefficient. Power expended against frictional drag will be the product DfU . Cf depends on a nondimensional number, Reynolds number, and boundary layer flow conditions. Reynolds number can be visualized as a ratio of inertial to viscous forces that can be closely approximated to

where RL, Reynolds number; e, length, the characteristic dimension related to size; v, kinematic viscosity of water. For well-engineered bodies and smooth flat plates with the long axis at zero angle of incidence to the flow, boundary layer flow tends to be laminar up to RL of approximately 5 x lo5.This Reynolds number would be achieved, for example, by a 30 cm fusiform body or flat plate at a speed of 180 cm/sec (6 t/sec). Above this critical Reynolds number transition tends to occur to turbulent boundary layer flow. Transition is encouraged by such factors as turbulence in the outer flow, adverse pressure gradients, and surface roughness as well as large size or speed that increase RL. Cf may be expressed as a function ofRL.For laminar boundary layer flow Cf lam = 1.33 R L - 0 . 5 (4)

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and for turbulent boundary layer flow

Cf turb = 0.072RL-o.2

(5)

Frictional drag calculated from Eqs. (4) and (5)is greater at a given

RL for turbulent boundary layer flow than for laminar boundary layer flow because of the additional motions of water particles in the former flow pattern. Pressure drag is more difficult to determine. It is dependent on the point at which the boundary layer separates. If the boundary layer separates prematurely, that is, relatively close to the shoulder on a streamlined body, pressure drag is greatly increased. Pressure drag is lowest on well-designed fusiform bodies when separation occurs close to the trailing edge. Then pressure drag can be calculated as a multiple of Cf so that

c, = cf [ i + i.s(d/e)1.5+ 7(d/t)31

( 6)

where C,,, total drag coefficient; d, mean of depth and width. The factors enclosed in the square brackets of Eq. (6) give values of the order of 1.2 for fish (Bainbridge, 1961). Equations (2) to (6) calculate the theoretical drag for a rigid body geometrically similar to a fish. This is the minimum possible drag for a swimming fish. Gray (1936) first applied such calculations of theoretical drag to compare thrust power required with estimated muscle power available for a porpoise and a dolphin. The animals were probably swimming at sprint speeds. Muscle power was calculated by comparison with the sustained performance of an Olympic rowing crew. Gray found that the estimates of power required exceeded the estimates of muscle power available, the result being the basis for “Gray’s Paradox.” Gray’s Paradox has been widely interpreted to imply that the drag of swimming fish and cetacea is lower than that of the best engineered manmade body. In order to attempt to improve on theoretical drag, measurements of drag have been made for dead fish, anesthetized fish, and models, collectively referred to as dead drag measurements. These are reviewed by Webb (1975a). Such measurements are of little value however because pressure drag is greatly increased as a result of fluttering of fins and the body or inadequate methods. The magnitude of dead drag measurements expressed as drag coefficients as a function of RL is included in Fig. 5. Results from drag measurements, both of theoretical and dead drag, have been inconclusive with respect to Gray’s Paradox, some apparently being supportive (Osborne, 1961;

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Brett, 1963, 1965; Smit et d.,1971) while others conflict (Bainbridge, 1961; Walters, 1966; Smit, 1965). With the perspective of time, it is clear that Gray did not have complete data (Bainbridge, 1961).Consequently, it is unfortunate that much subsequent effort has been expended in trying to explain Gray’s Paradox rather than evaluating the underlying assumptions. Bainbridge (1961) has discussed the question of muscle power, and his higher values for muscle power loading are now most commonly used. Using more comprehensive data than were available to Gray, Bainbridge (1961) found little problem for fish and cetacea in meeting theoretical drag power requirements. 4. FLOWA N D DRAGOF A SWIMMING FISH The basic mechanical assumption of the rigid-body analogy is that the flow around a swimming flexing fish is mechanically equivalent to that around an equivalent rigid body. There is currently no evidence to support this assumption, while the scant data available tend to refute the assumption. The body of most fish is not held rigid during swimming. Exceptions are apparently fish such as Carangids and some Scombrids, and also Cetaceans (Breder, 1926; Walters, 1962; Hertel, 1966; Fierstine and Walters, 1968; Magnuson, 1970). In most fish, both the body and caudal fin execute lateral movements with propulsive segments moving across, and at some angle to the incident flow. Large pressure differences will be set up on either side of a propulsive segment. As a result cross-flows are expected around dorsal and ventral surfaces leading to boundary layer separation and formation of a more extensive wake than for an equivalent rigid body. Such cross-flows have been observed by means of threads and dyes (Houssay, 1912; Rosen, 1959; Gray, 1968; Webb, unpublished observations). Pressure recordings along the.body of a swimming fish (DuBois et al., 1974) also suggest strong cross-flow (Section II,C, 1,c). Aleyev and Ovcharov (1969, 1971) present photographs of cross-flow about several species that show separation over the posterior half to one-third of the body of fish swimming in subcarangiform modes. The formation of a relatively extensive wake as a result of swimming movements will result in increased distortion of the outer flow and increased pressure drag. Some fish approaching and including the carangiform mode with lunate tail minimize this problem by concentrating thrust at the caudal fin while holding the body fairly straight and by streamlining of the caudal peduncle (Hertel, 1966; Magnuson, 1970) (see Chapter 4).

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Frictional drag of many fish is also expected to be greater than that for an equivalent rigid body as a result of premature transition from laminar to turbulent boundary layer flow. Observations by Allan (1961), Walters (1962), and Aleyev and Ovcharov (1969) show that projections such as eyes and nares or gill effluent can cause such premature transition. Turbulence is probably induced in some fish to reduce the chance of flow separation, notably in elasmobranchs covered with projecting scales which make the body surface rough (Walters, 1962; Bone and Howarth, 1966; Ovchinnikov, 1966; Bone, 1972). In addition, locomotory movements themselves will increase local frictional drag of propulsive segments. Such segments move discontinuously and with a mean resultant velocity higher than that of the forward speed of the fish. The boundary layer thickness is reduced on the leading surface and increased on the trailing surface, with an increase in the net velocity gradient in the boundary layer. Therefore this boundary layer thinning phenomenon increases net frictional drag (Lighthill, 1971; Webb, 1973a). An observation by Stevens (1950) has been widely used to support an alternate hypothesis that a laminar boundary layer is found under conditions where turbulent boundary layer flow would be expected. Stevens observed that the only disturbance caused by a dolphin swimming in phosphorescent water was two diverging lines in the wake. In contrast, the wake downstream of a seal was highly turbulent. The observations are clearly for the wake downstream of the trailing edge and not for the flow in the boundary layer anterior to that edge. Consequently no direct information on laminar or turbulent flow conditions in the boundary layer can be deduced. In practice, Stevens’ observation implies that the boundary layer flow remained attached for the dolphin but separated prematurely for the seal. Such separation would result in a highly turbulent wake as indicated by the extensive phosphorescence in the seal’s wake. The phosphorescence in the wake of the dolphin was probably caused by tip vortices (von Mises, 1945; see also Chapter 4) about the tail flukes (Webb, 1975a). These considerations suggest that the flow about a swimming fish will not be mechanically similar to that about a rigid body. Unfortunately, observations are few, and rigorous experiments have so far proved technically difficult (see, e.g., Allan, 1961). Nevertheless, it is clear that the rigid-body analogy should not be used to calculate swimming thrust or power unless the basic assumptions can be supported. This seems unlikely for most fish, so that further use of the rigid-body analogy is difficult to justify for calculating thrust and

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power for steady propulsion. Therefore an alternate method is desirable.

B. Hydromechanical Approach

1. MODELS Theoretical physicists, mathematicians, and engineers have usually attempted to formulate mathematical models describing the observed kinematics of fish. These lead to various hydromechanical models of how fish swim which are amenable to quantitative solution. Earliest hydrodynamic models were usually based on a quasistatic approach (Taylor, 1952; Gray, 1953b) and considered simplified undulatory motions in real fluids. Such models are generally oversimplified in terms of real fish motions and also in terms of real fish shapes (Webb, 1975a). In addition, interaction between segments is not included as Gray (1933a, 1953b) points out in connection with his quasi-static approach to propulsion models. Later models, starting with Gadd (1952) and particularly Lighthill (1960) and Wu (1961), considered more realistic fish-type motions but in an inviscid (frictionless) fluid when viscosity is neglected. Both resistive (viscous) and reactive (inertial) forces are involved in fish propulsion but the relative magnitude of these varies with Reynolds number. Reynolds numbers for fish commonly exceed lo3 when inertial forces are very much greater than viscous forces. Consequently, reaction, inertial forces are most important in thrust generation and resistive, viscous forces can initially be neglected. Lateral flattening typical of fish enhances the magnitude of inertial forces so that viscosity effects are further reduced relative to inertial effects (Lighthill, 1969, 1970). Although most models of fish propulsion have treated fishlike motions in an inviscid fluid, several have considered the effects of viscosity on model predictions. Such discussion leads to approximate solutions that further support the hypothesis that viscous forces are negligible at higher Reynolds numbers of the order observed for fish (Lighthill, 1960, 1970; Wu, 1971d). Numerous hydromechanical models have been formulated since the early models by Gadd (1952), Lighthill (1960), and Wu (1961) (see Webb, 1975a, for references). More recent models have emphasized a continuous range of propulsion patterns within which the various modes described by Breder (1926) are 'wlrvenient reference points. Variation in body/caudal fin locomotory systems can be mechanically

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separated into two types for nonscombroid fish up to the lunate tail condition and for scombroid fish, cetacea, and some extinct aquatic reptiles with a lunate tail (Lighthill, 1969). The models therefore provide a homogeneous approach to fish propulsion questions. However, the majority of models are mathematically complex and would require measurement of parameters that are difficult to obtain with reasonable or repeatable accuracy ffom live fish. Models formulated by Lighthill (1970) and Wu (1971a,b,c,d) lead to an important conclusion that for steady swimming, an acceptable estimate of the mean rate of working and mean thrust developed by the propulsive wave can be obtained from a simple treatment of trailing edge kinematics. This solution, obtained by Lighthill (1969),provides a key framework about which biological problems may be approached. Most hydromechanical models have also emphasized small amplitude harmonic lateral movements of long slender fish of constant depth. The assumption that lateral movements are harmonic permits mathematical treatment of overall propulsive movements, but is not necessary for detailed analysis (Lighthill, 1971). The assumption is not unreasonable, since the difference between observed fish motions and simple harmonic motion is small (Gray, 1933a). Furthermore, most fish are not long and slender, and neither are they of constant depth. Some of the most important recent advances in the physical approach to fish propulsion have come from models that take into account fish morphological variation ( Lighthill, 1969, 1970, 1971; Wu, 1971a,b,c,d; Wu and Newman, 1972; Newman, 1973; Newman and Wu, 1973). Current understanding of fish propulsion is based almost entirely on these recent studies that lead to new functional interpretations of morphology and swimming mode of fish. 2. LIGHTHILL’SSIMPLIFIEDBULKMOMENTUM MODEL In order to consider how fish swim, and to calculate mechanical power developed, the bulk momentum model described by Lighthill (1969) will be discussed. The detailed models of Lighthill (1960,1970) and Wu (1971a,b,c,d) consider mechanics and interaction among all propulsive segments, and lead to the conclusion that bulk momentum changes can be predicted from trailing edge kinematics. Lighthill’s bulk momentum model considers these latter movements and associated forces, and consequently provides a simple reference point about which to discuss locomotion problems. In the first instant, it is convenient to consider a long slender fish of negligible thickness compared to its length and of constant depth. A

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propulsive wave passes backward over the fish’s body at a velocity, V, greater than the fish’s forward velocity, U . Propulsive segments execute small amplitude lateral harmonic movements, the amplitude of which increases with distance along the body to a maximum at the trailing edge. These various assumptions will be subsequently relaxed. To visualize how the net effect of interacting propulsive segments can be described in terms of trailing edge motions, consider two adjacent segments of the fish body. Each segment is of unit length. It accelerates the water in its vicinity and thrust is generated proportional to the product of the mass of water affected and the increase in velocity given to that mass. Let the incident velocity to the first segment equal U . The water is accelerated to U1 > U , in time t, and the thrust T1 developed by the first segment is proportional to

u, - u

T1am-

t

where m is the mass of water affected. The incident velocity at the second segment is U , . Because amplitude increases along the body, the second segment further increases the velocity of the water to U 2 .Thus, thrust T2 is generated by the second segment proportional to

Since the fish is assumed to be of constant depth, m will be the same for each segment. As the propulsive wave will travel along the fish at reasonably constant velocity, t will also be the same for each segment. From Eqs. (7) and (8) the total thrust from both segments is then proportional to u 2

T1+T2am-

-u t

and hence the total velocity increment can be calculated from the kinematics of the second segment. This example shows that the propulsive wave can be visualized as a series of interacting segments that progressively increase the momentum of water in the vicinity of the fish to reach maximum values at the trailing edge. The rate at which momentum is shed by the trailing edge is equal to net thrust on the fish, generated by the propulsive movements of all interacting propulsive segments.

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Ligh6ill's bulk momentum model shows how net thrust and power generated by propulsive movements may be simply obtained from the kinematics of the trailing edge. From Eqs. (7) to (9) two aspects must be taken into account to calculate momentum changes of the water in the vicinity of the fish. These are the mass of water affected and the movements of the trailing edge, the latter accelerating the water to increase its momentum and hence generating thrust. As soon as a segment begins to move, the water in the vicinity is set in motion. The mass of water affected by movements of a segment is the virtual mass. At the trailing edge, m is given by

m = k p e r dT2 4 where dT,trailing edge depth; pe, density of environment; k, constant dependent on body sectional shape. The dimensions for Eq. (10) are mass x length-'. In order to understand how propulsive movements generate thrust, momentum changes are calculated for a water slice accelerated by a segment. In the small amplitude case, a water slice is given by Eq. (10) as a cylinder of unit length, with a diameter equal to dT oriented normal to the axis of progression of the fish. Orientation of the water slice normal to the segment becomes important for large amplitude motions, and the small amplitude restriction is relaxed below (Section II,B,4,a). The effects of propulsive movements on the water slice are considered for a propulsive segment at the trailing edge (Fig. 2). Movements of the segment are followed for a short period of time, t , after which the water slice is just left behind at the trailing edge. The length of the segment is defined for mathematical convenience in relation to the distance V t covered by the propulsive wave traveling backward over the body at velocity V. During the same period of time, the segment moves forward a distance Ut at the velocity of the fish U , and the trailing edge moves laterally a distance Wt at the trailing edge lateral velocity W. Thus the segment moves from aa, to bb, in Fig. 2. The water slice just left behind by the trailing edge at t is displaced a distance w t , given a velocity w smaller than W. The velocity w given to the water slice can be calculated from the geometry of movements of the segment. From similar triangles

wt

wt= and

(V - U ) t Vt

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B

Vt

Wt

Fig. 2. Simplified representation of body and trailing edge movements for the calculation of thrust and power generated by propulsive movements using Lighthill’s bulk momentum model. (A) Tracings of successive positions at 0.015 sec intervals of the body centerline of a trout (30cm total length) swimming at 50 cm/sec. The position of a water slice is represented that is just left behind by the trailing edge at position 4. (B) Representation of a segment at the trailing edge at two instances in time. The position of a water slice is illustrated that‘is just left behind by the trailing edge segment. This segment moves from u u , to bb, in time t. Further explanation is given in the text. (Modified after Webb, 1975a, Bull. Fish. Res. Bourd Can. No. 190, 159 pp.)

The momentum given to the water as a result of movements of the trailing edge segment is equal to mw. Water with momentum mw is shed to the wake (i.e., left behind at the trailing edge) as the fish moves forward at velocity U . Thus the rate of shedding momentum (thrust) is mwU. Power is generated by the trailing edge working against the wake momentum at the rate W. Therefore the net total power, P, expended b y propulsive movements is given by

P=mwUW

( 13)

P has the dimensions of mass x length’ x time-3 and is calculated in ergs sec-I or watts.

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P is the total rate of working of the propulsive system, but not all the power generated is available as thrust power to overcome drag. Some power is lost energy to the wake. This lost component arises from the energy required to increase the momentum of the water in the vicinity of the fish. Since each water slice is accelerated to w , the lost energy is equal to the kinetic energy of the water shed into the wake at U . The lost energy, PK,is therefore given by

The power component to overcome drag, the thrust power PT, is found by difference from Eqs. (13)and (14)

PT = P - PK

( 15)

In using a bulk momentum approach to fish propulsion, it is important to note that the average effect of all propulsive segments is obtained for a complete propulsive cycle. Thrust calculated for any shorter period of time must take into account instantaneous contributions of all segments. Parameters for use with Lighthill’s bulk momentum model are easily measured from photographs of swimming fish (Webb, 1971a, 1973a, 1975a). Measurements of the tailbeat frequency, f, amplitude, A, propulsive wavelength, A, and trailing edge depth, dT,are required at any speed, U . Then, assuming simple harmonic motion V

=fx

( 16)

By substitution for W and V in Eq. (12) we have

and m is given by Eq. (10). 3. EFFECTSOF BODYFORM O N

SWIMMING

MECHANICS

a. Body and Fin Sections. The virtual mass of a propulsive segment depends on the structure of the body and fins comprising that segments’ cross-sectional shape (Lighthill, 1970). The constant k in Eq. (10) is close to 1 for many typical fish body or fin sections. k is usually less than 1where the body section includes both body and fins (Fig. 3). Lowest values of k in this case occur when the fins represent

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A

k = 1.0

B

C

1.0 0.83

D

0.76

Fig. 3. Diagrammatic representation of some body and fin cross section shapes and values of k for Eq. (10).(A) Elliptical body section without fins; (B) fin section as at the caudal fin trailing edge; (C) elliptical body section with equal median fins comprising 25%of total depth; (D) circular body section with equal median fins comprising 25%of total depth. Values for k based on Lighthill (1970).

approximately 25% of total depth, a not uncommon value for fish. Thus for a fish with an elliptical body section and equal dorsal and ventral fins comprising 0.25 total depth, k would be 0.83, and for a circular body section but the same fin depth, k would be 0.76. k would be closer to 1 for greater proportions of fin or body depth and also for a single dorsal or ventral fin comprising the same proportion of total depth (Lighthill, 1970; Wu, 1971~).

b. Znteraction between Median Fins. The depth of most fish is not constant, but is discontinuous because of median fins and tapering b,ody Sections. The trailing edge of any fin does work in the same way as the trailing edge of the body. A wake is formed downstream of any trailing edge carrying that ‘momentumand energy given by the trailing edge movements. In hydromechanical theory, a vortex sheet is shed at any trailing edge carrying that momentum and energy. The vortex sheet concept is important in treating flow in inviscid fluids. It permits more realistic treatment of discontinuous flow patterns to describe flow that would occur in a fluid with viscosity (Prandtl and Tietjens, 1934a,b; Schlichting, 1968). The vortex sheet shed b y an upstream median fin flows along the body at the speed of the fish. Where there is a second re-entrant me-. dian fin (that is, a second downstream fin with depth exceeding that of the vortex sheet) the vortex sheet is absorbed at the second fin’s lead: ing edge. Thus the gap between the fins is filled by a vortex sheet. The vortex sheet shed by the second fin’s trailing edge is dictated by that edge’s motion, and the upstream vorticity does not contribute to the wake. However, the vortex sheet filling the gaps between the fins functions in the same way as a continuous fin (Lighthill, 1970; Wu, 1971c,d; Wu and Newman, 1972; Newman and Wu, 1973; Newman, 1973).

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The phenomenon of vortex sheets filling gaps between fins leads to improved propulsive effectiveness for ~o mechanically different body and median fin patterns. The first pattern is typical of Gadids, where the gaps between fins are small. The second is typical of elasmobranchs where gaps are large. In both cases, the vortex sheet filling the fin gap does not reduce thrust generated nor energy loss (efficiency). However, the surface area of the body is reduced between the fins so drag will be lower (Lighthill, 1970; Wu, 1971c,d). In contrast to the case where fin gaps are small, thrust can be increased in addition to the reduction in drag when fin gaps are large (Lighthill, 1970; Wu, 1971d). This occurs when the phase difference between momentum carried by the vortex sheet and the lateral movement of the trailing edge exceeds 0 . 5 ~ The . phase difference in lateral movements between an anterior fin trailing edge at a positionx, along the body and a posterior fin leading edge at X2 is given by

However, the vortex sheet shed by the anterior fin moves downstream at velocity U while the propulsive wave travels backwards at a velocity, V, greater than U . Consequently, the phase difference, 4, between body motions incident to the vortex sheet is

Gray ( 1933c) shows figures of the elasmobranch Acanthias vulgaris (8 = 46.0 cm) with U = 17.8 cm/sec, and V = 25.6 cm/sec. The trailing edge of the first dorsal fin was about 19.4 cm from the nose. The second dorsal fin was small so the bulk of the vortex sheet from the first dorsal fin trailing edge would be absorbed at the caudal fin leading edge, approximately 37.1 cm from the nose. These data give a value of 4 of 0.52~. In many fish, the depths of the downstream fin leading edges are less than the depth of upstream trailing edges. Then, the upstream vortex sheet will not be completely absorbed at the downstream leading edge. Under these conditions upstream trailing edges contribute to both thrust and energy losses (Wu, 1971c,d). However, the net contribution of such anterior edges is likely to be relatively small. Although the virtual mass of these sections is higher than the trailing edge, lateral displacement and hence velocities and the momentum given to the water will be small in comparison with body trailing edge contributions.

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Just as gaps between median fins can lead to reduced drag without significantly affecting thrust and efficiency, so can scooping out the caudal fin. The central portion of a swept back caudal fin, typical of many pelagic fish, will be filled by a vortex sheet. The tail is then mechanically similar to a structurally complete tail fin (Lighthill, 1970) but drag will be reduced as a result of the decreased area. Relatively large savings in drag are possible because the drag per unit area will increase to a maximum along the body as a result of increases in lateral velocity of propulsive segments with caudally increasing amplitude. Then boundary layer thinning and hence frictional drag will increase toward the caudal fin trailing edge.

c . Viscosity and Virtual Mass. The effects of viscosity in real fluids are initially neglected by hydromechanical models. The virtual mass of a segment is affected by the boundary layer and hence viscosity. The importance of this modification to virtual mass is partially dependent on the distribution of depth along the body. Weihs (personal communication) showed that the virtual mass was reduced according to m - 2p6*d (21) where 6* is the displacement thickness of the boundary layer. Precise determination of 6* is difficult because of boundary layer thinning and possible boundary layer separation upstream of a segment (D. Weihs, personal communication). Standard hydrodynamic equations suggest that correction for virtual mass would be approximately 1.5% at the trailing edge of a 10 cm fish of constant depth swimming at 50 cm/sec, decreasing to 0.9% for a geometrically similar 100 cm fish swimming at the same speed. The thickness of the boundary layer increases along the length of any body and also increases with time. Where body depth varies, as with discrete fins, the boundary layer will tend to increase in thickness along each fin. Consequently, the boundary layer may be thinner for a discrete fin compared to a similar point on the body of a fish of constant depth. Therefore, it is likely that the virtual mass correction will be smaller for fish of discontinuous depth. In general, effects of viscosity on virtual mass are small enough to neglect. d . Tapering Body Depth. The body depth of many fish tapers, usually only as far as the caudal peduncle prior to a large caudal fin. When the body is lenticular in section or when there is a tapering median fin [Wu's (1971c,d) ribbon fin-type] a vortex sheet is shed from the sharp tapering trailing edge. The vortex sheet will be absorbed as usual by a reentrant downstream fin, most commonly the caudal fin,

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with little effect on thrust or energy loss (Lighthill, 1970; Wu, 1971c,d; Wu and Newman, 1972). Some fish, swimming in the anguilliform mode, do not have reentrant downstream fins. If the body or fin taper to the trailing edge is gradual, as in Anguilla, it has little effect on thrust or efficiency. When the body tapers over an extended’length, thrust and efficiency are affected (Lighthill, 1970; Wu, 1971d). Thrust is generated as usual by all propulsive segments in proportion to the mass of water affected and the lateral velocity. However, when the body tapers, the mass of water affected decreases, In the anguilliform mode, increases in lateral velocity are usually small over the tapering portion of the body (Gray, 1933a) so that there is unlikely to be compensation for the decrease in virtual mass. Therefore, more posterior segments will contribute little additional thrust, but the kinetic energy given to the water will contribute to wasted energy. Consequently, propulsive efficiency will be reduced. e. Body Thickness. In the first instance, basic hydromechanical models consider slender bodies, where body thickness is small compared to length. Most fish are relatively short and thick. Newman and Wu (1973) and Newman (1973) have shown that, under these circumstances, vortex sheets shed upstream can interact with body thickness to affect both thrust and drag. Newman and Wu (1973) and Newman (1973) considered flow for an axisymmetrical body (circular body section) with side fins. They found that the importance of body thickness depended on the proportion of total depth represented by side fins and the depth of the caudal fin relative to maximum depth. Both thrust and drag, and the ratio between thrust and drag, increase to some maximum as the body comprises an increasing proportion of total depth. The maximum depends on the depth ofthe caudal fin. The caudal fin dominates generation of thrust and drag as its trailing edge becomes large relative to the maximum depth of the body. When the caudal fin trailing edge is equal to, or exceeds, maximum upstream depth, effects of finite body width become neglible (Newman, 1973). For most fish, the caudal fin is large enough that body thickness effects are small enough to neglect.

4. EFFECTSOF

SWIMMING

MOVEMENTS

a. Large Amplitude Mouements. Real fish propulsive movements are of large amplitude. Lighthill (1971) showed that energy loss to the wake was increased by large amplitude movements because momentum shed at the trailing edge is not aligned with the axis of

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motion. Wake momentum is shed across a plane normal to the trailing edge and therefore energy loss to the wake increases in proportion to the magnitude of the angle subtended b y that plane to the axis of forward progression. If the angle subtended by that plane is K , then energy loss to the wake is increased by l/cos K, and thrust is reduced proportionally from Eq. (15). Lighthill (1971) corrected for large amplitude movements of Leuciscus using data from Bainbridge (1963) by calculating instantaneous values for all kinematic parameters including K. The mean value of Ucos K was 1.18.Data for Anguilla from Gray (1933a) indicate l/cos K would be 1.20. Measurements on a single trout at several cruising swimming speeds gave lower values, independent of swimming speed, the overall mean llcos K being 1.06 (Webb, unpublished observations).

b. Swimming Mode. A major evolutionary trend in bodykaudal fin propulsion of fish is rednction in the proportion of the body involved in significant lateral propulsive movements. This was recognized by Breder ( 1926), who identified various modes within a continuously changing spectrum from anguilliform propulsion (most of the body involved in several half wavelengths in large amplitude lateral displacements) to carangiform propulsion (less than one-half of the body included in. large amplitude displacements over less than half a propulsive wavelength). The trend toward decreasing the proportion of the body executing large amplitude movements is of mechanical importance because the mass of water affected by propulsive movements increases with time to exceed m as calculated from Eq. (10)(Lighthill, 1970; Wu, 1971d). When a segment moves, there is an immediate increase in the momentum of water affected that is proportional to the segment’s velocity and virtual mass. In addition there is a time-dependent increase in momentum and kinetic energy associated with the vortex force gradually shed by upstream segments (Lighthill, 1970). Lighthill (1960, 1970) showed that the time-dependent increase in vortex force momentum was poorly correlated with trailing edge motions; that is, the trailing edge works against a component of the total momentum that is out of phase with that edge’s movements. As a result, this momentum does not contribute to thrust but does increase energy losses to the wake. Crude estimates of the vortex force led to the conclusion that trends reducing the proportion of the body involved in locomotory movements would reduce the magnitude of that momentum poorly correlated with downstream lateral movements (Lighthill, 1970). For example, in the anguilliform mode, the high

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proportion of the body executing lateral movements permits time for the development of a relatively large vortelr force poorly correlated with the movements of the trailing edge. This is reduced to become insignificant in carangiform modes when the distance over which lateral movements increase in amplitude is relatively smaller with reduction in the time-dependent vortex force. The inclusion of a large part of the body in the propulsive wave also increases the time and distance over which cross-flows occur. Such cross-flow could encourage separation of the boundary layer and increase drag. With the progressive concentration of significant propulsive movements caudally, recoil forces are generated. In the anguilliform mode, lateral forces are more or less balanced b y equal and opposite lateral forces distributed along the more complete propulsive wave. Large recoil forces generated by the tail in carangiform modes tend to cause the anterior of the body to yaw. This would lead to a large energy loss unless minimized. The problem is greatest for fish swimming in the carangiform mode with lunate tail, this mode being the logical culmination in reducing the propulsive portion of the body. Recoil yawing movements are minimized by increasing body and fin depth anteriorly. The body is also frequently thicker anteriorly, concentrating body mass forward. As a result the virtual mass plus body mass is increased, increasing the inertial resistance to yawing forces. This is best illustrated in scombroid fish where the caudal fin and body are separated by a narrow caudal peduncle. The trend toward a reduced caudal peduncle is called narrow necking (Lighthill, 1969), and is a trend toward the separation of two mass centers, i.e., the tail generating thrust and yawing forces, with the latter being minimized by anterior body mass and enhanced virtual mass. Narrow necking is thus a morphological requisite for efficient propulsion in advanced carangiform modes (Lighthill, 1969, 1970). Fish swimming in the subcarangiform mode include a complete propulsive wavelength within the body length (Breder, 1926). However, recoil forces will be incompletely equalized because major increases in amplitude are restricted to the posterior half to third of the body. Such fish, for example, trout and salmon, have moderate narrow necking and anterior median fins increase virtual mass forward. Then recoil forces are partly offset by the inertia of the anterior part of the body together with some cancellation of recoil forces within the length of the propulsive wave. Narrow necking of a less abrupt form than in scombroid fish is a feature of many fish with elongate fusiform bodies, for example, most


211

small elasmobranchs. Illustrations in Gray ( 1933a,c) show that recoil yawing forces are not effectively minimized in comparison with fish having more truncate bodies and swimming in carangiform modes. Elasmobranchs typically have a fairly large anterior median fin which probably contributes more to thrust as for Acanthias vulgaris (Section II,B,3) and less to stability.

c . Kinematic Variability. Treatment of mechanics of fish movements considers two dimensional motions of plane surfaces. In practice, detailed movements are more complex, particularly for the caudal fin of fusiform fish. Variability in caudal fin movements has been described in greatest detail by Bainbridge (1963). He was also able to give approximate explanations based on hydrodynamic forces acting on the caudal fin during a propulsive cycle. However, much of the detailed kinematics are apparently under active neuromuscular control by the fish (Breder, 1926; von Holste and Kuchemann, 1942; Harris, 1937; Bainbridge, 1963; Webb, 1971a). Complex movements of the caudal fin web are presumably related to continuous fine control of thrust and stability. I n addition, some long slender fish swimming in the anguilliform mode may include spiral, three-dimensional components in the propulsive wave (see Chapter 1).The significance of such components is not known. They have not been reported for shorter, more truncate fish swimming in mechanically more advanced propulsion modes. 5.

PROBLEMS IN

APPLYINGHYDROMECHANICAL MODELS

Recent hydromechanical models permit increasing accuracy in interpreting propulsion mechanics relating to variability in fish functional design at cruising swimming speeds (Lighthill, 1969, 1970, 1971; Wu, 1971a,b,c,d; Wu and Newman, 1972; Newman and Wu, 1973; Newman, 1973). However, it is recognized that no current model is complete. I n some cases, solutions to hydromechanical aspects of morphological variation are approximate. For example, quantifying the effects of vortex force poorly correlated with lateral movements (Lighthill, 1970) or body thickness effects (Newman, 1973). Nevertheless, such studies indicate the order of magnitude of such interactions is usually small (Lighthill, 1970; Wu, 1971d; Newman, 1973). All hydromechanical models neglect viscosity effects. This again probably involves small error in determining thrust for most fish with compressed bodies swimming at high Reynolds numbers (Lighthill, 1969, 1970). Viscosity becomes important for small fish when

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PAUL W. WEBB

Reynolds number is low and when the body is not compressed. Lighthill ( 1969) clearly states the need for a composite reaction-resistance model but formulation of such a model is complex and problematic (Vlymen, 1974). Application of such models to practical biological problems is likely to be difficult. Taylor (1952) pointed out that complex models might lead to improvement in quality but when input data required become too great, simple collection of those data mitigates against applying the model in biologically comprehensive situations. Webb (1975a) suggested that a useful compromise would be the determination of modifying coefficients related to key morphological and kinematic parameters that could be applied within the framework of simpler models. Such an approach combines the advantages of detailed theoretical studies with limitations of practical observation and has recently been successfully applied to animal flight (Weis-Fogh, 1973). Comparative data for a sufficient number of fish species to test this approach are currently lacking. The difficult problem of including viscosity applies in theory mainly to smaller fish and less compressed fish swimming in anguilliform modes (Lighthill, 1970; Wu, 1971d). However, such effects probably change mechanical efficiency of larger fish swimming at lower cruising speeds in carangiform modes. The hydromechanical models discussed here predict very high efficiencies for the propulsive system (Wu, 1971c,d). For Lighthill’s bulk momentum model the mechanical efficiency of the propeller system would not be less than 0.5. This follows from Eqs. (12)-( 15)when caudal propeller efficiency, r),, is given by qP = 1 - 0.5

( v - u 7)

so that when U 4V, T , --* 1 and when U + V, qP + 0.5. In contrast, Webb (1971b) deduced that r), for rainbow trout (e = 29.2 cm) at low cruising speeds would be less than 0.5. For example, at a speed of 20 cm/sec r), would be 0.12 while the value from Eq. (22) is 0.67. The difference may be related to interactions between the upstream viscous vortex force growing with time but poorly correlated with trailing edge motions. The magnitude of this force, contributing to energy loss but not thrust, will be greater when V is large relative to U , compared to the case when V approaches U as is predicted for good propeller efficiency. Thus the relation U/V is often taken as representative of r), (Gadd, 1952; Taylor, 1952; Lighthill, 1960; Hertel, 1966; Wu, 1971d). When U / V is small, r), will be lowest from Eq. (22) and


213

further reduced through poor correlation of part of the vortex force with trailing edge motions. U / V increases with swimming speed so that prediction of qp is reasonably accurate for high steady speeds (Webb, 1971b, 1975a). Possible error in calculating vp does not apparently alter predictions of thrust. vp is reduced through increased energy loss to the wake (increased P K )and the total rate of working (P) will be increased by the same amount. Then thrust from Eq. (15)is not changed. In general, therefore, the bulk momentum model is expected to give good first approximations of thrust (=drag). These values can be improved b y correcting for large amplitude motions. Effects of upstream vorticity not absorbed by reentrant downstream fins and interactions with body thickness can be taken into account by detailed analysis, but corrections appear to be small. The same applies to viscosity corrections for virtual mass. Mechani.ca1 efficiency can also be calculated for higher swimming speeds but correction is required at low speeds. This requires more detailed experiments but can be determined. Problems of viscosity for small fish are recognized but cannot as yet be satisfactorily incorporated in a first principles model. For larger fish, neglect of viscosity is not likely to be important. 6. VALUESFOR THRUSTAND POWER Good estimates of thrust and thrust power can be calculated from propulsion parametersf, A, A, and K at a given U . Few studies have measured all these parameters and few consider a range of speeds. Most complete data can be compiled for Carassius, Oncorhynchus nerka, and Salmo gairdneri at cruising speeds (Bainbridge, 1958, 1963; Smit et al., 1971; Webb, 1971a, 1973a, 1975a). Thrust power for these fish is shown as a function of swimming speed in Fig. 4. The slopes of the relationship between thrust power and speed for salmonids are approximately 2.8 and for goldfish the slope is approximately 2.5. These are values that would be expected for theoretical drag of a rigid body with turbulent and laminar boundary layer flow, respectively. However, it cannot be concluded from these data that boundary layer flow is turbulent or laminar in each case. Thrust power exceeds theoretical drag and the slope of the powedspeed relationship may reflect changes in pressure drag with speed. Figure 4 also includes a comparison between three methods of determining thrust power; Lighthill’s bulk momentum model, a detailed quasi-static analysis following Lighthill ( 1971; Webb, 1975a) and measurements from added drag loads (Webb, 1971a). Agreement

214

PAUL W. WEBB

SWIMMING SPEED

-

cmlrec

Fig. 4. Relationships between thrust power and swimming speed for three species of fish. Curussius uurutus, solid line, thrust power calculated from Lighthill’s bulk momentum model using equations for kinematic parameters in Bainbridge (1963) and Smit et 01. (1971). Oncorhynchus nerku, closed squares calculated from Lighthill’s bulk momentum model modified for large amplitude using data for each speed shown. Data from Webb (19734. Sulmo guirdneri, open squares show thrust power calculated in the same way as 0. nerku. Open triangles show calculations from a detailed quasi-static analysis and open circles show values obtained from experiments with added drag loads. (Data from Webb, 1971a, 1975a.) Stippled areas show power required exceeding that from red muscle, and solid triangles show the percentage of myotomal white muscle required to make up the red muscle deficit. Further explanation is given in the text.

among the three methods is good and provides support for use of hydromechanical models. Thrust or thrust power can also be expressed as nondimensional drag coefficients calculated from Eq. (2) and expressed as a function of the nondimensional Reynolds number (Fig. 5). Such drag coefficients are variable among species but are most commonly three to five times theoretical drag values for turbulent boundary layer flow. Metabolic studies lead to similar conclusions (Kliashtorin, 1973).Most of the data in Fig. 5 are for fish swimming in subcarangiform modes. Preliminary calculations for propulsion in advanced carangiform modes suggest drag exceeds theoretical drag by a factor similar to that for subcarangiform propulsion (see also Chapter 4).

3.

215


I

I

to4

I

105 lo6 REYNOLDS NUMBER

10’

Fig. 5. Drag coefficients, based on thrust power, as a function of Reynolds number. Drag coefficients a;e calculated from thrust power values calculated from hydromechanical models using standard hydrodynamic equations [see Eq. (2)].The stippled area shows the range of observed dead drag coefficients, calculated in the same way from measurements on fish and models. Theoretical drag coefficients are shown for laminar (C, lam) and turbulent boundary layer flow (C, ,ulb). (Data and references are summarized in Webb, 1975a.)

7. ENERGETICS AND

VALIDATION O F

HYDROMECHANICAL MODELS

The various models for fish propulsion mechanics are based on hydromechanical theory and although predictions of thrust and thrust power appear reasonable they require validation. Ideally, validation would be based on observations of flow about swimming fish, but such observations remain problematic (Houssay, 1912; Gray, 1936; Allan, 1961; Kent et al., 1961; Rosen, 1959; Aleyev and Ovcharov, 1969, 1971). Comparison between models and measurements of thrust are tedious (Webb, 1971a). Estimates of muscle or metabolic power have most commonly been used for indirect evaluation of predictions of thrust and power (Gray, 1936; Hill, 1950; Bainbridge, 1961; Osborne, 1961; Brett, 1963; Smit, 1965; Walters, 1966; Smit et al., 1971; Webb, 1971a,b, 1973a, 1975a,b).

216

PAUL W. WEBB

Estimates of muscle power deduced from comparative studies by Bainbridge (1961) are most commonly used. Measurements of thrust power by Houssay (1912) indicate that Bainbridge's values are of the correct order of magnitude but are probably conservative (Webb, 1975a). A comparison between predictions of thrust power and maximum white muscle power is given in Fig. 6 for various fish. Half the myotomal muscle is assumed active at any instant. A caudal propeller efficiency of 0.75 was assumed, avalue that is probably conservative (Wu, 1971d). Thrust power values are within the range of expected power outputs for vertebrate white muscle systems. Red muscle is used at sustained cruising speeds and prolonged speeds. It is frequently found that insufficient red muscle power would be developed to meet requirements at higher prolonged speeds (Fig. 4). Red muscle power during swimming can be estimated assuming half the muscle works at any instant and that caudal propeller efficiency is 75%. For the species shown in Fig. 4, red muscle comprises 7.4% of the myotome for Carassius (Johnson and Goldspink,

WEIGHT

- gm

Fig. 6. A comparison between thrust power given by hydromechanical models and estimated propulsive muscle power output. Further explanation is given in the text. (Modified after Webb, 1975,Bull. Fish. Res. Bourd Can. No. 190, 159 pp.)

3.


217

1973a) and 4% of the myotome for the salmonids (Webb, 1975~). Myotomal muscle mass is assumed to be 50% of body mass. This figure is conservative (Bainbridge, 1963; Brett, 1963). However, support of the red muscle at prolonged speeds by small amounts of white or pink muscle would generate sufficient power. Direct and indirect observations support such joint muscle function at prolonged speeds (e.g., Brett, 1964; Beamish, 1968; Pritchard et al., 1971; Smit et al., 1971; Webb, 1971b; Hudson, 1973; Johnson and Goldspink, 1973a,b,c). Oxygen consumption data are available for fish swimming at cruising and prolonged speeds. Metabolic power can be calculated from oxycalorific equivalents. These data usually indicate sufficient metabolic power to generate thrust at normal overall efficiencies for the muscles and caudal propeller (Kilashtorin, 1973; Webb, 1975a). A major exception is known for goldfish (Smit et al., 1971) at prolonged speeds. However, energy accounting is not complete at such speeds because anaerobic energy of uncertain magnitude contributes to total metabolic power. Adequate data are not available to calculate metabolic power at burst speeds (Beamish, 1968; Johnson and Goldspink, 1973a; Webb, 1975a). In general, the current understanding of muscle and metabolic systems lends support to thrust predictions from models. However, because muscle powers are estimates, and metabolic data are frequently absent or incomplete, decisive validation of models from energetic data is not currently possible. Nevertheless, since comparative studies can suggest likely performance levels for components of the propulsive system, muscle and metabolism data can be used as a rough check on models. The same estimates can be used to suggest areas requiring modification, an approach that has been applied to bird flight (Tucker, 1973). The corrections required for qp at low swimming speeds of rainbow trout (Section II,B,5) are based on such estimates (Webb, 1971a,b). 8. EFFICIENCY

The overall efficiency of converting metabolic power to thrust power increases with swimming speed (Brett, 1963; Smit, 1965; Smit et al., 1971; Webb, 1971a, 1975a). Maximum efficiencies calculated for prolonged speeds are of the order of 20%,as for other animals (Webb, 1971b, 1973a, 1975a). Efficiencies at higher burst speeds are not known. Several different theoretical and empirical studies suggest mean routine speeds of one body length per second are common for

218

PAUL W. WEBB

nonscombroid fish (Brett, 1965; Weihs, 1973c; Kerr, 1971). If these were steady swimming speeds, overall efficiencies would be low, that is, less than 10%. Efficiencies for unsteady routine swimming are not known, but probably exceed those for steady speeds in covering a given distance in a given time (Weihs, 1974).

C. Drag Reducing Mechanisms Numerous mechanisms have been proposed that might reduce the drag of swimming fish (Webb, 1975a). Most plausible mechanisms are found for fish with high speed cruising swimming behavior, particularly scombroid fish. The following summary discusses only likely drag reducing mechanisms. Theories of drag reduction involve reduction of frictional resistance, reduction of pressure drag, and reduction in wake energy losses. Minimal frictional drag in normal fluids occurs with laminar boundary layer flow and maximum frictional drag with turbulent boundary layer flow. Minimum pressure drag occurs when the boundary layer remains attached to the body but is increased whenever the boundary layer separates prematurely. Pressure drag can greatly exceed frictional drag so that it is often more important to reduce the former. A laminar boundary layer is less resistant to separation than a turbulent boundary layer. Consequently, it is often advantageous to induce more stable turbulent boundary layer flow. Frictional drag is then increased but the potential reduction in pressure drag is very much greater with a net reduction in total drag.

1.

MECHANISMS TO

MAINTAIN LAMINARBOUNDARY LAYERFLOW

a. Distributed Dynamic Dumping. Walters (1963)has described a subdermal canal system in the integument of the trachypterid Desmodema, an elongate fish. Critical Reynolds numbers would be exceeded at even low swimming speeds. The fish swims in the amiiform mode holding the body straight and Walters postulated that the subdermal canal system could delay transitions by distributing local high pressure disturbances over the whole body via the canal system. This system is mechanically feasible but possible reductions in total drag are probably small. Drag associated with propulsive movements of the long dorsal fin is likely to greatly exceed that for the body. Pore canal systems have also been described in the Istiophoridae


219

(Walters, 1962) but it is doubtful if such a system could neutralize disturbances of the intensity expected at the swimming speeds of these fish. Ovchinnikov (1966) suggests these fish are covered by a completely turbulent boundary layer (Section II,C,2,a).

b. Body Shape. Well-designed body shapes can maintain a high proportion of laminar boundary layer flow by extending the distance up to the shoulder, experiencing a favorable pressure gradient (Walters, 1962; Hertel, 1966). In most nonscombroid fish the shoulder is fairly far forward (Houssay, 1912) so most of the body would in practice experience an unfavorable pressure gradient. Transition may be encouraged by propulsive movements (Section II,A,4). LaMinar boundary layer flow would be expected to cover a small area of such fish, but the major drag problem would be pressure drag. c . Properties of the Propulsive Wave. The propulsive wave propels water backward and the increase in water velocity will result in reduced pressure caudally. Such pressure reduction could partly offset the adverse pressure gradient otherwise found downstream of the shoulder (Gray, 1936; Lang, 1966). Webb (1975a) has pointed out that this effect must be small if propulsive efficiency is to be high, since the greater the increase in water velocity the greater the kinetic energy lost to the wake (Alexander, 1968). Measurements of pressure distribution along the sides of a swimming fish have shown that local pressure changes are small (DuBois et al., 1974). Pressures measured for the dorsal surface decrease in the required fashion to facilitate flow over the posterior portion of the body. However, since lateral pressures do not increase in the same way, the dorsal pressure changes probably result from cross-flow. Richardson (1936), Hertel (1966), and Wu (1971d) have suggested the harmonic nature of propulsive movements could stabilize laminar boundary layer flow. Such stabilization occurs with small amplitude harmonic oscillations (Schlichting, 1968), but the situation is not known for large amplitude fishlike movements when propulsive segments move at a small angle of attack to the incident flow. d. Ejection of Kinetic Energy into the Boundary Layer. Breder (1926), Walters (1962), and Gray (1968) have suggested that the gill effluent might inject kinetic energy into the boundary layer to maintain laminar flow, Observations on small fish have suggested gill effluents lead to transition and separation (Allan, 1961; Walters, 1962). Further observations under better controlled conditions are required (Aleyev and Ovcharov, 1971).

220

PAUL W. WEBB

2. MECHANISMS FOR THE DELAYAND PREVENTION OF SEPARATION a. Surface Roughness. Some fish have rough body surfaces. It is presumed that one of the functions of such a surface is to induce turbulent boundary layer flow, delaying separation. Fish in the family Istiophoridae have a rostrum with denticles to induce turbulent boundary layer flow. In Xiphids, the rostrum is sufficiently long that transition is expected without roughness (Ovchinnikov, 1966). Bone and Howarth (1966) have suggested the major drag problem for most elasmobranchs would be boundary layer separation and this would be minimized by turbulent boundary layer flow induced by denticles.

b. Vortex Generators. The integument of the castor-oil fish, Ruuettus pretiosus, includes special ctenoid scales, the tips of which project well beyond the body surface (Bone, 1972). Bone suggested that the scales could act as vortex generators, vorticity being shed by each scale caudally and towards the body. In this way energy derived from the free stream could assist boundary layer flow. These fish also possess a subdermal canal system that may inject fluid into the boundary layer when the fish swims. This fluid might increase turbidity of boundary layer flow or add further kinetic energy. 3. REDUCTION OF VISCOSITY It has been conclusively demonstrated that fresh fish mucus can reduce frictional drag. The literature is reviewed by Hoyt (1975) which may be referred to for further references. There is substantial variability in the effectiveness of mucus in reducing frictional resistance. This may occur because the concentration of active polymers has not been controlled, the experiments being performed on fresh homogenized mucus of unknown composition. There is an approximate relationship between swimming performance and the effectiveness of mucus in reducing frictional resistance (Rosen and Cornford,

1971). It is not certain that mucus functions to reduce drag under natural condition. Relatively large amounts of mucus are required to give major reductions in frictional resistance. For example, a 5% solution of mucus is close to maximally effective for many species. This concentration results in a 65% reduction in frictional drag of the Pacific barracuda (Rosen and Cornford, 1971). In addition, like other linear long-chain polymers, mucus only reduces friction in turbulent flow (Hoyt, 1975). Many fast swimming fish with effective friction-reducing


22 1

mucus swim in advanced carangiform modes and have streamlined body shapes that are assumed to maximize laminar boundary layer flow. If this hypothesis is correct, then mucus would be of little importance for these fish. Providing mucus concentrations were large enough in the boundary layer of swimming fish, frictional reduction would be most important for fish swimming in anguilliform and lower carangiform modes when turbulent boundary layer flow is expected. 4. BEHAVIOR

Schooling fish have frequently been reported swimming in regular diamond formations (e.g., Keenleyside, 1955; Nursall, 1973). Some forin of drag reduction through interaction among members of the school has been postulated (Breder, 1926; Belyayev and Zuyev, 1969; Zuyev and Belyayev, 1970; Weihs, 1973b). Weihs (1973b) has shown that interactions can occur between the wake generated by oddnumbered rows in a school and fish in downstream even-numbered rows when fish swim in a regular diamond formation. Interaction reduces thrust required by second row fish while third row fish experience a mechanically uniform incident flow. Weihs calculated that net thrust could be reduced approximately 10% in the horizontal plane. Further reductions of up to 30% were feasible for interactions in the vertical plane in three dimensional schools. It should be noted that the evolution of schooling among fish is difficult to explain on the basis of locomotory energetic savings alone. Instead, if fish school, for whatever reason, then locomotory energetic advantages may accrue to some members of school.

111. UNSTEADY PROPULSION

Unsteady propulsion is an integral part of normal locomotor activity. Houssay (1912) described normal routine activity of fish as bursts interspersed with glides, that is, continuous unsteady propulsion. High speed acceleration and maneuver, such as in predatodprey behavior, negotiating fish ladders and water falls, and avoidance of nets also involves unsteady activity. This area of fish propulsion has largely been neglected. Some metabolic measurements have been made for routine unsteady activity (Fry, 1957, 1971); mechanics and performance have been described for high levels of unsteady activity (Gray, 1933d; Hertel, 1966; Weihs, 1972, 1973a; Webb, 1975a,c, 1976, 1977).

222

PAUL W. WEBB

A. Kinematics Acceleration behavior is variable. Acceleration at high rates is found in behavior ranging from simple fast starts (Hertel, 1966; Weihs, 1973a) to turning maneuvers (Gray, 1933d; Weihs, 1972), most movements being intermediate between the extremes (Webb, 1975c; Eaton et al., 1977).The same variation is presumed to occur at lower routine unsteady activity levels. Although behavior patterns are variable, mechanics are fairly stereotyped. Two major kinematic patterns can be distinguished, described as C- and S-starts. In the former case, the body is bent into a C- or L-shape during the fast start. In S-starts the body bends into a double flexure, with an S-shape (Webb, 1976). In both cases, mechanics can be divided into three stages as illustrated for a C-start in Fig. 7. First, the body anterior and posterior to the center of mass (about which propulsive forces act) moves laterally and the fish begins to accelerate, as measured by the motion of the center of mass (frames 1 to 3). This kinematic stage 1 is followed by a kinematic stage 2 (frames 3 to 8) when thrust is dominated by the tail moving in the opposite direction to stage 1, at a small angle of attack to the water. Acceleration behavior is completed by a variable kinematic stage 3. During this stage, fish adopt various behavior patterns, ranging from an unpowered glide through steady swimming to continued acceleration (Hertel, 1966; Weihs, 1972, 1973a; Webb, 1975~). C-starts and S-starts differ in an important respect. During a C-start, the bending of both the anterior and posterior parts of the body in opposite directions during kinematic stage 1 results in a turn being included as part of the acceleration. The angle of the turn is proportional to acceleration rate (Hertel, 1966; Weihs, 1973a). The turn results from unbalanced recoil forces generated by the tail. In contrast, the double body flexure in an S-start results in more balanced recoil forces such that a turn is not an unavoidable concomitant of acceleration. Turns of various magnitudes are part of normal fast starts in both patterns and are under behavioral control b y the fish. The duration of kinematic stages 1 and 2 is short (Table I). The duration of kinematic stage 3 will, of course, depend upon the behavior of the fish and will be of variable duration. In considering the mechanics of acceleration, net forces and hence net body movements are determined for the center of mass. Figure 8 shows time relations for distance covered, velocity, and acceleration rate for the center of mass of the trout in the sequence illustrated in Fig. 7. For this sequence, distance covered and velocity do not in-

3.


223

Fig. 7. Tracings of the midline of a 33 cm trout accelerating from rest. Closed circles Biorlzeology 10,343-350. Copyright 1973 show the center of mass. (From Weihs, 1973~1, by Pergamon Press.)

crease linearly with time. The former increases exponentially while velocity first increases rapidly, but the rate of increase in velocity decreases with time. Acceleration rate is therefore not uniform for this sequence but decreases with time, presumably after an initial increase to a high level. The pattern of time relations for distance covered and velocity are similar among fish, but acceleration rate relations with time are variable. Acceleration rate often increases through kinematic stages 1 and 2. Distances covered during kinematic stages 1 and 2 are usually small (Table I) particularly at higher acceleration rates observed for fish (Section 111,B).Larger distances may be covered during kinematic

Table I Acceleration Performance of Fish During Fast Starts Using Various Methods

Species Salmo irideus Esox lucius Cyprinus carpio Scardinus erythrophthalamus Leuciscus leuciscus Salmo gairdneri Perca flauescens Thunnus albacares Acanthocybium solandri Salmo trutta Salmo gairdneri

Etheostoma caeruleum Cottus cognatus Esox sp Notropis cornutus Perca jlauescens Lepomis mcrochirus Lepomis cyanellus

Length (cm) 20.0 16.5-20.0 13.5

Mass (9)

-

-

-

22.0 18.5 29.0

-

-

108.9

98.0

-

113.1

-

33.0 9.6 20.4 29.6 38.7 14.3 18.4 19.5 6.2 8.2 21.7 10.7 15.5 15.3 8.0

7.2 79.0 270.8 561.9 27.3 48.41 69.90 2.25 6.94 41.80 11.18 33.48 64.50 8.18

Maximum acceleration rate (m/secP) 40 40 40 40 40 17 52 43 37 36 34 25 33 32 36 41 42 20 33 32 23 40 29

24 29 16

Mean acceleration rate (mlsecZ)

Initial velocity (cdsec)

Final velocity (cmisec)

Distance traveled (cm)

Duration (sec)

-

-

-

-

-

-

-

5 5 5

0.05 0.05 0.05

A A A

Gray ( 1953a) Gray ( 1953a) Gray (1953a)

-

-

-

-

-

5 5

0 -

260

-

346 204 1903 1305

1166 764 2082 1682

0.05 0.05 0.15 0.016 0.19 0.15 0.05 0.11

A

-

Gray ( 1953a) Gray ( 1953a) Hertel ( 1966) Gero (1952) Fierstine and Walters (1968)

-

16.0 15.1 15.7 17.6 12.9 8.0 10.6 10.3 6.1 10.4

11.0 9.3 12.3 8.4

-

0 0 0

0 0 0 0 0 0 0 0 0 0 0

-

-

-

-

153 167 181 285 121 133 158 89 77 156 114 115 131 67

3.5 7.3 9.5 16.3 5.4 8.4 8.7 2.4 3.4 8.5 3.8 5.2 5.9 2.9

-

0.071 0.078

Methodo

A

B C BC

Source

BC C C

Weihs ( 19734 Webb ( 1976)

C C C

Webb (19754 Webb ( 1977) Webb (unpublished) Webb (unpublished) Webb (unpublished) Webb (unpublished) Webb (unpublished) Webb (unpublished) Webb (unpublished) Webb (197%)

0.096 0.100 0.078 0.115 0.114 0.057 0.081 0.115 0.078 0.103 9.088 0.079

c

C C C

C C C

'(A) f = 2 . M . (B) f = ( U , - U , ) / t . (C) Acceleration rate calculated from moving point regressions from distance data obtained with high speed photography or similar. (BC)Velocity calculated as acceleration rate in (C), and acceleration calculated from the velocity data as in (B).f, acceleration rate; s, distance covered; t, time; Ut, initial velocity; U I , final velocity.

3.

225


$

6

0.04

' 0

, , , , , , ,

0.08

,

042

2200

.:

016

1

1

I

I

I

I

I

'

0.b4

'

Oh8

'

&!2

'

80

60 -I

9 40 20

' 0

V

;

Y 0.04

0.08

042

6oo0

0.16

TIME

800-

-

046

sac

Fig. 8. Time relations for (A) distance covered, (B) velocity, and (C) acceleration rate calculated for the acceleration sequence shown in Fig. 7.

stages 1and 2 at low acceleration rates, such as that illustrated in Fig. 8, but velocities attained will be relatively lower. Kinematic stage 3 appears important in covering large distances at the high speeds attained at the end of kinematic stage 2. Kinematic stage 3 is also important for orientation control. In C-starts, the center of mass yaws in proportion to the acceleration rate so that the path of the fish after acceleration differs from the original body axis (Hertel, 1966; Weihs, 1973a). Correction must be made by fish accelerating toward a specific objective such as shelter or prey, and this correction occurs during kinematic stage 3. The problem is less important in' S-starts because recoil forces are better balanced. Acceleration activity can be considered to be behaviorally composed of two phases. A phase 1coincides with kinematic stages 1and 2 during which high velocities are acquired. Phase 2 coincides with kinematic stage 3 during which large distances are covered and reorientations are made (Webb, 1975~).

226

PAUL W. WEBB

B. Acceleration Performance Fish may attain very high but transitory speeds by the end of kinematic stage 2. Walters and Fierstine (1964)report speeds in excess of 20 Clsec for wahoo (lengths from 92 to 113 cm) and yellowfin tuna obtained maximum veloci(lengths from 56 to 98 cm). Webb (1975~) ties of the same magnitude for rainbow trout (8 = 14.3 cm) and green sunfish (C = 8.0 cm). However velocities attained by the end of stage 2 ranged from 20 Clsec to less than 2 Clsec for the same species, with mean values of 8.5 Clsec for the trout and 8.3 tlsec for the sunfish. Consequently, the very high speeds recorded are probably not representative of normal activity. This is also suggested by data for wahoo and skipjack when speeds ranged from 6 to 21 elsec, the mean being 12 Clsec (Fierstine and Walters, 1968). Maximum acceleration rates of fish vary from about 16 to 50 mIsec2 (Table I). Where sufficient observations have been made (Gero, 1952; Weihs, 1973a, Webb, 1975c, 1976, 1977) it has been found that acceleration rates are time dependent, so that the maximum values do not adequately describe overall performance. Mean values of acceleration rates for a fast start are much lower, ranging from 6 to 16 mlsec?.

C. Mechanics The mechanics of uniform acceleration for fishlike motions of small amp1itu.de have been described by Wu (19714. More appropriate, large amplitude movements have been described by Weihs (1972, 1973a) starting from Lighthill's (1971) treatment of large amplitude movements in steady swimming. A single theory is appropriate for acceleration activity ranging from fast starts to turning maneuvers (Weihs, 1972, 1973a).Weihs (1972, 1973a) has shown that large area is required for good acceleration performance. Large area is particularly important caudally, usually the caudal fin, where lateral movements are greatest. The importance of these morphological requirements for thrust have been demonstrated experimentally (Webb, 1977).

D. Work Done in Acceleration Work is done during acceleration against frictional drag and body inertia. Webb (19754 describes a simple method for obtaining first estimates of work done against frictional drag and hence for calculating total drag. The proportions of the two components making up total work done varies with acceleration rate and speed attained (Fig. 9). Inertial work is calculated as the increase in kinetic energy which will


ACCELERATION RATE

-

227

cm/sec2

Fig. 9. Relationships for work done in accelerating from rest to a speed of 300 cm/sec (solid lines) and 600 cmlsec (dashed lines) at various acceleration rates for a hypothetical salmonid fish (C = 30 cm). Work done against frictional drag (EF), inertia ( E J ,and total work done (E) were calculated as described by Webb (1975a).

be constant for any acceleration rate when fish start from rest and accelerate to a given final speed. However, the work done against frictional drag in accelerating to a given final speed decreases with acceleration rate. Work done increases as final speed increases. Thus at high acceleration rates work done is mainly against body inertia. The relationships between the two drag components indicate that it is energetically advantageous to accelerate at high acceleration rates, as commonly observed.

E. Drag Reduction 1. BODY SHAPE Specialized predators, for example, Esox, with unsteady lunging behavior typically have elongated cylindrical bodies. This body shape

228

PAUL W. WEBB

minimizes body surface area and added mass while maximizing body volume for maximum muscle mass. The body shape consequently minimizes frictional and added mass drag during acceleration.

2. BEHAVIOR Houssay (1912) described the normal pattern of fish locomotion as bursts of activity followed by passive glides. Weihs (1973d, 1974) has shown that this bursvglide behavior can reduce the energy required to cover a given distance in a given time. In comparison with swimming at uniform velocity, bursdglide behavior can reduce thrust required up to 50%.

IV. UNSTEADY VERSUS STEADY PROPULSION A. Mechanics and Structure The structural requirements for high thrust in steady swimming differ from those for unsteady swimming. The former requires large trailing edge depth, concentrated primarily at a reentrant caudal fin. In contrast, high unsteady activity requires a large area concentrated caudally where lateral movements are largest. However, a large caudal area is associated with greatly increased drag in steady swimming (Webb, 1973a) resulting from boundary layer effects of propulsive movements (Lighthill, 1971). In the absence of morphological specialization, thrust increases with the trailing edge virtual mass, but drag increases with area in similar proportion to increased thrust. As a result, there is little change in steady cruising performance with an increase in tail depth and area. Thus, morphological requirements for high steady swimming must be qualified as large trailing edge depth without equivalent increase in area and related drag. These requirements are then apparently not consistent with high unsteady performance, such that morphological requirements for high unsteady activity and for high steady activity are mutually exclusive. As a result, body shapes that maximize acceleration do so at the cost of steady performance (Fig. 10). This does not present a problem for fish specialized for either high unsteady or high steady propulsion strategies. Fish specialized for lunging habits, for example Cottids or Esocids, tend to maximize area along the whole length of the body, or to maximize caudal area. However, their routine locomotory habits are commonly “hovering” in the

3.

229


r

h

m

A

B

C

D

E

F

Fig. 10. Relative performance of various lateral body profiles typical of fish in steady swimming and fast start acceleration; Performance is normalized with respect to that of a reference case, rainbow trout. (Data from Webb, 1977.)

water using alternate median fin propulsion (e.g., Esocids) or habits may be sedentary (Cottids). Fish specialized for cruising show well scooped out (swept back) caudal fin shapes leading to the specialized lunate tail of carangids and scombroids. Such caudal fin structure achieves a large'trailing edge depth with small tail area. The problem of unsteady versus steady performance is greatest for locomotor generalists when a balance of both activities is required. Because of the difference in morphological characteristics for the two types of performance, such generalists must be capable of modifying their lateral body profiles. This, in turn, is only possible with collapsible median fins which have evolved in bony fish. Such fish characteristically expand their median fins before accelerating (Eaton et al., 1977; Webb, 1977). Fish which are unable to significantly modify fin depth and area (notably Elasmobranchs) are not locomotor specialists.

B. Performance During and following acceleration, speeds are attained that are very much higher than normally attributed to fish. On theoretical energetics grounds (Webb, 1975a) a 10 cm salmonid might obtain a maximum (transitory) speed of 400 cm/sec (40t'/sec). Maximum speeds are expected to increase with size while specific speeds decrease as for steady swimming, so that a 50 cm salmonid might obtain a

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maximum unsteady speed of 550 cm/sec (11 t/sec). Maximum unsteady specific speeds of 20 e/sec have been reported for fish (Section III,B), but mean values are usually lower (Table I). Maximum unsteady speeds can thus exceed maximum steady speeds. The reason for this difference is that energy required is relatively small for a fish to accelerate rapidly (in usually 50.1 sec) to high speeds but covering a relatively small distance. I n comparison the energy required is high to sustain high speeds, for 21 sec, when a large distance is covered. For example, assuming swimming drag is four times theoretical drag, energy expended by a 30 cm salmonid swimming at 300 cm/sec for 1 sec is expected to be of the order of lo* ergs. According to theory (Webb, 1975a) the energy expended in accelerating at 5000 cm/sec2to the same speed is of the order of 1.8x los ergs. The difference is extremely large and is too large to be accounted for by error in assumptions made by Webb’s model for work done by accelerating fish. Consequently, it is important to distinguish between steady and unsteady performance in calculating energy expenditure. If this distinction is not made, excessive energy requirements may be calculated for the very high speeds observed for fish and cetaceans resulting in typical paradox situations analogous to Gray’s Paradox.

V. MECHANICS OF MEDIAN AND PAIRED FIN PROPULSION Breder (1926) describes a large number of morphological types of paired and noncaudal median fin propulsion systems. For mechanical purposes Breder’s classification can be simplified in the same way as body/caudal fin modes by differentiating between use of propulsive waves with short or long wavelengths. Fins with short waves relative to the fin base are found in the balistiform mode (long paired dorsal and ventral fins), the rajiform mode (long paired pectoral fins), the amiiform mode (long dorsal fins), and the gymnotiform (long ventral fins). The diodontiform mode includes fish using relatively short pectoral fins but which swim by means of short wavelength movements passed along that fin. Long wavelengths are found in the labriform mode with relatively short-based pectoral fins. The tetraodontiform mode uses short paired dorsal and ventral fins, probably using long wavelength propulsive movements. The mechanics of most non-body/caudal fin modes have only been discussed qualitatively ( Breder, 1926; Harris, 1937, 1953; Breder and Edgerton, 1943; Gray, 1968; Stickney et al., 1973; Webb, 1973a, 1975b), with the exception of models for skatelike movements in the

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rajiform mode (Kelly, 1961; Wu, 1961, 1971a; Siekmann, 1962, 1963). It is important to recognize that median and paired fins are often used primarily for maneuver rather than steady swimming. As a result movements are variable, and repeatability in experimental situations is problematic (Harris, 1937) except under unusual circumstances (Webb, 197313, 1975b).The paucity of data for these swimming modes is probably attributable to these problems of replicating experimental observations. The mechanics of median and paired fin modes can be discussed in terms of movements of propulsive segments as for bodyhaudal fin modes. Harris (1937)and Gray (1968)considered propulsive segments to generate thrust from a combination of resistive and reactive forces throughout a propulsive cycle in similar fashion to a fan. Alternatively, long fin modes may be compared to anguilliform body/caudal fin propulsion. However, long fin propulsion is undoubtedly less efficient than anguilliform propulsion because there is no increase in amplitude along the fin (Breder and Edgerton, 1943; Lissman, 1961).As a result successive propulsive waves will probably interfere because there would be no sequential increase in water momentum. Then more posterior segments may contribute relatively little to thrust but may increase energy losses. Skates and rays apparently include just over one wavelength within the length of the pectoral fins (Breder, 1926). The shape of the fin also tends to be triangular and the amplitude of the propulsive wave apparently increases to reach a maximum coinciding with the apex of the fin. Amplitude then decreases across the tapering posterior system. This system may be functionally different from most other long fins for amplitude functionally increases to the maximum width of the fin at the apex. Subsequently, amplitude decreases posteriorly but over a tapering trailing portion of the fin. Forces will be generated not only parallel to, but also normal to the fin base because lateral movements of the fin are restricted proximally by articulation with the body. Such normal forces relative to the fin base will not contribute to thrust when the fin base is parallel to the body axis but will increase energy losses. In some fish, for example, Balistes, the paired median fins are oriented backward and forces parallel and normal to the fin base will contribute to thrust. Forces normal to the fin base will generate yawing couples for pectoral fins and pitching couples for median fins. I n the majority of fin propulsion modes the occurrence of fins in pairs will cancel out these forces for symmetrical fin movements. Asymmetric movements will be important in powered maneuver. The situation is uncertain where fins are not paired, for example, Gymnarchus orAmia. These fish have not

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been reported to rise or sink in the water when swimming or gliding to rest, so buoyancy compensation for normal propulsive forces seems unlikely. Such fish do include relatively large numbers of propulsive wavelengths within the fin lengths (Breder, 1926; Breder and Edgerton, 1943; Lissman, 1961). It is possible that some movements, for example, a downward swing at the end of a cycle, might generate forces opposite to those during the remainder of the cycle. Then a large number of wavelengths would result in a net zero force component normal to the fin base. No data are available to confirm this hypothesis. Short fin propulsion mechanics are probably more similar to those of lifting surfaces comparable to the scombroid caudal fin or wings (Lighthill, 1969; Webb, 1975~).All such fins are paired and yawing and pitching forces would cancel out. Continuous steady propulsion is possible with short median fins, for example Mola, but usually the beating of short fins results in discontinuous movements. Fish recoil vertically during abduction and adduction movements and slip backward between these active stages (Webb, 1973b). These movements are associated with increased energy losses. The thrust developed and mechanical efficiency for fin modes are not well known. The maximum mechanical efficiency in generating thrust is of the order of 0.60-0.65 for Cymatogaster aggregata swimming by means of short pectoral fins (Webb, 197%). This efficiency is somewhat lower than expected for body and caudal fin propulsion at steady swimming speeds (Wu, 1971d; Webb, 1975a).The efficiency of long-based fin propulsion modes with short propulsive wavelengths is expected to be very much lower because of increased energy losses from non-thrust-enhancing segment interactions and as a result of forces normal to the fin base.

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metabolic rate of underyearling sockeye salmon. (Oncorhynchus nerka) at steady swimming speeds. J. E x p . Biol. 59, 565-581. Webb, P. W. (1973b). Kinematics of pectoral fin propulsion in Cymatogaster aggregata. J. Exp. Biol. 59, 697-710. Webb, P. W.(1975a). Hydrodynamics and energetics of fish propulsion. Bull. Fish. Res. Board Can. No. 190, 159pp. Webb, P. W. (1975b). Efficiency ofpectoral fin propulsion in Cymatogaster aggregata. In “Swimming and Flying in Nature” (T. Y. T. Wu, C. J. Brokaw, and C. Brennen, eds.), pp. 573-584. Plenum, New York. Webb, P. W. (1975~).Acceleration performance of rainbow trout Sulmo gairdneri (Richardson) and green sunfish Lepomis cyanellus (Rafinesque). J . E x p . B i d . 63, 451-465. Webb, P. W. (1976). The effect of size on the fast-start performance of rainbow trout, Salmo gairdneri, and a consideration of piscivorous predator-prey interactions. J. E x p . Biol. 65, 157-177. Webb, P. W. (1977). Effects of median-fin amputatiop on fast-start performance of rainbow trout (Salmo gairdneri).J.E x p . Biol. 68, 123-135. Weihs, D. (1972). A hydrodynamicd analysis of fish turning manoeuvres. Proc. R. SOC., Ser. B . 182,59-72. Weihs, D. (1973a). The mechanism of rapid starting of slender fish. Biorheology 10, 343-350. Weihs, D. (1973b). Hydromechanics of fish schooling. Nature (London)241,290-291. Weihs, D. (19734. Optimal cruising speed for migrating fish. Nature (London) 245, 48-50. Weihs, D. (1973d). Mechanically efficient swimming techniques for fish with negative buoyancy.]. Mar. Res. 31, 194-209. Weihs, D. (1974). Energetic advantages of burst swimming of fish. J. Theor. B i d . 48, 215-229. Weis-Fogh, T. (1973). Quick estimates of flight fitness in hovering animals, including novel mechanisms for life production.]. E x p . Biol. 59, 169-230. Wu, T. Y. (1961). Swimming of a waving p1ate.J. Fluid Mech. 10,321-344. Wu, T. Y. (1971a). Hydromechanics of swimming propulsion. Part 1. Swimming of a two-dimensional flexible plate at variable forward speeds in an inviscid fluid. J . Fluid Mech. 46,337-355. Wu, T. Y. (1971b). Hydromechanics of swimming propulsion. Part 2. Some optimum shape prob1ems.J. Fluid Mech. 46, 521-544. Wu, T. Y. (19714. Hydromechanics.of swimming propulsion. Part 3. Swimming and optimum movements of slender fish with side fins.J. Fluid Mech. 46,545-568. Wu, T. Y. (1971d).Hydromechanics of swimming fishes and cetaceans.Ado. Appl. Math. 11, 1-63. Wu, T. Y., and Newman, J. N. (1972). Unsteady flow around a slender fish-like body. Proc. Int. Symp. Directional Stabil. Control Bodies Mooing Water, London Inst. Mech. Eng. Publ., Pap. No. 7. pp. 33-42. Wu, T. Y. T., Brokaw, C. J., and Brennen, C. (eds.) (1975). “Swimming and Flying in Nature,” 1005 pp. Plenum, New York. Yuen, H. S. H. (1966). Swimming speeds of yellowfin and skipjack tuna. Trans. Am. Fish. SOC. 95,203-209. Zuyev, G. V., and Belyayev, V. V. (1970). An experimental study of the swimming of fish in groups as exemplified by the horse mackerel (Trachurus mediterruneus ponticus Aleev).J. Ichthyol. (USSR) 10, 545-549.


LOCOMOTION BY SCOMBRID FISHES: HYDROMECHANICS, MORPHOLOGY, AND BEHAVIOR J O H N J . MAGNUSON I. Introduction ................................................... 11. Observed Swimming Speeds.. . . . . . . . . . . . , . . . , . . . . . . . . . . . . . . . . . A. Sustained Swimming . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Prolonged Swimming . . . . . . . . . . . . . . , . . . . . . . . . . . . . . . . . . . . . . . . C. Burst Swimming .... .. .. .. ........ . ... . , ,....... ........... . 111. General Considerations of Swimming Equilibria . . . . . . . . . . . . . . . . . IV. Weight, Buoyancy, Hydrodynamic Lift, and Prediction of Sustained Speeds.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . . . . . A. Mechanisms of Hydrostatic Equilibrium . . . . . . . . . . . . . . . . . B. The Lifting Surfaces . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . . . . . . . . . C. Surface Loading of Lifting Surfaces . . . . . . . . . . . . , . . . , . . . . . . . . . . . . .. . . . . .. , . D. Predictions of Sustained Speed . . . . . . V. Resistance to Fonvard Movement.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . A. Components of Drag . . . . . . ts . . . , . . , . . . . . . . . . . . . . . B. Distribution of Drag among C. Adaptations for Drag Reduction.. . . . . . . . . . . . . . . . . . . . . . , . . . . . . . .. . . .. .. . . . . . . .. . . D. Summary . . . . . . . . . . . . . . . . . . . ... .. .. . .... .. ... .. . VI. Thrust Production . . . . . . . . . . . . . . . . . A. Anatomy . ... .. .. ... . . . .. .. .. .. . . .. . . . . . . . . . . . .. ............ B. Movements and Postures of the Caudal Fin ... . ........... C. Theory and Magnitude of Thrust . . . . . . . . . . . . . . . . . . . . . . . . . VlI. The Locomotory System . . , . . . . . . . . . . . . , . . . . . . . . . . . . . . . . . . . .. . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

.

..

.

.

..

..

.

.. .. . .

.

.

. ..

...

.

240 241 241 247 248 250 251 252 256 262 265 267 268 274 277 288 288 289 295 301 305 308

Symbols A

AR b b,

amplitude of trailing edge of caudal movement (Fig. 13) in centimeters aspect ratio of hydrofoil = b / c = b2/S span of caudal fin (Fig. 13) in centimeters span of pectoral fins (Fig. 4) in centimeters 239 FISH PHYSIOLOGY. VOL VII Copyright @ 1978 b y Academic Pre% Inc All right, of reproduction in m y form re5erved ISBN 0-12 350407-4

JOHN J. MAGNUSON

buoyant force in dynes chord length of hydrofoil in centimeters coefficient of friction plus form drag coefficient of friction drag coefficient of lift coefficient of lift for keel coefficient of lift for pectoral fins coefficient of thrust drag in dynes frequency of caudal fin beats in number per second ratio of gliding to swimming drag = ( 1 - qP)/l fork length in centimeters lift in dynes mass of fish in grams Reynolds number surface area of caudal fin, one side only (Fig. 13), in square centimeters projected surface area of keel (Fig. 4) in square centimeters total lifting area of pectoral fins (Fig. 4) in square centimeters wetted surface area of part in question in square centimeters weight of fish in dynes maximum transverse velocity of the trailing edge of caudal fin measured at axis of tail beat in centimeters per second root mean square transverse velocity or the average transverse velocity of trailing edge of caudal fin in centimeters per second swimming speed in centimeters per second maximum angle of attack of caudal fin measured when crossing axis of tail beat (Fig. 13E) in degrees or radians hydromechanical efficiency of the caudal fin or proportion of total thrust that contributes directly to forward movement proportion of thrust force lost as drag induced from caudal movement feathering angle (Fig. 13E) in degrees or radians density of environment in grams per cubic centimeter density of fish in grams per cubic centimeter angular velocity in radians per second angle of sweepback (Figs. 4,13) ofcaudal fin (Eq.28) in degrees

I. INTRODUCTION Fishes of the family Scombridae (tuna, bonito, and mackerel) swim quickly and swim continuously. These two unique features of their locomotion have stimulated two recurring questions in the literature:

4.

LOCOMOTION BY SCOMBFUD FISHES

24 1

Why do they never stop swimming, and how can they swim so fast? Partial answers to these and similar questions are to be found in considerations of hydromechanics and of the adaptations related to locomotion that seem to dominate the anatomy, behavior, and physiology of scombrids. Their continuous shimming is closely tied to hydromechanics because they are negatively buoyant pelagic fishes that oppose their weight with lift generated b y their extended pectoral fins as they swim forward (Magnuson, 1966,1970,1973).Their shape provides evidence to the idea that they are the most highly evolved teleosts in respect to minimizing resistance to forward movement (Walters, 1962; Aleev, 1963; Hertel, 1966). Their carangiform mode of locomotion with lunate tail (Lighthill, 1969, 1970, 1975; Wu, 1971; Chopra, 1975; Webb, 1975; Aleyev, 1977; Chopra and Kambe, 1977) concentrates all thrust at the caudal fin and represents the extreme of adaptations for fast and efficient swimming. While scombrids may best exemplify the fast and continuous swimmer of the pelagic ocean, they are not entirely unique. Mackerel sharks (Lamnidae) such as the shortfin mako, Zsurus oryrinchus, and white, Carcharodon carcharias, have the same general characteristics of both fast and continuous swimming as do the dolphin fishes, Coryphaenidae. In addition the mode of fast swimming with stiff body and rigid lunate tail is shared with other teleosts such as billfishes (Istiophoridae), the swoTdfish (Xiphias gladius), and with many marine mammals such as dolphins, porpoises, and whales. Many of these are not obligatory swimmers but can stop and float in the water. Similarly, many of the continuous swimmers do not have lunate tails nor swim with stiff body movements-some jacks (Carangidae), herring (Clupeidae), the bluefish (Pomatomus saZtaZtrix) to name a few, as well as most sharks. My purpose is to explore locomotion by scombrids, a group at the edges of two lines of specialization in regard to locomotionswimming quickly and swimming continuously. Swimming performance, hydromechanics, and related anatomy and behavior are treated.

11. OBSERVED SWIMMING SPEEDS A. Sustained Swimming Scombrids do not rest in the sense of not swimming (Magnuson, 1973). The minimum speed published for adults is for the wahoo (Acanthocybium solanderi) at 41 cmlsec (0.33t'lsec). Minimum speeds

242

JOHN J. MAGNUSON

observed for seven other species are usually greater than 1 t//sec and for two species minimum speeds are near 2 k'/sec (Fig. 1A; Table I). Roberts (1975) observed 2-12 cm long Atlantic mackerel (Scomber scombrus) holding stationary positions in an aquarium. On the other hand, I have observed the young, ca. 2-3 cm long, of other scombrids swimming actively in aquaria. Sccmbrids in large shoreside tanks and at sea settle into a mode of relatively steady continuous travel. Swimming is volitional and spontaneous. The mean speed of travel for eleven species (Table I; Fig, 1A) ranges from 22 to 280 cm/sec and 0.33 to 2.2 e/sec, with Reynolds numbers of from 4.2 x lo4 to 6.3 x lo6.The Reynolds number ( R L )is the product of the fish's length (8) and speed (U) divided by the kinematic viscosity of water: RL=

eu 0.01

The highest mean Reynolds number for sustained swimming (6.3 x 1@), observed for bluefin tuna over 200 cm long, is just above the range over which flow would be expected to be laminar over a rigid streamlined body (Webb, 1975). With seven exceptions, the above speeds were measured by an observer viewing a tank (7.5m in diameter and 1.1 m deep) from above through a clear acetate sheet onto which the path of the fish was traced (Magnuson, 1969). One species was observed in a water tunnel and one was observed in a 2.9 m diameter doughnut-shaped tank. Three species were observed at sea-two with acoustic transmitters attached to them and one from sequences of aerial photographs. Species do not all have the same speed of sustained swimming. In terms of fork lengths per second, the genera Acanthocybium and Thunnus are slower than A U X ~Euthynnus, S, and Sarda. The wahoo and yellowfin tuna that had the slowest sustained speeds (fork lengths per second) are the two species with the maximum burst speeds observed (Fig. 1B). The persistence of the sustained swimming of scombrids is impressive (Fig. 2). Time of day, temperature, dissolved oxygen, and food deprivation have little influence on sustained swimming. Most striking differences from other fishes are that sustained speeds or volitional activity do not change throughout the die1 period (Fig. 2A), at least when food is not present. These data for kawakawa (Euthynnus afinis) correspond with data from other species, in that day and night speeds are similar (Magnuson, 1973, Fig. 2). The persistence is not laboratory induced because two species observed at sea continued swimming all night (Fig. 1A; Table I).

4.

243

LOCOMOTION BY SCOMBFUD FISHES I

I

I

I

I

u

Q

c

E

n W W

n m n W

f a I-

In

3 In

0

1

0

25

I

I

I

50 75 100 F O R K L E N G T H (cm.)

I

,

125

2.000 0 P a c i f i c Bonito A l l a n l i c Bonilo Bullet Mackerel 0 Kowokawa 0 S k i p l a c k Tuna 0 Y e l l o w f i n Tuna

+

n

1,000 n In

t

m [L

3

m

500

0 25

50 75 L E N G T H (cm)

I00

125

Fig. 1. Swimming speeds of scombrids expressed in terms of distance per unit time, body lengthslsec (t?/sec),and Reynolds number ( R J . (A) sustained speeds and (B) burst speeds. Sources: (1) Blaxter and Dickson (1959); (2) Waiters and Fierstine (1964); (3) Magnuson and Prescott (1966); (4) Walters (1966); (5) Yuen (1966); (6) Yuen (1970); (7) Hunter and Zweifel (1971); (8) Magnuson (1973); (9) Dizon and Neil1 (unpublished); (10) Laurs et al. (1977);(11) Pyatetskiy (19704; (12) MacKay (1976). Bluefin tuna data from Table I are not shown but fish averaging 230 cm long swam at 280 cm/sec (Anonymous, 1975).

Table I Sustained Swimming Speeds of Eleven Scombrids Listed in Order of Decreasing Reynolds Number (RL) Speed R L

flsec

cmlsec

Length (cm)

7.5 x 106

1.6

350

213

6.9

1.3

300

226

6.4~ 106

1.1

270

241

6.2

1.3

290

216

5.5 x 106

0.88

220

250

5.3x 106

1.1

240

219

5.5

X

105

0.77

65

84

All night

5.5

X

105

0.76

65

85

All night

4.4 x 105

0.57

50

87

All night

Species l.a

4 4

Thunnus thynnus (bluefin tuna)

Thunnus alalunga (albacore)

X

X

106

106

Observed duration

Method

Source

Sequential aerial photographs Sequential aerial photographs Sequential aerial photographs Sequential aerial photographs Sequential aerial photographs Sequential aerial photographs Tracked fish with acoustic transmitter Tracked fish with acoustic transmitter Tracked fish with acoustic transmitter

Anonymous (1975) Anonymous (1975) Anonymous (1975) Anonymous (1975) Anonymous (1975) Anonymous (1975) Laurs et al. (1977) Laurs et al. (1977) Laurs et al. (1977)

Acanthocybium solanderi (wahoo) Sarda chiliensis (Pacific bonito) Euthynnus pelamis (skipjack tuna)

01

Thunnus obesus (bigeye tuna) Euthynnus afinis (kawakawa) Auxis rochei (bullet mackerel) Thunnus albacores (yellowfin tuna) Scomber scombrus (Atlantic mackerel) Sarda sarda (Atlantic bonito)

5 . 1 105 ~

0.33

41

125

Continuous

Cinema at sea

Magnuson (1973)

5.0 x 105

1.5

88

57

Continuous

3.5 x 105 3.3 x 105 3.3 x 105

1.5 2.2 1.7

72 84 76

48 39 44

Continuous Continuous All night

Magnuson and Prescott (1966) Magnuson (1973) Magnuson (1973) Yuen (1970)

2.2 x 105 3.3 x 105 1.7 x 105 2.7 x 105

1.6 1.1 1.3 2.1

59 60 47 76

38 55 36 36

Continuous Continuous Continuous Continuous

Time to swim 7.2 m in large tank Traced path large tank Traced path large tank Tracked fish with acoustic transmitter Traced path large tank Traced path large tank Traced path large tank Traced path large tank

2.1 x 105

2.2

68

31

Continuous

Traced path large tank

Magnuson 1973)

1.6 x 105

1.3

46

35

Continuous

Traced path large tank

Magnuson 1973)

9.0 x 104 4.2 x 104 5.6 x 104

0.88 1.2 2.2

28

32 19 16

Continuous Continuous 5-10 sec

Traced path large tank Traced path large tank Swimming" tunnel

MacKay (1976) MacKay (1976) Pyatetskiy (197Oa)

Slowest speed observed from Pyatetskiy's Fig. 2.

22 35

Magnuson Magnuson Magnuson Magnuson

1973) 1973) 1973) 1973)

246

JOHN J. MAGNUSON

Fig. 2. Persistence of sustained swimming of scombrid fish, genus Euthynnus, as influenced by (A) time of day, (B) dissolved oxygen, (C) water temperature, and (D) food deprivation. (A, D) Kawakawa in large shoreside tanks (modified from Magnuson, 1969). (B) Skipjack tuna transferred directly into each concentration from holding tanks saturated with 0,(modified from Gooding and Neill, 1978). (C) Skipjack tuna during day (modified from Dizon et al., 1977).

Sustained speeds of several species are also remarkably independent of ambient temperatures of from 14" to 34°C (Fig. 2C). Stevens and Fry (1972) found no significant change in sustained speeds of two skipjack tuna experiencing a decreasing temperature of 4"Clmin from 24" to 14°C in a small tank of 2400 liters. Dizon et al. (1977) expanded these measurements to more species and individuals, to slower rates of temperature change, and to a 20" range of temperature from lower to upper lethal temperatures. Slower rates of temperature change (l"C/ day over a range of 14"-34°C) did not greatly influence speeds sustained by kawakawa or skipjack tuna in small tanks of 2200 liters. Qlo for both species was approximately 1.1. Similar Qlo values were observed for skipjack tuna and kawakawa at intermediate rates of cooling (0.05"-0.1"C/min from 29" to 18°C) in a larger ring-shaped tank. On the other hand, three yellowfin tuna (Thunnus albacares),at intermediate rates of cooling and corrected for body temperature lags behind ambient temperature, had a Qloof approximately 2.1 (Dizon et al., 1977). Thus, speed of sustained swimming by the euthynnids was essentially temperature independent, but for the thunnid sustained speed in-

4. LOCOMOTION BY SCOMBRID FISHES

247

creased with increased temperature at a Qlonot unlike that observed for many physiological rates in nature. Sustained speeds of skipjack tuna (e = 30-50 cm) in small tanks are independent of dissolved oxygen from 4 to 7 mg/liter (Fig. 2C) (Gooding and Neill, 1978).Oxygen concentrations below 4 mg/liter produced faster swimming but these were not sustained speeds because the fishes almost always died within 150 min. Sustained swimming decreases somewhat with food deprivation (Fig. 2D) (Magnuson, 1969), but even after 5 days without food, kawakawa (C = 41 cm) continue swimming at speeds near 60 cm/sec (1.5k'/sec). These measurements were made in large shoreside tanks. In summary, scombrids of their own volition swim continuously at speeds usually in excess of 0.5 e/sec and as high as 2.2 t'/sec. For the largest species this can result in speeds with R L over 1 x 106. This speed is remarkably uniform for a given species at a given size and persists day and night, over a temperature range of 14"-34"C, over a range of 0, concentrations of 4-7 mg/liter, and in the face of food deprivation for 5 days.

B. Prolonged Swimming There are few data available on prolonged swimming to exhaustion in scombrids because few species have been forced to swim at speeds that result in fatigue. Observations on speeds of fish in feeding activities in the field and laboratory are intermediate to sustained and burst speed. Skipjack in feeding schools at sea had modal speeds of 210-290 cm/sec (3.4-4.3 e/sec) (Yuen, 1966) and feeding kawakawa in large shoreside tanks averaged 180 cm/sec (4.5 t?/sec) (Walters, 1966). Skipjack tuna schools have been followed for over an hour at 400 cm/sec (5-8 l//sec) (Commercial Fisheries Review, 1969). We do not know how long these speeds can be maintained. Several species have been forced to swim to exhaustion. Atlantic mackerel at 16"-17"C in a water tunnel swam about 300 lengths near their top speeds of 300 cm/sec (8.5 e/sec) or from about 35 sec (Table 11). In ongoing studies by Gooding and Neill (1978) skipjack tuna swam to exhaustion at low oxygen concentrations. Examples of these data are: at 1.5 mg/liter dissolved oxygen, the fish swam 10 min at 3.9 [/see before death, and at 3 mg/liter dissolved oxygen they swam 60 min at 2.1 Usec. Skipjack tuna were chased with brooms for 30 min in a large shoreside tank and did not die (Stevens and Fry, 1972),but one

248

JOHN J. MAGNUSON

chased with a dipnet in a small tank stopped swimming and died (Neill et al., 1976). C. Burst Swimming While scombrids have been long observed to be fast swimmers, Walters and Fierstine (1964)were the first to lend scientific credibility to the fact that speeds greater than 10 thee were possible. They measured the rate that yellowfin tuna and wahoo pulled a fishing line from a reel. The line was calibrated with iron filings that were counted by a magnetic pickup on the fishing reel. Speeds were as high as 2066 cm/sec (27 l/sec) for yellowfin and 2134 cm/sec (19 e/sec) for wahoo (Table 11, Fig. 1B). Since 1964 no additional values this high have been measured, but of the eight species for which data are available (Table 11, Fig. lB), measurements on five exceed 10 thee and on all but two exceed Reynolds numbers (R,) 1 x 106. This critical Reynolds number indicates the speed at which flow should shift from laminar to turbulent. Two species apparently exceed an R L of 1 x 10'. Earlier, Watanabe (1942) timed skipjack tuna over a 2 m distance alongside a fishing vessel and obtained speeds greater than 1 x 106 Reynolds number, but it is difficult to associate the size of fish with speeds from his paper. Speeds estimated by Magnuson and Prescott (1966), Walters (1966), Yuen (1966),and Dizon and Neill (unpublished) were all from frameby-frame analyses of motion picture films. Yuen made the estimate by filming feeding schools through underwater viewing ports from the R. V. Charles H. Gilbert. Other films were of fish feeding or pursuing food in large shoreside tanks. Speeds of the mackerels were measured in a swimming tunnel. Where information was given, speeds were measured over time intervals from 0.07 to 5 sec but, for the most part, the duration that speeds could be maintained cannot be extracted from the data. The highest speeds were for short periods as can be observed from two records in Fig. 2 of Walters and Fierstine ( 1964). Only data collected with the calibrated fishing line contain speeds that exceed an R L of 6 x 106 (Fig. l B , Table 11). Walters and Fierstine ( 1964) believed that their estimates, if biased, were underestimates because the fish could turn and thus not be going directly away from the boat, and in addition the line and lure would add to the drag and slow the fish. Yuen (1966)also felt that these high speeds were reasonable when compared to slower speeds he measured because the activities of the fish were quite different. Those collected with fishing

Table 11: Burst Swimming Speeds of Eight Scombrids in Order of Decreasing Reynolds Number (RL) Speed Species

RL

ekec cm/sec

Length '(cm)

Observed duration Method Calibrated fishing line Calibrated fishing line Calibrated fishing line Calibrated fishing line Calibrated fishing line Calibrated fishing line Calibrated fishing line Calibrated fishing line Cinema at sea Cinema at sea Cinema large tank

Source

106 106

7" 10 8 19

2134 1211 1201 2066 1253 993 688 522 545 636 950

113.T.L. 100 T.L. 92 T.L. 76 T.L. 76 T.L. 71 T.L. 71 T.L. 71 T.L. 52 F.L. 79 F.L. 50 T.L.

0.1-2.2 0.1-2.2 -

3.8 x 106

15

750

50 T.L.

0.5

3.6 x 106 3.3 x 106 3.4 x 106 2.1 x 106

9 14 10 6

562 688 588 770 370

64 F.L. 48 F.L. 57 F.L. 57 F.L.

0.1-2.2 0.1-2.2 0.1-2.2 0.1 -

Cinema at sea Cinema at sea Cinema at sea Direct observation at sea Cinema large tank

2.0 x 106 1.6 x 106 1.1x 106

12 10 8

500

400 300

40 F.L. 40 F.L. 36

0.1-0.2 0.1-0.2

-

Cinema large tank Cinema large tank Swimming tunnel

Walters and Fierstine (1964) Walters and Fierstine (1964) Walters and Fierstine (1964) Walters and Fierstine (1964) Walters and Fierstine (1964) Walters and Fierstine (1964) Walters and Fierstine (1964) Walters and Fierstine (1964) Yuen (1966) Yuen (1966) Dizon and Neill (unpublished) Dizon and Neill (unpublished) Yuen (1966) Yuen (1966) Yuen (1966) Watanabe (1942) Magnuson and Prescott ( 1966) Walters (1966) Walters (1966) Blaxter and Dickson (1959)

Scomberjaponicus

6.6 x 105

8

226

29

-

Swimming tunnel

Hunter and Zweifel (1971)

(Pacific mackerel) Sarda sarda (Atlantic bonito)

2.0 x 105

7.8

128

16 T.L.

Water tunnel

Pyatetskiy (197Oa)

Acanthocybium solanderi

(wahoo) Thunnus a1bacores

(yellowfin tuna)

Euthynnus pelamis

(skipjack tuna)

Sarda chiliensis (Pacific bonito) Euthynnus afinis

(kawakawa) Scomber scombrus

2.4 x 1.2 x 1.1 x 1.6 x 9.5 x 7.0 x 4.9 x 3.7 x 2.8 x 5.0 x 4.8 x

107 107 107

lo7 106 106 106 106

106

19 12 13 27" 16a 14" lo"

ca. 5

-

-

ca. 5

-

-

-

Cinema large tank

(Atlantic mackerel)

5-10

Body lengths per second were recalculated from Table 1 of Walters and Fierstine (1964) on the basis of median lengths of fish in school rather than mm2mum length of fish in school.

250

JOHN J. MAGNUSON

gear were fleeing, while Yuen's data were on fish in a feeding school. However, even if the data collected with the calibrated reel were dismissed as questionable, other measurements on three scombrids exceed an R L of 106. The skipjack tuna exceed an R L of 4 x 10s as measured b y two authors and 18 t'/sec by one author. While I think the estimates from the fishing reel may be on the high side, burst speeds between 10 and 20 t'/sec and in excess of an R L of 1 x 10s are well documented for scombrids. Burst swimming capabilities vary amofig scombrids. Ranking the species either by maximum lengths swam per second or maximum Reynolds number suggests that the genera Acanthocybium, Thunnus, and Euthynnus are faster swimmers for their length than are Sarda and Scomber. In summary, while burst speeds vary among scombrids, the fastest measured to date are near 2000 cm/sec, 20 t'/sec and R L of 2 x 107. Most have burst speeds that exceed 10t'/sec. Scombrids are among the fastest if not the fastest fishes for which good data are available.

111. GENERAL CONSIDERATIONS OF SWIMMING EQUILIBRIA

The swimming speeds of scombrids are well documented (see Section I1 and Chapter 2) and indicate that these fish are indeed continuous swimmers and that they can swim extremely fast. In both modes of swimming (sustained and burst), speeds of certain large sized or fast species exceed a Reynolds number of 1 x 106. One level of explanation for the necessity and the possibility of their particular swimming behaviors comes from an analysis of the equilibria between both the vertical and horizontal forces acting on the animal. These forces are weight, buoyancy, and hydrodynamic lift in the vertical direction and thrust and drag in the horizontal direction (Fig. 3). A swimming scombrid produces thrust and drag which oppose each other. The weight of the fish is opposed by buoyancy and hydrodynamic lift. When opposing forces are equal the fish is in equilibrium, that is, swimming at a constant speed or constant depth. If not, the fish accelerates or decelerates or rises or sinks until the forces are again in equilibrium. For scombrids the equilibrium between thrust and drag is intimately related to the equilibrium between weight, buoyancy, and lift. This is because scombrids are heavier than water and they balance the vertical forces by swimming continuously with pectoral fins extended. Hydrodynamic lift is produced on the pectoral fins. While this adds to buoyancy and balances the vertical forces, the imposed requirement of

4. LOCOMOTION BY

WElGWT

251

SCOMBFUD FISHES

:@!+gj ... .....

“t

BUOYANCY PLUS HlDRODVNbUlC LIFT

Fig. 3. Forces acting on a swimming scombrid and axis of yaw, pitch, and roll. @ indicates location of the center of gravity. (Adapted from Magnuson, 1970.)

swimming to produce hydrodynamic lift complexes the balance between horizontal forces. Drag or resistance, as expected, results from the movement of the animal through the water, but significant drag also is induced in conjunction with the lift produced on the pectorals and even, in a sense, from the thrust produced on the caudal fin. Thus, an understanding of the hydromechanics of swimming by scombrids involves not only an analysis of thrust and drag but also an analysis of the mechanisms and effects of maintaining vertical equilibrium. These relationships are treated below-vertical forces in Section IV, horizontal forces in Sections V and VI. The interdependencies are pointed out and discussed in each section but an attempt to integrate them is presented in Section VII. I n addition the hydrodynamic stability of the swimming fish can be considered in terms of pitch, roll, and yaw (Fig. 3) (Alexander, 1967). Pitch and yaw refer to longitudinal stability in the vertical and horizontal planes, respectively. Roll refers to lateral stability or rotation in a transverse plane. Forces produced by the paired and median fins oppose forces producing these instabilities, or forces produced by the paired and median fins contribute in a controlled way to pitch and yaw for vertical and horizontal steering. These aspects of swimming are not treated here.

IV. WEIGHT, BUOYANCY, HYDRODYNAMIC LIFT, AND PREDICTION OF SUSTAINED SPEEDS The sustained speeds cited above were referred to b y Magnuson (1970, 1973) as minimum speeds for hydrostatic equilibrium. Hydro-

252

JOHN J. MAGNUSON

dynamic lift on the extended pectoral fins is generated as the fish swims forward with thrust from the caudal fin. The lift on the pectorals balances weight not met by buoyancy and, as discussed in Section 111, results in an equilibrium between vertical forces. The mechanism of maintaining hydrostatic equilibrium is analyzed below to develop quantitative predictions of the speeds sustained by swimming scombrids. There are few other groups of fishes for which such an analysis can be used to accurately predict minimum levels of activity over the size range of the species. These estimates of speed and lift production also contribute to estimation of drag on a swimming scombrid.

A. Mechanisms of Hydrostatic Equilibrium 1. WEIGHT The estimation of the fish’s weight is a first step in the analysis. Weight, like all forces, is the product of a mass and an acceleration and is measured in dynes or as the force that will accelerate 1 g of mass 1 cm per second per second. Thus, a fish’s weight (WJ is equal to its mass (Mf) times the acceleration of gravity (g):

Wf = M , g where g is approximately 980 cm/sec2.

( 2)

The mass-length relationships common in fishery biology provide a good data base for weight estimation and, as expected, are approximately the function of length cubed for scombrids (Magnuson, 1973). Yet, weights of scombrids of the same length differ considerably; for example, yellowfin tuna are more than four times heavier than the wahoo of the same length. Such differences are significant in the balance between vertical forces and contribute to differences in predicted speed.

2. BUOYANCY Fortunately for a scombrid most of its weight is opposed by buoyancy that results from the large mass of water the fish displaces. If this were not the case, the hydrodynamic lift required would be too great to produce by sustained swimming as it would impose impossible speeds. The buoyant force (B is equal to the mass of water displaced ( M w ) times acceleration of gravity: f)

Bf = M w g

(3)

4.


253

where the mass of water displaced (M w) is equal to the volume of the fish (Vf) times the density of seawater (pe):

Mw = PeVf ( 4) Volume of the fish can be calculated by determining the density of the fish pf with Archimedes’ principle (Alexander, 1968) and dividing:

v f =Mf Pf

The resulting equation after substitution and rearranging to solve for buoyancy is

From Eq. (6) it can be seen that the buoyant force is equal to the weight of the fish ( M f g )times the proportion countered by buoyancy, pelpf.This ratio between the density of water and the density of the fish when multiplied by 1000 (an approximation of g ) has been referred to as the sinking factor (Lowndes, 1955; Jones, 1957). The following example will demonstrate that most of a scombrid’s weight is opposed b y buoyancy. A skipjack tuna with a mass of 10 kg ( M f = 10,000) weighs 9.8 x 106 dynes from Eq. (2) ( W f = 10,000 x 980 = 9.8 x 106 dynes). The proportion of the weight opposed by buoyancy‘is 0.94 (pelpf = 1.025l1.091 = 0.94) and the buoyant force is 9.2 x 106 dynes from Eq. (6)(B, = Wf x 0.94 = 9.2 x 106 dynes). Even though the skipjack has no gas bladder, 94% of its weight is opposed by buoyancy. All scombrids measured to date (Table 111) have densities greater than the seawater in which they were caught. Consequently not all of their weight is opposed b y buQyant forces. Since scombrids are pelagic, their excess weight also is not countered by resting on the bottom. Even though buoyant forces are great, weight does increase approximately as a cubic function of length, and large fish become exceedingly heavy for their length. One adaptation that increases the proportion of weight countered by buoyancy is the gas bladder. Many scombrids have no gas bladder, but some, such as the yellowfin tuna, bigeye tuna (Thunnus obesus), albacore (Thunnus alahnga), wahoo, and Pacific mackerel (Scomber japonicus), have. Some species such as yellowfin tuna (Magnuson, 1966, 1973)and albacore (Dotson, 1977)have allometric growth of the gas bladder that results in a greater proportion of their weight being

254

JOHN J. MAGNUSON

Table I11 Densities of Twelve Scombrid Species in Order of Decreasing Density Density of scombrids (g/cm3)

Species

Euthynnus pelamis" (skipjack tuna) Euthynnus afinis" (kawakawa) Auxis rochei" (bullet mackerel) Sarda sardab (Atlantic bonito) Sarda chiliensis" (Pacific bonito) Auxis thazordb (frigate mackerel) Thunnus albacoresn (yellowfin tuna) Thunnus alalunga (a1bacore) San Diego July" San Diego Sept." Thunnus ohesusn (bigeye tuna) Scomberjaponicuso (Pacific mackerel) Scomher scombrus 4tlantic mackerel) Juneb August Septemberb Novemberb September" AI rnthocyhiurn solanderi (wahoo)

Gas bladder present

Source

1.090 1.090 1.094 1.097 1.094 1.091

No

Magnuson (1973)

1.087 1.088 1.091

No

Magnuson (1973)

1.086

No

Magnuson (1973)

No

Aleev (1963)

1.075 1.080

No

Aleev (1963)

1.07

No

Aleev (1963)

1.086 1.087 1.068 1.058 1.054

Yes

Magnuson (1973)

Yes

Dotson (1977)

Yes

Magnuson (1973)

Yes

Magnuson (1973)

No

Aleev (1963)

Yes

Aleev (1963) MacKay (1976) Aleev (1963) Aleev (1963) Lowndes (1955) Magnuson (1973)

0-2

1.08

2-4

Mass (kg) 4-6 6-8

8-10

10

1.08

1.088 1.082 1.063 1.060 1.066 1.047

1.056

1.054

1.06 1.06 1.03 1.02 1.051 1.028

Density of habitat, 1.025 &m3. 1.01 g/cm3.

* Density of habitat,

carried by buoyancy after they attain masses greater than 2 kg. By the time yellowfin tuna reach 8-10 kg, their weight not balanced by buoyancy, would be twice as great if the gas bladder had not developed. The gas bladder of a 10 kg wahoo is sufficiently large that 99.7% of the fish's weight is opposed by buoyancy (Magnuson, 1973)

4. LOCOMOTION BY SCOMBRID

FISHES

255

in contrast to the 94% calculated above for skipjack tuna. Of those species that attain masses greater than 70 kg, all have gas bladders, whereas of those with a maximum mass less than 6 kg only 25% have gas bladders (Magnuson, 1973). Apparently, larger scombrids tend to have a gas bladder, to have lower densities, and to oppose a greater proportion of their weight by buoyancy than do smaller scombrids. Available evidence indicates that this generalization applies to comparisons both within and among species. A second mechanism for increasing the weight carried by buoyancy is to have reduced density by increased fat content. In some sharks, fatty livers greatly reduce density (Bone and Roberts, 1969; Baldridge, 1970, 1972). Aleev (1963) (Table 111) noted that seasonal changes in densities of Atlantic mackerel were associated in a sensible way with seasonal changes in fat content. The lowest density (Table 111) was associated with 23.1%fat in the flesh in fall and the highest density with 2.9% fat in spring. Albacore are more dense when first arriving on the California coast in July than after 2 months of feeding in coastal waters (Dotson, 1977). Calculations on kawakawa (Magnuson, 1970) indicate that 44% fat is required if buoyancy were to equal weight. Variations in observed densities of kawakawa are explained by a range of fat content of only 5-15% fat. However, any increase in fat content would reduce density, and 10%fat content in kawakawa can reduce the weight not balanced by buoyancy by about 25% over a fat-free condition. Of the species listed in Table I11 without a gas bladder, observed densities reveal that fat content is not sufficiently high to attain neutral buoyancy. Only the Atlantic mackerel is reported to have higher fat and lower density at larger sizes (Aleev, 1963). While gas bladders and fat contents reduce somewhat for scombrids the weight not countered by buoyancy, additional upward forces are required to obtain equilibrium between vertical forces. It is these forces remaining to be opposed by hydrodynamic lift that necessitate continuous swimming. For a realistic prediction of sustained speed, special care must be taken to obtain accurate measurements of density of fish that have a gas bladder (see Methods in Magnuson, 1970, 1973; Dotson, 1977).

3. HYDRODYNAMIC LIFT Among scombrids the excess weight not balanced by buoyancy is opposed by hydrodynamic lift generated b y the extended pectoral fins as the fish swims forward (Magnuson, 1966, 1970, 1973). The same mechanism has been explained by Aleev (1963) with sturgeon and by Alexander (1965, 1968) with sharks.

JOHN J. MAGNUSON

256

The lift (L) required to obtain hydrostatic equilibrium can be calculated as the difference between weight and buoyancy of the fish:

L=WI-BI

(7)

On substitution of Eqs. (2) and (3) and rearrangement, this becomes

which is the excess density (pr- pe) times the volume of the fish (&If/ p3 times the acceleration of gravity. Excess density, like sinking factor, has been used to characterize the weight-buoyancy relationships of fishes. It is the same as the “buoyancy A” of Aleev (1963). In summary, the lift required of a fish to balance the inequity between weight and buoyancy depends on the size of the fish (M3 and the difference between the density of the fish and its habitat. Less lift is required for smaller fish and those with a density closer to that of the water in its habitat.

B. The Lifting Surfaces 1. THE PECTORAL FINS

Scombrids not only swim continuously, but do so usually with their pectoral fins extended laterally from their body and with their pelvic and spiny dorsal fins appressed (Figs. 4 and 5) (Magnuson, 1966, 1970). The pectoral fins are structured and used in such a way that they are obvious lifting hydrofoils. Lift on a pectoral fin would be produced by the lower pressure on the upper than on the lower surface. Water flows farther and thus faster over the upper surface and the resulting pressure difference produces a net lift. The fin and fish are essentially lifted upward rather than pushed upward. In addition, two other sources of hydrodynamic liA have been considered for scombrids, the caudal keel and the body itself (Fig. 4A). Lift production b y a hydrofoil, such as the extended pectoral fins, depends directly on the lifting area of the fins (S J and characteristics of the hydrofoil that influence its coefficient of lift (CL), Lift is also proportional to the speed of the fish squared (U2)and the density of water. The equation that relates the required lift to speed and the characteristics of the lifting surfaces L = Y2peCL.SpU2

4.

LOCOMOTION BY SCOMBRID FISHES

257

Fig. 4. Diagrams based on kawakawa of the lifting surfaces, especially the pectoral fins (adapted from Magnuson, 1970).(A) Dorsal view showing lifting areas of the pectoral fins, keel, and body. (B) Angle of attack. (C) Dorsal view showing method to determine sweepback, span, and hydrodynamic center of the pectoral fins. (D) Examples of variable sweepback. (E) Dihedral angle from frontal view. (F)Longitudinal locations of centers of lift from pectoral fins, keel, and body, in respect to the center of gravity.

is taken directly from aerodynamics of wings. General discussions of its basis and derivation are in von Mises (1945), Prandtl and Tietjens (1934),von Kirmin (1954), and, in respect to aquatic animals, Alexander (1968). A number of other postural characteristics influence the coefficient of lift for the pectoral fin and consequently the relation between speed and lift production. A cambered fin (Fig. 4B) at zero angle of attack relative to the horizontal or even at slight negative

258

JOHN J. MAGNUSON

Fig. 5. Dorsal photograph of ( t o p )a euthynnid and (bottom)a thunnid showing variation in lifting areas and posture of pectoral fins. (Photos from National Marine Fisheries Service, Biological Laboratory, Honolulu.)

4.


259

angles of attack would produce lift. Within limits the greater the camber the greater the coefficient of lift (CL).The lift coefficient (C,) also increases with increasing angles of attack (Fig. 4B) until the fin stalls. A twisted fin has smaller angles of attack nearer the tip, a feature which helps prevent the tip of the fin from stalling first. The relations between lift and speed and the characteristics of the pectoral fins are well illustrated b y the behavior and postures of a scombrid swimming at different speeds. As a scombrid swims faster, lift increases as speed squared [Eq. (9)]but lift required remains constant. To maintain a level course at faster speeds, the pectoral fins must be regulated in such a way that hydrodynamic lift does not surpass excess weight and cause the fish to rise. Scombrids use at least two mechanisms to reduce lift from pectorals at faster speeds. Kawakawa reduce the time that the pectoral fins are extended from 100%at slow speeds to 0% at moderate speeds (Magnuson, 1970). For example, a captive kawakawa, 42 em long, that had just fed extended its fins continuously at 1.6 t'lsec and appressed them continuously at speeds of 2.8 t'lsec and greater. The second mechanism of sweeping them back farther at faster speed reduces the effectiveness of the extended pectoral fins of kawakawa (Magnuson, 1970) and Atlantic mackerel (MacKay, 1976). Increasing sweepback reduced the area, the span, and the lift coefficient of an extended pectoral fin. For example, 42 cm kawakawa in steady swimming swept the fins back more at faster speeds. They swam at 1.3 t'/sec with the pectorals swept back 25" after 5 days of food deprivation, but when just stimulated with food odor they swam at 3.0 tlsec with a 52" sweepback.

2. THE KEEL AND BODY

The keel and the body (Fig. 4A) are less obvious as lifting hydrofoils and may be rather unimportant in lift production compared with the pectorals (Magnuson, 1970). The body of scombrids sometimes can be discounted as a lifting surface at sustained speeds. In contrast to the bodies of sturgeon (Aleev, 1963) and sharks (Harris, 1936), they are not cambered (Magnuson, 1970). Kawakawa at sustained speeds swim with no angle of attack to the body (Magnuson, 1970), and no lift would be expected from a symmetrical body at zero angle of attack (Munk, 1924). But Atlantic mackerel do swim with a positive angle of 9" to the body (Muir and Newcombe, 1974) and the body was calculated to provide 14% of the lift (MacKay, 1976).

260

JOHN J. MAGNUSON

The keel (Fig. 4A,F) at best is a complex lifting surface (Magnuson, 1970). Water flow alternates across it with each beat of the caudal fin (Fig. 6). Flow is directed across it by the finlets that act as flow fences (Magnuson, 1970; Aleyev, 1977).The keel is a noncambered, flattened area with lateral extensions at the peduncle. At sustained speeds the caudal region behind the second dorial is deflected downward an average of 5"-6". Since flow passes across the keel and the keel has an angle of attack it should produce some lift. Its area is about 20%of the lifting area of the pectorals and has a lift coefficient similar to the pectorals (Magnuson, 1970). Since the caudal region is deflected slightly, the caudal fin would be expected to produce a vertically directed vector along with the horizontal vector of thrust. Magnuson (1970, 1973), in an analysis, discounted this as a significant source of lift for Euthynnus, Thunnus, A U X ~ Sand , Sarda. But in the Atlantic mackerel (MacKay, 1976) the caudal fin is expected to provide significant lift because the body is at a positive angle of attack and because that species also swims with the plane of the caudal fin tilted to the side. Thus a lift force is produced as the caudal fin is swept back and forth (Aleyev, 1977).

Fig. 6. Dorsal photograph showing keel and posture of finlets during sustained swimming. Keel and caudal fin being swept toward bottom of page. (From Magnuson, 1970, Hydrostatic equilibrium of Euthynnus ufinis, a pelagic teleost without a gas bladder, Copeia pp. 5685.)

4. LOCOMOTION BY SCOMBFUD FISHES

3.

COMPUTATION O F

26 1

LIFT COEFFICIENTS

Estimates of the lift coefficients of the lifting surfaces are needed to quantitatively relate swimming speed and required lift. The lift coefficient of the pectorals and keel can be computed from Eq. (9) solved for C L. Required lift, the density of the environment, the lifting area of the pectorals, and the speed of sustained swimming can all be measured (Magnuson, 1970). In addition, required lift to counter excess weight must first be partitioned between the pectorals and the keel. This can be done by solving two simultaneous equations (Alexander, 1968; Magnuson, 1970): one, that lift from the pectorals and keel must sum to equd required lift and, two, that the lift must balance around the center of gravity to maintain longitudinal stability. The excess weight can be considered to act at the center of gravity. The greater distance from the center of gravity to the keel than to the pectoral means that a smaller lift from the keel could balance the larger lift from the pectorals (Fig. 4F) b y analogy with a first order lever arm. In the solution for kawakawa, lift from the pectorals should be x l / x l = 0.46/0.11, or four times the lift from the keel. The location of the center of buoyancy could alter the above interpretation. In scombrids the center of buoyancy may be a few millimeters behind the center of gravity (Magnan, 1929; Bone, personal communication). If so, since the buoyant force is so large, it might, even with such a short level arm, balance the lift from the pectoral fins about the center of gravity for longitudinal stability. This would not alter the idea that the keel should act as a lifting hydrofoil based on its anatomy and posture, but perhaps the keel does not carry as much as 20% of the excess weight. Consequently Magnuson ( 1970) calculated lift coefficients for two situations: (1)lift behind the center of gravity from keel only, and (2) lift behind the center of gravity from buoyancy only. Computed coefficients pf lift (C,) (Table IV) calculated from captive kawakawa range from 0.6 to 1.0 for pectoral fins based on total lifting area (Fig. 4A)and from 0 to 0.9 for the keel. The coefficients are not unreasonable for efficient cruising but are less than the maximum that can be achieved from a wing with plain flaps when C, may equal 1.9, or modern slotted wings with leading and trailing edge flaps. Since the area of the hydrofoil is so important in determining the lift produced, the large variations among scombrids in pectoral fin size (Fig. 5) are important in determining the differences in sustained swimming speeds of scombrids (Magnuson, 1973). At a length of 100 cm, yellowfin tuna have a lifting area almost four times that of the wahoo. Fish with a larger pectoral should be able to produce more lift at a given speed. Those species that have a maximum mass greater

262

JOHN J. MAGNUSON

Table IV Coefficients of Lift (C,) of the Pectoral Fins and Peduncular Keel Computed for a Kawakawa, 42 cm long" Condition of fish Assumptions

Lifting surface

5 Days without food

Just fed

Lift behind center of gravity from keel Lift behind center of gravity from buoyancy

Pectoral fins Keel Pectoral fins Keel

0.8 0.9 1.0 0

0.6 0.6 0.8 0

a

Data from Magnuson (1970).

than 70 kg tend to have pectoral fins that are relatively longer than those of smaller species. As the fish grow, the lifting area increases approximately as a function of fish length squared. Exponents range from 1.7 to 2.7 (Magnuson, 1973; Dotson, 1977).Thus, both among and within species, lifting areas are relatively greater for larger than for smaller fish. Species with longer pectoral fins such as the bigeye tuna and yellowfin tuna have greater sweepback (A = 60")during sustained swimming than those with shorter pectoral fins such as skipjack tuna and kawakawa (A = 43") (Magnuson, 1973).Those with longer fins also have a higher aspect ratio (span/mean chord) which would increase the ratio of lift to drag over that of a shorter fin.

C. Surface Loading of Lifting Surfaces A number which allows comparison of the lifting characteristics of the pectoral fins and other lifting surfaces in the animal kingdom is the loading of the fin (LIS,), or the dynes of weight carried per square centimeter of lifting surface (dynes/cm2).Loading of scombrids range from about 400 dynes/cmZ for wahoo to 6000 dynes/cm2 for skipjack tuna (Fig. 7). The skipjack tuna is the maximum for scombrids because it is the largest species with small pectoral fins and no gas bladder and for which data are also available (Magnuson, 1973). If the keel were assumed to carry 20% of the weight as estimated for kawakawa, then maximum loading of the pectorals would be slightly less or about 5000 dynes/cm*.Three species without gas bladders that are larger than the skipjack tuna might have a higher loading: the black skipjack (Euthynnus alletteratus), king mackerel (Scomberomorms cavalla), and Scomberomorus commerson.

4. LOCOMOTION BY

263

SCOMBRID FISHES

0o0 l0,OOO

\OO'

A

00"

\O'

0O0 \*

0 Wahoo 0 P a c i f i c Bonito

+ Bullet

Mackerel

0 Kawakawa I

1,000

Bigeye 'H X Lemon

In Q c

Tuna Shark

,O0

21

-0

0

n

E

Atlantic Sharpnose Shork @ Tiger Shark A Bull S h a r k

@ .

0 \ v) 0)

t

\o

-," W

z -

I-

r c3

n U

\ s

W

3

10

I

I

10

too

1,000

10,000

L I F T I N G A R E A (ern?) Fig. 7. Comparison of the loadings of lifting surfaces among scombrids, sharks, birds, and bats. Diagonal lines are surface loading isopleths. Areas for bats i n d birds are for the wings, for fish S , in Fig. 4A. Weight is less buoyancy for fish or L in Eq. (7). Sources: albacore (Dotson, 1977); other scombrids (Magnuson, 1973); sharks (Baldridge, 1970, 1972, and personal communication); birds (Hertel, 1966); and bats (Findley et al., 1972). Line fitted by eye on twenty-four species.

At smaller size, skipjack tuna not only weigh less, but have lower fin loadings (Fig. 7). The weight carried per unit area increases approximately in direct proportion to the fish length for species with a constant density. The relations are given by L cc C3and S a e2 so that LISPa e. For skipjack tuna, L a e3.36and S, 0: P2*so that LIS, a (coefficients from Magnuson, 1973, Table IV). Consequently larger skipjack have to swim faster in absolute terms to produce sufficient lift than do smaller skipjack [see Eq. (9)]. Other scombrids without a gas bladder have fin loadings similar to skipjack tuna, but those with a gas bladder have lower loadings either for a given weight or lifting area (Fig. 7). This results not only because the gas bladder greatly reduces density but also because fish with a gas bladder often have larger pectoral fins as well. Pectoral fin loading for yellowfin tuna increases more slowly than for skipjack tuna as the fish grows larger (Fig. 7). At smaller sizes the

264

JOHN J. MAGNUSON

yellowfin have lower fin loading than skipjack tuna because their pectoral fins are larger than skipjack tuna's but as they attain weights near 100 x 103 dynes, the allometric growth of the gas bladder results in a greater proportion of their weight being assumed by buoyant forces. A trend of increasing fin loading with length is countered by the development of the gas bladder. For example, a yellowfin tuna 100 cm long has a fin loading only 1.1 times that of 25 cm fish. With the same change in length, fin loading of a skipjack tuna would have increased by a factor of four. Consequently for yellowfin, larger masses do not produce as great an increase in fin loading and they should be able to maintain'slower speeds than skipjack to counter their weight. Fin loadings of the albacore even decrease at larger sizes because both the gas bladder and the pectoral fins are growing allometrically (Dotson, 1977) with exponents greater than 3 for the gas bladder and greater than 2 for the pectorals. Data on large sharks are especially informative because fin loading has not been measured to date on any scombrid with a mass greater than 12 kg, the wahoo and largest albacore. Pectoral fin loading of the small Atlantic sharpnose shark, Rhizoprionodon terraenovae, and of three large sharks-the lemon shark (Negaprion brevirostris), the tiger shark (Galeocedo cuvieri), and the bull shark, (Carcharhinus levcas)-were all intermediate between scombrids without a gas bladder and birds (Fig. 7). The large sharks ranged from 60 to 240 kg in mass and the largest had the lowest loading among the large sharks. Large fatty livers increase the proportion of the sharks' weight carried by buoyant forces at larger sizes (Baldridge, 1970, 1972). Consequently, the large negatively buoyant sharks, like the larger scombrids, maintain lower fin loadings by lowered densities at larger sizes. They should be able to swim at slower sustained speeds at larger sizes. I think that large scombrids for which we have no data mag also have low fin loadings and retain slower speeds at larger sizes (Magnuson, 1973). Data for the lemon shark, compared with the bullet mackerel (Fig. 7), demonstrate the above point. The lemon shark has a mass of approximately 100 kg. Yet, its pectoral loading is the same as that of bullet mackerel that has a mass of only 0.5 kg but no fatty liver or gas bladder. Assuming that their lifting surfaces are equally efficient in producing lift, both should have to swim at the same speed to produce sufficient lift to keep from sinking. This speed, about 60 cm/sec, is approximately 2 e/sec for the bullet mackerel, but only 0.25 thee for the lemon shark. The lowered speeds and associated energetic advantage of lower fin loading are dramatic, especially for large fish.

4.


265

Some scombrids have lifting areas about one order of magnitude smaller than birds or bats at the same weight (Fig. 7). Thus they have fin loadings about one order of magnitude greater than birds or bats (Fig. 7). For example, a 22 kg skipjack tuna in seawater has about the same weight as an adult cormorant or vulture in air (Hertel, 1966) but has a lifting area similar to the wing areas of medium size birds such as woodpeckers and doves. As pointed out by Magnuson (1970) this order of magnitude difference results in part from the differences in the density of water and air. Water is about 860 times the density of air. If an airborne flyer and a waterborne flyer have the same weight in their respective media, then the product of the C LSJ 2 for the aquatic animal has only to be Vssoth of the same product for an aerial animal. Tuna can provide sufficient lift with smaller lifting surfaces, slower speeds, and perhaps less efficient lifting surfaces than birds and bats. The smaller lifting surfaces account for about one order of magnitude of the approximate three orders of magnitude difference in density between air and water. The other two orders of magnitude must be accounted for by faster speeds of birds or more efficient flight mechanisms. Lifting areas of all groups considered in Fig. 7 increase with weight. The slope or rate of increase appears similar for skipjack tuna, birds, and bats. Hertel (1966) indicated that for birds plus insects the relation was S = 15 W2'3 based on the surface-volume relationships. More recent analyses on birds give similar information (Greenwalt, 1975). The relationships fit data on insects and birds quite well. In all cases, however, the weight increases more rapidly than lifting area and the larger species or larger individuals carry more weight per unit area of lifting surface. Birds approach 1000 dynes/cm2 while scombrids approach 10,000dynes/cm2.The only animals plotted that do not seem to obey this particular two-thirds rule are the yellowfin tuna and albacore. Again this is because buoyancy from the developing gas bladder carries proportionately greater weight as the fish grows, and because (Dotson, 1977). for albacore lifting area increases not as t2but as P.s7 The largest scombrids would be expected to have pectoral loadings even more similar to birds, as was observed for large sharks that had surface loadings similar to storks and pelicans.

D. Predictions of Sustained Speed The minimum speed at which a scombrid can swim and still produce sufficient hydrodynamic lift to balance their excess weight can be

266

JOHN J. MAGNUSON

calculated from the information on required lift and the properties of their lifting surfaces discussed above. Basically Eq. (9) can be rearranged to solve for speed (U) under the condition that the pectoral fins are extended 100%of the time. This equation (Magnuson, 1970, 1973), including both the pectoral and keel lifting surface, is

where Uloo, the speed (cm/sec) of fish with pectorals continuously extended; CL,, coefficient of lift for pectorals; S p, total lifting area of pectoral (cm2);CL,, coefficient of lift for the keel; Sk, lifting area of keel (cmz);L, required lift (dynes); pe, density of environment (g/cc). Minimum hydrostatic speeds of various scombrids were computed from Eq. (10) and compared with observed sustained speeds of scombrids in shoreside tanks at Kewalo Basin, Honolulu. The predictions were quite close (Fig. 8A). Correlation coefficients were +0.9 if all lift were assumed to come from the pectorals or +0.8 if the lift was partitioned between pectorals and the keel. Thus, minimum speeds required for hydrostatic equilibrium are for practical purposes the same as the observed sustained speeds of captive scombrids. The model was used (Magnuson, 1973; Dotson, 1977) to predict sustained speed over a greater range of lengths (Fig. 8B,C). The poten-

d

4

lc

,Z+0.89 0.5

1.0

OBSERVED

1.5

2.0

S P E E D (f/sec.l

FORK

L E N G T H (em)

Fig. 8. Predicted speeds of sustained swimming for scombrids. (A) Comparison of predicted and observed speeds; (B) predicted speed (cmhec) related to t;and (C) predicted speed (tkec) related to t.(Adapted from Magnuson, 1973; Dotson, 1977.)


267

tial for lowered metabolic rates from the presence of a gas bladder is apparent both within and among species. Minimum speeds for hydrostatic equilibrium of the three thunnids (yellowfin tuna, bigeye tuna, and albacore) decline at larger sizes owing to development of the gas bladder and pectoral fins. Skipjack tuna, a species without a gas bladder, at lengths of 100 cm has a minimum speed 3.5 times greater than yellowfin tuna and many times greater than bigeye (Magnuson, 1973). The influence and potential energetic savings of large pectoral fins can be seen by comparing, at a length of 50 cm, the minimum speeds of yellowfin tuna with large fins and skipjack tuna with small fins. At this length the gas bladder has not developed, and yellowfin tuna speeds are 70% of the skipjack tuna speeds. The facts that scombrids do not stop swimming (Fig. 2) and that sustained speeds are predictable (Fig. 8A) are a product of the physical system by which they maintain a balance between vertical forces of weight, buoyancy, and hydrodynamic lift. In addition, variations in pectoral fin areas, gas bladder' sizes, and sustained speeds among species exemplify alternate solutions to balancing these vertical forces. Sustained swimming has brought with it other sets of adaptations-ram gill ventilation and perhaps the lunate tail. Ram gill ventilation, characteristic of scombrids, also requires continuous forward movement (Hall, 1930; Brown and Muir, 1970; Roberts, 1975). The structures for pumping water across the gills are poorly developed or even lost in some species. If these fish stop swimming suffocation results. The mechanisms by which scombrids maintain equilibrium among vertical forces, i.e., swimming continuously and producing hydrodynamic lift on the pectorals, and the related adaptations such as ram gill ventilation, significantly alter the relative importance of the various components of drag and thrust in the equilibrium amon'g horizontal forces. These interrelations are considered next.

V. RESISTANCE TO FORWARD MOVEMENT Scrombrids are among the most highly evolved fish in regard to adaptations to reduce drag or the resistance to forward movement. This is not surprising since they have both high sustained speeds and high burst speeds, and drag is proportional to speed squared. Adaptations of the body such as streamlined shape have been noted frequently (Walters, 1962; Marshall, 1965; Hertel, 1966; Alexander, 1967, 1968; Webb, 1975; Aleyev, 1977). Gill resistance and drag produced with hydrodynamic lift on the pectoral fins were considered

268

JOHN J. MAGNUSON

by Brown and Muir (1970) and MacKay (1976) but drag induced from

thrust by the caudal fin has not been evaluated in discussions of total drag. Other adaptations to reduce the energy requirement of swimming, such as variations in locomotory behavior, have been identified as possible in theoretical papers (Weihs, 1973a,b, 1974)but have as yet received little or no confirmation from experiment or observation.

A. Components of Drag Drag results from skin friction between a fish and the boundary layer of water (friction drag), from pressures formed in pushing water aside for the fish to pass (form or pressure drag), and from energy lost in vortices formed by the pectoral fins and the caudal fin as they produce lift or thrust (induced drag). Alexander (1968), Brown and Muir (1970), and Webb (1975) provide more complete explanations of these general sources of drag.

ESTIMATION OF DRAG The various structures producing drag and the components of drag are discussed below for scombrids. Methods of estimating drag are described and the magnitude of the components of drag for major structures are calculated and presented in Table VI for a skipjack tuna swimming at sustained speeds. When these component drag forces are summed they provide an estimate of the thrust required to oppose drag forces. Total drag can also be estimated by estimating total thrust and equating it to total drag as was done by Pyatetskiy (1970b). These estimates will be discussed in the section on thrust. a. Friction and Form Drug. Webb (1975) argued that theoretical calculation of drag and dead-drag measurements on towed fish produced unsatisfactory results with the possible exception of scombridlike fishes with stiff bodies and carangiform locomotion with lunate tail. Measurements which Webb (1975) cited from Bone of dead-drag on towed Atlantic mackerel were similar to theoretical calculations for laminar flow conditions. However, another set of measurements on free falling mackerel by Richardson (1936) produced estimates of drag coefficients that differed from theoretical estimates by three orders of magnitude (Webb, 1975, Fig. 46). Thus, care must be taken in any measurements of dead drag even for scombrids. Frictional drag (Of) is proportional to the density of water ( p J , a

4.

269


measure of surface area (S), speed squared (Uz),and a coefficient of frictional drag (CJ. It can be estimated from

D f = ‘/2Cfp&’U2

(11)

Mechanics of drag are discussed in Webb (1975). The coefficient of friction can be calculated for laminar, turbulent, or transitional flows as follows (Prandtl and Tietjens, 1934):

C

f

Cf laminar = 1.33 RL-l12

( 12)

cfturbulent = 0.074 RL-’’~

( 13)

transitional

= 0.074 R L-lI5

-

1700 R LP1

( 14)

At sustained speeds (Fig. 1A) R , for scombrids may be low enough for flow to be laminar over much or all of the body. At burst speeds (Fig. 1B) or sustained speeds for large bluefin tuna which are often above 1 x lOS, flow would become turbulent at some point along the body. Flows over the fins would be laminar because fins have short chords or lengths and consequently lower Reynolds numbers than the body. As mentioned earlier, drag coefficients measured by Bone (Webb, 1975) and those computed from Eq. (12) are similar (Table V). At R L from 7 x 104 to 1.4 x 105 the values were remarkably close to expectation with laminar flow. If turbulent flow were assumed, the estimates were usually higher than measured values but the fit was best at the highest and lowest RL.Laminar flow was assummed for calculations in Table VI for sustained speeds of skipjack tuna. I n spite of the prob-

Table V Coefficients of Friction Drag Measured from a 35 cm long Atlantic Mackerel by Bone in Webb (1975)Compared with Theoretical Values Computed from Eqs. (12)and (13)

Cf Speed (cm/sec)

RL

10

3.5 x lW

20

7.0 x 1W 1.0 x 1w 1.4x 1W 1.8 x 1w

30 40 50

Measured dead drag

1x 4x 4x 5x 5x

10-2 10-3 10-3 10-3 10-3

Calculated cf

laminar

7x 5x 4x 4x 3x

10-3 10-3 10-3 10-3 10-3

cf

luibulenl

9 x 10-3 8x 7 x 10-3 7~ 10-3 6x

270

JOHN J. MAGNUSON

Table M Total Drag Estimated for a 44 cm Skipjack Tuna Swimming at a Sustained Speed of 66 cmlsec" Type of drag

Part of body Body Second dorsal and anal fins Caudal fin Pectoral fins Gills Total

Friction [dynes

Form [dynes

Induced [dynes

Gills [dynes

Total [dynes

(%)I

(%)I

(%)I

(%)I

(%)I

4,720 (24)

1,180 (6)

0

-

5,900 (30)

500 (2) 1,340 (7) 870 (4)

120 (1) 1,080 (5) 700 (4)

0 2,970 (15) 2,900 (15)

-

-

-

-

7,430 (37)

3,080 (16)

5,870 (30)

3,400 (17) 3,400 (17)

620 (3) 5,390 (27) 4,470 (23) 3,400 (17) 19,780 (100)

-

Modified from Brown and Muir (1970) with recalculated values for gill resistance and fin drag and an inclusion of hydromechanical efficiency of the caudal based on Chopra (1975). Flow was assumed to be laminar over all parts and over the body. See text, Table XI, and the following tabulation (values of variables used in computation and their data source) for the calculations.

U S (cm/sec) (cm') Body* 66 Second dorsal and anal finsf 66 Caudal fin$ 73 Pectoral fins 66

840* 15 41 30 $

C

b

(cm)

(cm)

44 1.3 1.7 1.5f

12 24t

c,

RL

2.9 x 8.6 x 1.2 x 9.9 x

1W 101 104 101

0.0025 0.015 0.012 0.013

* Magnuson and Weininger (1978). f Brown and Muir (1970). $ Magnuson (1973) and Table X (this chapter). lems involved, additional measurements of dead drag and computations of theoretical drag on scombrids would be useful in future analyses of forces acting on a swimming scombrid. The coefficient of drag can be adjusted to include form drag. The thicker the body ( d ) in respect to length (8)the greater the form drag and so the greater the combined drag coefficient (C,) in respect to Cf. C , , the coefficient of frictional and form drag together, can be determined from (Hoerner, 1958, cited in Bainbridge, 1961)

c ,= C J 1 + is(d/e)+ 7(d/e)31

( 15)

Brown and Muir (1970), using test data from Hoemer (1965), judged form drag of the body to equal 25%of the body friction drag for

4.


271

skipjack tuna. They also estimated form drag for all extended fins (pectorals, second dorsal, anal, and caudal fins) as 50% of friction drag from the same sources. Since I am interested in the individual contribution of each fin I did not use the 50% average. Rather I used the figure of 80% suggested for the pectoral fins by Brown and Muir for pectorals and caudal fins. I used 25% for the anal and second dorsal that operate at no angle of attack. I n addition I used more recent values for the wetted areas of the exposed pectoral fins and the span and area of the caudal fin than had been used in Brown and Muir. Speed of the caudal fin was increased slightly (1.1 x U ) over swimming speed to account for its oscillatory path. The above computations do not include resistance to water flow from ram gill ventilation used by scombrids (Brown and Muir, 1970), nor do they account for induced drag from the lift produced on the pectoral fins (Brown and Muir, 1970) or the thrust from the caudal fin.

b. Gill Resistance. Scombrids ventilate their gills by swimming forward with mouth slightly agape. Water passing through the mouth, over the gills, and out the opercular gap produces internal drag and loses momentum. Brown and Muir (1970) estimated that speed of water through the respiratory path declined by about 30% from entrance at the mouth to exit at the opercular gap. As can be observed from Eq. (16), gill resistance (R.) is directly proportional to ventilation volume (VG),swimming speed ( U ) , water density (pe), and approximately to the head loss (AH):

This equation developed by Brown and Muir (1970) appears to provide a good fit to observed data (Stevens, 1972). The problem of accurate estimation is to obtain reasonable values for ventilation volume and head loss from a “difficult” experimental animal. Ventilation volume was estimated by Brown and Muir (1970) from observed rates of oxygen consumption, the fraction of oxygen removed from the water, and the oxygen concentration in water. They used VG of 56 ml/sec or 33 ml/sec . kg for a 44 cm skipjack tuna based on preliminary work. The value is probably low. Stevens (1972) was unable to keep restrained skipjack tuna alive for even 1 hr at similar rates of gill perfusion but had better luck at rates near 50 ml/sec * kg. Reasonable values for head loss seem to be about 2000 dynes/cm2 or about twice the value used by Brown and Muir (1970). Stevens (1972) directly measured head loss on restrained skipjack tuna (AH = 1885 dynes/cm2, n = 6, mass = 1.5-1.7 kg) and a restrained

272

JOHN J. MAGNUSON

kawakawa (AH = 1816 dynes/cm2, mass = 2.3 kg). Roberts (1975) has also determined for small Atlantic mackerel a minimum speed at which ram ventilation is used. This speed by his estimates would produce a head loss of 2100 dynedcm2. The best estimate of gill resistance is 3400 dynes for a 44 cm skipjack tuna. This estimate, about three times the first estimate by Brown and Muir, was obtained from Eq. (16) with pe = 1.025 g/cc, U = 70 cm/sec, AH = 2000 dynes/cm2, and VG= 85 ml/sec.

c. Induced Drag. Hydrodynamic lift from the pectoral fins and thrust from the caudal fin are not produced without some losses from tip vortices and trailing edge vortices (Fig. 9). Prandtl and Tietjens (1934),Alexander (1968),and especially Lighthill ( 1975)provide more complete discussion of the vortices. Not shown in the diagram is the lateral movement of the trailing edge vortices observed in scombrids by McCutcheon (personal communication, cited in Lighthill, 1975). Owing to greater pressure below the fin or on alternative sides of the beating caudal fin, some water flows around the tips of the pectoral fins or the caudal fin and forms a vortex behind the fish (Fig. 9). Also trailing edge vortices on the caudal fin result from the water accelerated backward by the caudal movement (Hertel, 1966; Lighthill, 1969, 1975). This induced rotating motion of water left in the wake adds to the drag. Induced drag (D,)from the pectorals is directly proportional to the required lift squared (L2).It is inversely proportional to the speed of and the span of the fins squared (b:). The magthe fish squared (U2)

@TIP VORTICES @TRAILING EDGE VORTICES

Fig. 9. Diagram of vortices induced at the tips of pectoral fins and at the tips and trailing edge of the caudal fin that are the sources of drag induced by production of lift and thrust. (Adapted from two-dimensional views-Prandtl and Tietjens, 1934, Fig. 154; Lighthill, 1975, Fig. 8.)

4. LOCOMOTION BY SCOMBRID

FISHES

273

nitude of induced drag can be estimated from an equation taken from Prandtl and Tietjens (1934):

D,=-

2LZ

mU2bP2

where E = an efficiency factor of approximately 0.85. Brown and Muir (1970) estimated induced drag from the lift on the pectorals at 2800 dynes for a 44 cm skipjack tuna with a fin span of 24 cm. Induced drag is slightly higher, 2900 dynes in my calculations because required lift I used was greater. Lift (100,000 dynes) was calculated from Eq. (8) from data in Magnuson (1973, Table V) for a fish with a stomach content equal to 5% of body weight. Preliminary estimates of drag resulting from thrust from the caudal fin can be obtained by methods developed by Wu (1961) and Lighthill (1969, 1975) and reiterated in Webb (1975). A hydromechanical efficiency factor (qp) for thrust production estimates the proportion of power exerted by the caudal fin that goes into producing thrust. One minus the efficiency factor ( 1 - qp)is used here as an estimate of losses owing to induced drag. The magnitude of the efficiency factor depends on the posture, form, and rate of movement of the caudal fin. Parameters for estimating efficiency factors were developed by Webb (1975, p. 98) and will be discussed in more detail under thrust production. The values for efficiency from Table 17 in Webb (1975) for kawakawa swimming 3-4.7 t/sec varied from 0.77 to 0.86 to give losses (1- qp)of 0.14-0.23. For present purposes I use 0.15 as the proportion of total thrust power lost to induced drag based on a reanalysis of data on kawakawa presented in the section on thrust. Total drag can be calculated, as can drag induced from thrust (0.15 x total drag) by summing all drag other than that induced by the caudal fin, and then solving for total drag b y Total drag = (0.15 total drag) drag from all sources other than induced drag from the cuadal fin (18)

+

Drag from all other sources than induced by the caudal fin was summed from Table VI.

d . Total Drag. The estimate of total drag on the 44 cm skipjack tuna swimming at sustained speed of 66 cm/sec was 19,780 dynes (Table VI). This includes frictional and form drag on the body and extended fins, induced drag on the pectoral fins and caudal fin, and gill resistance. Usually these components cannot be isolated and total drag regardless of source is sometimes related with a single drag coefficient

274

JOHN J. MAGNUSON

to the body surface area and speed (see, e.g., Pyatetskiy, 1970b; Sharp and Francis, 1976). For this skipjack the coefficient of total drag is 0.010 from 19,780/(0.5 x 1.025 x 840 x 66) in analogy with Eq. (11) for frictional drag. Total drag and coefficients of total drag were also estimated in the section on thrust for kawakawa swimming at faster speeds. Estimates were from summing components of drag and from calculations of total thrust which should equal total drag (Table XI). For R L of 5.0 X 1 8 1.3 x 108 total drag coefficients of kawakawa average 0.012 (range, 0.009-0.016) from the component of drag analysis and 0.027 (range, 0.011-0.044) from thrust analysis. The values from the two methods of estimation are within a factor of 2 of each other and are two and four times larger than the frictional drag coefficient for turbulent flow from Eq. (13). The coefficients for total drag appear to reach a maximum near R , of 7 x lo5(Table XI, column 27). Pyatetskiy (1970b) estimated coefficients of total drag based on calculations of thrust for 16 cm Atlantic bonito. At speeds between R L of 1 and 2 x 105 these values were near 0.010, but at speeds just below 1 x lo5 values near 0.04 were calculated. The best estimate of the coefficient of total drag for a swimming scombrid, genera Euthynnus and Sarda, is 0.01-0.03.

B. Distribution of Drag among Components 1.

SUSTAINED-SWIMMING

SKIPJACKTUNA

For skipjack tuna swimming at sustained speeds, the calculated magnitudes of drag components are given in Table VI. The first dorsal fin and pelvic fins were not included in the calculation because they are appressed at sustained speeds. Calculations were described above and values were taken or recomputed from Brown and Muir (1970) and Webb (1975). Values will certainly change as methods and data are refined. Similar values were obtained b y MacKay (1976) with slightly different components for Atlantic mackerel. Frictional drag and form drag on the body and fins constitute 53% of total drag b y my calculations. The remainder comes from induced drag from lift and thrust (30%)and from gill resistance (17%).Viewed in another way only 30% of the drag comes from the body while 53% comes from the various fins and again 17% &om the gill resistance. Drag resulting from the use of the pectorals to maintain hydrostatic equilibrium is 23% of total drag and somewhat greater than the 17% going to gill resistance. Together, these two functional aspects of continuous swimming account for 40% of the drag. Fish not required to

4.


275

meet these functions by swimming would be expected to have lower drag at the same speeds. The importance of adaptations to reduce drag from the production of thrust and lift become especially apparent when their magnitude is compared with the drag on the streamlined body. A total of 50% of total drag comes from the caudal and pectoral fins but only 30%comes from the body at sustained speeds. The most surprising conclusions from an analysis of the components of drag on a skipjack tuna at sustained speeds (Table VI) are (1) most resistance to forward movement comes from the fins, not from the body, and (2) the two functions of continuous swimming, hydrostatic equilibrium and gill ventilation, increase resistance to forward movement b y a factor of 1.7.

2.

CHANGES IN

DISTRIBUTION OF DRAG

The distribution of drag among sources (Table VI) will be expected to vary with speed of swimming, and among species and sizes of scombrids. a . Changes with Speed. Gill resistance will decrease with increasing speed because at burst speeds a scombrid closes its mouth. Closing the mouth would reduce drag b y about 17%, a considerable saving. Even at sustained speeds Pacific bonito (Sarda chiliensis) in the oceanarium at Marineland of the Pacific closed their mouth up to 42% of the time (Magnuson and Prescott, 1966) and may have thereby obtained a 7% reduction in drag (0.17 x 0.42 = 0.07). Drag produced by the pectoral fins will decrease to zero with increasing speed because at faster speeds they appress their pectorals for increasing proportions of time. For example, captive kawakawa, that had just eaten, extended the pectorals 100% of the time while swimming at 1.6 tlsec but 0% of the time at 2.8 Msec and faster (Magnuson, 1970). At burst speed, drag on pectorals would b e zero. Also, the ratio between form and frictional drag on the body should decrease at faster speeds because at Reynolds numbers near 106 the change of flow from laminar to turbulent should decrease the form drag (Alexander, 1968). Thus, at burst speeds, relative savings in drag would be expected from absence of gill resistance and absence of drag on the pectorals and from reduction in form drag on the body. However, even though gill resistance and the pectorals contribute 30%of the drag of a slowly swimming scombrid (Table VI), saving at high speeds would be small because gill resistance and induced drag on the pectorals would re-

276

JOHN J. MAGNUSON

main relatiGely constant with increase in speed. Drag on a burst swimming scombrid, while not calculated here, would be dominated by friction on the body and induced drag from the caudal fin (see Table XI).

b. Changes with Species and Size. Most forms of drag are proportional to speed squared so drag would be lower for species with slower sustained speeds. Species with larger gas bladders and larger pectoral fins have slower sustained speeds (Magnuson, 1973) and should have less drag as a consequence. Differences in distribution of drag among components in different species also will result from differences in morphometry, especially morphometry associated with the determination of the minimum speed necessary for hydrostatic equilibrium. Induced drag on the pectorals is directly proportional to weight squared [Eq. (17)] and induced drag on those species that were lighter would tend toward zero and could reduce total drag by up to about 15%. In addition induced drag on the pectorals is inversely proportional to the span squared, and species with long fins such as yellowfin tuna should have less drag from the pectorals for that reason alone. However, induced drag is also inversely proportional to speed squared and the slower sustained speed of species with long fins would cancel some of the savings. Species with larger fins should also have more frictional and form drag on their fins than those with smaller fins. Frictional drag is directly proportional to surface area and pectoral areas differ markedly among species. For example, areas of pectoral fins are four times greater for bigeye tuna than for wahoo (Magnuson, 1973), and two times greater for small albacore than for skipjack tuna (Dotson, 1977). Similar differences would occur among sizes of the same species because growth of gas bladders and pectoral fins are allometric (Magnuson, 1973; Dotson, 1977). For example, yellowfin 50 cm long have no gas bladder and have faster sustained speeds than larger yellowfin that do have a gas bladder. Consequently small yellowfin should have a greater proportion of drag as induced drag than would larger yellowfin. Species with more optimum body shapes would have reduced form drag on the body. Many scombrids, Scomber, Sarda, Euthynnus, Thunnus, and Auxis, have shapes near optimum for sustained swimming, but others such as Acanthocybium have bodies more slender than optimum (Magnuson, 1973). In summary, species and sizes with more optimum body shapes would have reduced form drag on the body, those with adaptations for slower sustained speeds would have less induced drag from the pec-

4.


277

toral fins, and those with relatively smaller fins in general would have less frictional and form drag associated with the fins. Since all of these factors are interactive, the net effect of all differences would have to be considered in concert with one another.

C. Adaptations for Drag Reduction Energetic consequences of adaptations that reduce drag are selfevident. Among scombrids with their continuous swimming and their continuous production of thrust with the caudal fin, lift with the pectorals, and drag from ram gill ventilation, adaptations for drag reduction have developed to perhaps a greater extent than in any other group.

1.

SHAPE AND STRUCTURE

Most scombrids have nearly ideal longitudinal streamlining of body shape (Fig. 10) in terms of thickness ratio measured here by maximum thickness as a percentage of length. Larger estimates for thickness are obtained if only maximum height is used rather than when maximum width and height are averaged, but the latter seems more representative of shape and is used here. For bodies of the same volume, drag is minimum when the body thickness is about 22% of length and is increased by less than 10% when between 14 and 33% (Alexander, 1968; von Mises, 1945; Webb, 1975; Hertel, 1966). Three genera, Thunnus, Euthynnus, and Auxis (Table VII), have body thicknesses between 21 and 23% of length or have almost exactly the optimum shape. Sarda and Scomber are somewhat more slender with a thickness of 1618%.Acanthocybium with a thickness of 12%is the only species for which data are published that is too slender to have minimum drag per unit volume. Scomberomous has a shape similar to

Acanthocybium. A second feature of body shape, the position of maximum thickness along the length, is an index to the proportion of the body over which laminar flow can be expected at high speeds. A laminar profile has the thickest portion farther from the snout and tends to maintain laminar flow over a greater length of the body. Scombrids have laminar flow profiles with the position of maximum thickness 4&50% (Table VII) of the distance from the snout to the tail. A 70% figure given by Webb (1975) originates from a single photograph from a semidorsal view of an unidentified miniature tuna hanging from a hook (Fig. 166 in Hertel, 1966). I think this value is an overestimate. Values in Table VII,

278

JOHN J. MAGNUSON

1 1

30

B

0

20

40

I

I

60

80

0 100

P e r c e n t o f B o d y L e n g t h , E x c l u d i n g the Keel

Fig. 10. Body shape of kawakawa 32 cm fork length showing,(A)cross section shape and (B) longitudinal disbibution of average height calculated by dividing cross section area by maximum width. (From Magnuson, 1970, Hydrostatic equilibrium ofEuthynnus nfinis, a pelagic teleost without a gas bladder, Copein pp. 56-85.)

usually about 41%, are probably underestimates because the length used included the length of peduncle (Aleev, 1963) and the caudal fin (Magnuson, 1973). Exclusion of the caudal fin gives numbers near 46% and an estimate for kawakawa with length terminated just anterior to the keel is about 50% (Fig. 10). Cross sections of the body of a scombrid are a series of vertical ellipsoids along most of the length (Fig. 10). Anteriorly the body is wider above the midline. Just anterior to the peduncle it becomes first circular and, at the peduncle, well-developed lateral keels form a horizontal ellipse which in some species has sharp extended edges. Horizontal keels at the peduncle probably reduce turbulence from the rapid lateral movements that occur here as the tail beats back and forth (Walters, 1962; Aleev, 1963; Webb, 1975). Finlets along the dorsal and ventral midline direct flow across the peduncle (Magnuson, 1970; Webb, 1975).The vertically thin, horizontally reinforced peduncle, with finlets to direct flow, appears to be an adaptation that reduces form drag during lateral movements and still provides a strong, me-

4. LOCOMOTION

279

BY SCOMBFUD FISHES

Table VII Longitudinal Streamlining of the Bodies of Scombrids Distance from snout to position

Maximum maximum body thickness height (% 0 (% 0

of

Species"

Thunnus Bigeye tuna Yellowfin tuna Albacore Median Euthynnus Kawakawa Skipjack tuna Median Aunis Bullet mackerel Frigate mackerel Median Sarda Pacific bonito Atlantic bonito Median Scomber Atlantic mackerel Acanthocybiurn Wahoo

tb (cm)

Maximum body thickness, (height + width)/2 (% 0

Source

4660 28-45 68

37 41 46 41

28.6 27.8 26.6 28

23.5 22.3 23 (4.3)c

Magnuson (1973) Magnuson (1973) Aleev (1963)

37-43 37-57

40 42 41

27.2 25.9 27

22.6 21.0 22 (4.6)e

Magnuson (1973) Magnuson (1973)

32-37 39

40 46 43

24.3 23.0 24

20.8 21 (4.8)"

Magnuson (1973) Aleev (1963)

45-65 14-45

40 34-49 41

21.8 21.0 21

18.4 18 (5.6)?

Magnuson (1973) Aleev (1963)

12-25

4G50

19

16d(6.2)'

Aleev (1963)

123-130

37

15

12 (8.4)?

Magnuson (1973)

Species listed by genera in order of decreasing thickness. Aleev (1963) used length of skeleton. Fineness ratio ( t h a x i m u m thickness) is given in parentheses for each genera. Estimated by reducing maximum height by 3% to give maximum thickness.

chanically advantageous link (Fierstine and Walters, 1968) between the body musculature and the caudal fin. Internally the tendons to the fin pass over the bony lateral extensions which serve as a pulleylike bearing surfice. Other functions of the keel were discussed above under hydrostatic considerations. The body is smooth. Scales are usually absent except in a small corselet immediately behind the opercular opening. The eyes, nares, jaw, and opercular bones provide extremely smooth exterior surfaces. Pelvic fins and first dorsal fin are used only in maneuvers (Magnuson, 1970).During sustained swimming they are appressed into grooves or

280

JOHN J. MAGNUSON

depressions in the skin surface which are perfectly shaped to receive the appressed fins and retain a smooth body surface. At burst speeds the pectorals are also appressed into grooves on the side. Walters (1962) speculated that the corselet of scales and the thick skin just behind the opercular gap might act as a tripping wire to reduce form drag, but Webb’s (1975) idea that it provides the fairing for the appressed pectoral fins seems more likely. Areas between the fin rays on the caudal fin, pectoral fins, and the anal and second dorsal fins are filled with tissue and provide a smooth surface to the water. Fish slime when mixed with water can reduce friction of water in turbulent flow through a tube (Rosen and Cornford, 1971). But slimes of scombrids were the least effective of eight species tested and were considered exceptions. Slime from Pacific mackerel (Scomber japonicus) was not effective until the solutions were 50% slime. For Pacific bonito even 100% slime did little to reduce friction over ordinary seawater. Slimes as suggested by Breder (1926) might streamline the body by reducing surface irregularities, but the slippery nature of slime itself is probably unimportant, at least to scombrids. Breder (1976) argues that slimes are more effective in solitary than in schooling fishes like scombrids. Various methods of damping disturbances in the flow with unique structures of the skin have been proposed (Walters, 1962) to help maintain laminar flow. Webb (1975),in a review of evidence, doubts if they occur in scombrids and Aleyev (1977) presents interesting information that indicates no drag reduction even when they do occur in mammals, Walters (1962) suggested that a scombrid body with ram ventilation acted like a leading edge slat with water entering the mouth and being injected to the boundary layer behind the opercular gap with favorable effects. The injection of high energy water from the gills would delay boundary layer separation and decrease surface drag. Whether this applies is not clear. Brown and Muir (1970)calculate that water coming from the gills would be lower in energy and it thus might not have the desired effect. Rather it appears that gill effluent causes turbulence (Webb, 1975). Further discussion can be found in Walters (1966) and Breder (1965). The shapes of the pectoral fins (Magnuson, 1970) and caudal fins (Fierstine and Walters, 1968) are characterized by high aspect ratios. The aspect ratio (AR) is the ratio between span and mean chord. Induced drag is less per unit of lift or thrust for fins with higher aspect ratios. As indicated by Eq. (17) induced drag is inversely proportional to span squared. For pectoral fins of kawakawa AR of the exposed area

4.


281

ranged from 6 to 7 (Magnuson, 1970). If the span across the body is included, AR is greater than 10. Kawakawa have relatively short fins for a scombrid, and species with long pectorals such as the thunnids have AR well over 10 by either method of computation. For the caudal fin Fierstine and Walters (1968)measured AR that ranged from 5.2 to 7.7 from nine scombrid species. These will be compared in more detail with more recent estimates in the section on thrust production. But with the exception of fast swimming istiophorids such as sailfish and marlin they are the highest known among bony fishes. Pectoral fins are high (>lo) and the caudal fin median (5-7) AR devices when compared with flying animals and airplanes. AR for planes ranges from 2 to 15 (Perkins and Hage, 1949) and from 3 to 12 for birds (Hartman, 1961; Storer, 1948; Greenwalt, 1975). The greater AR of pectorals may explain in part the observed higher lift : drag ratio of the pectorals compared to the caudal fin. For example, lift : drag and thrust :drag ratios of a 44 cm skipjack tuna can be calculated and are 22 : 1 (100,000: 4470) for pectoral fins and 4 : 1 (22,870: 5390) for the caudal fin. The 22 : 1 lift :drag ratio for the pectoral fins is somewhat above the maximum of 17 : 1 for a thin cambered airfoil (see von Mises, 1945, Fig. 109). The lift coefficient for such an airfoil operating at a maximum lift : drag ratio would be about 0.9 (von Mises, 1945, Fig. 109) and is in the range of estimates for swimming kawakawa (Table IV). The estimates of thrust : drag ratio for the caudal fin was not nearly as high as for the pectorals. While it provides no further explanation for the difference, it is interesting that the vertical forces in sustained swimming are much greater than horizontal forces. Total drag force on the 44 cm skipjack swimming at 66 c d s e c are about 20,000 dynes or one-fifth of the total lift force of 100,000 dynes required by the fish to maintain hydrostatic equilibrium. In summary, two general adaptations characterize the shape and structure of scombrids in regard to drag reduction. These are (1) smooth streamlining of the body and fins, and (2)high aspect ratios for fins that produce lift or thrust.

2. PHYSIOLOGICAL ADAPTATIONS Any increase in efficiency of oxygen uptake could contribute to drag reduction. Gill resistance in Eq. (16) was directly proportional to respiratory volume, Given a particular metabolic rate, the less water that was required to ventilate the gills, the lower the drag from ram gill ventilation. Scombrids have highly specialized gills with surface areas similar to small mammals of equal mass and almost an order of mag-

282

JOHN J. MAGNUSON

nitude greater than most other fishes (Muir and Kendall, 1968; Muir, 1969; Muir and Hughes, 1969; Muir and Brown, 1971). Oxygen removal from ventilated water (Stevens, 1972) averaged 71%for six skipjack tuna and 79%for one kawakawa. Averages for individual skipjack tuna ranged from 47 to 94%.These uptake efficiencies are adaptations of scombrids and are much higher than for other fishes. If they were half as efficient, had twice the ventilation volume, gill resistance would double its present level. Webb (1975) discounted the hypotheses by Walters (1962) that tuna could warm their boundary layer sufficiently to decrease viscosity.

3. BEHAVIORALADAPTATIONS Several exciting ideas have been developed that if true would be significant adaptations to reduce the energy required of scombrids to swim through the water. These are that properly spaced schooling fish cancel the vortices in each other’s wakes (Breder, 1965,1976; Belyayev and Zuyev, 1969; Weihs, 1973;, 1975) and that alternating swimming and gLJing reduces energy expenditures for a given distance covered (Weihs, 1973b, 1974). a. Schooling. Scombrids with rare exceptions are schooling fishes (Magnuson, 1963) of the obligatory type as defined by Breder (1967). Polarized, parallel orientation is maintained except during feeding and courtship (Magnuson and Prescott, 1966) by these continuous swimmers with an attraction for each other. Schools are composed of animals of the same species and approximate length (see references in Magnuson, 1963). Even in so-called mixed schools of yellowfin and skipjack tuna, parallel orientation is among those of the same species (Yuen, 1962). In such a formation the caudal fin of each fish sheds two rows of trailing edge vortices spinning in opposite directions in the wake (Fig. 11). These vortices degenerate and fade as the fish pulls away. Weihs (1973a) points out that one fish swimming directly and closely behind another would have to swim at a faster relative speed to counter the backward directed flow in the wake of the first fish (Fig. 11). This tandem position is avoided by the nearest neighbor as demonstrated in an aerial photograph of about 100 bluefin tuna (Thunnus thynnus) in which only four appear to be in tandem (Breder, 1965). Rather their spacing was more in a diamond or diagonal pattern more typical of schooling fishes (Breder, 1976). In the diamond pattern (Weihs, 1973a, 1975) the second row of fish in a school swims diagonally behind and midway between fish in the

4.

283


ROW 1

ROW 2

-ROW 3

Fig. 11. Diagram of scombrid school showing possible interaction between trailing edge vortices and swimming efficiency (modified from Weihs, 1973a, 1975). Distances and angles between fish based on Atlantic mackerel (van Olst and Hunter, 1970). See text for rationale. Not diagrammed is Weihs' (1975) suggestion that fish abeam from each other beat in opposition.

first row and obtains a swimming advantage because these fish are traveling in the direction of vortex rotation induced by the first row of fish (Fig. 11). In analyses of overhead photographs of small schools of captive kawakawa, few of the nearest neighbors swam in the abeam position (Cahn, 1972). The direction to the nearest neighbor in small schools of captive Pacific mackerel averaged 14" from the heading of the following fish (van Olst and Hunter, 1970). A fish in the optimum position (Weihs, 1975) behind the first row of fish could have its relative speed reduced by 50-60%. Since drag is proportional to speed squared, the possible savings in energy is even greater. Weihs (1973a) goes on to show that fish swimming in third or later rows in a school would be swimming through water in which the vortices from fish in the front two rows tend to cancel each other (Fig. 11) if the lateral distance to the abeam fish is twice the width of the vortex trail. By his calculations the energy savings of an entire school would be one-half the savings of the second row discussed above. Tip vortices from the pectoral fins may also produce a favorable

284

JOHN J. MAGNUSON

result in schools, Weihs (1975) points out that in the diamond pattern the tip vortices from the pectoral fins produce upwash from which following fish may receive some lift or reduced induced drag on their pectorals. In birds, a 71% reduction in induced drag is suggested (Lissaman and Schollenberger, 1970). Weihs ( 1973a, 1975) discussed still another hydromechanic advantage of schooling. Fish directly abeam and above or below may act as streamlined walls and as such should also positively influence thrust without any change in energy expenditure or caudal movements. This effect is greatest when fish are close together and is essentially absent at lateral distances of 1 e. Increases in thrust could be 10% or more. Estimates of the lateral distance between the longitudinal axis of nearest neighbors range from 0.4 to 0.6 C for adult scombrids in schools (bluefin tuna, Breder, 1965; Pacific mackerel, van Olst and Hunter, 1970; kawakawa, Cahn, 1972). Greater distances of 2.4 e were observed for subadult Pacific mackerel, 5 cm long, (van Olst and Hunter, 1970) and 0.6-22 e for bluefin tuna (Anonymous, 1975). When kawakawa were separated by transparent Plexiglas partitions they tended to swim directly abeam of the nearest neighbor at a lateral distance of 1.3-2.9 e and Cahn (1972) concluded that hydrodynamic clues were necessary for normal spacing. The above observations suggest that scombrids often space themselves appropriately in a school to take advantage of the savings described by Weihs. Data to substantiate the energetic advantages of swimming in a school do not exist for scombrids but Zuyev and Belyayev (1970) observed for the similarly shaped horse mackerel, (Truchurus mediterruneus), that fish of the same length that were farther back in the school swam at the same speed as lead fish, but with a slower rate of tailbeat. Tailbeat rate of the second, third, and fourth fish in the group averaged 88, 85, and 83%, respectively, of the tailbeat rate of the lead fish. These results suggest a possible savings of ca. 10-20% from schooling.

b. Gliding. Gliding downward with no swimming movements and then swimming to regain altitude should result in significant energy savings by negatively buoyant fish according to a theoretical analysis by Weihs (1973b). Using kawakawa about 42 cm long as an example, he estimated savings of 20% to travel the same horizontal distance in 7% more time. This comes out to about a 25% savings in energy expended per unit time. The pattern of swimming proposed by Weihs (1973b) is diagrammed in Fig. 12. The fish glides down from A to B at an angle of descent, a,and then actively swims to the surface at angle p to point C.

4. LOCOMOTION

285

BY SCOMBRID FISHES

WATER SURFACE

c B

Fig. 12. Diagram of path of a negatively buoyant scombrid alternating gliding and active swimming-a behavior that could decrease energy used per unit time (modified from Weihs, 1973b). Terms and rationale in text [see Eqs. (18)-(23)l.

Horizontal distances traveled are a , for descent and u2 for active swimming to regain altitude. The maximum and minimum depth of swimming are separated by distance h. Angles, distances, and energy savings (Table VIII) can be estimated from the following equations derived by Weihs (1973b) for the path with maximum energy savings per horizontal distance traveled:

D L

a = arc sin -

(18)

1 -a p = arc cos k,

( 19)

Table VIII Optimum Swimming Behavior and Expected Energy Savings of a Negatively Buoyant Euthynnid and Thunnid Obtained by Alternating Gliding and Active Swimming as Described in Fig. 12 and TexP Equations (18)-(23)

State variables

e Species Skipjack Albacore

L

(cm) (dynes) 45 45

D

h

(dynes) k I b I(m)

100,OW 20,OoOe 100,OOod 5,OW

1.2 100 1.2 100

a

p

a,

u2

(m)

(m)

12" 21" 470 260 0.3" 33.2" 20,000 150

Energy savings (proportion)

0.07 0.16

T

1.04 1.00

" Model from Weihs (197313). k, based on hydromechanical efficiency of qp = 0.15 from Table XI. Approximate values for fish in Table VI. Approximate values based on manuscript by Dotson (1977) that estimated minimum speed of 45 cm albacore as about 0.5 that of skipjack tuna. I assumed a drag reduction to 0.25 of drag from skipjack tuna since most drag values are proportionak speed squared.

286

JOHN J. MAGNUSON

where D, drag during gliding; L , excess weight; kl, ratio between swimming and gliding drag or about 1.2 for a scombrid (estimated from Table VI).

a , = h cot a

( 20)

p

(21)

tan a

(22) (1+Ga) sin a

a2 = h cot Energy saving = 1 -

sin

p + (tan a)(cos p)

or the proportion of energy saved compared with level swimming. 7=

+

sin a sin /3 sin(a + p)

(23)

where r , ratio of time to travel a given horizontal distance by sinking and rising versus level swimming. The euthynnid with no gas bladder and with small pectoral fins would sink rapidly in a glide (ca. 14 cm/sec) and rise steeply to obtain maximum advantage (Table VIII). The thunnid, here an albacore with gas bladder not yet developed but with large pectoral fins, sinks slowly (0.2 cm/sec) and rises steeply. Possible energy savings are 16% by the albacore compared with 7% for the skipjack tuna (Table VIII). Weihs (1973b) points out that greater savings are to be expected for fish that are capable of smaller glide angles. Also the'greater the ratio (k,)between drag during swimming and gliding, the greater the possible savings. Variations in angle of ascent (p) on the other hand have little influence over calculated energy savings. Scombrids with large well-developed gas bladders could have a problem with this mode of swimming near the surface because the rapid ascent can cause over expansion of the gas bladder. But the mode of swimming is quite reasonable over shorter vertical distances at water depths near 100 m or so (at the thermocline in the Central Pacific) where vertical displacement has less influence on gas volume than it does near the surface (Boyle's law). A number of scombrids are believed to live in the region of the thermocline (see Chapter 5 ) and conceivably they could swim and glide to their advantage in a path between lower and upper avoidance temperatures. Weihs (1973b) notes that observational data are not available to verify whether scombrids use this mode of swimming. Strasburg (1961)recorded that skipjack tuna schools in the Central Pacific often disappear from the surface and reappear every 3-38 min. A skipjack tuna carrying an acoustic transmitter in the Central Pacific was deeper than 4 m 39% of the day and 3% of the night hours (Yuen, 1970).

4.


287

Skipjack tuna then do change depth, but the pattern of this movement is not known with enough precision to test Weihs’ idea. However, the ideas raised by Weihs (1973b) are attractive and seem plausible for scombrid fishes. Weihs’ (1973b) ideas also raise the possibility that scombrids can soar in vertically moving water like birds do in rising air (Cone, 1962; Lighthill, 1974) by gliding. The possible sites for soaring are two, (1) in the surface waves, and (2) in internal waves at the thermocline. In surface waves vertical velocities of water particles (Sverdrup e t al., 1942) are greater than the rates of sinking expected for gliding scombrids. The skipjack tuna and albacore in Table VIII should sink at 14 and 0.2 cm/sec, respectively. Vertical velocities in surface waves are of this magnitude as deep as 2-20 m below the surface for a wave as low as 1 m high. The major problem with soaring in a surface wave is that its horizontal velocity (624 cm/sec for a 1 m high wave) is so fast that a gliding scombrid probably would be left behind. However, the prolonged speeds recorded for some scombrids at sea are as high as 400 cm/sec (Commercial Fisheries Review, 1969). The possibility that scombrids can glide this fast should be considered especially if an occasional burst of tailbeats is used to keep up with the progress of a surface wave. Internal waves are out of consideration for euthynnids because they sink too fast, but are more promising for thunnids that sink slowly while gliding. Vertical velocities of internal waves near the thermocline in Sverdrup et al. (1942, Fig. 155) are as fast as 0.5 cm/sec and forward progress of such waves are apparently in the order of 60-200 cm/sec. The thermocline may be an especially suitable location for large thunnids to meet needs of gill ventilation, migration, and food search with little muscular effort. If this were true negative buoyancy (necessary for gliding) would be energetically advantageous compared to neutral buoyancy. Another possible technique of burst swimming and gliding may result in energy savings even for neutrally buoyant fish (Shebalov, 1969; Weihs, 1974). It is again based on the ratio between the drag on gliding and swimming fish and, according to Fig. 2 in Weihs (1974), could save as much as 20%for a fish such as a scombrid. Savings nea; 50% are projected for fishes that produce more drag during active swimming than scombrids do. The slower the average speed and the smaller the variation between burst and gliding speeds, the greater the expected savings. Speeds of 1-2 lengths per second were in the range to provide significant savings in calculations on nonscombrids. In my experience, a captive scombrid does tend to beat its tail regularly for a few seconds and then miss a few beats during steady swimming at a

288

JOHN J. MAGNUSON

constant depth, I do not know whether such behavior qualifies for the savings described above. Sustained speeds of scombrids also fall within the general magto provide the nitude of optimum speeds proposed by Weihs (1973~) greatest distance traveled per unit of energy expended.

D. Summary Scombrids are rich with adaptations to reduce drag or to move efficiently through the water with minimum energetic costs. All external structures are streamlined. Pectorals and caudal fins have high aspect ratios with a resulting reduction in drag induced from lift and thrust production. Gill resistance is reduced by a remarkably efficient uptake of oxygen from ventilated water. Behaviors such as schooling, gliding, and possibly even soaring, promise great savings based on theoretical analyses. Drag forces have apparently exerted intense selection during scombrid evolution. Yet, drag resulting from continuous swimming, induced from lift production on the pectorals and resulting from the gills by ram ventilation, imposes on scombrids sources of and a persistence of drag generation not faced by many other groups of fishes. This drag is large and must be balanced by a continuous production of large amounts of thrust, to be discussed next.

VI. THRUST PRODUCTION Scombrids have the extreme form of carangiform locomotion, name-

ly, carangiform with lunate tail (Lighthill, 1969, 1970, 1975; Wu, 1971; Webb, 1975; Aleyev, 1977) (see Chapter 1). The name comes from the carangid fishes that swim with movements confined to the posterior half of the body (Breder, 1926), and from the high aspect ratio caudal fin which has the appearance of a quarter moon. Lighthill (1975) sees three stages in the evolution of the lunate tail and Aleyev (1977) compares the differences among fishes. First is the development of the highly forked tail of many fishes such as the herrings (Clupeidae). No thrust should be lost by the loss of surface area between the lobes because the vortex-sheet in the gap functions as part of the fin, but drag should be reduced by the reduction of surface area. Second is a decrease in sweepback such as found in many carangids. This results in increased span without increased area, and increases thrust with less drag. Third is the development of the high aspect ratio caudal fin with the lunate form which Lighthill believes to be the

4.


289

culmination of adaptations for speed and efficiency of aquatic swimmers. The adaptation is shared by some marine mammals, the fast swimming lamnid sharks, and with the extinct reptile Ichthyosaurus. Thrust is generated in the same general way as in carangiform swimming but is concentrated, not in the posterior half or third of length, but in the enlarged caudal fin that only occupies the posterior 10% of the length of scombrids. Amputation of the caudal fin rays from two yellowfin tuna reduced the pull that each exerted on a hand-line by about 90% (Fierstine and Walters, 1968). The little pull that remained was believed to come from the bases of the rays and the hypural supports that had not been amputated.

A. Anatomy

The shapes of the body and peduncle minimize the disturbance to the water encountering the caudal fin (Lighthill, 1969).The vertically narrow peduncle, referred to as narrow necking b y Lighthill, imparts minimum motion to the water immediately anterior to the caudal fin and the streamlined body should induce little turbulence. Flow around scombrids has not been studied but pictures of flow around the Pacific white-sided dolphin (Lagenorhynchus obliquidens) (Rosen, 1961) show surprisingly little disturbance, and photographs oi flow around a 14 cm long horse mackerel (Trachurus mediterraneus) indicate that turbulence formed behind the fish would affect primarily the middle of the caudal fin in the middle of a sweep (Aleyev and Ovcharov, 1973). I n the dolphin photo the cross-flow appears to be smooth across the flattened keel rather than turbulent as would be expected from flow across a less streamlined structure. The keeled peduncle of scombrids should perform as well in horizontal movement as that of a dolphin in vertical movement. Breder (1926) observed that the body of Atlantic mackerel had little lateral movement compared to the tail. Measurements by Fierstine and Walters (1968) on kawakawa indicate that the anterior half of the body moves laterally 0.02-0.03 +?or only about 10% of the caudal fin’s lateral excursions. Minimizing these lateral movements of the body not only reduces the disturbance caused by the body in swimming movements but also maximizes the lateral movement of the caudal fin for a given muscular contraction. The lateral movement of the body or recoil that results from the lateral forces exerted by the caudal fin is reduced by longitudinal distribution of body mass and the body profile (Lighthill, 1969). The mass of the fish is concentrated well forward and the body is a series of

290

JOHN J. MAGNUSON

vertical ellipses (Fig. 10). They are not round in cross section. For seven scombrids maximum height was 1.49 (range 1.40-1.65) times maximum width (Magnuson, 1973). A greater ratio of height to width increases the virtual mass of water that would be displaced by lateral movement of bodies with equal volume. The second dorsal fin and anal fin maintain and accentuate the larger vertical dimensions posteriorly to a point about two-thirds the distance from the snout to the fork of the caudal fin. This position is only a short distance anterior to the location of maximum bending of the body in swimming movements. We built a small mechanical skipjack at the National Marine Fisheries Laboratory in Honolulu that swam with oscillating caudal movements. Removal of the artificial second dorsal fin and anal fin increased lateral movement of the body and decreased even more its feeble swimming. The importance of the median fins in this regard can be easily visualized in Gray’s mechanical spring model (Gray, 1968, Fig. 2.11) which shows that a strong lateral force develops at the position of the anal and second dorsal fins during a sweep of the tail. The caudal fin itself is a tapered hydrofoil with high aspect ratio, curved leading edge and moderate sweepback (Fig. 13D). In cross section the fin is shaped like a thin symmetrical airfoil with a rounded anterior or leading edge and a sharp posterior or trailing edge (Chopra, 1975). The rounded leading edge is essential to leading-edge suction that results from the low pressures that occur here as water flows more rapidly around the thickened section. The taper of the fin in combination with moderate sweepback (Fig. 13D) concentrates the surface area near the three-quarter chord location. The front of the fin is pulled from left to right by the lateral movements of the peduncle. Since the area of the fin is to the rear, the fin changes its angle of attack around a yawing axis that is near the rear. An axis near the three-quarter or full chord location would be optimum for efficient thrust production based on theoretical work by Lighthill (1970, 1975), Wu (1971), Chopra (1975), and Chopra and Kambe (1977). The Atlantic mackerel (Aleev, 1963) and other scombrids have two deflector keels near the base of the caudal fin that may help direct flow smoothly along the chord. Aspect ratios of caudal fins range from about 4.5 to 7,O among adult scombrids (Table IX). Skipjack tuna have the highest, 7.2, and Japanese mackerel have the lowest, 4.6. Genera with the highest AR are Euthynnus, Auxis, and some Thunnus, and with the lowest are Scomber, Acanthocybium, Sarda, Scomberomous, Allothunnus, and

4. LOCOMOTION BY SCOMBEUD FISHES

291

PATH

OF

C

FISH

L L . I I I

w-? CAUDAL FIN PATHOF

D

Fig. 13. Diagram of the shapes, postures, and movements of the,caudal fin. (A) Tracings of top view of swimming kawakawa during one-half of a complete tailbeat (adapted from Fierstine and Walters, 1968). (B) Posterior view of swimming kawakawa showing dihedral angle (adapted from Fierstine and Walters, 1968). (C) Diagram of path of an oscillating caudal fin showing amplitude (A), wave length (A), and fin postures (adapted from Gray, 1968). (D) Lateral view ofcaudal fin showing surface area (S J, span (b),sweepback angle (A), and a cross section and chord (c)at one location along the span. (E) Diagram for caudal fin of angle of attack (a)and angle of feathering (0).

some Thunnus. Those with higher AR should be the more efficient and faster swimmers (Nursall, 1958; Kramer, 1960; Aleev, 1963; Lighthill, 1969, 1975; Wu, 1971; Webb, 1975; Aleyev, 1977), all other things being equal. The higher the aspect ratio, the longer the leading edge that is important in leading-edge suction. The longer trailing edge increases the mass of water deflected posteriorly by the fin’s lateral movement. Induced drag from tip vortices is also less important rela-

292

JOHN J. MAGNUSON

Table IX Aspect Ratios (AR) of the Caudal Fins from Seventeen Scombrids Listed in Order of Decreasing AR ARa

6.8-7.2

6.3-6.7 5.8-6.2

5.3-5.7 4.8-5.2 4.3-4.7

Species

Euthynnus pelamis (skipjack tuna) Auxis rochei (bullet mackerel) Euthynnus afinis (kawakawa) Thunnus albacares (yellowfin tuna) Thunnus obesus (bigeye tuna) Euthynnus alletteratus (little tunny) Euthynnus lineatus (black skipjack) Auxis thazard (frigate mackerel) Allothunnus f a h i (slender tuna) Thunnus alalunga (albacore) Sarda chiliensis (Pacific bonito) Scomberomorus sierra (sierra) Sarda sarda (Atlantic bontio) Scomber scombrus (Atlantic mackerel) Acanthocybium solanderi (wahoo) Thunnus thynnus (bluefin tuna)

-

Scomber japonicus (Japanese mackerel)

Sourceb

3,4 4 4 1, 3, 4 4 1 1, 3 2, 3 3 2, 3 3, 4 1, 3 2 2 3 3

3, 4

Values for AR (spanVcauda1 area) differed greatly among authors owing to method of measurement. Data were adjusted for bias as follows for each source: (1) + 1.8, (2) +0.8, (3) -0.6, and (4) +0.6. These were based on the differences between species where the same species was estimated by two authors and on the assumption that the mean between sources 3 and 4 was the best estimate. Fierstine and Walters expanded the fin as much as possible for measuring span; Magnuson did not. * Sources: (1) Nursall (1958); (2) Aleev (1963); (3)Fierstine and Walters (1968); (4) Magnuson (Table X and Fig. 19, this chapter).

tive to lift production in high aspect ratio hydrofoils. With high AR more of the caudal fin extends beyond the wake of the body. Aspect ratio increases with the length of the fish (Table X, Fig. 14C) and values near 8 characterize the largest skipjack tuna. The AR of Atlantic mackerel also increases with length from about 3 when 12 cm long to 5 when 25 cm (Aleev, 1963). The report that the AR’s of yellowfin tuna and skipjack tuna do not change with length (Fierstine and Walters, 1968) appears to result from a sample with too narrow a range of lengths. An increased AR and efficiency at larger sizes would be of value, since larger animals should encounter more drag per unit length than do smaller ones. Body surface area, important in friction drag, increases as P . Also longer fish are more likely to swim at faster speeds.

4. LOCOMOTION BY

293

SCOMBRID FISHES Table X

Relation between Size and Form of the Caudal Fin and Fork Length (t)of Seven Scombrids: Sweepback (A), Aspect Ratio (AR), Caudal Span ( b J ,and Caudal Area for Thrust (S,)" Correlation coefficients significant at p 5 0.01 Sample size

Scomber japonicus

A and

e

AR and C

Area (cm?

-

-

b , = 0.54+ 0.2&

s, = 0 . 0 1 ~ ~ ~ 7

14

-

-

b , = -2.22

S,

11

-

-

+ 0.2% b , = -3.24 + 0.3M

36

-0.73

+0.70

b , = -2.12

+ 0.34t

S,

31

-0.73

+0.77

b , = - 1.94 + 0.31t

31

-

+0.62

b , = -2.27

+ 0.3%

S , = 0.013P"

21

-

+0.63

b , = -3.07

+ 0.37e

S,

(Pacific bonito)

Auris rochei

Span (cm)

25

(Pacific mackerel) Sarda chiliensis

Regressions

0.022P.8B

1

S , = 0.017t'.ffl

(bullet mackerel)

Euthynnus afinis (kawakawa)

Euthynnus pelamis (skipjack tuna)

Thunnus albacares (yellowfin tuna)

Thunnus obesus

=

0.011P~08

S, = O.OOW*~M

=

0.012Pm

(bigeye tuna) Regressions shown in Fig. 14. New data on same fish used for morphometrics in Magnuson

(1973).

Interestingly, AR increases with length more rapidly for the two euthynnids than for the two thunnids. Since the sustained speed also increases more rapidly with length for the euthynnids than the thunnids (Fig. 8B,C), the greater AR for larger euthynnids again seems a reasonable adaptation. A curved leading edge of this tapered hydrofoil reduces leadingedge suction without reducing the total thrust produced, based on a mathematical analysis by Chopra and Kambe (1977). They point out that there is an advantage because if leading-edge suction were too high, boundary layer separation could occur and significantly reduce thrust. The mean sweepback angle (Fig. 13D) of the caudal fin ranges from about 25"-50" in adults of seven species (Fig. 14D). The hydromechanical efficiency of a high thrust device such as the caudal fin declines slightly with increased sweepback (Chopra and Kambe, 1977, Fig. 5b). This feature appears to have influenced the evolution of caudal shape. For example, the sweepback was less for larger fish (Table X) and for species with faster sustained speeds (Fig. 8) than for

4 294

Y

JOHN J. MAGNUSON I B '

'

'

"

'

'

c Q 0

F

'

'

'

'

'

'

'

1

20

FORK

-

'

'

~

~

'

"

"

"

'

'

'

1"-

10

0

-

:' -

0

'

0 '

=-

LENGTH Icml

-d

5,-

/--O A.

20

10

60

111

100

lZ0

*o

0

20

.o

80

80

100

120

,lo

smaller fish or those with slower sustained speeds. The caudal fins with greater sweepback should be able to operate at greater angles of attack (Fig. 13E), a feature that should be helpful at the slower sustained speeds (Fig. 1A) that characterizes most of the species or sizes with greater sweepback in Fig. 14D. Species with greater sweepback on the caudal fin also have lower aspect ratios (Fig. 14C, D). This observation is consistent with analyses by Hopkins (1951) that a lower aspect ratio is required for longitudinal stability of a wing with greater sweepback. Other comments on sweepback are that tails with greater sweepback have the center of thrust farther back on the fin, and that greater sweepback contributes to vertical stability (von Kirmin, 1954) of the laterally moving caudal fin, i.e., it should help prevent the fin from twisting on the peduncle. Areas and spans of caudal fins vary among species (Fig. 14A, B) in ways probably important to each species. The two thunnids have the greatest spans and areas. For example, at 80 cm lengths the caudal span of a yellowfin tuna is 1.2 times that of a skipjack tuna. Its caudal area is 1.7 times that of a skipjack tuna. Since thrust is proportional to area, those with larger area should be able to produce more thrust if all

4.


295

other things were equal such as angle of attack and speed of caudal movement. Apparently, they do produce more thrust because yellowfin tuna travel farther per tailbeat than do skipjack tuna (see Fig. 16). Alternatively, species with a greater caudal area should be able to produce the same thrust at lower tailbeat frequencies or lower amplitudes of caudal movement. The greater spans should help reduce drag induced at the tips of the caudal fin.

B. Movements and Postures of the Caudal Fin

The caudal fin beats back and forth as the fish moves forward and traces an oscillating path of movement (Fig. 13C) (Gray, 1968; Fierstine and Walters, 1968; Magnuson, 1970; Webb, 1975). Since it is at the end of the stiff peduncle formed from fused vertebrae (Fierstine and Walters, 1968; Nursall, 1956) it has accentuated lateral movement as if the fin were at the end of a pendulum. Bending of the fish body is concentrated at the prepeduncular joint just anterior to the peduncle (Fig. 13A).I n a comparative study by Aleev (1963) the scombrids were the most specialized in regard to concentrating the body bending in an area between 0.6 and 0.8 8. The wavelike path of the caudal fin (Fig. 13C) can be characterized by a peak to peak amplitude (A), a wavelength (A), a frequency 0, and a period. The fin has the same forward velocity as the fish (V), a lateral velocity (W) at right angles to the direction of swimming, and a speed along its oscillating path (Fig. 13C). It has an angle of attack (a)in respect to its path and a feathering angle ( 6 ) (Fig. 13E). Feathering is the angle between the path of the fin and the direction of movement of the fish. In addition, camber and a dihedral angle develop with the lateral movement of the fin. Most fishes appear to have amplitudes approximately equal to 0.21 8 that do not vary with length (Hunter and Zweifel, 1971) nor with frequencies above five tailbeats/sec (Bainbridge, 1958). Amplitude has been measured on three scombrids but does not follow the above generalities. For Pacific mackerel 30 cm long A = 0.18 8 (Hunter and Zweifel, 1971, Fig. 6). For kawakawa amplitude more than doubled from 0.16 t' to 0.34 e as frequency approximately doubled from eight to fourteen beats/sec (Fig. 15). For Atlantic bonito 16 cm long ampliiude was highest at slowest speeds (0.30e at 2 8/sec), reached a minimum of 0.22 at 5-6 tlsec, and appeared to increase slowly to about 0.24 e at 8 81sec (Pyatetskiy, 1970b, Fig. 6). Thus, the amplitude is varied by scombrids to obtain appropriate swimming performance and is not as constant as previously implied. Species such as wahoo with a long narrow body may have even greater amplitude than kawakawa. This

296

JOHN J. MAGNUSON SWl M M ING SPEED

E X T R E M E AXIS

AMPLITUDE

FREQUENCY

EXTREME

Fig. 15. Transverse caudal velocity during a tailbeat at five swimming speeds. Amplitudes and frequency of tailbeat are also given. (Adapted from Fierstine and Walters, 1968.)

could compensate, in the wahoo, for a relatively low AR for the caudal fin and a body shape that does not minimize drag. Wahoo (Fig. l B , Table 11) has one of the fastest burst speeds measured. The hydromechanical efficiency (7) of the caudal fin is expected to be fairly high over a wide range of tailbeat amplitudes (Chopra, 1976) or, in other words, the proportion of total thrust lost in wake vortices does not vary much with amplitude (A). This is apparent in Chopra’s analysis of the effects of reduced frequency. Reduced frequency [see Eq. (24)] is defined as a ratio of time to swim distance equal to the chord of the caudal fin and the time for one tailbeat (Lighthill, 1975; Chopra, 1975). This value, computed from data of Fierstine and Walters (1968) and used later to calculate thrust force (Table XI), is 0.7 based on my calculations, 0.6 from Webb (1975), and 0.8 from Chopra (1976) (the original values of Webb and Chopra converted to equilvalent units). Note that reduced frequency in this chapter is defined the same as in Webb (1975), Lighthill (1975), and Chopra and Kambe (1977), but is twice that as defined in Chopra (1975, 1976) owing to differences in the definition of the caudal fin’s chord (c), Transverse caudal velocity (Fig. 15) when crossing the axis of pro-

4.

297


gression of the fish ranged between 133 and 500 cm/sec or about 1.5 times the swimming speed of kawakawa (see calculation of W,,, in Table XI). Thrust from the caudal fin increases in proportion to transverse velocity squared. At speeds of less than 4 t/sec transverse caudal velocity was slowest at the beginning and end of a sweep and maximum at the axis (Fig. 15C). But at the faster speeds it was much greater in the last half of each sweep (Fig. 15E). This asymmetry may be important in producing extra thrust such as suggested from underwater movements b y man (Seireg et al., 1971, personal communication 1976).The increase is also closely tied to a corresponding decrease in angle of attack during a sweep. Fierstine and Walters (1968) suggested that the increase in transverse velocity and the concurrent decrease in angle of attack are functionally related to maintain constant thrust during all phases of a tailbeat cycle. Speed appears to increase linearly with increases in tailbeat frequency (Fig. 16) at rates between 0.5 and 0.8 t per tailbeat. A tailbeat is a full cycle back and forth; Fig. 13A is only 0.5 tailbeat. The two species that go farther per tailbeat were those with the greatest caudal span per unit length ( b ,= 0.31-0.35 t versus 0.24-0.29 t) and the highest aspect ratio (6.8-7.2 versus 4.3-6.2). Frequencies of 13 beatshec have been recorded (Yuen, 1966). In I

A

-

I

Pacific M a c k e r e l

0 Pacific Bonito 10

0

-

W v)

a -

30cm F L 57cm F L

0 Atlantic Bonita

16cm T L

0 Skipjack Tuna

57cm F L

0 Yellowfin Tuna

53cm F L

a W

W

n. u)

(35 -

5 5

r3 v)

-0

n

A 5

10

15

TAIL B E A T S I S E C .

Fig. 16. Relation between frequency (f) of tailbeats and swimming speed (t'/sec) for five scombrids. Sources: A Hunter and Zweifel (1971); [?1 Magnuson and Prescott (1966);0 Pyatetskiy (1970a); 0 and 0 Yuen (1966).

298

JOHN J. MAGNUSON

Table Calculation and Comparison of Theoretical Thrust Thrustb (2)

(1)

( 3)

(4)

(5)

(6)

( 7)

(8)

( 9)

Proportional feathering ( 1Y

A

e (cm) ~

U

r

(cmisec) 124 158 160 188 328

"mnr

(cyclesisec)

Proportion of e

cm

(cmisec)

Degrees

Radians

7.7 9.1 10.1 12.5 14.5

0.16 0.26 0.25 0.20 0.34

6.4 10.4 10.0 8.0 13.6

146 23 1 289 298 500

25 50 30 30 40

0.44 0.87 0.52 0.52 0.70

wm,,

~~

40 40 40 40 40

(19)

( 20)

(21)

0.4 0.6 0.3 0.3 0.5 0.42 (mean)

(22)

Theoretical body friction

40 40 40 40 40

124 152 160 188 328

5.0 x 6.1 x 6.4 x 7.5 x 1.3x

18

lo5 10' 18 108

c,

S

( 1)

(cm')

0.0052 0.0050 0.0050

720

0.0048 0.0043

720 720 720 720

Drag force (dynes) 3.0 x 4.3x 4.7 x 6.2 x 1.6 x

l@

I@ I@ I@ 10'

Proportion of total thrust force 0.31. 0.24 0.11 0.14 0.14 0.28 (mean)

" Following methods similar to Webb (1975); however, rather than using Webb's estimates, new values were used tor most parameters tyased oil a reanalysis of source d a b Key: (1) e most likely used by Fierstine and Walters (1968) from Walters (1966). (2) 40 cm x ekec from Fig. 15. (3) Froin Fig. 15. (4) From Fig. 15. (5) 40 cni x (column 4). (6) (ZA)(f)(measured W at axis/measured mean W of full cycle). Ratios were 1.48, 1.22, 1.43, 1.49, 1.27. Taken from Fig. 15 and Webb (1975). (7) Measured LI at axis of cycle from Walters and Fierstine (1968). (8) x 0.0174. (9) From Eq. (24). (10) From Eq. (28), c = 1.9 cm, or S,, h,. (11) From Fig. 17. (12) From Fig. 17. (13) Root mean square lateral .;peed = 0.707 W,,,. (14) Froin Tiihle X. (15) From Eq. (25). (16) From Eli. (26). (17) Same BS (2). (18) R,. = UP/O.OI. (19) From Eq. (13), i.e., turbulent. (20) 0.279 P ':I from Magnuson and Weininger (1978). (21) D,from Eq. (11). (22) (Column Pl)/(column 15). (23) (Column 21) +form drag on body + friction on second dorsal and anal +form drag on second dorsal and anal + friction on caudal + form drag on caudal. Flows over fins were assumed to be laminar and friction drag wiis computed with Eqa. ( 11) and (12) using morphometry data as follows:

comparison, hummingbirds average almost 30/sec (Hertel, 1966). For scombrids to attain speeds near 20 Usec, frequencies over 20/sec are probably required. Wavelength ranges among species from 0.2 to 1.9 e at 2 tailbeatshec, from 0.7 to 1.0 f/sec at 5 beatshec, and 0.7-0.8 G at 10 beats/sec (estimated from data in Fig. 16). With the exception of the Pacific mackerel, wavelength decreases at higher frequencies, i.e., the fish goes a shorter distance per tailbeat. The angle of attack (Fig. 13E) of the caudal fin measured from overhead photographs of swimming kawakawa varied from 25" to 50" at

299

4. LOCOMOTION BY SCOMBRID FISHES XI and Theoretical Drag Forces for a 40 cm Kawakawa Swimming at Five Speeds" (10)

(12)

(11)

Reduced frequency (1) 0.7 0.7 0.8 0.8 0.5 0.70 (mean)

c,

V"

(1)

(proportion)

0.8 0.6 0.9 0.9 0.8 0.80 (mean)

(23) (24) Same as 21-22 plns fomi drag on liody and friction and fonn drag on fins (wxond dorsal, anal, and caudal)

W,.,, (cmlsec)

S, (cnil)

I03 163 204 211 354

22 22 22 22 22

0.8 0.9 0.8 0.8 0.9 0.84(mean)

(25)

(14)

(13)

( 15)

(16)

Thrust force (dynes)

Total thrust power (ergskec)

9.6 x 1.8 x 4.2 x 4.5 x 1.1 x

lW

1.2 x 2.7 x 6.7 x 8.5 x 3.6 x

I05 10) I05 IoR

107 107

107 10' 1oR

(26)

Same aa 2.>24 plus drag iqduced from caudal fin Coefficient of totd drag

DKlg force (dynes)

4.5 x lW

1W 6.9 x 1W 9.2 x lW

6.4 x

2.3x 10)

Proportion of total thnist force

Drag force (dynes)

0.47 0 3 0. I6 0.20 0.21 0.28 (rilean)

6.4 x 8.2 x 1.5 x 1.8 x 3.4 x

I@ I@ 10% 10' 105

Proportion of total thrust force

From drag calculation

0.011 0.0094 0.016 0.014 0.0086 0.012 (mean)

0.67 0.46 0.36 0.40 0.31 0.44 (mezin)

Fina

c (cm)

S (cnil)

Anal and second dorsal C;ludal

1.3

15 44

1.7

From thrust calculation 0.016 0.011 0.044 0.034 0.028 0.027 (mean)

b (4

12

(column 15). (26) (Column Form drag w a s calculated iih i n Table VI. (24) Column 23)/(column 15). (25) (Column 23) + ( 1 = total dragtp,SU* where total 25)/(mlumn 15). (27) C , ,,,ti,,= total drag/hp,SU* where total drag = column (25); C. drag = colinnii (15). The number I indicates nondimensional.

the point where the fin crossed the axis of progression (Fierstine and Walters, 1968, Fig. 6). It averaged about 30" over a whole cycle but attained values as high as 100". Angle of attack changed systematically-starting large at the beginning of a sweep from one side to the other and ending small at the end of a sweep. Within limits, the coefficient of thrust increases directly with angle of attack, but greater hydromechanical efficiency results at lower angles of attack (Chopra, 1976). The angle of attack is maintained positively during lateral movements in each direction by rotation at the postpeduncular joint (Fig. 13A). Forces for the rotation of the fin are primarily from

300

JOHN J. MAGNUSON

water pressure rather than overt muscular activity (Fierstine and Walters, 1968). The fin is somewhat flexible and is stoutly attached at its base. Consequently, during lateral movement the tips lag behind the center and a dihedral angle develops (Fig. 13B).This angle remains positive in respect to the lateral movement of the tail because pressure alternates from one side of the fin to the other when the sweep changes direction. The dihedral angle contributes to stability and helps prevent the fin from twisting (rolling) on the end of the peduncle. The same forces deflect the trailing edge of the fin and camber develops during each sweep. However, as noted by ‘Fierstine and Walters (1968),the direction of camber is opposite to typical hydrofoils because it is convex on the high pressure side. Proportional feathering, an important concept put forth by Lighthill ( 1969), greatly influences thrust production. The parameter geometrically is a ratio of slopes between a and 8 in Fig. 13E (Wu, 1971). The parameter can be computed (Webb, 1975): Proportional feathering = amaxU/W,,,

(24)

where amax,angle of attack in radians, i.e., the slope of a; W,,,, maximum lateral velocity of the fin (cmisec); U , forward velocity of the fin or swimming speed (cmlsec).W,,, and a,,, can be measured from overhead photographs of swimming fishes at the point in lateral movement where the caudal fin passes through the axis. U can also be measured. The easiest way for me to think about proportional feathering is to note that when the angle a in Fig. 13E and 8 are equal they have the same slopes and proportional feathering = 1. In this case the fin is oriented parallel to the fish’s direction of forward progression. When a = 0, proportional feathering = 0 and the caudal fin is oriented parallel to its own path. Thrust is obtained from a caudal fin by leading-edge suction and from the backwardly inclined component of lateral forces (Lighthill, 1975; Chopra, 1975). When proportional feathering = 1, little lift is produced because no water is directed posteriorly since the fin is not inclined to the direction of the fish’s swimming. The thrust coefficient is also very low (Lighthill, 1969, 1975; Wu, 1971; Chopra, 1975). When proportional feathering = 0, again no water is directed to the rear and all thrust comes from leading-edge suction. In this case the fin has a high coefficient of thrust, but has a low hydromechanical efficiency. At intermediate values of proportional feathering the fin deflects water to the rear, and postures that optimize combinations of leading-edge suc-

4. LOCOMOTION BY SCOMBFUD FISHES

301

tion and hydromechanical efficiency occur with proportional feathering between 0.6 and 0.8 (Lighthill, 1975). Proportional feathering of the caudal fin of a kawakawa, based on data from Fierstine and Walters (1968), is between 0.3 and 0.6 (see calculations by me in Table XI)and from the same data between 0.3 and 0.9 by Webb (1975). C. Theory and Magnitude of Thrust Models to represent thrust were reviewed by Webb (1975) and are under development by Wu (1961, 1971), Lighthill (1969, 1970, 1975), Logvinovich ( 1970), Chopra (1975, 1976), Chopra and Kambe (1977), and James (1975). The most appropriate model for scombrids is developing from a two-dimensional theory of oscillatory airfoils. The two-dimensional model is expected to result in an overestimation of thrust and some attempts are being made to improve it by considering three dimensions (Chopra, 1975, 1976; Chopra and Kambe, 1977; James, 1975; Lighthill, 1975). In particular, hydrofoils of different aspect ratio, sweepback, and leading edge curvature are being considered, as are larger amplitude oscillations with large angles of attack. Thrust is derived by directing a jet of water backward over a large span as depicted in Fig. 9. Forward thrust can be considered a reaction to this “jet stream” (Wu, 1971). A vortex train is set up like a vortex sheet behind a stationary object, but with the rotation in the opposite direction to that behind a stationary object. The rotation is induced by the posteriorly directed flow. A discussion of a reaction model and useful diagrams of how a caudal fin moving laterally and forward at an angle of attack sheds vortices into the wake to accomplish useful work is presented in Lighthill (1969,1975) and Webb (1975)(see Chapter 3). Thrust is also obtained at the same time as mentioned earlier from leading-edge suction. The thrust (Tforcein dynes) generated, as taken from Lighthill (1970) and Webb (1975), is proportional to the area of the caudal fin (SJ, a measure of lateral velocity of the fin (WrmJ,water density (pJ, and the coefficient of thrust (CT):

The thrust power (TpOwer in ergslsec) is

Power is force exerted over a distance or work done per unit time. As discussed earlier, not all the power expended on the water produces

302

JOHN J. MAGNUSON

useful thrust. Some is wasted in vortices that either do not contribute to thrust or do not do so efficiently. Consequently, the actual thrust power obtained is equal to:

(27)

%TPOWBI.

where r), is hydromechanical efficiency (Lighthill, 1969, 1975). In the present analyses I have considered these losses ( 1 - r),) as a part of drag induced by the propulsive movement of the caudal fin. S, can be measured from dead fishes (Table X), and W and U can be estimated from overhead photographs of swimming fish (see Table XI for computation). CT and 77p can be interpolated from graphs of functional relations developed by Lighthill (1975) and Chopra (1975) (see Fig. 17). Both values depend on proportional feathering that can be calculated from Eq. (24) and reduced frequency (c)(Lighthill, 1970): OC

(+=-

U

where o = angular velocity for assummed harmonic motion or 27rf in radians, c = mean chord of the caudal fin (caudal area t caudal span) in cm. Proportional feathering and the frequency parameter are the keys to the estimatiou problem. The relation between them and C Tand qp will differ as the models are refined. For the present computation in Table XI, I used Chopra’s (1975) graphs for a rectangular hydrofoil with AR of 4. The mean coefficient of thrust from this model applied to Fierstine and Walters (1968) data on Kawakawa (Table XI) is C , = 0.8. This is lower than that obtained if Lighthill’s (1975) model for an

-

OO

10

wc -

U

2.0

; OO

1.0

2.0

w c -

U

Fig. 17. Graphs for estimating the coefficient of thrust (C,) and the hydromechanical efficiency (qp)of the caudal fin at different values of the frequency parameter (wclU)and proportional feathering (0). Based on a rectangular caudal fin with AR = 4 with the pitching axis at full chord. Modified from Chopra (1975). Lunate-tail swiinming propulsion. In “Swimming and Flying jn Nature” (T. Y. T. Wu, C. J. Brokaw, and C. Brennen, eds.), Vol. 2, pp. 635-650. Copyright 1975 by Plenum Press.

4.


303

infinitely long wing were used, C T= 1.0, and it is also lower than if Chopra and Kambe’s (1977) model for a curved and tapered hydrofoil (their B2 model) with an AR of 8 were used, C T =0.9. None of the models specified matches the dimensions of the caudal fin of kawakawa, which has a shape similar to the tapered hydrofoil with curved anterior and posterior margins (model B2 in Chopra and Kambe, 1977) but an AR of about 6 (Fig. 14), intermediate between 4 and 8, for which graphed relationships (Chopra, 1975) are published for hydrofoils with a finite span. The choice of model does not influence significantly the value for the hydromechanical efficiency of the caudal fin ( 7 ) .With all three models, it averages 0.84 (Table XI). Thrust is computed in Table XI for kawakawa swimming at speeds of from 3 to 8 Msec. The method is taken largely from Webb (1975, Table 17) with a reanalysis of data on the swimming kawakawa (Fierstine and Walters, 1968), new data from the present paper, and the use of Chopra’s (1975) relations between feathering, reduced frequency, and C Tand y p(Fig. 17). Methods of calculation and sources of data are given in the footnotes to the table. Drag calculations are also made in Table XI following procedures outlined earlier in this paper. Four values of drag were made that included different components. The first estimate included only friction on the body assuming turbulent flow. This averaged 18% of the predicted thrust (see column 22). This percentage is similar to the percentage of total drag provided by friction on the body (Table VI) of a skipjack tuna swimming at sustained speeds. If friction on the body actually produced one-fourth of the total drag on these kawakawa swimming at these faster speeds, then the estimate of total thrust and total drag for these kawakawa would be very close. This would suggest a remarkable agreement between theoretical calculations of thrust and drag which of course should equal each other. However, at these faster speeds, friction should make up a larger portion of total drag [perhaps about 40% from (column 2l)/(column 25) in Table XI] than at the slower sustained speeds. A second estimate of drag to compare with thrust calculation included friction and form drag at the body plus friction and form drag on the permanently extended fins (columns 23 and 24). Flow over the fins was assumed to be laminar. These values equaled 28% of the calculated thrust and were still too low. A third estimate included the drag induced by the caudal fin and averaged 44% of the calculated thrust. The analysis implies that either drag is underestimated or thrust is overestimated. Yet, the agreement between calculations of thrust and drag was good. The calculations were easily within one order of mag-

304

JOHN J. MAGNUSON

nitude and closer to a factor of 2 to each other after other components of drag were added to body friction. The agreement was slightly better in my analysis than in Webb’s (1975) because I included sources of drag from the fins and thrust production and because I used Chopra’s ( 1975) calculations for C for a three-dimensional hydrofoil rather than Lighthill’s (1975) for a two-dimensional hydrofoil. Underestimates of drag could have resulted from underestimates of surface areas or frictional drag coefficients, overestimates of hydromechanical efficiency,or the exclusion of any induced drag from lift. In addition, the postures of the fins for the fish were not known. I assumed that the pelvic, pectoral, and first dorsal fins were appressed and that the mouth was closed, as they should have been at these speeds. Yet Fierstine and Walters (1968) noted that the dorsal fin was extended in some sequences and the fish may have been turning (Fierstine, personal communication). However, even if drag on the pectorals and gill resistance were computed and included in the drag estimates, the total thrust estimates would still exceed the total drag estimates. Induced drag from lift should be negligible at these high speeds even if the body were acting as a lifting surface. Since turbulent rather than laminar flow over the body was assumed, I doubt that frictional drag coefficients were too low. If laminar rather than frictional drag coefficients had been used for the body, the agreement between drag and thrust would have been poorer. Perhaps the most realistic assumption would be to assume laminar flow over the anterior half of the body and turbulent flow over the posterior half based on flow and pressure observations discussed in Aleyev (1977). Overestimates of thrust could result from overestimates of either hydromechanical efficiency or the lift coefficient of the caudal fin. Only five sequences of a swimming scombrid have been analyzed to provide data for the above analysis. In four of the five measurements the distances traveled per tailbeat were only about one-half of those observed for other scombrids in Fig. 16. Perhaps the reversed camber of the caudal fin reduces thrust. Perhaps the body interferes with thrust production even with narrow necking because much of the caudal fin still lies in the turbulent wake left by the body. The agreement between thrust and drag calculations suggests we may be reaching a useful level of prediction and that the mechanisms for thrust and drag production by scombrids are reasonably well represented in the models and coefficients. Even so, it is apparent that further refinements in the models and additional data on swimming scombrids are still needed. Also, independent collaboration of thrust and drag estimates are needed from data on metabolism.

4.


305

VII. THE LOCOMOTORY SYSTEM Scombrids are astounding bundles of adaptations for efficient and rapid swimming. All features of hydromechanics, morphology, and behavior, while discussed above in pieces, are parts of an interactive and coherent locomotory system. Still other pieces of the system such as those related to maneuvering and stability, physiology and metabolism, and ecology and the acquisition of energy were not considered here. The entire biology of scombrids is tightly linked to swimming as a way of life. All life’s activities occur in motion. Feeding, courtship, spawning, and resting are all done on the move (Magnuson and Prescott, 1966; Magnuson, 1969). Parental care is restricted to leaving the fertilized eggs in a suitable water mass in pelagia. Sustained swimming keeps scombrids from sinking, ventilates their gills, brings them in contact with food, and moves them rapidly over the vast distances of the open ocean. Burst swimming serves primarily in escape from predators and the pursuit of prey. In feeding schools food is only available in presence of other competitors and the development of a fast feeding attack may have evolved in response to getting there first, rather than catching up with the prey per se. Scombrids can easily outdistance their prey. While all scombrids are continuous and rapid swimmers, each species is a unique evolutionary solution for life that exemplifies a welI-tuned locomotory system. Three genera (Euthynnus, Thunnus, and Acanthocybiurn) will be discussed here to point out the integration of the locomotory system. Euthynnids, represented by the skipjack tuna and kawakawa, are small to medium in size and have fast rates of sustained swimming. Thunnids, represented b y yellowfin tuna, bigeye tuna, and albacore, are large species with intermediate rates of sustained swimming. Acanthocybium, represented by the wahoo, is a large and elongate species with slow rates of sustained swimming and the highest burst speeds. The first thing to note is that most locomotory adaptations are more closely correlated to continuous or sustained swimming than to burst swimming (Table XII). For example the aspect ratio of the caudal fih and blood hemoglobin concentrations are greatest for euthynnids with the fastest sustained speeds but with the slowest burst speed. Second, the locomotory adaptations are more closely correlated to speed measured in lengths per sec (t/sec) than to speed in either Reynolds number (RL) (Table XII) or absolute units (cmhec). For example, at sustained speeds Acanthocybium with the highest RL has the lowest

306

JOHN J. MAGNUSON

Table Comparison of Swimming Speeds and Hydromechanic Parameters Lift and weight

Swimming speed ( 2)

( 1)

(3)

(4)

(5)

(6) Pectoral loading

Sustained Genus

Euthynnus Thunnus Acanthocybiurn

Nsec

2.3 0.97 0.33

R,

3.0 x 1oJ 3.7x 1P 5.1 X 1oJ

Burst elsec

12 14 15

R

,.

3.4 x 10s 7.3x 10s 1.6 X lo7

Lengths Per tailbeat

4.2 5.0

-

( 1000 Pe

(g/cc)

1.091 1.052 1.028

S, (cm')

72 88

-

dynes1 cm')

9.4 2.4 0.4

0 Key: (1) mean from Table I; (2) mean from Table 11; (3)from Fig. 16 at 5 beatslsec; (4)largest fish measured (Table 111); (5)calculated for 50 cm long fish from Magnuson (1973,Table 4) and from Dotson (1977);( 6 ) mean from Magnuson (1973,Table 3);(7)mean from Table IX; (8)calculated for 50 cm long fish from Table X; (9)calculated for 50 cm long fish from Table X; (10)from

sustained speed in elsec, as well as the lowest aspect ratio of the caudal fin and the lowest blood hemoglobin concentration. The euthynnids have sustained speeds (e/sec) that are 2.4 times those of thunnids and 7.0 times those ofAcanthocybium (Table XII). The differences are due to the hydromechanics of countering their weight in water which they do by generating lift on their extended pectoral fins during continuous swimming. Differences in sustained speeds are expected from differences in surface loadings of the pectoral fins which for euthynnids are 4.0 times those of thunnids and 24 times those ofAcanthocybium. Faster sustained speeds have evolved along with adaptations for efficient thrust production and drag reduction. For example, the average aspect ratio of the caudal fin of euthynnids 7.0 compares with 6.5 for thunnids and only 5.5 for Acanthocybium (Table XII). Likewise the body ofAcanthocybium is not as well streamlined for sustained swimming as the euthynnids and thunnids. Finally, the physiological resources for sustained swimming are greater for euthynnids than thunnids, and for thunnids than Acanthocybium (Table XII). Magnitudes of muscles and the oxygen transport system are the physiological resources considered here. Blood hemoglobin concentrations of euthynnids are 1.1 times those of thunnids and 1.7 times those ofAcanthocybium. Gill areas of euthynnids are 1.3 times those of thunnids. Both euthynnids and thunnids have a greater body mass at a given length than Acanthocybium and consequently should have a greater total muscle mass. In addition the

4.

307


XI1 of Euthynnus, Thunnus, and Acanthocybium" Thrust (7 )

(8)

Drag

(9)

b,

AR

S, (cm')

(cm)

7.0 6.5 5.5

30 38 -

14 15 -

(10)

(11)

Body Position thick- maximum ness thickness (% e) (% l')

22 23 12

41+ 41+ 37+

Physiological resources ( 12)

Induced from lift High Medium Low

(13)

(14)

(15)

Red

Blood hemoglobin

(kg)

muscle (%M,)

(g/100 ml)

2.4 2.5 1.0

8.4 7.6 1.8

17 15 10

MI

(16) Gill area (m')

4.0 3.0

-

Table VII; ( 11) from Table VII; (12) proportional to pectoral loading; (13) calculated for 50 cm long fish from Magnuson (1973, Table 4) and from Dotson (1977); (14) means from Magnuson ( 1973, Table 7); (15) means from Magnuson (1973, Table 7); (16) calculated for 2.5 kg fish from equations in Muir and Hughes (1969).

red muscle (% mass) used for sustained swimming (Rayner and Keenan, 1967) is 1.1 times larger in euthynnids than in thunnids and 4.7 times larger than in Acanthocybium. Thus, adaptations that dictate fast sustained speeds are closely related to observed speeds as are adaptations for efficient thrust production, drag reduction, oxygen transport, and development of muscular forces. Burst speeds do not differ among the three genera as much as the sustained speeds do, and those slight differences observed are in the reverse order. Acanthocybium had the fastest burst speed, and euthynnids had the slowest. The burst speed of Acanthocybium was 1.2 times those of euthynnids while sustained speed of euthynnids was 7 times those ofAcanthocybium. I would guess that the faster speeds are possible for a shorter time in Acanthocybium because the white muscles are smaller, as indicated by the mass-length relationship, and because the oxygen transport system is less developed, as indicated by low concentrations of blood hemoglobin. The faster burst speeds may be related to greater caudal areas or speed of lateral movement by the caudal fin, but data are lacking. The thunnids had faster burst speeds and swam farther per tailbeat than euthynnids (Table XII). This could b e predicted in part by the large caudal area of thunnids and perhaps by a greater amplitude of tail movements. However, comparative data on amplitudes and tailbeat frequencies are not available. It appears that variation in speed of sustained swimming has more

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JOHN J. MAGNUSON

closely influenced the evolution of swimming adaptations among scombrids than have considerations of burst speeds. All have fast burst speeds and the adaptations for continuous swimming apparently serve well in fast swimming. With the magnitude of forces involved in continuous swimming it is not surprising that adaptations for producing large amounts of thrust and lift as well as reducing drag i r e finely tuned. What is more surprising is the necessity of continuous locomotion in the first place. The loss of or reduction of the gas bladder is the adaptation that results in continuous swimming and its attendent drag for a pelagic teleost. What selective pressures have molded evolution along this energy demanding path? The most likely idea is that it increases vertical mobility especially near the sea surface (Magnuson, 1966, 1973; Lighthill, 1969,1975). This would be important in food capture and in escape from predators. Species are not slowed by the requirement to absorb expanding gases from the gas bladder during a rapid ascent. A new hypothesis, considered above, is that the negative buoyancy makes possible gliding and soaring by scombrids in waves near the surface or in the thermocline. This would make horizontal movements in the sea effortless under certain conditions. Data to support these ideas are skimpy or absent entirely. Regardless of evolutionary history, the locomotory system that has evolved in these negatively buoyant, pelagic teleosts will continue to challenge the biologists and engineers. ACKNOWLEDGMENTS

I thank my wife, Norma, for her help with.this study. I also thank T. Y. T. Wu for occasional help in translating mathematics to English for me; R. McN. Alexander, C. D. Sharp, and P. W. Webb for their comments on an early draft; and J. L. Brooks for his encouragement. New information presented on the morphometry of scombrids was extracted from photographic data from the files of the Honolulu Laboratory of the National Marine Fisheries Service. REFERENCES Aleev, Y. C . (1963).“Funktional ’nye Osnovy Vneshnego Strecniya Ryby (Functional and Cross Morphology in Fish),” 245 pp. Izd. Akad. Nauk SSSR, Moscow. (Transl. by Isr. Program Sci. Transl., T T 67-51391,268 pp. Natl. Tech. Inf. Sew., Springfield, Virginia, 1969.) Alexander, R. McN. (1965).The lift produced by the heterocercal tails of Se1achii.J. E r p . B i d . 43, 131-138.

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Alexander, R. McN. (1967). “Functional Design i n Fishes.” Hutchinson, London. Alexander, R. McN. (1968).“Animal Mechanics.” Univ. of Washington Press, Seattle. Aleyev, Y. G. (1977).“Nekton.” Dr. W. Junk b.v. Publishers, The Hague. Aleyev, Y. G., and Ovcharov, 0. P. (1973).The three-dimensional pattern of flow round a moving fish.J. Zchthyol. (USSR) 13, 933-936. Anonymous (1975).A study of the applications of remote sensing techniques for detection and enumeration of giant bluefin tuna. Southeast Fish. Cent. Contrib. No. 437 (MARMAP No. 108). Bainbridge, R. (1958). The speed of swimming of fish as related to size and to the frequency and amplitude of tail beat.J. E x p . Biol. 35, 109-133. Bainbridge, R. (1961).Problems of fish locomotion. Zool. Soc. London 5, 13-32 (Vertebrate Locomotion Symposium). Baldridge, H. D., Jr. (1970). Sinking factors and average densities of Florida sharks as functions of liver buoyancy. Copeia pp. 744-754. Baldridge, H. D., Jr. (1972). Accumulation and function of liver oil in Florida sharks. Copeia pp. 306-325. Belyayev, V. V., and Zuyev, G. V. (1969).Hydrodynamic hypothesis of school formation in fishes.J. Zchthyol. (USSR)9, 578-584. Blaxter, J. H. S., and Dickson, W. (1959).Observations on the swimming speeds of fish.J. Cons., Cons. Perm. Znt. Explor. Mer 24, 472-479. Bone, Q. (1975).Muscular And energetic aspects of fish swimming. In “Swimming and Flying in Nature” (T. Y. T. Wu, C. J. Brokaw, and C. Brennin, eds.), Vol. 2, pp. 493-528. Plenum, New York. Bone, Q., andRoberts, B. L. (1969).The density of e1asmobranchs.J. Mar. Biol. Ass. U.K. 4% 913-937. Breder, C. M., Jr. (1926). The locomotion of fishes. Zoologica (N.Y.) 4, 159-256. Breder, C. M., Jr. (1965). Vortices and fish schools. Zoologica (N.Y.)50,97-114. Breder, C. .M., Jr. (1967). On the survival value of fish schools. Zoologica (N.Y.) 52, 25-40. Breder, C. M., Jr. (1976). Fish schools as operational structures. Fish. Bull. 74,471-502. Brown, C. E., and Muir, B. S. (1970). Analysis of ram ventilation of fish gills with application to skipjack tuna (Katsuwonus pelamis). J . Fish. Res. Board Can. 27, 1637-1652. Cahn, P. H. (1972).Sensory factors in the side-to-side spacing and positional orientation of the tuna, Euthynnus aflinis, during schooling. U S . Fish Wiidl. Serv., Fish. Bull. 70, 197-204. Chopra, M. G. (1975).Lunate-tail swimming propulsion. In “Swimming and Flying in Nature” (T. Y. T. Wu, C:J. Brokaw, and C. Brennen, eds.), Vol. 2, pp. 635-650. Plenum, New York. Chopra, M. G . (1976). Large amplitude lunate-tail theory of fish locomotion. J . Fluid Mech. 74, 161-182. Chopra, M. G., and Kambe, T. (1977).Hydromechanics of lunate-tail swimming propulsion. Part 11. J. Fluid Mech. 79, 49-69. Commercial Fisheries Review (1969).Underwater tuna school tracked by sonar. Commer. Fish. Reu. 31(11), 9-10. Cone, C. D., Jr. (1962). Thermal soaring of birds. A m . Sci. 50, 180-209. Dizon, A. E., Neill, W. H., and Magnuson, J, J. (1977).Rapid temperature compensation of volitional swimming speeds and lethal temperatures in tropical tunas (Scombridae). Enu. Biol. Fish. 2, 83-92.

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Dotson, R. C. (1977).Minimum swimming speed of albacore (Thunnus alalunga). Natl. Mar. Fish. Serv., Southwest Fish. Cent., La Jolla, California. Fierstine, H. L., and Walters, V. (1968). Studies in locomotion and anatomy of scombroid fishes. Mem. South. Calilf.Acad. Sci. 6, 31 pp. Findley, J. S., Studier, E. H., and Wilson, D. E. (1972).Morphological properties ofbat wing. J. Mammal. 53, 429-444. Gooding, R. M., and Neill, W. H. (1978). Routine respiration rate and resistance to low oxygen levels in skipjack tuna, Katsuwonus pelamis. Natl. Mar. Fisheries Serv., Biol. Lab., Honolulu. Gray, J. (1968). “Animal Locomotion.” Clowes, London. Greenwalt, C. H. (1975). The flight of birds. Trans. Am. Philos. SOC.65(4), 1-67. Hall, F. G. (1930).The ability of the common mackerel and certain other marine fishes to remove dissolved oxygen from sea water. Am. J. Physiol. 93, 417-421. Harris, J. E. (1936). The role of the fins in the equilibrium of the swimming fish. I. Wind-tunnel tests on a model ofMustelus canis (Mitchell).J. E x p . Biol. 15,32-47. Hartman, F. A. (1961). Some locomotor mechanisms of birds. Smithson. Misc. Collect. 143(1), 1-91. Hertel, H. (1%6). “Structure-Form-Movement,” 1st Engl. Ed. Reinhold, New York. Hoerner, S. F. (1965). “Fluid Dynamic Drag.” Hoerner, Midland Park, New Jersey. Hopkins, E. J. (1951).Lift, pitching moment, and span load characteristics of wings at low speed as affected by variations of sweep and aspect ratio. Natl. Adu. Comm. Aeronaut., Tech. Notes No. 2284. Hunter, J. H., and Zweifel, J. R. (1971). Swimming speed, tail beat frequency, tail beat amplitude, and size in jack mackerel, Trachurus symmetricus, and other fishes. U . S . Fish Wildl. Sera, Fish. Bull. 69, 253-266. James, E. C. (1975).Lifting-line theory for an unsteady wing as a singular perturbation prob1em.J. Fluid Mech. 70, 753-771. Jones, F. R. H. (1957).The swimbladder. In “The Physiology of Fishes” (M. E. Brown, ed.), Vol. 2, pp. 305-322. Academic Press, New York. Gamer, E. (1960). Zur Form und Funktion des Locomotionapparates der Fische. Z. Wiss. Zool. 163, 1-36. Laurs, R. M., Yuen, H. S. H., and Johnson, J. H. (1977). Small-scale movements of albacore, Thunnus alalunga, in relation to ocean features as indicated by ultrasonic tracking and oceanographic sampling. Fish. Bull. 75,347-355. Lighthill, M. J. (1969).Hydromechanics of aquatic animal propulsion. Annu. Reo. Fluid Mech. 1,413-466. Lighthill, M. J. ( 1970).Aquatic animal propulsion of high hydromechanical ei3ciency.J. Fluid Mech. 44, 265-301. Lighthill, M . J. (1974). Aerodynamic aspects of animal flight. BHRA Fluid Eng. pp. 1-30. Lighthill, M. J. (1975). “Mathematical biofluiddynamics.” Soc. Ind. and Appl. Math., Philadelphia, Pennsylvania. Lissaman, P. B. S., and Shollenberger, C. A. (1970). Formation flight of birds. Science 168, 103-105. Logvinovich, G. V. (1970).Hydrodynamics of a thin, flexible body (evaluation of hydrodynamics of fish). In “Hydrodynamic Problems of Bionics,” Bionika, Vol. 4. Kiev. (Transl. from Russ.), JPRS 52605, pp. 4-11. Natl. Tech. Inf. Serv., Springfield, Virginia, 1971.) Lowndes, A. G. (1955). Density of fishes. Some notes on the swimming of fish to be correlated with density, sinking factor and load carried. Ann. Mag., Nat. Hist. 12(8), 241-256.


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MacKay, K. T. (1976). Population biology and aspects of energy use of the northern population of Atlantic mackerel, Scomber scombrus L. Ph.D. thesis, Dalhousie University, Halifax, Nova Scotia, Canada. Magnan, A. ( 1929). Les caracteristiques geometriques et physiques des poissons. Ann. Sci. Nut., Zool. 10(12), 5-133. Magnuson, J. J. (1963).Tuna behavior and physiology, a review. FA0 (FA0 U N ) Fish. Rep. 3(6), 1057-1066. Magnuson, J . J. (1966).Continuous locomotion in scombrid fishes. Am. Zool. 6(4), 5. Magnuson, J. J . (1969). Swimming activity of the scombroid fish Euthynnus afinis as related to search for food. FA0 (FA0 U N ) Fish. Rep. 62(2), 439-451. Magnuson, J. J. (1970).Hydrostatic equilibrium of Euthynnus afinis, a pelagic teleost without a gas bladder. Copeia pp. 5G85. Magnuson, J . J. (1973).Comparative study of adaptations for continuous swimming and hydrostatic equilibrium of scombroid and xiphoid fishes. U S . Fish Wildl. Seru., Fish. Bull. 71, 337-356. Magnuson, J. J., and Prescott, J . H. (1966).Courtship, locomotion, feeding, and miscellaneous behaviour of Pacific bonito (Sarda chiliensis).Anim. Behau. 14,54-67. Magnuson, J. J . , and Weininger, D. (1978). Estimation of minimum sustained speeds and associated body drag on scombrids. In “The Physiological Ecology of Tunas” (G. D. Sharp and A. E. Dizon, eds.). Academic Press, New York. Marshall, N. B. (1965).“The Life of Fishes.” Weidenfeld & Nicolson, London. Muir, B. S. (1969).Gill dimensions as a function of fish si2e.J. Fish. Res. Board Can. 26, 165-170. Muir, B. S., and Brown, C. E. (1971). Effects of blood pathway on the blood-pressure drop in fish gills, with special reference to tunas.J. Fish. Res. Board Can. 28, 947-955. Muir, B. S., and Hughes, G. M. (1969).Gill dimensions for three species of tunny.J. E x p . Biol. 51, 271-285. Muir, B. S., and Kendall, J. I. (1968).Structural modifications in gills of tunas and some other oceanic fishes. Copeia pp. 388-398. Muir, B. S., and Newcombe, C. P. (1974). Laboratory observations on filter feeding in Atlantic mackerel, Scomber scombrus. Marine Ecology Laboratory, Dartmouth, Nova Scotia (cited in MacKay, 1976). Munk, M. M. (1924). The aerodynamic forces on airship hulls. Natl. Ado. Comm. Aeronaut., Rep. No. 184. Neill, W. H., Chang, R. K., and Dizon, A. E. (1976).Magnitude and ecological implications of thermal inertia in skipjack tuna, Katsutoonus pelamis (Linnaeus).Eno. Biol. Fish. 1, 61-80. Nursall, J. R. (1956). The lateral musculature and the swimming of fish. Proc. Zool. Soc. London ( B ) 126, 127-143. Nursall, J. R. (1958).The caudal fin as a hydrofoil. Evolution 12, 116-120. Perkins, C. D., and Hage, R. E. (1949).“Airplane Performance Stability and Control.” Wiley, New York. Prandtl, L., and Tietjens, 0. G. (1934).“Applied Hydro- and Aeromechanics.” Dover, New York. (New Ed., 1957.) Pyatetskiy, V. Y. (19704. Kinematic swimming characteristics of some fast marine fish. In “Hydrodynamic Problems of Bionics,” Bionika, Vol. 4. Kiev. (Transl. from Russ., TPRS 52605, pp. 12-23. Natl. Tech. Inf. Serv., Springfield, Virginia, 1971.) Pyatetskiy, V. Y. (1970b). Hydrodynamic swimming characteristics of some fast marine fish. In “Hydrodynamic Problems of Bionics,” Bionika, Vol. 4. Kiev. (Transl. from Russ., JPRS 52605, pp. 24-31. Natl. Tech. Inf. Serv., Springfield, Virginia, 1971.)

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Rayner, M. D., and Keenan, M. J. (1967). Role of red and white muscles in the swimming of skipjack tuna. Nature (London) 214, 392-393. Richardson, E. G. (1936).The physical aspects offish locomotion.]. Exp. Biol. 13,63-74. Roberts, J. L. (1975). Active branchial and ram gill ventilation in fishes. Biol. Bull. (Woods Hole, Mass.) 148, 85-105. Rosen, M. W. (1961). Experiments with swimming fish and dolphins. Am. Soc. Mech. Eng. Publ. No. NWA 203, pp. 1-11. Rosen, M. W., and Cornford, N. E. (1971).Fluid friction of fish slimes.Natur-e (London) 234, 49-51. Seireg, A., Baz, A., and Patel, D. (1971). Supportive forces on the human body during underwater activities. J . Biomech. 4, 23-30. Sharp, G. D., and Francis, R. C. (1976).An energetics model for the exploited yellowfin tuna, Thunnus albacares, population in the Eastern Pacific Ocean. U.S. Fish Wildl. Seru., Fish. Bull. 74, 3 6 5 0 . Shebalov, A. M. (1969). Some questions of the influence of non-stationarity on the “mechanism” of resistance formation. Bionika 3, 61-66 (cited in Aleyev, 1977). Stevens, E. D. (1972). Some aspects of gas exchange in tuna. J . E x p . Biol. 56,809-823. Stevens, E. D., and Fry, F. E. J . (1972).The effect of changes in ambient temperature on spontaneous activity in skipjack tuna. Comp. Biochem. Physiol. A 42,803-805. Storer, J. H. (1948). The flight of birds analyzed through slow motion photography. Cranbrook Inst. Sci. Bull. 28, 1-94. Strasburg, D. W. (1961). Diving behavior of Hawaiian skipjack tuna. J. Cons., Cons. Perm. Int. Explor. Mer 26, 223-229. Sverdrup, H. U., Johnson, M. W., and Fleming, R. H. (1942).“The Oceans, their Physics, Chemistry, and General Biology.” Prentice-Hall, New York. van Olst, J. C., and Hunter, J. R. (1970).Some aspects of the organization of fish schools. J. Fish. Res. Board Can. 27, 1225-1238. von Khrmhn, T. (1954).“Aerodynamics.” McGraw-Hill, New York. von Mises, R. (1945).“Theory of Flight.” Dover, New York. (New Ed., 1959.) Walters, V. (1962).Body form and swimming performance in the scombroid fishes. Am. 2001.2, 143-149. Walters, V. (1966).On the dynamics of filter-feeding by the wavyback skipjack (Euthynnus afinis). Bull. Mar. Sci. 16, 209-221. Walters, V., and Fierstine, H. L. (1964).Measurements of swimming speeds of yellowfin tuna and wahoo. Nature (London) 202,203-209. Watanabe, N. (1942). A determination of the bodily density, body temperature, and swimming speed of the skipjack (Katsuwonus pelamis). Nippon Suisan Gakkaishi 11, 146148. Webb, P. W. (1975). Hydrodynamics and energetics of fish propulsion. Bull. No. 190. Dep. Environ., Fish., Mar. Serv., Ottawa. Weihs, D. (1973a). Hydromechanics of fish schooling. Nature (London) 241,290-291. Weihs, D. (1973b). Mechanically efficient swimming techniques for fish with negative buoyancy. J. Mar. Res. 31, 194-209. Weihs, D. ( 1 9 7 3 ~ )Optimal . fish cruising speed. Nature (London) 245,48-50. Weihs, D. (1974). Energetic advantages of burst swimming of fish. J. Theor. Biol. 48, 215-229. Weihs, D. (1975).Some hydromechanical aspects of fish schooling. In “Swimming and Flying in Nature” (T. Y. T. Wu, C. J. Brokaw, and C. Brennin, eds.), Vol. 2, pp. 703-718. Plenum, New York. Wu, T. Y. (1961).Swimming of a waving plate. J . Fluid Mech. 10, 321-344.

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Wu, T. Y. (1971). Hydromechanics of swimming of fishes and cetaceans. Adu. Appl. Mech. 11, 1-63. Yuen, H. S. H. (1962). Schooling behavior within aggregations composed of yellowfin and skipjack tuna. FA0 (FA0 U N ) Fish. Rep. 6(3), 1419-1429. Yuen, H. S. H. (1966). Swimming speeds of yellowfin and skipjack tuna. Trans. Am. Fish. SOC. 95, 203-209. Yuen, H. S. H. (1970). Behavior of skipjack tuna, Katsuwonus pelamis, as determined by tracking with ultrasonic devices.]. Fish. Res. Board Can. 27, 2071-2079. Zuyev, G . V., and Belyayev, V. V. (1970). An experimental study of the swimming of fish in groups as exemplified by the horsemackerel (Trachurus mediterraneus ponticus Aleev). J . Zchthyol. (USSR) 10, 545-549.


5 BODY TEMPERATURE RELATIONS OF TUNAS. ESPECIALLY SKIPJACK E . DON STEVENS and WILLIAM H . NEILL

I . Introduction .................................................. I1. History ...................................................... I11 . What Is the Real (i.e., Typical) Excess Body Temperature

ofTunas? .................................................... A . The Problem and a Definition of Excess Temperature ....... B . Effect of Captivity on Excess Temperature .................. C . Effect of Activity on Excess Temperature ................... IV. What Is the Heat Source Responsible for Large Excess Body Temperatures in Tunas? ................................. V. Anatomical Basis of Warm-Bodiedness in Tunas ................. A . Introduction .............................................. B. Role of Vascular Anatomy in Tuna Systematics .............. C . Systematic Distribution of Retia in Tunas ................... VI . Exchange of Heat between Tunas and Their Environment ....... A . The Rate of Change of Core Temperature ................... B. Relative Heat Exchange via Gills and Body Surface ......... C . Estimates of Effectiveness for Heat Exchange ............... VII . Do Tunas Regulate Their Body Temperature? .................. A . Regulation of Heat Gain ................................... B. Regulation of Heat Loss ................................... C . Long-Term Temperature Responses or Thermoregulation? . . . VIII . Adaptive Values of Warm-Bodiedness and Large Thermal Inertia .............................................. A . Increased Muscle Power at Elevated Temperatures ......... B. Decreased Time between Bouts of Burst Activity at Elevated Temperatures .................................... C . Benefits Accruing from Body Temperature Stability ......... D . Perception of Weak Horizontal Temperature Gradients ...... E . Retia Function to Retard Mass Transfer Rather than Heat Transfer ............................................. IX. Physiological Insights into the Natural History of Tunas ......... X . Conclusion: A Thermocentric Overview of Tuna Evolution . . . . . . References .........................................................

316 317 319 319 319 320 321 325 325 326 328 334 334 338 338 340 341 344 346 348 349 350 350 352 353 353 354 356

315 FISH PHYSIOLOGY. VOL . VII Copyright @ I 1978 by Academic Press. Inc . All rights of reproduction in any form reserved. ISBN 012-350407-4

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I. INTRODUCTION There is only one existing review of tuna autecology (Magnuson,

1963); it is concerned mostly with behavior and a list of what, in 1963, was unknown about tuna physiology. In fact, papers on tuna physiology (that is, those based on experimental work with live fish) probably still number less than thirty. One might then ask, “Why devote a chapter exclusively to tunas when there are 1000 times more published pages on salmonids?” For those of us who have -had the privilege of working with these animals, the answer comes quicklytunas are unique in many interesting ways. They are the fastest swimmers, among the largest of fishes, have the warmest bodies, have the highest metabolic rates, and are exceptional in many biochemical respects (unique hemoglobins; lactate, glycogen, actomyosin concentrations highest). Indeed, tunas are such extraordinary fishes that the tuna researcher frequently finds himself dividing all fishes simply into tunas and “nontunas”-a practice into which we slip in the pages that follow. The same attributes that so perfectly attune tunas to their continuously active existence in the pelagic zone of the high seas unfortunately make for serious logistical difficulties in carrying out research on captive subjects. A tank, even of oceanarium size, is a confining and otherwise alien environment for tunas. Some of the problems inherent in working with tunas recently have been overcome at the Kewalo research facility of the National Marine Fisheries Service in Honolulu, the only site in the world where tunas are routinely kept in captivity. Thus, many of the data and ideas offered in this chapter had their origins in work at the Honolulu laboratory; however, we have also drawn freely on other work, especially that of Frank Carey and his associates at Woods Hole Oceanographic Institution. The focal point of this paper is the issue of tunas’ body temperatures and their relation to activity and metabolism. Central to the construct “tuna” is warm-bodiedness: Tunas’ core tissues, especially the propulsive musculature, may be 20°C warmer than the surrounding seawater. Although the fact that tunas are warm has been known since at least 1835, the “how” and “why” of warm-bodiedness are only now yielding to experimental attack. Thus, much of the following information is a necessarily sketchy and tentative preview of work yet to appear in print. To the authors and sponsors of that work, we are sincerely grateful.

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317

11. HISTORY Eschricht and Muller (1835)provided an early account of the unusual ,circulatory anatomy of tunas and excellent descriptions of some of these fishes’ vascular devices that have come to be regarded as countercurrent heat exchangers. At about the same time Davy (1835), a British physician who voyaged in the tropics, reported that tunas had warmer bodies than nontunas caught from the same waters. H e observed that skipjack tuna (Katsuwonus pelamis) were as much as 10°C warmer than the water from which they were caught. That is, tunas are significantly warm-bodied. The next major report was a beautiful monograph on the anatomy of the scombroids by Kishinouye (1923). In it he described the location and extent of the vascular countercurrent heat exchangers and drew attention to their possible relationship with activity and warmbodiedness: “The higher temperature of the body than surrounding water, and consequently great activity of fishes of the Plecostei is undoubtedly due to the peculiar circulatory systems” (p. 367). Subsequent temperature measurements, especially by Japanese and Russian workers, failed to confirm that tunas in fact d o have high body temperatures. Most of these studies were based on a few observations. However, an extensive report of tuna body temperatures over a wide range of sea temperatures showed a maximum excess muscle temperature of only 3°C in skipjack tuna (Uda, 1941).That is, tunas are not especially warm-bodied. These workers were hampered by the usual problems of working with large, active fish at sea and by the additional difficulty of making their measurements with mercury thermometers. The first observations made with an electronic thermometer on muscle temperatures of freshly caught tunas are those reported by Barrett and Hester (1964) for skipjack and yellowfin (Thunnus albacares). In 20°C water, skipjack muscle was on the average 8°C warmer than the water, and in some fish it was as much as 11°C warmer (Fig. 1B). The excess was smaller in fish taken from warmer waters and was smaller in smaller fish. Shortly thereafter, Carey and Teal (1969b) reported large excesses achieved by giant bluefin tuna (T. thynnus) swimming in cold water (Fig. 1A). That is, tunas are very warmbodied. The observation that excess was much larger in bluefin caught from cold water than in those from warm water was taken to indicate that these fish possess the capacity to regulate their body temperature.

E. DON STEVENS AND WILLIAM H. NEILL I

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Fig. 1. Maximum red muscle temperatures of bluefin tuna (Carey, 1976 personal communication) and skipjack tuna ( x from Barrett and Hester, 1964; 0 from Stevens and Fry, 1971).

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319

Subsequent measurements of temperature in freshly caught tunas (Stevens and Fry, 1971; Graham, 1973, 1975) have confirmed that tunas are indeed several degrees warmer than the water from which they are caught. However, reflection on these data has suggested a number of interpretative problems, not the least of which is the effect of precapture activity on the magnitude of the core temperature excess.

111. WHAT IS THE REAL (i.e., TYPICAL) EXCESS BODY TEMPERATURE OF TUNAS? A. The Problem and a Definition of Excess Temperature Tunas undoubtedly have higher excess muscle temperatures than nontunas of the same weight caught from water of the same temperature. However, the typical magnitude of the excess is still in question; the problem is that many of the large values mentioned above were obtained from fish that may have been hyperactive just prior to their capture. Throughout the discussion that follows, T , refers to ambient water temperature, Tb to body temperature, and T , to excess body temperature, or Tb - T,. In steady-state conditions with respectto T,, T , is the result of a combination of factors that affect the balance between metabolic heat production and heat loss to the environment.

B. Effect of Captivity on Excess Temperature Stevens and Fry (1971) observed that T , in skipjack tuna decreased from about 9.1"C at capture to 2"-4"C for the same group of fish during captivity (Fig. 2). In a long series of experiments, Neil1 et al. (1976) determined excess tissue temperatures of captive skipjack tuna and related them to a number of variables. In these experiments, the fish were lightly sedated and restrained in a water-filled trough. Excess tissue temperatures were described by the following set of regression equations: red muscle: white muscle: brain:

log T , = 0.1608 + 0.5800 log W - 0.000% log T , = 0.1110 0.6067 log W - 0.000% log( T , + 1) = -0.1724 + 0.0105 T ,

+

where W, wet weight (kg); T,, water temperature ("C); t, time fish had

320


SKIPIACK

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I

Fig. 2. The decrease in excess red muscle temperature in skipjack tuna following capture. (Adapted from Stevens and Fry, 1971.)

been restrained (min). Thus, excess temperature relations of red and white muscle were similar to each other but different from that of brain. Muscle T, depended on fish weight and restraint time, whereas brain T , depended only on ambient temperature. The dose of sedative was unrelated to T , in all three tissues. Point solutions for red muscle T , at t = 0 min are 0.85 and 2.99"C for fish weighing 0.4 and 3.5 kg, respectively. It is clear that excess temperature is lower in captive tuna. The next question is: "Is it lower because of lower activity levels in captivity?"

C. Effect of Activity on Excess Temperature Stevens and Fry (1971)exercised captive skipjack tuna strenuously for 30 min and effected a small increase in red muscle mean excess temperature-from 3.3"Cbefore chasing to 4.6"C after chasing. Neill et al. (1976) continuously monitored red muscle T , in free-swimming skipjack. Chasing the larger of two fish to exhaustion caused T , to increase from 2.3" before to 5.7"C after the exercise. Thus, neither Stevens and Fry (1971) nor Neill et al. (1976) were able to generate excesses comparable to those observed in ocean-caught fish, even through violent chasing to exhaustion. However, Dizon ( 1976personal communication) has recorded excess core temperatures greater than 8.5"Cin Euthynnus afinis that were in captivity for more than a year. He telemetered temperature data from fish in a large oceanarium. Muscle temperature increased rapidly (8.5"Cwithin a few minutes) when the fish were active during feeding. We doubt that wild skipjack tuna have excess core temperatures

5. BODY TEMPERATURE RELATIONS OF TUNAS

32 1

much different from those of equally active captive fish; but captive skipjack have not been stimulated to levels of activity as high as those attained by wild fish in feeding frenzy. Moreover, the observation that schools of skipjack tuna are highly variable in the extent to which frenzy feeding develops upon live-bait chumming (Yuen, 1959, 1966) suggests that variation in Tx's recorded in the field may be as much a function of activity and feeding motivation as of ambient temperature. Thus, we believe that the excess core temperature in wild skipjack is likely to be 1"-2"C per (kg)o,6except when extremely high metabolic rates are attained during a feeding frenzy or other violent activity. The effect of activity on core temperature appears to be different in bluefin tuna when compared to the response in skipjack tuna. Activity increases core temperature in skipjack tuna. Carey and Teal (1969b) have published evidence that exercise lowers core temperature in giant bluefin tuna. They found that core temperature of trap-caught fish (little activity because they were pursed up and shot in the head, usually in less than 5 min) was higher than in fish caught by hook and line (fought for 1 to 8 hr). Although the type of exercise produced by fighting on a hook and line is different from the exercise of chasing prey, there also may be a fundamental difference between bluefin and skipjack tunas related to size difference or to the type of retia (see Section V).

IV. WHAT IS THE HEAT SOURCE RESPONSIBLE FOR LARGE EXCESS BODY TEMPERATURES IN TUNAS? Skipjack tuna get much warmer during (or after) burst activity than they are during periods of routine activity. In typical fishes, white muscle produces much of the energy for burst activity (Rayner and Keenan, 1967), and it .is generally held that white muscle metabolizes anerobically. But anerobic metabolism in white muscle cannot produce enough heat to cause the very large temperature excesses observed in the muscle ofjust-caught tunas. If initial glycogen levels are high, say, 0.0131 g glycogen/g white muscle (mean of five highest values from Barrett and Connor, 1964), then instantaneous conversion of all the glycogen to lactate with all of the chemical energy appearing as heat would increase muscle temperature only 2.5"C! Yet in one group of skipjack w e observed white muscle excess of 8.6"C and red muscle excess of 9.1"C. So, where does the heat come from? Clearly, the major portion of the heat produced during burst swimming is aerobic. And most of aerobic heat production occurs in the red muscle. Histochemical and


322

electrophoretic studies show that the necessary enzymes are in high concentrations in red muscle, but in low cpncentrations or absent in white muscle. For example, 60% of the total cytochrome oxidase activity is present in red muscle in the eel even though red muscle constitutes only 13% of the total muscle (Malessa, 1969). Certainly, tuna white muscle possesses some ability to metabolize aerobically because Gordon (1968) was able to measure oxygen uptake from white muscle minces. But, red muscle-mince metabolism was 6 to 8 times that of white muscle. Because red muscle mass is one-sixth that of white muscle in tunas, red and white muscle make nearly equal contributions to total routine aerobic metabolism [assuming that Gordon's results are representative of routine metabolism-but see Neill et al. (1976)l. Values from Gordon for red muscle at 30°C are 1580 mm3 O2 g-' hr-1 (0.12 cal min-' g-'). For a body weight of 1 kg, that is, 1580mm3 X- 1 hr a hr 60min Y

1 cm3 x -4.7 cal 1000mm3 cm3

85.3g fish = 10.6 cal

min-' fish-'

Similarly, for white muscle (0.02 cal min-' g-'), aerobic metabolism in a 1-kg fish is 260mm3 x - 1 xx 4.7 x 574.7 = 11.7 cal min-' fish-' g hr 60 1000 The total contribution of red plus white muscle to aerobic metabolism, then, is 22.3 cal min-* fish-'. The value obtained from restrained skipjack is very similar: 25 cal min-' kg-' [mean of minimum values from six restrained skipjack (Stevens, 1972) 1. The value obtained from free-swimming skipjack is nearly identical. Gooding et al. (1976 personal communication) measured oxygen uptake from nine pairs of routinely active skipjack tuna. The mean of the nine pairs for the lowest (i.e., minimal activity) of four readings from each pair was 25.3 cal min-' kg-l. Thus oxygen uptake values determined from muscle minces, restrained fish, and free-swimming fish are similar. The values based on the muscle mince data must be slightly high because they neglect the contribution of tissues other than muscle to total metabolism. Tissues other than muscle contribute 2 5 4 5 % to the total metabolic rate for fishes swimming at speeds similar to those of routinely active skipjack tuna (Fry,1971). Neill et al. (1976) have estimated red muscle metabolism in freeswimming skipjack tuna based on measurements of red muscle temperature and the rate of cooling of red muscle. They reasoned that the rate of heat production is proportional to the product k, the coefficient

5.


323

of temperature change, and T,, the excess muscle temperature under steady-state conditions. For a l-kg fish the value was 0.051 cal min-' g-1 . From the above estimates we conclude that red muscle metabolism during routine swimming in skipjack tuna is between 0.05 and 0.12 cal min-I g-I. Maximum values of oxygen uptake for free-swimming skipjack tuna during heightened activity (immediately after capture from a frenzy-feeding school) corresponded to a metabolic rate of 113 cal min-I kg-' (median value of fourteen observations was 74 cal min-' kg-') (Neill, unpublished observations). These values are more than twice as great as those for any other fish under any condition (cf. Brett, 1972; Fry and Brett, 1974). It is likely that much of the increase in oxygen uptake during heightened activity is due to red muscle, and that white muscle aerobic metabolism remains at 11.7 cal min-' fish-'. Using the maximum value, then, red muscle metabolism during this time is

113 - 11.7 =

min fish

x - -fish - 1.19 cal min-l g-' red muscle 85.3g

or 10-20 times the routine value. Neill et al. (1976) estimated red muscle metabolism in vigorously chased, captive skipjack to be only 0.42 cal min-' g-l, based on measurements of T , and k . If all the energy appears as heat and no heat is lost, 1.19 cal min-' g-' is sufficient to increase red muscle temperature 1.5"C in 1min, or 15°C in 10 min [assuming heat capacity of skipjack red muscle is 0.8 cal g-' OC-' (cf. Slavin, 1964; Charm and Moody, 1966)l. Obviously, some of the heat is lost: Some is lost to the environment, and some is distributed to other tissues by circulation of the blood. I n fact, the actual course of the temperature rise in red muscle can be calculated by taking heat loss into account. The rate of temperature change in the red muscle is the difference between the rate of potential temperature increase d u e to metabolism, or 1.5"C min-' in the present case, and the rate of potential temperature decrease d u e to cooling, k (Trm- T,), where k is the coefficient of temperature change in "C rnin-' "C-' and T,, is red muscle temperature:

dt

= 1.5"C min-I - k ( T , - T , )

rearranging,

5% dt

+ kT,,

=

1.5 + kT,

324

E . DON STEVENS AND WILLIAM H . NEILL

But (as later shown)

i.e., red muscle warms or cools at a rate that depends on the difference between its equilibrium (T,) and actual ( T,,) temperature (Neill and Stevens, 1974). To find out the value of T, in the present case, we combined the preceding pair of equations to get

+ kT,,

k(Te - T,,)

kT,

= =

1.5 + kT, 1.5 + kT,

or,

T,

=

15 - + T,

k

The value of k for a point in the deep red muscle of a 2 k g skipjack is about 0.033"Cmiii-' "C-' (Neill et ul., 1976). Thus, T, is 45.45"Cabove ambient temperature! Of course, our fish will not get that hot; it will simply end its bout of burst activity as muscle temperature approaches the upper critical level (perhaps about 35°C). But let's see what does happen to the red muscle of this 2-kg fish during a 10 min period of burst swimming in water at 20°C:

gives

T,,

= T, -

[T, - T,,( 0) I e-kt

Assuming the fish's red muscle is 2.0"Cwarmer than the water at the start of burst swimming [i.e., T,,(O) = 22.0°C], T,, rises to 34.21"C after 10 min as shown in the tabulation below. T,, if no heat loss ("C)

Actual T,,

2 4 7 10

22.0 23.5 25.0 28.0 32.5 37.0

22.0 23.41 24.78 27.37 30.96 34.21

(x

P

t (min)

0 1

-

-

("C)

45.45 = T,)

5.


325

We conclude that aerobic metabolism occurring primarily in the red muscle reasonably accounts for the 10°C excess temperature measured in the muscle of skipjack tuna. This is probably also true for other tunas as well.

V. ANATOMICAL BASIS OF WARM-BODIEDNESS I N TUNAS A. Introduction Thus far, we have reviewed the evidence that tunas are warm (but not always extremely warm) and have explored the question of heat source, concluding that tunas are exceptional in their red muscle’s capacity for aerobic heat production. But, for any fish to be very warmbodied, more is required than heat production, even at the remarkedly high rates achieved by’ tunas. The difficulty, so eloquently described by Carey (1973), is that any heat produced in metabolically active tissues tends to be carried by the blood to the gills where it is lost to the water (for fish gills must be excellent exchangers of heat if they are to be effective exchangers of respiratory gases)-unless that heat is short-circuited, from the venous to arterial sides of the circulatory system, before it reaches the gills. This would appear to he exactly the function of certain retia mirabila (“wonderful nets”) found only in the tunas and fast-swimming sharks of the family Lamnidae. These retia are systems of parallel arterioles and venules in close contact; direction of blood flow in the arterioles is counter to that in the venules. The retia are so arranged in the circulatory system that their role as countercurrent heat exchangers has never beerl doubted; however, experimental verification of that function has been accomplished only recently. And the possibility that the retia exchange something other than heat remains unexamined. Before w e pursue physiological and ecological aspects of heat exchange in tunas, we first will review the special and diverse features of vascular anatomy that retard the flow of heat between the core tissues of tunas and their environment. To do so conveniently w e also must delve (although not deeply) into scombrid systematics and evolution. A discussion of the anatomy of the vascular system in different types of tunas is made difficult by the large number of names that have been employed to describe the same species. For example, Gibbs and Collette (1967) recognize only seven species within the genus Thunnus, but report that over 160 different scientific names have been

326


ascribedto the seven species. This problem has arisen because of the difficulty in maintaining and examining adequate collections ( 1000-lb tuna do not fit into the standard museum jar), and because many early workers held the erroneous opinion that the tunas were geographically limited rather than having, as most do, circumglobal distributions. Many workers have used the presence, location, and peculiarities of the vascular retia as important distinguishing characters in tuna systematics (Godsil and Holmberg, 1950). Nakamura (1965) has argued that it is more appropriate to base a taxonomic scheme on osteology. His contention is supported by the fact that cutaneous retia are also present in pelagic sharks (Bume, 1923; Carey and Teal, 1969a); such convergence indicates that vascular heat exchangers are evolutionarily quite plastic. The evolution of tunas may be characterized as a series of adaptations for very rapid swimming, both horizontally and vertically. The obvious features of tuna anatomy, physiology, and natural history certainly point in that direction. Although lamnid sharks, xiphoids, coryphaenids, and a number of carangids also can attain high burst speeds, tunas are exceptional in this regard. Scheme 1 summarizes important evolutionary developments for fast swimming in the family Scombridae. All of the Thunnini possess retia that presumably can act as countercurrent heat exchangers to reduce the rate of heat loss; none of the other tribes of Scombridae possess such devices. Still, our scheme is far from perfect. For example, loss of the gas bladder has occurred at more than one point in the scombrid line. Among the Spanish mackerels, Scomber scombrus lacks a gas bladder, whereas the chub mackerel, Scomber colias, has a well-developed gas bladder. Thunnus tonggol has only a rudimentary gas bladder.

B. Role of Vascular Anatomy in Tuna Systematics Vascular anatomy has been of importance in the systematics of tunas. Regan (1909) and Stark (1910), using the traditional classification characteristics of osteology, placed the tunas and mackerels in the single family Scombridae. Kishinouye ( 1915, 1917, 1923) recognized four separate families and placed the tunas in the order Plecostei, separate from all other higher bony fishes. His analysis was based in part on the extraordinary vascular anatomy of the tunas. His placement of tunas into a separate order has been followed by Berg (1955) and

5.


327

(1) streamlined body of fusiform shape; dorsal, anal, and pectoral fins retract into grooves (2) sickle-shaped caudal fin with high aspect-ratio; dorsal and anal finlets to reduce turbulence of water in path of the caudal fin (3) large muscle mass relative to body length (4) white and red muscle fibers segregated; white muscle with very high concentrations of contractile proteins and substrate for anaerobic metabolism. (The above features tend to be progressively developed through the family) \ SCOMBRINI (primitive mackerels) and SCOMBEROMORINI (Spanish mackerels) ( 5 ) complete, bony peduncular keel develops [vertically stabilizes caudal fin and acts as a pulley to permit more powerful pull by tendons on the caudal fin (see Fierstine and Walters, 1968)l 1 SARDINI (bonitos)

THUNNINI (advanced tunas) ~ T H U N N U S (7) gas bladder lost (permits rapid vertical movements) (8) squamation reduced to anterior corselet of fine scales (presumably reduces drag at high speeds) (9) metabolism becomes temperature-independent (or nearly so) K A T S U W O N U S E U T H Y N N U S AUXIS

I

Scheme 1

Morrow (1957), but .has been disputed by most systematists (Takahashi, 1926; Fraser-Brunner, 1950; Gibbs and Collette, 1967; Collette and Chao, 1975). Certainly one of the main features that distinguish the tunas from other fishes are their retia and cutaneous blood vessels. The location and type of vascular rete have also been used to distinguish between the various taxa of advanced tunas. Table I is not meant to be systematically complete but provides a useful scheme for comparing extent and locations of retia (based on Gibbs and Collette, 1967; Nakamura, 1965). The very large tunas tend to have cutaneous retia but no central exchangers, whereas small tunas have central retia but cutaneous retia are either small or ab'sent. Gibbs and Collette (1967) reviewed the gross anatomy of the lateral and central vascular sheets; Carey et al. (1971) reviewed the anatomy of the lateral and

328


central retia in relation to measurements of excess muscle temperature; and Graham (1975) has related anatomy and body temperature to aspects of the natural history of the various tunas (Table I).

C. Systematic Distribution of Retia in Tunas 1. CUTANEOUSRETIAL SYSTEMS Among all of the bony fishes, only the genera Thunnus, Euthynnus, Katsuwonus, and Auxis possess cutaneous arteries and veins. This is one feature that separates the tunas from their relatives, the bonitos and mackerels. The cutaneous system is very large in the bluefin tuna group (see Table I), and in fact is the major avenue of blood supply for the muscle. The relative unimportance of central blood supply is evidenced b y a reduced dorsal aorta and the absence of the postcardinal vein. In all of the other tunas the cutaneous system is present, but the dorsal aorta and the postcardinal vein are also well developed. The anterior dorsal aorta is not different from that of other fishes. It is formed by the union of the efferent branchial arteries and continues along the dorsal body wall to the hemal canal. Partially encircling the aorta at this point is a peculiar, small, almost transparent ligament found in all the tunas (Godsil, 1954). It runs posteriorly, passes ventral to the aorta, and just posterior to the coeliacomesenteric artery it turns forward again toward the occipital region on the opposite side. Its function is not known. The unpaired coeliacomesenteric artery always arises on the right side of the dorsal aorta beneath the third or fourth vertebra to supply the liver and viscera. The small subclavian arteries arise at about the same point on the dorsal aorta. The paired cutaneous arteries arise posterior to the origin of the coeliacomesenteric artery and course laterad through the kidney and body musculature. The point of origin of the cutaneous arteries differs among the tunas (Table I). Along their length, the cutaneous arteries give off arterioles so dense that they form a continuous sheet, the cutaneous rete, that runs into and nourishes the muscle. The cutaneous arteries also give rise to segmental arteries, one per segment, and, although the cutaneous segmental artery and vein parallel one another, there is no vascular plexus.

a. Bluefin Tuna Group. In the bluefin tuna group, the dorsal aorta is much reduced in size after emergence of the cutaneous arteries. The cutaneous artery on each side forms two branches (hypaxial and epaxial) that run parallel. The branches are united caudally by a posterior commissure in all species of Thunnus except albacore and sometimes

Table I Specific Differences in the Heat Exchange Retia of Tunas: Family Scombridae, Tribe Thunnini" Cutaneous retia

Maximum

Bluefin group Thtrnnrrs thynnrrs

Common name

size (kg)

Bluefin tuna

730

Habitat

Retia

Vertebra number at which cutaneous artery originates

Number of rows of arterioles from cutaneous artery

Large ( 10 mm thick) Large

3-4

2

44

Migrates 6"-20"c Cool water

%4

1, Mesial side

Central rete

Visceral retia

Postcardinal vein

Central rete

Large retia on liver and gut Large retia on liver and gut Large retia on liver and gut

None

Thtrnnes altrlrrnga

Albacore

Thrrnnirs maccoyii

Southern bluefin tuna

225

Cool water

Large

%4

2

Bigeye tnna

198

Cooler water than yellowfin

Small (2-5 mm

6 8

2

Small retia

None

Very small (2-5 mm thick) Very small Very samll

6 8

1, Lateral

Arteriolar reticiilar network surrounds hepatic portal vein

6 8 6 8

Two central retia; total smaller than skipjack

1. Lateral Arteriolar reticular network surrounds hepatic portal vein

Largest

Intermediate Tlitcnntrs obestis

Yellowfin group Thunntrr albacores

Yellowfin tuna

200

Tropical

Blackfin hina Lnngtail tuna

16

27

Tropical Tropical

Skipjack tnna

22

Tropical

Etrthynnus afinis

Kawakawa

18

Tropical

Etrthynntrs lineattrs

Black skipjack

5

Tropical

Etrthynnus alletterotrrs

Atlantic

5

Tropical

Atrxis thaiard

Frigate mackerel

2

Tropical

Thrrnntts atlantictrs Thrtnnus tonggol Skipjack group Katsrriconis pelamis

None None

thick)

Small (1 mm thick) Small, expaxial rete only Small, expaxial rete only Small, expaxial rete only Small, expaxial rete only

5

1, Lateral

2 1 1

Large Large Large

6

Data from Gibbs and Collette (1967);Goadby (1972): Gndsil and Byers (1944); Graham (1975); Magnuson (1963); Nakamura (1965);Collette and Chao (1975).

Large

330


bigeye. In a large bluefin tuna, the capillary sheet of the retia can be as much as 1cm thick (Carey and Teal, 1969b).The vessels that make up the rete are about 0.1 mm in diameter. Vascular bands of alternating arterioles and venules as much as sixty vessels wide (1-4 mm) but only a single layer thick branch from the rete and penetrate the muscle. The vascular bands divide into triads (arte,riole-venule-arteriole) that eventually nourish the muscle. The vascular bands from the rete are the main blood supply for the red muscle. There is only one segmental branch from each cutaneous artery per body segment; the branch from the epaxial runs dorsad and that from the hypaxial runs ventrad. The segmentals give rise to smaller vascular bands, about twenty vessels wide and a single vessel layer thick. These bands also divided into triads (arteriole-venule-arteriole) that eventually provide the main blood supply to the white muscle.

b. Yellowfin Tuna Group. Thunnus albacares is unique in that it has large parallel trunks connecting posterior epibranchial and cutaneous arteries on each side. Thus blood enters the cutaneous artery from both this branch and via the dorsal aorta. The alternate avenues may be involved in the control of the distribution of blood, but this bypass is unique to this species. Other aspects of the cutaneous system are similar to those of the bluefin group except that the lateral rete is not quite as thick (does not contain as many vessels). The vessels in the rete and in the segmental vascular bands are similar in size to those in the bluefin tuna group. c. Skipjack Group. Katsuwonus, Euthynnus, and Auxis have in common the fact that the ventral branch of the cutaneous artery is short and dendritic, and does not form a vascular plexus. The cutaneous system of skipjack differs from that of all the other tunas in many respects. Only in the skipjack do the cutaneous arteries divide before reaching the ribs. The arterioles and venules are sparse and more erratic in course and origin than in other tunas. The dorsal and ventral cutaneous veins do not fuse anteriorly; they empty directly into the duct of Cuvier rather than into the postcardinal vein as in the case of all other species. In Euthynnus, the dorsal cutaneous artery runs the length of the body. It gives rise to dorsal and ventral segmental arteries that do not form vascular plexuses, but do run adherent to segmental veins. It also gives rise to a single row of arterioles that form the capillary sheet of the cutaneous rete. Euthynnus is also unique in that the dorsal cutaneous artery is always dorsal and adherent to the dorsal cutaneous vein. In Auxis, the dorsal branch of the cutaneous artery does form a


33 1

rete-the artery is ventral to the vein and has one row of arterioles which form the rete; the vein has two rows of venules that pass to either side of the artery and into the rete. The dorsal segmental branches of the cutaneous artery are large, but the ventral branches are smaller and form superficial capillary strands.

2. VISCERALRETIA Carey et al. (1971) measured visceral temperature in tunas and found it varied; temperatures ranged from as high as those of the warmest muscle to slightly above that of ambient water. High visceral temperatures probably speed digestion and absorption, thereby compensating for the small size of the gut in tunas. a. Bluefin Tuna Group. The bluefin group of the genus Thunnus (Table I) is characterized by having large, complex retia on the liver and gut; these retia were first described (and beautifully illustrated) by Eschricht and Muller (1835).The branches of the coeliacomesenteric artery, upon reaching the liver, give off myriads of minute vessels that ramify in the lobes of the liver so that a transverse section of the liver of an injected specimen resembles the cross section of a rope. After passing through the liver the vessels pass into other retia dorsal to the liver in the form of large cone-shaped, vascular masses and then to the gut. The above also applies to the venous circulation. In a large bluefin, one of these liver retia may be as much as 5 cm in diameter.

b. Bigeye Tuna. There is a slight retial system associated with the liver in the bigeye tuna. c . Yellowfin and Skipjack Groups. In these tunas, the branches of the coeliacomesenteric artery pass directly through the substance of the liver without any plexus formation. The liver is nourished by a few discrete branches. Although there are no retia as in the bluefin, some branches of the coeliacomesenteric invariably become dispersed into a complex, fine network that completely envelopes that portion of the hepatic portal vein with which it is associated (Godsil, 1954; Godsil and Byers, 1944). 3. RETIA NEARTHE BRAINAND EYES Brain and eyes of all tunas yet examined are considerably warmer than ambient water but are not as warm as muscle (Table 11).Linthicum and Carey (1972) observed e y e and brain Tx’s of 16°C in two bluefin specimens taken from 7°C water. Heat is produced by the brain and eyes and is retained by the operation of the retia. The only

332


Table I1 Brain, Eye, and Muscle Temperature Excesses in Tunas"

Species

Thunnus thynnus Thunnus thynnus Thunnus alalunga Thunnus obesus Katsuwonus pelamis Euthynnus afinis Euthynnus alletteratur

Weight (kg)

180-400 6-12

2 2

Water temperaturd

Temperature excess ("C)

("C)

Brain

Eye

21.0 21.7 17.8 19.2 26.1 25.0 18.1

6.1 5.1 4.2 5.5 3.9 3.7 7.5

6.1 3.4

8.8

4.3 4.8

13.2 9.7

-

6.3

Muscle

9.2

8.8 4.8

11.7

Referenceb

1 1 1 1 2 2 1

In nontunas the excess is usually less than 0.5"C.

* 1, Linthicum and Carey (1972); 2, Stevens and Fry (1971). anatomical description of the retia supplying the brain and eyes is given by Linthicum and Carey (1972) for Thunnus, and the following is based on their account. The vascular exchangers (one on each side) in the brain of bluefin and albacore are located dorsal and anterior to the first efferent branchial arteries and are closely applied to the ventral surface of the prootic bone. The major source of blood is the carotid arteries; the opercular artery makes a smaller contribution. The external carotid gives off many small branches that contribute to the rete. The carotid retia are not as well developed in bigeye and yellowfin. The main vessels supplying the retia in the bigeye tuna are the external carotid arteries. In the yellowfin, branches of the external carotids pass through most of the retia before breaking up into small vessels; the opercular artery is more important than the carotids in supplying the retia. In all species so far examined the veins of the retia are arranged concentrically around the arteries. The arterioles in the rete are 80-120 pm in diameter with thick muscular walls; the venules are 40-150 pm in diameter. Linthicum and Carey (1972) pointed out the possibility of regulating brain temperature by regulating the proportions of blood flowing via alternate routes. They reported that the excess brain temperature of bluefin caught in cold water (T, = 7°C) was 16"C, whereas that of fish caught in warm water (T, = 23°C) was only 4.5"C. Although short-term regulation has not been demonstrated, avenues of blood flow are present that would constitute a partial bypass of the rete.

5 . BODY TEMPERATURE RELATIONS OF TUNAS

333

4. THE CENTRALRETE The central rete is best developed in species with the least developed cutaneous retia and is completely absent in the bluefin tuna group, which has the most elaborate lateral retia system.

a. Bluefin Group and Bigeye Tuna. In these tunas the central rete is completely absent. In the bluefin group the postcardinal vein is absent and the dorsal aorta becomes very small posterior to the point at which the cutaneous arteries branch. In the bigeye tuna, a small postcardinal vein is present.

b. Yellowfin Group. The central rete is small and forms as two capillary sheets about 1 mm thick, one on either side of the dorsal aorta. c. Skipjack Group. In Euthynnus lineatus the venules in the central rete do not branch into smaller vessels (Godsil, 1954), but are surrounded by a mass of arterioles. The extent of branching and size of the retial vessels in the other Euthynnus species and Auxis are unknown. The central rete is best developed in Katsuwonus (Stevens et al., 1974). Cool arterial blood passes from the dorsal aorta through the central rete and then to segmental arteries. Warm venous blood from the tissues collects in segmental veins and then passes throhgh the rete to the postcardinal vein. In a 2 k g skipjack the rete is about 7 mm wide and the exchanger vessels are 10 mm long. The arterial vessels in the rete are approximately the same diameter as arterioles and so are referred to as arterioles. These vessels are thick walled and contain smooth muscle but are not innervated. The retial arteriples unite into collecting vessels at the top of the rete, and the collecting vessels become segmental vessels. (Figs. 3, 4,and 5). At the top of the rete, segmental veins divide to become collecting veins that are thin walled and invariably contain regularly spaced protuberances which look like incomplete septa. These protuberances probably act as valves to prevent backflow due to the high resistance offered by the venules in the rete. The collecting veins divide repeatedly to form the venules of the rete. Venous blood, after passing through the rete, collects and passes around the dorsal aorta to empty into the postcardinal vein. The number of arterioles is very nearly equal to the number of venules in the rete, but the venules are much larger. Numbers and dimensions of central rete vessels in a 1.9kg skipjack tuna examined by Stevens et al. (1974) are shown in the following tabulation.

334


Number of vessels Internal diameter (pm) Cross-sectioned area (cmz) Volume (cm3) Inside surface area (em')

Arterioles

Venules

133,721 35.7 f 1.32 1.34 1.21 1350

120,652 83.82 4.47 6.65 5.99 2858

The presence of the rete reduces the velocity of blood flow in the rete arterioles to 1/80 of that in the dorsal aorta, that in the rete venules to l/so of that in the postcardinal vein. The rete vessels contain about 5% of the total blood volume. VI. EXCHANGE OF HEAT BETWEEN TUNAS AND THEIR ENVIRONMENT

A. The Rate of Change of Core Temperature The observations by Stevens and Fry (1971)showed that the large excess temperatures observed in immediately sampled, ocean-caught tuna decreased to about one-half within 20 min after capture (for dead

Fig. 3. Schematic drawing illustrating the features of the vascular heat exchanger of skipjack tuna. DA, dorsal aorta; K, kidney; M, muscle; PCV, postcardinal vein; V, vertebra. Left inset shows pattern of arterial blood flow, right inset shows pattern of venous blood flow, and small arrows indicate heat transfer from venules to arterioles in the exchanger. (From Stevens et ul., 1974.)

5.


335

Fig. 4. (A) Cross section of a 2-kg skipjack tuna. The vascular heat exchanger is below the vertebral canal. Red muscle appears dark. (B) Tangential section ofthe vascular heat exchanger of a formalin-perfused skipjack tuna (that is, a cross section of the vessels of the exchanger). The number of thick-walled arterioles is about the same as the number of thin-walled veins. (C) Same section as (B) except that the tissue was fixed rather than perfused. Red blood cells (10 pm diameter) are evident and reveal the size of the vessels. The arterioles have thick, muscular walls, whereas the venules are thin walled. (From Stevens et ( I / . , 1974.)

336


-

Fig. 5. Cross section of skipjack hina showing - the vascular heat exchanger. ComDare with Fig. 3. Small vessels in the exchanger are about 1 cm long. (From Stevens et al., 1974.) ~~

skipjack in air) and to about one-third after a few days in captivity. Neil1 et al. (1976) have examined in detail the rate of change of core temperature as a function of changes in ambient temperature in restrairied skipjack tuna. In their experiments, tuna were subjected to

5.


337

5°C increases or decreases in T,, and tissue temperatures were continuously monitored until they ceased changing. Core temperatures of larger fish changed more slowly than those of small fish. The coefficient of temperature change, k, when plotted on double logarithmic axes against body weight, was linear with a slope of -0.45 for red muscle, white muscle, and brain (Fig. 6A). Brain cooled and warmed about 3.3 times as rapidly as muscle of the same fish, over the fish weight range of 0.1-3.5 kg. There was no difference between the rates the tissues cooled and the rates at which they warmed. Stevens and Fry (1974) have compiled coefficients of core temperature change for a variety of fishes and aquatic reptiles. Comparing k's of animals of equal weight, skipjack tuna come into steady state with a new water temperature only about 60%as rapidly as typical teleosts and even somewhat more slowly than aquatic reptiles (Neil1 et al., 1976; see also Fig. 6B). Considering that fishes must achieve respiratory exchange with water (which has much greater heat capacity and

1

0.20

0

O.

0.10-

t

- 0.06x

0.02'

' ' ' ' "' 0 4 0.6 1.0

'

'

2.0

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Body Weiqht (hq)

; 1.-

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o Turtle d

Marine lquana

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Fig. 6 . (A) Relation between fish weight and the coefficient of temperature change (k) in the red muscle, white muscle, and brain of the skipjack tuna. (B) Relation between skipjack body weight and red muscle k compared with that for other fishes and aquatic reptiles.

338


much less oxygen per unit volume than air), the observation that skipjack tuna change temperature more slowly than aquatic lung breathers is evidence of high efficiency in the skipjack's countercurrent heat exchanger.

B. Relative Heat Exchange via Gills and Body Surface Brill et al. (1978)have measured the rate of heat flow from the body surface in restrained skipjack tuna when ambient temperature was not changing. These results show that 10-40% of heat produced (estimated from oxygen uptake) was transferred through the skin. Furthermore, heat was transferred in a relatively uniform fashion across the body surface; that is, there were no areas where heat flow was exceptionally high or low. The rate of heat flow was related to the volume of muscle mass below the surface. The only area of significant heat loss in the head was the area over the eye. The rather uniform pattern of heat loss in skipjack contrasts sharply with that in Thunnus. Carey (1976 personal communication) measured heat loss in yellowfin, bigeye, and bluefin; all showed the same pattern: Heat loss varied by a factor of 2-4 around a fish's body and was highest in the region of the pectoral fin groove where probing with thermistors showed the steepest thermal gradients. The different patterns of heat loss in Thunnus, compared to the uniform heat loss in skipjack, is clearly related to the different positions of the heat exchangers in these fish. That 10-40% of the metabolic heat in skipjack tuna is transferred through the body surface is consistent with the findings of Neill et al. (1976). From their Fig. 7 it may be estimated that heat transfer between the environment and a point in the deep red muscle is partitioned between the gills and the general body surface 5 0 : 50% in a 0.5kg skipjack and 65: 35% in a 3.0-kg fish.

C. Estimates of Effectiveness for Heat Exchange

The effectiveness of the heat exchanger may be estimated by a number of different methods. Obviously it is highly effective because the rate of heat exchange in tuna is less than in nontunas (Figs. 6B and 11). Neill et al. (1976)have computed the efficiency of the skipjack tuna exchanger as a thermal barrier based on the following estimates and assumptions.

5.


339

1. Temperature excess of venous blood just before it reaches the gills is about 0.1 times that of red muscle (measured). 2. Arterial blood entering the heat exchanger has a negligibly small temperature excess (assumed). 3. Venous blood entering the heat exchanger has a temperature excess equal to that of red muscle (assumed). 4. Venous blood not passing through the exchanger has temperature excess equal to that of the body average excluding red muscle (=0.2 T, of red muscle, assumed). 5. Of venous blood in the bulbus arteriosus 60% has passed through the heat exchanger, and 40% has not (assumed by Stevens et al., 1974). 6. Changes in blood temperature during transit of large arteries and veins are negligibly small (assumed). Then 0.60(Txexchanger output blood) + 0.4O(Tx nonexchanger output blood) = O.l(T, red muscle), and 0.60(Tx exchanger output blood) = O.l(T, red muscle) - 0.4(0.2 x T , red muscle) = 0.O2(Tx red muscle). Therefore, T , exchanger output blood = 0.02/0.60 = 0.O3(Tx

Fig. 7.Record of a heat pulse applied to the water perfusing the gills of a restrained skipjack tuna. Note that the pulse is contained within the vascular compartment and appears in venous blood but does not change the tissue temperature. The change in blood temperature has a direct effect on the heart; its rate increases with an increase in temperature.

340


red muscle). That is, 97% of the heat is transferred from venous to arterial blood within the exchanger. If the 0.2 value in assumption (4) is, in fact, between 0.1 and 0.4, or if the 60% value in assumption (5) is, in fact, between 50 and loo%, then the efficiency of the exchanger still lies between 90 and 100%. We also have examined more directly the effectiveness of the heat exchanger as a thermal barrier by looking at what happens to a heat pulse within the vascular system of skipjack tuna (Fig. 7). A heat pulse applied to the water perfusing the gills is transferred to blood passing through the gills and appears in the dorsal aorta. The efficiency of the heat exchanger as a thermal barrier is revealed by the extent to which the temperature pulse is contained within the vascular compartment and not transferred to the tissues. Thus, if the exchanger were very efficient, the heat pulse should be transferred to venous blood in the exchanger (and not to the tissues) but will be reduced in magnitude because of dilution by blood not passing through the exchanger and of longer duration because of unequal path lengths within the circulatory system. In our experiments approximately 150 cal were put into a skipjack's dorsal aorta (assuming that the temperature of blood came into equilibrium with that of water) when perfusion-water temperature was increased 5°C for 15 sec. Muscle temperature was unaffected by the heat pulse. The heat pulse appeared in the ventral aorta in about 15 sec or about three times as fast as if it had traversed the entire vascular system. The temperature of the blood in the ventral aorta only increased 0.5"C; the rise persisted more than 15 sec due to unequal path lengths within the circulatory system. More important, 73-85% of the pulse did appear in the ventral aorta. That is, assuming that the exchanger effectiveness was loo%,73-85% of the blood flow passed through the exchanger. If exchanger effectiveness was only 95%,then 77-88% of the blood flow passed through the exchanger. There is no question that heat is exchanged very effectively in the rete and that a large fraction of the blood flows through the rete in skipjack tuna.

VII. DO TUNAS REGULATE THEIR BODY TEMPERATURE? Definitive experiments to demonstrate whether tunas do, in fact, acutely regulate body temperature have not been carried out. Thermoregulation implies regulation of either heat gain (metabolic rate), or heat loss, or both in order to achieve a specific body temperature or excess body temperature suited to a particular circumstance. It is our

341

5. BODY TEMPERATURE RELATIONS O F TUNAS

view that thennoregulation does not require that body temperature be indefinitely maintained at some absolute level. There is reasonable evidence that some tunas thermoregulate.

A. Regulation of Heat Gain 1. EFFECTOF AMBIENT TEMPERATURE ON ROUTINE OXYGENUPTAKE Tunas could, all other things being equal, elevate body temperature by increasing metabolic rate. If the object of the game is to maintain body temperature constant, then we would predict that tunas would elevate metabolic rate at lower ambient temperatures. Only one experiment of this type has been carried out with tuna (Chang et al., 1976). In this experiment pairs of skipjack tuna were placed in a large annular respirometer, and oxygen uptake was monitored during spontaneous activity at a variety of ambient temperatures. Over the range of temperatures tested, 18"-30"C, there was no significant effect of temperature on the rate of oxygen uptake during spontaneous activity (Fig. 8).We can conclude that skipjack tuna do not maintain body temperature by increasing heat production when ambient temper, ature is decreased. I n contrast with many other fishes, h o ~ e v e rthey 1

.

5

1.0-

'

~I

~,

,

,

,

,

,

,

,

I

0

.a .7-

0

0"

,

73

.9-

-0 -k

1

/

C

.6-

.sd

.4 16

'

1

18

'

1

20

I

'

22

1

'

24

1

"

26

'

28

1

I

Fig. 8. Oxygen uptake in free-swimming skipjack tuna at a variety of ambient water temperatures. Fish were acclimated to 25°C.

342


do maintain metabolic rate constant over a wide range of ambient temperatbes during routine activity. Since tunas swim continuously, the major site of metabolic demand (and, thus, the major source of heat production) is the red muscle mass used during routine swimming activity. It is not surprising, then, that swimming velocity is also independent of temperature. ON ROUTINE 2. EFFECT OF AMBIENTTEMPERATURE SWIMMING SPEED

Reports of swimming speed as a function of ambient temperature indicate that, at least in skipjack tuna, routine swimming speed is maintained constant independent of changes in ambient temperatures. Tunas swim continuously in order to maintain vertical position (they are negatively buoyant) and also to maintain an adequate water flow over the respiratory interface (they ram water over the gills rather than pump it). Standard metabolism is thus meaningless for these obligatory swimmers. So, experimental work has focused instead on routine spontaneous activity and associated metabolic demands. In a crude experiment, Stevens and Fry (1972) reported that routine swimming speed of skipjack tuna remained unchanged over a temperature range of 16"-25"C. Subsequent and more refined experiments by Dizon et al. (1976) have also shown that skipjack tuna swimming speed remains independent of temperature over a temperature range of 18"-30"C (Fig. 9A). Interestingly, Dizon et al. (1976) have shown that yellowfin tuna, Thunnus albacares, decrease their swimming velocity in response to decreases in temperature (Fig. 9B). Deductions regarding benefits derived by the skipjack through maintaining constant swimming velocity in the face of changing ambient temperatures are complicated by the fact that temperature change also causes changes in the characteristics of water. For example, when ambient temperature is decreased from 30" to 20°C there is a benefit to the tuna because oxygen solubility increases about 15%. At the same time, however, there is a 26% increase in the viscosity of seawater that causes a 12% increase in frictional drag (Brown and Muir, 1970; Webb, 1975).Because the benefit of the increase in oxygen solubility is offset by the increase in drag, the metabolic cost of respiration at any particular swimming speed remains unchanged. In addition, a change in body temperature may affect the efficiency with which chemical energy is converted to mechanical work in the muscles, and the effi-

5.

343

BODY TEMPERATURE RELATIONS OF TUNAS I

1.6

-

I

I

I

SKIPJACK TUNA 47.0 cm F.L.

1.4-

I

I

1

,

I

28 -

22

M

1

,

x)

100

I50

200

250

300

350

ELAPSED TIME (MINI

Fig. 9. Swimming speed in free-swimming skipjack and yellowfin tunas at a variety of ambient water temperatures. Fish were acclimated to 25°C.

ciency of converting mechanical work in swimming muscles to propelling power; neither of these efficiencies has been quantified for swimming tuna. In conclusion, metabolic rates at various temperatures have been determined only for skipjack tuna, in which metabolic rate during routine swimming activity is constant over a wide range of ambient temperatures. Routine swimming speed also is invariant over a wide range of ambient temperatures and probably accounts for the constancy of metabolic rate because muscular work constitutes the major energy expenditure. In another tuna, the yellowfin, routine swimming speed decreases when ambient temperature is lowered, and it is likely that there is a concomitant decrease in metabolic rate. There is no evidence that tunas increase heat production in response to a decrease in ambient temperature.

344


B. Regulation of Heat Loss Body temperature regulation could be achieved, even if there is no direct regulation of heat gain, by regulation of the rate of heat loss.

1. SKIPJACK TUNADO NOT REGULATETHE U T E O F HEATLOSS The rate of heat loss, or more exactly, the rate of cooling and warming, under a variety of experimental circumstances has been examined in detail in skipjack tuna by Neill et al. (1976; see also Section VI,A). The rate at which red and white muscle cooled was the same as the rate at which they warmed. Moreover, the rate of cooling and warming did not vary systematically with the level of ambient temperature. Therefore, skipjack tuna do not seem to regulate the rate ofheat loss in response to changes in ambient temperature.

2. THERMALINERTIA IN LARGETUNAS Carey and his associates have used telemetry techniques to make many observations of core and ambient temperatures in freeswimming giant bluefin tuna. On the basis of these observations they have argued that giant bluefin tuna encountering abrupt changes of ambient temperature are capable of rapid physiological thermoregulation in the same sense as mammals. Their evidence is that body temperature changes very little and very slowly when the fish swims into water of very different temperature. Neill and Stevens (1974) have offered a different interpretation of these telemetry data-i.e., the observed stability of body temperature in the face of changes in water temperature could reflect a constant but small k coupled with constant heat production. Neill and Stevens refer to this as thermal inertia, as opposed to physiological thermoregulation. The analysis by Neill and Stevens is based on the assumption that the process of heat exchange in large bluefin tuna can be described by the same relationships that appear to be valid for skipjack tuna. That is, the rate at which the fish warms or cools is proportional to the disequilibration temperature excess (T, - Tb):

where dTb/dt, change in body temperature ("C min-I); k, coefficient of temperature change ("Cmin-' "C-l);T,, equilibrium temperature, the body temperature that would ultimately obtain at any given ambient temperature; T , = T , T,. Neill et al. (1976) have shown that this model adequately describes the rate of cooling in skipjack tuna.

+

345


Neill and Stevens used the above model to simulate body temperature responses observed by Carey and Lawson (1973). For the analysis we assumed that the fish did not thermoregulate-i.e., did not alter heat gain or heat loss. Body temperatures predicted under the assumption of no physiological thermoregulation agreed very well with the observed body temperatures (Fig. 10).Thus it was possible to explain, in large part, the telemetry data by assuming that these tuna

. .. .. ........

9.

0

.

..

..

a.

B

Fig. 10. Actual and modeled body temperatures of two bluefin tuna swimming in a heterothermal environment. Actual body ( X ) and water (0)temperatures were estimated at 20 min intervals and to 0.5"C from graphs presented by Carey and Lawson (1973).By exponentially filtering the water temperature series to which a constant temperature had been added, modeled body temperatures (-0-)were generated under the hypothesis that each fish had a constant rate, i.e., did not physiologically regulate body temperature. Lack of substantial physiological thermoregulation is suggested by how closely the model, optimized with reasonable values ofthe parameters, could b e made to fit the data. (A) Muscle temperature, bluefin tuna No. 8. (B, C) Stomach temperature, bluefin tuna No. 14. (From Neill and Stevens, 1974, Science 184, 1008-1010. Copyright 1974 b y the American Association for the Advancement of Science.)

-

7

346


did not thermoregulate physiologically. We emphasize here (as we did in 1974) that this interpretation does not preclude the possibility of physiological thermoregulation; it simply shows that we do not have definitive evidence proving or disproving rapid physiological thermoregulation in tunas. It may be that, in order to demonstrate physiological thermoregulation in tunas, the fish must not be under any nonthermal stress. The Neill-Stevens model also shows that thermal inertia is important in its own right, especially in large tunas. Large thermal inertia makes possible a kind of physical thermoregulation that can result in large excess body temperatures and protection of core tissues from large, rapid fluctuations in environmental temperature persisting for periods up to several hours.

C. Long-Term Temperature Responses or Thermoregulation? In the previous section we have argued that there is no definitive evidence to support the hypothesis of short-term physiological thermoregulation in tunas. The hypothesis when originally proposed was based on observations of body temperature in tunas caught at a variety of locations with different surface water temperatures (Carey and Teal, 1966; Stevens and Fry, 1971). Excess body temperatures of tunas caught from cold water tend to be greater than those of conspecifics caught from warmer water, i.e., regressions of observed body temperature on water temperature tend to have slopes less than unity (Fig. 1). The relation is weak for yellowfin tuna, stronger for skipjack tuna, and strongest for bluefin tuna, in which observed body temperatures are nearly independent of water temperature. These observations have suggested to their examiners (Carey and Teal, 1969b; Stevens and Fry, 1971) that bluefin tuna, skipjack tuna, and yellowfin tuna are, respectively, good, fair, and poor thermoregulators. The presumption was that the body temperatures measured in just-caught fish are unbiased estimates of typical temperatures maintained by tunas as they go about their routine activities. For skipjack tuna we now are reasonably confident that this interpretation is invalid; rather, we believe that muscle excess in unexcited, routinely active skipjack is only 2”-4”C,independent of ambient temperature. But, when the fish are feeding or engaged in other speed-demanding activity, excess increases dramatically, doubling or trebling for periods up to several hours and reaching even higher levels for briefer periods. We think it likely that the skipjack tuna “regulates” only the upper

5.


347

limit of core temperature, by simply reducing the intensity, duration, and/or frequency of activity bouts as body temperature approaches some critically high value (about 35°C; see Neil1 et al., 1976). According to our view, then, the thing that changes as a function of ambient temperature is neither resistance to heat transfer (k)nor “normal” rate of heat production but rather the fish’s thermal scope for activity, being greatest at low ambient temperatures and approaching zero at T, = [(-35°C) - routine T, 1. Decrease in thermal scope for activity with increased T, would lead automatically to distributions of observed body temperature that ( 1)are related to ambient temperature by slopes less than 1.0and (2) have lower variance at higher Ta’s. Neither of these results is inconsistent with the actual data (Fig. 1). Some major sources of variation in observed muscle temperatures of skipjack tuna, then, are (1)the extent of muscular activity during the feeding frenzy preceding capture (which may differ for skipjack in water of different temperatures because of direct effects of temperature on the fish or because of indirect effects of temperature acting to influence the kinds, distribution, and behavior of natural prey and also behavior of the live chum); (2) the time elapsing between initiation of heightened activity and measurement of muscle temperature (which varies with fishing tactics and success, with fish size, between observers, and also for a particular observer in differing sea conditions); and, (3) the immediate thermal history of the fish (which varies with vertical distribution of the fish in conjunction with thermal structure of the ocean in the fishing area). The last error source is particularly troublesome in that the T , recorded opposite a particular body temperature observation may be very much in error; a T , measured at the sea surface (as is customary) necessarily overestimates the ambient temperature experience of any fish not swimming continuously at the surface during the hour or so preceding capture. Some of the factors that cloud the issue of physiological thermoregulation in skipjack tuna also apply in the case of the bluefin tuna. However, the weight of the evidence for thermoregulation in large bluefin is convincing. Bluefin in 7°C water have an excess of 19”C, but the excess is only 2.4”C in 30°C water (Fig. 1). The regression line describing the relation between bluefin muscle and water temperature, based on all available data (173 fish; T, = 7”-30°C; Carey, personal communication, Woods Hole Oceanographic Institution), is

Tb = (0.237

* O.028)Ta + 25.25”C

where 0.028 is the standard error of the slope. Unfortunately, the data at extreme values of T , are least reliable. The fish from warmest water

348


were taken by hook and line rather than by trapping; in Carey's opinion, the hook-caught fish were more likely to have had abnormal body temperatures than fish taken in traps. The trap-caught fish taken at lowest temperatures had been at those temperatures less than 24 hr (following a storm that brought cold water into the trapping area); therefore, these fish may not have been in thermal steady-state at the time measurements were made. But, even if these questionable data are deleted, the regression relation changes very little; the more conservative regression line, based on 162 fish from Ta's between 13"and 23"C, is

Tb = (0.206

* O.049)Ta + 25.84"C

The slope of this line is significantly different from that of perfect conformers (1.0)and, in fact, is nearer that of perfect thermoregulators (0.0). When one considers that heightened activity in bluefin tuna decreases excess body temperature (Carey, personal communication), the above regression relationship constitutes convincing evidence that these fish thermoregulate. Bluefin tuna migrate annually and may acclimate to different water temperature conditions. Giant bluefin tuna of the western Atlantic spend winter in the warm south (Gulf of Mexico and Caribbean Sea) and migrate north from May to June to spend the summer in the northwest Atlantic (Butler, 1971). They enter Conception Bay, Newfoundland, when the water temperature is 6°C but are rarely hooked until water temperature increases to 10°C.It is very likely that anumber of adaptive physiological acclimatory processes, including an alteration in the anatomy of the rete or an alteration in the pattern of circulation through the various retia, occur during the migration. It may be that acclimation is different in some tunas than from typical teleosts in that tunas may compensate for cold to some extent by producing more heat or reducing the rate at which it is lost. However, nothing empirical is known about thermal acclimatory responses of tunas.

VIII. ADAPTIVE VALUES OF WARM-BODIEDNESS AND LARGE THERMAL INERTIA Tunas are warm-bodied both because they produce metabolic heat at near mammalian rates and because their retia retard the loss of that heat to the water. Their exceptionally high metabolic rates are, in turn, associated with their capability for exceptionally fast swimming. We begin our search for adaptive values by accepting a priori that,

5.


349

for tunas, the capability for fast swimming is adaptive; this leads to a consideration of how warm-bodiedness may promote fast swimming. Then we return to the issue of physiological thermoregulation in tunas. Finally we consider some potential benefits of large thermal inertia that are independent of warm-bodiedness and, also therefore, of heat production.

A. Increased Muscle Power at Elevated Temperatures Carey has argued (Carey et al., 1971) that the adaptive value of tunas' heat exchangers lies in elevated body temperatures which promote greater muscle power for swimming. This is a logical proposition, but has not been empirically demonstrated for tuna muscle. Carey's original argument was based on experiments with isolated frog muscle b y Hill (1951). More recently, Wardle (1975) has shown that the time taken from a stimulating pulse to the peak of contraction in isolated fish white muscle and in intact fish is very temperaturesensitive. An increase in body temperature from 14"to 20°C was associated with an increase in maximum burst swimming speed from about 4.5 m sec-' to 5.3 m sec-' for a fish with a body length of 50 cm. Neil1 and Dizon (unpublished observations) have cinephotographed captive skipjack tuna, as these fish chased food thrown across a large tank, swimming at speeds on the order of 18 body lengths (C) sec-' (Le., 10 m sec-l for 50-cm fish) at an ambient temperature of 24°C. Muscle temperature during this period was not measured, but it was likely to have been between 30" and 32°C. The observed speed is greater than that predicted [5.8 m sec-' at 24°C extrapolated from the data of Wardle (1975)l by 72%,and some portion of this greater speed is likely attributable to the higher body temperature. Extrapolating Wardle's data to a body .temperature of 32°C yields a predicted maximum burst speed of about 8 m sec-*. Thus, tunas can burst-swim at greater speeds than nontunas and tunas are warmer than nontunas. But are tunas warmer because they swim faster, or are they faster because they are warmer? One difficulty in assessing this question is that there are no good simultaneous observations on fishes' core temperatures and maximum swimming speeds during burst activity. Walters and Fierstine (1964) reported a maximum of 21 e sec-l for a tuna (yellowfin) and 19 e sec-l for a nontuna (wahoo, Acanthocybium solandri).Yet the excess core temperature of the tuna was probably twice that of the nontuna. [There are many measurements of core temperatures in tunalike nontunas (Lindsey, 1968; Carey et al., 1971); all indicate that these fishes' core temperatures scarcely exceed l"C.1

350


B. Decreased Time between Bouts of Burst Activity at Elevated Temperatures Black and his colleagues have shown that the recovery time from severe exercise is very long in fish compared to mammals (Stevens and Black, 1966).For typical fishes, 12-24 hr elapse before levels of muscle and blood lactate return to pre-exercise levels, whereas in man recovery takes only 30-60 min. Barrett and Connor (1962, 1964) showed that in yellowfin and skipjack tuna lactate levels return to pre-exercise levels in about 2 hr-much more quickIy than in nontunas. Skipjack tuna, at least, are especially warm after severe exercise, and they recover from exercise quickly. These two aspects of tuna physiology may be related causally; this may be an important value of warm-bodiedness, considering that the recovery process is likely temperature-sensitive. (The temperature-sensitive process could be a physiochemical process such as the diffusion of lactate from muscle to blood or it could be biochemical.) An adaptive value of being warm after severe exercise then is that it speeds recovery, thereby permitting more frequent feeding frenzies with concomitant increases in the rate of food capture and perhaps of growth.

C. Benefits Accruing from Body Temperature Stability Whether or not tunas benefit from being consistently warmer than their environment (and relatively warmer than other fishes), tunas may profit from a relatively stable body temperature.

1. PHYSIOLOGICAL THERMOREGULATION Physiological thermoregulation permits optimization of physiological processes over a relatively narrow range of temperature. No doubt fishes would enjoy the benefits of physiological thermoregulation to the same extent that birds and mammals do-if its costs were not so great for the water breathers. Tunas, however, have already made an evolutionary investment in physiological thermoregulation. And the evidence suggests that large bluefin tuna, at least, practice substantial thermoregulation. But, why do the tunas as a group not physiologically thermoregulate more effectively on a short-term basis, simply by passing more or less blood through their exchangers? The answer seems to be that the tunas have not yet cashed in on their investment.

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351

2. THERMAL LAG-MORE TIMEBELOWTHE THERMOCLINE Even in the absence of physiological thermoregulation, tunas achieve substantial independence from fluctuations of environmental temperature through large thermal inertia. We have shown that skipjack tuna cool only one-half as quickly as a nontuna of the same weight when exposed to the same decrease in ambient temperature. Thus, if the rate of some process is controlled by temperature, then the warmer tuna have an advantage. The small difference between the muscle temperature of the tuna and nontuna in steady state becomes considerably magnified when ambient temperature is changing (Fig. 11). Even small tunas, say 3-kg skipjack, can sound for several minutes into the cool water below the thermocline with only a small depression of core temperature. If higher core temperatures are necessary for faster swimming, these minutes of thermal lag may mean the difference between life and death to a skipjack being pursued through the thermocline by a marlin.

3. INSTANTANEOUSTEMPERATURE COMPENSATION-ADISCLAIMER There is some evidence that certain enzymes in some organisms compensate instantaneously for changes in temperature by changing

n CORE EXCESS

STEADY STATE

E$''

"Nu

0 03725

EXTRA TIME TO COOL 5 C'

X EXTRA TIME

:

IS 7 I min NONTUNA'K' - TUNA'K" NONTUNA *K'

,,oo

* 38 X For 3Lp

Time Imin)

Fig. 11. Simulated changes in core temperature of a tuna compared to a nontuna when ambient temperature decreases from 26" to 16°C (for example, if both swam through the thermocline). It takes 38% longer for the tuna to cool 5°C so that it will have an advantage over the nontuna if some processes slow upon temperature decrease.

352


affinity for substrate and for modulators (Hazel and Prosser, 1974). If this is so in tunas, then constant temperature is of no advantage in enzyme catalyzed reactions. However, temperature stability may be very important in certain physiochemical processes that cannot be compensated for by changes in enzyme characteristics. For example, the rate at which muscle can contract is limited by the rate at which Ca2+can move from the sarcoplasmic reticulum into the sarcoplasm. The diffusion of Ca2+ into the sarcoplasm may be extremely temperature-sensitive; if so, maximum swimming speed is temperature-dependent, whether or not the enzymatic machinery is instantaneously temperature compensated.

D. Perception of Weak Horizontal Temperature Gradients The rete increases thermal inertia to such an extent that it may enhance or permit detection of weak horizontal gradients of temperature (Neill et al., 1976). Such a mechanism could account for the effect of weak horizontal temperature gradients on the distribution of tunas in the oceans. The tuna changes core temperature so slowly that the difference between core temperature and a slowly changing ambient temperature increases sufficiently to be detected. Neill et al. (1976) suggest that fishes perceive changes of environmental temperature as a disequilibration of core temperature (Tbf T,). If this is so, tunas have a distinct advantage over typical fishes in sensing weak temperature gradients. Not only do tunas swim faster, thereby enhancing contrasts of ambient temperature over time, but their large thermal inertia causes core temperature to lag substantially for even very gradual changes in environmental temperature. Neill et al. illustrated the second point by simulating core temperature in a 2-kg skipjack swimming into a gradient of only 1°C km-' at a speed of 1.77 e sec-l (50 m min-'). After the fish had swam only 250 m into the gradient (5 min), core temperature had diverged from its equilibrium value by 0.23"C, which is approximately twice the threshold for detection of a temperature step-change in tuna (Steffel et al., 1978). For the simulation to yield the same result with a Zkg nontuna (which has about half the thermal inertia and swims at about half the speed of the tuna), the required gradient is four times as steep-4"C km-'. To put the contrast in terms of limits, we may ask, "How steep must a lineary temprature gradient be to just permit sensory detection under the model?" The answer is given by

k threshold swimming speed

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353


where "threshold" is the minimum disequilibration ( Tb - T,) that is perceptible. (The above formula follows from integration of the equation in Section VII,B,2 after substituting [T,(O) gradient speed . t ] for T,) If we insert in the formula the following tabulated values, the answers to the question raised above are ?O.O66"C km-I for the tuna and +0.264"C km-' for the nontuna.

+

-

~~

k("C min-I "C-1) Speed (m min-I) Threshold ("C)

2-kg Tuna

2-kg Nontuna

0.033 50.0 0.1

0.066 25.0 0.1

We hasten to add that Neil1 et al. labeled their model for gradient " perception speculative." The basic hypothesis remains untested, to the best of our knowledge.

E. Retia Function to Retard Mass Transfer Rather than Heat Transfer We have no evidence that the exchanger exchanges anything but heat. However, lack of evidence does not preclude this possibility. If, for example, lactic acid passes across the exchanger vessels, lactate would be contained within the muscle. This would reduce the potentially deleterious effects of lactic acid on other tissues after a bout of strenuous activity. In addition, lactate would pass directly from white muscle to red muscle without entering the general circulation. It has been suggested (Braeken, 1956, reviewed in Bilinsky, 1974) that red muscle in fish functions like mammalian liver in the metabolic sense. White muscle provides the energy for swimming and produces lactate as a by-product; red muscle also provides energy for swimming but in addition oxidizes the lactate to provide more substrate for white muscle.

IX. PHYSIOLOGICAL INSIGHTS INTO THE NATURAL HISTORY OF TUNAS Barkley et aZ. (1976) have recently extrapolated laboratory data on temperature and dissolved oxygen requirements of skipjack tuna to predict geographic distribution of this species in the tropical Pacific Ocean. The predictions are consistent with Rothchilds (1965) migration model for the eastern Pacific skipjack tuna population.

354


Barkley et al. suggest that only pre-adolescent skipjack tuna can continuously inhabit tropical surface waters. The habitat of adult skipjack in the tropics, they argue, is the upper thermocline and not the surface layer, as has generally been thought. Their physiologically based model contends that the normal habitat of skipjack tuna is limited to those waters bounded by (1) a lower threshold for incipient thermal stress which may vary with prior conditioning but which apparently lies between 15" and 18°C; (2) a lower threshold for incipient oxygen stress, at or slightly below 3.5 ml liter1 (5 ppm) of dissolved oxygen; and (3) a speculatively inferred upper threshold of incipient thermal stress, ranging from 30°C for the smallest skipjack tuna normally caught by fisherman to 20°C or less for the oldest and largest of these fish. While the lower temperature and oxygen limits of the habitat may be the same for skipjack tuna of all sizes, the upper temperature limit occurs deeper in the water column and is more restrictive for the larger fish. In broad areas of the eastern tropical Pacific, the critical oxygen isopleth comes near the surface, intersecting the isotherms that mark the upper temperature limits for skipjack larger than 4 kg. Therefore, skipjack are excluded from progressively larger fractions of the eastern tropical Pacific as they grow larger than 4 kg. For example, 9 k g skipjack in summer along 119"W long. find essentially no habitable water between 5" and 12"N lat., a distance of more than 700 km (400 nautical miles). What happens to these larger fish? They logically move westward, toward the central Pacific, where deep water is both cool and oxygen-rich. Such a migration pattern is consistent with Rothschild's ( 1965) hypothesis: Mature and maturing skipjack (40-65 cm long, 1.2-6 kg) leave the Mexican and Central American fisheries, migrate westward, then spawn in the equatorial Pacific south of Hawaii. In the central Pacific and in other areas where the upper temperature limit is subsurface, skipjack tuna probably adopt a cyclical pattern of depth distribution, alternately rising to the surface to feed and navigate, then sounding below the thermocline to cool (Neil1 et al., 1976).

X. CONCLUSION: A THERMOCENTRIC OVERVIEW OF TUNA EVOLUTION Tunas inhabit parts of the world-ocean that are devoid of solid structure, highly transparent, and nutritively dilute. Forage for 10-


355

1000 kg carnivores is not only scant but also is very patchily distributed. These properties of the tropical epipelagic zone have resulted in two divergent strategies of adaptation among tuna-sized fishes. Some, the energy frugalists, survive by minimizing energy expenditures through a nearly planktonic existence. The ocean sunfish (Molidae) represents the extreme case for this group; large opah (Lamprididae), too, reasonably fit the model of energy thrift. At the other extreme are the energy speculators. These fishes are wide-ranging and capable of high-speed swimming. They operate to maximize energy gain by gambling large energy expenditures (activity) on the expectation of proportionately large energy returns. In this group are certain carangids, coryphaenids, billfishes (istiophorids and Xiphius),and, at the very extreme, the lamnid sharks and the tunas. Specialization in energy speculation has brought tunas to the ragged edge of piscine existence. By this, we mean that tunas very nearly have beaten the system that we think of as “fish.” In particular, tunas are not poikilotherms; at least one tuna, the bluefin, is in fact on the verge of homiothermy. Scombrids gave up poikilothermy when they invested in vascular devices that retard heat transfer between body core and environment. An effective countercurrent heat exchanger not only damped vacillations of core temperature but also permitted high metabolic rates to be expressed as warm-bodiedness in the advanced tunas. Warmbodiedness, by the reasoning in Section VIII, enabled even higher (near mammalian) rates of metabolism in support of activity levels surpassing those of any other teleost group. But, there was a potential flaw in the tunas’ strategy for maximizing swimming speed: Any device that gets warmer as it operates faster and operates faster as it gets warmer is susceptible to the positivefeedback loop called by electrical engineers, “thermal runaway.” Tunas have obviated the potential for thermal runaway by opening the loop in at least two different ways. The skipjack group has evolved temperature-independent metabolism; that is, they do not operate faster as they get warmer. The bluefin tuna (and probably other Thunnus species) has adopted an alternative strategy. This largest of tunas, in contrast to the skipjack, has developed circulatory and metabolic arrangements that permit cooling during periods of maximum activity. Because the bluefin does not necessarily get warmer as it operates faster, it has no need for temperature-independent metabolic machinery. And, in fact, the yellowfin tuna, a congener of the bluefin, exhibits the usual elevation of metabolism with increase in temperature.

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On the whole, it would seem that the bluefin’s solution to the temperature-activity dilemma is superior to that of the skipjack group. Although activity-induced increases in body temperature do not feedback into increased activity in skipjack, large skipjack still risk overheating in warm waters when they must be highly active to catch prey and avoid predators-a factor that may progressively restrict both vertical and geographic distribution of skipjack as they grow. Risk of overheating and the attendant restriction of thermal niche have been compromised through evolutionary limits on maximum body size; none of the skipjack group exceeds 22 kg in maximum weight. In contrast, four Thunnus species have maximum weights near or exceeding 200 kg (Table I). Large mass and correspondingly large thermal inertia have enabled the bluefin group to exploit much cooler waters than the skipjack group; at the same time, the bluefin’s capacity to be active without overheating allows it to live also in waters as warm as those inhabited by the skipjack group. Moreover, the bluefin’s solution to the temperature-activity problem has brought fishes to the verge of homiothermy. ACKNOWLEDGMENTS We thank Drs. Jeff Graham and Frank Carey for extensive and useful comments on the manuscript. Dr. Carey was especially helpful in providing us with raw data and details of how it was collected. We also thank Dr. Andy Dizon for supplying details of unpublished work from the National Marine Fisheries Laboratory at Honolulu. REFERENCES Barkley, R. A., Neill, W. H., and Gooding, R. M. (1976). Hypothetical habitat of skipjack tuna based on temperature and oxygen requirements. Nat. Mar. Fish. Sew., Honolulu, Hawaii. Barrett, I., and Connor, A. R. (1962). Blood lactate in yellowfin tuna and skipjack tuna following capture and tagging. Inter-Am. Trop. Tuna Comm., Bull. 6,231-280. Barrett, I., and Connor, A. R. (1964). Muscle glycogen and blood lactate in yellowfin tuna and skipjack following capture and tagging. Inter-Am. Trop. Tuna Comm., Bull. 9, 219-252. Barrett, I., and Hester, F. (1964). Body temperatures of yellowfin and skipjack tuna in relation to sea surface temperatures. Nature (London)203, 9 6 9 7 . Berg, L. S. (1955). Classification of fishes and fishlike animals, both recent and fossil (2nd Ed.). Tr. 2001.Inst., Akad. Nauk S S S R 20, 286 pp. Bilinsky, E. (1974). Biochemical aspects of fish swimming. In “Biochemical and Biophysical Aspects in Marine Biology” (D. C. Malins and J. R. Sargent, eds.), Vol. 1, pp. 239-288. Academic Press, New York. Brett, J. R. (1972). The metabolic demand for oxygen in fish, particularly salmonids, and a comparison with other vertebrates. Respir. Physiol. 14, 151-170.


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Brill, R. W., Guernsey, D. L., Dizon, A. E., and Stevens, E. D. (1978). Temperature profiles and heat loss in skipjack tuna. Nat. Mar. Fish. Serv., Honolulu, Hawaii. Brown, C. E., and Muir, B. S. (1970). Analysis of ram ventilation of fish gills with application to skipjack tuna.]. Fish. Res. Board Can. 27, 1637-1652. Burne, R. H. (1923). Some peculiarities of the blood vascular system of the porbeagle shark, Lamna cornubica. Philos. Trans. R . Soc. London Ser. B 212, 209-257. Butler, M. (1971). Biological investigation on aspects of the life history of bluefin tuna. Newfoundland Labrador Tourist Dev. Off., St. John’s. Carey, F. G. (1973).Fishes with warm bodies. Sci. Am. 228(2), 3 6 4 4 . Carey, F. G., and Lawson, K. D. (1973). Temperature regulation in free-swimming bluefin tuna. Comp. Biochem. Physiol. A 44, 375-392. Carey, F. G., and Teal, J. M. (1966). Heat conservation in tuna fish muscle. Proc. Natl. Acad. Sci. U.S.A. 56, 1461-1469. Carey, F. G., and Teal, J. M. (1969a). Mako and porbeagle: Warm-bodied sharks. Comp. Biochem. Physiol. 28, 199-204. Carey, F. G., and Teal, J. M. (1969b). Regulation of body temperature by bluefin tuna. Comp. Biochem. Physiol. 28, 205-213. Carey, F. G., Teal, J. M., Kanwisher, J. W., Lawson, K. D., and Beckett, J. S. (1971). Warm-bodied fish. Am. Zool. 11, 135-143. Chang, R. K. C., Ito, B. M., and Neill, W. H. (1976). Temperature independence of metabolism and activity in skipjack tuna. Natl. Mar. Fish. Serv., Honolulu, Hawaii. Charm, S. E., and Moody, P. (1966). Bound water in haddock muscle. ASHRAE J . 8, 39-42. Collette, B. B., and Chao, L. N. (1975). Systematics and morphology of the bonitos (Sarda)and their relatives (Scombridae, Sardini). US.Fish. Wildl. Seru., Fish. Bull. 73, 516625. Davy, J. (1835). On the temperature of some fishes of the genus Thunnus. P+oc. R . SOC. London 3,327-328. Dizon, A. E., Magnuson, J. J., and Neill, W. H. (1976). Swimming speed as a function of temperature in three species of tunas. Natl. Mar. Fish. Serv., Honolulu, Hawaii. Eschricht, D. F., and Muller, J. (1835).Uber die arteriosen and venosen Wundernetz an der leber und einen merkwiiidigen bau dieses Organes beim thunfische. Abh. Dtsch. Akad. Wiss. Berlin pp. 1-30. Fierstine, H. L., and Walters, V. (1968). Studies in locomotion and anatomy of scombrid fishes. Mem. South. Caltf. Acad. Sci. 6, 1-31. Fraser-Brunner, A. (1950). The fishea of the family Scombridae. Ann. Nat. Hist. Ser. 12 3, 131-163, Fry, F. E. J. (1971). The effect of environmental factors on the physiology of fish. In “Fish Physiology” (W. S. Hoar and D. J. Randall, eds.), Vol. 6, pp. 1-98. Academic Press, New York. Fry, F. E . J., and Brett, J. R. (1974). Oxygen consumption: Fishes. In “Biological Data Book” (P. L. Altman and D. S. Dittmer, eds.), 2nd Ed., Vol. 3, pp. 1625-1630. Fed. Am. SOC.Exp. Biol., Bethesda, Maryland. Gibbs, R. H., and Collette, B. B. (1967). Comparative anatomy and systematics of the tunas, genus Thunnus. U.S. Fish. Wildl. Seru., Fish. Bull. 66, 65-130. Goadby, P. (1972).“Big Fish and Blue Water,” Holt, New York. Godsil, H. C. (1954). A descriptive study of certain tunalike fishes. CaliJ Dep. Fish Game Bull. No. 97. Godsil, H. C., and Byers, R. D. (1944).A systematic study of the Pacific tunas. Calif. Dep. Fish Game Bull. No. 60. Godsil, H. C., and Holmberg, E. K. (1950). A comparison of the bluefin tunas, genus

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Thunnus, from New England, Australia, and California. calif. Dep. Fish Came Bull. No. 77. Gordon, M. S. (1968).Oxygen consumption of red and white muscles from tuna fishes. Science 159, 87-90. Graham, J. B. (1973).Heat exchange in the black skipjack, and the blood-gas relationship of warm-bodied fishes. Proc. Natl. Acad. Sci. U.S.A. 70, 1964-1967. Graham, J . B. (1975).Heat exchange in the yellowfin tuna and skipjack tuna, and the adaptive significance of elevated body temperatures in Scombrid fishes. U.S. Fish. Wildl. Sew., Fish. Bull. 73, 219-229. Hazel, J. R., and Prosser, C. L. (1974).Molecalar mechanisms of temperature adaptation in poikilotherms. Physid. Rev. 54, 620-677. Hill, A. V. (1951).The influence of temperature on the tension developed in an isometric twitch. Proc. R. Soc., Ser. B 138,349-354. Kishinouye, K. (1915).A study of the mackerels cybiids, and tunas. Suisan Gakkwai H O 1,l-24.(In Japanese, trans]. by W. G. Van Campen, U S . Fish Wildl. Seru., Spec. Sci. Rep.-Fish. No. 24.) Kishinouye, K. (1917).A new order of teleostomi. S U ~ S QGakkwai ~ H O 2, 1-4. (In Japanese, trans]. by W. G. Van Campen, US.Fish Wildl. Seru., Spec. Sci. Rep.Fish. No. 50,pp. 1-3.) Kishinouye, K. ( 1923).Contributions to the comparative study of the so-called scombrid fishes. J. Coll. Agric., Imp. Uniu. Tokyo 8, 293-475. Lindsey, C. C. (1968).Temperatures of red and white muscle in recently caught marlin and other large tropical fish. 1. Fish Res. Board Can. 25, 1987-1992. Linthicum, D.S.,and Carey, F. G. (1972).Regulation of brain and eye temperatures by the bluefin tuna. Comp. Biochem., Physiol. A 43, 425-433. Magnuson, J. J. (1963).Tuna behavior and physiology, a review. FA0 Fish. Rep. 6(3), 1057-1066. Malessa, P. (1969).Beitrage zur Temperaturadaptation des Aales. Mar. Biol. 3,143-158. Morrow, J. E. (1957).Shore and pelagic fishes from Peru, with new records and description of a new species of Sphoeroides. Bull. Bingham Oceanogr. Collect. 16, 5-55. Nakumura, I. (1965).Relationships of fishes referable to the subfamily Thunninae on the basis of the axial skeleton. Bull. Misaki Mar. Biol. lnst., Kyoto Uniu. 8, 7-38. Neill, W.H., and Stevens, E. D. (1974).Thermal inertia versus thermoregulation in “warm” turtles and tunas. Science 184, 1008-1010. Neill, W. H., Chang, R. K. C., and Dizon, A. E. (1976).Magnitude and ecological implications of thermal inertia in skipjack tuna. Enoiron. Biol. Fish. 1, 61-80. Rayner, M. D., and Keenan, M. J. (1967).Role of red and white muscles in the swimming of the skipjack tuna. Nature (London)214,392-393. Regan, C. T. (1909).On the anatomy and classification of the scombroid fishes. Ann. Mag. Nat. Hist. Ser. 8 3, 66-75. Rothchild, B. J. (1965).Hypothesis on the origin of exploited skipjack tuna in the eastern and central Pacific Ocean. U.S. Fish Wildl. Sew., Spec. Sci. Rep.-Fish. No. 512. Slavin, J. W.(1964).Freezing seafood-now and in the future. ASHRAE J. 6,43-48. Stark, E.C. (1910).The osteology and mutual relationships ofthe fishes belonging to the family Scombridae. J . Morphol. 21, 77-99. Steffel, S., Dizon, A. E., Magnuson, J. J., and Neill, W. H. (1978).Temperature discrimination by captive free-swimming tuna, Euthynnus afinis. Trans. Am. Fish. Soc. 105,~8-591. Stevens, E. D. (1972).Some aspects of gas exchange in tuna. J. E x p . B i d . 56,809-823. Stevens, E.D.,and Black E. C. (1966).The effect of intermittent exercise on carbohydrate metabolism in rainbow trout. J . Fish. Res. Board Can. 23,471-485.


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Stevens, E. D., and Fry, F.E. J. (1971).Brain and muscle temperatures in ocean-caught and captive skipjack tuna. Comp. Biochem. Physiol. A 38, 203-211. Stevens, E. D., and Fry, F. E. J. (1972).The effect of changes in ambient temperature on spontaneous activity in skipjack tuna. Comp. Biochem. Physiol. A 42, 803-805. Stevens, E.D.,and Fry, F. E. J. (1974).Heat transfer and body temperatures in nonthermoregulatory teleosts. Can. J. Zool. 52, 1137-1143. Stevens, E.D.,Lam, H. M., and Kendall, J. (1974). Vascular anatomy of the countercurrent heat exchanger of skipjack tuna.J. E x p . B i d . 61, 145-153. Takahashi, N.(1926).On the Plecostei, an order of the Teleostomi, established by Prof. Kishinouye.]. Coll. Agric., Imp. Unio. Tokoyo 7 , 383-398. Uda, M. (1941).The body temperature and bodily features of “Katuo” and “Sanma.” Nippon Suisan Gakkaishi 9,231-236.(In Japanese, transl. by W. G. Van Campen, U.S. Fish Wildl. Seru., Spec. Sci. Rep.-Fish. No. 51.) Walters, V., and Fierstine, H. L. (1964).Measurement of swimming speeds of yellowfin tuna and wahoo. Nature (London)202,208-209. Wardle, C . S. (1975).Limit of fish swimming speed. Nature (London) 255,725-727. Webb, P. W. (1975).Hydrodynamics and energetics of fish propulsion. Bull., Fish. Res. Board Can. 190, 1-159. Yuen, H. S. H. (1959).Variability of skipjack response to live bait. U.S. Fish. Wildl. S m . , Fish. Bull. 60, 147-160. Yuen, H. S. H. (1966).Swimming speeds of yellowfin and skipjack tuna. Trans. Am. Fish. SOC. 95, 203-209.


6 LOCOMOTOR MUSCLE QUENTlN BONE I. Introduction .................................................... 11. The Organization of the Myotomes .............................. 111. Fin M u s cl es . . .................................................. IV. Fiber Types .................................................... A. General Considerations ...................................... B. Histology ................................................... C. Ultrastructure and Histochemistry in Different Fish Groups ................................................ D . Ontogeny of Fiber Types .................................... E. Innervation ................................................. F. Electrical and Mechanical Properties ......................... G. Functional Role of Different Fiber Types .....................

.......................

VI. Fish Muscle and the Muscles of Higher Forms .................... References

.........................................................

36 1 363 368 368 368 373 377 390 393 397 405 410 416 417

I. INTRODUCTION Muscular tissue forms a larger part of the mass of the fish body than it does of other vertebrates: Some 40-60% of the total body mass in most fish is locomotor musculature (Table I). In part this is because economy in weight is not mandatory as it is for terrestrial and aerial forms, and in part because stringent demands are placed on the locomotor system by the density of the medium, so that a large amount of muscle is needed to generate sufficient power for rapid swimming. In addition to sheer mass (which of course gives fish their culinary and economic importance), there are Several design features of the muscular system that are not commonly found in the muscles of other classes of vertebrates. For example, in many fish, twitch fibers are multiply innervated; again, no fish muscles contain muscle spindles: Such features give fish muscle an especial comparative interest. It must be emphasized at the outset, however, that despite the efforts of a 361 FISH PHYSIOLOGY, VOL VII Copyright @ 1978 by Academic Preu, In' A l l light* of reproduction in m y form re\erved ISBN 0-12 350407 4

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QUENTIN BONE

Table I The Amount of Locomotor Muscle as a Proportion of Total Body Weight in Different Fish Species

% Muscle

Comments.

Authority

Galeocerdo arcticus Prionace glauca Scyliorhinus canicula Centroscymnus owstoni Katsuwonus pelamis Salmo irideus Carassius auratus Leuciscus leuciscus

37 36 45 55-60 68 55-67 33-45 42-60

Incl. vertebrae

Warfel and Clague (1950) Stevens (1976) Bone and Roberts (1969) Higashi et al. (1953) Fierstine and Walters (1968)

Incl. skin

Bainbridge (1960, 1962)

number of investigators (beginning with Lorenzini, 1678, who first described different muscle fiber types), knowledge of fish muscle is as yet relatively scanty. This chapter can thus only serve as a progress report, rather than as a definitive account of the muscular systems employed in locomotion. In several important respects, fish muscle is well-suited for physiological study (despite the disadvantages inherent in the myotomal muscle preparation), and certain puzzling features of vertebrate muscle fibers are perhaps most likely to be understood by work on fish. The great majority of fishes swim using the segmental myotomal musculature, so most of this chapter will deal with the arrangement of the myotomes and of the muscle fibers within them. A few fish (e.g., some Trachyurids, many labrids, rays, and holocephali) swim by using the musculature of the paired or unpaired fins: These muscles will be considered in less detail. The nomenclature of fish muscles has been bedeviled by synonymy, but fortunately Winterbottom (1974) has provided a helpful guide to the nomenclature of the locomotor (and other) muscles. In limiting this chapter only to locomotor muscles, it is important to observe that although this may yield a more uniform view of sets of fibers designed for similar ends in different forms, interesting work on other kinds of fish muscle fibers has to be omitted. For example, fish eye muscles have provided valuable material for experimental study of selective re-innervation (e.g., Mark and Marotte, 1972); the very rapid sonic muscles of the swimbladder in some forms have proven interesting (Skoglund, 1961); the gill muscles may yield useful mechanical preparations (Levin and Wyman, 1927);the muscular systems of fish barbels offer peculiar problems of coordination and control.

6.

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Fascinating as these muscles all are, they fall outside the scope of this chapter.

11. THE ORGANIZATION OF THE MYOTOMES

The lateral musculature in all fish groups is subdivided into serially arranged myotomes of complex shape, delimited by connective tissue myosepta into which the myotomal muscle fibers insert. Figure 1 shows something of myotomal shape in different fish groups. There is plainly a phylogenetic increase in complexity of shape, from the simple V-shape in amphioxus via the shallow W-shape of the Agnatha, to the deep W-shape of gnathostomes. This phylogenetic change is reflected in the ontogeny of the higher fish groups where the somite first forms a V-shape, before folding further to yield the adult W-shape.

Fig. 1. Simplified diagrams of myotomal shape in various fish groups. An enlarged view of a midtrunk myotome in each is shown at right; a teleostean caudal myotome at bottom. Not to scale. (Redrawn from Nursall, 1956, Proc. Zool. SOC.London 126, 127143.)

364

QUENTIN BONE

A number of workers have attempted to provide a functional basis for the complex shape of the fish myotome, and for its internal arrangement. These attempts have been more successful in explaining the orientation of muscle fibers within the myotomes than the shape of the myotomes themselves; yet both presumably reflect the properties of the contractile units of the system and the properties of their insertions. The important properties insofar as myotomal design is concerned would seem to be the following. 1. Contraction takes place without volume change. 2. The muscle fibers insert onto deformable but inextensible partitions which are attached to the flexible but incompressible notochord or vertebral column. 3. Deformation of the myosepta is often (but not always) restrained b y intermuscular bones. 4. Flexion of the body is required only in the lateral plane. 5. During flexion, the radius of curvature will be least next to the vertical column, largest just under the skin. 6. Both frequency and amplitude of flexions may vary. The end result of the operation of the myotomal units with these properties is, of course, the lateral oscillations of the body brought about by transferring the contraction forces to the central strut. In the simple myotomes of amphioxus, the muscle lamellae run nearly parallel to the long axis, and the distance between inner and outer surface of the myotome in these animals is small. A single muscle lamella may span the whole of this distance (see Fig. 8), but the difference between the radii of curvature of its inner and outer edges is insignificant. The V-folding of the myotome is probably related to the need to avoid dorsoventral flexion. The notochord lies dorsally to accommodate the viscera below it, and if the myotomes were simple inclined blocks (the greater part of which lay below the strut), contraction would lead to ventral flexions of head and tail. With the V-shaped myotome arranged so that the arms of the V are unequal in length, and that the apex lies at the level of the notochord, solely lateral flexions are possible. It is significant that with increase in scale, all other fishes have their myotomes arranged so that the muscle fibers of the greater part of the myotome do not run parallel to the long axis. Indeed, as van der Stelt (1968) and Alexander (1969) point out, the muscle fibers of the white or fast part of the myotome may make large angles with the long axis. Alexander (1969) found that some muscle fibers in the myotomes of both sharks and teleosts were oriented at nearly 40"to the long axis. These orientations are not random; Fig. 2 shows the two patterns of

6.

LOCOMOTOR. MUSCLE

I

365

(a)

Fig. 2. Thick transverse slices across (a) selachian, and (b) teleostean body showing orientation of myotomal muscle fibers as viewed from behind. ac, anterior cone; pc, posterior cone; t, tendon. (From Alexander, 1969,J. Mar. Biol. Assoc. U . K . 49,.263-290.)

orientation found b y Alexander in sharks and in higher teleosts. Alexander was able to show that these two patterns of orientation of the fast or white fibers of the myotome were a consequence of the requirement for all of these fibers to contract at about the same rate, whatever their position in the myotome. In other words, although during flexion the radius of curvature of the fish as a whole will b e greatest next to the vertical column, and least superficially, suitable orientation of the fibers in these positions in the myotomes will enable each to contract to the same extent as the body flexes. The importance of this result is that, as Hill (1950) has pointed out, the shape of the forcehelocity curve for muscle fibers means that maximum power will be produced at a particular rate of contraction. We do not know the shape of the forcehelocity curve for the myotomal muscles of any fish, but we can assume that for most fishes, the white or fast portion of the myotome will b e designed for maximum power (see Section IV). The orientation of the muscle fibers directly reflects this requirement, for if they were not able to contract at about the same rate throughout the myotome, the power extractable from the fast portion of the myotome would be much lessened. Note that this argument does not apply to the superfi-

366

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cia1 sheet of slow (red) muscle fibers, for it is thin enough that the fibers which make it up can run more or less parallel to the long axis and yet all contract at about the same rate. It is interesting that sharks and higher teleosts adopt different fiber orientations in the rnyotomes. Alexander has shown that the helical teleost arrangement (Fig. 3) will give a faster rate of body flexion for the same rate of contraction of the muscle fibers than will the selachian arrangement (at the expense of a weaker bending moment), and suggests that this is a better compromise for the teleosts since they swim faster than sharks of similar size. It is difficult to know whether this proposition is always applicable, since there are no measurements of the speed of Isurids; it would certainly be very interesting to know if the selachian arrangement found b y Alexander in Hexanchus, Scyliorhinus, and Squalus also obtains in Carcharodon or Zsurus. In the caudal peduncles of higher teleosts, there is a transition to the selachian pattern of fiber orientation, and Alexander suggests that this is to enable the fish to cope with the larger stresses in this region while maintaining a similar rate of contraction of muscle fibers throughout the body. Alexander’s analysis was notable, for it gave the first convincing functional explanation of the fiber orientation of the myotomes. What is more, it seems likely that this fiber orientation underlies the complex

Fig. 3. Schematic dorsal and lateral views of typical teleost showing course of myotomal muscle fibers in successive myotomes along the body. The helices shown were found by taking the origin of one muscle fiber from the point at which the muscle fiber in the myotome next anterior inserts onto the common myoseptum, and so on along the fish. (From Alexander, l969,J. Mur. B i d . Assoc. U .K. 49, 263-290.)

6.

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367

shape of the gnathostome myotomes. The myotomal folding is so arranged that the muscle fibers insert into the myosepta at approximately the same angle, despite their very different orientations with respect to the long axis of the body. It would evidently be interesting to examine fiber orientations during ontogeny as the myotomes gradually achieve the W-shape, to provide a test of this view. The larger scombroids have the most specialized teleost myotomes. In these fish, the inertia of the caudal peduncle and foil has been reduced as much as possible (just as in the legs of fast-running terrestrial vertebrates) and the foil is oscillated by tendons passing over a flexible joint in the vertebral column (Fierstine and Walters, 1968). These tendons are formed by a series of nested cones derived from successive myosepta (an analogous arrangement is found in the caudal region of certain rays), similar smaller tendons also run anteriorly to insert upon the pectoral girdle. The result of this arrangement is that these fish have achieved the hydrodynamically desirable separation of the power source from the caudal propellor. Body flexions are less than those of fish swimming in less efficient and less rapid ways (see Chapter 3), and since the muscles used during cruising form the inner portion of the myotome (Fig. 4), it is possible that these contain muscle fibers oriented parallel to the long axis of the body. Fiber orientations have not yet been studied in the larger scombroids, nor in the similarly adapted Isurid sharks.

4a D

Fig. 4. Diagrammatic transverse sections across the body of various teleosts and elasmobranchs to show disposition of slow (red) muscle fibers in the myotomes (shaded).A, Katsuwonus; B, Rhina; C, Squalus; D, Atherina; E, Euthynnus; F, Alosa. A, redrawn from Rayner and Keenan (1967); remainder original.

368

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Little work has been done upon the myosepta themselves. Some of the problems of their design have been considered by Willemse (1975), who describes the organization of the connective tissue fibers in teleost myosepta. In many teleosts intermuscular bones of different forms lie in the myocommata, limiting the directions in which they may b e deformed. Jarman (1961) pointed out that these bones could be arranged so that they did not interfere with contraction of the myotomal muscle fibers, but a functional analysis of the different patterns and numbers of these elements in different groups is yet to be made. They are absent from sharks.

111. FIN MUSCLES The arrangement of the muscles of paired and unpaired fins is illustrated diagrammatically for many groups by Winterbottom (1974). In most, small and large fiber portions of the fin musculature are anatomically similar in arrangement, the small-diameter fibers lying superficially to the larger-diameter fibers. In rays, the pectoral fin muscles are divided into superficial small bundles of small-diameter fibers, which arise on the pectoral girdle, and pass along the fin rays, to insert about halfway across the “wing” of the ray. These muscle fibers are, therefore, very long. By contrast, the larger-diameter fibers of the main portion of the fin ray musculature are arranged obliquely to the axis of the fin ray, inserting on the fin ray, and upon a connective tissue sheet underlying the superficial slow fibers. In this way, these fibers are virtually pinnate in arrangement. Calow and Alexander (1973) have shown how more power can be extracted from a pinnate fiber organization. In those teleosts where the fins are used for locomotion, e.g., Cymatogaster (Webb, 1975), or Gasteropelecus, the fibers are not pinnate, so far as is known. The arrangement in Holocephali is probably similar to that of the rays (see Kryvi and Totland, 1978).

IV. FIBER TYPES

A. General Considerations The muscle fibers of the myotomes or fins of few fishes have been examined histologically, yet fewer physiologically, but the different muscle fiber types found are remarkably similar in those fish where they have been studied. Although there are great differences in gen-

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era1 morphology between, say, acraniates and dipnoi, their locomotor muscle fibers are arranged in fundamentally the same way. It is reasonable therefore to generalize from the few cases which have been examined. At first sight this may seem surprising, but it is a consequence of the density of the medium in which fish swim. The greater part of the drag opposing forward motion in most fishes is skin friction drag (see Chapter 3), approximately proportional to Vz, so that the thrust required at constant speed will also be proportional to Vz, the power required from the locomotor muscles proportional to V3. There are complications of detail in the power dependence of the velocity (owing to uncertainties about the forcelvelocity curves of fish muscle and the nature of the boundary layer, see Webb, 1975; Bone, 1975) but this is an order of magnitude argument: Increased speed in water requires a great increase in power output. It is common observation that in individual species speed ranges of at least four times, and sometimes u p to twenty times are found; such performances demand a wide range of power from the locomotor system, and have led to a highly specialized arrangement of the locomotor muscle fibers. Faced with the conflicting demands of low speed cruise economy, and short bursts of maximum speed, all fishes have devised the same solution, and have divided the locomotor musculature into two very different parts, each specialized for one of these functions. Naturally enough, as we should expect, the muscle fibers composing each of the two conttasting parts are entirely different in design, differentiated by a whole spectrum of histological and ultrastructural features, as well as by biochemical and physiological criteria. For example, the “cruising” muscle fibers have a high content of mitochondria and high oxidative enzyme activity, as compared with the fiber type used during burst locomotion. The remainder of this chapter will mainly b e concerned with considering these differences, which are summarized in Table I1 and Fig. 5. Most fish use the same locomotor organs (caudal region and caudal fin, or paired pectoral fins) whether they are cruising slowly or swim-. ming rapidly for short bursts, and the two different parts of the locomotor system are therefore adjacent to each other in the myotomes or in the fin muscles. In rays, for example, the paired fins are employed during slow and fast swimming. In Holocephali, however, and such teleosts as labrids, many carangids, notopterids, young stromateoids, and alepocephalids, the paired fins only are used during slow swimming, and the myotomal musculature only during bursts of rapid swimming so that the two main muscle fiber types are physically divorced from each other.

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A Comparison of Fast and Slow Muscle Fibers in Fish Slow Smaller diameter (20-50% of fast) Well vascularized Usually abundant myoglobin, red color Abundant large mitochondria Oxidative enzyme systems Low activity Ca*+-activatedmyofibrillar ATPase Little low molecular weight protein Stored lipid and glycogen Myosatellite cells abundant Sarcotubular system usually less in volume than in fast fibers Z-lines broader than fast fibers in some cases Distributed cholinergic innervation Subjunctional folds usually absent Lower resting potentials than fast fibers N o propagated muscle action potentials, except under experimental conditions Long-lasting contractions evoked by depolarizing agents

Fast Larger diameter (may be more than 300 Pm) Poorly vascularized No myoglobin, usually white Few smaller mitochondria with fewer cristae Enzymes of anaerobic glycolysis High activity of enzyme Rich in low molecular weight protein Glycogen stored, usually little lipid Fewer myosatellite cells Relatively larger sarcotubular system Z-lines usually thinner than in slow fibers Focal or distributed cholinergic innervation Subjunctional folds usually present Higher resting potentials Propagated muscle action potentials usual; may not always occur during activity of multiply innervated fibers Brief contractions evoked by depolarizing agents

In a crude way, the two main fiber types can be recognized macroscopically, even where they are both found together, because in most fish, fiber types are segregated so that a region of fibers rich in myoglobin with a large vascular bed appears as a red or pink zone as compared with the adjacent pale zone of fibers of contrasting type. The vascular bed of teleost red and white muscle has been described by Mosse (1978) and by Bone (in press). The striking difference between the vascularization of the two main fiber types can be seen by the tenfold difference in the capillary to muscle fiber ratio in favor of the red fibers. In the myotomal musculature of many fish, a superficial red layer of fibers covers the main mass of myotomal white fibers (Fig. 4).The proportions of these two fiber types differ in different species (Table 111). There are some difficulties in comparing data given by different workers, for example, Greer-Walker and Pull (1975) examined the proportion of red and white fibers at a given level in different

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Fig. 5. Schematic comparison between slow fiber (above) and fast fiber. The fast fibers of some teleosts (see text) are multiply innervated. On the left, a transverse section showing comparative capillary and mitochondria1 density.

fish, whereas other workers have calculated the total amounts of the two types of fiber within the myotomes; moreover the proportions of the two fiber types may change with fish size (Magnuson, 1973). In 84 species examined by Greer-Walker and Pull (1975),red muscle fibers never constituted more than a quarter of the total myotomal Table 111 Relative Amounts of Slow and Fast Myotomal Muscle Fibers in Different Fish" ~~~

Species

Percentage of slow fibers in caudal region

Percentage of slow fibers overall

Scyliwhinus canicula Prionace glauca Scomber colias Gadus oirens Gadus pollachius Chimaera monstrosab Capros ape+ Raia spp!

18 22 30 11 3 0.6 0.5 0.0

8 10-11

" Data for teleosts and Chimaera

from Greer-Walker and Pull (1975). The last three fish swim slowly by means of the paired fins.

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musculature, and in most less than 10%.If only from consideration of the power output required from the musculature at different speeds, this distribution would suggest that the red fibers were employed during cruising, the much larger mass of white fibers during bursts of speed (see Section V). In few fish is this procrustean division of fiber types into red and white an absolute one, and although it is convenient to begin by considering the locomotor apparatus as composed of two main fiber types, it is important to avoid the temptation of falling into what Austin (1962) called the deeply ingrained worship of tidy-looking dichotomies. In most fish there are more than two fiber types and, apparently, some overlap in function between these different types. It is for these reasons that the original simple division of myotomal muscle fibers by their color [as, for example, by Lorenzini (1678) or by Arloing and Lavocat (1875)l is probably best abandoned. Nevertheless, the proportion of visibly red muscle in the locomotor apparatus gives some kind of an indication of the habits of the fish, and various workers have commented on this relationship (Boddeke et al., 1959; Bone, 1966; Greer-Walker and Pull, 1975); color is still a useful macroscopic guide to the fiber types which are found. This is, naturally, of particular importance in biochemical or electromyographic investigations. It is difficult to decide on an acceptable alternative to color as a description of the two main fiber types that does not have unsupported biochemical or physiological implications; but on the whole, it seems most appropriate to contrast slow and fast fibers. It is admittedly unsatisfactory to categorize muscle fibers by their speed when in very few instances only has this been determined, but other suggested terms, such as anaerobidaerobic, or twitchhon-twitch are still less satisfactory. In higher vertebrates, for example, in mammals (e.g., Burke et al., 1971), or in Anura (Smith et al., 1974), good correlations have been established between muscle fiber histochemistry, morphology, and speed of contraction; the method of glycogen depletion has proven invaluable in distinguishing the scattered fibers belonging to a single motor unit. The situation is very different in fish, for although morphologically and histochemically different fiber types are arranged in discrete zones or layers so that they can be distinguished by their position, the inconvenient physiological “preparation” of the myotome has not been investigated in any detail, so that no correlations have been established between fiber types and contraction velocity. Apart from crude experiments such as those of Ranvier (1873), Barets (1961),and Bone (1966) differentiating the contractions of slow and fast muscle fibers, nothing has been done in this regard for

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locomotor muscle fibers, apart from the elegant work of Tefavainen and Rovainen (1971) on lamprey slow and fast myotomal units. The significance of the various morphologically different slow or fast fiber types is therefore not clear, and the problem is complicated by the continuous growth of fish, for this may mean that some fiber types should b e regarded simply as stages in the development of others, rather than as types of especial contraction velocity and function. Thus Barker (1968) suggests that certain elasmobranch fibers are “slowtwitch” fibers, instead of “immature” twitch fibers (Bone, 1966), by analogv with the fiber types of higher forms, but this analogy may be invalid. Davies (1972) has shown that in mammals substantial changes take place in fiber types (based on histochemical criteria) as the muscle fiber population adapts to increase in body weight during growth; it is not yet known whether similar changes take place in fish muscle fibers, for detailed developmental studies are not available for any fish group (see Section IV,D). However, there is biochemical evidence, for example, in Anguilla anguilla (Bostrom and Johansson, 1972), that there are significant changes in enzyme activity profiles during development and growth, and these are probably reflected in such morphological parameters as mitochondria1 content and vascularization. I n most fish the slow fibers form a superficial sheet (the Seitenlinie) covering the main mass of myotomal fast fibers. In rays, the slow fibers form’a superficial zone in the fin ray muscle bundles. Presumably in these peripheral positions they are at a better mechanical advantage. They are only found deep in the myotome in secondarily flattened fish such as Rhina, or in fish where the slow fibers are operated above ambient temperature (Carey and Teal, 1966) (Fig. 4). There is some evidence that superficial and “deep” slow fibers in tuna aye different in properties (see Section IV,F,5). It may be that this reflects the effects of different fiber contraction velocity on different positions within the myotome, and myotomal muscle fiber arrangement and physiology in tuna should repay further study (see Sharp and Dizon, in press).

B. Histology Myotomal muscle fibers are often very long (in large fish, several centimeters) and insert at both ends into connective tissue sheets; fingers of connective tissue push into the ends of the muscle fibers in a complex interdigitation. At these points, there are couplings between the inpocketed tubes containing collagen fibers and the sarcoplasmic reticulum. These terminal couplings (first observed in anuran and

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lamprey muscle fibers b y Nakao, 1975)are also found in elasmobranch fibers, and probably in all fish fibers. Nakao suggested that the couplings represented sites of calcium transfer and were in some way related to growth in length of myofibrils, but there is no evidence for this function. It is perhaps more probable that the couplings represent the response of the sarcoplasmic reticulum to an ingrowing portion of the sarcolemma, analagous to the SR response to the T-system. The organization of the sarcoplasmic reticulum and T-system is similar in most fish groups, triads occurring at Z-line level (e.g., Patterson and Goldspink, 1972; Kryvi, 1977; Kryvi and Totland, 1978).Exceptions to this general arrangement are seen in the Agnatha and Acrania. Few quantitative studies of SR and T-systems in fish locomotor muscle have been carried out. Most of these (e.g., Hidaka and Toida, 1969; Nag, 1972; Korneliussen and Nicolaysen, 1975; Kryvi, 1977) agree with studies on other vertebrates where it is found that in slow fibers these systems concerned with activation are of lesser extent than in fast fibers. However, Patterson and Goldspink (1972) were unable to find significant differences between these systems in fast and slow myotomal fibers of Gadus virens, in agreement with Kilarski’s (1967) original observations. It is, perhaps, probable that in these cases where no obvious quantitative difference between the SR of slow and fast fibers can be discerned, the fibers may overlap in function, and the dichotomy of function may not be so clear as once assumed. For example, there is indirect evidence for Gadus virens that the “fast” fibers may be active at slow speeds (Greer-Walker and Pull, 1973). Morphological correlates of the metabolism of the different fiber types (manifested by their oxygen consumption, e.g., Gordon, 1968; Modigh and Tota, 1975) are seen in the different abundance, size, and cristal complexity of mitochondria (see Section IV,C), and also in the abundance of stored metabolites. Glycogen particles are found in all fiber types, usually as small units, but occasionally (e.g., in Scyliorhinus white fibers) in chain formations. Lipid is chiefly found in slow fibers, though in some species, such as Squalus, Cetorhinus, and Ruvettus, buoyancy lipid may be stored in fast fibers (Bone and Roberts, 1969; Bone, 197213). In “fatty” fish, such as herring or mackerel (Bone, in press), not only is lipid stored in the slow fibers, but there are fat cells among the muscle fibers (Fig. 6G). Metabolic lipids ofthis kind, as distinct from buoyancy lipid, are often found in close association with mitochondria as pointed out by Nishihara (1967) and Nag (1972). Ultrastructural investigations of fish storing wax esters in muscle fibers for buoyancy would be of some interest; it is possible that “metabolic” and “buoyancy” lipid stores may b e differently compartmented within the muscle fibers. During starvation (Greer-

Fig. 6. (A) Transverse section of the edges of a slow (S) and a fast (F) myotomal muscle fiber of amphioxus, showing the larger subsarcolemmal cisternae (representing the sarcoplasmic reticulum) in the fast fiber. (B) Multiply innervated myotomal fast fibers in Euthynnus. (C) Focal innervation of pectoral fin fast fibers in Scylioshinus. (D) Single e n d formation from multiply innervated slow fibers of pectoral fin of Scyliorhinus. (E) Multiply innervated fast fibers of pectoral fin of Periopthalrnus. (F) Rich vascular b e d of slow fibers from myotome ofEsor. (G) Lipid-filled cells adjoining capillaries in the fast myotomal musculature of Gempylus serpens; these cells probably contain wax esters to provide static lift. (H) Large-diameter axon passing to focally innervated fast fiber portion of pectoral fin muscle in Clupea. Note division of axon at arrows. ( I ) Terminal pattern of innervation i n the myotomal musculature of Alepocephalus. The myoseptum runs vertically at the right, muscle fibers pass from their insertions on the right obliquely to the left. (J) Focal innervation of fast fiber from pectoral fin ofRoia; several nerve processes pass to motor endplate. All except (A) from whole mounts of silver-impregnated material. Scale bars: 100 Frn except for (A) 0.5 pm.

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Walker, 1971; Johnston and Goldspink, 1973a,b), the different fiber types are affected differently; glycogen and protein diminish in the fast fibers although lipid and protein are little affected in the slow fibers. The result of protein loss is to increase the water content of the fibers to a maximum around 90%. A fairly large group of mesopelagic teleosts belonging to different families have the myotomal musculature naturally very watery as part of a general reduction of dense components in the absence of a swimbladder (Denton and Marshall, 1958; Blaxter et al., 1971).There has been no systematic investigation of the locomotor muscles in such fish; the few that I have examined (alepocephalids, stromateoids, stomatoids) have achieved economy of the dense myofibrillar protein components by reducing muscle fiber diameter and increasing interfiber spacing, as compared with normally dense fish of the same size. Greer-Walker (1971)found that after 130 days starvation, white (fast) fibers of cod were reduced in diameter by 40%, red (slow) fibers by 15%. Ultrastructural studies by Johnston and Goldspink (1973b) on carp starved experimentally for 16 weeks showed that protein decline in the white fibers due to starvation chiefly represented loss of myofibrillar protein. In the red fibers, mitochondria degenerated and disappeared. There are then some similarities between fish where reduction of dense components is a consequence of starvation, and the mesopelagic fish where it is part of the normal life of the fish. It has been found that both slow and fast fibers increase significantly in diameter during exercise (Greer-Walker and Pull, 1973). Bainbridge (1962) found no appreciable change in total muscle mass (in trout) after 1 year of continuous swimming, but his measurements did not take account of the (small) amount of slow muscle involved in this exercise. Slow fibers are smaller in diameter than fast fibers [between 22 and 53% on a series of marine teleosts examined by Greer-Walker and Pull (1975)] and are usually rich in myoglobin. Wittenberg (1970) has given grounds for supposing that myoglobin is equally distributed throughout the slow fibers, despite earlier attempts to localize it histochemically in specific regions of the sarcomeres in formalin-fixed material. In some groups, for example, Anura (Smith and Ovalle, 1973), several distinct fiber types are recognizable by their myofibrillar patterning [recalling the crude but useful distinction made by Kruger (1950) between Feldenstruktur and Fibrillenstruktur fibers], and it is probable that closer investigations will show that this is also the case for fibers in different fish groups. For example, superficial and slow fibers in sharks are recognizable in this way (Fig. 7) but distinctions between the different slow fibers have not yet been quantified. Very rapid mus-

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cles, such as those of the seahorse dorsal fin, are rich in sarcoplasm and have relatively few myofibrils (Bergman, 1964a). A similar paucity of myofilaments occurs in certain mesopelagic fishes where the dense myofilament proteins have been reduced for buoyancy requirements (see Section IV,E). The obverse of myofibrillar patterning is the mitochondrial distribution within the fibers. Here there is a rather wide range in size and abundance of mitochondria in different fiber types, and although quantitative studies are few, in some slow fibers mitochondria make up around 15-25% of the total cross-sectional area of the fiber (Patterson and Goldspink, 1972; Best and Bone, 1973).In Scomber, up to 45% of the slow fiber volume may be occupied by mitochondria (Bone, in press). In most fiber types, the distribution of mitochondria seen in cross section of the fiber is more or less uniform, but in some fibers there may b e a peripheral mitochondrial zone, with a central zone where mitochondria are absent or rare. In sharks, Kryvi (1977) found that subsarcolemmal mitochondria make up about 10% of the crosssectional area of the slow fibers. Accumulations of mitochondria are common under nerve terminals, particularly where these are not embedded within indentations of the sarcolemma (see Section IV,E). In some species, myelin figures derived from mitochondria are abundant in different fiber types, and occasional multilamellar bodies are also observed. The possible significance of these organelles is discussed by Kordylewski (1974) and Bone (in press). Individual fiber types in the different fish groups are considered in the next section. The reader is again warned to bear in mind that the general description of slow and fast fibers given above (summarized in Table I1 and Fig. 5) represent in most fish the different ends of a discontinuous spectrum of fiber types, so that in a given fish there may b e several morphologically distinct slow fibers, or two fast fiber types. The essential plasticity of the muscular system, well shown by the changes between silver and yellow eels (Bostrom and Johansson, 1972), naturally means that fiber types may differ more in related fishes of different habit than between, say, elasmobranchs and teleosts of the same habit, but Acrania and Agnatha have peculiar arrangements of their myotomal fibers that are not seen in other fish.

C. Ultrastructure and Histochemistry in Different Fish Groups 1. ACRANIA In amphioxus (Brunchiostomu),Flood (1966, 1968)has shown that there are three distinct fiber types, each only a few micrometers thick

Fig. 7. (A, B, and C) Histochemical differentiation of myotomal fiber types in Scylio rhinus. Stained for malate dehydrogenase activity. Sup, superficial fibers; SI and SII, type1 andtype11 slow fibers;FIandFII,typeIandtypeIIfastfibers.Alltosamescale. (D, E, and F) Low power electron micrographsofsuperficia1,typeI slow,andtypeIIfastfibers respectively; from young specimen ofScyliorhinus. Note differences inmitochondrial size

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Fig. 8. Diagrammatic view of amphioxus myotome as seen from an internal aspect, showing three types of muscle fibers, and their connection (at SC) with the motor neurons at the surface of the spinal cord. F, fast fiber; S, slow fiber; I, intermediate fiber. (Redrawn after Flood, 1968,Z. Zellforsch. Mikrosk. Anat. 84, 389-416.)

(Fig. 8). A T-system is absent, and in these exceedingly flattened fibers, the sarcoplasmic reticulum is represented only by subsarcolemma1 cisternae (Hagiwara et al., 1971; Flood, 1977) (see Fig. 6A). Similar cisternae (in addition to the more usual triad couplings) have been reported in various muscles of higher vertebrates (Spray et al., 1974); I have observed them in slow fibers of Scyliorhinus and they are probably figured in lamprey fibers by Teiavainen (1971, his Fig. 21). Superficial fibers contain abundant mitochondria and glycogen, as compared with the deeper mitochondria-poor fibers. The two fiber types send processes to the spinal cord (forming the ventral root “nerves”); each is in connection with a different region of the spinal cord. A third intermediate type of fiber was found to share this innervation region with the deep fibers. By analogy with other fish, it may be tacitly assumed that the superficial fibers (succinic dehydrogenase-positive) represent “slow” fibers, the deep fibers “fast” fibers. The unusual subsarcolemmal cisternae representing the sarcoplasmic reticulum support this identification, since these are larger in the deep than the superficial fibers (Fig. 6A). The status of the intermediate fibers is not clear. Flood suggests that they may perhaps be immature deep fibers, but the ontogeny of the system has not yet been examined at the ultrastructural level. Hagiwara and Kidokoro (1971) obtained physio-

and abundance, and in myofibrillar patterning. All to same scale. (G, H, and I) Different fiber types in the myotome oflophius, differentiated by succinic dehydrogenase staining. Note SDH-negative small diameter fibers in (G) (the superficial zone of the myotome), large SDH-negative fibers in (H) surrounded by SDH-positive fibers, and in (I), great variation in size of SDH-negative fibers from the fast zone of the myotome. All to same scale. Scale bars, 100 p m except for D, E, and F, 2 pm.

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logical evidence for electrotonic coupling of adjacent fibers, but as they pointed out, no gap junctions have been observed between fibers.

2. AGNATHA In lampreys, the myotomal muscle fibers are arranged in compartments (Fig. 9) built from more or less cylindrical small-diameter slow parietal fibers, enclosing several layers of flattened fast central fibers. In different species the arrangement of the central fibers differs slightly, but in all, the central fibers closest to the parietal slow fibers are different in several respects from those in the middle of the compartment. Thus these “juxtaparietal” fibers are richer in mitochondria and oxidative enzymes than are the interior central fibers and have a richer capillary bed (Lie, 1974). On histological or histochemical grounds they might b e considered to be an intermediate fiber type. However, ultrastructural and physiological investigations by Tefavainen (1971) have shown that all central fibers within a compartment are coupled together electrically, and that all contract together, although only the most central are innervated. There are desmosomal connections between central fibers and between central and parietal fibers, but (as in amphioxus) the usual gap junctions correlated with electrical coupling were not observed by Teravainen, or by Jasper (1967). SR and T-systems triads occur at Z-line level, but the T-tubules may run longitudinally along one sarcomere (Jasper, 1967). Tefavainen’s work showed conclusively that, despite some morphological diversity, the central fast fibers all operated as a unit. This result is of importance, for it shows that so-called intermediate fiber types recognized by virtue of ultrastructural or histochemical

Fig. 9. Diagrammatic view of lamprey myotome from an internal aspect. Note absence of innervation of intermediate fibers (I); innervation ofdeep central fibers (C); and multiple innervation of slow fibers bordering muscle unit (S).

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properties, need not have different functional characteristics from neighboring fibers of similar innervation pattern. We should be wary of multiplying functional fiber types on purely morphological grounds. Lie (1974) noted that in ammocoetes of Lampetra Juviatilis the compartments contained only a single central fiber, flanked b y two intermediate fibers, whereas the adult compartments contained one or two central fibers. He concluded that the new central fibers had differentiated from intermediate fibers and that the latter could be considered as stages of development of central fast fibers. In hagfish, detailed ultrastructural studies by Korneliussen and Nicolaysen ( 1973, 1975) have established three morphologically and histochemically distinct fiber types, first defined histochemically by Flood and Storm-Mathisen (1962) and by Dahl and Nicolaysen (1971). As in lampreys, the Myxine myotome is divided into muscle units composed of a regular arrangement of the different fiber types (see Fig. lo), and the three fiber types are segregated in these units in a regular way. Ultrastructhdly, the three fiber types are distinguished by their content of glycogen, lipid, and mitochondria, by the pattern of the myofilament fields, and b y the organization of the Z-lines. All three fiber types possess M-lines; all three possess a T-system with triads at the A-I junction (unlike those of other fishes); in each fiber type there is a different relation between fiber volume and volume of the T-system. The familiar arrangement of the T-system as a cpllar around the muscle fiber is not found in all fiber types in Myrine, and Korneliussen and Nicolaysen (1975) ingeniously analyzed the density of triads to show that slow fiber myofilament bundles are only rarely encircled by T-tubules, whereas fast fibers are rarely devoid of them.

Fig. 10. Hagfish myotome viewed from an internal aspect. Fast fibers (F) terminally innervated, slow fibers (S) irmervated by axons passing onto fibers from both myoseptal ends. Occasional intermediate fibers (I) scattered around borders of muscle unit next to slow fibers; these are apparently terminally innervated.

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Regular elegant views of the T-system and its segmental relations with the 'sarcoplasmic reticulum have been demonstrated in many teleosts (e.g., Kilarski, 1965, 1967),so that it may seem unusual to find such diversity in arrangement as demonstrated for Myxine. Nevertheless, as will be seen, a similar less ordered system is found in elasmobranch myotomal muscle, and is probably common during muscle fiber ontogeny in different fish groups. The ultrastructural differences between the three fiber types briefly considered above are similar to those of the elasmobranch, where they will be considered in more detail. It is important to notice that physiological investigation (Andersen et al., 1963) has only distinguished two functional fiber types, and the significance of the (morphologically) intermediate fibers is not yet clear, although myosin ATPase activity (Dahl and Nicolaysen, 1971) suggests that they may be intermediate in contraction speed.

3. ELASMOBRANCHS In the dogfish, Scyliorhinus, which has been studied in the most detail, four fiber types were initially recognized in the myotomes, on the basis of color, lipid content, and innervation (Bone, 1966). However, closer investigation (Bone et al., 1978b) has shown that while the distinction between fast, slow, and superficial fibers seems to be an absolute one, the fast and slow fiber types should each be subdivided further into two types. There are, then, in the dogfish myotome five types of muscle fibers recognizable upon structural and histochemical grounds [just as there are in the anuran limb (Smith and Ovalle, 1973)], but this is not to say that these all play different functional roles (see Section IV,F,4). The general arrangement of the myotome is seen diagrammatically in Fig. 11; Figure 7A-C shows the distribution of fiber types seen after malate dehydrogenase staining. Similar results are obtained when sections are incubated for other oxidative enzymes such as citrate or succinate dehydrogenase (SDH). After incubation for Ca2+-activatedmyofibrillar ATPase (Bone and Chubb, 1978), the same five fiber types are distinguishable; the ATPase activity increases from the outer surface of the myotome inward and is lowest in the superficial fibers and highest in the inner fast fibers. The outer border of the myotome consists of a single, sometimes interrupted, layer of SDH-negative superficial fibers, forming a sort of thin skin over the myotome. Such superficial fibers are not found in all sharks. I have not observed them in the spurdog SquaZus acanthias (Fig. 12), for example, and they do not occur in Galeus or Etmopterus (Kryvi, 1977). Immediately below (internal to) the superficial fibers

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Fig. 11. Scyliorhinus myotome from an internal aspect. Superficial fibers (SU) overlie slow fibers (I and 11); fast fibers are terminally innervated and mainly of type I. Note dual innervation of fast fibers.

are the typical slow fibers, or type I slow fibers, which are strongly SDH-positive. There may be a number of layers of these type I slow fibers, but they then merge into a second type of slow fiber which is less strongly SDH-positive, and usually larger in diameter than the type I fibers. There are two or three layers of these type I1 slow fibers, and an abrupt discontinuity where fibers that are nearly completely SDH-negative begin and make up the remainder of the myotome. At the zone of contact with the type I1 slow fibers, thesefast fibers are

Fig. 12. Diagrammatic transverse sections of postanal region showing fiber types in myotomal musculature. Upper row, fast fibers focally innervated; lower, fast fibers multiply innervated. A, Clupeids, probably also eels; B, Scyliorhinus; C, Squalus, probably also Dipnoi; D, Salmonids, some cyprinodonts; E, Some cyprinodonts, gadoids; F, Lophius. Slow fibers, dark hatching; intermediate fibers, light hatching; fast fibers, unhatched.

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only a little larger than the slow fibers in diameter, and faintly SDHpositive. As the interior of the myotome is approached, after three or four rows of fibers, the type I fast fibers merge into larger SDHnegative type I1 fast fibers. Apart from the mosaic arrangement of salmonids, or the little known Lophius pattern, this myotomal organization is as complex as any and hence may be taken as a paradigm of the fiber types in fish locomotor musculature. The ultrastructure of these different fiber types are shown in Fig. 7D-F. It is evident that the superficial fibers are entirely distinct from the adjacent type I slow fibers, and from the type I fast fibers with which Brotchi (1969) equated them. The inconspicuous M-line, virtual absence of lipid, the paucity and simplicity of the mitochondria, and the few triads of T-system and SR set these fibers aside as a particular type rather different from either slow or fast fibers. Fortunately, their position in the myotome allows us to categorize them by a noncommittal term1 Interestingly enough, the superficial fibers at hatching are characterized by a simple myofibrillar arrangement recalling that of embryonic muscle cells, although the other fiber types are similar to their homologues in the adult fish. The slow fibers of both types are rather similar ultrastructurally, differing in details of myofibrillar arrangement and mitochondria1 density, but they are clearly separated histochemically when myotomal sections are incubated for glucose phosphoisomerase, since the type I1 slow fibers are positive, while the type I fibers are virtually negative. The fast fibers of both types differ from both types of slow fiber in the virtual absence of mitochondria, in a thinner Z-line, more extensive sarcoplasmic reticulum, and abundant triads with the T-system. It is not yet clear whether the T-system is significantly different in slow and fast fibers: Identical values of C, (membrane capacitance) were obtained b y Stanfield (1972) for both types of fibers (Table IV). In Galeus and Etrnopterus, Kryvi (1977) found similar values for T-tubule volume in slow, fast, and intermediate fibers, but the volumes of sarcoplasmic reticulum were higher in fast than in slow fibers. There are relatively more mitochondria in the type I fast fibers, and these fibers are weakly SDH-positive (they were originally termed intermediate fibers). Again, there seems to be a transition from type I to type I1 fast fibers over several fiber rows, the general impression gained is that the type I fibers are in some respects like the adjacent type I1 slow fibers, but that divorced from this propinquity, the fast fibers are uniformly of type 11, evidently highly specialized hnctionally. In Torpedo, but not in Scyliorhinus, type I fast fibers are differently innervated to type I1 fast fibers.

Table N A Comparison of Membrane Properties of Different Fish Muscle Fibers' Resting potential (mV)

Diameter (pm)

-85.2 -71.7

150 50

0.14 0.75

108 136

SIOW

-82.4 -73.1

60 63

1.01 1.4

294 389

fast slow

-87.8 - 74.5

fast

-75-85 -46 - 53

Species

Sc yliorhinus Myotomal

fast

SIOW Carassius Fin

Lamvetra Central Myxine Myotomal

fast

S~OW

Amphioxus

Input resistance

RP Rm 7 Cm (M) (Wcm) (Idl/cmz) (msec) (pF/cm2)

0.19 8.5 56-155 56.4 1-2 pm thick

10.0 0.8-1.2

40 40

1.59 5.4

15.9 47

10.3 10.2

A (mm)

2'36 2.27

Stanfield (1972)

'"

Hidaka and Toida (1969)

10.9 7.0

48'4 26.6

2.55

2.1

5.0 30.0

4.4 123

2-6 4.0

250pm 4.0

7'23

3.68 2.25

5.5 39.6 1.2-2.0

Authority

Teravainen (1971)

Nicolaysen (1976a,b) Hagiwara and Kidokoro (1971)

Most values are the means of a number of experiments. Different experimental techniques and assumptions complicate direct comparisons between different species. Ri, specific internal resistance; R,, membrane resistance; T , time constant; C,, membrane capacitance; A, space constant.

386

QUENTIN BONE

Although ray fin muscle was long ag0,investigated b y Ranvier

(1873), it has received little attention since that time. As in the myotomes of sharks, there are slow and fast fibers distinguished b y their color, diameter, and SDH activity (Bone and Chubb, 1975);superficial fibers are apparently absent, but there are both SDH-positive and negative small-diameter “slow” fibers, These fibers form a superficial strap in each fin ray muscle, unlike the “pinnate” fast fibers (see Section IV,A).

4. TELEOSTS Slow and fast fibers (red and white fibers) were first characterized morphologically in teleosts (Arloing and Lavocat, 1875), and subsequent investigations at the ultrastructural level have apparently confirmed the existence of only two fiber types in several teleosts (Buttkus, 1963; Kilarski, 1965, 1967; Nishihara, 1967; Patterson and Goldspink, 1972; Nag, 1972). As usual, the two fiber types are distinguished b y diameter, mitochondria1 and lipid content, and sometimes by Z-line thickness and b y difference in volume of the tubular systems. In some cases, e.g., in the fin muscle of goldfish, Carassius, or in the myotomal musculature of pike, Esox, no differences were observed between the sarcotubular systems of the two fiber types. As Nag (1972) remarks, it is possible that earlier workers did not appreciate the difficulties of making accurate estimates of the T-system. Since a large part of the membrane capacitance of the fiber resides in the T-system, it is desirable to know values of C, to check morphological estimates of the extent of the T-system. In Carussius, fin muscles, for example, C, for fast fibers is 7.23 pF/cm2, as compared to 2.55 pF/cm2 for slow fibers (Hidaka and Toida, 1969); although Nishihara (1967) did not note any difference in extent of the sarcotubular systems in the two fiber types, it is probable that such could only be detected by quantitative electron microscopy. It seems to be the case that the volume of the sarcoplasmic reticulum (that is, the internal tubular system excluding the T-system) may be very similar in both slow and fast fibers, even if the volume of the T-system may be different. It is possible that Patterson and Goldspink (1972) were unable to demonstrate sarcotubular differences between slow and fast fibers in Gudus virens because SR and T-system were considered together. In many teleosts (e.g., catfish, Barets, 1952; Mollienesia, Franzini-Armstrong and Porter, 1964), the muscle fibers have peculiar ribbonlike myofibrillar bundles round the edges of the fiber. In

6.

LOCOMOTOR MUSCLE

387

species with fibers of smaller diameter, these elongate bundles may occupy the entire fiber which then resembles a wheel with the myofibrillar bundles arrayed like spokes from a small central sarcoplasmic hub. This ribbonlike myofibrillar arrangement [which was utilized b y Lansimaki (1910) to categorize several muscle fiber types] is apparently unique to teleosts. However, sufficient investigation has not been made in such groups as Holostei and Dipnoi to exclude these: Certainly ribbon-myofibrils are not found in elasmobranchs, holocephali, or higher vertebrates, so far as is known. Lansimaki’s different categories have not been found valuable in distinguishing functionally different muscle fiber types, but the simple duality of teleost muscle fiber types described so far (even if true in the cases mentioned), is in many teleosts complicated by the existence of “intermediate” fibers, and b y the mosaic organization of the myotomes in different species. Barets (1952) described type I fast fibers (his aberrant fibers) in the catfish Ameiurus, and Greer-Walker (1970),using lipid staining noted in cod (G. morrhua), that there was an apparent mosaic arrangement among the type I1 fast fibers, as well as an intermediate fiber type lying between the slow and fast fibers. The situation in cod has been examined b y Korneliussen et al. (1978). Brotchi (1968) described intermediate fibers in carp (C. carassius) on the basis of SDH staining [they make up 7% of the myotome (Johnston, 1977)], and both SDH and myofibrillar ATPase activity differentiate several sorts of fiber in the herring Clupea harengus (Bone et al., 1978a), in the angler (Lophius),and in various other species (Johnston and Tota, 1974; Patterson et al., 1975; Mosse and Hudson, 1977). Figure 13 summarizes these various results. As yet, insufficient ultrastructural investigations have been made to allow comparison of these different fiber types with those of elasmobranchs. It seems evident, however, that the superficial red fibers correspond in all to type I slow fibers, but it is not clear whether “pink” or intermediate muscle fiber types should be considered as part of the slow or fast systems. In carp, Johnston et al. (1977) have shown intermediate fibers to b e active at intermediate swimming speeds (see Section IV,G). The mosaic arrangement reported in cod by Greer-Walker (1970) is similar to that observed in the deep lateral (fast) muscles of herring and Lophius where larger diameter fast fibers (equivalent to type I1 fast fibers of elasmobranchs) are surrounded by a regular array of smaller diameter fibers which are richer in mitochondria, slightly

388

QUENTIN BONE ACANTHOPTERYCII

CARACANTHOPTERYGll

Lophllformr

I

Coblnwiformrr

P8rclform darlntlrct

I

Smrprenlforma Burxholdlformer

\I

ATHERINOHORPHA

-

\ OSTEOGLOSSOMORPHA

\--7 **- .

Jurassic Protoelopold

’

Pholldophorold

1 holorceans

\

PROTACANTHOPTERYGII

I

.

. .

Mrctophoidr Alcpocephalidr

>’’

Fig. 13. Distribution of terminally innervated fast fibers (underlined) in teleost groups. All higher teleosts have multiply innervated fast fibers. Only Hiodon of the Osteoglossiformes has terminally innervated fast fibers; a few catfish of the Ostariophysi also show terminal innervation. (Modified from Bone, 1970; redrawn from Greenwood et d., 1966, B d . Am. Mus. Nat. Hist. 131, 339-456.)

SDH-positive, and contain more glycogen than the type I1 fibers. These fibers (Fig. 71) are probably to b e equated with the type I fast fibers of elasmobranchs. Korneliussen et al. (1978)have categorized no less than seven different fiber types in cod (on the basis of cryostat sections incubated for different enzymes), and three of these are found in the deep “fast” motor system. As these authors imply, it is an open question whether histochemical and morphological diversity of this kind in the teleost fast motor system (indeed in elasmobranchs and agnatha also) reflects functional diversity, or whether it is a simple concomitant of the extensive pattern of growth in fishes. In lampreys, the accident of coupling between the central and intermediate fibers (Ter‘avainen, 1971, see Section IV,C,2) taken together with Lie’s observations on growth strongly suggest that intermediate fibers should properly be considered as growth stages in the formation of type I1 fast fibers. We do not know whether this is the case in other groups of fish,

6.

LOCOMOTOR MUSCLE

389

but the results of Korneliussen et al. (1978)certainly are most simply interpreted in this way. The problem of the status of intermediate fiber types distinguished by morphology and histochemistry is particularly acute in salmonids. Here, it has long been recognized that there are small-diameter “red” fibers scattered among the deeper portion of the myotome, as well as segregated in a superficial lateral zone, as in other fish. T h e mosaic of the deep portion of the musculature (Boddeke et al., 1959) was at first interpreted as a mixture of fast fibers with slow fibers that were the same as those of the lateral zone, i.e., that salmonids possessed “extra” slow fibers (e.g., Webb, 1971). More recently, Johnston et al. (1975) have examined the histochemistry of fiber types in Salmo gairdneri, and conclude that the mosaic portion of the myotome is composed of large-diameter fast fibers, and of small-diameter fibers which differ from those of the superficial zone in SDH and myofibrillar ATPase activity. Their conclusions ?re summarized in Fig. 12D. The similarity with the pattern found in the herring or in Lophius (Fig. 12F) is striking, and it is equally striking that there is in the mosaic muscle an almost continuous distribution of fiber size (from 15 to 95 pm). Evidence from electromyography of salmonids (Hudson, 1973; Bone et al., 1978a) considered in Section IV,G, is conflicting, and as yet, insufficient to decide whether slow fibers are intermingled with fast fibers, or whether the morphologically and histochemically similar mosaic of clup‘eids and gadoids indicates that the small-diameter fibers of the salmonid myotome are growth stages in the development of the larger fibers. A special case is presented by Lophius (Bone and Chubb, 1978)for in the myotomal musculature of this relatively inactive fish, there are a great variety of fiber types. As well as the mosaic fibers-of the deep (white) portion of the myotome, already referred to, which resemble those of salmonids or clupeids, Lophius is remarkable in having among the usual SDH-positive, lipid-rich, small-diameter fibers of the superficial lateral zone (the type I slow fibers), both bundles of SDHnegative, lipid-poor small-diameter fibers, and also occasional similar fibers of large diameter. This complex situation is seen in Fig. 7G-I. These fiber types are found in Lophius. of different sizes; their significance is not understood, for although the mosaic arrangement in the deep portion of the myotome may b e viewed as a consequence of a pattern of continued growth, it is less easy to interpret the arrangement in the superficial zone in such a way. It is obvious that further investigations are needed, both of the physiology of fiber types, and of their development in the mosaic muscle.

390

QUENTIN BONE

In thefins, so far as is known, slow and fast fibers are segregated, as they are in the fin muscles of other teleost groups (e.g., Nishihara, 1967).

D. Ontogeny of Fiber Types There are two linked problems in the differentiation of muscle fibers in fish. First, there is differentiation in embryonic development giving rise to the fiber types and relative numbers found on hatching or metamorphosis; second, there are the separate problems raised b y the continuous growth in all fish and, in some, the changes occurring prior to a migratory phase (as in AnguiEla). As the fish grows, increasing in length and mass, the relative amounts of slow and fast fibers change (at least in some species), in addition to actual increase in numbers of each fiber type. In other species, such as some of the pelagic stromateoids, there is a complete change in locomotor behavior during adolescence, which is probably again reflected in changes in the relative amounts of slow and fast fibers. How are the various fiber types differentiated, and what are the mechanisms for the changes observed in the fiber populations (e.g., Magnuson, 1973) as fish grow? Although it is manifest that (as Nag and Nursall, 1972, put it) “fish muscle fibers offer an interesting problem in differentiation because of the presence of two types of fibers (white and red) which are involved in two kinds of swimming activities, which in their turn appear in different stages of development of the fish,” there are few recent studies of these problems. In teleosts, Nag and Nursall studied the histogenesis of fiber types in the myotomes of Salmo gairdneri up to the free-swimming fry stage, and Waterman (1969) examined the development of the same system in the cyprinid Brach ydanio rerio. Fortunately both accounts are in substantial agreement, strongly indicating that differentiation begins from the inner (medial) face of the myotome outward and that (in the way that Vialleton, 1902, had suggested) deep myoblasts differentiate into deep fast fibers, whereas surface myoblasts later differentiate into the superficial slow fibers. As Waterman emphasized “the two main fiber types exhibit structural differences from the time of their formation and differentiate along separate pathways leading to dissimilar adult configurations.” The somites are initially made up of more or less rounded cells with large intercellular spaces between them; as development continues these cells become more closely apposed and either develop

6.

LOCOMOTOR MUSCLE

391

specialized embryonic or focal intermediate junctions (Bruchydunio) or adjacent cell membranes show indications of fusion (Salrno).The medial cells in each somite then elongate and begin fibrillogenesis to become myoblasts, containing bundles of myofilaments and the beginnings of a patterned SR. At this stage, the superficial presumptive myoblasts of the somite are not much elongated, nor do they contain myofilaments. These develop at a later stage, by which time the deep myoblasts have developed myofilament fields and may b e considered as young fast muscle cells. During this process, the myoblasts destined to become fast muscle fibers become relatively less rich in mitochondria; indeed, the early myoblasts are, perhaps, more similar to the developed slow fibers than they are to the developed fast fibers. This is not to say that fast fibers pass through an “embryonic” slow stage, or that all myotomal fibers commence as slow fibers; development of the two seems to be quite separate. Waterman found that fibrillogenesis could occur either in mononucleate myoblasts or in the multinucleate later stages of the deep myoblasts, but he did not observe nuclear division or cytoplasmic fusion in his material. On the other hand, Nag and Nursall observed appearances indicating cytoplasmic fusion at different stages and suggest that multinucleated fibers are derived by coalescence of myoblasts and presumptive myoblasts. It is certainly possible that there are species differences and perhaps more significantly, differences between embryos of different dimensions, but further investigations are needed before a “norm” of development can b e established. I n any event, considering only the broad categories of slow and fast fibers, these are apparently “fixed” from an early stage, and it is natural to ask whether this dichotomy is regulated by the nervous system. Waterman (1969)observed the first axons in the myotomes close to the medial ends of young superficial muscle cells, and concluded that this fiber type was the first to come under nervous control. Previous large irregular movements of the embryo were held to be due to myogenic contractions of the deep fast fibers, as yet not in connection with the nervous system. In a similar way, Nag and Nursall observed initial twitching movements of advanced embryos within the eggs, and stimulation of early larvae produced only short bursts of vigorous tail beats. Slow tail movements were not observed until a later stage, as Waterman had found. The early development of swimming movements is probably best known in dogfish (Harris and Whiting, 1954), and a preliminary study of the development of fiber types in dogfish ontogeny has shown the sequence to b e similar to that in teleosts. That is, deep fast fibers develop first and seem to become

392

QUENTIN BONE

innervated later than the slow fibers which appear after the fast fibers in ontogeny. The last fibers to appear are the superficial fibers which even after hatching are notably “embryonic” in appearance. Later development of Etmopterus slow and fast fibers has been studied by Kryvi and Eide (1977), who found that postembryonic growth takes place largely by muscle fiber hypertrophy; evidently this process gives rise to the notably uniform diameter of fibers in the fast region of the adult myotome, as compared to that in such teleosts as carp or herring, whose differentiation of fibers from myosatellite cells presumably continues throughout growth. Willemse and van den Berg (1978) examined the growth of myotomal fibers in Anguilla over a %year period and found that initial growth of red fibers takes place by increasing in diameter; later, new fibers are added, as they are in the white zone of the myotome at all stages, probably from myosatellite cells. Underlying the early myogenic activity of the deep fast fibers of the myotomes in both dogfish and teleosts are longitudinal connections between the muscle cells of adjacent somites, first observed in teleosts by Waterman. These interm yotomal connections are transient in both groups, presumably disappearing as the deep fibers receive innervation from the segmental nerves. It does not seem then, that the fiber types differentiate from an uniform population of late myoblasts following outgrowth of motor axons of different motoneuron classes, but it is obvious that further work is needed before the regulation of myogenesis is understood. I n this field, fish muscle offers interesting material to the experimental embryologist, for the general agreement that fiber types are fixed from an early stage, and the segregation or zonation of fiber types at once suggests possibilities of experimental alteration to determine the effects of propinquity of one fiber type upon another, or the influence of innervation upon the different fiber types. More detailed histological studies are needed too, particularly upon species which have “intermediate” fibers of various sorts, and upon scombroids with a medial mass of slow fibers. It will not have escaped notice that Nag and Nursall’s description of the development of the salmonid myotomal fiber types up to the free-swimming stage only dealt with superficial slow fibers and deep fast fibers. Yet in the adult salmonid, the deep portion of the myotome is typically “mosaic” (Section IV,C,4), containing a mixture of fiber types. It is not yet clear how this mosaic fiber population arises, nor (in other species) how the relative amounts of slow and fast muscle fibers are altered. The continuous growth shown by fish is reflected in some

6.

LOCOMOTOR MUSCLE

393

species, for example, Lophius (Figs. 12F and 7G-I), by patterns of muscle fiber types arranged in such a way that the generation of the arrangement is evident. I n most fish which have been examined, myosatellite cells are abundant and show in young specimens all stages of development of myofilament fields. I n the shark Galeus melastomus Kryvi (1975) found that myosatellite cells were about twice as abundant on the slow fibers as on the fast fibers. As he observed, the presence of peripheral microtubules, of extensions deep into the body of the muscle fiber, as well as lysosomes and dense bodies in the satellite cell cytoplasm, all suggest that the functions of fish myosatellite cells have not yet been fully determined and the possibility of some trophic influence on adjacent cells has been suggested (Flood, 1971). No detailed study has yet been made of the organization of satellite cells in fish of different ages (see, however, Kryvi and Eide, 1977), but preliminary examination of Scyliorhinus material indicates that they become less abundant as growth proceeds, in accord with observations in teleosts by Nag and Nursall(l969). It is agreed that myosatellite cells are persistent myoblasts, and that increase in fiber number during growth is attributable to differentiation of myosatellite cells, but how this process is regulated is unknown. The view that the mosaic nature of the myotomal population in many teleosts is simply a reflection of continued differentiation of myosatellite cells has certainly the merit of simplicity. If it is true, then growth in sharks seems to occur rather differently, since their myotomes do not show a mosaic of fiber size. Nor, however, does there seem to be a special growth zone (for example, between the deepest slow fibers and the most superficial fast fibers) so that it is not known how the system increases in fiber number. Plainly, slight changes in the rates of differentiation of myosatellite cells in the slow and fast portions of the myotome during growth will result in changes in the relative amounts of slow and fast fibers in the myotomes, such as are found as fish increase in size.

E. Innervation The innervation of fish muscle fibers presents unusual features since many fish have multiply innervated twitch fibers, and the pattern of innervation is of taxonomic value. There are, further, hints in some fish motoneurons of transmitter substances other than acetylcholine, and of dual innervation of the muscle fibers. In all fish groups, myotomal superficial slow fibers are multiply

394

QUENTIN BONE

innervated by small-diameter myelinated fibers that terminate in en grappe endings (Barets, 1961; Bone, 1964, 1966, 1970; Best and Bone, 1973). Where two types of slow fiber are recognized, as in dogfish, both are innervated in a similar way. In teleosts, the nerve terminals are usually embedded in the sarcolemma, and subjunctional folds are absent (Nishihara, 1967; Barets, cited in Barker, 1968); in dogfish, there are subjunctional folds under terminals on superficial and type I and type I1 slow fibers (Bone, 1972a). The slow fibers of the hagfish myotome are innervated by two axons only, passing onto the fiber at each of its myoseptal insertions (Andersen et al., 1963) but in other groups, more than two axons probably innervate each slow fiber. I n the fins, slow fibers are also multiply innervated, although the endformations may be larger than in the myotomal slow fibers (Fig. 6D and J). The interval between terminals along slow muscle fibers has been measured in a number of preparations and where the membrane constants of the fiber have also been measured there is a normal safety factor of around 10 times. For example, Stanfield (1972) found A to be around 2.27 mm for slow fibers in dogfish myotomes; motor terminals along these fibers are some 150-200 pm apart. Acetylcholinesterase is demonstrable at the terminals on all slow fibers investigated; in teleosts Pecot-Dechavassine (1961)found that other esterases (e.g., butyrylcholinesterase) are absent. However, an interesting possibility has been raised in hagfish, b y Korneliussen’s (1973) suggestion that slow fibers may have monoaminergic innervation. He showed that dense core vesicles were especially abundant in nerve terminals on slow fibers of the hagfish myotome and craniovelar muscle, although formaldehyde-induced fluorescence proved inconclusive. Earlier work by Andersen et al. (1963) showed that acetylcholine was probably the transmitter at the neuromuscular junctions on slow and fast fibers in the myotome; Korneliussen’s observations await further investigation. To judge from pictures by Teriivainen (1971) and Nakao (1976), dense-core vesicles are not found in unusual number in lamprey slow fiber terminals. The innervation of fast fiber types is, however, of more interest than that of slow fibers, for there are large differences between different fish groups, such that the pattern of innervation may serve as a taxonomic character (Bone, 1970). In all groups except most of the teleosts, the fast fibers are focally innervated at their myoseptal ends (Fig. 61); sometimes at both ends of the fiber (according to Barets, in Ameiurus),but more usually, at one end of the fiber only (in hagfish and elasmobranchs). This terminal innervation is also found in amphibia (at both ends of the fiber) and seems to be the original innervation pattern in lower chordate myotomal fast fibers. Best and Bone

6.

LOCOMOTOR MUSCLE

395

(1973) have suggested (see also Bone, 1975) that this innervation pattern is part of the various specializations of the fast fibers to increase power output b y devoting the maximum space to myofilaments. In elasmobranchs, in urodele amphibia, and in certain teleost groups, each fast fiber is apparently innervated by two separate axons, which both contribute to the formation of a single motor endplate. In most of these forms, there is no recognizable difference between the two motor terminals, but in some elasmobranchs (Bone, 1972a) they are recognizable by their different vesicle content. One type of terminal at the endplate contains “typical” cholinergic electron-lucent vesicles 50 nm diameter, while the other contains a high proportion of much larger dense core vesicles (up to 100 nm). As in the hagfish slow fibers, formaldehyde-induced fluorescence studies have so far proved inconclusive, and only acetylcholinesterase has been found in the subsynaptic folds. The significance of this dual innervation is therefore unresolved. In the dogfish, as in most focally innervated species examined, every type of fast fiber is innervated terminally, even if (as in herring) they may be diverse in size. So both type I and type I1 fast fibers are terminally innervated in dogfish, and no difference has been recognized between the motor terminals on each fiber type. But in two cases, the “aberrant” fast fibers of Ameiurus (Barets, 1952), and the most superficial fast fibers of the myotomes in Torpedo (Bone, 1964), there is focal innervation in the midregion of the fiber. Again, the significance of this situation (rather unusual in fish groups with terminal innervation since it has not been observed in clupeids, eels, holostei, dipnoi, sharks, or other rays) is not understood. No intermediate types of innervation are observed, and it does not seem very probable that the terminal innervation pattern is derived from the midregion en plaque type. In Ameiurus (and possibly also in Torpedo),these peculiarly innervated fast fibers lie external to the connective tissue fascia separating the slow fibers from the main mass of fast fibers. It is premature therefore to equate them with the type I fast fibers in dogfish, and to suppose that their different innervation precludes the type I fast fibers of other fishes from being developmental stages in the formation of type I1 fibers. Terminal innervation is found in certain teleost families (Barets, 1961; Bone, 1964, 1970);these have an interesting taxonomic distribution (Fig. 13). It is apparent from Fig. 13 that no acanthopterygians have this pattern and that, of the families regarded as primitive on other grounds, only the salmonids lack the terminal innervation pattern. The systematic position of a number of the groups possessing terminal innervation (for example, the alepocephalids) has not been

396

QUENTIN BONE

agreed upon. The pattern of innervation of other taxonomically vagrant groups (e.g., many deep-sea families) has not been examined. The “innate conservatism” of soft parts should allow us to employ muscle innervation as a character in determining the relationships of teleosts where skeletal structures give conflicting evidence for their affinities. With the exception of the groups indicated in Fig. 13, all teleost families so far investigated (species in 55 families have been examined) have an entirely different innervation of the fast fibers. Each muscle fiber is multiply innervated (Barets, 1961; Hudson, 1969); the innervation is similar to that of the superficial slow fibers, distributed and punctate (Fig. 14). According to Barets the fast fiber innervation is more distributed than that of the superficial slow fibers. As in the slow fibers, the motor terminals are embedded in the sarcolemma and subjunctional folds are absent. The richness of the innervation of teleost multiply innervated fast fibers is astonishing (Fig. 6B and E); the nexus of axons resembles the capillary bed of slow fibers in its abundance and nerve terminals are scattered all along the muscle fibers. The contrast with focal terminal innervation as seen in other fish fast fiber systems is very great and invites functional interpretation (see Section IV,F,5). Thus far, myotomal muscle fiber types have been considered. In the fin muscle, a similar division exists between the multiply innervated fast fiber fin muscles of higher teleosts (Fig 6E), and the focally innervated fast fibers of other groups (Fig. 6C). I n the fin fast muscle fibers, however, innervation is not terminal; large en plaque endings are found in the midregion of the fibers. These end-formations may be very large, and derived from several branches of the same axon which have divided earlier along its course and come into proximity again at

Fig. 14. Higher teleost myotome viewed from an internal aspect showing multiple innervation of all fiber types. It is not known whether any overlap of innervation takes place between fast (F) and intermediate (I) fibers.

6.

LOCOMOTOR MUSCLE

397

Fig. 15. Drawing from whole mount preparation of fast fibers of pectoral fin in Torpedo showing overlap of innervation between muscle fibers; a and b are two axons supplying muscle fibers labeled according to which axons innervate them.

the motor endplate. Figure 15 illustrates the complexity of motor terminations in Torpedo, perhaps directed to prolonging the period of subjunctional permeability in these large diameter muscle fibers. The ultrastructure of focally innervated fast fibers in the fins has not been examined, but that of multiply innervated fibers has been studied in several families (e.g., Nishihara, 1967; Bergman, 1964a), and resembles that of the body muscles, viz., in the absence of subjunctional folds.

F. Electrical and Mechanical Properties Several workers have investigated the electrical properties of myotomal muscle fibers in different fish groups (e.g., Barets, 1961;

398

QUENTIN BONE

Teiavainen, 1971; Stanfield, 1972), and, in Agnatha, Teravainen and Rovainen (1971) have been able to obtain simultaneous intracellular records from myotomal muscle fibers and the motoneurons supplying them; but the mechanical properties of myotomal fibers have been little studied, probably because the myoseptal insertions of these fibers are inconvenient for attachment to recording apparatus. The recent work of Wardle (1975) shows that such investigations are likely to prove rewarding. Fin muscle fibers provide better physiological preparations, and their mechanical properties are therefore easier to study (Bergman, 1964b; Hidaka and Toida, 1969; Yamamoto, 1972). I n elasmobranchs, fin muscle fibers are often of large diameter, and thus offer suitable material for studies on membrane properties (e.g., Hagiwara and Takahashi, 1974).

1. AMPHIOXUS

The interesting work of Hagiwara and his colleagues (Hagiwara and Kidokoro, 1971; Hagiwara et al., 1971) on the myotomal muscle lamellae (Fig. 8) of amphioxus has shown that there are two independent mechanisms for permeability increase; the normal action potential is mainly the result of increase in sodium conductance, but sufficient calcium ions enter during the spike to play a significant role in excitation-contraction coupling. Hagiwara and his colleagues consider that in practice what happens is that the sodium spike is important in conducting an impulse from the central motor endplate along the thin nervelike portion of the muscle fiber to its expanded contractile region where the calcium influx is concerned with excitation of the contractile apparatus. They also present evidence indicating that the subsarcolemmal cisternae of the SR are concerned with sequestering calcium rather than releasing it during contraction (as in higher forms). These unusual properties are of course related to the unique morphology of the system, presumably also responsible for the low values for the membrane resistance and time constant (Table IV). Electrical coupling between separate muscle cells was detected in half of the tests made; the morphological basis for this has not yet been established (Section IV,C,l) and it would b e interesting to know more of the properties of the (morphologically) different fiber types. 2. AGNATHA

Lampreys and hagfish offer favorable material for determination of the electrical and mechanical properties of muscle fibers. In lampreys, Teiavainen’s (1971) analysis has shown that the slow and fast (lateral

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and central) fibers have different input resistances and time constants, as expected from their differences in dimensions (Table IV); only fast fibers showed propagated overshooting action potentials (Fig. 16). Miniature endplate potentials were observed in both slow fibers and in fast central fibers (sometimes of two different rise times in the same fiber), but were not seen in lateral fast fibers. These last are electrically coupled to the central fast fibers, and are not directly innervated themselves. Again, as in amphioxus, gap junctions have not been observed; the morphological basis for electrical coupling has not been determined (Section IV,C,2). Recording tension directly from the abdominal surface of the myotome, Ter‘avainen was able to show (Fig. 17) that nerve stimulation gave a tetanic plateau at 2O/sec, and that relaxation followed a dual time course, presumably because the slow and fast fibers relaxed at different rates. In hagfish, Andersen et al. (1963) obtained similar mechanical results from the myotomes, i.e., single stimuli to the myotomal nerve gave evidence for the existence of slow and fast components, the slow component having a much longer relaxation time. As in lampreys, fast fibers gave propagated overshooting action potentials, from slow fibers only junctional potentials were elicited. But these junction potentials are unusual in their size, up to 30 niV, which is near to zero membrane potential! They have been studied b y Alnaes et al. (1963).Jansen and his colleagues conclude from records such as that of Fig. 18 where discontinuities are found on the junction potentials, that the slow fibers in hagfish may produce abortive spikes when stimulated indirectly. Stanfield (1972) suggests from his study of slow fibers in the dogfish Scyliorhinus (see next section) that the observations in hagfish may be explained in terms of some sodium conductance in these fibers. The ionic basis of electrical activity in hagfish fibers has not been investigated fully, and would seem to be of interest in view of the more recent observations of “spikes” in slow fibers when these are

Fig. 16. Overshooting spikes recorded from fast (central) muscle fibers of lamprey. Note that A (an innervated fiber) shows a prolonged after potential, whereas B is a record from a noninnervated fiber coupled to an innervated fiber and thus does not show this endplate potential. (From TerBvBinen, 1971.J. Neurojhysiol. 34, 954-973.)

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Fig. 17. Tension records from abdominal surface of myotome after nerve stimulation at 6/sec (upper) and 2O/sec. Early and late relaxation seen in lower record presumably result from activity of fast and slow fibers, respectively. (From Teravainen, 1971, J . Neurophysiol. 34, 954-973.)

immersed in experimental solutions (e.g., Hidaka and Toida, 1969). Most recently, Nicolaysen (1976a,b) has examined the spread of potential in the T-system of hagfish fast and slow fibers using sinusoidal transmembrane currents.

3. ELASMOBRANCHS Hagiwara and Takahashi (1967, 1974) and Stanfield (1972) have examined the membrane properties of the fin muscles of several

Fig. 18. Junction potentials from hagfish slow fibers. Note discontinuity on rising phase (arrow) interpreted as an abortive spike (see text). (From Andersen et nl., 1963).

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species of tropical stingrays, and of the myotomal muscle fibers of the dogfish, Scyliorhinus. The cable properties of the myotomal fibers investigated are seen in Table IV. Fast fibers in fins and myotomes gave overshooting propagated action potentials as expected from their focal innervation; slow fibers never gave propagated potentials, but an abortive spike was seen b y Stanfield on one occasion. Using a twoelectrode clamp, Stanfield found that eight of twenty-seven myotomal slow fibers showed sufficiently large inward sodium currents as soon as depolarized to suggest that they were capable of propagating action potentials. Six other slow fibers showed no inward sodium current on depolarization, and others showed a small inward sodium current. Figure 19 illustrates active current-voltage relations in the extreme cases. No significant difference in cable properties was found between slow fibers capable of showing a marked conductance change to sodium and those in which no change was found. These results are interesting, for they suggest that reports of abortive spikes and small spike potentials at the break of strong inward currents are to be explained in terms of some sodium conductance, as Stanfield pointed out. Since Stanfield wrote, there have been further investigations of morphology of the two fiber types, and it is known that the slow fibers can b e divided into two types according to their histochemistry and position within the slow fiber portion of the myotome. Yet Stanfield

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Fig. 19. Active voltage-current relations obtained from dogfish slow fibers using a two-electrode voltage clamp technique, In A, the dashed line shows the voltagemembrane current relation obtained from Cole’s theorem. Note delayed rectification and absence of inward sodium current. In B, also a slow fiber, filled points indicate currents flowing at end of 100 msec pulse, open points initial currents flowing at about 2 msec. In this fiber, delayed rectification is again found, but significantly, there are large inward sodium currents, resembling those of the fast fibers. Threshold for the sodium conductance was around 60 mV. [From Stanfield, 1972,J. Phy~iol.(London) 222, 161186.I

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emphasized the absence of sequestration of fibers with and without sodium currents in different parts of the slow fiber portion, so that it is not clear whether type I and type I1 slow fibers are different in this respect. Although there exists the possibility of propagated events among the slow fibers, no evidence has yet been adduced to suggest that these are found during normal swimming; crude records suggest that the slow fibers do indeed have the mechanical properties of slow fibers, contrasting with the twitch fast fibers.

4. TELEOSTS Barets (1961) and Hudson (1969) have examined myotomal muscle fibers, but most workers have used fin muscle preparations. In a variety of freshwater and marine teleosts there is good agreement between the results obtained from fibers that are innervated in a comparable way. All authors agree that slow (red) fibers of fins or myotomes do not propagate action potentials; the properties of these slow fibers are similar to those of other fish groups; as in elasmobranchs (Stanfield) there are hints of a sodium conductance mechanism in some teleost slow fibers. Where fast fibers are focally innervated, as in the myotomes of the catfish Ameiurus (Barets, 1961), or the fins of Conger (Hagiwara and Takahashi, 1967), typical overshooting propagated action potentials are found, similar to those in other vertebrate groups. Many teleosts, however, possess multiply innervated fast fibers, and here the situation may be different. Most workers have found that muscle action potentials from fibers of this kind are characterized by failure to overshoot, or by overshoots close to zero membrane potential (Takeuchi, 1959; Barets, 1961; Hagiwara and Takahashi, 1967; Hidaka and Toida, 1969). Hudson (1968) found in the marine teleost Cottus that 20 mV overshoots (Fig. 20) were obtained provided care was taken to experiment using a Ringer solution containing appropriate values of Ca2+ and Mg2+ ions. Reduction of these ions b y 50 and 30%, respectively, gave overshoots close to zero membrane potential. It is certainly tempting to suppose that appropriate ionic adjustments to the Ringer solutions used by previous workers would have allowed them to observe overshooting spikes, as Hudson suggests, but this has yet to be demonstrated. Alternative explanations of nonovershooting spikes are possible (e.g., in some fish high internal sodium may lower the sodium equilibrium potential), and as Hagiwara and Takahashi observe, multiply innervated fibers may be able to afford a lower safety factor than focally innervated fibers since contraction is not uniquely dependent upon propagated action potentials. In this way

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Fig. 20. Overshooting spike from multiply innervated fast myotomal fiber of Cottus. The arrow indicates the second of two summated junction potentials on the rising phase. (From Hudson, 1969.)

they could effect economies in ion transfer across the sarcolemma. However this may be, Hudson’s (1969) work revealed several interesting points about teleost multiply innervated fast fibers. By simultaneous recording from the nerve which was stimulated, and a single muscle fiber (Fig. 21), Hudson showed that each muscle fiber was innervated by at least two axons in a single spinal nerve and b y a similar number of axons in each of four neighboring spinal nerves, a remarkably high degree of polyneuronal innervation. Until tension records are taken simultaneously with electrical records from multiply innervated fast fibers, it will not be known for sure if such fibers are capable of local contractions and also of twitches following propagated action potentials. Observational data (e.g., Barets, 1961; Takeuchi, 1959; Bone et ul., 197th) suggest that this is the case; the functional advantage of such an arrangement is considered in the next section. The number of muscle fibers innervated by single axons (i.e., the size of the motor unit) is not well known in either myotomal or fin muscles. Teravainen and Rovainen (1971) suggest that in lamprey myotomal muscle, about ten to twelve fast motoneurons on each side of the spinal cord innervate an equal number of muscle units on that side, each muscle unit consisting of the central fibers and accompanying electrically coupled (noninnervated)lateral central fibers. In such focally innervated systems it is of course in principle possible to count motor axons in the nerve passing to the muscle, and divide the number obtained into the number of muscle fibers (making due allowance for the presence of different muscle fiber types where necessary). On this basis, the myotomal fast motor unit in Scyliorhinus consists of some 50-100 muscle fibers. Since this fiber type is apparently used only during burst swimming, it would not be surmised that it was finely

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Fig. 21. Simultaneous recordings of the compound action potential from spinal nerve (upper) and concomitant electrical activity of a single muscle fiber (lower), when stimulus intensity is varied. Zero membrane potential indicated in all except (f) by baseline of nerve record. In (f) small changes in stimulus intensity give different (superimposed) muscle responses at similar latency. The experimental situation is shown at the bottom. S, stimulating electrodes; E, earth electrode. CRO, recording electrodes to oscilloscope. (From Hudson, 1969.)

graded. The focally innervated fast fibers of the pectoral fin in herring are supplied by very few large axons which branch repeatedly (Fig. 6H): Gradation must be relatively coarse in this case. It is manifestly more complicated to unravel the possibilities of gradation in the multiply innervated fin or myotomal systems. Roberts (1969b)observed in slowly swimming spinal dogfish that there was good correlation between the duration of the muscle bursts (cf. his Fig. 21), the number of impulses in the burst, and the swimming frequency, indicating that the frequency and composition of the discharges of the motoneurons were controlled by a single mechanism. That is to say, the slow motor system is graded (as in amphibia) by variations in the amplitude and frequency of the junction potentials. Observations on the slow motor system of the unpaired fins led to the same conclusion. These are slow fibers which apparently d o not exhibit propagated muscle action potentials. Gradation in the multiply innervated fast fibers of teleosts is considered b y Hudson (1973), who suggests that

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during sustained swimming activity, motor units may be rotated in the fast motor system. The speed of fish locomotor fibers varies widely, from fusion frequencies up to 120 Hz for seahorse fin muscles (Bergman, 1964b) to 20 Hz for lamprey fast fibers (Terivainen, 1971). Isometric muscle contraction time for the seahorse fin fibers was as little as 10 msec. Wardle (1975) has given comparative isotonic muscle contraction times for fast myotomal muscle fibers in various teleosts, ranging from 20 to 45 msec, contraction time being related, as expected, to the size of the fish (increasing as fish length increases). Little is known in fish of the factors determining contraction velocity of different fiber types from a single fish. It is possible that the low molecular weight proteins studied by Hamoir and his colleagues (e.g., Syrovy e t al., 1970; Hamoir et al., 1972), which are known to be present in fish fast fibers but are much less abundant in slow fibers, may be concerned in some way in regulating muscle contraction velocity, perhaps by their effects on calcium-activated myosin ATPase, acting as calcium buffers in a situation where there are few mitochondria.

G . Functional Role of Different Fiber Types A variety of suggestions have been made for the functions of the two main fiber types in fish muscle. These are summarized in Bone (1966), but it is now generally agreed that the superficial slow fibers are utilized by the fish for sustained slow-speed swimming or cruising and the deeper fast fibers for bursts of higher speed. Several lines of evidence point to this conclusion. First, direct electromyographic recording from teleosts swimming freely or in tunnel respirometers, or from spinal sharks, has shown that electrical activity is fouud within the zone of the superficial fibers when the fish is swimming slowly and within the deeper zone of the fast fibers during rapid swimming (Bone, 1966; Rayner and Keenan, 1967; Hudson, 1973; Bone et al., 197th). Second, biochemical and metabolic studies (reviewed in Bilinski, 1974) have shown that slow fibers operate mainly by aerobic glycolysis and lipolysis, fast fibers b y anaerobic glycolysis. Examination of fish after exercise of different kinds has shown the expected utilization of metabolites by slow and fast fibers (see Chapter 8). It was perhaps natural to follow Arloing and Lavocat (as did Boddeke et al., 1959) in supposing that red and white fibers (or slow and fast fibers) were distinct and separate systems, utilized for different patterns of swimming at different speeds. The earlier electromyographic work on spinal dogfish showed that muscle action potentials

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could only be recorded from fast fibers in the deep portion of the myotome when the fish was strongly stimulated and swam very vigorously for a few tailbeats (see Fig. 22). At the usual slow spinal swimming rate of some 35 strokedmin, the fast fibers are silent, as they are even if the rhythm is speeded up b y deliberately oscillating the fish to higher tailbeat frequencies. There seems to be no question that in sharks, the deep fast fibers are only utilized during fast bursts of swimming. Calculations based upon the rate of depletion of the fast fiber glycogen reserves suggest these fibers could only operate for around 2 min of sustained activity (the time actually observed). This is less disadvantageous than might appear, for it would allow (in Scyliorhinus) a distance of some 600 m to be covered if the fish swam continuously. Of course, the fast fiber system is normally used by the fish to swim for a few rapid tailbeats and then glide to rest or to slow sustained swimming using the slow fiber system. Rather few teleosts have focally innervated fast fibers such as the dogfish, the herring is the only one in which fiber function has been investigated directly (Bone et al., 1978a). By observing herring swimming in a tunnel respirometer at different water velocities it is a simple matter to show that muscle action potentials from the deep fibers are only obtained when the fish is swimming in rapid bursts, and that up to 5 Clsec, herring must utilize only the slow fibers, since action potentials are not found. It is important to realize that the mosaic arrangement in the herring fast fiber portion of the myotome does not represent a mixture of larger focally innervated fibers with small mul-

1

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Fig. 22. Records obtained from swimming spinal dogfish using concentric needle electrodes. Upper in each, electrical activity; lower, record of movement of fish. (A) Activity of slow myotomal fibers; (B) absence of activity from fast fibers during slow spinal swimming; (C) prolonged bursts of action potentials from fast fibers during movements evoked by pinching tail. Note that electrical activity in C is recorded at a lower amplification than in A. Time bar: 0.5 sec.

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tiply innervated fibers. All are focally innervated; hence muscle action potentials must be a concomitant of their activity. A certain amount of evidence has accumulated from different lines of investigation that where fast fibers are multiply innervated (i.e., in higher teleosts), the simple duality of slow and fast portions of the myotome is an oversimplification. There is now rather convincing support for the idea that in these fish, fast fibers are active during continuous swimming at speeds well below that which the fish is capable of sustaining for long periods. Thus, Greer-Walker (1971) and Greer-Walker and Pull (1973) found hypertrophy of both slow fibers and fast fibers when coalfish (Gadus uirens) were swimming for long periods at 2 and 3 t'lsec. Using the same species, and also the crucian carp (C. carussius) Johnston and Goldspink (1973a,b,c) were able to demonstrate from measurements of muscle lactate, that after continuous swimming at 2 Clsec and above, the fast fiber system was active. Direct evidence for this conclusion was obtained in carp b y Johnston et al. (1977) and b y Bone et al. (1978a). A similar conclusion was drawn by Hunter (1971) in an interesting study of a fast swimming species (Trachurus s ymmetricus). Hudson (1973) placed electrodes in lateral superficial slow fibers and in deep mosaic fast fibers in trout ( S . gairdneri),and swam the fish in a tunnel respirometer at different speeds. He found that electrical activity was recorded from the superficial slow fibers at all swimming velocities, but the mosaic muscle was silent until the fish reached around 75% of the maximum sustainable swimming speed. At this swimming speed, the fast fibers showed electrical activity similar to that of the superficial slow fibers, but at burst speed, much larger electrical events were observed. Hudson's interesting results suggested that at intermediate and high cruising speeds, fibers in the fast portion of the myotome were operating without the production of muscle action potentials, whereas during bursts, the fast fibers produced action potentials. Similar conclusions were drawn from electromyography in carp (Bone et al., 1978a), except that in this species, the fast fiber portion of the myotome was active even at the lowest speeds the fish would swim in the respiroineter (Fig. 23). It is not known whether these different patterns of activity from the fast motor system during cruising and during bursts of rapid swimming represent the activity of different fast fiber types. Functionally, it would be a neat trick if the fish were able either to operate the fast motor system b y local contractions of the fibers so that the fibers contracted slowly when the fish swam slowly, or could contract them rapidly (with propagated muscle action potentials) during bursts of

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Isec

Fig. 23. Similar records to those of Fig. 22 obtained from fast myotomal muscle fibers ofcarp swimming in tunnel respirometer at different water velocities. At low swimming speeds (upper two records), only low amplitude electrical activity is obtained, but at higher speeds, (lower records) large events appear, probably muscle action potentials recorded extracellularly. (From Bone et al., 1978a, Fish Bull., in press.)

speed. The same fiber could then operate at the appropriate point on different force/velocity curves in both situations for maximum efficiency. Until single fiber activity records are obtained, the question must remain open, but results such as those obtained by Barets (1961) on tench (Tinca) do not rule out the possibility of two kinds of electrical (and mechanical) activity from single muscle fibers. It is something of a paradox to find that it is apparently common in higher teleosts for muscle fibers specialized for short periods of anaerobic burst swimming to play a part in sustained long-term activity. During sustained swimming the requirement must be for efficient and economical utilization of metabolites, and anaerobic glycolysis yielding lactate is a relatively inefficient source of ATP (Bilinski, 1974; see also Chapter 8). Since little lactate is excreted during sustained swimming (Bilinski, 1974), an obvious solution to the paradox is that lactate is oxidized at various sites outside the fast motor system of the deep portion of the myotome. The fish would then be in overall oxygen balance, and no oxygen debt would have to be repaid after the period of swimming (as it has to be repaid after short bursts of swimming at high speed). Two alternative sites have been proposed as capable of complete oxidation of lactate: the gills and the superficial slow muscle fibers. The discovery b y Bilinski and Jonas (1972) that gill tissue in trout had a high capacity for lactate oxidation suggested that the energy re-

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quired for exchange processes there is at least in part supplied in this way, so that lactate produced by the operation of the fast fibers at maintained high cruising speeds is oxidized to supply energy to drive the ion pumps of the gills. It is known that trout gill oxidizes lactate, but whether this mechanism is used to keep the fish in overall oxygen balance during sustained higher speed cruising is not known. It would be interesting to compare the capacity of the gill tissue to oxidize lactate in focally innervated forms (e.g., herring) which do not utilize the fast motor system during the cruise condition, with those from fish which are known to use the fast motor system during cruising (e.g., gadoids). Various workers have suggested that lactate produced by the activity of fast fibers can be oxidized by the superficial slow fibers. Some, (e.g., Braekkan, 1956) have supposed that the superficial muscle fibers are indeed not concerned with thrust generation at all, acting solely as a sort of peripheral liver, accessory to the metabolism of the fast fibers. It is plain that this view is untenable, but some evidence suggests that the superficial (red) fibers may play a part in the glycolytic metabolism of the deep fast (white) fibers. I n a series of papers Wittenberger (earlier references in Wittenberger et al., 1975) has examined the metabolic interrelationships of the two muscle types after simple experimental procedures, and has concluded that the superficial fibers store glycogen for subsequent transfer to the fast fibers as well as oxidizing lactate derived from the fast fibers. Similarly, Smit and his colleagues (Smit et al., 1971), observing that goldfish were able to swim at sustained fast speeds (up to 8.5 flsec for over 3 hr) without incurring an oxygen debt, assumed that slow fibers oxidized the lactate produced b y the fast fibers, which must presumably have been active at these high speeds. As Bilinski (1974) emphasizes, further experimental evidence is needed before this concept of “cooperative metabolism” between the two main fiber types can be accepted. The idea is in some ways an attractive one; what is needed are not only more experimental biochemical data but also some simple physiological data about diffusion pathways and capillary exchange between the two zones of the myotome. The poor vascularization of the deep fast fibers, and their distance from the superficial slow fiber zone in most fishes, would seem to make cooperative metabolism a very long-term process except in fish such as scombroids or carangids, where the deep fibers are better vascularized. Interestingly enough, the study by Pritchard et al. (1971),taken with that by Hunter (1971),on the carangid Trachyurus, and that by Johnston et al. (1977) on carp suggested sustained fast

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fiber activity over a wide speed range. If it is supposed that the mosaic portion of the myotomes in salmonids are composed of a mixture of slow and fast fibers (as, e.g., by Webb, 1971), then such an arrangement would certainly allow efficient exchange of metabolites between slow and fast fibers. Johnston (1977) has investigated the glycolytic enzyme profiles in slow and fast fibers of trout and mirror carp and has shown that these are similar in the carp, but differ in trout. As he points out, either there is something lacking in our understanding of anaerobic pathways in carp (but see Chapter 8) or there must be noncirculatory transfer of metabolites from white to red fibers which would require novel transport phenomena. The experimental myography, biochemistry, and histology considered in this section, have on the whole been at a relatively crude level, so that it has only been possible to consider the roles of slow or fast fibers. The diverse other fiber types have been conflated in one or other of these two categories, and until more detailed studies are carried out, the functions of such fibers as the superficial fibers in the dogfish are unknown. An early hint of different roles for two types of slow fibers was obtained by Rayner and Keenan’s (1967) electromyographic work on tuna where it was found that the superficial slow fibers and the deep, elevated temperature “chiai” slow fibers could operate under different conditions. Curiously enough, as Graham ( 1975)points out, the reason for maintainance of an elevated (slow) muscle temperature in larger scombroids and isurids is not entirely clear. There is no direct evidence for the function of the different fiber types in the fins of fishes, so far as the author is aware, but since there are two main fiber types in fin muscle, very similar in most respects to the slow and fast fiber types of the myotomal musculature, it is natural to suppose that they function in a similar way. Nishihara (1967) points out that the pectoral fin muscles in goldfish are mainly red, slow fibers, whereas the pelvic fin muscles are chiefly composed of white fast fibers, and relates this to the different function of the two sets of fins.

V. PROPRIOCEPTION Despite careful histological search by a number of workers, neuromuscular spindles have never been observed in the muscles of any fish. It seems extremely probable that they are indeed lacking, and that the few reports of their presence are mistaken. Either fish differ from other vertebrates in not requiring proprioceptors to regulate muscular contraction, or their proprioceptors are different to those of

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higher vertebrates. At present, except for elasmobranchs, there is insufficient evidence available to rule out the first possibility, but in some fish groups proprioceptors of different kinds are known, and on the whole it seems likely that they will eventually be found in all groups. I n two groups, the sharks and the rays, there is good histological and physiological evidence for proprioceptors associated with the locomotor musculature. In rays elongate beaded endings (Fig. 24B) among the fin ray muscles were found in the last century [they have been most recently investigated histologically by Barets (1956) and by Bone and Chubb (1975)l. Their position between muscle fibers, i.e., in parallel with the muscle fibers, naturally suggested that they were stretch receptors, and Fessard and Sand (1937) demonstrated that the static sensory discharge from the fin ray nerves was dependent upon the tension imposed upon the fin ray muscles. More recently, Ridge (1977) has investigated the dynamic properties of these endings, find-

Fig. 24. The three proprioceptive endings known from elasmobranchs. (A) Wunderer corpuscles from flank of body in Scyliorhinus. Note division of parent fiber at arrow and complex coiling within corpuscles. (From Bone and Chubb, 1976,J. Mar. Biol. Assoc. U.K. 56,925-928.) (B) Stretch receptive ending from among slow fibers of pectoral fin in ray. (C) Similar receptor from caudal myotome surface in Raia. In this case, the ending is apparently more closely associated with a muscle fiber than are the endings ofthe pectoral and pelvic fins. All from whole mounts of silver-impregnatedmaterial. Scale bar: 100pm.

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ing that they resemble neuromuscular spindles in certain respects (Fig. 25). There are some interesting features in the morphology of these elongate endings. First, they are only found between smalldiameter multiply innervated muscle fibers which form the superficial zone of the fin ray muscle bundles. The main mass of the fin ray muscle, consisting of larger focally innervated muscle fibers, does not possess these endings. Second, the coupling between the sensory neurites and the muscle fibers themselves is relatively loose. For most of the length of the ending the neurites are only coupled to the muscle fiber b y loose strands of collagen, but at certain points, the sarcolemma is invaginated and the coupling is more direct. Because there is no capsule, and the endings are large and visible b y means of Nomarski optics in the living state, it seems likely that the ray endings may be of interest to physiologists examining general aspects of stretch receptor function. It is certainly significant that these endings lie only among small-diameter muscle fibers which probably do not propagate muscle action potentials. In this respect they are similar to the nonencapsulated stretch receptors of urodele muscle (Bone et al., 1976). On the surface of the caudal myotomes just internal to the dermal connective tissue sheet, there are beaded brushlike endings derived from large diameter nerve fibers that are similar to those found in the fin ray muscles (see Bone, 1964, for reference to earlier observations).

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Fig. 25. Discharge frequency of stretch receptor endings from pectoral fin of Raia claoata in response to ramp stretches at different velocities. Lower records (solid lines), record of displacement ( 1 mm); upper record, discharge frequency (instantaneous frequency meter record). (A) Stretch at 1.25mm/sec; (B) stretch at 2.5,5,10, and 20 mm/sec. (From Ridge, unpublished.)

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These endings lie superficial to the large-diameter terminally innervated fast muscle fibers of the caudal region, near to the insertions of the muscle fibers (Fig. 24C). They are therefore unlike the endings of the fin muscles (between slow fibers). Presumably, as the tail is flexed, these endings would be stimulated by pressure from the overlying connective tissue sheet, as well as, or alternatively, b y the tension exerted by the muscle fibers next to the ending; no physiological investigations have yet been made however. It should be pointed out that, although the elongate endings of rays are the best known, both histologically and physiologically, of fish proprioceptors, it is not yet clear what use the fish makes of the information which they provide. Since spinal rays do not show the same kind of reflex swimming as do sharks, the necessity of proprioceptive input for the swimming rhythm has not yet been demonstrated. However, having entered this caveat, it is obviously reasonable to suppose that (as Fessard and Sand suggested) the elongate receptors regulate the swimming rhythm. The function of the superficial endings of the tail is less easy to apprehend, since in most rays, the tail is relatively immobile. In sharks, these elongate receptors are either absent or very rare. Fessard and Sand observed similar responses to those given by the elongate endings of rays in certain (unspecified) muscles of Scyliorhinus; Barets (personal communication) has occasionally observed them among the fin muscles. They are not found in the myotomal musculature, so far as I have been able to observe. Instead, endings of rather different morphology are found. These endihgs lie just superficial to the myotomes at the level of the myosepta. They are derived from large-diameter axons which form coiled corpuscles embedded in the connective tissue of the outer edge of the myospetum. Occasionally they are found among the superficial muscle fibers in the partition between two muscle stacks. These endings were first carefully described by Wunderer (1908) from the bases of the fins, where they were later examined physiologically by Lowenstein ( 1956), who showed them to be slowly adopting mechanoreceptors. In morphology they resemble most the coiled corpuscular endings of higher forms (e.g., Munger, 1961) being formed of a twisted skein of neurites surrounded b y connective tissue elements. Roberts (1969a) recorded from portions of the body wall as it was flexed, and showed that receptors existed which were sensitive to the frequency and amplitude of flexure. In all probability these receptors are the coiled corpuscles shown in Fig. 24A, but this has not yet been definitely proven. If so, they function during swimming as second-

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order proprioceptors, being stimulated b y the alternate compression and release of the endings as the fish oscillates its body, just as at the bases of the fins they signal the bending of the fins. Spinal sharks appropriately set up (i.e., ventilated and held free from the bottom of the tank) swim continuously with a regular slow rhythm. This rhythmic activity is dependent upon sensory input; surgical removal of input abolishes the spinal swimming rhythm (Lissmann, 1946). It is very probable that it is the alternating proprioceptive input of the corpuscular endings of the myoseptal margins which maintains this swimming rhythm. There is some controversy (Grillner, 1974) whether the spinal swimming is dependent upon central oscillators, but whatever view is taken of the central organization, it is clear that proprioceptive input is of importance. The occasional occurrence of the corpuscular endings between muscle fascia rather than superficial to the muscle fibers is of some interest, for in this position the endings (more elongate than usual) are presumably stimulated by pressure from contracting myotomal muscle fibers themselves rather than less directly; perhaps we have a hint here of the way in which proprioceptors linked to muscle fibers may have arisen from mechanoreceptors. During investigation of the corpuscular endings of sharks, Roberts (19694 found similar activity from the nerves passing to the body wall of the gurnard Trigla C U C U ~ U S(L,), but the endings responsible have not been examined histologically. On the whole it seems unlikely that these endings (or indeed, any possible proprioceptive endings of teleosts) can be morphologically very noteworthy. Many histologists have examined teleost muscles without discovery of assodiated corpuscular or beaded endings that could be proprioceptive, so that such endings are probably simple branching endings in the myosepta, as are found in the hagfish, Myxine (Bone, 1963). In the hagfish it was possible to recognize the endings as sensory, since the nerve fibers giving rise to them could be traced back to their cells of origin in the dorsal root ganglia, but this is rarely likely to be possible. Since spinal teleosts do not normally exhibit steady swimming rhythms of the shark kind, it has not been shown whether proprioceptive input is required during myotomal locomotion. A number of teleosts swim by means of the paired fins, as also d o holocephali, and I have examined both groups without observing special sensory terminations associated with the fin musculature. In Trigla, the bases of the free fin rays of the pectoral fins are innervated by branching fibers resembling the endings found in the joints of

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4 15

higher vertebrates. Similar endings are found between the joints of the fin rays of elasmobranchs, between the vertebrae and fin ray joints of dipnoi, (personal observations) and are probably found in most teleosts. They have not received any attention physiologically, so far as I am aware. Holmes (cited in Barker, 1974) has found complex branching endings superficial to the musculature in the mobile, barbell-like. fins of the dipnoan Protopterus; again, these endings are somewhat similar to the joint receptors of amphibia. Despite these rather scattered examples of proprioceptors associated with locomotor muscle fibers in different fishes, it seems to be correct to suppose that the innervation of any locomotor muscle in any fish is set apart from that of higher vertebrates, not only by the lack of spindles, but also b y the poverty of the sensory component. I n cat hindlimb muscles, for example (Barker, 1974), some 75% of all the axons in the nerves passing to the muscle are sensory; if fusimotor axons are included, around 81% of the axons in the nerves pass to or from receptors. This is indeed very different from the arrangement in fish. Even in the fin muscles of rays, the large diameter axons supplying the elongate sensory terminals make u p at most some 15% of the total muscular nerve supply. Partly, perhaps, this is because in fish, where the body weight is wholly or almost entirely supported by the water, postural problems are of little account (Bone, 1966), and so a rich sensory innervation giving a detailed pattern of information about muscle length and tension is not required. It is notable that the aquatic urodeles resemble fishes in that they are devoid of neuromuscular spindles in the myotomal locomotor musculature; they d o have, however, sensory endings in the limb muscles which are sensitive to stretch (Bone et al., 1976). The absence of neuromuscular spindles from fish muscle is striking to the physiologist accustomed to higher forms, but to the fish physiologist what seems remarkable is that only in rays are there proprioceptive endings which seem analogous to spindles in that they are directly associated with muscle fibers, rather than being “secondorder” proprioceptors as are all the other sensory endings assumed to be proprioceptive in function. It may be that the ray method of swimming demands very delicate control of the fin ray musculature, unobtainable b y indirect proprioception, but anyone who has watched the barbels of feeding mullet or the dorsal fins ofNotopterus or gymnotids, will be aware of remarkably precise muscular movements apparently without benefit of direct proprioception. It is probably in delicately controlled muscles such as these that morphologically specialized

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proprioceptive endings will first be found in teleosts. Ono (personal communication) has found, however, only simple branched sensory endings in the barbels of Mullus. From the account above it will be at once evident that further investigations are required before the role of proprioception in the control of fish muscles is understood; only in elasmobranchs have we a reasonable understanding of the system.

VI. FISH MUSCLE AND THE MUSCLES OF HIGHER FORMS The preceding sections have indicated some of the differences between the muscles of fishes and those of terrestrial vertebrates. The differences are real, and they are differences not only of degree but also of kind. For example, neuromuscular spindles are absent, and they occur in all terrestrial vertebrates so far as is known; again, different fiber types are segregated or zoned to a much greater degree than they are in terrestrial forms. What is more, slow and fast fibers are more different from each other.than they are even in amphibia. Not only are slow fibers apparently non-twitch fibers, but the fast twitch fibers are normally highly specialized for anaerobic operation, which is to say, for maximum power at the expense of sustained operation. On the whole, these differences between the muscle fibers of fishes and of terrestrial forms can be understood in terms of the rather stringent conditions set by the density of the water in which the fish lives. Fortunately for fish, the density of the water which imposes a requirement for a large power increase for small increment of swimming speed, also provides the possibility of achieving neutral buoyancy by storing small amounts of gas or lipid, and, so, with the possibility of greatly increasing the mass of locomotor muscle. The myotomal mass of fast fibers only used occasionally during escape or predatory movements is but a light penalty for the fish to carry around, since it is buoyed up by the water; such an arrangement of a mass of muscles used only as an emergency power pack would be quite unsuitable for a terrestrial animal subject to gravity. Curiously enough, although all terrestrial vertebrates (with the exception of mammals) seem to have both multiply innervated slow fibers and focally innervated fast fibers in their locomotor muscles (see review by Barker, 1968), the function of the different fiber types is only known clearly in mammals. In amphibia, reptiles, and birds, it is possible that slow fibers are used for slow movements, perhaps additionally or alternatively, for isometric postural contractions, but

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this awaits investigation. Part of the difficulty resides in the mosaic arrangement of fiber types in most muscles of terrestrial forms, as opposed to the zonal fish arrangement. It seems most appropriate to end this chapter b y reminding the reader of two points. First, the study of fish muscle is as yet in a preliminary state; so far, few fishes out of the many different groups have been examined. Much remains to be done. There are a variety of fish groups still living, from acrania to dipnoi, and comparative studies are likely to prove fruitful in interpreting the functional roles of different fiber types. Second, fish muscle is very suitable experimental material (as Bilinski has already noted) for a wide variety of problems.

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Roberts, B. L. (1969a).T h e response of a proprioceptor to the undulating movements of dogfish.]. E x p . Biol. 51, 775-785. Roberts, B. L. (196913).The co-ordination of the rhythmical fin movements of dogfish.]. Mar. Biol. Assoc. U . K . 49, 357-425. Sharp, G.,and Dizon, A. (eds.)(in press). “The Physiological Ecology ofTunas.” Academic Press, New York. Skoglund, C. R. (1961). Functional analysis of swimbladder muscles engaged in sound production of the toadfish. J . Biophys. Biochem. Cytol. 10, 187-200. Smit, H., Amelink-Koutstall, J. M., Vijverberg, J . , and von Vaupel-Klein, J. C. (1971). Oxygen consumption and efficiency of swimming goldfish. Comp. Biochem. Physiol. A 39, 1-28. Smith, R. S., and Ovalle, W. K. (1973).Varieties of fast and slow extrafusal muscle fibers in amphibian hind limb muscles. J. Anat. 116, 1-24. Smith, R. S., Blinston, G., and Ovalle, W. K. (1974).Organization of skeletal muscle in the amphibia. In “Control of Posture and Locomotion” (R.B. Stein, K. G. Pearson, R. S. Smith, and J. B. Redford, eds.), pp. 1-13. Plenum, New York. Spray, T. L., Waugh, R. A., and Sommer, J. R. (1974). Peripheral couplings in adult vertebrate skeletal muscle. J. Cell Biol. 62, 223-227. Stanfield, P. R. (1972).Electrical properties of white and red muscle fibers of the elasmobranch fish Scyliorhinus canicula. J. Physiol. (London) 222, 161-186. Stevens, J. (1976).The ecology of the blue shark Prionuce glauca. Ph. D. thesis, Univ. of London. Syrovy, I., Gaspar-Godfroid, A,, and Hamoir, G. (1970). Comparative study of the myosins from red and white muscles of the carp. Arch. Int. Physiol. Biochim. 78, 9 19-934. Takeuchi, A. (1959). Muscular transmission of fish skeletal muscles investigated with intracellular microelectrode.]. Cell. Comp. Physiol. 54, 211-220. Teraviinen, H. (1971).Anatomical and physiological studies on muscles of lamprey. J. Neurophysiol. 34, 954-973. Teraviinen, H., and Rovainen, C. M. (1971).Fast and slow motoneurons to body muscle of the sea lamprey. J. Neurophysiol. 34, 990-998. van der Stelt, A. (1968). Spiermechanica e n myotoombouw Bij Vissen. Ph. D. Thesis, Univ. of Amsterdam. Vialleton, L. (1902). Le developpement des muscles rouges. C . R. Assoc. Anat. Part 4, pp. 47-53. Wardle, C. S. (1975). Limit of fish swimming speed. Nature (London) 255, 725-727. Warfel, H . E., and Clague, J. A. (1950). Shark fishing potentialities of the Philippine seas. Fish Wildl. Sero. (U.S.),Res. Rep. No. 15, pp. 1-19. Waterman, R. E. (1969). Development of the lateral musculature in the teleost Brachydanis serio: A fine structural study. Am. J. Anat. 125, 457-494. Webb, P. W. (1971).The swimming energetics of trout. I. Thrust and power output at cruising speeds. J. Exp. Biol. 55, 489-520. Webb, P. W. (1975). Hydrodynamics and energetics of fish propulsion. Bull., Fish. Res. Board Can. No. 190, 158 pp. Willemse, J . J . (1975).Some remarks on the structure and function of musculus lateralis in the European ee1,Anguilla anguilla (L.)(Pisces, Teleostei). 2. Morphol. Tiere 81, 195-208. Willemse, J. J., and van den Berg, P. G. (1978).Growth of striated muscle fibres in the M. lateralis of the European eel Anguillo unguillu (L.) (Pisces, Teleostei).]. Annt. 125. 447-460.

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7 THE RESPIRATORY AND CIRCULATORY SYSTEMS DURING EXERCISE DAVZD R . JONES and DAVZD J . RANDALL I. General Introduction . . . . . . . . . . . . . . . . . ................... 11. Assessment of Exercise Performance ............................. A. Introduction ..... ..................... ..... B. Th e Relation betw gen Metabolism and ................................... Swimming Speed, C. Anaerobic Contrib Exercise Metabolism . . . . . . . . . . . . . . . D. Limitations on Maximum Performance; Fatigue ............... 111. Th e Respiratory System during Exercise . . . . ........... A. Introduction ....................... ................ B. Respiratory Adjustments to Exercise .......................... IV. The Circulatory System during Exercise .......................... A. Introduction ...................... ............... B. Cardiac Adjustments to Exercise ............................. C. Arterial Blood Pressure and Total Peripheral Resistance during Exercise . . . . . . . . . . .......... D. Venous Pressure and Venous Return d References .................................... ...............

425 426 426 427 437 438 442 442 443 466 466 467 480 486 492

I. GENERAL INTRODUCTION Exercise is the stress which animals most frequently experience and may be defined as work performed on the environment b y the locomotory muscles. Exercise is accompanied b y an increase in the rate of energy conversion from the resting rate. This increase provides for the energy requirements of the locomotory muscles as well as for extra work performed by the heart and respiratory muscles in supplying oxygen demanded in exercise. In this chapter the emphasis is placed on the ability of fish to increase the rate of gas exchange at the gills and tissues and the changes which occur in the components of the respiratory and circulatory systems facilitating this increase in gas exchange. On many 425 FISH PIIYSIOLOCY, VOL VII Copyright @ 1978 by Ar.idemii Pre\

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