Locomotion of Animals

169 Pages·1982·3.814 MB·English

by  R. McNeill Alexander D.Sc. (auth.)

Locomotion of Animals
TERTIARY LEVEL BIOLOGY
A series covering selected areas of biology at advanced
undergraduate level. While designed specifically for course
options at this level within Universities and
Polytechnics, the series will be of great value to
specialists and research workers in other fields who require
a knowledge of the essentials of a subject.
Titles in the series:
Experimentation in Biology Ridgman
Methods in Experimental Biology Ralph
Visceral Muscle Huddart and Hunt
Biological Membranes Harrison and Lunt
Comparative Immunobiology Manning and Turner
Water and Plants Meidner and Sheriff
Biology of Nematodes Croll and Matthews
An Introduction to Biological Rhythms Saunders
Biology of Ageing Lamb
Biology of Reproduction Hogarth
An Introduction to Marine Science Meadows and Campbell
Biology of Fresh Waters Maitland
An Introduction to Developmental Biology Ede
Physiology of Parasites Chappell
Neurosecretion Maddrell and Nordmann
Biology of Communication Lewis and Gower
Population Genetics Gale
Structure and Biochemistry of
Cell Organelles Reid
Developmental Microbiology Peberdy
Genetics of Microbes Bainbridge
Biological Functions of Carbohydrates Candy
Endocrinology Goldsworthy, Robinson
and Mordue
The Estuarine Ecosystem McLusky
Animal Osmoregulation Rankin and Davenport
Molecular Enzymology Wharton and Eisenthal
Environmental Microbiology Grant and Long
The Genetic Basis of Development Stewart and Hunt
TERTIARY LEVEL BIOLOGY
Locomotion
of Animals
R. McNeill Alexander, D.Sc.
Professor of Zoology
University of Leeds
Blackie
Glasgow and London
Distributed in the USA
by Chapman and Hall
New York
Blackie & Son Limited
Bishopbriggs, Glasgow G64 2NZ
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© 1982 ~Iackie & Son Limited
First published 1982
Softcover reprint of the hardcover 1s t edition 1982
All rights reserved.
No part of this publication may be reproduced,
stored in a retrieval system, or transmitted,
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without prior permission of the Publishers
British Library Cataloguing in Publication Data
Alexander, R. McNeill
Locomotion of animals.-(Tertiary level biology)
1. Animal locomotion
I. Title II. Series
591 .1 '852 OP301
ISBN-l3: 978-94-011-6011-7 e-ISBN-13: 978-94-011-6009-4
DOl: lO.lO07/978-94-011-6009-4
For the USA, International Standard Book Numbers are
cloth 0-412-00001-6
paper 0-412-00011-3
Filmset by Advanced Filmsetters (Glasgow) Ltd
Preface
This book is about how animals travel around on land, in water and in the
air. It is mainly about mechanisms of locomotion, their limitations and
their energy requirements. There is some information about muscle
physiology in Chapter 1, but only as much as seems necessary for the
discussions of mechanisms and energetics. There is information in later
chapters about the patterns of repetitive movement involved, for instance,
in different gaits, but nothing about nervous mechanisms of coordination.
I have tried to include most ofthe widely-used methods of locomotion, but
have not thought it sensible to try to mention every variety of locomotion
used by animals.
This book is designed for undergraduates, but I hope that other people
will also find it interesting.
It is possible and sometimes illuminating to use complex mathematics
in discussions of animal locomotion. This book includes many equations,
but little mathematics. Such mathematics as there is, is simple.
Discussions of the mechanisms and energetics of locomotion inevitably
involve mechanics. I expect that some readers will know a lot of mechanics,
and some hardly any. I have tried to help the latter without boring
the former, by putting a summary of the necessary mechanics in an
appendix (p. 140). References from the main text to the appendix will tell
readers where they can find help, if they need it. Figures and equations in
the appendix have numbers distinguished by a prefix A (for instance,
Figure A.3).
There is a list of references and suggestions for further reading at the
end of the book. References in the text indicate principal sources of
information, but I have not thought it desirable to insert the much larger
number of references that would be needed to show the authority for every
statement.
Dr H. C. Bennet-Clark and Dr C. J. Pennycuick read the typescript and
made many very helpful suggestions.
R. McNeill Alexander
v
Contents
Chapter 1 SOURCES OF POWER 1
Muscle. Types of muscle. Arrangement of muscles. Other sources
of power.
Chapter 2 SWIMMING 13
Swimming by undulation. Rowing. Swimming with hydrofoils. Jet
propulsion.
Chapter 3 BUOYANCY 39
Dense animals. Low-density materials. Gas-filled floats. Buoyancy
and ways of life. Advantages of different buoyancy aids.
Chapter 4 FLIGHT 54
Gliding. Soaring. Fast flapping flight. Hovering and slow flight.
Take-off and landing.
Chapter 5 WALKING, RUNNING AND JUMPING 81
Walking slowly. Walking faster. Running bipeds. Running quad-
rupeds. Energetics. Stance. Climbing. Jumping.
Chapter 6 CRAWLING 114
Two-anchor crawling. Peristalsis. Pedal waves. Serpentine crawl-
ing. Amoeboid crawling.
Chapter 7 LOCOMOTION IN GENERAL 126
Comparisons. Escape and capture. Herds, flocks and shoals.
Appendix BASIC MECHANICS 140
Units. Vectors. Movement. Force. Energy. Properties of materials.
Similarity. Bodies in fluids.
REFERENCES AND FURTHER READING 154
INDEX 159
Vll
CHAPTER ONE
SOURCES OF POWER
The movements described in this book are powered by muscles, cilia,
flagella or cytoplasmic streaming. This chapter is mainly about muscle but
includes brief accounts of the other sources of power.
Muscle
Muscle fibres do work by shortening while exerting a force. The structures
that generate force have been identified in electron microscope sections
and are shown diagrammatically in Figure l.la,b (see also White, 1977).
They are protein filaments a few micrometres long, arranged parallel to
the length of the fibre. There are thick filaments of myosin and thin ones
of actin and tropomyosin. The muscles that move the skeletons of
vertebrates and insects are of the cross-striated kind shown in the figure.
Interdigitating bands of thick and thin filaments alternate along the length
of the fibre, and partitions called Z-discs cross the fibre, through the mid
points of the thin filaments. Each repeat of the resulting pattern of stripes
is called a sarcomere. A different, obliquely-striated type of muscle fibre is
found in nematode and annelid worms and in many of the muscles of
molluscs. Its sarcomeres run obliquely across the fibre.
The thick filaments have projections called cross-bridges that seem to be
capable of attaching to a thin filament and then swinging through an
angle, making the filaments slide past each other. They can detach, swing
back and reattach to a different point on the thin filament. In this way the
cross-bridges can pull on the thin filaments like a man pulling in a rope
hand over hand. Each sarcomere can be shortened from the state shown
in Figure l.1a to that shown in Figure l.1b. Notice that if the sarcomere
were stretched beyond the state shown in Figure l.1a the thin filaments
1
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SOURCES OF POWER 3
would be pulled right out from between the thick ones and the cross
bridges could no longer attach. Also, sarcomeres cannot shorten much
beyond the point shown in Figure 1.1 b because the thick filaments abut
against the Z-discs. Therefore, cross-striated muscle can operate only over
a limited range of lengths: the minimum length is not much less than half
the maximum. There is an intermediate length at which all the cross
bridges can attach but none of the disadvantages of excessive shortening
operate. This is the length at which most force can be exerted.
Since the cross-bridges transmit the force from the thick filaments to the
thin ones, the force that a muscle fibre can produce is proportional to the
number of cross-bridges in each sarcomere. Muscles with long filaments
can therefore exert more stress than muscles with shorter ones. Vertebrate
skeletal muscles have thick filaments about 1.61lm long and can exert
maximum stresses of about 0.3 MPa, * but locust leg muscle has filaments
about 5.5 11m long and can exert 0.8 MPa.
Imagine (if you can) a vertebrate muscle of volume 1 m3• When this
particular muscle is fully extended its fibres are 1.4 m long, and when it is
fully shortened they are just half as long, or 0.7 m. About halfway through
the contraction the fibres are 1 m long so the cross-sectional area is 1 m2,
and if the stress is OJ MPa the force is 0.3 MN. The fibres shorten by 0.7 m
while exerting this force, so the work done is 0.7 x 0.3 = 0.21 MJ. The mass
of 1 m3 muscle would be about 1000 kg, so this work is 210 J per kg muscle.
This is a very crude argument, but a more precise one leads to a similar
conclusion. Vertebrate skeletal muscle cannot do more work than about
200 J /kg in a single contraction.
There is a limit to the rate at which cross-bridges can attach, pull and
detach again. There is therefore a limit to the rate at which they can make
the filaments slide past each other. The rate varies in different muscles: let
it be u in a muscle fibre that has length I when its sarcomeres have length A..
Each sarcomere can shorten at a speed 2u and the fibre as a whole can
shorten at 2ul/), because it has 1/), sarcomeres. The fastest known muscles
seem to be a rat eye muscle and a mouse toe muscle, which can shorten at
rates corresponding to 25 fibre lengths per second (i.e. 2u/ A = 25 s -1 ).
Mammal muscles have sarcomeres about 2.5 11m long, so this implies a
sliding speed u of about 30llm/s. Notice that the rate of shortening of the
fibre would be less (for given u) if the sarcomere were longer. Long
sarcomeres give high stresses but low rates of shortening.
The faster a muscle is shortening, the less force it can exert. Conversely,
* A megapascal (MPa) is one million newtons per square metre or 102 grams weight per
square millimetre. See the explanation of units in the appendix.
4 LOCOMOTION OF ANIMALS
the less resistance it experiences, the faster it can shorten (Figure 1.1c). The
maximum stress of 0.3 MPa exerted by typical vertebrate skeletal muscles
can be exerted only when the muscle is shortening very slowly or not at all.
The maximum work of 200 J kg - can therefore be done only in a very
1
slow contraction. The maximum speed of shortening (25 lengths s -
1 )
given above for the fastest rat and mouse muscles can be achieved only
when no external load acts on the muscle.
The power output of a muscle is the force it exerts multiplied by the rate
of shortening. At the highest rate of shortening no force is developed, so
the power is zero. A large force can be exerted if the rate of shortening is
zero but the power is then again zero. Power output is greatest at an
intermediate speed (Figure 1.1c). The flight muscles of various insects and
hummingbirds have been shown to be capable of power outputs of about
200 W per kg muscle-this is the mean power output over a series of cycles
of contraction and relaxation, and no muscles are known to produce much
more power than this. These muscles work aerobically, and have up to
about half of their volume occupied by mitochondria. It is possible that a
very fast anaerobic muscle containing fewer mitochondria and more thick
and thin filaments could produce more power. Aerobic and anaerobic
muscles are discussed in the next section of this chapter.
A muscle that shortens while exerting a force does (positive) work. One
that is forcibly extended while exerting a force has work done on it and
degrades this work to heat Gust as work is degraded to heat in the brakes
of a vehicle). This is often described by saying that the muscle does
negative work. Figure 1.1c shows that large forces cause lengthening
(negative rates of shortening) of muscles. Muscles have to do negative
work when a running animal slows down, or decelerates a moving limb.
The rates at which animals use chemical energy can be calculated from
their rates of oxygen consumption (unless anaerobic metabolism is being
used). This is the basis for many measurements of muscle efficiency. For
instance, the rates of oxygen consumption have been measured for people
resting and doing work at a known rate by pedalling a bicycle ergometer.
The difference gave the metabolic power used for pedalling, so the
efficiency could be calculated as (mechanical power output) -;- (metabolic
power consumption). This experiment showed that over a wide range of
rates of pedalling, the efficiency of doing positive work is about 0.25.
Measurements of the rates of oxygen consumption of people, squirrels
and other mammals running up steep gradients, and of birds flying up
gradients in wind-tunnels, have confirmed that muscle can do positive
work with efficiencies up to about 0.25. (Experiments involving running up