Locomotion and Energetics in Arthropods

544 Pages·1981·17.11 MB·English

by  Clyde F. Herreid II (auth.)

Locomotion and
Energetics in
Arthropods
Locomotion and
Energetics in
Arthropods
Edited by
Clyde F. Herreid II
and
Charles R. Fourtner
State University of New York
Buffalo, New York
PLENUM PRESS • NEW YORK AND LONDON
Library of Congress Cataloging in Publication Data
Main entry under title:
Locomotion and energetics in arthropods.
"Proceedings of a symposium on locomotion and exercise of arthropods, held
December 27-28,1980, as part of the 1980 Seattle meeting of the American
Society of Zoologists, held at the University of Washington, Seattle, Washington"
-Versot.p.
Includes bibliographies and index.
1. Arthropoda-Physiology-Congresses. 2. Animal locomotion-Congresses.
3. Bioenergetics- Congresses. I. Herreid, Clyde F. II. Fourtner, Charles R. III.
American Society of Zoologists.
QL434.72.L63 595.2 '041852 81-13779
ISBN-13: 978-1-4684-4066-9 e-ISBN-13: 978-1-4684-4064-5 AACR2
DO I: 10.1007/978-1-4684-4064-5
and
EXERCISE
of
ARTHROPODS
Proceedings of a symposium on Locomotion and Exercise of Arthropods. held
December 27-28, 1980, as part of the 1980 Seattle meeting of the American
Society of Zoologists, held at the University of Washington, Seattle, Washington
© 1981 Plenum Press, New York
Softcover reprint of the hardcover 1s t edition 1981
A Division of Plenum Publishing Corporation
233 Spring Street, New York, N.Y. 10013
All rights reserved
No part of this book may be reproduced, stored in a retrieval system, or transmitted,
in any form or by any means, electronic, mechanical, photocopying, microfilming,
recording, or otherwise, without written permission from the publisher
PREFACE
At the 1980 Christmas meetings of the American Society of
zoologists in Seattle, Washington, the Division of Comparative
Physiology and Biochemistry sponsored a symposium on the locomo
tion and exercise of arthropods. This book is an outgrowth of
that symposium. To our knowledge, the symposium and this volume
are the first attempts to deal with all of the major modes of
locomotion (flight, swimming, and pedestrian travel) among the
arthropods in a comprehensive fashion.
The time seems propitious to focus on arthropod locomotion.
In the last decade enormous strides have been made in understand
ing locomotion - both arthropod and vertebrate alike. There has
been an explosion of new ideas, new techniques, and new data.
These deserve greater attention and discussion than is possible
in specialized journals. Hopefully this book will fill this gap;
moreover, it should serve as a benchmark for newcomers to see what
has happened to date and perhaps act as a launching pad for re
search to come. Whatever the case, a symposium volume such as
this serves to highlight our current strengths and weaknesses. In
the present case it reveals the relative abundance of information
on flying and walking and the dearth of data available on swimming;
it exposes the fact that insects and crustaceans are fairly well
studied and arachnids are not. Symposium volumes in general re
flect the unevenness of knowledge, the diversity of approaches
and idiosyncrasies of investigators perhaps better than any other
method of publication. Such works, for better or worse, are
microcosms of science. It is no different with this volume. Its
major virtue is its immediacy - it is a good look at arthropod
locomotion and exercise, circa 1981.
There are many people to thank who assisted us in publishing
this book, not the least of whom are the seminar speakers who
became our authors, sometimes under duress. We thank our illus
trator, James Stamos, who came to our rescue on many occasions.
We thank Plenum Press for having the extraordinary ability to
publish a manuscript in so short a time. We thank the American
Society of zoologists and Mary Wiley for financial and spiritual
assistance. We thank, and we bless, our manuscript typist, Jeanne
Pease, for her expertise, good sense and good humor in the face of
v
PREFACE
impossible demands. We thank Bob Full, Dan Golder, Larry Lee and
Sandra Woolley for help with the indexing. And we thank the people
of the United States of America who through NIH and NSF grants to
the editors have supported work on locomotion of animals radically
different from themselves.
c. F. Herreid
c. R. Fourtner
CONTENTS
I. EVOLUTION
Locomotion in Arthropods: An Evolutionary
Phantasmagoria 1
C.F. Herreid
Evolution of Arthropod Locomotion: A Crustacean
Model 9
R.R. Hessler
II. MECHANICS AND KINEMATICS
Decapod Crustacean Leg Coordination During walking 31
F. Clarac
Arachnid Locomotion 73
R. Bowerman
Insect Locomotion on Land 103
F. Delcomyn
Insect Flight Aerodynamics 127
W. Nachtigal!
III. NEUROMUSCULAR INTERACTIONS
Neuromuscular Mechanisms of Insect Flight 163
A.E. Kammer and M.B. Rheuben
Role of Muscle in Insect Posture and Locomotion 195
C.R. Fourtner
Does Exercise Influence the Differentiation of
Lobster Muscle? 215
C.K. Govind
vii
viii CONTENTS
IV. MUSCLE BIOCHEMISTRY
Biochemical Adaptations in Insect Muscle • 255
D. Stokes and C.R. Morgan
V. CIRCULATION AND GAS EXCHANGE
Respiratory and Circulatory Coordination in
Decapod Crustaceans • 277
J .L. Wilkens
Oxygen Uptake and Acid-Base Balance During Activity
in Decapod Crustaceans • 299
B. McMahon
Insects - Spiracle Control • 337
C. Kaars
Ventilation in Active and in Inactive Insects • 367
P.L. Miller
VI. TEMPERATURE REGULATION
Temperature Regulation During Locomotion in Insects • 391
B. Heinrich
VII. ENERGETICS
Insect Flight Energetics • 419
T.M. Casey
Energetics of Crustacean Swimming • 453
B.R. Hargreaves
Energetics of Pedestrian Arthropods • 491
C.F. Herreid
VIII. OVERVIEW AND SUMMARY
Arthropod Locomotion as Seen Through a "Vertebrate"
Eye • • 527
C. Gans
Index • 541
LOCOMOTION IN ARTHROPODS: AN EVOLUTIONARY PHANTASMAGORIA
Clyde F. Herreid II
Department of Biological Sciences
State University of New York
Buffalo, New York
Animals move. Movement is a hallmark of their "animalness".
With their muscles, pseudopodia, flagella, and cilia aflutter, they
burrow, flit, scamper and undulate through their environment using
an amazing assortment of locomotory styles. Nowhere is this diver
sity better seen than in the arthropods - animals that constitute
over 75% of the world's species. Here among the insects, crusta
ceans, spiders, centipedes and millipedes, we find the most
beguiling array of fliers, swimmers, and pedestrians known to man.
Consider the fliers: varying from diminutive fruit flies and
mosquitoes with wing beat frequencies numbering in the hundreds per
second to the giant tropical butterflies that lazily glide about.
We see fliers that dart like fighter planes and others that hover
like helicoptors. We see body forms that vary from the graceful
filamentous dragonflies moving like exclamation marks over a summer
pond to the bulbous bumble bee scrambling from flower to flower.
We see monowings and biwings. We see fliers such as grasshoppers
that are aloft for but a few wing beats to monarch butterflies that
soar for thousands of kilometers. And what of the spiders that
sail through the sky as arthropodial balloonists bouyed up by their
silken threads into the clouds?
Consider the swimmers: varying from backstroking water beetles,
sidestroking blue crabs, to the upside-down and rightside-up shrimp
sculling their way like translucent phantoms through the deeps. We
see the explosive tailflipping escape reaction of a crayfish and
long distance swimming by the blue crab that migrates over 100 km
up the Chesapeake Bay.
2 C.F.HERREID
Or consider the pedestrians: varying from the underwater
walkers like the spiny lobsters moving with their eight-legged gait
in single file in a queue stretching across the sandy bottom of the
Great Bahama Bank and washed by the Gulf stream to the maurading
six-legged army ants shredding a path through the tropical jungle.
Among caterpillars, inchworms, praying mastises, cockroaches, scor
pions, and centipedes, we see leggless locomotion, quadrupedalism,
hexapedalism, octapedalism and polypedalism of ingenious variety.
We see runners, jumpers, and burrowers aplenty: cockroaches
sprinting, fleas catapulting and grubs grubbing.
All this locomotor diversity is spectacular and is accompanied
by an equally impressive array of internal support and control sys
tems: skeletal, neuromuscular, respiratory, circulatory and the
like. In the pages to follow, as we survey such diversity, one can
easily be enchanted by the details, the virtuoso performance.
However, we must not neglect the search for general patterns. To
assist us in this effort there are two logical places to turn:
evolutionary theory and the extensive literature describing loco
motion systems among the vertebrates. Neither of these two frame
works is as useful as they might be because our knowledge of the
arthropods is still so rudimentary. Nevertheless, a few remarks
about each will help set the stage for the papers to come.
ORIGIN(S) OF THE ARTHROPODS
Baron Georges Leopold Chretien Frederic Dagobert Cuvier called
them Articulata. Later in 1949 van Siebold and Stanius designated
them the phylum Arthropoda - segmented animals with a hard exoskel
eton and jointed appendages: insects, scorpions, spiders, centipedes,
millipedes, crustaceans, and their relatives.
The origin of the Arthropoda is murky at best. The earliest
fossils appear cir. 600 million years ago in the Cambrian along
with most other invertebrate phyla. The first fossils were marine
and possessed many serially arranged jointed legs which were used
for walking along the bottom. The limbs were biramous in nature
with gill-like appendages on the ou~er branches. This group mayor
may not have given rise to later arthropods.
Because of structural and developmental similarities, most
biologists believe the annelids and arthropods have close evolu
tionary ties. Commonly, one will find in general text books that
arthropods evolved from an annelid ancestor. There is little
evidence to support this view. Certainly, the parapodia of the
marine polychaete worms, long believed to be the ancestral limbs,
have little relationship to the arthropod limb structure, (Manton,
1977). Today most specialists believe that both annelids and arth
ropods have a common ancestral origin springing from some pre
annelid, soft-bodied, segmented invertebrate.
LOCOMOTION IN ARTHROPODS 3
There are two schools of thought about the origins and early
evolution of the arthropods: the monophyletic and polyphyletic
views. The monophyletic view until the last 25 years has been the
accepted and unassailed version of arthropod evolution. Essen
tially, this hypothesis postulates that there was a single ancestral
arthropod type which subsequently evolved into the groups we have
today. The monophyletic view has been promulgated by zoologists
such as Snodgrass (1938), Sharov (1966), and more recently cham
pioned by Boudreaux (1979). Fig. lA shows one example of the
monophyletic hypothesis. Early arthropods are believed to have
developed along two major lines: the Cheliceromorpha, animals with
pincer-like appendages in front of their mouth and the Gnathomorpha,
animals with true jaws. The Cheliceromorpha is represented by the
Pycnogonida (sea spiders), the Xiphosurida (represented today by the
horseshoe crab, Limulus ~.), the Eurypterida (extinct sea scorpions)
and the Arachnida (spiders, mites, ticks, and scorpions). The latter
are the first terrestrial arthropods, according to fossil evidence.
The Gnathomorpha gave rise to the Trilobita and Crustacea (both of
which are believed by some authorities to have arisen from proto
chelicerate ancestors) and the Hexapoda (insects) and the Myriapoda
(centipedes and millipedes). Fig. lA also shows two other groups
of uncertain parentage which are sometimes included as arthropods:
the Onychophora (e.g., Peripatus ~.), once believed to be an
intermediate step linking annelids with arthropods, and the Tarti
grada ("water bears") of ambiguous ancestry.
The polyphyletic hypothesis of arthropod evolution was seri
ously proposed by Tiegs and Manton (1958) and later expanded by
Manton (1964, 1973, 1977, 1979) and Anderson (1973, 1979) among
others. They point out that there is an absence of fossils linking
major groups such as crustaceans, chelicerates, trilobites, and the
insect-myriapod line. Their studies of functional morphology and
embryology suggest to them independent origins of these groups from
soft-bodied segmented ancestors. A polyphyletic view is presented
in Fig. lB as envisioned by authors such as Manton(1977). There
are at least three and possibly four groups that have independent
origins and deserve status as distinct phyla: the Chelicerata,
Crustacea, Uniramia and possibly the Trilobita. According to this
view, the Uniramia are specialized into four groups: the hexapods,
myriapods, onychophorans, and tartigrades. The limbs of the Unir
amia are different from those of any known annelid, and Manton (1977)
proposed they are specializations of the lobopodial type of limb
seen only today in the Onychophora.
In conclusion, both the monophyletic and polyphyletic view
points of arthropod evolution have strong supporters, and their
various positions have been laid out quite clearly in an important
book "Arthropod Phylogeny" (Gupta, 1979). Unfortunately, the con
fusions among specialists will hinder our appreciation of the
possible evolution of locomotor mechanisms.