The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation

603 Pages·1993·17.315 MB·English

by  Bernd Heinrich (auth.)

The Hot-Blooded Insects
The Hot-Blooded Insects
STRATEGIES AND
~
MECHANISMS OF -·
THERMOREGULATION ~~~;~
BERND HEINRICH
SPRINGER-VERLAG BERLIN HEIDELBERG GMBH
Copyright © 1993 by Bernd Heinrich
Originally published by Springer-Verlag Berlin Heidelberg in 1993
Softcover reprint of the hardcover 1st edition 1993
All rights reserved
10 9 8 7 6 5 4 3 2
ISBN 978-3-662-10342-5 ISBN 978-3-662-10340-1 (eBook)
DOI 10.1007/978-3-662-10340-1
This book is printed on acid-free paper and its binding
materials have been chosen for strength and
durability.
Designed by Gwen Frankfeldt
Contents
Prologue
1 Night-Flying Moths 17
2 Butterflies and Wings 76
3 Dragonflies Now and Then 117
4 Grasshoppers and Other Orthoptera 143
5 Beetles Large and Small 191
6 Bumblebees Out in the Cold 227
7 Tropical Bees 277
8 Hot -Headed Honeybees 292
9 The Tolerance of Ants 323
10 Wasps and the Heat of Battle 334
11 Flies of All Kinds 343
12 Sweating Cicadas 369
13 Warm Caterpillars and Hot Maggots 382
14 Fever 411
15 Cold Jumpers 422
16 Social Thermoregulation 447
Summary 510
References 525
Acknowledgments 585
Index of Authors Cited 590
General Index 598
Prologue
N
o
aspect of the physical environment is more important
to insects than temperature. In most environments tem
perature fluctuates through time, but insects also ex
perience extreme temperature variations in space. A large mass,
such as a human body weighing 65 kg, would register no mea
surable temperature increase by stepping from shade to sunshine
for several minutes; a 10 mg fly, however, heats up some 10 C
0
in only 10 seconds when it lands in a sunfleck. Needless to say,
the thermal environment faced by insects is potentially much more
severe than it is to us or to any other vertebrate animal. And it is
probably not an exaggeration to claim that insects have evolved
some of the most amazing feats of thermal adaptation and ther
moregulation in the entire animal kingdom. Yet, little over 20
years ago, that statement would have seemed eccentric.
As we sat one night in 1969 in front of a white sheet illuminated
by a lantern on Mount Kainde in New Guinea among dark forest
trees festooned with orchids, moss, and tangles of lianas, one after
another beautiful moth, of dozens of different species, flew out of
the darkness. I captured the arriving insects by net and thrust a
thermocouple probe into each one to measure its body tempera
ture. My host, Peter Shanahan, owner of the coffee plantation
and of the white sheet, kindly tolerated my unusual routine.
I was grasping for any and all clues that might ultimately allow
me to figure out what to me seemed a deeply puzzling question:
How could moths, who have no sweat glands, no lungs, no cap
illary system for peripheral blood circulation, and no major mus
cles besides those used for flight-how could such creatures
possibly regulate their body temperature and fly at the same time?
After two years of grappling with the problem for my Ph.D. thesis
under George A. Bartholomew and Franz Engelmann at UCLA, I
had only recently become convinced that some sphinx moths
could, indeed, stabilize their thoracic temperature within 2-3 °C
of 40 °C while in free flight over a wide range of air temperatures.
But it was still a mystery to me how they did it. There were no
clues to go on and no precedent. Except for work being done at
one other laboratory, there was also little or no interest in the
question. Almost nobody was thinking about "insect thermoreg
ulation" then.
It had been difficult enough for me to trust my own previous
data of a sphinx moth stabilizing its thoracic temperature in flight
over a wide range of ambient temperature while its level of heat
production appeared to remain totally unchanged. This result was
either unprecedented or a big faux pas. I suspected the latter
because a team of other researchers on the topic had just published
not one but a whole series of papers with a conclusion entirely
different from mine. But now in New Guinea I was pleasantly
shocked to find that some of the smaller moths with large wings
barely heated above air temperature. Some of the sphinx moths,
however, maintained thoracic temperatures near the phenome
nally high level of 46 °C . The night was chilly, and these large,
narrow-winged moths, being heated some 9 °C above my own
body temperature, were clearly not warm-blooded. They were
hot-blooded.
As would later become apparent from comparative studies of
many other insects described in this book, neither the "hot" nor
the "cold" moths that night were an exception. Some moths (and
other insects) even fly with body temperatures near DoC, the
freezing point of water. In a few short years I've come to believe
that certain insects are among the most highly evolved organisms
on earth with respect to mastering temperature as a variable of
the physical environment. In that and many other respects they
are as adequate as any homeotherm.
The insects were the first animals on earth to evolve social
systems. They were the first group of organisms in the history of
life on earth to fly. Millions of years before the dinosaurs appeared,
the invention of flight by insects had already made their diversi
fication possible. And flight made many of them the first endo
thermic, or hot-blooded, and ultimately also thermoregulating
animals on earth. (Later, endothermy became not only a conse
quence of flight, but also in some cases a necessity for it.)
2 THE HOT-BLOODED INSECTS
Insects are delicate microscopic whiteflies and massively chunky
goliath beetles. They are colorful butterflies flying lonely missions
through the jungle, and they are teeming masses of blind termites
building towering castles of clay taller than a two-story building.
It is difficult to imagine a group of animals more different from
us, or more varied. As Howard Ensign Evans so aptly pointed out,
it is as if they were an independent form of life from another
planet. Their riot of forms and exuberance of diverse life-styles
make them ideal organisms for the comparative studies needed to
umavel evolutionary mechanisms, especially those that relate to
temperature adaptation. Despite their usefulness for illuminating
general theoretical insights, insects have often been looked upon
as if they were indeed from another planet. As I write, a just
published book on new directions in ecological physiology gives
less than passing lip service to this, the most abundant, diverse,
and species-rich group of animals on earth. Yet I believe (and this
is a personal opinion that I hope will be supported in this book)
that insects, perhaps more than any other animals, have much to
teach us about how physiological adaptations contribute to be
havior and ecology.
In insects the implications of thermoregulation have routinely
been explored to the ecological levels of organization (particularly
in bees, beetles, butterflies, and grasshoppers) because their ther
moregulation is often closely and intimately related to ecology. In
contrast to our close study of vertebrate animals, however, our
ignorance of physiological mechanisms in insects still looms large,
and it is still plagued by glaring controversies and disagreements.
As one of the more prominent workers on insect thermoregulation
has told me, "One of the things I most like about working with
insects is that much physiology is so poorly understood that you
constantly confront the sorts of basic questions that were solved
in vertebrates a century or two ago. Vertebrate physiology seems
bankrupt by comparison." I share this idea that, in comparison
with vertebrate biology, the study of insects has yielded many
important new insights, and there is more still to learn.
There are several reasons for the slow progress with insects until
recently. Undoubtedly one impediment was the view of insects as
primitive animals easily classified as "poikilotherms"-animals
whose body temperature follows that of the environment. This
notion was hardly one to spark exciting questions.
Another reason for slow progress on insect thermal physiology
is their body size. Julian S. Huxley speculated in 1941 (in "The
PROLOGUE 3
Uniqueness of Man") that insects have been cut off from further
"progress" by their breathing mechanism: "The land arthropods
have adopted the method of air-tubes or tracheae, branching to
microscopic size and conveying gases directly to and from the
tissues, instead of using a dual mechanism of lungs and a blood
stream. The laws of gaseous diffusion are such that respiration by
tracheae is extremely efficient for very small animals, but becomes
rapidly less efficient with increasing size, until it ceases to be of
use at a bulk below that of a mouse. It is for this reason that no
insect has ever become, by vertebrate standards, even moderately
large." He goes on to argue that it is also for this same reason that
none has become even moderately intelligent, because none has
reached a size large enough to provide the minimum number of
neurons required for "the multiple switchboards that underlie
intelligence. "
The small body size of insects that clamps a low ceiling on their
intelligence also severely taxes human ingenuity to study their
physiology of thermoregulation. Thermoregulation can be accom
plished only by studying intact organ systems, and it usually
involves the simultaneous and smooth operation of many organ
systems, those involving locomotion, water balance, blood circu
lation, and gas exchange. All must often be operating simulta
neously before the phenomenon under study can be observed.
And instrumental observations are difficult and often nearly im
possible to make without doing gross damage to the system when
that system is of minute dimensions. Many aspects of normal
experimentation that are easily possible with vertebrate animals
are difficult with insects. But this is part of their charm.
The available evidence for some physiological mechanisms in
insects is sometimes still more circumstantial than one might wish.
Since the insects' small size often places a large burden on an
experimentalist's skill and the instruments used, it is sometimes
debatable whether or not the data on the simplest of measure
ments, such as body temperature, are reliable. This is a legitimate
concern, and I shall point out repeatedly in this book where I
believe studies have gone astray. I hope here to provide not only
a review and a synthesis of over 1,000 technical research papers
from the scientific literature, which has been growing steadily
since 1965 (see Figure P.l), but also a critique of the available
work and suggestions for how it may be improved. Most of these
articles are each as long as some of the following chapters, and
I've been forced to reduce many of them to one-liners. For these
4 THE HOT-BLOODED INSECTS
80
•
•
•
70 •
(;j • • •
~ 60
~ • •
c:
~
"5
~ 50
o
E
•
Q)
:E
i •
•
.£; 40
oc: • •
o~ • •
~ •
:c 30
:a::l. •
•
'0
~ •
E •
~ 20 •
10
••
•
1960 1970 1980 1990
Fig. P.I Number of publications on insect thermoregulation per year from
1965 to 1990, as retrieved by a computer search (BIOSIS database, cross
indexing body temperature/thermoregulation and insects/Insecta) by Craig A.
Robertson.
perhaps unavoidable indignities I apologize, nevertheless. Much
of the work I explore has not been previously consolidated and
critically digested so as to make it accessible even to a scientific
audience.
If the data are taken into consideration, then we have come a
remarkably long way in understanding insect thermoregulation
since a thermometer was first laid alongside the abdomen of
PROLOGUE 5
insect resting in a little closed container over a century ago, even
though only a tiny fraction of the species which might reasonably
be expected to thermoregulate has been examined. Despite the
million or so insect species that exist, it is reasonable to expect
that mechanisms of thermoregulation are relatively conservative
because research so far has been consistent with this supposition.
Patterns are emerging and major puzzles are being solved, and I
felt that it was now appropriate to consolidate our information.
No generalities may be made until accurate empirical infor
mation is established. In insect biology, because of the very small
size, the complexity, and the variety of animals, and also the ease
of getting (some) data (and ease of misapplying it), there is much
imperfect knowledge of how different physiological systems in
teract. Furthermore, the same sets of data often have entirely
different relevance when viewed from the ecological rather than
the physiological perspective. Both views are necessary, but both
are often not available from the same data set. It is difficult for
me to imagine a scientific field at times so muddled with contro
versies as a result of imperfect information or the complexities of
getting good information and applying it critically to the appro
priate perspective. These are problems for any young field, and to
counter them I describe experiments in those cases where there
is reasonable doubt, one way or the other, on how to interpret
them. Indeed, I feel that the designs of the experiments used to
answer questions are fascinating in their own right, and try to
give at least a feel for how new knowledge in the field is acquired.
This book is based on the primary literature. Nevertheless, there
are numerous reviews of insect thermoregulation and particular
details of insect thermoregulation that the reader may wish to
consult for other coverage, for historical knowledge, and for other
points of view. Biochemical considerations (Hochachka and So
mero, 1984), the effects of energetics (Heinrich, 1979) and loco
motion on thermoregulation (Kammer and Heinrich, 1978; Heath
and Heath, 1982), and aspects of thermal energy budgets and the
thermal environment affecting body temperature are found else
where (Parry, 1951; Gates, 1980; Gates and Schmerl, 1975; Porter
and Gates, 1969; Willmer, 1982; Cossins and Bowler, 1987).
Other selected aspects of invertebrate (Wieser, 1973) and insect
thermoregulation have been previously reviewed (Cloudsley
Thomson, 1970; Heinrich, 1974, 1981; May, 1979, 1985; Casey,
1988).
In organizing this book I faced the choice of highlighting topics
6 THE HOT-BLOODED INSECTS