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Marine Biological Laboratory bbrary 

Voods Hole, Massachusetts 




Presented by the MBL Associates-1971 Gift 



methuen's monographs on biological subjects 



General Editor: Kenneth mellanby 



THE PHYSIOLOGY OF INSECT SENSES 



The Physiology 
of Insect Senses 



V. G. DETHIER 

Professor of Zoology and Psychology 
University of Pennsylvania 




London: METHUEN & CO. LTD 
New York: JOHN WILEY & SONS INC 



First published September 1963 

Reprinted 1964 

1.2 

© 1963 Vincent G. Dethier 

Printed in Great Britain by 

Richard Clay (The Chaucer Press), Limited 

Bungay, Suffolk 

Catalogue No, 12/4125/62 



Contents 



PREFACE Vii 

I INTRODUCTION J 

II GENERAL CHARACTERISTICS OF THE SENSORY 

SYSTEM 5 

III MECHANORECEPTION 26 

The Tactile Sense-Sensilla Trichodea - Proprioceptors - 
The Role of Mechanoreception in Locomotion - 
Responses to Gravity 

IV SOUND RECEPTION 77 

Tympanic Organs - Hairs as Sound Receptors - The 
Johnston's Organ of Culicidae - Perception of Vibra- 
tions in Solids 

V CHEMORECEPTION 112 

The Receptors - Olfaction - Contact Chemoreception 

VI RESPONSE TO HUMIDITY 156 

VII PHOTORECEPTION 162 

The Compound Eye - Colour Vision - Polarized Light 
- Form Perception - Ocelli - Stemmata 

REFERENCES 214 

INDEX 256 




Preface 



Thirty years have elapsed since the appearance of Eltringham's 
The Senses of Insects (first published 1933 in this series). In the inter- 
vening time our knowledge of sensory physiology has advanced 
further than during any previous period of study. The augmented 
and accelerated advance may be attributed to new technological 
developments and a notable increase in the number of research 
workers interested in insects for their own sake or as material 
uniquely suited to the solution of one or another basic biological 
problem. 

The two most powerful modern tools placed at the disposal of the 
sensory physiologist are electronic apparatus for detecting electrical 
events in nerve tissue and the electron-microscope. The first has been 
responsible for removing from the realm of mystery the function of 
so-called Type II neurons in insects, for confirming the facts that 
campaniform sensilla are mechano- rather than olfactory receptors, 
and for initiating the unraveUing of the multitude of events that occur 
as a part of vision. Electric recording from neural tissue has greatly 
expanded our rather conservative estimation of sense organs in 
general. 

Developments in the field of electronics has not, however, ren- 
dered the behavioural approach to sensory physiology obsolete. 
In fact, experiments in behaviour not infrequently point the direc- 
tion that electrophysiological research should follow. Two cases in 
point are the studies of the tympanic organ of moths and of the 
chemoreceptors of flies. Without behavioural correlates the electro- 
physiological findings are of small value. 

Just as behavioural studies have engendered electrophysiological 
experiments, these in turn have driven the physiologist back to 
structure. Whereas in many instances conventional histology has 
been extended to its limit, in others it has barely scratched the sur- 
face, and large areas of the nervous system are still empty areas 
whose only detail is the notation 'unexplored'. Where light micro- 
scopy has reached the limit of resolution, the electron-microscope 
has opened up vast new areas of investigation and stimulated addi- 
tional electrophysiological studies, which in turn have posed new 
behavioural questions to bring the endeavour full turn. 

vii 



Vm PREFACE 

We are in the midst, therefore, of a revolution in sensory physio- 
logy. There is no better evidence for this than the high element of 
controversy that flourishes in many areas indicating that exploration 
is still in its early stages. This state of affairs is best illustrated by the 
controversies in photoreception. The final verdict is by no means 
rendered. In many cases our knowledge is still in a state of flux. 
While every effort has been made in this book to present both sides 
of questions, a personal bias has been applied. This bias is fashioned 
by an appraisal of how well the antagonists have presented their 
cases in the literature. 

Recent advances in the physiology of the insect sensory system 
have proceeded at such a pace that it is impossible to refer to every 
published report. In the field of sound reception alone there are over 
2,000 articles. For all phases of this book, about 2,000 references in 
toto have been examined. Of these, about 700 have been selected for 
listing, but the accumulated knowledge of others has been built upon 
freely. For the reader interested in the older literature, the works of 
Demoll and von Buddenbrock should be consulted. For all purposes, 
the works of Wigglesworth and Roeder are invaluable. Where 
possible, references have been made to reviews rather than to the 
multitudes of individual papers. Where an investigator has published 
a series of papers on a given subject, only the most recent has been 
quoted unless an eariier paper is germane to some particular point. 
During the period of preparation of this book insect physiologists 
have not been idle. The most recent papers have probably been 
treated somewhat cavalierly, since a running revision is hardly 
feasible, but at the very least they are included in the references to 
assist the reader in pursuing the matter himself. 

The segment of knowledge represented by this book has been 
rather narrowly circumscribed, a circumstance dictated by the enor- 
mous volume of literature but ameliorated by the fact that other 
excellent volumes exist to fill the lacunae. The subject matter has 
been 'sensory physiology'; behaviour, as such, has been neglected. 
It is well represented, however, by Carthy's fine book, by Roeder, 
by Wigglesworth, and by von Buddenbrock. Also, I have not ven- 
tured farther into the central nervous system than the lamina gang- 
lionaris of the optic lobes, partly because I have been interested 
primarily in sensory input and the interaction of sense organs and 
their environment and possibly because one naturally hesitates to 
venture far into an unexplored jungle. And finally, the temperature 
sense has been completely neglected. This, in part, merely reflects the 



PREFACE ix 

neglect that it has received at the hands of research investigators. 
There is considerable Hterature on the behavioural aspects of tem- 
perature sensitivity, little of value on the physiological aspects. 

The co-operation and courtesy of a number of persons and organi- 
zations has been invaluable in the preparation of this book. Paul B. 
Hoeber, Inc. has granted permission to reprint sections of Chapter 
II which formerly appeared in Roots of Behavior, edited by E. L. 
Bliss. Similarly, the Society for Experimental Biology has granted 
permission to reprint sections of Chapter V which appeared in 
Symposium No. 16of the Society for Experimental Biology. Figs. 17, 
18, 21, and 25 were supplied through the courtesy of M. L. Wolbarsht ; 
Figs. 40 and 41, through the courtesy of O. Lowenstein and L. H. 
Finlayson; Figs. 56, 65, 66, and PI. I, through the courtesy of K. D. 
Roeder and A. E. Treat; PI. Ill, through the courtesy of J. R. Adams. 
Peter G. Walsh has assisted in the preparation of illustrations. To 
all of these I express my sincere gratitude. 

V. G. Dethier 

E. Blue Hill, Maine 
June 1962 



CHAPTER I 

Introduction 



The gross characteristics of the planet earth are the same for all living 
things inhabiting it. It has a characteristic gravitational field; it re- 
ceives radiant energy from outer space to the extent determined by the 
filtering properties of its atmosphere; it is built of specific kinds of 
chemical compounds in certain quantitative relationships. The details 
of these properties differ from place to place on the planet. Some are 
more conducive to animal life than others, and the uneven distribution 
of animals in the biosphere is a measure of this and of the adjustments 
that various forms of life have made to the details. To regulate their 
relations with the earth's environment, animals have evolved sensing 
devices for detecting such details as are of direct adaptive value. 

Since we *see' the world with our own particular sensing devices, it 
is difficult to understand fully how other animals *see' it. What picture 
of the details of the world is perceived by the bee that sees in the ultra- 
violet, the snake that is deaf to air-borne sounds but detects infra-red, 
the shrew that cannot see colour, the electric fish that detects changes 
in the electric field about it? To appreciate these points of view, let 
alone understand the manner in which all biological sensing devices 
work, it is helpful to look first at the world, not at the level of detail 
perceived by us but at a level that we cannot perceive directly, the 
elementary particles whose interactions and combinations form 
the universe. 

Of the thirty or so kinds of particles that make up earth or come to 
it from outer space, the only stable ones are protons, neutrons, 
neutrinos, electrons, and photons (Ruderman and Rosenfeld, 1960). 
Some of these (e.g., photons, neutrinos) occur free; others, usually 
combined into atoms and molecules. Some, such as electrons and 
photons with certain energy, have profound effects on living material ; 
others, such as neutrinos, pass through organisms undetected and 
without effect. All have different kinds of energy. In the final 
analysis it is to these particles that animals must make adjustments. 
Organisms living in other parts of the universe would be exposed to 
other kinds of particles and would have to evolve differently, each 

in its own milieu. 

1 



2 THE PHYSIOLOGY OF INSECT SENSES 

Pertinent details of an animal's environment are detected first 
by utilizing the energy of particles to perform work in the biological 
system. Thus, light is detected by virtue of an absorber which trans- 
forms the energy of photons of certain specific energy. There is no 
absorber to transform the energy of photons which, for example, 
make up X-rays and gamma-rays. Heat is detected by absorbing the 
energy of photons of a different energy level. Electricity is detected by 
utiUzing the energy of electrons. Tastes and smells are detected by 
utilizing the potential energy existing in the mutual attraction and 
repulsion of the particles making up atoms. Sound is detected by 
using the energy of moving particles of molecular size. 

A sense organ is a part of an organism specialized to receive a small 
amount of energy from certain of the sources mentioned above and to 
utiUze it to set off a train of events culminating in a nerve impulse. 
Many cells and parts of cells do work with energy derived from the 
sources mentioned. Many cells use the potential energy in carbo- 
hydrates to do work, yet they are not sense organs. Certain of the cells 
of green plants absorb photons of certain energies and perform work 
much as the pigment rhodopsin of the eye absorbs protons and does 
work. A sense cell differs from these in at least three major respects : 
first, the work which is done by the sense cell is done at the expense of 
its own potential energy, the energy of the environment is merely a 
trigger; second, all sense organs, as far as we know, transform their 
potential energy into electrical energy; third, they transmit this 
electrical energy to another cell. And this energy, in turn, is transmitted 
by an element which by itself could not have detected the original 
environmental energy. 

A sense organ implies another element that will receive the change. 
In this sense our attitude towards sense organs is teleological, but 
there seems to be no escape from this attitude. As Granit (1955) has 
concluded: Tor many purposes, e.g. physiochemical studies of 
primary events, we can neglect the teleological aspects of the sensory 
message and the general problem of central decoding of the code of 
spikes, but I want to emphasize that research into special senses 
differs from many other recognized branches of physiology in pre- 
supposing and accepting the fact that understanding of biological 
purpose is part of its aim, be it movement or perception. To close 
one's eyes to this aspect of sensory physiology is to neglect the 
biological, psychological, and philosophical implications of a branch 
of natural science which actually is capable of giving some meaning 
to "meaning' 



.'♦ > 



INTRODUCTION 3 

Receptors change reversibly when energy is apphed to them (i.e., 
they are sensitive, they detect), they do work (i.e., they are responsive)] 
they generate a message to be transmitted beyond their boundaries. 
Thus, there are three levels at which the physiology of receptors may 
be considered. 

Considered first as detectors, receptors would not make much 
information available to an organism if they were so imperfect as to be 
insensitive to any but the greatest energy changes or so perfect as to 
be sensitive to every single elementary particle. Furthermore, their 
usefulness would be limited if they were so indiscriminate as to detect 
equally all kinds of particles and so simple as to detect only the pres- 
ence or absence of a stimulus. From the point of view of an animal's 
survival, there must be an optimum sensitivity, a capacity for discrim- 
inating different kinds of stimuli, and a capacity for measuring not 
only on-off, but rate of change, magnitude of change, absolute change, 
and direction of change. 

It is characteristic of protoplasm that it has moderate sensitivity to 
many forms of stimuli and may be sensitive to more than one para- 
meter of the stimulus. But receptors have become specialized in that 
they possess enhanced sensitivity to some particular form of energy 
and to some particular parameter. First, there is development of 
special characteristics at the molecular level. The presence of a pig- 
ment to absorb radiant energy in some particular wavelength 
(rhodopsin in the rods and cones of the vertebrate eye) or the presence 
of molecules to uncouple the potential energy in sugar molecules 
(sweet taste receptors) are more well-known examples. 

In addition to specialized sensitivity per se, receptors have also 
become surrounded with accessory structures whose presence 
modifies in various fashions the incident energy. A striking example is 
the complicated accessory structures of the auditory labyrinth of the 
vertebrate ear. These accessory structures may not only affect the 
sensitivity of the combined system but may also determine which 
parameter (magnitude, rate of change, etc.) of a stimulus may be used. 
Thus, refinement of the receptor from a generalized non-discriminat- 
ing sensing element with many imperfections has come about through 
evolutionary specialization of the sensing part of the receptor itself 
and the structures with which it has become associated. 

In addition to looking at the sensitivity of a receptor, one must also 
look at its responsiveness. In transforming the energy that comes to 
it to do some form of work, the receptor does not maintain a one-to- 
one ratio between input and output. A great deal of integration 



THE PHYSIOLOGY OF INSECT SENSES 




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INTRODUCTION 5 

(putting parts together into a whole) takes place in the receptor, so it is 
probably desirable to anticipate a bit and to present a general picture 
of events as they occur in a receptor cell. 

Energy impinging upon the cell initiates changes that ultimately 
generate a propagated all-or-none nerve impulse. As Bullock (1958, 
1959) has pointed out, 'The determination of firing is not merely the 
build-up of an adequate stimulus or its transduced and amplified 
resultant to a critical level, but rather it is a sequence of labile couplings 
between graded events, each occurring in a limited fraction of the 
neuron.* A series of separate steps with alternate pathways lead to 
firing. Some are reflected in changes in the cell membrane potential 
(Fig. 1). Others are excitability cycles and the presence or absence of 
after-effects not reflected in the membrane potential. Between the 
advent of the physical stimulus from outside the receptor, therefore, 
and the final production of a nerve impulse, there is a long complicated 
series of events. The importance of these is that the receptor, a highly 
complex, physiologically non-uniform cell, not only detects energy 
and transduces it but also carries out a considerable amount of 
integration. 

When it comes to the transmission of information from the receptor, 
one begins the long and difficult intellectual trek into the central 
nervous system. This is beyond the scope of our endeavour here ; 
however, it is worth pointing out that much additional integration is 
possible long before the central nervous system is reached. Different 
channels (nerves) from the receptor may have very different trans- 
mitting characteristics - different gain, time constants, and maximum 
output (cf. Bullock, 1953). 

Thus, the sensory physiologist is interested in the way in which 
accessory structures filter or direct the energy going to a receptor, the 
way in which the receptor transduces this energy into another form, 
and how there is generated a propagated nerve impulse which is a 
code relating to the central nervous system or to special effectors the 
nature and parameters of a stimulus. And in seeking answers to these 
questions, it is of no import to the sensory physiologist whether the 
stimulus originates outside of the animal or from within or whether or 
not it is ever perceived at a conscious level. 



CHAPTER II 

General Characteristics of the 
Sensory System 

One of the biggest challenges that animals faced in their evolutionary 
history occurred when they essayed terrestrial life. By all counts the 
sea is a more permissive environment than land. It is above all a 
more stable and uniform environment. It exhibits no profound 
temperature changes; humidity is no problem; osmotic relations are 
constant. Consequently, the need to develop sense organs to detect 
changes in these realms is minimal. The physical properties of water 
obviate the necessity of differentiating between olfaction and taste 
in the sense that terrestrial organisms do. Density precludes distant 
vision as well as limiting wavelength discrimination. Since water is a 
medium of transport, food procurement does not present all the 
problems that confront the terrestrial animal. By the same token 
water serves as a medium of dispersal of eggs and sperm and as a 
cradle for the young so that the complex sensory discrimination and 
behaviour patterns which have evolved among land animals for 
reproduction and parental care are largely absent in the sea. 

One of the more fundamental problems that confronted animals on 
emergence to land was that of support, since air does not lend the 
helping hand that water does. Before emerging on land, animals had 
already set out on two paths of skeletal development. The arthropods 
cast the die for an exoskeleton; the chordates, for an internal 
skeleton. The choice of skeleton had profound effects upon the 
direction that the development of the nervous system followed. The 
skeleton is a major limiting factor; all other organs accommodate to 
it. The arthropod exoskeleton determined the method of growth - the 
only way to increase size is by moulting - and it also limited the overall 
size of the animal. Once free of the support of the sea, the animal was 
limited in size by the engineering principles of a frame dwelUng (cf. 
Thompson, 1943). This may be one of the reasons why insects in 
general are small animals (although during the Carboniferous one 
dragonfly attained a wingspread of more than 2 ft.). The largest living 
species are somewhat larger than the smallest mammals, while the 

6 



GENERAL CHARACTERISTICS OF THE SENSORY SYSTEM 7 

smallest are smaller than many protozoa (Folsom and Wardlc, 1943). 
The range extends from about 166 mm. (the Venezuelan grasshopper 
Tropidacris latreillei and some East Indian walking sticks which arc 
even larger) down to a fraction of a millimetre (some springtails, 
ceratopogonine midges, and beetles of the family Trichopterygidae). 

An exoskeleton and small size are therefore two of the outstanding 
characteristics of insects. Clearly they must impose upon the nervous 
system certain restrictions which will be reflected in behaviour. For 
example, smallness reduces the distance over which conduction of 
impulses is required. This would imply, other things being equal, more 
rapid response and movement. At the same time, however, size 
limitations compel a reduction in the number of neurons possible in 
the system. A reduction in number of units implies a reduction in the 
informational capacity of the system. Reduction is carried further by 
the development of so-called giant fibres. Thus, in the abdominal 
nerve cord of the cockroach Periplaneta americana the giant fibres 
occupy about 12 per cent of its cross-sectional area (Roeder, 1948). 
The largest of these fibres measure 30 microns in diameter, exceeding 
in this respect the largest (alpha) fibres in the mammalian system. 

Roeder (1959) argues persuasively that the relative merits of a 
nervous system composed of a few large units versus one consisting of 
many small units can be appreciated if one concluded that detail of 
information has been sacrificed for speed. It is noteworthy that large 
insects tend to react more slowly than smaller ones and that one at 
least, the giant Australian cockroach {Macropanesthia rhinocerus 
Suass.), lacks giant fibres (Day, 1950). A large fibre cannot carry as 
much information from one point to another as can a number of 
smaller fibres because of the on-off or all-or-none nature of the nerve 
impulse, but it can transmit its information more rapidly. The giant 
fibres are the internuncial units in an alarm reaction. In the detection 
of, and escape from, predators, speed has greater survival value than 
detailed information. From the point of view of a predator also, speed 
is important, since attack must be as rapid as the startle response of a 
prey. Here, however, the information required is of a much more 
complex nature, but it, too, must be handled by a small nervous system 
with relatively (as compared with vertebrates) few units. 

Another example of the parsimony of neuronal elements is seen in 
the motor system of insects. As Hoyle (1957) has pointed out, there 
are functionally important muscles which are microscopically small 
and yet move joints with precision and delicacy. In contrast with 
vertebrate muscles, which are innervated by hundreds of nerve fibres 

B 



8 THE PHYSIOLOGY OF INSECT SENSES 

under a complex central control, the insect muscle is supplied with a 
very small number of motor fibres. Some muscles are supplied by four 
or more axons; some are mono-axonic. More commonly, a muscle is 
supplied by two axons. Thus, the entire system of nervous control 
differs from that in the vertebrates (Hoyle, 1957). 

In the sensory system, too, there is a limitation on the number of 
neurons. This is related not only to the small size of the body but also 
to the fact of its being encased in a rigid non-living cuticle. Only at 
certain points do the energies of the external environment filter 
through to sense cells. As compared with the integument of an 
echinoderm, which may have as many as 4,000 sense cells per square 
millimetre of surface, and a mammal, whose skin receptors may run 
into the millions, the integument of an insect is relatively barren and 
insensitive. The fourth-stage larva of Rhodnius, for example, has only 
about 420 receptors on the entire ventral surface of each abdominal 
segment (Wigglesworth, 1953); the sensory complement of the entire 
leg of a fly is less than 500 (Grabowski and Dethier, 1954; Dethier, 
1955 b) ; the total number of stress receptors on the whole body of the 
drone honeybee is only about 2,948 (Mclndoo, 1914 b, 1916). It is 
only when one counts the cells in the two most highly developed 
sensory areas of insects, the eye and the antennae, that the number of 
receptors becomes large. And even then they fall short, by several 
orders of magnitude, of equalling the number in vertebrates. The 
maximum number of receptors in any compound eye is that found in 
Odonata and is estimated to be approximately 210,000 (Snodgrass, 
1935). The number is more usually a few hundred or thousand. The 
antennal sense cells of the honeybee only number between 30,000 and 
500,000 (Vogel, 1923 b; Snodgrass, 1956). 

Economy of cells is seen further in the remarkable organization of 
the nervous system whereby stimulation of a single sense cell may be 
adequate to set off a whole chain of behaviour. Stimulation of one 
neuron in the labellar taste organs of flies initiates proboscis extension 
and the initial steps in the feeding pattern (Grabowski and Dethier, 
1954; Dethier, 1955 a; Arab, 1959). Roeder and Treat (1957) have 
shown that the acoustic response in noctuid moths is mediated by 
only two receptor cells. Similarly, stimulation of one neuron in tactile 
receptors can initiate a whole series of behaviour patterns ranging 
from simple withdrawal of an appendage to running. 

The ultimate in parsimony is achieved by all known receptors being 
primary sense cells, that is to say, they are true neurons rather than 
modified epithelial cells connected synaptically to a neuron (vom 



GENERAL CHARACTERISTICS OF THE SENSORY SYSTEM 9 

Rath, 1888, 1895, 1896; Hanstrom, 1928). Although the sensory 
system of vertebrates also contains some primary sense cells (e.g., the 
rods, cones, and olfactory receptors), the taste receptors and auditory 
receptors are specialized non-neural cells connected with neurons. 
Possession of primary sense cells means that one cell does the work of 




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Q 







Fig. 2. Stages in the embryonic development of a hair. Tr, trichogen cell; 
To, tormogen cell; N, bipolar neuron. (Redrawn from Krumins, 
1952.) 

at least two; it performs the multiple function of detecting environ- 
mental energy, transducing it, and initiating and transmitting im- 
pulses to the appropriate ganglion. From the point of view of the 
sensory physiologist, the primacy of the insect receptor is a boon 
to investigations, since all events occur in the one cell. It is 
generally believed, furthermore, that the primary neurons make their 



10 THE PHYSIOLOGY OF INSECT SENSES 

connexions directly with the central nervous system. From time to 
time peripheral ganglion cells have been described, but these not 
infrequently turn out to be non-neural cells. On the other hand, one 
of the more recent reports, that of Peters (1961) describing a multi- 
polar neuron in the labellum of flies, warrants further investigation. 

While it has generally been accepted for some time that sense cells 
arise by mitosis from epidermal cells (vom Rath, 1888, 1895, 1896; 



Fig. 3. A 'circular nerve' in the integument of fourth-stage larva of 
Rhodnius and the cell bodies from which it was derived following an 
extensive burn of the cuticle in the third-stage. (Redrawn from 
Wigglesworth, 1953.) 

Haffer, 1921; Hanstrom, 1928; Snodgrass, 1935) (Fig. 2), proof that 
the cells are primary sense cells is of relatively recent origin. Vogel 
(1 923 b) claimed that in Hymenoptera the sensory axon grows out from 
the central nervous system and joins the sense cell. Newton (1931), 
Henke and Ronsch (1951), and Krumins (1952) maintained that the 
epidermal sense cells differentiate axons which then grow centripetally 
to join the central nervous system. The matter would seem to have 
been settled, at least for Rhodnius prolixus, by Wigglesworth (1953), 



GENERAL CHARACTERISTICS OF THE SENSORY SYSTEM 11 

who proved by interrupting sensory nerves that axons are regenerated 
by epidermal cells and grow centripctally until they encounter a 
nerve. If they do not encounter a nerve or if they become trapped 
above the basement membrane, which separates the epidermis from 
the rest of the body space, they grow in loops and circles, apparently 
indefinitely (Fig. 3). 




Nc Oc 




Fig. 4. A. Stages in the moulting of sensilla in a fourth-stage larvae of 
Rhodnius. B. Campaniform organ (haematoxylin). C. Tactile hair 
(haematoxylin). D. Campaniform organ (Romanes' method). E. 
Tactile hair (Romanes' method). N, nerve; S, sense cell; Dp, distal 
process; A, axon; Tr, trichogen ; To, tormogen; Nc, new campaniform 
organ; Oc, old campaniform organ; Ns, new seta; Os, old seta; Ni, 
neurilemma cell; Nso, new socket; E, extension of distal process from 
new to old seta. (Redrawn from Wigglesworth, 1953.) 



12 THE PHYSIOLOGY OF INSECT SENSES 

At each moult, when new receptors arise to service the increased 
body size, they, just like regenerating receptors, send axons centri- 
petally to the central nervous system (Fig. 4). Whether or not the 
axons fuse when they come together is still in doubt. Pringle (1938 a) 
was of the opinion that fusion did occur in the cockroach, but 
Wigglesworth (1953) felt that the matter was in doubt in Rhodnius. 




Fig. 5. A small area of the integument of a fourth-stage larva of Rhodnius 
showing hairs and neurons. The number of axons present in each nerve 
as calculated from the number of sensilla is indicated by the figures. The 
inset shows the distribution of epidermal cell nuclei. (Redrawn from 
Wigglesworth, 1953.) 



He showed in Rhodnius (Wigglesworth, 1959) by making a rough 
count of the numbers and types of sensilla on the antenna and a count 
of the axons in the antennal nerve that there must be a fusion of at 
least fifteen sense cells to one axon. Similar counts in the leg indicated 
that similar fusion of the tactile fibres here does not occur. He pointed 
out that a lack of fusion is understandable in view of the need of 



GENERAL CHARACTERISTICS OF THE SENSORY SYSTEM 13 

accurate touch localization. On the other hand, fusion of axons within 
groups of campaniform sensilla, hair plates, and some chordotonal 
sensilla does occur in the leg of the cockroach (Pringle, 1938 a; 
Nijenhuis and Dresden, 1952). 





A B 

Fig. 6. Diagrammatic representation of two types of ommatidia. A. Apposi- 
tional type of diurnal Lepidoptera. B. Superpositional type of nocturn- 
al Lepidoptera. Co, cornea; Cp, corneal process; Cn, crystalline cone; 
CnN, crystalline cone nuclei; R, retinal cell; Rh, rhabdom; T, tracheal 
tapetum. (Redrawn from Snodgrass, 1935 after Nowikoff.) 

The presence or absence of fusion is a matter of considerable 
importance to the electrophysiologist, who must try to interpret 
recordings from afferent nerves. Another unsettled question of 
importance is whether or not the large cells frequently observed at 
the junction of uniting nerves or axons are multipolar nerve cells. 
If they are, it means that a synapse is interpolated between the 
peripheral sensory neuron and the central nervous system. Otherwise, 



14 



THE PHYSIOLOGY OF INSECT SENSES 





Fig. 7. Examples of Type II neurons. A and B. Subepidermal nerve plexus 
in the larva of Melolontha. (Redrawn from Zawarzin, 1912.) 



the path from the primary neuron to the central nervous system is a 
direct one. According to Snodgrass (1935) there are no cells in 
sensory nerves, and Wigglesworth (1953) is of the opinion that the 
cells seen there are actually neurilemma cells. 

Morphologically there are two broad categories of sense cells: 
those whose dendrites are nearly always associated with the cuticle or 
its invaginations (apodemes, tracheae, and cuticle of preoral and oral 
cavities) (Type I) (Fig. 5) ; multipolar neurons never associated with 



GENERAL CHARACTERISTICS OF THE SENSORY SYSTEM 15 

cuticular processes but lying instead on the inner face of the body wall, 
the walls of the alimentary canal, muscles, and connective tissue 
(Type II). Only the cells of photoreceptors lack an obvious distal 
process or dendrite, although even in these cells the distal end is 





B • ^ 

Fig. 8. Type II neurons. A. The hypopharynx of termites. (Redrawn from 
Richard, 1951.) B. The muscles of the mid-gut of Melolontha larvae. 
C and D. The muscles of the oesophagus of Oryctes larvae. (Redrawn 
fromOrlov, 1924.) 

structurally modified (Fig. 6). Depending on the position of the 
neurocyte with respect to the epidermis. Type I neurons are termed 
intraepidermal or sub-epidermal, but there are certainly all gradations 
between the two positions. 

The ontogenetic origin of Type II neurons from the ectoderm has 
not yet been determined (Snodgrass, 1935). Numerically they are less 



16 THE PHYSIOLOGY OF INSECT SENSES 

common than Type I and are most abundant in soft-skinned larvae. 
Their branching distal processes may form an elaborate subepidermal 
net, as in the larva of Melolontha vulgaris (Fig. 7) (Zawarzin, 1912 b). 
They also occur in the walls, muscles, and connective tissue of the 





B 




Fig. 9, Types of campaniform sensilla. A. From the haltere of Calliphora 
erythrocephala. B. From the cercus of Gryllus domes ticiis. C. From the 
cercus of Blatta orientalis. (Redrawn from Hsii, 1938.) 



alimentary tract of some insects {Periplaneta americana [Zawarzin, 
1912 a] and larvae of scarabaeid beetles [Orlov, 1924] [Fig. 8]). 
Richard (1951) has described them in the labium, labrum, and 
hypopharynx of termites (Fig. 9). Until Finlayson and Lowenstein 
(1955, 1958) studied some Type II receptors electrophysiologically, 



GENERAL CHARACTERISTICS OF THE SENSORY SYSTEM 17 

C 




Fig. 10. A campaniform sense organ from the antenna of a grasshopper. N 
bipolar neuron; S, scolopoid sheath; A, axon; D, dendrite; C, cuticular 
dome. (Redrawn from Slifer et aL, 1959.) 

there was no certain knowledge of the function of any of them. 
Electrophysiological studies of those associated with muscle and 
connective tissue have proved them to be proprioceptors. Their 
structure and function will be described in Chapter III. 
Type I neurons and the cells giving rise to the cuticular structures 



18 THE PHYSIOLOGY OF INSECT SENSES 

with which they are usually associated originate from the same parent 
epidermal cell. The combination of the neuron (or neurons), the 
immediate cuticular area, when present, and its generative cells is 
termed a sensillum. A sensillum is thus a sense organ ; the neuron is 
the receptor. With the possible exception of the photoreceptors, all 
sensilla are believed to be homologous and to have been derived from 
setae. Classically, because of the ease of examining the cuticular 
portion, sensilla were classified on the basis of external form. They 



Fig. 1 1 . Sensillum placodeum 
from the antenna of the 
honeybee. N, bipolar 
neuron; A, axon; D, 
dendrites; P, plate; F, 
attachment of fibres. (Re- 
drawn from Snodgrass, 
1935.) 




include setiform varieties (sensilla trichodea), bristles (sensilla 
chaetica), scales (sensilla squamiformia), pegs and cones (sensilla 
basiconica), pegs, cones, or bristles sunk in shallow depressions 
(sensilla coelonconica) or in deep pits (sensilla ampullacea) (Schenk, 
1903). 

Other sensilla whose external cuticular structures are not seta-like 
are undoubtedly derived from setae (Snodgrass, 1935; Lees, 1942). 
The campaniform organs (sensilla campaniformia, sense pores, etc.) 
are visible externally as minute pits in the cuticle, but in section are 
seen to possess a bell-shaped cuticular cap (Figs. 10, 30). Each is 
innervated by a single neuron. Their structure will be discussed in 



GENERAL CHARACTERISTICS OF THE SENSORY SYSTEM 19 

detail in Chapter III. The plate organs (sensilla placodea) are marked 
externally by an oval or elliptical plate surrounded by a narrow 
membranous ring. Each is innervated by a number of neurons (Fig. 1 1). 
One type of sensillum (sensillum scolopophorum, scolopoid 
sensillum, peg organs, chordotonal organs, stiftfUhrcnder Sinnesor- 




FiG. 12. Different forms of scolopoid sensilla. A. Terminal peg from a 
grasshopper sensillum. (From Eggers.) B. Terminal peg from the 
tracheal organ of Gryllus. (From Schwabe.) C. Terminal peg from the 
femoral chordotonal organ oiPediculus. (From Graber.) D. Terminal 
peg from a chordotonal organ in the abdomen of a cerambycid larva. 
(From Hess.) E. A simple chordotonal organ with one sensillum. 
(From Eggers.) F. A. chordotonal sensillum from the haltere of a 
muscid fly. (From Pflugstaedt.) G and H. Scolopoid sensilla from the 
tympanic organ of Cicadetta coriaria S- (From Vogel.) I. Sensillum 
from the tibial organ of Decticus. (From Schwabe.) J. Sensillum from 
the subgenual organ of Decticus. (From Schwabe.) 

gane) does not fit conveniently into any category. The sense cell is a 
bipolar neuron, but its dendrite is not always associated with a 
particular cuticular structure. These sensilla usually do not occur 
singly. They are generally gathered together in bundles having a 
common point of attachment to an undifferentiated part of the body 
wall. Sometimes a small external pit, thickened disk, or nodule 



20 THE PHYSIOLOGY OF INSECT SENSES 

marks the point of attachment. In special cases they are associated 
with a tympanic membrane. They all possess in the region of the 
dendrite a cuticle-like sheath, usually ribbed, and in the majority of 
cases capped with a prominent refractile body. Because of the 




Fig. 13. a sensillum basiconicum from the antenna of a grasshopper. N, 
bipolar neuron; S, scolopoid sheath ; A, axons ; D, dendrites. (Redrawn 
from SHfer^/^/., 1959.) 

resemblance of the combined sheath and cap to a peg-shaped rod, 
the structure has been termed the scolops (Stift). A terminal strand 
may or may not extend from the cap distally to the point of attachment 
on the body wall. 
There is no completely satisfactory name to apply to these sensilla. 



GENERAL CHARACTERISTICS OF THE SENSORY SYSTEM 21 

They were called chordotonal organs by Graber (1882 a) because 
many of them stretched like taut cords from point to point and were 
believed to be auditory organs. Those with a terminal strand were 
termed amphinematic because they appeared to be stretched between 
two threads; the others were termed mononematic (Graber, 1882 a). 
It soon became clear that these sensilla were neither exclusively audi- 




FiG. 14. A thick-walled sensillum basiconicum from the antenna of a 
grasshopper. N, bipolar neuron; S, scolopoid sheath; A, axons; 
D, dendrites; Tr, trichogen cell; To, tormogen cell. (Redrawn from 
Slifer et al., 1957.) 



tory nor always cord-like in appearance. In recognition of the 
universal existence of a peg-like rod within them, Eggers (1923, 1924, 
1928) proposed that they be called scolopophorous or scolopal organs. 
With this terminology one sensillum would be called a scolopidium 
(by analogy with the ommatidium of the eye) and a group of scolopidia 
comprising a unit would be termed a scoloparium. Even Eggers 
admitted, however, that other kinds of sensilla possessed peg-like 



22 THE PHYSIOLOGY OF INSECT SENSES 

rods, and it now appears that such structures are a constant feature of 
insect sensilla. In recognition of this fact Snodgrass (1926) originally 
preferred the term chordotonal in deference to custom ; however, he 
later (1935) switched to the term scolopophorous sensillum. Neither 




Fig. 15. Sensillum coeloconicum from the antenna of a grasshopper. N, 
bipolar neuron; S, scolopoid sheath; A, axons; D, dendrites; Tr, 
trichogen cell; To, tormogen cell; M, dried residue from moulting 
fluid. (Redrawn from Slifer et al, 1959.) 



term seems singularly appropriate, so the choice at the moment is a 
matter of taste (for a complete discussion of this matter see Eggers, 
1923, 1924, 1928; Snodgrass, 1926, 1935). 

A typical sensillum consists of a minimum of four cells (Fig. 16): 
(1) the trichogen or hair-forming cell; (2) the tormogen or socket- 




B 
Fig. 16. A. Tactile hair from the larvae of Vanessa urticae. B. Scolopoid 
body in the tactile hair of the larva of Fieri s rapae. S, scolopoid sheath; 
Sb, scolopoid peg; D, dendrite; N, bipolar neuron; A, axon; Tr, 
trichogen cell ; To, tormogen cell. (Redrawn from Hsii, 1 938.) 
C 



24 THE PHYSIOLOGY OF INSECT SENSES 

forming cell; (3) the bipolar neuron; (4) the reniform neurilemma cell 
(Haffer, 1921; Wigglesworth, 1933; Hsu, 1938). This group of cells 
may be surrounded on all sides by the epithelium of the integument 
or may lie sunken in a subepidermal position. In any case, the base- 
ment membrane of the cells is continuous with the basement 
membrane of the epidermis, so that the whole unit is walled off from 
the body cavity except where the neuron enters. 

The different types of sensilla depart from this general picture in 
details, and considerable variation exists among any single type from 
one insect to another or from one part of an insect to another. The 
most significant variations occur with respect to the number of 
neurons and their relations with other parts of the sensillum. The 
number of neurons associated with a sensillum may range from one 
to more than fifty (Fig. 13) (Slifer, Prestage, and Beams, 1959). The 
distal process, or dendrite, of the neuron may terminate at the 
base of a seta or extend variable distances up the shaft. The exact 
relations between the dendrites of the neurons and the cuticular 
portions of the sensillum is imperfectly known despite extensive 
studies (Snodgrass, 1926; Hsli, 1938; Vogel, 1923; Sihler, 1924; 
Eggers, 1928; Debauche, 1935; Slifer, 1961). In almost all cases the 
dendrite enters a sheath (not of neural origin) whose optical and 
staining properties resemble in many respects that of cuticle. The 
sheath, best described as a cuticula-like tube, has been variously 
termed sense rod, scolopale, Stift, Stiftkorperchen, corps scolopoid, 
Hiille, Chitineurium, etc. The exact relation of the dendrite to this 
tube differs in the various sensilla. In chemoreceptors especially the 
top (distal) end of the tube may open to the shaft of the hair or peg 
so that the dendrites can extend the length of the tube and into the 
lumen of the external process (Fig. 14). Or it may open to the outside, 
in which case the dendrites pass through openings in the side of the 
tube and continue in the lumen of the hair or peg (Fig. 13). 

In many mechanoreceptors the top of the tube is capped with 
a dark-staining apical body. In some cases the dendrite terminates 
within or just beneath this cap. This is the case with many tactile hairs 
(Fig. 16) and campaniform sensilla (Figs. 9, 10, 30) and with most 
chordotonal sensilla (Figs. 12, 48). In some cases, especially in 
chordotonal organs, a long filament may extend from the cap to the 
cuticle (Fig. 12). There are, however, chordotonal organs in which the 
terminal filament is absent (Figs. 47, 48). 

Recent studies with the electron-microscope (Gray and Pumphrey, 
1958; Gray, 1960; Slifer, 1961; Adams, 1961; Larsen, 1962; Dethier, 



GENERAL CHARACTERISTICS OF THE SENSORY SYSTEM 25 

Larsen, and Adams, 1963) have revealed a most extraordinary 
complexity in the structure of the dendrites and scolopoid bodies of 
sensilla. Since details appear to differ so much from one sensillum to 
another, specific cases will be dealt with in later chapters. 

While certain generalizations can be made about the function of 
some types of sensilla (e.g., sensilla campaniformia are mcchano- 
receptors sensitive to deformation of the cuticle, and chordotonal 
sensilla are mechanoreceptors sensitive to sound, vibration, and 
stretching of parts of the body), it is dangerous as well as unprofitable 
to attempt to link a particular structure with a particular function. 
This is so because a type of sensillum which may subserve one function 
in one species may subserve a different function in another. Further- 
more, a single sensillum may consist of more than one type of receptor 
(e.g., the labellar hairs of Phormia, which have two chemoreceptors 
and a mechanoreceptor associated with them). Each is a case unto 
itself. 



CHAPTER III 



Mechanoreception 



Every insect maintains its body in a particular attitude with respect to 
gravity. This attitude, its primary orientation, means for most 
ventral-side down. There are, however, many that habitually live 
upside down (the backswimmers, praying mantids, many lepi- 
dopterous larvae) and a few, such as those living in vertical burrows, 
whose normal attitude is posterior-end down. For aquatic insects 
and flying insects, both of whom are freely suspended in a homo- 
geneous medium, there must be sense organs that can give information 
about the direction of the force of gravity. Vision is of some help in 
this connexion, especially in flying insects, since the sky is invariably 
up and the ground down, but that is not the prime service of vision. 
Insects in contact with a substrate derive some information from 
sense organs touching the substrate, but this information tells them 
only which surface of the body is in contact, not what the attitude of 
their body is with respect to gravity. 

In addition to maintaining a primary orientation all insects have 
characteristic postural relations. To maintain these, to have infor- 
mation concerning the position of one part of the body with respect to 
another, requires special sense organs. The same sort of information is 
needed to be able to move one part of the articulated body precisely 
with respect to another in order to walk, swim, fly, spin cocoons, dig 
burrows, court, copulate, and feed. Finally, for the proper working of 
the internal organs there must be information concerning the presence 
of faeces in the rectum, eggs in the ootheca, and food in the alimentary 
canal. 

Serving all of these needs is a whole spectrum of sense organs 
responding to energy derived, in the final analysis, from the surface 
gravitation of the earth. They are organs sensitive to stretch, com- 
pression, or torque imparted to cuticle, connective tissue, or muscles 
by the weight (which is a measure of the force with which the earth 
attracts it) of parts of the body, the relative movement of parts, the 
gyroscopic effects of moving parts, and impingement of the substrate 
or surrounding media. Since there is no neuron directly sensitive to 
gravitational force, all of the receptors concerned with primary 

26 



MECHANORECEPTION 27 

orientation, postural relations, and touch are associated with compli- 
cated and highly specific accessory structures whose function is to 
transduce the energy of the stimulus into mechanical deformation of 
the protoplasm of the neuron. Many cells are sensitive to mechanical 
deformation, but the mechanoreceptors are highly specialized in this 
respect. The different accessory structures and the different response 
characteristics (e.g., rate of adaptation) of the receptor determine the 
sensitivity of the sense organ and to which parameter of the stimulus 
it will respond. 

THE TACTILE SENSE-SENSILLA TRICHODEA 

A non-living, tough, and most often rigid cuticle effectively insulates 
tissues from all but the grossest mechanical disturbances of the 
external environment. To provide the surface sensitivity denied by the 
exocuticle there are numerous thin, hollow extensions, the sensilla 
trichodea, on all surfaces of the body. They are most numerous on 
those areas, such as legs, which come most frequently into contact 
with the substrate, those, such as the antennae and mouth-parts, which 
are employed in palpating or manipulating the environment, and on 
such extended portions of the body as the antennae and cerci which 
represent perimeter guards of the body. They also occur abundantly 
on surfaces between joints, segments, and other appressed areas of the 
body where their function is proprioceptive. Their shape, mechanical 
properties, and the physiological properties of the neurons associated 
with them vary considerably, depending upon the service they are 
designed to perform. Those at the joints are short and slow adapting; 
those on the cerci, extraordinarily long and delicate, and hence 
sensitive to the most gossamer disturbance ; the thick tibial leg spines, 
gross and slow adapting. 

The sensilla trichodea are set in membraneous sockets. The shaft is 
so rigidly constructed that any force appUed to the structure is trans- 
mitted to the socket. It is here that movement takes place and, because 
of the leverage, is greatly ampHfied. The simplest sensilla trichodea are 
those that are innervated by one neuron. These are simple mechano- 
receptors. There are others, however, that are innervated by more 
than one neuron, and these are compound sense organs. In the labellar 
hairs of the blowfly, for example, one neuron is the mechanoreceptor 
responding when the hair is moved in its socket ; the remaining neurons 
are chemoreceptors responding when certain chemicals touch the tip 
of the hair (cf. Chapter V). 

The exact manner in which the dendrite of the neuron is associated 



28 THE PHYSIOLOGY OF INSECT SENSES 

with mechanoreceptive hairs is not always clear (Fig. 16). It is reported 
as being inserted on that part of the hair shaft that extends below the 
socket, on the socket itself, or at some point part way up the shaft of the 
hair. It is enclosed in a scolopoid sheath, but may or may not be 
capped with an apical body. The sheath may be ribbed and possess 
hickened zones. Just below the cap may be seen with the light micro- 
scope some darkly staining spots, the sense rods (Snodgrass, 1926) or 
points sensoriels (Hsu, 1938). Further observation with the electron- 
microscope may reveal more complicated structural relationships 
similar to those seen in tympanal chordotonal sensilla (Gray, 1960). 

Richard (1952) showed clearly in the case of sensilla trichodea of 
termites that at moulting the sheath and the neuron process extending 



.«''sw>'»«*».^n«<JujW 



1.0 
MV 



1 1 



MMMiffMMI 



Fig. 17. Response to repetitive mechanical stimulation of a chemosensory 
hair on the wing ofSarcophaga. The arrow indicates the onset of a rapid 
one-directional displacement, and the direction of the displacement 
with reference to the preceding stimulus. Positive potential at recording 
electrode is down. Time marks recur at 0-2-second intervals. (Courtesy 
of M. L. Wolbarsht.) 

through and beyond it are lost. A new sheath and filament are regener- 
ated to supply the new hair. During the period when the new cuticle is 
forming the distal fibre remains attached to the old hair to provide 
tactile sensitivity until the last moment. Shortly before the moult the 
distal fibre ruptures, and at this time there is a loss in tactile sensitivity 
(Richard, 1952; Wiggles worth, 1953). 

From the geometry of these sensilla it is likely that bending of the 
hair in its socket deforms the terminal region of the distal process of 
the neuron. The response to angular deflexion varies with direction 
relative to the long axis of the joint (Pumphrey, 1936; Pringle, 1938 a). 
Stimulation is followed by an electrical response that can be divided 
into two components. The work of Wolbarsht (1960) has shown that 
there is a graded slow potential, the receptor potential, that can be 
recorded from the distal process. It occurs prior to any impulses, varies 



MECHANORECEPTION 29 

smoothly, and must attain some critical level before any impulses are 
initiated. 

All hairs have a steady resting potential until a mechanical stimulus 
is applied. The potential may be either positive or negative, depending 
upon the type of hair. When the hair is stimulated an increase in 
negativity, which varies smoothly as the stimulus is increased or 
decreased, is seen at the recording electrode. Two types of receptor 
potentials have been observed. In one kind of hair the potential per- 
sists only during the motion of the hair (Fig. 17); in another kind, it 
lasts as long as the hair is deformed (Fig. 18). In the former the return 
of the hair to the unstrained position initiates another receptor 



-wi^/^^^wftifmri^^ 





Fig. 18. Response of mechanosensory hair on outer clasper of male 
Phormia to mechanical stimuli. A, B, and C are successive records taken 
from the same hair, but the stimuli were not the same. Arrows indicate 
onset and cessation of deformation. The deformation of the hair was 
approximately proportional to the amplitude of the response for each 
record. Positive at recording electrode is down. Time marks recur at 
0-2-second intervals. (Courtesy of M. L. Wolbarsht.) 



potential. This kind of hair adapts very rapidly. The other type adapts 
very slowly. Sometimes adaptation is still incomplete at the end of 
twenty minutes. 

The impulses always have an initial positive phase in contrast to the 
negative-going receptor potential. They are usually monophasic. 
Impulses occur only after some threshold of receptor potential has 
been reached. The threshold receptor potential for two types of fast- 
adapting hairs which is accompanied by an impulse is plotted for a 
series of test stimuli in Figs. 19 and 20. There is also a relation between 
the frequency of discharge and the magnitude of the receptor potential. 
Bernhard, Granit, and Skogland (1942) had shown that frequency was 
determined by the refractory period of the spike-generating mech- 
anism and the magnitude of the generator potential. Up to the point 
where the increase in generator potential causes no further increase in 



30 THE PHYSIOLOGY OF INSECT SENSES 

frequency because the interval between impulses is equal to the re- 
fractory period of the neuron there is a direct relation between fre- 
quency and the amplitude of the generator potential. These relations 
hold for the insect mechanoreceptor (Figs. 21, 22). 

The most striking feature of insect mechanoreceptors is the change 
in size of the impulse as the receptor potential changes (Figs. 23, 24, 



o 
o 

o 



Threshold Receptor Potential for Appearance of impulses MV 

Fig. 19. The threshold receptor potential of a mechanoreceptor on the 
grasshopper claw which is accompanied by an impulse is plotted for a 
series of test stimuli. In the largest number of trials the threshold was 
2-5 MV with the spread as shown. (Redrawn from Wolbarsht, 1960.) 



25) (Wolbarsht and Dethier, 1958; Wolbarsht, 1960). Wolbarsht 
(1960), after analysing the electrical events occurring in the mechano- 
receptor, concluded that: the mechanical stimulus effects a change 
in the membrane resistance at the receptor site; the receptor potential 
(which is undoubtedly the generator potential) is the difference 
between the potential across the membrane at the receptor site and the 
general polarization of the cell; the impulses are generated proximad 







MECHANORECEPTION 












31 


30 


— 






to 












C 20 


._ 










O 












-ij 












<XJ 












c- 
















<u 
















-Q 
















O 
















«-*- 
















o 
















1^ 
















a> 
















_o w 


'~~ 














E 
























3 
























^ 


1 1 i 1 

































Threshold Receptor Potential for Appearance of Impulses Ml/ 

Fig. 20. The threshold receptor potential of the mechanosensory neuron of 
a chemosensory hair on the wing of Sarcophaga which is accompanied 
by an impulse is plotted for a series of mechanical stimuli. In the 
largest number of trials the threshold was 0-38 MV with the spread as 
shown. (Redrawn from Wolbarsht, 1960.) 

of the receptor site and do not invade it ; changes in impulse size are due 
to changes in the membrane resistance of the receptor site ; there is a 
high resistance between the fluid-filled centre of the hair and the 
general body fluid ; the value of this resistance is effectively determined 
by the close anatomical conjunction of the receptor membrane and 
the lumen of the hair cavity. In most respects the electrical response of 
the insect mechanoreceptor is similar to that of the Pacinian corpuscle 
of vertebrates. 



-r* 



_U^ 



f{rm'^''f^^rfmrf0m^^, 



t 



^tf^. 



O^^'^^f^v* 



10 
MV 



Fig. 21. Response of mechanosensory hair on the anal plate of a female 
Pliormia to changing mechanical stimulation. The left-hand arrow 
indicates the approximate beginning of the deformation; the middle 
arrow, the minimum; and the right-hand arrow, the return to the 
undeformed position. Positive at the recording electrode is down. 
Time marks recur at 0-2-second intervals. (Courtesy of M. L. 
Wolbarsht.) 



32 THE PHYSIOLOGY OF INSECT SENSES 

While it is convenient to speak of all sensilla trichodea as a class of 
sensilla responding to deflexion, the variations in structure, hence in 
physiological characteristics, impart to the different ones quite 
different functions in the economy of the insect. One of the salient 
differences encountered is the rate of adaptation. Generally, the 
smaller, more delicate hairs adapt rapidly during prolonged deflexion 
while the stouter spines adapt more slowly and incompletely. The 
nature of the process is still unclear. 



160 


— 


















140 


- 
















• 


120 


— 


















oioo 


- 














• 


, 


■-60 














• 


















• 








60 


— 




• 


• 


• 










40 


~" 


• 
















n 




1 




1 






1 


1 


1 



6 

Receptor Potential MV 



Fig. 22. Receptor potential amplitude plotted against frequency of 
impulses for a mechanosensory hair on the anal plate of a female 
Phormia. Each point is the average of 2 seconds. (Redrawn from 
Wolbarsht, 1960.) 



Evidence has been presented to show that the generation of impulses 
follows depolarization of the neuron membrane. The rate of adapta- 
tion appears to be closely related to the rate of decay of the depolariz- 
ation. The generator potential of the rapidly adapting Pacinian 
corpuscle of the cat (Alvarez-Buylla and de Arellano, 1953 ; Gray and 
Sato, 1953), the fast adaptory crustacean muscle receptor (Eyzaguirre 
and Kuffler, 1955), and the sensory hairs on the wings of flies (Fig. 17) 
(Wolbarsht, 1960) fall rapidly below threshold. The slowly adapting 
frog-muscle spindle (Katz, 1950), the slow muscle receptor of Crust- 



MECHANORECEPTION 



33 



— 6 



—6 



O"— 2 



TlH 



^ nl— ?U- 



c • 



}5 



T 



• 1.} 






B« - • 5 



T O 



.?' 



I 



A • 



Receptor Potential M V 

Fig. 23. Impulse size plotted against receptor potential for a mechano- 
sensory hair on the outer clasper of a male Phormia. Points are average 
values; bars denote extreme values. (Redrawn from Wolbarsht, 1960.) 

acea, and the mechanosensory hair on the claspers of male flies 
(Fig. 18) (Wolbarsht, 1960) exhibit slow potentials that are main- 
tained above threshold for a considerable period of time. It has been 
assumed, at least in some cases, that depolarization is a consequence 
of the unfolding of the cell membrane (Katz, 1950; Gray and Sato, 
1953). Lowenstein (1956) has suggested that the degree to which the 



34 THE PHYSIOLOGY OF INSECT SENSES 

membrane can unfold imparts a mechanical component to adap- 
tation. As he pointed out, this concept, while not explaining rates of 
adaptation, brings it to another level of understanding. 
All types of mechano -hairs studied (Wolbarsht and Dethier, 1958; 






7 — 



• } ■• 



Receptor Potential M V 

Fig. 24. Impulse size plotted against receptor potential for a mechano- 
sensory hair on the second antennal joint of Melanopliis. All points 
except lowest receptor potential are averages of at least twenty impulses. 
Lowest value is a single impulse. Bars denote extreme values. (Redrawn 
from Wolbarsht, 1960.) 



Wolbarsht, 1960; Pumphrey, 1936) appear to fall into two classes: 
velocity sensitive and pressure sensitive. The former fire only while the 
stimulus is changing. Some, such as the hairs on the leading edge of the 
wings of flies and other insects (Wolbarsht and Dethier, 1958), may 
fire at a rate of 600 or more impulses per second. Pressure-sensitive 
hairs show a repetitive discharge during a static deformation. 



MECHANORECEPTION 35 

Tactile receptors are usually of the velocity-sensitive type and are 
most common on those portions of the body that encounter the en- 
vironment as the animal progresses or on those appendages with which 
the animal explores its environment. Pressure-sensitive receptors are 




.hf^H^^^*^^llk0iifm0^F^'^i ( I i ! 1 1 I 1 I 



M 



4.0 
MV 



I 



i4iYiTfrrf^T>^^ 



Fig. 25. Response of a mechanosensory hair on the second antennal joint 
of Melanoplus to increasing mechanical stimulation. Approximate 
onset of stimulation is indicated by arrow. The stimulus continues until 
the end of the record. A and B are responses to successive stimuli of 
approximately the same size. Positive at the recording electrode is 
down. Time marks recur at 0-2-second intervals. (Courtesy of M. L. 
Wolbarsht.) 

most common on those areas where positioning is important. They are 
found, for example, in the genital regions and between joints. They 
are proprioceptors. 

PROPRIOCEPTORS 

Proprioceptors may be defined as sense organs capable of continuous 
response to deformations (changes in length) and stresses (tensions 
and compressions) in the body (Lissmann, 1950). They provide some 
of the information necessary for the animal to maintain certain re- 
lations of one part of the body with another and of the body as a whole 
with respect to gravity. In this capacity they are assisted by other recep- 
tors, as photo- and tactile receptors, for example, whose primary 
function may lie in another realm. In other words, the insect maintains 
position by assessing much information from a multitude of receptors. 



36 THE PHYSIOLOGY OF INSECT SENSES 

Five kinds of sensory structures are known to take direct part in 
proprioception: hair plates, campaniform sensilla, stretch receptors, 
chordotonal organs, and statocyst-like organs. 

Hair Plates (Position Receptors) 

Concentrations of minute sensilla trichodea similar in general 
structure to tactile hairs were first described by Lowne (1890) on the 
anterior part of the thorax of the blowfly (Fig. 26). Similar structures, 
termed hairplates by Pringle (1938 c), are distributed in the joints of the 
legs and palpi of cockroaches (Fig. 27). Others occur in the dragonfly 
and mantis (Fig. 27) (Mittelstaedt, 1950, 1952, 1957) and in the honey- 




FiG. 26. The prosternal organ of Calliphora. B, basal part of head; C, neck 
sclerite; Co, connecting membrane; N, nerve; P, prothorax. (Redrawn 
from Lowne, 1890.) 

bee (Lindauer and Nedel, 1959). Single hairs of varying size and shape 
were found in the body articulations of the cockroach by Diakonoff 
(1936). Hair plates are undoubtedly a common feature among insects. 
In all cases the sensilla are stimulated by folds of the intersegmental 
membrane or contact with adjoining surfaces as the joints are moved. 

The hair plates of the cockroach have been studied in some detail 
(Markl, 1962; Peters, 1962). The discharge of these receptors is 
proportional to the degree of bending of the hairs as the joint is 
flexed. The initial frequency may be 800 or more per second (Fig. 
29). The rate of adaptation is very slow. Thus, the hair plates act as 
'position' organs and behave independently of muscular tension. 

The proprioceptive function of hair plates is strikingly illustrated 
by Mittelstaedt's (1952, 1957) analysis of prey capture by mantids. 
Successful prey capture is a problem of absolute optic localization. 



MECHANORECEPTION 37 

Mantids lying in ambush detect tlieir prey visually. The eyes being 
immovable, the head is turned so that the prey is always faced. 
Although the mantis may then turn its body to line it up with the prey, 
it can capture a prey which sits at a considerable lateral deviation 
from the median plane of the thorax. If the prey is close enough it is 
seized by a rapid (10-30 milliseconds) stroke of the prothoracic legs. 
The accuracy of hitting in normal mantids is about 85 per cent. Since 





Fig. 27. A. Proprioceptors of the neck region of the mantis. S, sterno- 
cervical hair plate; N, tergocervical plate. (Redrawn from Mittel- 
staedt, 1957.) B. Proprioceptors of the second leg of Periplaneta. 
C, coxa; I, inner coxal hair plate; O, outer coxal hair plate; T, troch- 
anteral hair plate. (Redrawn from Pringle, 1 938 c.) 



the speed of the stroke is so great, its direction is not controlled by 
watching the difference between its direction and that of the prey. Its 
direction is predetermined by information concerning the position of 
the prey relative to the plane of the prothorax. Thus, the message 
steering the stroke must contain information about the direction of the 
prey relative to the head and of the position of the head relative to the 
prothorax. The first information is provided by the compound eyes ; 
the second, by hair plates in the neck region. Two pairs of plates are 
involved ; the sternocervical plate (Pringle, 1938 c) and the tergocervical 



38 THE PHYSIOLOGY OF INSECT SENSES 

plate (Mittelstaedt, 1952) (Fig. 27). The role of these sensory systems 
was demonstrated by the following series of experiments. If the inner- 
vation from all hair plates is cut so that no information is forthcoming 
from these organs the accuracy of hitting drops to 20-30 per cent. 
With deafferentation of the left side only, missing increases, and there 
is a tendency to strike to the right. In other words, proprioceptive 
information coming only from the right misleads the animal into 
believing that its head is turned to the right whereas it is not. If the 
head is held in a fixed position relative to the prothorax by a balsa- 




FiG. 28. Ventral view of the campaniform sensilla in the trochanteral region 
of the third right leg of Pe rip lane ta. C, coxo-trochanteral condyle; 
E, extensor trochanteris and its accessory apodemes ; F, flexor troch- 
anteris; H, trochantero-femoral hinge joint; 2, 3, 4, groups of campani- 
form sensilla. (Redrawn from Pringle, 1938c.) 

wood bridge so that the neck region is not touched accuracy of hitting 
decreases to 25 per cent if the head deviates from the body axis by 
10-30 degrees. The prey is missed to the left if the head has been turned 
to the right, and vice versa. 

If head fastening and unilateral extirpation of proprioceptors are 
combined the effects of both are superimposed, the loss of one-half of 
the neck receptors being equivalent to a deviation of the head of less 
than 20 degrees. If the free head is loaded with an extraneous force 
performance remains normal until the load surpasses twice the head 
weight at twice its diameter. In short, direction of stroke depends on 
feedback processes which control the position of the head. Fixation 
movements of the head are steered by the difference between the 
optic-centre message (a function of the angle between prey and 



MECHANORECEPTION 



39 



700- 



500 



400 



c 
o 

a. 

C 300 
U; 200 



100 



\«. • " • ' 

♦ -•— • • — « . 



5 6 

Seconds 
A 




B 

Fig. 29. A. Adaptation of a nerve-ending in the inner coxal hair plate of 
Periplaneta to a stimulus of a constant deflexion of the hairs. Two 
records from the same preparation. B. Diagram to illustrate the 
method of excitation of the inner coxal hair plate by a fold of the inter- 
segmental membrane. C, coxa; H, hair plate; P, pleuron. (Redrawn 
from Pringle, 1938c.) 

fixation-line) and the proprioceptive-centre message (a function of 
the angle of the head with respect to the body axis). If fixation move- 
ments have come to rest the direction of stroke is determined by the 
optic and, to a lesser extent, by the proprioceptive-centre messages, 
which then both contain the required information (Mittelstaedt, 
1957). 

D 



40 



THE PHYSIOLOGY OF INSECT SENSES 



Campaniform Sensilla (Compression and Stretch Receptors) 

The term sensilla campaniformia was proposed by Berlese (1909) to 
apply to all sensilla similar to those originally described by Hicks 
(1857). These organs consist of a canal in the cuticle covered by a 
domed cap and innervated by a single bipolar neuron (Fig. 11, 30) 
(Newton, 1931; Vogel, 1911; Sihler, 1924; Pflugstaedt, 1912; 
Mclndoo, 1914 a, 1914 b ; Snodgrass, 1935 ; Hsu, 1938 ; Slifer, Prestage, 
and Beams, 1959). The cap is lined with a substance that has different 
staining properties from the rest of the cuticle. The dome may extend 
above the general cuticular surface, be flush with it, or be recessed. The 
distal neuronal process extends within the scolopoid sheath (Slifer 




Fig. 30. Structure of the cuticular parts of various types of campaniform 
sensilla. A, outer lamella of dome; B, inner lamella of dome; C, cuti- 
cular connexion of dendrite of sense cell. (Redrawn from Snodgrass, 
1935.) 



et al, 1959) and is inserted on the underside of the cap by a highly 
refractile body. 

These sensilla occur on practically all parts of the body. One of the 
earliest suggestions that they are proprioceptive organs came from 
Demoll (191 7), many of whose speculations concerning the mechanism 
of action were given substance by the work of Pringle (1938 b). It is 
interesting that there is no known case of these sensilla occurring on a 
part of the cuticle free from strain. They are concentrated especially 
where stresses are set up by muscular contractions (e.g., leg, wing, 
haltere, ovipositor, and mandibular joints). A model has been 
constructed by Pringle (1938 b) to explain their probable action 
(Fig. 31). 

A thin, flat surface such as the cuticle can be subjected to bending 



MECHANORECEPTION 41 

by forces at right angles to its plane or shearing in its plane, as illus- 
trated by a sheet of rubber stretched over a rectangular frame (Fig. 3 1 ). 
When the surface is distorted by changing the rectangle to a parallel- 
ogram there is tension in the direction AC and compression in the 
direction BD. 

Any force applied to a hollow cylinder sets up shearing forces (see 
Fig. 31). This is the situation as it occurs in a homogeneous surface to 
which forces are applied evenly. Insect limbs do not conform to this 
ideal, but, as Pringle pointed out, the important point is that on a 
hollow structure such as the insect exoskeleton all stresses can be ex- 







FiG. 31. Diagram to illustrate the resolution of shear forces into com- 
pression and extension components. A, a flat surface; B and C, a 
hollow cylinder subjected to twist and bend. Continuous lines, ex- 
tension. Broken lines, compression. D, model representing actual 
sensillum; E, model constructed in a circular framework for measure- 
ment of the effect of compression in different directions. (Redrawn 
from Pringle, 1938 b.) 

pressed as shearing, which can be resolved into compression and 
extension components. 

Based upon these ideas, the probable mode of action of a campani- 
form sensillum can be explained in terms of a second model (Fig. 31). 
In a sheet of rubber stretched over a frame a circular or oval hole 
corresponding to the cuticular canal of the sensillum is cut. A domed 
strip of paper is fastened across the long diameter of the oval aperture. 
This corresponds to the longitudinal thickening frequently seen in the 
dome of the sensillum where the nerve fibre is attached. The rest of 
the cap, assumed to be more elastic, is omitted from the model. The 
assumption of differential elasticity of the two parts is essential to the 
theory. 

Distortion of the model from the rectangular shape causes the hole 



42 



THE PHYSIOLOGY OF INSECT SENSES 




150 



50 92 100 

Resistance (arbitrary units) 

Fig. 32. Graph obtained from the model in Fig. 3 IE showing the relation 
between the angle of the applied compression force and the resistance 
of the electrolytic cell for various values of the compression force. 
(Redrawn from Pringle, 1938 b.) 

to be lengthened in one direction and shortened in another. As a result 
of this action, the paper strip humps up in the middle. If the end of the 
neuron is imagined as being inserted on the underside of the middle of 
the strip it will be stretched by movement in one direction and com- 
pressed by that in the other. The magnification of movement is very 
large. 
In order to provide some measurement of the force involved, 



MECHANORECEPTION 43 

Pringle constructed another model in which there were two strips of 
paper, one on each surface (Fig. 31). The movement measured 
between the two and the relation between the angle of the applied 
compression force and the resistance of the detecting electrolytic cell 
is shown in Fig. 32. 

If it be assumed excitation occurs only with increased doming, then 
the neuron will be excited when the compression component of the 
shear force makes an angle of less than a certain critical value with the 












^^f ..fl^ 






/i) 



<tBB^ 









Fig. 33. Details of the orientation of the groups of campaniform sensilla on 
the third leg oiPeriplaneta. (Redrawn from Pringle, 1938 b.) 

direction of thickening of the cap membrane. The sensitivity of the 
sensillum will depend, among other things, on the absolute length of 
the long diameter of the cap. Sensilla with parallel orientation will 
respond to the same type of shear force. Each group will act as a unit 
and, if innervated from the same fibre, will extend the range of these 
fibres quantitatively but not quaHtatively (Fig. 33). This condition 
occurs in the sensilla of the palps (Pringle, 1957). 

Although there is yet no direct evidence that the sensillum has 
undirectional sensitivity, considerable circumstantial evidence sup- 
ports the idea. In many instances groups of sensilla are orientated in 
the same direction. The sensilla on the tarsus have their long diameters 



44 THE PHYSIOLOGY OF INSECT SENSES 

parallel to the length of the leg (similarly in the palps) and when the 
tarsus is pressed against the ground the compression lines in the cuticle 
of the upper surface, where these sensilla are located, will also be 
longitudinal. It must be the compression component which is effective. 
Electrical recordings have shown clearly that these sensilla are most 
sensitive to pressure on the cuticle (Pringle, 1938 b). Adaptation is 
slow and incomplete. 

Stretch Receptors 

Certain of the Type II receptors for which no function had been known 
have recently been shown by Finlayson and Lowenstein (1955, 1958) 




Fig. 34. Stretch receptor in the right side of the fourth abdominal segment 
of Periplaneta. The broken lines indicate the posterior ends of the 
fourth and fifth muscle bands, counting from the dorsal mid-line. 
(Redrawn from Finlayson and Lowenstein, 1958.) 



to be stretch receptors analogous to the stretch receptors of Crustacea 
discovered by Alexandrowicz (1951, 1952 a, 1952 b, 1954, 1956) and to 
the muscle spindles of vertebrates. Firstdescribedby Zawarzin(1912 a) 
and Rogosina (1928) in dragonfly larvae, they have now been found in 



MECHANORECEPTION 45 

Orthoptera, Hymenoptera, and Lepidoptera by Slifer and Finlayson 
(1956) and Finlayson and Lowenstein (1955, 1958). 

Three types of stretch receptors are known : those associated with 
connective tissue, those associated with muscle, and those consisting 
of a specialized muscle fibre. They are represented by receptors in 
dragonfly larvae, bees, and cockroaches, by those in Orthoptera, and 
by those in moths respectively. 

Each connective tissue receptor is a multipolar neuron embedded in 
a strand of connective tissue which stretches either from an inter- 




FiG. 35. Right half of the sixth abdominal segment of a full-grown larva of 
Aeschna juncea with various muscles cut to reveal the three stretch 
receptors. Dva, dorso-ventral anterior muscle; Dvm, dorso-ventral 
median muscle; Dvp, dorso-ventral posterior muscle; Sx, sextic 
longitudinal tergal muscle; Obi, oblique receptor; Lo, longitudinal 
receptor; Ve, vertical receptor. (Redrawn from Finlayson and 
Lowenstein, 1958.) 

segmental fold or from a nerve to a point on the body wall (Fig. 34). 
In the cockroach Periplaneta americana a pair has been found in the 
dorsal region of abdominal segments two to seven. In dragonfly larvae 
{Aeschna juncea) three pairs of receptors have been found in each 
abdominal segment one to eight (Fig. 35). In the honeybee there is a 
pleural pair in each abdominal segment three to six. In all cases the 
neuron is encapsulated in connective tissue. The capsule is multi- 
nucleated. Detailed studies with light- and electron microscopy of 
the abdominal stretch receptor of the cockroach Blaberus (Osborne 
and Finlayson, 1962; Osborne, 1963) have shown that the terminal 



46 THE PHYSIOLOGY OF INSECT SENSES 

regions of the dendrites are naked, that is, not invested by Schwann 
cells, and embedded in the connective tissue matrix. There are no 
connexions with the collagen-like connective tissue fibrils. They 
resemble very closely the sensory terminations of the vertebrate 
muscle spindle and Pacinian corpuscle. 

In Orthoptern (Acrididae) a pair of muscle receptor organs is present 
in each of abdominal segments one to ten in the region of the mid- 
dorsal line. The receptor organ is usually attached to the medial edge 
of one of the longitudinal muscle bands, although it may be nearer the 




Fig. 36. Dorsal longitudinal muscles of the third and fourth abdominal 
segments of a pupa of Antheraea pernyi, with a part of the band in the 
fourth segment removed to show the receptor. Motor and sensory 
innervation of the receptor are shown. (Redrawn from Finlayson and 
Lowenstein, 1958.) 



middle. Each consists of a large multipolar neuron surrounded by a 
thick nucleated capsule and a modified muscle fibre. There are also 
many neurilemma cells. The muscle fibre originates near the anterior 
end of the segment, and is inserted on the anterior end of the following 
segment. The fibre possesses striations. Attached to it are numerous 
thick connective tissue fibres which also extend to adjacent muscle 
fibres. The axon of the receptor joins the ventral branch of each 
segmental tergal nerve. 

The most complex receptors are those in the larvae, pupae, and 
adults of Lepidoptera. In the larvae there is a pair in the meso- and 
meta-thorax and abdominal segments one to nine (Fig. 36). They are 



MECHANORECEPTION 47 

present in the abdominal segments of pupae and adults but have not 
been found in the thorax. The receptor consists of a multipolar re- 
ceptor cell, a modified muscle fibre, and motor innervation to the fibre 
(Fig. 37a). The neuron is enclosed in the usual connective-tissue sheath . 





Fig. 37. A. Diagram of the structure and innervation of a lepidopteran 
stretch receptor, based on a preparation from the right side of the fifth 
abdominal segment of a pupa of Antheraeapernyi. The receptor is short 
because no tension is applied. B. Diagram showing the relative sizes 
and positions of the two giant nuclei, the neuron sheath, and the fibre 
tract of a lepidopteran stretch receptor. (Redrawn from Finlayson and 
Lowenstein, 1958.) 

Its dendrites sometimes run on finger-like extensions of the sheath, 
which is continuous with a tubular sheath extending along the edge of 
the receptor (Fig. 37b). The muscle which constitutes the bulk of the 
receptor has fainter striations than normal muscles. At the centre there 
is a clear swelling with a giant nucleus (100-360 ijl). Adjacent to this 
is another large nucleus. This muscle has its own separate motor 



48 THE PHYSIOLOGY OF INSECT SENSES 

innervation. The resemblance of this receptor to the vertebrate muscle 
spindle is striking. Both have rich motor innervation, an absence of 
striations in the central region, and much nuclear material (nucleus in 
the insect; nuclear bag in the vertebrate). In Crustacea and other 
insects there is no giant nucleus, but there is, as already described, a 
richly nucleated sheath. 

Despite morphological differences, the mode of action of all of these 
receptors is nearly identical. Under minimum tension, a condition 




Time fsec.) 

Fig. 38. A series of curves showing the discharge frequencies from the 
stretch receptor of the larva of A. pemyi in response to stretch of 
different intensities plotted against time. Arrows indicate beginning and 
end of stretch. Figures below the curves denote the stretch in mm. The 
broken line indicates response to 'over-stretch'. (Redrawn from 
Finlayson and Lowenstein, 1958.) 



approaching the normal situation, the receptor discharges impulses at 
the rate of 5-10 a second. Under zero tension it is silent. The basal 
rate is maintained for hours. When the receptor is stretched there is a 
large increase in the frequency of discharge (Fig. 38). This drops very 
rapidly to a new level which is maintained for a long period. Upon 
release there is a post-stimulatory reduction in discharge. The rela- 
tively large drop in initial discharge is probably due both to neuronal 
adaptation and a mechanical accommodation to stretch. Over what 
may be judged a normal range of stretch there is a linear relation be- 
tween the intensity of stretch and the frequency of impulses (Fig. 39). 
Beyond a certain point this relationship breaks down, probably 



MECHANORECEPTION 49 

because of *over stretch', i.e., extension beyond the physiological 
range. The slowly adapting receptors clearly serve a static function. 

The corresponding organs in Crustacea possess two neurons, a 
*fast' and a *slow' one; that is, a phasic and a static receptor. It turned 
out when the insect organs were examined with phasic stimulation 
that the single neurons were in fact dual-purpose receptors (Lowen- 
stein and Finlayson, 1960). At rest the discharge activity is, within 
certain limits, a linear function of absolute length or total displace- 



so 



ii 40 



3 




mm. 



Fig. 39. Peak discharge frequencies plotted against intensity of stretch. 
A, larva of A. pernyi; b, longitudinal receptor of larva of A. juncea. 
(Redrawn from Finlayson and Lowenstein, 1958.) 

ment. With plastic alternation of stretch and relaxation the impulse 
activity is a combined function of displacement and velocity. At low 
stimulus frequencies the phase relation of maximum response is 
approximately constant, and maximum activity coincides with maxi- 
mum slope (= max velocity) (Fig. 40). Impulses begin to drop out as 
higher stimulus frequencies (1-5-5 c/s) occur (Fig. 41). Above 5 c/s 
the organ fails to signal phasic stimuli accurately, although the res- 
ponse is still in phase with the stimulus. Up to this point the stimulus- 
response relationship is linear (Fig. 42). 

This receptor is thus seen to respond to displacement at low stretch 
velocities, but from 3 to 4 c/s onward there is no response activity at 
maximum displacement and during relaxation. Lowenstein and Fin- 
layson (1960) were convinced that the decline of activity after the 
velocity peak of the stretch is passed is accentuated by post-excitatory 



50 



THE PHYSIOLOGY OF INSECT SENSES 



I f I I I ( I r ( c I I I r t f :i ( I c. ( r ( ( f r (. t. f I I I r f r rr r- t r.c r r 1- 1 r I t I I 1 I f I I i; r I I- 1 t., 

a'i,i| iiilillil li i i ilii i lllli lillll t lll l lll l|l l llill l ll| ll l ll l l l l ll i li i U' 

1 second i __ -»___^___-^________^__. 



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t (• III r I I r I ( I I (.1 I I. i'l I 'r ri '( t c t f c I c i. i i i"( i- c,- 1 l i c. c i i. ( ( r, l, u l t c r r c i; c'l. c l 

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r r I I r r r r (. I r. r. l r i rmTTTTTm"^rrT c f i r- r f r f i l- r r l r. c- r r t. r 




UiMllliilllllllilllilllllll 



t.t t I c 1 1 I < r I I I ( L 1 .1 r c t.i I r c C fe I t t 1^1 I I I ( I. f r ( i I I ( ( I, I ( ( I ^ I I ; I I 1 J ( i t 1 
•t^i^cTT r' I CI I I .f't I r t.i r. ui t.t i- 1- 1. i-.cL*cin*t t>f i r l i r i i i i i i i. i i i i i" i 1. 1 i i r i i i' 




I.I I « I I I I I I I I 



Fig. 40. Response to phasic stimulation during a continuous experiment 
with a range of frequencies of alternation between stretch and re- 
laxation, a, resting discharge ; b-e, frequency of stimulus and velocity 
of stretch respectively, 0-25 c/s, 4-3 mm./sec; 0-5 c/s, 7-3 mm./sec; 
1 -5 c/s, 22-2 mm./sec. ; 2 c/s, 33 -6 mm./sec. (Redrawn from Lowenstein 
and Finlayson, 1960.) 



il l W^'iV itl i V 'W ' l jl ' i 'i i' ' k 'iii Mi i i\ "i'i\" 




mAAAAAAAAAAAAAAAAAAA 

f) J ■. I .: J I 'i 1 1 1 .1 1 :) I- I I 1 I T 1 I I 1 1 1 1 I I I 1 1 1 1 1 ) I J J I I I o 1 i I 1 1 I 1 I 1 I 1 I 1 1 I I I 



<) J 1 I I .1 I I I 1 J .1 .1 J I .1 I 1 I I I I I ' I I I I 1 I 1 I I I J ] I I I 1 I I I I I I I I ) I I I .1 ) I I I I I I I I 

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H 1 J D 1 ■; J .1 J J :j > i J ! J J .) .1 J ) .) .1 J '1 .1 •.! .1 r J .1 .1 I.I II II I I I J I 1 I i r I I ) I ) I 1 II A I I 1 i' 




m^^^ w^.^^^ ■ » I p^^ ^fi^A^ y^^^^mmm^m^tf^^m 



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Fig. 41. Continuation of experiment in Fig. 40. a-e, 4 c/s, 67-2 mm./sec; 
5 c/s, 71 mm./sec; 15-5 c/s, 89 mm./sec; 18-5 c/s, 59 mm./sec; 
recordings of responses in a and b respectively at ten times speed. 
(Redrawn from Lowenstein and Finlayson, 1960.) 



MECHANORECEPTION 51 

inhibition. Thus, the gradual disappearance of response to displace- 
ment and the transition from a static to a dynamic response is related 
to the post-excitatory silencing. 

The range of accurate frequency monitoring is more than adequate 
to keep pace with such rhythmic activity as respiratory movements. In 
their static capacities these stretch receptors are able to provide 
information as to the relations of one part of the body with respect to 



3^100 



Q~- 



1 


1 


1 1 1 


1 lo y^ 1 








/ • o 




• / 


y^ * 






i 


1 1 


1 1 1 



2 



Stimulus Frequency cjs (•) 

Fig. 42. Stimulus-response relationship. Frequency of phasic stimulus 
(solid circles) (abscissa). Velocity of stretch (open circles) (abscissa). 
Impulse frequency (ordinate). (Redrawn from Lowenstein and 
Finlayson, 1960.) 

another. In the dragonfly larvae, for example, the three pairs of 
receptors are well adapted to supply information for analyses of body 
movements. As Fig. 43 illustrates for dragonfly larvae, the oblique 
receptor will be stretched during respiration (A) and relaxed during 
expiration (B). In longitudinal abdominal movement, as, for example, 
jet propulsion locomotion, the vertical and longitudinal receptors 
will act antagonistically. 



52 



THE PHYSIOLOGY OF INSECT SENSES 



Chordotonal Sensilla 

Cord-like sensilla devoid of a specialized exocuticular component 
and stretching from one point of the body wall or its derivatives to 
another are peculiar to insects and have been found in every species 
in which they have been sought (Siebold, 1844; Leydig, 1851 ; Graber, 
1882a, 1882b; Eggers, 1924, 1928; Snodgrass, 1926; Debaisieux, 




Fig. 43. Diagrams to illustrate probable alterations in tension of the three 
stretch receptors of Aeschna larvae. A (inspiration) and B (expiration) 
show the movements of the sternal and pleural regions of the body 
wall during ventilation. Upper figures, dorso-ventral muscles. Lower 
figure, oblique receptor of right side. The oblique receptor will be 
stretched during A and relaxed during B. C and D illustrate probable 
effects of longitudinal movement on longitudinal and vertical re- 
ceptors. (Redrawn from Finlayson and Lowenstein, 1958.) 



1935, 1938 ; Debauche, 1935; and others). They are widely distributed 
in the body. In all insects they occur in the appendages of the mouth 
and in the legs. They are universally present at the bases of the wings 
(Fig. 44) and halteres (Fig. 45) and in the antennae (Graber, 1882 a, 
1882 b; Schon, 1911; Vogel, 1912; Lehr, 1914; Eggers, 1928). They 
occur segmentally in the abdomen. In many species simple chordo- 
tonal organs are associated with the tracheal system (Demoll, 1917; 
Larsen, 1955). They are especially numerous in larval insects, where 
they stretch from one point on the body wall to another and criss- 



MECHANORECEPTION 



53 




^^^^^=^^^i^^=:.^-^^g^^ 




Fig. 44. A. Right wing oiEmpis. B. Enlarged viewof insectshowinglocation 
and orientation of campaniform sensilla. Ri, R2, R3, radial groups; 
Sci, Scg, Scg, subcostal groups with arrows indicating the orientation of 
the long axes of the sensilla. C. Right wing of Panorpa communis 
showing the location of chordotonal sensilla. 1, 2, 3, 4, ante-alar, 
radial, medial, and cubital sensilla respectively; Co, costa; Sc, sub- 
costa; R, radius; M, media; Cu, cubitus; A, anal. (Redrawn from 
Pringle, 1957 after Zacwilichowski.) 



54 THE PHYSIOLOGY OF INSECT SENSES 

cross in many directions (Fig. 49) (Graber, 1882 a, 1882 b; Radl, 
1905; Hess, 1917). 

Typically the sensilla are stretched between two undifferentiated 
points of the body wall by a ligament at the proximal (i.e., axonal) end 
and by the cap cell or accessory cells at the distal (dendritic) end. 
Consequently, the organs have the appearance of thin strands 
(Fig. 46) or sheets (Fig. 47). 




Cue 



Fig. 45. Dorsal view of the base of the left haltere of Tipula paludosa 
showing the location and orientation of the group of campaniform 
and chordotonal sensilla. Re, Cue, aac, radial cubital, and ante-alar 
chordotonal organs respectively; Ri, Rg, R3, Scg, radial and subcostal 
groups of campaniform sensilla with arrows indicating long axes of 
sensilla. (Redrawn from Pringle, 1957 after Zacwilichowski.) 

The structure of chordotonal sensilla is very complex and has yet 
given no clue as to their exact mode of action. Each sensillum consists 
of one bipolar neuron and a minimum of two companion cells which 
are probably homologous with the trichogen and tormogen of other 
sensilla (Schwabe, 1906; Schon, 1911 ; Vogel, 1912; Snodgrass, 1926; 
Eggers, 1928). The three cells are arranged in overlapping linear 
fashion. One, the enveloping cell, surrounds the proximal portion of 
the dendrite ; the other, the cap cell, surrounds the remaining length 



MECHANORECEPTION 55 

of the dendrite. As in the case of other sensilla, the dendrite of the 
neuron is enclosed terminally in a ribbed scolopoid sheath. This is 
invariably capped with a darkly staining, peg-shaped apical body 
(Fig. 48). In some instances there is a terminal strand extending from 
the apical body to the distal point of attachment of the sensillum. 

Although they were originally thought to be exclusively audio- 
receptors, it is now known that they are not organs of constant 
function. A proprioceptive function has been demonstrated for many. 




Fig. 46. Longitudinal vertical section of a 
pleural tubercle of Monohammus con- 
fusor showing a simple chordotonal 
organ. (Redrawn from Hess, 1917.) 



and it is likely that all not associated with tympanic membranes or 
grouped to form sub-genual and Johnston's organs (which have a 
mixed proprioceptive and exteroceptive function and in Culicidae and 
Chironomidae are auditory) will eventually be proved to be proprio- 
ceptive. Their association with skeletal articulations, tracheae, pulsa- 
tile organs, and blood cavities has led to hypotheses that they are con- 
cerned with position, passive body movements, active muscle move- 
ments, blood pressure, tracheal air pressure, and vibrations (Radl, 
1905; Demoll, 1917; Hertwick, 1931; Debaisieux, 1938). It can 
actually be seen by direct observation in many cases that the organs 
change in length as the insect moves (Radl, 1905; Larsen, 1955). 

E 



56 THE PHYSIOLOGY OF INSECT SENSES 

Proprioceptive chordotonal organs are usually much simpler than 
those concerned with sound reception, although there are some note- 
worthy exceptions (e.g., the tympanic organ of noctuid moths). 
Whereas the auditory organs may consist of tens to thousands of 
chordotonal sensilla, organs subserving a proprioceptive function 
consist of very few sensilla, sometimes only one. 




Fig. 47. Subgenual organ of Formica sangidnea. A, accessory cell ; C, cap 
cell ; E, enveloping cell ; S, sense cell ; N, nerve. (Redrawn from Schon, 
1911.) 



In the water bug Aphelocheirus, Larsen (1955) discovered a single 
chordotonal sensillum attached to each of the large tracheal sacs of 
adults and larvae. He suggested that the sensilla are concerned with 
respiratory behaviour. When air pressure within the animal falls, as it 
does according to Larsen, and when an animal in poorly oxygenated 
water has used up its air supply, there is a decrease in the volume of the 
air sacs. The decrease triggers the chordotonal sensilla, and the animal 



MECHANORECEPTION 57 

can attempt to move to a more favourable environment before acute 
respiratory distress ensues. 

It has been suggested that other chordotonal sensilla in the abdomen 
of insects may act as rhythmometers in respiration (Eggers, 1928; 




Fig. 48. Diagrammatic repre- 
sentation of a chordo- 
tonal sensillum. C, cap 
cell; E, enveloping cell; 
S, sense cell; Sb, scolo- 
poid body; D, dendrite; 
A, axon. (Redrawn from 
Schwabe, 1906.) 



Hughes, 1952). In Dytiscus and Locusta comphcated sensory activity 
has been recorded in afferent segmental nerves of the abdomen 
(Hughes, 1952). Three patterns of impulses have been recorded, indi- 
cating that there are some end-organs that discharge during inspira- 
tion, others that discharge during expiration, and some whose 



58 THE PHYSIOLOGY OF INSECT SENSES 

discharge is inhibited during inspiration. Some end-organs with fibres 
in the segmental nerves respond to whistUng, ground tapping, and 
respiration, others to sound only, others to respiratory movements 
only. Those responding to sound are sharply tuned to about 100 c/s, 
and the only parameter of the stimulus to which their frequency of 
discharge is related is intensity. Since the segmental nerves from which 
these signals were recorded are known to contain fibres from seg- 



FiG. 49. A segment of the 
larva of Corethra 
plumicornis showing 
the location of one of 
the segmental chordo- 
tonal organs (C). (Re- 
drawn from Graber, 
1882.) 




mental chordotonal organs, it was suggested that they are the sensilla 
involved in these activities (Hughes, 1952). Pumphrey (1940) also 
suggested that the activity recorded from the segmental nerves of 
locusts arises in chordotonal sensilla and not in hairs as formerly 
believed (Pumphrey and Rawdon-Smith, 1936 c). It should be re- 
membered, however, that the Type II neurons of stretch receptors are 
also sensitive to respiratory movements and to periodic motion, so 
that further investigation of chordotonal responses is needed. 



MECHANORECEPTION 59 

Johnston's Organ 

In 1855 Johnston discovered in the antennae of cuhcine mosquitoes 
the compound chordotonal organ that now bears his name. Its 
structure was not investigated in any detail until nearly forty years 
later (Child, 1894). Since then it has been found to be almost a con- 
stant feature of insect antennae, and much intensive study has been 
given to its structure (e.g., Lehr, 1914; Eggers, 1923, 1924, 1928; 
Debauche, 1936; Richard, 1956, 1957; Urvoy, 1958). In its classical 
form it is basically a hollow cylinder or truncated sphere in the second 
antennal segment (pedicel), where it stretches from the base of the 
segment distally to the synovial membrane of segment three. The 
sensilla comprising the organ vary in number from tens to hundreds in 
the different species. Although the sensilla differ from those in other 
chordotonal organs in that they lack caps or apical bodies, both 
Eggers (1923, 1928) and Snodgrass (1926, 1935) agreed that they are 
chordotonal sensilla. 

Each sensillum consists of a bipolar neuron, a scolopoid sheath, a 
cap cell, and an enveloping cell (Eggers, 1928). As seen with the hght 
microscope, the scolopoid sheath, which is ribbed like most, becomes 
attenuated distally into a bundle of thin fibres. The fibres from a 
number of sensilla are grouped together for common insertion into a 
pore, cleft, or some other attachment on the synovial membrane. In 
the simpler Johnston's organs, where the total number of sensilla is 
small, each bundle with a common point of attachment is clearly 
separate from every other bundle. This arrangement suggests that the 
Johnston's organ is really a compound structure composed of many 
chordotonal organs. The closed cylinders of the complex Johnston's 
organs are a consequence of the extraordinarily large number of 
sensilla that must terminate in the limited space of the pedicle 
(Eggers, 1928). 

The organ is enormously developed in Culicidae and Chironomidae. 
So many sensilla are crowded into the pedicel that the neurons lie in 
several layers, and the cap and enveloping cells are so forced out of 
position that they were originally described as supporting rods (Child, 
1894). Furthermore, there is a corresponding modification of the 
synovial membrane to accommodate the large number of sensilla. The 
base of the third segment in male culicine mosquitos, for example, 
flares to form a reinforced circular plate from which rigid spines 
extend radially far into the pedicel. The sensilla are attached to these 
spinous processes. In these and other species where the organ is a 



60 THE PHYSIOLOGY OF INSECT SENSES 

hollow cylinder both its inner and outer surfaces are covered with 
epithelium that is a continuation of the hypodermis. In one case 
(Hymenoptera) every sensillum is individually ensheathed in epi- 
thelium. In addition to Johnston's organ there are smaller more typical 
chordotonal organs present in the scape, pedicel, and flagellum of 
many insects. 

Everyone who has ever looked at Johnston's organs is impressed 
by the fact that they are ideally situated to respond to movements of 
the third antennal segment with respect to the second. This means, 
essentially, movement of the entire flagellum of the antennae with 
respect to the base, since all antennal muscles are located in the scape 
and insert on the pedicel. 

The stimuli for motion of the antennae may be many. Johnston 
(1885) surmised that the organs of Culicidae were sensitive to air- 
borne sounds, and Mayer (1874) demonstrated that the long hairs on 
the shaft of the flagellum could be set in motion when a tuning fork 
was struck near by. Child (1894) decided that in Culicidae and 
Chironomidae the organ has an auditory function, but otherwise is a 
tactile organ. The legend has grown up that Johnston's organs in 
general are auditory organs, but Demoll (1917) and Eggers (1928) 
went to great pains to point out that the only evidence for an auditory 
function to date, and that not conclusive, was the observation of 
Mayer (1874) for Culicidae. They therefore considered Johnston's 
organs to be organs concerned with movements of the antennae used 
actively as tactile appendages and with passive movements induced by 
air currents. 

As might have been suspected from the fact that the Johnston's 
organ is a compound and complicated organ, the kinds of mechanical 
stimuli to which it can react are varied. A study of the action potentials 
produced in the antennae of the blowfly {Calliphora erythrocephald) 
revealed that the majority of sensilla house phasic receptors, but that 
some of these respond to torsional movements independent of direc- 
tion, while others are sensitive only to movements in one of the two 
possible directions (Burkhardt, 1960). When wind blows on the an- 
tenna it causes the arista to act as a lever arm which rotates the 
funiculus outwards around its long axis (Burkhardt and Schneider, 
1957). A typical electrical response from a single rotation consists of a 
large (+5 mV) action potential (on-wave) foflowed by a series of 
decreasingly small action potentials during the course of stimulation 
and ending with a large off'-wave at the termination of stimulation. 
The small potentials are released by oscillations superimposed at the 



MECHANORECEPTION 61 

time of rotation. The amplitude of the on-wave increases with stimulus 
intensity. It seems that the on-wave represents the summation of many 
synchronously discharging neurons. The change in amplitude with 
change in stimulus intensity is a reflection of the dilTcrcnccs in thres- 
hold of the contributing units. 

The time-course of the off-wave differs slightly. If the direction of 
rotation of the funiculus is reversed the on-wave now resembles the 
off-wave at the end of the stimulus for the original direction of ro- 
tation, and vice versa. Burkhardt (1960), by way of explanation, 
suggested that some of the receptors respond to turning in one direc- 
tion only, while others respond to turning in any direction. The 
geometrical arrangement of sensilla is such that mechanical stress in a 
particular direction serves as a stimulus; however, different sensilla 
are oriented differently with respect to the axis of rotation. Directional 
sensitivity of this sort had already been described for Locusta by 
Uchiyama and Katsuki (1956) on the basis of action potentials 
recorded by means of a microelectrode. There is no support for the 
suggestion of Kuwabara (1952 b) that the Johnston's organ is stimu- 
lated by changes in the pressure of body fluid in the pedicel caused by 
its moment of inertia during antennal movement. 

The pattern of discharge following rhythmic stimuli of short dura- 
tion changes as the frequency of stimulation changes. As the intervals 
between stimuli are shortened below 20-30 msec, the off-wave of one 
stimulus approaches more closely the on-wave of the succeeding stim- 
ulus. When intervals are double the duration of stimuli the on- and 
off-waves present a picture of regularity resembling the pattern 
elicited by air-borne sound (Burkhardt and Schneider, 1957). The 
response to sound frequencies up to 500 c/s reported by Burkhardt and 
Schneider (1957) probably arises from rigidly synchronized discharges 
at the beginning and end of each torsional vibration stimulus (Burk- 
hardt, 1960). As the duration of stimulus is decreased the on- and off- 
waves approach one another, and eventually the off-wave disappears. 
It appears to be inhibited by the on-wave rather than to sum with 
it. Thus, minute changes in stimulus pattern elicit marked altera- 
tions in the spatio-temporal excitation pattern in Johnston's organ 
(Burkhardt, 1960). 

Other patterns of excitation can also be detected in antennae, but 
the identity of the sensilla in which they originate is not known. There 
are a few unknown tonic receptors (Burkhardt and Schneider, 1957) 
(also in Locusta, Uchiyama and Katsuki, 1956), by means of which a 
constant deflexion of the antenna can be signalled. When subjected to 



62 THE PHYSIOLOGY OF INSECT SENSES 

Steady air-flow, however, the antennae appear to tremble. Under these 
circumstances the phasic receptors would register on- and off-waves 
and thus could also register a mean deflexion (Burkhardt, 1960). In 
short, Johnston's organ can provide the central nervous system with 
rather accurate information about the strength and time course of 
antennal deflexion. 

THE ROLE OF MECHANORECEPTION 

IN LOCOMOTION 
Walking 

Locomotion requires the co-ordination of moving parts. Although it 
is possible that movements associated with locomotion can arise from 
an innate central pattern, especially in the case of flying, as Wilson 
(1961) has shown for the desert locust {Schistocerca gregaria Forskal), 
a steady stream of information about the position of parts relative to 
one another and about the magnitude of forces acting upon them is 
undeniably necessary. In so far as flight is concerned, Weis-Fogh 
(1956) and Pringle (1957) favour a complete reflex explanation of 
movements. The consensus now is that walking, too, is reflexly con- 
trolled (Pringle, 1940; Hughes, 1957, 1958). 

In addition to feedback loops from the moving parts, locomotion 
also requires information about the orientation of the insect as a whole 
in the gravitational field. The source of all of this information is pre- 
dominantly the mechanoreceptors. All types of mechanoreceptors 
provide the service, and one of the marvels of the central nervous sys- 
tem is its ability to integrate all of the incoming signals so that the 
necessary adjustments in the performance of the effectors can be made 
quickly and accurately. 

In walking, for example, the reflex action of the leg muscles is evoked 
by stimulation of mechanoreceptors. Most of the muscles of the insect 
leg are innervated by two nerve fibres only, a *quick' and a 'slow' 
(Hoyle, 1957). Stimulation of the quick fibre is followed by a large 
electrical change and a rapid twitch, whereas stimulation of the slow 
fibre is followed by a smaller electrical change and a tonic contraction. 
In the cockroach Periplaneta americana L., as Pringle (1940) has 
shown, the depressor reflex is evoked by stimulation of campaniform 
sensilla on the trochanter; the levator response, by touch on the upper 
side of the leg or on the tibial spines. Most of the campaniform sensilla 
are located and oriented so as to be stimulated by forces produced in 
the leg when the insect is standing normally. The situation may actually 
be much more comphcated than this because of the possibihty of the 



MECHANORECEPTION 63 

muscles being compound ones (Bccht, 1959) and because of the large 
number of mechanoreceptors (tactile hairs, hair plates, campaniform 
sensilla, chordotonal sensilla) and their complicated innervation 
(Nijenhuis and Dresden, 1952; Dresden and Nijenhuis, 1958). That 
the situation is indeed complicated is further suggested by the detailed 
cinematographic studies of Hughes (1952, 1957) on normal cock- 
roaches and amputees. As various legs are amputated, the mechanical 
aspects of walking change. There is a corresponding change in proprio- 
ceptive feedback, with the result that gait and other aspects of walking 
are altered. 

In the stick insect (Carausius morosus) the posture in walking is 
regulated by feedback control via hair plates which measure the angle 
between the coxa and trochanter-femur (Wendler quoted by Mittel- 
staedt, 1961). In the normal insect the body is held free from the 
ground as a result of this feedback. The distance above the ground 
remains the same even when the insect is carrying four times its weight. 
If the sense organs are eliminated the insect touches the ground under 
its own weight. 

Flying 

Flight, of all forms of locomotion, is the most demanding of infor- 
mation. Whether one believes that the basic co-ordination of flight is 
an inherent function of the central nervous system modulated by sen- 
sory feedback (Wilson, 1961) or that flight is more exclusively a matter 
of reflex control (Weis-Fogh, 1956; Pringle, 1957), it is certain that its 
initiation, maintenance, adjustment, and termination can be effected 
by means of elaborate sensory mechanisms. A brief survey of the prob- 
lems involved will indicate the role of the mechanical senses. A com- 
plete treatment is given by Pringle (1957). 

The most specific and universal reflex for initiating flight is the 
'tarsal reflex' originally described by Fraenkel (1932). When the feet of 
most insects are removed from the substrate, flight commences. (There 
is a similar reflex in giant water bugs, Lethocerus americanus and 
Benacus griseus, whereby breaking of contact with the substrate ini- 
tiates swimming movements [Dingle, 1961].) So essential to flying 
insects is this reflex that in some species (Phormia, Calliphora, Vespa) 
amputation of the legs interferes with the ability to cease flying. Con- 
versely, contact with the substrate terminates flight. The electro- 
physiological studies of Pringle (1938 b, 1940), have shown that at 
least in Periplaneta the principal receptors involved are sensilla 
campaniformia on the trochanter and femur. On the other hand. 



64 THE PHYSIOLOGY OF INSECT SENSES 

amputation of the tarsi of flies abolishes the reflex (Fraenkel, 1932; 
Friedman, 1959). 

In Periplaneta another flight-initiating reflex has been described by 
Diakonoff'(1936). This is a change in the relative positions of the pro- 
and mesothorax, the so-called 'fall-reflex'. The sense organs concerned 
are small trichoid sensilla functioning in a manner similar to that of 
hair plates. A similar mechanism can cause flight to commence in 
giant water bugs (Dingle, 1961). Giant water bugs are also stimulated 
to fly by action of wind on sensilla trichodea located on the head 
between the eyes. 

Although some insects {Drosophild) may continue to fly to ex- 
haustion without further mechanical stimulation (Chadwick, 1939; 
Wigglesworth, 1949), others (e.g., Muscina and Schistocerca) require 
continuous stimulation. In the case oi Muscina stabulans a flow of air 
against the antennae, causing the arista-bearing segment to move with 
respect to the second joint, results in the legs being flexed in the flying 
position. Air flow against the antennae also seems to be necessary for 
sustained flight (Rollick, 1940). 

In Schistocerca ten groups of sensilla trichodea bilaterally arranged 
on the leading surfaces of the head are sensitive to wind. When they are 
stimulated the forelegs are flexed in flight attitude and continuous 
flight occurs (Weis-Fogh, 1949, 1956). They assist in stabihzation in a 
horizontal plane (yaw), as is shown by the fact that the locust turns if a 
jet of air is directed on the hairs from the side rather than from the 
front (Weis-Fogh, 1949). Whether they are static or phasic receptors 
or both has not been satisfactorily ascertained. It has been observed 
that they do not vibrate in the wind; they are damped. The hair plates 
on the legs oi Periplaneta, which these resemble, are sensitive both to 
continuous deformation and the vibrations of a loudspeaker (Pringle, 
1938 c). According to Weis-Fogh (1956), *wind on the wings' is also an 
adequate stimulus for the maintenance of flight in Schistocerca. 

Maintenance and alterations of flight velocity depend in con- 
siderable measure upon information supplied by the Johnston's organ . 
The detailed experiments with Calliphora (Burkhardt and Schneider, 
1957), Aedes (Bassler, 1957, 1958), and Apis (Reran, 1957, 1959) have 
revealed its hitherto unsuspected role. When insects are flying, air 
currents impinging on the antennae cause the Johnston's organ to be 
stimulated. As a result of the sensory information received, flight 
velocity is reduced and the antennae are actively brought forward. 
Forward alignment reduces the angle of attack of the air current, with 
consequent reduction in the intensity of stimulation. Reran suggested 



MECHANORECEPTION 65 

that proprioceptive information about the position of the antennae 
relative to the head supplements information from Johnston's organ 
for steering flight velocity. 

When the funiculi of the fly's antennae are rotated in their sockets 
and fixed in the position which they would normally assume if wind 
were blowing on them the flies fly much more slowly than controls 
(Burkhardt and Schneider, 1957). In aphids flight is impaired when the 
flagella of the antennae are removed; however, when artificial flagella 
are supplied as replacements control is regained (Johnson, 1956). 

Change in velocity of flight can be eff'ected in a number of ways. The 
experiments of Hollick (1940) with Mucina showed that these flies 
shift the path travelled by the wing tip cranially if they are subjected to 
a current of air from in front and if they are in possession of their 
antennae. In the absence of antennae, there is no shift. Wing-beat 
amplitude is also altered as a result of information received through 
the Johnston's organ. Bees reduce the wing-beat amplitude in the face 
of air currents, but if they lack antennae the reduction is less marked 
(Heran, 1959). In the case o{ Aedes there is a greater wing-beat ampli- 
tude in air currents when antennae are lacking than in still air when 
antennae are intact (Bassler, 1957, 1958). 

Burkhardt and Schneider (1957) had pointed out that the antennae 
of Calliphora also respond electrophysiologically to sound in the range 
1 50-250 c/s, the same range as the wing-beat frequency. They proposed 
that this response might possibly be employed to register the acceler- 
ation due to each wing-beat, since the funiculi of the antennae vibrate 
at this frequency as a result of the discontinuous air stream arising with 
each wing thrust. Support for the hypothesis is derived from the obser- 
vation that the resonance frequency of the bee's antennal flagellum 
also agrees well with the wing-beat frequency, and the Johnston's 
organ is most sensitive to vibrations of 200-350 c/s (Heran, 1959). 
No tonic component similar to that detected in Calliphora can be seen 
in electrical activity in the bee's antenna. Furthermore, if vibrations 
too fast for the flagellum to follow are forced upon the antenna it is 
bent outwards but no longer vibrates, and the bees do not respond to 
the change in position (Heran, 1959). 

Information from the Johnston's organ is also used to correct yaw. 
In turning about the vertical axis the angle of attack of the antenna 
on the outside of the turn becomes larger. Since intensified current on 
an antenna reduces wing-beat on the same side, a passive rotation 
produces an active torque in the opposite direction by which the 
straight flight course is stabilized (Heran, 1959). 



66 THE PHYSIOLOGY OF INSECT SENSES 

Other monitoring of the movements of the wings occurs as a result 
of stimulation of wing receptors. As many investigators (e.g., Vogel, 
1911, 1912; Lehr, 1914; Erhardt, 1916; Eggers, 1928; Hertwick, 
1931; Zacwilichowski, 1936) have shown, the wings of insects are 
elaborately equipped with sense organs (Fig. 44). These are sensilla 
trichodea, sensilla campaniformia, and chordotonal sensilla. They 
are strategically situated to respond to wind on the surfaces of wings or 
to forces acting on the veins. With the exception of one chordotonal 
organ, all sensilla are located distal to the hinge; consequently, they 
will be subjected to strains and distortions set up by aerodynamic and 
inertial torques, but not elastic torques (Pringle, 1937). Several 
investigators have shown by electrophysiological monitoring that 
considerable information is fed back to the central nervous system by 
these sense organs (Sotavalta, 1954; Wolbarsht and Dethier, 1958; 
Wilson, 1961). 

The sensilla trichodea are clearly tactile. Although Pringle (1957) 
did not exclude the possibility that they react to air flow, he suggested 
that this is improbable, because the small fibre diameter precludes 
rapid enough impulse conduction to meet the demands of quick flight 
reflexes. On the other hand, it is known that these hairs mPhormia fire 
at great speed and adapt very rapidly (Wolbarsht and Dethier, 1958), 
hence might respond to turbulence. The loss of control during the few 
wing-beats necessary to allow time for nervous conduction might be 
inconsequential considering the high rate of wing-beat in most insects. 

The sensilla campaniformia are distributed singly and in groups. 
The former are usually circular, hence not markedly directional in 
their sensitivity. Grouped sensilla are usually oval. The direction of the 
long axis is uniform within a group but differs from one group to 
another. As Pringle (1938 b) has demonstrated, each group constitutes 
a unitary organ selectively sensitive to strains whose compression axis 
is oriented parallel to the direction of the long axis of the sensillum 
dome. 

The location of each group is such that the sensilla are maximally 
sensitive to a particular direction of torque in the vein wherein they He. 
Pringle (1937) has discussed at length the probable mode of action 
of these sensilla in relation to the torques acting on the wing during 
flight. Probable modes of action of the chordotonal organs have been 
deduced with less certainty (Pringle, 1937). 

Any flying machine must possess stability, that is, a tendency to 
return to a characteristic attitude when displaced if it is to be con- 
trollable in the air (Pringle, 1950). In this respect insects are able to 



MECHANORECEPTION 67 

control lift and to stabilize reflexly in all three planes of rotation, that 
is, to correct for pitch, yaw and roll. In insects with four wings much of 
the required information derives from mechanoreceptors on the wings. 
As a result, changes in pronation, supination, and angle of attack of 
the wings are made until stable flight is achieved. Details of the res- 
ponse characteristics of the various sensory structures of the wing, 
however, are poorly known. 

More information is available about the halteres of Diptera. These 
structures, homologues of the hind wings, are radically specialized as 
balancing organs. They are lavishly equipped with all types of 
mechanoreceptors whose homologies can be traced to those of the 
wings of non-dipterous insects (Pflugstaedt, 1912; Zacwilichowski, 
1936). Essentially, each is a heavy mass of tissue on the end of a thin 
stalk. The folding of the base is very complicated, consisting of a main 
hinge and a condyle of secondary articulation (Fig. 45) (Pringle, 1948). 
In these regions are concentrated, in Calliphora, for example, about 
418 mechanoreceptors. They include the following sensilla as des- 
cribed by Pflugstaedt (1912) : 

Campaniform Sensilla 

Dorsal scapal plate 
Ventral scapal plate 
Basal plate 
Dorsal Hicks papillae 
Ventral Hicks papillae 
Undifferentiated papilla 

Chordotonal Sensilla 

Large chordotonal organ 
Small chordotonal organ 

All but thirty-five are located in the three plates and the large chordo- 
tonal organ. It is significant that the axons from these sensilla do not 
fuse as is the case with the campaniform sensilla in the palps of the 
cockroach (Pringle, 1938 b, 1948). The arrangement of sensilla is 
basically the same in all families of Diptera (Brauns, 1939). It has been 
suggested (Pringle, 1948) that strains produced by vertical oscilla- 
tion of the haltere are detected by the dorsal and ventral scape plates, 
the dorsal and ventral Hicks papillae, and the small chordotonal 
organ. Strains produced by gyroscopic torques are presumed to be 
detected by sensilla of the basal plate and the large chordotonal organ. 



68 THE PHYSIOLOGY OF INSECT SENSES 

The undifferentiated papilla may be sensitive to all strains in the 
cuticle of the base. 

The beat of the two halteres is synchronized. They are oscillating 
masses which generate forces at the base of the stalk as the whole fly 
rotates (Pringle, 1948). They are thus gyroscopes, but it is questionable 
that they act as direct stabiHzing gyroscopes (Schneider, 1953). It is 
more likely that their action is indirect, in that the activity of their 
sense organs signals the nervous system to set up the necessary correc- 
tions in the flight mechanism (Pringle, 1957). There is convincing 
experimental evidence that they are instrumental in the control of yaw 
(Pringle, 1948; Faust, 1952; Schneider, 1953), pitch (Faust, 1952), and 
roll (Faust, 1952). 

Finally, in the control of flight there are visual stimuli (e.g., Schaller, 
1960). Movement in the visual field is employed directly by Calliphora 
in incorrecting yaw (Schneider, 1956) and roll (Faust, 1952 ; Schneider, 
1956). Vision is also employed indirectly (Antrum and Stocker, 1952; 
Mittelstaedt, 1950) to correct roll, as the following example of dragon- 
fly (Anax) behaviour illustrates. 

The head is a broad, heavy object, and rotations of the body produce 
movement in the neck region. The position of the body relative to the 
head is signalled by two pairs of prothoracic hair plates. When the head 
of a flying or stationary dragonfly is twisted there is a compensatory 
twisting of the wings. In flight this corrects rolling; when the insect is 
perched it assists in the maintenance of balance. In nature the insect 
moves its head so that the light intensity is always greatest dorsally. By 
means of proprioceptive feedback from the hair plates, the body is 
then rotated until it is ahgned with the head (Mittelstaedt, 1950). 

Swimming 

Insects that swim beneath the surface of water are faced with orienta- 
tion problems more nearly resembling those encountered in the air 
than on land. They can move freely in three dimensions in a homo- 
geneous medium and must possess stability, just as must flying insects. 
In Notonecta, Naucoris, and Macrotorixa the normal swimming 
position also represents the stable equiUbrium position. This position 
is maintained in the imago oi Naucoris and Macrotorixa by the distri- 
bution of air and the position of the legs; in Notonecta larvae, princi- 
pally by the location of the centre of gravity of the body mass (Oever- 
mann, 1936). When these insects are Winded, deprived of the air film 
on the surface of the body, and artificially weighted so that the position 



MECHANORECEPTION 69 

of Stable equilibrium is altered they are still able to orient with respect 
to gravity (Oevermann, 1936). No special localized static organ has 
been found; however, in Notonecta, Plea, Naucoris, and Corixa the 
Johnston's organ is employed in conjunction with a bubble of air to 
mediate position sense (Rabe, 1953). Notonecta and Plea swim ventral 
side uppermost. When they are properly oriented an air bubble 
trapped between the antennae and the surface of the head causes by its 
buoyancy the antennae to be deflected away from the head. If the 
insect is turned upside down the antennae are then deflected towards 
the head. In each instance the deflexion activates the Johnston's organ. 
If the bubble is removed, Notonecta placed in darkness will swim dorsal 
side up (that is, reversed) because the antennae by their own weight 
lean away from the head. For Corixa, which swims dorsal side up, the 
mechanism is the same but acts in reverse (Rabe, 1953). 

Lack of a speciahzed static organ is characteristic of many aquatic 
species, and it appears that much assistance is derived from extero- 
ceptors. BHnded insects, while not losing their ability to retain their 
normal attitude and position with respect to gravity entirely, do tend 
to show locomotory aberrations (Oevermann, 1936; Tonner, 1938; 
Hughes, 1958; Dingle, 1961). Compensatory movements to rotation 
cease when eyes are blackened, and some species show a tendency to 
swim in spirals when unilaterally bhnded. In larvae o^ Acilius sulcatus 
and Dytiscus marginalis, which possess twelve simple eyes (stemmata), 
Schone (1950) has shown that the structure and arrangement of these 
eyes are especially suitable to mediate optical orientation in space by 
sensing the distribution of brightness in the visual space. In rotations 
around the longitudinal axis a displacement of the ratio of excitation 
between the right and left groups of eyes occurs ; in rotations around 
the transverse axis a change in the quotient front : back forms the 
basis of regulation. 

Exteroceptive information concerning water movement is received 
via the antennae. It is assumed that Johnston's organ is involved. A 
swimming Dytiscus holds its antennae at a slight angle to the median 
line. Any deviation from the axis of swimming causes the antennae to 
bend (Hughes, 1958). Some proprioceptive information is necessary 
in any case. Giant water bugs possess hair plates on the trochanters at 
the coxo-trochanteral joints which are important for the co-ordination 
of swimming (Dingle, 1961). When the legs are flexed, as when grasping 
a stem or when flying, the hair plates are stimulated by a covering fold 
of cuticle. When the legs float freely in the water in an extended 
position the hair plates are no longer stimulated by the fold, and 



70 THE PHYSIOLOGY OF INSECT SENSES 

swimming occurs. Destruction of the hair plates interferes with normal 
swimming. 

By analogy with marine invertebrates, especially Crustacea, it might 
be expected that statocysts would be common in aquatic insects. Such 
organs are ideally constructed for responding to gravity in a medium 
where cues are few. Aside from a series of questionable cases studied 
by Wolff (1922) and Studnitz (1932), however, no true statocysts have 
been reported. In the larvae only of many Limnobidae (Diptera) there 
is located on the terminal segment a pair of small sacs, open to the 
outside, and equipped with muscles by which water can be pumped in 




Fig. 50. The organ of pressure sense of Nepa. T, trachea ; N, nerve ; M, 
membrane of overlapping expanded margins of scale sensilla; C, 
closed spiracle ; S, sensory papilla. (Redrawn from Thorpe and Crisp, 
1947.) 



and out (Fig. 51). Invariably each pouch contains a few minute par- 
ticles either formed by the larva itself or picked up from the outside. As 
the muscles of the sac contract and relax, the particles are rattled 
about the interior. 

In the interior of the sac are usually two sensory hairs, one at the 
blind end or deepest part of the sac, the other, in a lateral position. 
Wolff (1922) was convinced that these organs were not static in 
function. Studnitz (1932), on the other hand, after proving that uni- 
lateral or bilateral destruction of the organs abolished the positive 
geotaxis characteristic of the normal larvae, concluded that they were 
indeed statocysts. 

In water bugs (A^e/?^ and ^/j/ze/oc/ze/rw^) there are elaborate mechano- 
receptive organs which appear to be designed to respond to pressure 



MECHANORECEPTION 71 

changes and are presumed to have a static function. The organs in 
Nepa, situated adjacent to the spiracles of the third, fourth, and hfth 
abdominal segments, consist of groups of peg-shaped sensilla alter- 
nating with umbrella-shaped sensilla (Fig. 50). According to Hamilton 
(1931), the whole is covered by a thin membrane which docs occlude 
the adjacent spiracle, but Thorpe and Crisp (1947) considered the 
membrane to consist of the overlapping umbrella-like portions of the 
sensilla which do indeed cover the spiracle. Baunacke (1912) con- 
sidered these organs to be hydrostats. After he ascertained that a 
blinded Nepa placed on an underwater seesaw would reverse its 
direction of crawling as the inclination was reversed, he eliminated the 




Fig. 51. Statocyst in the larva of an aquatic dipteran (Limnobiidae). The 
black objects are particles in the cavity. (Redrawn from Wolff, 1922.) 

organs. Elimination abolished the bug's response to the change of 
inclination. Oevermann (1936) and Thorpe and Crisp (1947) con- 
firmed these observations. Oevermann, however, demonstrated that 
there must be proprioceptive information from the legs, because a 
weighted insect can still make position corrections. 

Baunacke (1912) believed that the three pairs of organs act as a 
system and respond to relative changes in pressure. In other words, the 
lowest pair (on the fifth sternum) are under greater pressure than 
the upper pair (third sternum) when the bug is in certain attitudes. For 
this system to work the gas-filled cavities of all of the sense organs 
must be in communication with one another via the tracheal system. 
According to Hamilton, who described the organs as covered with a 
membrane sealing them from the trachea, this is not so, but Thorpe 

F 



72 THE PHYSIOLOGY OF INSECT SENSES 

and Crisp maintained that there is communication. They performed a 
series of extirpation experiments that are in agreement with 
Baunacke's hypothesis (Fig. 52). In the control (A) bugs on a seesaw 
gave sixty-eight correct performances out of ninety- two. B did not 



. Controls intact 


B. Middle pair 
extirpated 


C. All on one side 
extirpated 


O 
O 
O 


O 

X 

O 


o 

X 

O 


O X 
O X 
O X 


D. Anterior and 
posterior pair 
extirpated 


E. Posterior pair 
extirpated 


F. Middle of one 
side only extirpated 


X 

O 

X 


O 
O 

X 

A 


O 

o 

X 


O O 
O X 
O O 


KP 


Kl^ 




Kp 


1 ^ : 











Fig. 52. A. Diagram illustrating the various operations performed on the 
three pairs of pressure organs in Nepa. (Redrawn from Thorpe and 
Crisp, 1947.) B. Diagram to illustrate the principle of action, when 
tilted in water, of a system of distensible membranes enclosing an air 
space and connected by an air-filled tube, of three pressure receptors 
of one side of Nepa. (Redrawn from Thorpe and Crisp, 1947.) 

differ statistically from A, C and D were generally negative; E res- 
ponded fairly well and F less well. It was concluded that the three pair 
of organs in Nepa were indeed co-ordinated as a differential mano- 
meter system. 

A less-compHcated organ occurs in adults of the predatory water 
bug Aphelocheirus (Fig. 53). There is a pair of oval sensory plates on 



MECHANORECEPTION 73 

the second abdominal sternum. Each consists of a shallow ovoid 
depression in which the usual plastron hairs are replaced by large 
hydrofuge hairs (± 60,000 per sq. mm.), among which are delicate 
innervated sensilla trichodea (Fig. 53). It is assumed that increases of 




53. A. Ventral view of the left 
spiracular 'rosette' on the second 
abdominal segment of Aphelo- 
cheinis with the specific organ of 
pressure sense and the col- 
lapsible air sac. B. Section 
through the edge of the organ 
of pressure sense of Aphelo- 
cheirus showing one sensory hair 
and its bipolar neuron and the 
plastron hair pile. (Redrawn 
from Thorpe and Crisp, 1947.) 



pressure due to water currents and turbulence, depth, or the animal's 
position with respect to gravity are registered because the large slant- 
ing hairs press down upon the sensilla (Thorpe and Crisp, 1947). 
Unilateral damage causes the animal to swim in spirals, but this is only 
indirect proof of their static function (Larsen, 1955). 
The air space around the pressure organs is continuous with tracheal 



74 THE PHYSIOLOGY OF INSECT SENSES 

air spaces ; hence, if the organs are to give meaningful information 
regarding external pressure changes the internal air pressure must 
be kept constant. Thorpe and Crisp (1947) have suggested that large 
tracheal air sacs near these organs damp internal pressure changes. A 
different interpretation of the function of these air sacs has already 
been discussed (Larsen, 1955). 

Comparable, though simpler, so-called static organs have been 
described in Ranatra, Lethocerus, and Belostoma, but little is known of 
their physiology (MoUer, 1921). 

On the surface of water insects do not encounter the same sensory 
problems as underwater, but, because of the great speed of swimming 
that is possible, obstacle avoidance is a problem. Some imaginative 
experiments by Eggers (1936 b, 1927) with the whirligig beetles Gyrinus 
marinus and G. natator suggest that the antennae play a prominent 
role. Beetles on the surface of water in a small container (diam. 35 cm.) 
are able to avoid collisions with one another and with the walls of the 
container. If the walls of the container are coated with paraffin so that 
the meniscus is convex instead of concave or if the surface of the water 
is carefully cleaned of all dust particles the frequency of collisions 
against the walls increases markedly. When swimming beneath the 
surface of the water the beetles also hit the wall. Neither vision, nor 
detection of waves bouncing from the walls, nor air pressure produced 
by the beetle moving towards the walls appear to be involved in 
obstacle avoidance. Eggers postulated that detection of the meniscus 
and detection of the resistance of the surface dust layer as it is com- 
pressed between the beetles and the wall informs the beetle of the 
proximity of the obstacle. It was presumed that the antennae, and 
possibly their Johnston's organs, are the sensing elements involved. 
Ordinarily the Johnston's organ is not highly developed in Coleoptera 
(as compared with Diptera), but in Gyrinus it is fairly complex, and the 
antennae have pecuhar structural modifications which, according to 
Eggers, permit the pedicel to glide on the water surface while the 
flagellum sticks up into the air. The pedicel would be very sensitive to 
irregularities (menisci) in the water surface and to the resistance of 
floating particles such as dust; when moved, it would cause counter- 
movements of the flagella, with a consequent stimulation of John- 
ston's organ. Amputation of the antennae results in an increased 
number of collisions. 



MECHANORECEPTION 75 

RESPONSES TO GRAVITY 

As the foregoing discussions have impHed, insects lack receptors 
designed specifically for the detection of gravitational force. Infor- 
mation required for maintenance of primary orientation is derived 
secondarily by the central nervous system from many receptors whose 
primary function may have little to do with responses to gravity. The 
precision with which some insects respond to gravity and the import- 
ance of a critical evaluation suggests that there may be some receptors 
whose information is critical. Buckmann (1954) has demonstrated, for 
example, that the staphylinid beetle BUdius bicornis Grm., which 
burrows in sea sand, responds to gravity with a precision of the order 
of one angular degree. This precision is not inferior to that exhibited 
by other animals which possess statocysts (Buckmann, 1955 a). 
Centrifugation experiments have indicated that neither light nor 
surface features are cues. Unfortunately the nature of the required 
sensory information is not known. In any event, the antennae are not 
required (BUckmann, 1955 b). 

Another insect for which a precise response to gravity is critical is the 
honeybee. In order to be able to communicate the direction of food 
sources by transposing the angle of flight with respect to the sun to an 
angle of dancing with respect to gravity in a dark hive, the bee must 
be able to assess very accurately the direction of gravitational force. 
Vowles (1954), working with ants, had shown that the antennae were 
of importance in these species. Iron filings were cemented to various 
parts of the bodies of ants climbing a vertical surface. The ants were 
then suddenly subjected to a magnetic force. Only when the filings 
were on the funiculi of both antennae did the ants suddenly change 
orientation. This result plus the knowledge that different orientations 
with respect to gravity normally impart different rotational forces on 
the funiculus led to the hypothesis that the Johnston's organs are 
involved in geotaxis. 

With the honeybee, however, the antennae are not so critical. 
Instead, hair plates in the neck region and at the articulation of the 
thorax and abdomen play a prominent role (Lindauer and Nedel, 
1959). When the bee is standing on a horizontal surface the hairs of the 
pro-thorax are in even contact with the back of the head. When the bee 
crawls up a vertical surface the head will incline towards the sternum 
because of its low centre of gravity. In this position the more ventral 
hairs of the hair plate will experience maximal shearing forces. The 
less the substrate is inclined towards the vertical, the smaller the 



76 THE PHYSIOLOGY OF INSECT SENSES 

shearing forces on the whole organ. When the bee is crawHng down a 
vertical surface the head will incline dorsally and the dorsal areas of 
the hair plate will be maximally stimulated. When a bee on a vertical 
surface turns to the right or left the hair plates on different sides of the 
thorax will be unequally stimulated. In this mechanism there is 
potentially a very fine capacity for analysing the position angle on the 
vertical plane. The degree of bending of individual hairs and the 
spatial distribution of bend in the hair plates as a whole could provide 
the necessary information (Lindauer, 1961). Severing the nerves to 
these organs, immobilizing the head, or changing the centre of gravity 
of the head by weighting it results in impairment of responses to 
gravity and ability to orient communication dances correctly with 
respect to gravity. The hair plates at the articulation of the thorax 
and abdomen function in a similar fashion. They appear to be subord- 
inate to the cervical organs, however, because they alone are unable to 
regulate responses to gravity when the cervical organs are eliminated 
or when the head is fixed or weighted. 

A comparative study of the occurrence and structure of hair plates 
at the joints of representatives of five famihes of ants, the honeybee, 
and Vespa saxonica has shown that these setal fields occur at the 
antennal, cervical, petiolus, and gaster joints and on the joints 
between the thorax and coxae and coxae and trochanters (Markl, 
1962). By removing sense organs, disconnecting the various joints, 
or cementing the joints in abnormal positions, Markl was able to 
demonstrate that the cervical hair plates are the most important for 
gravity reception. The others in decreasing order of importance are 
the petiolus, the antennal, the coxal, and the gaster. In agreement 
with Vowles (1954) it was found that the antennal organs serve as 
gravity receptors but they represent only one, and by no means the 
most important, receptor system for gravity. In supplementing the 
results of Lindauer and Nedel (1959) it was shown that the receptors 
at the coxal joints but not those of the antennae serve for gravity 
reception in the honeybee. Since the hair plates are able to perceive 
active movements of the joints, it is argued that multiple development 
of hair plates is necessary if these organs are to serve as gravity 
receptors. Only a message in the same direction from one or more of 
the hair plates is related to gravity by the central nervous system, 
whereas aberrant responses from one or more areas are interpreted 
as joint movement independent of gravity (Markl, 1962). 



CHAPTER IV 



Sound Reception 



The to-and-fro motion of a particle repeatedly displaced from equili- 
brium is termed vibration. In a continuous medium a vibrating particle 
causes periodic displacement of neighbouring particles by elastic 
forces. The resulting disturbance takes the form of periodic com- 
pressional v^aves. Sound reception is the process of detecting these 
waves whether they occur in gases, liquids, or solids. Whether one 
defines all vibration detection as 'hearing', restricts the term 'hearing* 
to the detection of air-borne sounds by specialized receptors and 
relegates other sound reception to a 'vibration sense' (von Budden- 
brock, 1952), or limits 'hearing' to that condition where an animal 
behaves as if it has located a sound source (sound being defined as any 
mechanical disturbance whatever which is potentially referable to an 
external locaHzed source) (Pumphrey, 1950) is not important to an 
understanding of how the receptors work. The crucial question, 
physiologically speaking, is to what extent insects can detect periodic 
motion or vibration in their environment and which parameters of the 
wave are detected. In this respect it is helpful to inquire first what kind 
of sounds or vibrations insects are exposed to normally. 

Many sounds are produced by insects themselves. Many are inci- 
dental to ordinary movements, but nearly all orders of insects have 
members that produce specialized sounds. Fringsand Frings (1958), 
in their review of the subject, have listed the following specialized 
methods of sound production: (1) tapping the substrate; (2) explosive 
expulsion of air or other material through a small orifice ; (3) snapping 
a prosternal spine from a cavity in the mesosternum ; (4) vibrating the 
body without flight to produce a buzzing, whining, or piping; 
(5) snapping the wings in flight; (6) snapping tymbals or tymbal-like 
organs; (7) stridulation (rtibbing specialized surfaces of the elytra 
together or stroking the elytra with the hind femora) ; (8) expulsion 
of air over a specialized vibrating membrane. The sounds produced 
by insects are principally connected with sexual activity, territoriality, 
defence against predators, and maintenance of cohesion in flying 
swarms (Haskell, 1957). In addition to responding to sounds of these 

77 



78 THE PHYSIOLOGY OF INSECT SENSES 

origins, insects respond aggressively to sounds produced by prey (e.g., 
the antlion to its prey) and defensively to sounds produced by pred- 
ators (e.g., moths to the sounds of bats). Insects can also detect a 
certain amount of the white noise that fills the physical environment. 
So far as is known, only two kinds of mechanoreceptive sensilla 
are sensitive to sound, sensilla trichodea and chordotonal sensilla, 
although there is nothing about the structure of campaniform sensilla 
or stretch receptors that precludes the possibility of their also respond- 
ing to sound. Indeed, stretch receptors accurately signal phasic 
stimulation up to 5 c/s (Lowenstein and Finlayson, 1960). Hairs 
sensitive to sound do not differ fundamentally from those concerned 
with tactile and proprioceptive functions (hair plates on the legs of 
Periplaneta respond to loudspeaker sounds [Pringle, 1938c] ) nor do 
the chordotonal sound receptors differ appreciably in structure from 
proprioceptive chordotonal sensilla. The more highly specialized 
chordotonal receptors, however, are grouped together and associated 
with elaborate accessory structures enhancing their sensitivity to 
sound. These organs include: tympanic organs, Johnston's organ in 
culicine mosquitoes, and subgenual organs. 

TYMPANIC ORGANS 
Morphology 

Few external structural details escaped the eyes of nineteenth-century 
taxonomists, so it is not surprising that the occurrence of tympana was 
noticed in a number of insects. In some cases the structures were 
examined only with a view of their taxonomic usefulness ; in others, 
guesses were made regarding their function. Those who guessed 
correctly believed the organ to be an instrument of sound production. 
Miiller (1826), studying the paired tympana on the first abdominal 
segments of Acrididae, decided that they were organs of hearing. 
Tympanic organs were then discovered in the tibiae of the prothoracic 
legs of Tettigoniidae and GryUidae (Siebold, 1844) and later in moths 
and butterflies. Among the Lepidoptera tympanic organs occur in the 
abdomen of adults in the super-families Geometroidea and Pyraloidea 
and in the metathorax of Noctuidea (Swinton, 1877; Jordan, 1905; 
Deegener, 1909; Eggers, 1911, 1919; von Kennel, 1912). Abdominal 
tympanic organs occur in the Cicadidae (Vogel, 1923 a) and in Corixa 
andafewother Hemiptera (Graber, 1882 a, 1822 b; Hagemann, 1910; 
Wefelscheid, 1912; Schaller, 1951), although in some of these forms 
the variation from an obvious tympanic organ makes those sensilla 
associated with tracheae look suspiciously like the proprioceptive 



SOUND RECEPTION 79 

chordotonal organs usually associated with tracheae in other species 
Some chordotonal organs in the wings of Satyridae are associated with 
tympana (Vogel, 1912). 

The detailed inner structure of tympanic organs was investigated 
thoroughly by Schwabe (1906), Eggers (1911, 1919, 1924, 1928), Vogel 
(1923 a), Hers (1938), Roeder and Treat (1957), and Treat (1959). 
These studies have been extended by the electron-microscope studies 
of Gray (1960). 

All tympanic organs have certain features in common. These 
include: a thin cuticular membrane, a closely appressed internal 
tracheal sac, and a group of chordotonal sensilla. The sensilla may be 




Fig. 54. Diagram to show the method of attachment of the neural elements 
to the inner surface of the tympanum of the locust. A, auditory nerve; 
Fo, fold; Si and S2, location of sense cells; E, elevated process; S, 
styliform body; L, leg; B, base; D, drum; P, pyriform vesicle; Fi, 
fusiform body. (Redrawn from Gray, 1960.) 



attached directly in the middle of the tympanum (Acrididae), to its far 
edge (Cicadidae), or to the trachea instead of the tympanum itself 
(Tettigoniidae and GrylUdae). They vary in number from two in 
certain moths to 1,500 or more in cicadas (Figs. 55, 57, 58, 59). 

Of all these, the tympanic organs of Acrididae have undoubtedly 
been studied in greater detail than any others. The tympanum is a thin 
(2-3 (J.), imperfectly ovoid area of exocuticle lying in a crater-like 
depression (sometimes likened to the auditory meatus of the human 
ear) formed by an incomplete rim of thickened cuticle (Fig. 54). The 
tympanum is further strengthened circumferentially as a consequence 
of a thickened cuticular invagination. It is thus a rigidly supported 
drumhead. It is hned internally, as is almost all cuticula, by a thin layer 
of hypodermal epitheHum. Closely appressed to the internal side of the 
tympanum is a tracheal sac fed by a branch from the main trachea 



80 



THE PHYSIOLOGY OF INSECT SENSES 




Fig. 55. Tympanic organ of the prothoracic leg of Orthoptera. Ta, anterior 
trachea; Tp, posterior trachea; Sb, subgenual organ; I, intermediate 
organ; A, acoustic organ; SbN, subgenual nerve; TmN, tympanic 
nerve; C, cap cells, S, scolopoid cells. (Redrawn from Schwabe, 1906.) 



(analogous to the Eustachean tube), whose spiracle lies at the anterior 
border of the tympanum. The tympanum is in fact lined by two layers 
of epithelium, that of the hypodermis and that of the tracheal sac, and 
is bordered by air on both surfaces. 

The tympanal nerve, a branch of the tergal nerve of the third thor- 
acic ganglion, enters the region in a fold of the tracheal epithelium, 
branches, and attaches at several points of the drum (Fig. 54) : the 
folded body (rinnenformiges Korperchen), the styliform body (stiel- 



SOUND RECEPTION 81 

formige Korperchen), the elevated process (zapfenformige Korper- 
chen), and the pyriform vesicle (birnformiges Korperchen). These 
bodies are merely complex thickened areas of the drum. A small 
branch of the nerve goes to the folded body, where it innervates a few 
hairs and other sensilla. The main portion of the nerve, before branch- 
ing to each of the four points of attachment, swells. This swelling has, 




Fig. 56. Schematic dorsal stereogram of noctuid tympanic organ and 
related structures. B, Biigel; C, conjunctiva or accessory tympanic 
membrane; CTC, countertympanic cavity with external orifice 
indicated by arrow; CTM, countertympanic membrane; E, epaulette 
or nodular sclerite ; EL, electrode site ; H, hood ; L, ligament ; M^, muscle 
originating on antero-median portion of metascutum and inserting on 
metapostnotum anterior to CTM; Ma, muscle originating dorsally 
on metascutum and inserting on epimeral band; MP, mesophragma; 
MS, metascutum; Pi, pocket I of tympanic frame; PTG, pterothoracic 
ganglion; S, sensillum; Si, metathoracic spiracle; Sg, first abdominal 
spiracle ; SP, scutal phragma ; TAS, tympanic air sac lined with tracheal 
epithelium; TM, tympanic membrane; TN, tympanic nerve; TR, 
tympanic recess. (Courtesy of Roeder and Treat.) 



82 THE PHYSIOLOGY OF INSECT SENSES 

unfortunately, been called a ganglion by Gray (1960). It is in fact the 
aggregation of most of the cell bodies (of which there are 60-80) 
of the neurons making up the sensilla. It is invested by two layers of 
cells, one of which is the epithelium of the tracheal air sac surrounding 
the nerve, the other being the accessory cells of the sensillum. 

Prothoracic leg tympanic organs lie in the proximal region of the 
tibiae, one member on the anterior side, the other, posterior. They lie 




Fig. 57. Right tympanic air sac and associated structures of a noctuid as 
seen from within the metathorax. A portion of the air sac is represented 
as cut away to show the sensory elements. ATP, anterior tendon plate ; 
B, Biigel; DLg, second dorsolongitudinal muscle of metathorax; 
EP, epaulette ; L, ligament connecting chordotonal organ with scutal 
phragma; PI, PII, pockets of tympanic frame; S, acoustic sensory 
cells; TAS, tympanic air sac; TM, tympanic membrane; Tr, tracheal 
twig from metathoracic spiracle. (Redrawn from Treat and Roeder 
1959.) 



thus back to back separated by two branches of a trachea, an anterior 
and a posterior (Fig. 55). Whereas in the Gryllidae the tympanic mem- 
branes lie on the exposed surface of the leg, they are sunken in the 
Tettigoniidae and are exposed to the outside only via a slit. The 
sensilla, of which there are about seventy in each leg, lie in a long row 
on the dorsal side of the anterior trachea. The dendrites and scolopoid 
bodies are oriented in such a way that they are not inserted on the 
tympanic membrane but instead on a membrane, presumably derived 



SOUND RECEPTION 83 

from the basement membrane of the hypodermis and trachea, border- 
ing on the blood cavity of the leg. The cells thus stretch between the 
trachea and this membrane (Fig, 55). This organ is innervated by a 
purely sensory nerve, the tympanic nerve, originating from the first 
thoracic ganglion. This nerve also innervates part of the subgenual 
organ and the intermediate organ. The rest of the subgenual organ is 
innervated by a branch of the leg nerve. 

The metathoracic tympanic organ of Lepidoptera is the simplest 
organ of this type. It lies in the anterior wall of a deeply recessed cavity 




Fig. 58. The tympanic organ of the cicada Tibicina haematodes as seen 
when the abdomen is cut transversely. H, heart; G, gut; A, auditory 
cavity in which a window has been cut; T, tympanum. (Redrawn from 
Vogel, 1923.) 



bounded posteriorly by parts of the first abdominal segment (Fig. 56). 
As in the Acrididae, the membrane is lined with hypodermal epithel- 
ium plus that of the associated tracheal sac. Two chordotonal sensilla 
are attached to the inner surface of the tympanic membrane. The 
axons, forming part of the tympanic nerve, extend anteriorly, receive 
support en route from a thin ligament, turn at an angle to receive 
further support from a cuticular projection, the Bugel, then continue 
on through the tracheal sac ultimately to join the pterothoracic 
ganglion (Fig. 57). Like the comparable structure in the locust, the 
nerve is ensheathed in tracheal epithelium. 



84 THE PHYSIOLOGY OF INSECT SENSES 

The tympanic membrane faces only part of the tracheal air sac. 
The rest of it is faced by another membrane whose upper surface is 
exposed to the air by a narrow slit which is the orifice of a large 
counter-tympanic cavity. This cavity and membrane are regarded as 
accessory resonating structures. 

The paired tympanic organs of cicadas are located ventrally in the 
region of the first and second abdominal segments. They differ from 
others described chiefly with reference to the point of attachment of 
the chordotonal sensilla. These, approximately 1,500 in number, occur 
in a single large bundle, their proximal ends attached to one corner of 




Fig. 59. Frontal section through the base of the abdomen of Cicadetta 
coriaria showing the left auditory capsule. S, sense cells ; E, enveloping 
cells; N, nerve; B, blood; Sp, spiracle; O, outer air; I, inner air space; 
T, tympanic membrane. (Redrawn from Vogel, 1923.) 

the tympanic membrane and their distal ends to the cuticle of the body 
wall (Figs. 58 and 59). 

The tympanic organs of Orthoptera and Lepidoptera have two so- 
called tympanic muscles associated with them. The function of these 
muscles is unknown, although it has been suggested from time to time 
that they might be concerned with altering stresses on the tympanic 
organ. In moths it is certainly true that distortion of the skeletal 
elements of the tympanic organ reversibly changes the excitability of 
the sensilla (Roeder and Treat, 1957). 

The Sensilla 

The chordotonal sensilla, as viewed with the light microscope, are all 
basically the same. So far only those of the tympanic organ of the 



SOUND RECEPTION 85 

locust Locusta migratoria migratorioides have been examined with the 
electron-microscope. The relations between the various cells compos- 
ing the unit are clearly revealed (Fig. 60). The axon and cell body of 
the neuron are enveloped in a Schwann cell. Each Schwann cell may 
envelope several neurons. Distal to the Schwann cell, at the base of the 




Fig. 60. A diagrammatic section through the sensory region of the locust 
tympanic organ to show the method of attachment of the sensory cells. 
H, hypodermis; E, elevated process; C, cap cell; Ci, cilium-like pro- 
cess; S, scolopoid body; Sc, scolopale cell; D, dendrite; Sw, Schwann 
cell; A, axon; F, fibrous sheath cell. (Redrawn from Gray, 1960.) 



dendrite, lies another enveloping cell, the fibious sheath cells (prob- 
ably the Bindesubstanz of Schwabe). The remaining portion of the 
dendrite is enclosed in the enveloping cell (Hiillzelle of Schwabe, 
scolopale cells of Gray). Between this cell and the hypodermis lies the 
cap cell (Kappenzelle of Schwabe, Deckzelle of Eggers, attachment 



86 THE PHYSIOLOGY OF INSECT SENSES 

cell of Gray). These cells, as Schwabe (1906) observed, are in contact 
with each other by finger-hke processes and interdigitate with the 
hypodermal cells by folds. 

The scolopoid body exclusive of its cap is a hollow tube composed 
of several concentric rods. It lies within the cytoplasm of the envelop- 
ing cell. The apical body or scolopale cap is an extracellular body lying 



L 




Fig. 61 . Details of the scolopoid region of the tympanic organ of the locust. 
Cs, scolopoid-cap ; Ci, cilium-like process; Sc, scolopale cell; D, 
dendrite; A, axon. (Redrawn from Gray, 1960.) 

in a depression of the cap cell and fitted into a rim of the enveloping 
cell containing the fused ends of the scolopale. 

As the dendrite proceeds from the cell body it presents a ring-shaped 
dilation just before entering the scolopoid body, a less-pronounced 
dilation followed by a marked reduction in diameter after it has entered 
the scolopale, and, finally, a subterminal sweUing. Its tip is inserted 
into a channel in the cap (Fig. 61). 

The axial fibre which can be seen by light microscopy is shown by 



SOUND RECEPTION 87 

electron-microscopy to be a very complicated cilium-like structure 
consisting of basal rootlets fusing into a root as they ascend within the 
dendrite (Fig. 62). Marked periodic cross striations are present. The 
distal portion of the cilium-like structure consists of nine fibrils 




Fig. 62. Diagrammatic longitudinal section through the sensillum in the 
tympanic organ of the locust. Cs, scolopale cap ; Ci, cilium-like process ; 
Sc, scolopale cell; C, cap cell; F, fibrous sheath cell; Sw, Schwann 
cell; Sr, scolopale rod; D, dendrite. (Redrawn from Gray, 1960.) 

surrounding a central core. Its resemblance to the typical motile 
cilium is so striking that Gray (1960) called it a cilium. Since there is no 
evidence that it is functionally a cilium, it seems inadvisable to identify 
it so completely with those structures. 'Cilium-like' is a more appro- 
priate designation. 

Mechanism of Action 

It will be recalled that vibrational disturbance in a homogeneous 
medium produced both a local increase in pressure and a displacement 



88 THE PHYSIOLOGY OF INSECT SENSES 

of contiguous particles away from the source of disturbance. It follows 
that the waves resulting from this disturbance may be detected either 
by a device sensitive to pressure change or by one sensitive to displace- 
ment. As Pumphrey (1940) has stated in his discussion of the physics 
of sound detection, the prerequisites of a pure pressure receptor are a 
massive, opaque (to sound) chamber closed by a stiff diaphragm whose 
displacement is vanishingly small. A recording system coupled to the 
diaphragm would measure the excursions which are proportional to 
the pressure amplitude. The orientation of the instrument with respect 
to the source of sound is unimportant. The auditory mechanism of 
the mammal is undoubtedly a receiver of this type, as are most 
commercial microphones. 

A displacement receiver requires a diaphragm or moving vane 
whose mass and hinges are so slight as not to offer resistance to 
motion. For maximum efficiency a receiver of this type should be 
oriented in such a way that the incidence of sound is normal to the 
plane of the moving element. 

Judging from their structure, all insect sound-detecting organs are 
displacement rather than pressure receptors. There is one ingenious 
experiment reported which was designed to ascertain whether or not 
the sound receptors were indeed displacement receptors (Antrum, 
1936). Ants {Formica rufa and Myrmica spp.) can respond to loud 
artificial sounds. Antrum directed sound vertically downwards upon 
a reflecting surface, and so set up standing waves. In one experiment 
ants were allowed to walk upon the reflecting surface ; in another, they 
walked upon gauze suspended at a critical level above the surface. 
Under these conditions of a standing wave the reflecting surface was 
the region of maximum pressure change and minimum displacement, 
whereas at the gauze, this being an antinode, the reverse was true. 
Ants responded most vigorously when walking on the gauze ; that is, 
they were most sensitive to displacement. Unfortunately, as Pumphrey 
(1940) pointed out, the sounds employed were extremely intense 
(10^1 times human threshold at 1,000 c/s), and there is no indica- 
tion as to whether the ants were responding to air-borne sound 
waves or to vibrations in the substrate. It is not known what organs 
were involved. As Pumphrey further pointed out, it is not necessarily 
true, as Antrum maintained, that velocity was the critical factor, since 
displacement, velocity, and acceleration are all maximal at an 
internode. 

In any event, there is at this time absolutely no conception in terms 
of structure of the manner in which chordotonal sensilla operate. 



SOUND RECEPTION 89 

As Gray (1960) pointed out for Locust a, displacement of the 
membrane is presumably transmitted to the cap cell. The cap appears 
to be rigidly seated on the scolopale, which in turn seems to be firmly 
locked to the dendrite. The cilium-like tip of the dendrite lies freely in 
the extra cellular cavity of the scolopale and cap. What moves in 
respect to what is obscure. Now that the electron-microscope is 
revealing more clearly the structural relationships of these sensilla, 
earlier speculations upon their mode of action based upon the partial 
knowledge provided by the light microscope have only historical 
value. 

Function - Orthoptera 

The earliest attempt to analyse thoroughly the function of tympanic 
organs was that of Regen (1908, 1912, 1913, 1914 a, 1914 b, 1924, 1926). 
As experimental animals he employed the cnckti Liogryllus campestris 
and the long-horn grasshopper Thamnotrizon apterus. He demonstra- 
ted that females would orient to a telephone transmitting the sound of 
a male in another room and that two males could sing in concert. 
Between the Vorspiel (prelude) and the Nachspiel (coda) of the duet, 
that is, the beginning and end, where the two were in synchrony, there 
was almost always an intermediate period during which the chirps of 
the two alternated regularly. Furthermore, naive (newly moulted 
adults) males could be induced to sing in concert with many kinds of 
artificial sounds ranging in frequency from i 400 c/s to + 28,000 c/s. 
All of these experiments proved that the insects were sensitive to air- 
borne sound. When both tympanic organs were amputated the res- 
ponses were almost completely abolished (some residual sound 
perception remained), thus proving that the tibial tympanic organs 
were the principal sound receptors. 

These conclusions were confirmed a few years later, when Wever 
and Bray (1933) recorded nerve activity in the forelegs of crickets 
{Gryllus assimilis) and tettigoniids {Amblycorypha oblongifolia and 
Pterophylla camellifolia) by means of electrodes inserted therein. The 
frequency range for crickets was 300-8,000 c/s; for the tettigoniids, 
800-45,000 c/s. The electrical response was asynchronous at all fre- 
quencies. These experiments alone were not conclusive, because, by 
inserting their electrodes into the leg rather than directly upon the 
tympanic nerve, Wever and Bray might conceivably have been record- 
ing from tactile hairs and other chordotonal organs of the leg as well as 
from the tympanic organ (cf. also Wever, 1935). An attempt to 
circumvent these difficulties was made with Decticus by Antrum 



90 THE PHYSIOLOGY OF INSECT SENSES 

(1941), who recorded from legs in which the subgenual organs pre- 
sumably had been destroyed. Unfortunately, the precision of the 
operation was not confirmed histologically post mortem. In any event, 
the sensitivity to air-borne sound waves extended from 1,000 c/s to the 
upper limits of the stimulation apparatus (10,000 c/s). The higher the 
frequency, the lower the threshold. Responses at frequencies below 
1,000 c/s were obtained only by employing intensities so high that it is 
doubtful that they truly fell within a physiological range. 

The abdominal tympanic organs of two acridids {Locusta migratoria 
migratorioides and Arphia sulphured) were sensitive over the range 
300-10,000 c/s (Wever, 1935; Pumphrey and Rawdon-Smith, 1936 b) 



30 — 



o 

V 

<u 
c 

o 
o 

\) 

U 

c 

t 

TO 

■^ 
C 
03 

CU 

o 



c 
o 



30 



60 



90 




300 



3,000 



10.000 



Frequency (c/sec) 

Fig. 63. a, Threshold curve for tympanic organs of Arphia sulphurea 
averaged from Wever's figures, b, Threshold curve for an isolated 
tympanic organ of Locusta. c, Human threshold subjectively de- 
termined (from Wegel, 1932). (Redrawn from Pumphrey, 1940.) 



SOUND RECEPTION 91 

(Fig. 63). Again over the entire range the nerve response was asyn- 
chronous. Since 10,000 c/s was the limit of the apparatus used, it would 
appear that the tympanic organ is much more sensitive than the 
human ear at frequencies above 10,000 c/s. In the neighbourhood of 
3,000 c/s, according to one report of Pumphrcy and Rawdon-Smith 
(1936 c), the tympanic organ ofLocusta exhibits maximum sensitivity. 
At this point the frequency is only 20 db above the ear of man at its 
maximal sensitivity. On the other hand, in an earlier paper (Pumphrey 
and Rawdon-Smith, 1936 b) it was indicated that the threshold con- 
tinues to fall with increasing stimulus frequency (see also Pumphrey, 
1940). A continuous fall was observed by Antrum (1941). 

In any case, the tympanic organ is insensitive in the frequency range 
that is optimal for man and extends into the ultrasonic range. At its 
optimum the organ responds to a stimulus of about 7 x 10"^^ 
ergs/sec, about the same as for man, and thus is operating at the 
physical hmit. In contrast to the human ear, the tympanic organ of 
Orthoptera does not fatigue readily. No diminution in the response to 
a 2,000-c/s tone could be detected after continuous stimulation lasting 
one-half a minute (Pumphrey and Rawdon-Smith, 1936 c). 

Although the tympanic organs are not the only receptors possessed 
by Orthoptera (there are in addition hair sensilla and chordotonal 
organs not associated with tympana), it is clear that they are the 
principal, if not sole, receptors involved in detecting noises produced 
by stridulation of the same and other species. Since Orthoptera can 
discriminate among the various kinds of calls and can distinguish 
between some artificial and genuine calls (Regen, 1926), it is obvious 
that the tympanic organ does have some specialized characteristics. 

Songs of Acrididae are, on the whole, broad-band noises at 
2-12,000 c/s with maxima at 4,000-8,000 c/s and intensities of 
30-40 db, re 0-0002 dynes/sq. cm., at 10-30 cm. (Busnel, 1953 ; Haskell, 
1955; Loher and Broughton, 1955). The Tettigoniidae also produce 
wide-band noises at frequencies up to 100,000 c/s (maxima 8,000- 
15,000 c/s) and intensities of 46-70 db (Horror, 1954; Busnel, 1953; 
Busnel and Chavasse, 1950; Pasquinelly and Busnel, 1955; Pielemeier, 
1946 a, 1946 b; Pierce, 1948). Gryllidae produce relatively pure tones 
at 2,000-6,000 c/s and intensities of 40-60 db (Alexander, 1957; 
Busnel, 1955 a, 1955 b; Haskell, 1955; Pasquinelly and Busnel, 1955; 
Pierce, 1948). 

The songs can be described physically by five parameters: fre- 
quency, intensity, wave form, phase, and the temporal distribution 
of sound units (Frings and Frings, 1958). Successive units may be 



92 THE PHYSIOLOGY OF INSECT SENSES 

combined to form more complex arrangements, and this in turn 
further multipHed. 

The tympanic organ is sensitive to the entire frequency range of 
sounds produced by stridulation, but regardless of the frequency, the 
pattern of discharge in the tympanic nerve is asynchronous. From this 
it has been concluded that the organ is incapable of frequency discrim- 
ination, and this may indeed be so. On the other hand, there have been 
no recordings from single fibres in Orthoptera, and this should be done 
to clinch the argument, even though Pumphrey (1940) has argued on 
structural grounds that harmonic analysis, that is, different fibres 
responding to different stimulus frequencies, is impossible. The fact 
that no frequency discrimination has been observed in the moth 
tympanic organ, where the presence of only two fibres permits a precise 
analysis (Roeder and Treat, 1957), adds weight to the argument. It 
also supports the idea that there is no frequency pattern in the nerve 
mirroring the frequency pattern of the stimulus. On the other hand, 
it is possible that the insect itself may be able to analyse frequency to 
some degree by means of central interpretation of input from a 
number of organs each having a different frequency range (Katsuki 
and Suga, 1960; Suga and Katsuki, 1961). 

Pumphrey and Rawdon-Smith (1939) proposed that the tympanic 
organ, being sensitive to intensity, detected changes in intensity, that 
is, amplitude of the sound wave, and that the different sounds of 
insects differed most importantly by the periodic changes (modulation) 
in intensity of the sound. In other words, any sound wave of a fre- 
quency within the detectable frequency range was merely a carrier 
wave upon which was imposed a pattern of amplitude modulation. 
By contrast, the human ear is very sensitive to frequency changes in 
the carrier wave but relatively insensitive to changes of the modulation 
frequency. This hypothesis was supported by records showing that an 
organ stimulated by an amplitude-modulated sound discharged 
volleys of impulses at the modulation frequency of the stimulating 
sound. These results were confirmed in a number of species by Haskell 
(1956 b), and as he pointed out, it would be reasonable to assume that 
the different pulse rates found in the different songs of various species 
would be the parameter signalled by the receptors, and hence the key 
to the recognition of songs. Busnel (1955) and his co-workers (Busnel, 
Loher, and Pasquinelly, 1954), on the other hand, have suggested as a 
result of experiments in which natural and artificial songs were played 
to species of Chorthippus that the essential element in songs that aids 
discrimination is 'transients' (sudden changes in intensity). To test the 



SOUND RECEPTION 93 

latter hypothesis Haskell (1956 b) played the identical stimulus again 
and again to a tympanic organ and recorded the pattern of discharge 
from the tympanic nerve. He found that the resultant volleys of spikes, 
although synchronous with the pulse frequency of the stimulus, were 
variable in themselves and that this variability bore no simple relation- 
ship to any quality of the stimulus. On the basis of this evidence he 




Fig. 64. Sensitivity of an isolated tympanic organ of Locusta plotted on 
polar co-ordinates as a function of direction of incidence of the test 
stimulus. Sensitivity (log reciprocal of threshold amplitude) is plotted 
radially and the minimum sensitivity is arbitrarily taken to be zero. 
The line 0-180 degrees lies in the sagittal plane of the animal, and 
for angles of positive or negative sign the test stimulus is incident on 
the external or internal aspect of the tympanic organ respectively. 
(Redrawn from Pumphrey, 1940.) 

concluded that the characteristic of stridulation that permits inter- 
specific recognition is the pulse repetition of the songs. Many ques- 
tions about sound recognition remain to be answered, however, and 
Haskell's (1956 b) discussion should be consulted. 

One feature of the early field experiments that turned up repeatedly 
was the ability of the insects to locahze sound. Regen (1924), for 
example, showed that unmated females could orient from a distance 



94 THE PHYSIOLOGY OF INSECT SENSES 

of approximately 10 metres to a chirping male. A female's path of 
approach was nearly a straight line. Even with one tympanic organ 
destroyed, orientation was possible, although the line of approach 
now became more devious. These observations suggesting that the 
tympanic organ has directional characteristics are supported by 
experiments in which sensitivity was tested to a stimulus given 
successively at different directions of incidence (Pumphrey, 1940). A 
plot on polar co-ordinates of the sensitivity of an isolated tympanum 
o^ Locust a as a function of the direction of incidence of the stimulus 
illustrates the pattern of the directional characteristics (Fig. 64). This 
finding is in agreement with the assumption that the tympanic organ 
is a displacement rather than a pressure receiver (also Autrum, 1955 c) 
Also, as these experiments revealed, the tympanic organ responds 
equally well to 'push' and to 'pull'. 

Function - Lepidoptera 

Moths and butterflies also are known to be sensitive to sound (Stobbe, 
1911 ; Turner, 1914; Turner and Schwarz, 1914; Eggers, 1925, 1926 a, 
1928; Frings and Frings, 1956, 1957). Many of the sounds employed 
for testing in early experiments were non-specific (e.g., squeaks of a 
glass stopper twisted in a bottle), and the responses, too, were not 
always specific (e.g., partial erection of the antennae, folding of the 
wings, flexing of the antennae, running, or flying). It was difficult to 
know what kind of sounds to employ as test stimuli for the simple 
reason that no one knew what sounds moths responded to in nature. 
One of the earliest speculations regarding the normal role of sound 
perception in behaviour was the suggestion of White (1877) to the 
effect that auditory receptors, in moths specifically, might assist in 
detecting the approach of insectivorous bats. This idea gained plaus- 
ibility from a number of field and laboratory observations (Schaller 
andTimm, 1950; Webb, 1953; Treat, 1955), and was finally established 
on a firm experimental basis by Roeder and Treat (1957, 1961 a, 
1961 b). 

The principal sound receiver is the tympanic organ. The sensitivity 
of this organ in noctuids to air-borne sounds was demonstrated by 
Eggers (1925, 1926 a, 1928), first confirmed by the behavioural studies 
of Schaller and Timm (1950) and of Treat (1955), and ultimately by 
electrophysiological techniques. Other sound receptors must exist 
because, as is true with Orthoptera, there is still a residual response to 
intense sound after destruction of both tympanic organs (Stobbe, 
1911; Eggers, 1925; Treat, 1955; Frings and Frings, 1957). Further- 



SOUND RECEPTION 95 

more, species in which tympanic organs are not known to occur on 
the body are somewhat sensitive to sound. For example, the satyrid 
butterfly Cercyonis pegala responds to air-borne sounds of high 
intensity (100-1 10 db). It should be remembered, however, that there 
exist on the ventral surface of the basis of the wings of this insect 
chordotonal sensilla associated with minute tympanic membranes 
(Vogel, 1912), and some people have tendered the suggestion that 
sound reception by these organs is possible (Vogel, 1912; Pringle, 
1957). 

The tympanic organ is sensitive to very high sound frequencies. Res- 
ponses in the frequency range 3,000-20,000 c/s have been recorded 
from the tympanic nerves of the moths Phalera bucephala (Notodon- 
tidae) and Arctia caja (Arctiidae) (Haskell and Belton, 1956). The very 
thorough investigations of Roeder and Treat (1957, 1959, 1961a, 
1961b) with a number of noctuids have shown that the sensitivity 
extends up to stimulus frequencies of 100,000 c/s. These investigations 
have also revealed many of the characteristics of these organs. A rest- 
ing discharge occurs at the ordinary noise level of the laboratory. It 



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lAAAAAAAAAAAAAAAAAAAAAAAAAAA 

Fig. 65. Tympanic nerve activity in the noctuid Prodenia eridania. A, 
activity in the tympanic nerve at laboratory noise level. The large spike 
belongs to the non-acoustic unit. B, response in one acoustic unit to 
continuous sound of 70 kc/s. C, response in both acoustic units to 
30 kc/s. Time marks, 100 c/s. (Courtesy of Roeder and Treat.) 



C/5 <U k> 

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SOUND RECEPTION 97 

takes the form of a series of discharges of a large spike at a steady 
frequency of 5-20 per second. Haskell and Belton (1 956) believed these 
to be motor discharges, but in Rocder's and Treat's preparation they 
were clearly afferent. In addition, two species of small spikes discharge 
randomly, in all probability, as a result of low-level random noise in the 
laboratory. These two spikes represent the acoustic units of the 
tympanic organ; the large spike is a non-acoustic unit whose function 
is not clearly understood (Fig. 65). 

Both acoustic units respond to sound by a high-frequency discharge 
which shows no change with stimulus frequency. The two differ only 
in their threshold. For both, the greatest sensitivity lies between 
15,000 and 60,000 c/s. In response to a click, with many transients, or 
a short pulse (0-02-1 msec.) of pure sound at threshold, the more 
sensitive fibre responds after a latency of 3-5 msec, with one spike 
(Fig. 66). When the stimulus intensity is increased, the latency de- 
creases and there is an after-discharge of two-three spikes at a fre- 
quency of 700 per second. A further increase in stimulus intensity 
brings in the second acoustic unit. The variety of overlap observed 
indicates that there is no regular alternation of activity or coupling of 
the units. Although one cannot state categorically that only two units 
are firing, this appears to be the case. It fits well with the histological 
facts. 

Contrary to the situation found in orthopteran tympana, these 
organs adapt rapidly. From an initial frequency of about 1,000 spikes 
per second the discharge drops to 50 per cent of this value in the first 
0- 1 second and to 25 per cent by the end of the second. 

Various operations on the tympanic organ prove that the effects 
observed electrophysiologically are truly indicative of activity in the 
two chordotonal sensilla. Touching the sensilla or disengaging them 
from the tympanic membrane terminates their activity. On the other 
hand, tearing the membrane or opening the air sac behind it fails to 
alter the response significantly. Occluding the external tympanic recess 
narrows the band of frequency reception to its middle range and raises 
the threshold. 

These experiments are in agreement with the idea that this organ is a 
displacement-sensitive receiver. They show that the tympanum must 
be free to vibrate but that uniformly distributed elastic tension is not 
necessary. The direction of the displacement, in so far as the sensillum 
is concerned, is apparently not critical, since in many noctuids the axis 
of the sensillum is not normal to the plane of the tympanic membrane ; 
instead, it forms an acute angle with it. 



98 THE PHYSIOLOGY OF INSECT SENSES 

The function of the non-acoustic unit may be proprioceptive. If the 
acoustic sensilla are rendered inoperative resting activity may be re- 
corded from the non-acoustic unit alone, but only so long as the 
attachment to that structure known as the Bugel is intact (Fig. 57). In 
this region is located a single Type II neuron (Treat and Roeder, 1959). 
The rate of discharge of this unit changes as various portions of the 
tympanic frame are distorted, as they would be during flight or as a 
result of activity of the two tympanic muscles (Fig. 56). 

The fact that the moth tympanic organ exhibits after-discharge, a 
form of physiological amplification for stimuli of short duration, and 
rapid adaptation fits it very well for the reception of short, rapid bursts 
of sound of the sort given off by hunting bats. Furthermore, its maxi- 




FiG. 67. Polar plot of the distances at which a 1-msec. click of fixed intensity 
elicits the same response from the right tympanic organ when placed 
at various angles relative to the median axis of the moth (0-1 80 degrees). 
The moth was headed towards degree and inclined upward at about 
30 degrees to the plane of measurements. Distances in metres from the 
moth are indicated on the 90-270-degree line. Open circles and solid 
line, Acronycta; broken line, Gmphip/iora; solid circles and solid line, 
Lucania. (Redrawn from Roeder and Treat, 1961.) 



PLATE I. The cry of a Hying bat (Myotis) recorded by a Granith microphone 
(upper trace) and the acoustic cells of the noctuid moth AK'ropcrina 
diibitans (lower trace). Time mari<, 10 msec. Made in collaboration 
with Dr Fred Webster. (Courtesy of Roeder and Treat.) 




PLATE II. Triply innervated chemosensory hair of Phormia (pig- 
ment layer omitted). HY, hypodermis; DF, distal fibres 
(dendrites); PF, proximal fibres (axons); N, neuron cell 
bodies; TR, trichogen; TO, tormogen; d, thin-walled 
cavity; C2, thick-walled cavity; VA, vacuole; TA, tracheole; 
SP, sensory papilla. (From Dethier, 1955.) 




m 



PLATE III. Electron-micrograph of the 
tip of a tarsal contact chemo- 
receptor of Stomoxys calcitrans 
(X 20,000). (Courtesy of J. R. 
Adams.) 




PLATE IV. Photomicrographs of images of newsprint formed by the corneal 
lens of ocelli of the caterpillar Isia Isabella, ex is seen through a unitary 
type cornea; x, through a tripartite type. (From Dethier, 1942.) 



SOUND RECEPTION 99 

mum sensitivity is in the range ( 1 5,000-60,000 c/s) corresponding to the 
predominant frequencies in the cries of flying bats of the family 
VespertiHonidae (Griffin, 1950, 1953). Actual tests in which electrical 
recordings were made from tympanic organs in the presence of bat 
cries prove beyond all doubt that the organs could be used for detect- 
ing these predators (Roeder and Treat, 1957) (PI. 1). Behavioural 
studies (Roeder and Treat, 1961 a, 1961 b) have shown that free-flying 
moths take evasive action when they are stimulated by bat cries. This 
is random action, at least when the bat is near, in that it bears no par- 
ticular relation to the flight path of the bat. 

Like the tympanic organ of Orthoptera, the organs of moths are 
directional receivers (Roeder and Treat, 1961 a). Localization is 
theoretically possible with one, but is obviously more efficient with 
two. At low sound intensities, that is, when the bat is not too near, 
there is a differential response from the two organs, but as the intensity 
increases, when the bat would be close, the differential nature of the 
binaural response disappears (Roeder and Treat, 1961b) (Fig. 67). 

Another role of the tympanic organ may be concerned with navi- 
gation during flight. It has been suggested (Hinton, 1955) that some 
moths may orient themselves by echo-location. Although no experi- 
mental proof exists, there is direct evidence that moths can detect the 
sounds of a flying moth and presumably those of their own flying 
(Roeder and Treat, 1957). This evidence suggests that moths might be 
able to detect the reflection of their own flight sounds from nearby 
objects, and hence to echo-locate. For this to succeed, however, numer- 
ous obstacles would have to be overcome, not the least of which would 
be the ability to distinguish between direct and reflected flight sounds. 

Function - Hemiptera 

Little is known about the tympanic organs of this Order. Males of the 
waterboatman, Corixa, stridulate. Females respond to the chirping, 
and other males chirp in chorus as long as the tympanic organs are 
intact (Schaller, 1951). These are the only insects for which a sensitivity 
to water-borne sound has been demonstrated. 

HAIRS AS SOUND RECEPTORS 

Many insects that lack tympanic organs are sensitive to sound waves in 
air. As early as 1779, Bonnet recorded that caterpillars respond to 
sound by thrashing about of the anterior portion of the body. Since 
that time many naturalists have recorded this phenomenon, a response 
brought about by convulsive contractions of the longitudinal muscles 



100 THE PHYSIOLOGY OF INSECT SENSES 

in the anterior trunk. Some species respond by a complete cessation of 
movement, a 'freezing'; some respond by 'freezing* followed by 
thrashing. The response probably serves as a protective device. It re- 
mained to Minnich (1925, 1936, 1937) to attempt a physiological 
investigation of the response. He studied seven species of butterfly 
larvae and eight species of moth larvae, bringing to a total of twenty- 
eight the number of lepidopterous larvae known up to that time to be 
sensitive to sound. It is likely that all caterpillars detect sound. The 
range of frequency sensitivity extends from 32 to 1,000 c/s. By cutting 
larvae into fragments and noting that the fragments responded, 
Minnich showed that the receptors for sound were diffusely distributed 
throughout the body. 

Early experiments were confined to relatively hairy species, and in 
these the responses to sound were abolished when the hairs were 
loaded with flour dust or droplets of water. Upon removal of the dust 
or water, responsiveness returned. A steady stream of air directed 
against the hairs inhibited response. These experiments support 
strongly the idea that the hairs are the sound receptors. On the other 
hand, similar behavioural responses to sound were obtained with 
'hairless' species. Although even these species possess minute setae, 
Minnich (1936) entertained doubts that sound reception here was in- 
deed mediated by hairs. The question is still open. 

In the belief that the sensory hairs of the hirsute caterpillars were 
resonant structures, that is, that different lengths and sizes would reso- 
nate to different frequencies of stimulus, Minnich (1936) attempted to 
fatigue the response to one frequency and test for a response to 
another. He found, in fact, that fatiguing at low frequency inhibited 
responses to all higher frequencies, but that the reverse was not true. 
As Pumphrey (1940) pointed out, these results are inconsistent with a 
hypothesis of reaction by resonance. He pointed out further that the 
results obtained in the experiments on fatiguing are explicable on the 
grounds that low-frequency stimuU will be much louder to the animal 
than those of equal intensity but higher frequency and would therefore 
probably have a greater fatiguing effect. This interpretation is based on 
a study of action potentials recorded from cereal hairs of cricket and 
cockroaches (Pumphrey and Rawdon-Smith, 1936 a, 1936 b, 1936 c). 

The cerci of cockroaches and Gryllus and many other Orthoptera 
are clothed with extremely delicate, long, lightly hinged hairs (Sihler, 
1924). They are typical sensilla trichodea. In Periplaneta americana 
there are several hundred on each cercus. Each hair is about 0-5 mm. 
long and i 0-005 mm. in diameter. They move visibly to light puff's of 



SOUND RECEPTION 101 

air and to sounds of adequate intensity over a wide frequency range; 
that is, the response is not resonance. As Pumphrey and Rawdon- 
Smith(1936a, 1936b, 1936c) showed, these hairs are pure displacement 
receptors sensitive up to about 3,000 c/s. Threshold measurements over 




Frequency Q^/sec) 

Fig. 68. Experimentally determined thresholds of the cercus of Gryllus 
for pure tones at various frequencies (solid circles). The heavy line 
represents a constant displacement amplitude of 560 A. The light line 
represents the human threshold of hearing from Wegel's data. 
(Redrawn from Pumphrey, 1940.) 



the frequency range 50 c/s to + 1 ,000 c/s (Fig. 69) reveal that the res- 
ponse is to a constant displacement amplitude of 560 A. (Pumphrey, 
1940). If the hair acts as a rigid lever this finding suggests that 
the threshold displacement of the dendrite at the base of the hair 
cannot greatly exceed 0-5 A. Pumphrey (1940) suggested that the 



102 THE PHYSIOLOGY OF INSECT SENSES 

'spontaneous' activity recorded from nerves in silent surroundings 
may represent random movement of the dendrites by Brownian 
agitation of the molecules in their vicinity. Conditions are similar for 
the cricket and the cockroach. 

In contrast to the tympanic organ, the cereal hairs exhibit a number 
of characteristics seen in recordings from the mammalian cochlear 
nerve. One of these is synchronization. At low stimulus frequencies 
the action potentials in the nerve are exactly synchronized with the 
stimulus. At the low end of the frequency range the nerve may be 
synchronized or show what Pumphrey and Rawdon-Smith (1936 a, 
1936 b, 1936 c) term 'frequency doubling'. At high frequencies it may 
show frequency halving or quartering. Thus, at a stimulus frequency 
of 400 c/s the nerve may discharge at 400 c/s or at 800 c/s, and at a 
stimulus frequency of 400 c/s, fire at 300 or 150 c/s. In the 400 c/s 
range of stimulation the nerve that is firing in synchrony may begin 
halving if the intensity of the stimulus is reduced by about 10 db. 
Pumphrey and Rawdon-Smith (1936 c) suggested that these phe- 
nomena may exemplify the condition known as 'alternation'. In the 
mammalian Vlllth nerve the synchrony in the whole nerve at high 
stimulus frequencies is believed to result from each fibre firing to 
alternate sound waves and the different fibre groups being 180 degrees 
out of phase. In the cereal nerve the alteration is diff'erent in that all 
fibres fire to every other sound wave but all are in phase, that is, the 
whole nerve alternates, hence, the response frequency is halved or 
quartered. It was suggested, however, that true alternation of the 
mammalian type also occurs, at least during the first fraction of a 
second of response, when the nerve momentarily fires at 600-800 c/s. 
At higher stimulus frequencies the nerve responds asynchronously. 

Another resemblance to the mammahan Vlllth nerve is the occur- 
rence of equilibration, that is, a decline with time in the amplitude of 
massed spikes in the nerve. This phenomenon is interpreted as a 
reduction in the number of impulses at each sound wave with time as 
the result of the lengthening of the relative refractory period of each 
fibre. 

Electrophysiological studies of the cereal sensilla of a number of 
Acrididae are in general agreement with the results just described; 
however, no clear evidence of equilibration or frequency halving or 
doubling was obtained (Haskell, 1956 a, 1956 b). 

Hairs on other parts of the body, especially of Orthoptera, are 
believed also to be receptors sensitive to air-borne sound waves, but 
the evidence is not always convincing, because it is derived primarily 



SOUND RECEPTION 103 

from electrophysiological records of activity in segmental nerves 
known to carry fibres from other types of sensilla, particularly chordo- 
tonal sensilla. Pumphrey and Rawdon-Smith (1936 c), studying the 
locust, believed that the responses originated in trichoid sensilla. Later 
Pumphrey (1940) suggested that the segmental chordotonal organs 
were perhaps involved (see also Hughes, 1952). Working with a num- 
ber of acridid species, Haskell (1956 a) inclined to the view that res- 
ponses did indeed emanate from hairs because smearing the abdomen 
with vaseHne abolished the response. In any event, the receptors 
involved fired asynchronously at all stimulus frequencies and required 
high stimulus intensities (+ 7 dynes/sq. cm.). Even after smearing with 
vaseline, however, a residual sensitivity to sound occurred, and 
Haskell (1956 a) suggested that in this instance the chordotonal organs 
might be involved. Other sensilla on the abdomen of grasshoppers, 
presumed to be sensitive to vibrations of the substrate, will be dis- 
cussed later. 

Little is known about the functions of hair sensilla sensitive to 
sound. It is unlikely that those in Orthoptera are concerned with 
reception of noises produced by stridulation (Haskell, 1952 a). In the 
cockroach stimulation of cereal hairs with a puff of air evokes the 
'evasion response'. This kind of response is not well developed in 
locusts. In Orthoptera in general mechanical stimulation of the cerci 
seems to be of great importance during copulation, and perhaps this 
is the principal role of cereal hairs. 

Hairs most highly developed for the reception of air-borne sounds 
differ in performance from tympanic organs in several respects : they 
respond over much lower frequency ranges; they respond synchro- 
nously with stimulus frequency over certain ranges and thus do 
exhibit a limited frequency discrimination; they fatigue fairly rapidly; 
they tend to equilibrate. Like tympanic organs, however, they are 
displacement receivers. 

THE JOHNSTON'S ORGAN OF CULICIDAE 

In the males of Culicidae and Chironomidae the Johnston's organ 
attains an extraordinary complexity manifested by such an enormous 
multiplication of sensilla that the pedicel is bulbous and a special 
internal cuticular framework has developed to serve as points of 
attachment for the many sensilla. This exceptional organ is demons- 
trably able to be stimulated by air-borne sound waves as Johnston 
(1855) and Child (1894) originally surmised. 
When Mayer (1874) demonstrated that the hair (or fibrillae) 

H 



104 THE PHYSIOLOGY OF INSECT SENSES 

comprising the whorls on the antennae of male Culex vibrated in the 
presence of a vibrating tuning fork he did not indeed prove, as many 
authors have pointed out (e.g., Fulton, 1928), that the antennae are 
auditory organs. Nor did his experiments impHcate the Johnston's 
organ. Furthermore, since the different forks employed gave different 
intensities, and hence stimulus energy could not be controlled, the fact 
that the hairs vibrated most extensively at 512 c/s is not especially 
significant. In an experiment with Culex pipiens pallens in which 
intensity was controlled, Yagi and Taguti (1941) found that the hairs 
which vibrated in the stimulus frequency range of 193-870 c/s vibrated 
most widely at 217 c/s. As Mayer had shown, maximum vibration 
occurs when the sound wave advances at right angles to the longi- 
tudinal axis of the hairs. 

The literature is replete with accounts of mosquitoes reacting to 
sound. In a most extensive study Roth (1948) found that males of 
Aedes aegypti respond to the sound of a flying female and to artificial 
sounds of comparable frequencies by orienting to the source of sound 
and displaying the mating response, which consists of seizing and 
clasping. To sounds of other frequencies they: rub the antennae with 
the forelegs, rub the hind legs together, rub the abdomen or wings with 
the hind legs, jerk the body, suddenly fly, or suddenly become 
immobile. 

The frequencies which induce the mating response are different 
for males of different ages. The effective range extends from about 
100 to about 800 c/s, and the spectrum is narrower for non- virgin 
males. For virgin and non-virgin alike the effective band widens with 
age. This shift to higher frequencies has been correlated with the ex- 
tension of the antennal fibrillae. When males first emerge, the hairs or 
fibrillae He recumbent along the shaft of the flagellum. By 48 hours 
they are fully extended. This correlation suggests either that the apical 
fibrillae vibrate at higher stimulus frequencies than the lower or that 
a larger total of fibrillae must be set in motion at higher stimulus 
frequencies in order to mediate a response. 

Males can be adapted to one frequency (as judged behaviourally) 
and still retain responsiveness to other frequencies (Roth, 1948). Since 
intensities were not controlled in these experiments, the significance is 
in doubt. With minor deviations the same story holds for Anopheles 
quadrimaculatus, Culex pipiens, and Psorophora confinnis. 

The correlation between the degree of extension of antennal fibrillae 
and the extension of responses to higher stimulus frequency suggests 
that the fibrillae are concerned with sound reception ; however, they 



SOUND RECEPTION 105 

are not innervated in mosquitoes. Early workers postulated that the 
vibrating fibrillae acted as mechanical amplifiers which set the flagellar 
shaft in vibration. The movement of the shaft with respect to the 
pedicel was presumed to be detected by Johnston's organ. In an 
extensive series of experiments with Aedes aegypti Roth (1948) ob- 
tained results that confirmed this hypothesis. The mating response of 
males to sound is abolished by completely removing the flagellum, 
joining the flagellum rigidly to the pedicel with shellac, or weighting 
the tips of the antennae with large beads of shellac. In all cases res- 
ponsiveness returns when the shellac is removed. When the fibrillae 
are removed from the antennae greater intensities of sound are re- 
quired in order to elicit responses. 

Although no electrophysiological studies of the Johnston's organ 
of mosquitoes have yet been reported, these experiments of Roth, 
taken in conjunction with Burkhardt's electrophysiological analysis of 
the Johnston's organ of Calliphora, establish beyond reasonable doubt 
that this organ in Culicidae is indeed adapted to respond to air-borne 
sound waves. 

PERCEPTION OF VIBRATIONS IN SOLIDS 

It had been suspected for many decades that insects were sensitive to 
vibrations in solids because they gave clear behavioural responses 
when the substrate upon which they were standing or walking was 
subjected to this form of motion. No very meaningful experiments 
were performed, however, prior to the introduction of electro- 
physiological methods of analysis. By recording from leg and seg- 
mental nerves it has now been possible to demonstrate that there are 
rather specific responses by some insects to vibration. A few clues as 
to the identity of the sensilla involved have been obtained. 

The two types of sensilla suited to the task are trichoid sensilla and 
chordotonal sensilla. It is to be expected that those parts of the body 
immediately in contact with the substrate, that is, the legs and abdo- 
men, would be especially equipped with the requisite organs ; however, 
aside from a few experiments showing that in Locusta there are hairs on 
the sternites which mediate responses to vibrations of the substrate 
(Haskell, 1956 a), there is no extensive work on areas of the body other 
than the legs. 

The legs certainly possess elaborate sensory equipment. In addition 
to trichoid sensilla they invariably possess numbers of chordotonal 
sensilla (Eggers, 1928; Debaisieux, 1935, 1938). Generally the legs 
contain chordotonal organs at four locations ; the femur, the proximal 



106 THE PHYSIOLOGY OF INSECT SENSES 

tibia (the subgenual organs), the distal tibia, the tarsus-pretarsus. The 
degree to which the organs are developed varies from Order to Order 
and species to species. The number of sensilla in a group varies from 
one to two hundred or three hundred. Each group, with the exception 
of the subgenual organ, is associated with an articulation of the leg. In 
the subgenual region there may be one or two concentrations of sen- 
silla or none at all. The true subgenual organ lies immediately distal to 
the femur-tibia articulation. When a second group of sensilla occurs, 
it lies distal to the true subgenual organ. True subgenual organs have 
not been found in the thysanuran Machilis, the beetle Rliagonycha, or 
in Diptera, Heteroptera, Homoptera, and Neuropterpodea. Even the 
more distal organ is absent in Machilis, Rhagonycha, and Diptera 
(Debaisieux, 1938). 

Subgenual organs are unusually diverse in structure, shape, and 
numbers of component sensilla. They are most highly developed in 
Orthoptera, Hymenoptera, and Lepidoptera and take the form of 
cones, or sails, or fans. They are unique in that they more or less 
completely occlude the dorsal blood sinus of the leg (Figs. 47, 56). At 
the same time they lie in close proximity to the main tracheal trunk. 
They are innervated by a branch of the leg nerve or, in the case of 
insects possessing a tibial tympanic organ, by a branch of the tympanic 
nerve and a branch of the leg nerve combined. They are supported 
proximally by their nerves and distally by accessory cells which form a 
ligament attached most often to the cuticula of the leg. Standard 
chordotonal sensilla comprise the sensory elements. In number they 
range from ten to forty. Extensive descriptions of these organs have 
been given by Schwabe (1906), Schon (1911), Eggers (1928), and 
Debaisieux (1935, 1938). 

It has not been easy to ascertain just which of the many sense organs 
in the legs mediate responses to vibrations of the substrate. The most 
extensive experiments have been those of Autrum (1942, 1943), 
Antrum and Schneider (1948), and Schneider (1950). Data are based 
upon electrophysiological recordings of total activity in leg nerves 
while the preparation was 'standing' on a metal plate which was set into 
sinusoidal oscillations of measurable amplitude (Autrum, 1941). 
Tests were conducted with Orthoptera, Lepidoptera, Hymenoptera, 
and Coleoptera. In many, the prothoracic legs are the least sensitive; 
the mesothoracic, the most. 

All of the insects tested fall roughly into two groups as regards 
sensitivity. In the less-sensitive group are the beetles, Carabus, Silpha, 
Pterostrichus, and the Hymenoptera, Vespa and Bombus, The more 



SOUND RECEPTION 



07 



100,000 



10.000 — 



1000 



100 



I- 




001 — 



0001 



50 100 200 400 800 1.000 2,000 4000 8,000 

Cycles per Second 

Fig. 69. Vibration thresholds in my. (ordinate) in relation to frequency 
(abscissa) for insects representing three levels of sensitivity. (Redrawn 
from Antrum and Schneider, 1948.) 



sensitive forms include the beetles Geotrupes and Melolontha, the 
butterfly Pyrameis, the cockroach Periplaneta, and the cricket 
Liogryllus (Autrum and Schneider, 1948; Schneider, 1950). In the 
insensitive group there are responses to stimulus frequencies ranging 



108 THE PHYSIOLOGY OF INSECT SENSES 

from 50 to about 1,000 c/s; in the sensitive group, up to 8,000 c/s. In 
both groups the threshold drops with increasing stimulus frequency; 
however, in the sensitive group it shows a minimum in the 1,000 c/s 
band of the frequency spectrum (Fig. 69). The rise in threshold at 
higher frequencies following the minimum may be an artefact 
(Antrum and Schneider, 1948; Schneider, 1950). The smallest meas- 
ured amplitude that causes any response (middle leg of Decticus at a 
stimulus frequency of 2,000 c/s) is 0'36A, a distance equal to about 
one-third the diameter of the hydrogen atom. From this it follows 
that the sense organs involved are developed to the physical limit, but 
the minimum energy required is greater than the energy content of the 
unitary elemental process (i.e., collision of one molecule) of which the 
stimulus consists (Antrum, 1943). 

Threshold can be recorded either as amplitude or in terms of 
acceleration. The acceleration b which a substrate vibrating sinusoid- 
ally imparts to an object lying on it is given by the expression —a-cxi^ 
sin out (maximum aoj ^) in which a is the amplitude and w (= lirv) is the 
angular frequency. A comparison of the thresholds as accelerations 
of the two groups of insects, sensitive and insensitive, shows that a 
different range of acceleration is necessary for each group. For the 
sensitive group it ranges from 2- 10~^* to \0~^g{g = 981 cm. sec. 2); for 
the insensitive group, from S-IO"^ to g). On the other hand, for a 
given insect threshold acceleration is more nearly constant over the 
range of stimulating frequencies than is threshold amplitude. For 
this and other reasons Antrum and Schneider (1948) and Schneider 
(1950) felt that acceleration was the crucial physical parameter to 
which the sense organs respond and that regardless of the stimulus 
frequency the organs must undergo equally large accelerations. 

There is only indirect evidence as to which of the several organs in 
the leg are actually responding to the vibrations. Of the species 
studied by Antrum and Schneider (1948), the least sensitive of those in 
the insensitive group lack true subgenual organs, while the sensitive 
species possess them. When an operation designed to destroy sub- 
genual organs was performed on those species possessing them the 
threshold of response to vibration rose and the effective frequency 
band became narrow so that these sensitive insects now resembled 
insensitive ones (Antrum, 1941). 

From these experiments it was concluded that the sensitive insects 
possessed an organ especially adapted to detect vibrations in the 
substrate and that this organ was the subgenual collection of chordo- 
tonal sensilla. The insensitive insects, on the other hand, were pre- 



SOUND RECEPTION 109 

sumed to be reacting primarily to stimuli outside the normal biological 
range and doing so through the agency of organs not finely adapted for 
this function. Coating the legs with paraffin did not abolish the res- 
ponse so it is unlikely that hairs or spines mediate the response. As 
already pointed out, other chordotonal organs in the leg are associated 
with articulations. The articulations are also equipped with hair plates. 
Either of these groups could be concerned. Whichever types they are, 
it is probably the tarsal ones that are important in perception, since 
response to vibration is lost following amputation of the tarsi (Antrum 
and Schneider, 1948). 

In flies (CalUphora and Eristalis), which are among the least sensi- 
tive insects, there is no subgenual organ of any sort. Responses are 
probably mediated through a tibial chordotonal organ which con- 
sists of three sensilla (Schneider, 1950). The upper frequency limit of 
this organ is about 100/cs. At frequencies up to this, the discharge in 
the nerve is synchronized with the stimulus. At higher frequencies it 
is asynchronous. 

Antrum and Schneider (1948) decided that sensitivity is connected 
with the anatomical structure of the subgenual organs. Where these 
are fan-shaped, thresholds are low (e.g., Orthoptera); where they are 
conical and compactly constructed (e.g., Hymenoptera), thresholds 
are higher. On the other hand, the beetles Geotrupes and Melolontha, 
which lack true subgenual organs, are very sensitive to frequencies be- 
tween 600 and 1,000 c/s and 600 and 1,500 c/s respectively and still are 
responsive to 4,000 and 8,000 c/s respectively (Schneider, 1950). 
Recordings obtained following successive amputations of lengths of 
leg suggest that the receptors are the ten chordotonal sensilla in the 
distal end of the tibia. In any case, sensitivity does not depend upon 
the number of sensilla. Camponotus sp? with a subgenual organ 
containing about twenty sensilla is as sensitive as Apis with about 
forty. 

The curious anatomical position of the subgenual organ with res- 
pect to the blood sinus of the leg invites speculation about the func- 
tional association of this organ with the blood. Work with a model has 
shown that vibrations would establish vortices in the blood such that 
a rather constant pressure would be applied to the outer surface of the 
subgenual organ (Antrum, 1942). It has been postulated that the effect 
is a rectifying one and that it serves to permit the nerve to transmit 
frequencies higher than the 200-500 c/s that represent the top limit 
permitted by the refractory period of nerves (Antrum, 1942; Antrum 
and Schneider, 1948). While it is possible that vibrations act indirectly 



110 THE PHYSIOLOGY OF INSECT SENSES 

by means of disturbances in the blood, the argument that it is necessary 
in order to permit the organ to respond to higher stimulus frequencies 
is not valid. For example, alternation of firing in the various fibres, as 
in the cereal hairs, would accomplish the same purpose. 



5 10 




100 



300 400 



4000 6000 8.000 



600 800 1000 1.500 2,000 2.500 

Cycles per Second 

Fig. 70. Comparisons of the vibration thresholds of flies (O 

men (O O), bullfinches (• •), bees (• • ) 

cockroaches (C €). (Redrawn from Schneider, 1950.) 



•O), 
and 



Those who would consider sensitivity to vibrations in solids a 
separate sense, compare the abilities of man, birds, and insects (the 
only animals for which threshold values are known) in this respect and 
find insects to be the most as well as the least sensitive. The cockroach 
at its optimum range is more sensitive by a factor of 10,000 than the 



SOUND RECEPTION 111 

bird which in turn is more sensitive than man (Schneider, 1950). 
Flies are among the least-sensitive animals (Fig. 70). 

Pure vibrations at these high frequencies do not generally occur in 
nature, but such high frequencies undoubtedly exist as transients in 
the single pulse-hke vibrations of the substrate to which insects are 
ordinarily exposed. Suddenness is the important factor, so perception 
of these transients, even without frequency discrimination, may be 
the contribution which the subgenual organs make to behaviour 
(Autrum, 1959). 



CHAPTER V 



Chemoreception 



The accomplishment of many sexual, reproductive, social, and feeding 
activities of insects depends to a great extent upon the detection and 
assessment of specific chemical aspects of the environment. With the 
exception of feeding, where most of the chemical energy of the stimu- 
lating materials is utilized for purposes remote from the activity of the 
sense organ, the energy of compounds eliciting the other behaviour 
patterns serves merely to trigger excitation in receptors. 

These receptors are not chemosensitive simply because of fortuitous 
anatomical location, or exposure to the environment, or the possess- 
ion of permeable coverings (Dethier, 1962). On the contrary, they are 
inherently highly specialized and specific. Because of their specificity it 
v^ould probably be more meaningful to speak of salt, sugar, or sex- 
attractant receptors than of olfactory and contact chemoreceptors ; 
however, since our knowledge of their physiology is still fragmentary, 
the two broad but ambiguous categories are still convenient (cf. 
Dethier and Chadwick, 1948 a). 

It was postulated long before being demonstrated that chemo- 
receptors generated impulses as did other receptors. There is nothing 
unique about this part of the train of events initiated by stimulation. 
At the opposite end of the train, a beginning is being made towards an 
understanding of the behavioural correlates (cf., e.g., Dethier, 1957). 
The great unknown now is the basis of specificity and the nature of the 
transducing mechanism (Dethier, 1956, 1962). 

THE RECEPTORS 

The identification of chemoreceptors (whose nature is never so obvious 
as that of photoreceptors and sound receptors) has probably been 
retarded more than that of any other sense modality by the tendency to 
assign the function of chemoreception to all sensilla whose structure 
conforms to some postulated norm. There is, therefore, a voluminous 
literature on the structure of chemoreceptors real and supposed (for 
detailed reviews consult Kraepelin, 1833; Rohler, 1906; Forel, 1908; 
Mclndoo, 1914 a, 1914 b; von Frisch, 1921; Minnich, 1929 a; Mar- 
shall, 1935; Dethier and Chadwick, 1948 a; Dethier, 1953). 

112 



CHEMORECEPTION 113 

By observing the responses of insects (from which various append- 
ages or parts thereof have been extirpated) to food, naturally occurring 
attractants, and odours to which they have been conditioned, it has 
been established that the principal sites of chemoreceptors are: 
antennae, maxillary and labial palpi or their homologues, legs, and 
ovipositors. Since all of these areas contain a large and heterogeneous 
population of sensilla, the assignment of a chemoreceptive function to 
specific ones has been an arduous and uncertain task (cf. Dostal, 1 958 ; 
Schneider, 1961). Thus, despite extensive histological studies from 
those of Hauser (1880), Schenk (1903), and Vogel (1923 b) to the 
present time, the identity of chemoreceptors is known in fewer than a 
score of cases. 

Olfactory Receptors 

An olfactory function has been assigned to the following receptor types 
with a fair degree of certainty : in the honeybee, sensilla placodea (von 
Frisch, 1921; Dostal, 1958), sensilla basiconica, and possibly sensilla 
coeloconica (Dostal, 1958); in the dung beetles, Geotrupes sylvaticus, 
G. vernalis, Necrophorus tomentosus, N. vespilloides, Silpha novebor- 
acensis, and S. americana, sensilla basiconica (Warnke, 1931, 1934; 
Dethier, 1947 a) ; in lepidopterous larvae, sensilla basiconica (Dethier, 
1941; Morita and Yamashita, 1961); in the human louse, sensilla 
basiconica (Wigglesworth, 1941); in housefly larvae, sensilla basi- 
conica (Bolwig, 1946); in Drosophila, sensilla basiconica (Begg and 
Hogben, 1946); in Phormia regina, sensilla basiconica (Dethier, 
unpublished) ; in saturniid moths, probably sensilla trichodea, sensilla 
basiconica, sensilla coeloconica (Schneider, 1961) ; in the grasshoppers 
Melanoplus differentialis and Romalea microptera, sensilla basiconica 
and sensilla coeloconica (Slifer, 1961). 

The saUent features of sensilla placodea as seen with the light 
microscope are illustrated in Fig. 11. Details of structure have been 
clarified by the electron-microscopic studies of Richards (1951) and 
Slifer (1961). The sensillum is essentially a thin circular or oval plate 
connected to the surrounding cuticle by a delicate circumferential 
membrane and equipped with twelve to eighteen bipolar neurons 
(Vogel, 1921, 1923 b). Each dendrite possesses one or two minute 
refringent bodies of unknown function, the Riechstabschen (Vogel, 
1923 b). Furthermore, each dendrite ends in a cilium-like structure 
(Slifer, 1961) similar to that described in tympanic organs. From each 
cilium-like structure there extends a fibrous strand. The strands termi- 
nate on the extreme edge of the plate (Slifer, 1961). The antenna of a 



114 THE PHYSIOLOGY OF INSECT SENSES 

honeybee possesses from 3,000 to 30,000 sensilla placodea (Schenk, 
1903; Mclndoo, 1914b; Vogel, 1923 b; Melin, 1941 ; Kuwabara and 
Takeda, 1956; Dostal, 1958). Although the behavioural experiments 
of von Frisch (1921) and Dostal (1958) support the idea that these 
sensilla are olfactory, it is still difficult to comprehend in what way 
their structure is particularly suited to chemoreception (see also 
Snodgrass, 1935; Slifer, 1961). 

Sensilla basiconica are so variable in size, shape, and number of 
neurons that a general description is meaningless. Extensive electron- 





FiG. 71. Diagram of a thin- walled sensillum basiconicum from a grass- 
hopper antenna. A, section through a perforation showing finger-like 
processes of dendrite ; B, small portion of scolopoid sheath showing the 
dendritic processes passing through; C, longitudinal section of peg 
showing dendrite passing through scolopoid sheath at base ; D, external 
surface showing permeable basal spot and numerous fine perforations 
of peg. (Redrawn from Slifer et al., 1959.) 

microscope studies have been made only of grasshoppers on the an- 
tennae of which two types occur (Slifer, 1961). The length of a typical 
thick-walled peg (sensillum basiconicum) is 20-50 [i (Fig. 14) (Slifer, 
Prestage, and Beams, 1957). The tip possesses an opening about 2 (x in 
diameter. A tubular cuticular sheath extends from this opening down 
the lumen of the peg, constricts in the region of its base, then again 
widens. It is the scolopoid sheath. The dendrites of the neurons, usually 
five, are conducted within this sheath to the tip of the peg, where, 
according to Slifer, Prestage, and Beams (1957), they are exposed to 
the air and bathed in a fluid derived from the vacuole of the tormogen 
and trichogen cells. At moulting the cuticular sheath is drawn out 
through the orifice at the tip of the peg. 



CHEMORECEPTION 115 

The typical thin-walled sensillum basiconicum of the grasshopper 
antenna is 16 [j. long and 3 fx in diameter at its base (Fig. 13). The scol- 
opoid sheath, instead of extending to the tip as in the thick-walled 
pegs, makes a right-angle turn at the base of the peg and comes to the 
surface. At moulting the old sheath is pulled out through this area. 
The dendrites of the forty to sixty neurons enter the scolopoid sheath 
in the usual manner, but when the latter turns, they perforate its side 
and continue into the lumen of the peg (Fig. 71). Within this fluid-filled 
cavity each one branches once or twice and each branch terminates at 
one of about 150 openings on the peg's surface (Slifer, Prestage, and 
Beams, 1959). At its termination each branch is composed of about 
twenty-four parallel finger-like processes (Fig. 71). The long, hotly 
debated question as to whether the neurons of chemoreceptors are 
exposed to air, a question for which the conventional answer had been 
negative (cf. Dethier, 1954 b) would now seem to have been answered 
in the affirmative. 

Contact Chemoreceptors 

Receptors sensitive to stimulation by chemical solutions applied 
directly have been identified positively in Diptera, Lepidoptera, 
Hymenoptera, and Coleoptera. They are trichoid sensilla located on 
the legs and mouth-parts. Small sensilla basiconica on the labella of 
flies have also been identified as gustatory receptors. There is no doubt 
that there are also other types of gustatory receptors, but their identity 
still requires confirmation. For details regarding the location of con- 
tact chemoreceptors in various insects the review of Frings and Frings 
(1949) should be consulted. 

The contact chemoreceptive hairs, as exemplified by those on the 
tarsi and labella of Diptera, are actually compound sensilla ; that is, 
they are organs containing several kinds of receptors. In the black 
blowfly, Phormia regina, the receptors occur as groups of three, four, 
or five bipolar neurons associated with long (30-300 \l) hairs which 
characteristically possess two lumina (PL II). The cell bodies of the 
neurons lie in a subhypodermal position beneath the hair in association 
with the tormogen and trichogen cells and one or more neurilemma 
and tracheal cells. The entire group of cells is wrapped in a thin 
membrane which is continuous with the basement membrane of the 
surrounding hypodermis and with the sheath enveloping the nerve. 
The nerve consists of the axons of the receptor cells, which are be- 
lieved to extend, without synapsing, to the central nervous system. The 
dendrites of the neurons extend into a scolopoid sheath and then up 



116 THE PHYSIOLOGY OF INSECT SENSES 

the thicker walled of the two lumina to the tip of the hair. In triply 
innervated hairs as originally described in Phormia by Grabowski and 
Dethier (1954) and Dethier (1955 a) the fibres from two neurons extend 
to the tip of the hair while the third terminates on the base. The exis- 
tence in Phormia of hairs equipped with four neurons was only recently 
suggested by behavioural evidence (Dethier and Evans, 1961) and 
confirmed electrophysiologically (Mellon and Evans, 1961) and by 
electron-microscopy (Larsen, 1962). Hairs with three, four, and five 
neurons have been found in Calliphora (Sturkow, 1960; Peters, 1961). 
The only part of the hair that is sensitive to chemical stimulation is 
the extreme tip, which in some hairs is prolonged into a terminal 
papilla into which the dendrites extend (Dethier, 1955 a; Dethier and 
Wolbarsht, 1956). In the stable fly Stomoxys calcitrans Adams (1961) 
has found that the terminal processes of the dendrites extend through 
a pore in the cuticle (PI. III). 

OLFACTION 
Acuity 

Although the behaviour of insects in their natural environment 
suggests that their olfactory sense may be extraordinarily sensitive 
by human standards, attempts to measure acuity accurately have not 
been outstandingly successful. With the exception of Schneider's work 
with Bombyx mori and associated species, electrophysiological meas- 
urements have not been made. All measurements of the performance 
of olfactory receptors have been based upon behavioural thresholds. 



80 



- )^ 60 



o 

^ 40|- 

UJ 

20f- 



UJ 

o 
cr 

UJ Q 
Q_ UJ 



20- 















THE STIMULATING EFFECT OF 
■ ISO-VALERALDEHYDE ON MUSCA DOMESTICA 






0^,,,--^ 










- 



J 


/' 








— 


/ 


o 








/ 

/ 
















1 1 1 1 1 1 1 1 1 J 


J 


J L 


MM 


1 


1 



IxlO'S IxlO'^ IxlO' 

MOLAR CONCENTRATION 

Fig. 72. Change in behaviour with change in concentration of the odour of 
iso-valeraldehyde. (From Dethier, 1954.) 



CHEMORECEPTION 117 

As the concentration of a stimulating odour exceeds that necessary 
to stimulate the most sensitive receptor element, a behavioural res- 
ponse occurs in the form of antennal movements, movements of the 
mouth-parts, occasionally salivation or grooming movements whereby 
legs or antennae are drawn through the mouth-parts or rubbed against 
one another. A further increase in concentration results in an oriented 
movement which may carry the insect towards or away from the 
source of odour. If the initial response is towards the odour, an addi- 
tional increase in concentration may cause a reversal in orientation 
(Fig. 72). An odour which is initially repellent usually remains so at all 
higher concentrations. An attractive odour may become repellent at 
higher concentrations (Dethier, 1947 b; Dethier, Hackley, and Wag- 
ner- Jauregg, 1952). 

Measurements of acuity thus depend in large measure upon which 
behavioural threshold is chosen for testing. Numerous attempts to 
measure threshold have been made (Barrows, 1907; von Frisch, 1919; 
Wirth, 1928; Folsom, 1931; Warnke, 1931; Reed, 1938; Wietingand 



Table 1 

(From Schwarz, 1955) 

Differences between the olfactory thresholds of man and honeybees 





THRESHOLD CONCENl RATION I MOLECULES/CC AIR 


Odour 










Man 


Author 


Bee 


Difference 


Propionic acid 


4-2 . IQii 


v. Skramlik 


4-3. 1011 


10. 1010 


Butyric acid 


7-0. 10^ 


V. Skramlik 


1-1 . 1011 


10-3 . 1010 


Valeric acid 


60. 1010 


v. Skramlik 






iso-Valeric acid 


4-5. 10i« 


Schwarz 


1-6. 1011 


11-5. 1010 


Caproic acid 


20. 1011 


V. Skramlik 


2-2. 1011 


2-0.1010 


Ethyl caproate 


1-3. 1011 


Schwarz 


3-8. 1011 


2-5. 1011 


Ethyl caprylate 


3-7. 1010 


Schwarz 


5-4. 1010 


1-7. 1010 


Ethyl pelargonate 


3-1 . 1010 


Schwarz 


3-7. 1010 


6-0.10^ 


Ethyl caprate 


4-2 . 10« 


Schwarz 


5-6. 10^ 


1-4. 10« 


Ethyl undecylate 


1-4. 1010 


Schwarz 


1-8. 1010 


40. 10» 


Methyl 










anthranilate 


2-6.1010 


V. Skramlik 


1-9. 10« 


24-1 . 10» 


Phenyl propyl 










alcohol 


6-5. 10» 


Schwarz 


2-2. 10» 


4-3 . 10» 


Nerol 


5-7. 10^ 


Schwarz 


3-2. 10« 


2-5. 10» 


lonon-a 


31 .10« 


Zwaardemaker 


1-5. 1010 


146-9 . 108 


Eugenol 


8-5.1011 


Ohma 


2-0. 1010 


8-3 . 1011 


Citral 


4-0. 1011 


V. Skramlik 


6-0. 1010 


3-4.1011 



118 THE PHYSIOLOGY OF INSECT SENSES 

Table 2 

(From Schwarz, 1955) 

Olfactory thresholds for man and various insects 







THRESHOLD CONCENTRATION 




Odour 


Species 






Author 










Original value 


Mol.jc.c 




' 


Man 


3-2. 101" M/50ml. 


1-84.108 


V. Skramlik 




Necrophorus 


0-00009 g./lOOml.W. 


4-17.101* 


Abbott, 1937 


Skatol ^ 


Geotrupes 


0-003 -0-009 mg./l. 


1-83.1013- 
-4-61.101* 


Warnke, 1931 


- 


Hydrous 


0-0000625% 




Ritter, 1936 


Benz- 
aldehyde I 


Man 


0-44 . 10-« g./l. 


2-49.1012 


Ohma 


Pieris rapae 


580. 10-'' g./l. 


3-28.101* 


Dethier, 1941 


Malacosoma 


435 . 10-' g./l. 


2-46.101* 


Dethier, 1941 


r 


Man 


2-0 . 10^^ M/50 ml. 


4-0 .1013 


V. Skramlik 


Benzol - 


Habrobracon 


0-5-3-0 mg./l. 


3-87.101°- 
-2-3 .10i« 


Wirth, 1928 


c 


Man 


1-6. 101' M/50 ml. 


3-2 .101^ 


V. Skramlik 




Musca 


0-23 g./l. 


3-01. 10i« 


Wieting & 


Ethyl 
alcohol 


domestica 






Hoskins, 1939 


Habrobracon 


5 -20 mg./l. 


4-7 .10i«- 








-1-8 .101' 


Wirth, 1928 




Phormia 


2-4. 10-*mol. 


1-44.10'^° 


Dethier & 


- 


regitia 






Yost, 1952 



Hoskins, 1939; Dethier, 1941; Crombie, 1944; Dethier and Yost, 
1952; Hodgson, 1953; Schwarz, 1955; Fischer, 1957; Dostal, 1958; 
and others [see Dethier, 1947 b] ). A few data are given for comparison 
in Tables 1 and 2. 

Attempts have been made to correlate the acuity of olfaction in the 
various species with the numbers of sensilla, but the correlation is 
highly conjectural in as much as the identity of the receptors is un- 
certain in many species, and quantitative tests of acuity have not been 
undertaken. It is certainly true that some correlation exists between 
the number of receptors and behavioural response to odours. The 
number of olfactory sensilla in an insect varies from species to species. 
There may be as few as 9-10, as in the human louse, or there may be 
as many as 30,000 in the drone honeybee (Schenk, 1903 ; Vogel, 1923 b; 
Mclndoo, 1914a, 1914b). Lice and lepidopterous larvae, which live 
on their hosts and have little apparent need for an extremely acute 
olfactory sense, possess few sensilla. In the life of the honeybee, on the 
other hand, many odours are encountered and are highly significant. 



CHEMORECEPTION 119 

Among the Diptera Liebermann (1926) has shown that the so-called 
olfactory pits (Fig. 73) average 820 in dung-feeding species which de- 
pend largely upon odour for locating their food, while in the flower- 
visiting species, which depend more on vision, the average number is 
494. Moreover, the pits are more numerous in males than in females. 
This difference is presumed to be related to the fact that males employ 
the olfactory sense in the search for females. 

In an individual there is clearly a relation between threshold and the 
number of sensilla stimulated. The phenomenon was first investigated 




Fig. 73. Olfactory pit on the antenna of a dipterous insect. (From 

Liebermann, 1926.) 



with hygroreception. Pielou (1940) suggested that a threshold number 
of receptors is required by Tenebrio molitor for a response. Detailed 
confirmation was provided by the experiments of Roth and Willis 
(1951 a), which showed that the percentage of response of a population 
of Tribolium was closely correlated with the number of sensilla 
basiconica remaining on each individual after surgical operation. The 
change in threshold with unilateral antennectomy is illustrated by the 
figures in Table 3 based on data of Roth and Willis (1951 b). For 
olfaction the first quantitative data were those of Dethier (1952 b), 
which showed that in Phormia regina there is a definite relation be- 
tween the threshold and the number of receptors functioning. The 
data suggest that for a response to occur a given number of molecules 
I 



120 THE PHYSIOLOGY OF INSECT SENSES 

must hit a given number of receptors and that the probabihty of a 
response can be increased by increasing either the concentration or the 
number of receptors. 

Table 3 
(From Dethier, 1952 b) 

Effects of unilateral and bilateral operations in the responses of beetles 

given a choice between 0% and 100% R.H. at 27°C. 

(Data from Roth and Willis, 1951b) 



Species 



Receptor areas remaining on 
Antenna 



% Response 



Rhyzopertha dominica 
(thin-walled sensilla 
present on segments 
8-10) 



Latheticus oryzae (thin- 
walled sensilla present 
on segments 7-11) 



Tribolium castaneum 
(thin-walled sensilla 
present on segments 
9-11) 



Tribolium confusum 
(thin-walled sensilla 
present on segments 
7-11) 



Segments 
Segments 
Segments 
Segments 
Segments 
Segments 
Segments 

Segments 
Segments 
Segments 
Segments 

Segments 
Segments 
Segments 
Segments 
Segments 



Segments 

Segments 

segments 

antennae 

Segments 

Segments 

Segments 

Segments 

Segments 

Segments 

Segments 



-10 on both (normal) 

-10 on one 

-9 on other 

-9 on both 

-10 on one 

-7 on other 

-7 on both 

-1 1 on both (normal) 
-1 1 on one 1 
-10 on other/ 
-10 on both 

-1 1 on both (normal) 
-9 on both 
-9 on one 
-8 on other 
-8 on both 



1 1 on both (normal) 
-11 on one 
on other 



-7 on both 
-7 on one 
-6 on other 
-6 on both 
-11 on one 
-6 on other 
-6 on both 



76±2-7 
69±30 
56±3-4 
61±2-9 
01±7-0 

87±3-l 
73±3-2 
46d=2-7 

80±10 

75±2-9 

78di3-6 
31±5-4 

86±l-7 

76±30 

-0-2±2-2 
23±l-6 

12±3-9 

5±4-l 

75±2-l 
5±4-l 



A more detailed investigation of this phenomenon has been made 
by Dostal (1958), who studied the response of honeybees to the sub- 
stance Nerol R (CjoHigO), a synthetic constituent of rose oil. She 
showed that with successive amputation of one to six antennal seg- 



CHEMORECEPTION 121 

ments the acuity of olfaction decreases only slightly. After extirpa- 
tion of seven segments a pronounced decrease occurs, and amputa- 
tion of eight segments abolishes all response. A comparison of the 
frequency distribution of sensilla on the antennae and the threshold 
of response reveals a logarithmic relationship which Dostal relates 
to the Weber-Fechner law. An examination of the data which Schanz 
(1953) obtained by measuring thresholds in the potato beetle after 
differential amputation of antennal segments reveals similar relation- 
ships. 

Not all olfactory receptor fields of an individual are equally sensi- 
tive. As a rule response thresholds are lowest when the antennae are 
intact. Many insects lose their ability to respond to attenuated odours 
when the antennae are rendered inoperative, but can respond to 
higher concentrations as long as the palpi are still operative (Warnke, 
1931; Frings, 1941; Dethier, 1941, 1947 a, 1952 b). 

The Stimulus 

As with man the number of gaseous materials, natural and synthetic, 
to which insects respond is very great. Many attempts have been made 
to relate stimulating effectiveness to some molecular property, and 
many data have been collected by workers interested in insect attract- 
ants and repellents. When these data can be translated into terms of 
threshold some interpretation is possible. One of the earliest of such 
studies was that of Cook (1926). It was designed to ascertain the re- 
lation between the optimum attractiveness to flies and the physical 
properties of aliphatic alcohols from Q to C5 and esters from acetates 
to valerates. Within a homologous series acceptance threshold de- 
creases with increased boiling point. The relationship is logarithmic. 
Instead of ascertaining the relative stimulating effect of members of 
a homologous series by testing each member separately over a concen- 
tration range as Cook had done, one may derive the same information 
by testing a number of compounds simultaneously and employing the 
number of insects attracted as an index for efficiency. Employing this 
method, Speyer (1920) found that homologous alcohols and esters 
become more attractive as the chain length is increased. Increasing the 
chain length on the acid side of the ester molecule results in a more 
pronounced and uniform increase in effectiveness than do similar in- 
creases on the alcohol side. Comparable experiments with codling 
moths yielded similar results (Eyer and Medler, 1940). Olfactometric 
experiments with the blowfly Phormia regina have shown that the 
rejection threshold to homologous alcohols decreases logarithmically 



122 THE PHYSIOLOGY OF INSECT SENSES 

as the chain length is increased until a cut-off point is reached at or near 
Cii (Dethier and Yost, 1952). With aldehydes both rejection and 
acceptance thresholds reveal similar relationships (Dethier, 1954 a). 

Mechanism of Olfaction 

The nature of the process whereby the odour molecule initiates de- 
polarization in the olfactory receptor remains a mystery despite 
numerous theories, of which those of Ehrensvard (1942), Davies 
(1953a, 1953b), Mullins (1955 a, 1955b), and Davies and Taylor(1959) 
are the more comprehensive. Analyses of relationships between thres- 
hold of response and molecular characteristics have contributed much 
of the groundwork for theorizing. On the basis of measurements made 
with Phormia (Dethier and Yost, 1952; Dethier, 1954 a) and with man 
(MulHns, 1955 a), it is clear that olfactory thresholds, stated as thermo- 
dynamic activities, for members of homologous series of aliphatic 
alcohols, aldehydes, and saturated hydrocarbons are nearly constant 



< 
o 



-2 



12 3 4 

LOG foo (ZS^'C) 

Fig. 74. Comparison in terms of thermodynamic activity of the stimulating 
effectiveness of the first eight normal alcohols acting in aqueous 
solution (open circles) on tarsal chemoreceptors and as gases (solid 
circles) on olfactory receptors of blowflies. In each case the value 
represents a threshold of rejection. The vertical lines represent 2-575 
standard errors for aqueous thresholds and 2 for vapours. (From 
Dethier and Yost, 1952.) 



CHEMORECEPTION 123 

over the middle range of chain length (Fig. 74). Olfactory thresholds 
for fatty acids measured in the dog (Neuhaus, 1953 a, 1953 b) and the 
honeybee (Schwarz, 1955) do not show such a precise relationship. 
For these two animals the thresholds, expressed as molecules per c.c. 
of air, are lowest in the region Co to C4. Dethier (1954 b) pointed out 
that the relationship observed with alcohols suggests that olfaction in 
these cases may involve the establishment of an equilibrium, and as 
such represents a physical rather than a chemical process which in- 
volves specific receptor substances (Dethier, 1956). Mullins (1954) 
further analysed the date of Dethier and Yost (1952) by plotting the 
product of the thermodynamic activity at threshold and the molal 
volume of the compounds against chain length and assigning a cal- 
culated membrane solubility parameter of 11 -5. The analysis suggested 
that the vapour of the first three alcohols might not have been in 
equilibrium with the organism. Additional data and analyses indicated 
that olfaction does not involve an equilibrium process and that excita- 
tion is probably a result of the ability of the odour molecules to pro- 
duce local disorder in the oriented molecular structure of the cell 
membrane (Mullins, 1955 a, 1955 b). 

The theories of Ehrensvard (1942) and Davies (1953 a, 1953 b) 
postulate that odour molecules must first adsorb into the plasma mem- 
brane of the olfactory neuron. Ehrensvard suggested that the potential 
changes due to the adsorption actually initiated impulses in the re- 
ceptor. The Davies theory envisions the adsorbed molecules as dislo- 
cating the membrane, thus permitting an exchange of sodium and 
potassium ions across it, with the consequent initiation of impulses. 
The effectiveness of compounds depends not only upon the concen- 
tration of adsorbed molecules but also upon their size and shape 
(Davies and Taylor, 1959). Olfactory threshold data for Phormia, as 
well as for dogs and man, confirm that both shape and adsorption are 
important factors (Fig. 75). 

Electrophysiological studies thus far have not clarified our under- 
standing of the receptor mechanism. Summed spontaneous activity in 
antennal nerves has been recorded by Boistel and Coraboeuf (1953), 
Boistel, Lecompte, and Coraboeuf (1956), Roys (1954), Smyth and 
Roys (1954), Schneider (1955, 1957 a, 1957 b), Schneider and Hecker 
(1956), and Morita and Yamashita (1961). Firing from individual 
neurons has occasionally been detected in the antennae of Bombyx 
mori and related species (Schneider, 1957 b), but it has not been pos- 
sible to ascertain from which type of sensillum the activity originated 
(Schneider, 1961). When the olfactory stimulus is extract of female sex 



124 THE PHYSIOLOGY OF INSECT SENSES 

attractant (Bombyx mori) hexadeca-diene-(10, 12)-ol-(l) (Butenandt, 
Bechmann, Stamm, and Hecker, 1959), electrical activity increases in 
the male antenna but not in that of the female. When cyclohexanon or 
sorbinol are employed as stimuli activity increases in both sexes. The 
spikes are superimposed on a complex slow potential which Schneider 
(1957 a) has termed the electroantennogram (EAG). The amplitude 



-70 — 



-60 



:2 

o 

^ -50 



-40 



-30 



-20'^ 




Fig. 75. Plot of the logarithm of the olfactory rejection concentration for 
blowflies against the adsorption constant at an oil/air interface 
(logio Kojd). The broken line represents the slope expected if Ijp were 
to increase regularly with chain length. Threshold data from Dethier 
and Yost (1952). (Redrawn from Da vies and Taylor, 1959.) 

depends upon the concentration of the odour, and the wave form, on 
the kind of molecule. Many compounds in high concentration elicit 
an EAG (ether, ethanol, propanol, butanol, xylene, etc.), but at 
extreme dilution only the natural sex attractant elicits an EAG. Its 
wave form is characteristically different (Schneider, 1961). There are 
no significant differences in the normal EAGs of a male antenna 
when the stimuli employed are the glands of related saturniid species, 



CHEMORECEPTION 125 

although the conspecific gland tends to elicit the largest response 
(Schneider, 1962). 

Recently Morita and Yamashita (1961) have been able to record 
directly from a simple large sensiHum basiconicum on the antenna of 
the larva of Bombyx mori. This had been shown to be an olfactory 
organ innervated by approximately twenty neurons (Dethier, 1941). 
When odours of substances contained in the essential oil of mulberry 
leaves (e.g., Py-hexanol and /z-butylaldehyde) were applied to the sen- 
sillum a slow negative potential accompanied by an increase in action 
potential frequency occurred. Some compounds evoked a slow diph- 
asic potential, from negative to positive, while anaesthetics evoked 
slow positive potentials accompanied by a decrease in impulse fre- 
quency. A complete interpretation of these results is rendered difficult 
by the fact that the sensillum is multiply innervated; however, the 
available evidence strongly suggests that the slow negative potential 
evoked by naturally occurring food substances is a true receptor 
potential. 

Odour Qualities 

It is clear from studies of attractants and repellents that for all insects 
there are at least two odour modaUties, that is, 'acceptable' and 
'unacceptable', but it is unlikely that these represent accurately the 
olfactory world of insects. For many insects that respond in a highly 
specific manner to one particular odour, as, for example, the male 
silkworm to female sex-attractant, and many monophagous cater- 
pillars to the odour of their one food-plant, it is possible that the ol- 
olfactory receptors are tuned only to that odour. Electrophysiological 
recordings from the antennae of male Bombyx mori thus far have not 
revealed a sensitivity to any compound other than the natural and 
synthetic sex attractants of Bombyx and the natural attractants of 
closely related species (Schneider, 1962). 

The honeybee, on the other hand, is obviously sensitive to many 
odours, but does it confuse them as one or can it discriminate? By 
training bees to associate a particular odour with food, von Frisch 
(1919) was able to show that a number of odours were discriminated. 
Furthermore, compounds with different structure, which to man 
possessed similar odours, were confused as one by the bee, whereas 
compounds with nearly identical structure but obviously different 
odours were easily distinguished. Within the following pairs the two 
members are easily distinguished by the bee : amyl acetate and methyl 
heptenone, bromstyrol and phenylacetaldehyde, isobutyl benzoate 



126 THE PHYSIOLOGY OF INSECT SENSES 

and salicylic acid amyl ester, /?-cresol methyl ether and w-cresol 
methyl ether. 

CONTACT CHEMORECEPTION 
Sensitivity 

Many behavioural studies have been conducted with numerous species 
of insects for the purpose of locating and mapping contact chemore- 
ceptors, determining limits of qualities, and elucidating the nature of 
receptor action. These studies, centred for the most part around feed- 
ing behaviour, have usually been designed as measurements of accept- 
ance and rejection thresholds. Extension of the proboscis, duration of 
feeding, and measurement of crop loads have been a few of the criteria 
employed (for details consult Dethier and Chadwick, 1948 a). 

Table 4 

(From Dethier and Chadwick, 1948 a) 

Comparison of taste thresholds 



Compound 



Threshold Concentrations 



Sucrose 



Sodium chloride 



Hydrochloric 

acid 
Quinine 



Man, 0-02M; bee, 0-06-0-125M; butterfly (Pyrameis), 
average ca. 0-OlM, in starvation as little as 
8 X IQ-^M; Danaus,9'S x lO-^M;hoTSQfiy(Tabanus) 
0005-0 IIM. 

Man, 0-009M; bee, rejects ca. 0-24M in 0-5M sucrose; 
various caterpillars reject at 0-2M, whereas others 
accept over the full range up to and including 5 -OM. 

Man, 000125M; bee, rejects OOOIM in 1 OM sucrose; 
various caterpillars reject at 0-01-0-2M. 

Man, 1 -5 x 10" "^M; bee , rejects at 8 x 10"* in 1 -OM 
sucrose; various caterpillars reject at 0002-0-033M; 
aquatic beetles were conditioned to respond to 
1-25 X lO-^M. 



Data on man are for specific thresholds, adapted from Moncrieff" (1944); 
for the bee, from von Frisch (1934); for Pyrameis, from Minnich (1922); 
for Danaus, from Anderson (1932); for caterpillars, from Eger (1937); for 
aquatic beetles, from Bauer (1938). The figures for insects are thresholds 
of response. 



Threshold studies have revealed many of the characteristics of the 
contact chemical sense. They have shown, for example, that the 
thresholds are frequently lower than those of man for similar sub- 
stances (Table 4). They have revealed among individuals differences 
that follow a common pattern. For example, the scattering of 



CHEMORECEPTION 127 

thresholds in a population ofPhormia is not significantly different from 
a normal distribution when plotted against the logarithm of concentra- 
tion (Dcthier and Chadvvick, 1947). Where sufficient data have been 
reported a similar relationship can be shown to exist with other insects 
(e.g., Eger, 1937; Frings, 1946; von Frisch, 1935; Weis, 1930; 
Hodgson, 1951). 

Threshold determinations have revealed that sensitivity of response 
varies with the receptor field stimulated. In the horsefly Tabanus the 
mean labellar threshold for sucrose is 0-02 IM; the tarsal threshold, 
0-060M (Frings and O'Neal, 1946). In CallipJwra erythrocephala the 
labella are generally more sensitive than the tarsi (Haslinger, 1935). In 
C. vomitoria, on the other hand, the tarsi are sixteen times more 
sensitive than the labellum to sucrose (Minnich, 1931), but lactose 
elicits a response only when applied to the labellum (Minnich, 1929 b). 
Musca domestica, Cochliomyia americana, and Phormia regina exhibit 
lower rejection thresholds following oral stimulation than tarsal 
stimulation (Deonier, 1938, 1939;Dethier, 1955a). Similar results have 
been obtained WiihPieris (Verlaine, 1927). The antennae of honeybees 
are more sensitive to solutions than the legs (Frings, 1944; Marshall, 
1935 ; Minnich, 1932) ; the proboscis, more sensitive than the antennae 
(Kunze, 1933). In the beetle Hydrous the labial palpi are sensitive to 
hydrochloric acid and insensitive to sodium chloride and sugar, while 
the maxillary palpi are sensitive to sodium chloride and sugar (Ritter, 
1936). In the related species Laccophilus the antennae are more 
sensitive than either pair of palpi to acids, salts, and alcohols (Hodgson, 
1951). 

The aforementioned studies do not reveal whether the differences 
in threshold reflect central phenomena, variations in the sensitivity of 
the receptors, summation, or differences in sensitivity due merely to 
the number of receptors stimulated. 

Differences between acceptance thresholds following unilateral and 
bilateral tarsal stimulation had suggested that some relation does 
exist between sensitivity and the number of receptors stimulated 
(Imamura, 1938). An analysis of thresholds following stimulation of 
one tarus versus two tarsi in Phormia showed that the bilateral thres- 
hold for sugar is lower than the unilateral threshold (Dethier, 1953 b). 
This difference could be due, however, either to summation or to a 
simple statistical bias. In the analogous visual case where comparisons 
have been made between monocular and binocular vision, Pirenne 
(1943) and Barany (1946 a, 1946 b) pointed out that the experimental 
procedure by its very nature assures that the two eyes will see more 



128 THE PHYSIOLOGY OF INSECT SENSES 

clearly than one. 'Let us assume that the visual acuities (or other 
thresholds) of both eyes fluctuate independently of one another . . . 
and that the instantaneous thresholds for monocular vision have the 
same distribution in both eyes, . . . then if the one eye alone has the 
chance of a of seeing the symbol, both eyes together have the chance 
2a— a^. As a is smaller than 1, this expression will always be greater 



7.0 



(f) 
h- 

d) 
O 

Q. 
O 



o 

< 



UJ 

o 
cr 

UJ 



6.0 



5.0 



• I LEG-RANDOM 
O 2 LEGS-RANDOM 




•3.0 



2.0 



1.0 



0.0 



LOG MOLAR CONC. SUCROSE 



Fig. 76. Comparison of the distribution of acceptance thresholds for 
sucrose, as a function of concentration, for flies stimulated unilaterally 
or bilaterally. The broken line represents the theoretical distribution 
of bilateral thresholds (two-legged flies) calculated from the expression 
\—q^, where q equals the fraction of the population of one-legged flies 
not responding. (From Dethier, 1953.) 

than a - that is to say, two eyes will be able to see better than one solely 
as a result of random combination' (Barany, 1946 b, p. 127). And as 
Smith and Licklider (1949) went on to state, the same source of bias is 
inherent in the procedure as appHed to the determination of thresholds 
in other sense modalities. 

The idea can be clarified still further by quoting from the study of 
hearing by these authors (p. 279). *In order to estimate the magnitude 
of the bias, it is necessary to define the null condition under which we 



CHEMORECEPTION 129 

should say that there is no binaural summation. We can imagine, for 
this purpose, two monaural listeners, one with only a right ear, the 
other with only a left ear. The two listeners have no means whatsoever 
of communicating with each other, but both report to the same experi- 
menter. To obtain measures of monaural and "binaural" sensitivity, 
the experimenter tests the two listeners separately (successively), then 
together, in the latter instance recording a positive response whenever 
either hstener reports hearing the stimulus tone.' The case of unilateral 
versus bilateral tarsal stimulation of Phormia is similar. The results 
show that the bilateral threshold for sucrose is lower than the unilateral 
threshold by a factor that is never greater than can be satisfactorily 
accounted for on a simple probabihty basis, that is, the greater the 
number of available receptors, the greater that chance that the number 
required for a threshold response will be stimulated (Fig. 76) (Dethier, 
1953 b). 

Discrimination 

Threshold measurements do not permit evaluation of intensity dis- 
crimination over the complete effective concentration range of a com- 
pound. Von Frisch (1935) had demonstrated that honeybees responded 
differently to 0-125M and 0-156M sucrose and to 0-25M and 0-3125M 



Table 5 
(From Dethier and Rhoades, 1954) 
Intensity discrimination of sucrose 



Intensity 


Nearest cone, which 
can be distinguished 


Mil 


Mil 

{geometric 
mean) 


0001 


000007 


0-99 


2-4 


0001 


007 


60 




001 


007 


0-3 


0-387 


001 


0015 


0-5 




01 


0088 


012 


012 


01 


0112 


012 




10 


0-70 


0-3 


0-346 


10 


1-40 


04 




2 


10 


0-5 


0-418 


20 


2-7 


0-35 





130 THE PHYSIOLOGY OF INSECT SENSES 

sucrose, a ratio of 1 : 1-24 (AS IS = 0-25). Frings (1946) and Frings 
and O'Neal (1946) had found that Periplaneta americana and Tabanus 
sulcifrons could also discriminate at this level. On the basis of tests 
with two specimens Verlaine (1927) claimed a slightly greater sensi- 
tivity for Pieris, 

A technique permitting the measurement of A/// for the complete 
effective concentration range of a compound was developed by Dethier 
and Rhoades (1954) and employed with Phormia. The smallest ratio 
found (0-12) indicates better discrimination than that obtained in 
earlier studies. An examination of the results tabulated in Table 5 
shows that discrimination is best over the middle ranges of concentra- 
tion and is optimum at about the same concentration for which there 
is a maximum preference. The discrimination factor for the chemical 
senses of man is about 0-3 according to Moncrieff (1944) but earlier 
Lemberger (1908) had recorded optimum values of 0-15 for sucrose 
and 0-11 for sodium-saccharin and higher values at both extremes of 
the concentration range (cf. also Dahlberg and Penczek, 1941; 
Schutz and Pilgrim, 1957). 

Rejection Thresholds - Electrolytes 

The number of compounds that can be detected by insects is very great. 
From a behavioural point of view the only manifestation of stimula- 
tion by the majority of them is the rejection of acceptable solutions 
(e.g., sugar or water) to which they have been added. Rejection thres- 
holds, therefore, represent the concentration of substances necessary 
to prevent responses to sugar or water. Because the test solutions are 
always mixtures, the thresholds involve : the sensitivity of two different 
receptors, possible interactions at the receptor level, and demonstrated 
interaction at the central level. Despite these complications, it has been 
possible to estabhsh rather precise relationships between the stimulat- 
ing effectiveness of many compounds and their molecular properties. 
Electrolytes were among the first compounds studied. Tests con- 
ducted with the mouth-parts of the cockroach Periplaneta americana 
showed that for several series of salts with a common union (acetates, 
bromides, chlorides, iodides, nitrates, and sulphates) the stimulative 
efficiency could be correlated directly with ionic mobilities (Frings, 
1946). Similar results had been obtained earher with the oral receptors 
of cecropia moth larvae (Frings, 1945). Extensions of these studies to 
the tarsal receptors of the horsefly Tabanus sulcifrons (Frings and 
O'Neal, 1946), the ovipositors of parasitic Hymenoptera (Dethier, 
1947 c), oral receptors of the hQetle Laccophilus (Hodgson, 1951), the 



CHEMORECEPTION 131 

labellar receptors ofPhormia (Dethier, 1955 a), and the receptors of a 
number of other species (Frings, 1948) showed that the same general 
relationships held. According to Frings, the data are in substantial 
agreement with most of the data reported in the literature for chemical 
stimulation of other animals by the series of cations employed, namely, 
in decreasing order of thresholds: Li+ > Na+ > Mg++ > Ca++ = 
Sr++>K+ = Cs+ = Rb+>NH4+>>>H+. As pointed out by 
Frings, the order of effectiveness is also that of partition coefficients, 
which parallels that of ionic mobilities (Osterhout et ai, 1934). The 
arrangement for anions is less clear. The work of Frings (1946) estab- 
lished the following order of thresholds: PO4 > Ac~ > SO4 = 
CI- ^ Br- > I- > NO3- > > > OH-. 

The situation is actually much more complex than these generaliz- 
ations imply. For example, the activity of divalent cations is anom- 
alous in that they do not fit any of these series. Furthermore, the 
behaviour of insects towards divalent ions is noticeably different from 
their behaviour towards monovalent ions (cf. Hodgson, 1951). In 
addition, there are species differences. It is possible that these may 
reflect differences in the molecular structure of the receptors, as has 
been proposed for mammals (Beidler, 1953, 1954, 1960; Beidler, Fish- 
man, and Hardiman, 1955). 

Rejection Thresholds - Non-electrolytes 

The rejection thresholds of over two hundred aliphatic organic com- 
pounds have been measured by employing flies that had been rendered 
anosmic by removal of the antennae and labella (Dethier and Chad- 
wick, 1947, 1948 b, 1950; Chadwick and Dethier, 1947, 1949). A 
number of significant relationships were revealed by these data. 

Within any homologous series exceptionally high correlations were 
found between the stimulating power of the compounds and such 
properties as boiling point, molecular area, oil-water partition coeffi- 
cients, molecular moments, vapour pressures, and activity coefficients. 
Molecular weight, number of carbon atoms, and osmotic pressure 
were eliminated from consideration in part by the use of isomers, 
which proved usually to have different thresholds, and the correlation 
with vapour pressures was inverse. Because of the paucity of data 
relating to the various chemical and physical properties enumerated 
above, it became convenient to plot stimulative efficiency against the 
chain length of the molecule. Graphs so constructed (Fig. 77) show 
clearly that for all series of homologous aliphatic compounds studied 
the members of the series are rejected at logarithmically decreasing 



132 THE PHYSIOLOGY OF INSECT SENSES 

concentrations as the carbon chain length is increased. It is apparent 
from Fig. 77 that this relation is not a continuous one. For each series 
the curve shows a sharp break in the region of a definite chain-length 
characteristic for each series. 

Taking a saturated straight-chain hydrocarbon as a starting-point, 
one may, without altering appreciably the arrangement of the carbon 




ijj — 



-2.0 



-3.0 



20 



LOG NUMBER OF C- ATOMS 

Fig. 77. Rejection thresholds of glycols and alcohols by Phormia. (From 
Dethier and Chadwick, 1948 b.) 

linkages, substitute various kinds of polar groups for one or more of 
the hydrogen atoms. Whereas all such substitutions raise the molecular 
weight and the boiling point, the effect on solubility is variable. The 
different polar groups may be arranged in increasing order of solu- 
bility as follows: Br < CI < CHg < CHO < C =- O < OH. The CH3 
radical represents the unsubstituted compound. This series also repre- 
sents in reverse order the relative stimulating efficiencies of these polar 
groups. When the number of substitutions of the groups to the right of 



CHEMORECEPTION 133 

the CH3 (in the above representation) is increased the stimulating 
efficiency decreases. Thus, glycols are less effective than alcohols, and 
diketones are as a rule less effective than ketones. Increase of the 
number of substitutions of those polar groups to the left of the CH3 
tends to increase stimulating effectiveness. Thus, dibromo compounds 
are more effective than monobromo homologues. 

The effects of the positions of the functional groups are illustrated by 
experiments with the glycols. The following rules are found to hold : 

(1) juxtaposition of two hydroxy! groups in a short molecule 
(e.g., 1, 2-butanediol) makes for a high threshold; this effect is re- 
duced as chains become longer; 

(2) in a chain with no terminal OH groups, i.e., subterminal but 
not adjacent (e.g., 1, 3-butanediol) the thresholds are low; 

(3) if both OH groups are terminal thresholds are intermediate; 

(4) branching tends to raise the threshold, other factors being 
equal. 

Taken all together, the foregoing results state essentially that the 
length of the free alkyl group largely determines the stimulating 
effectiveness and that its power is modified to varying degrees by the 
nature of the attached polar groups. The length of the alkyl group is 



4' 




-i\\ 



M W. " 



-3 -2 

LOe SOLUBILITY GRAM MOLES PER UTRE 



Fig. 78. Correlation between concentration required for stimulation and 
the solubility of compounds at 25-27 degrees C. in water. Each of the 
forty-six points represents a different aliphatic compound. (From 
Dethier and Chadwick, 1950.) 



134 THE PHYSIOLOGY OF INSECT SENSES 

also of prime importance in determining the solubility characteristics 
of compounds of this type ; hence the same structural characteristics 
that decrease water solubility likewise decrease threshold. 

There is then only one molecular property, for which data are 
available, which brings all the data from the different series into a 
single homogeneous system. This is water solubility (Fig. 78). The 
order of stimulative efficiencies follows the inverse of the order of 
water solubilities with fewer contradictions than appear in most of the 
other comparisons attempted. Additional evidence that solubility is of 
importance in this connexion has been presented by the work of 
Dethier (1951a), which showed that the thresholds of alcohols are 
altered as the alcohol is presented as an aqueous solution, a glycol 
solution, or a mineral oil solution (Fig. 79). 

When threshold values are expressed as thermodynamic activities 
rather than as moles the differences between successive homologues of 
a series are not so marked, but a plot of the logarithm of these values 
against the logarithm of activity coefficients (Fig. 74) does not produce 
a straight line of the sort that one is accustomed to expect from 
parallel experiments on narcosis (for a complete discussion consult 
Ferguson, 1951 ; Brink and Posternak, 1948; Dethier, 1954 b). 

In spite of the generally good correspondence between low solu- 
bility in water and high stimulating power, it seems likely, from the 
data on oil-water partition coefficients, that plots of threshold values 
against water solubihties would also yield a smaller slope for the 
lower than for the higher range of compounds in each series if such an 
analysis could be made. This type of relationship seems to have no 
conterpart in any of the tabulated values for the physical properties, 
and its consistent recurrence prompted Chadwick and Dethier (1949) 
to consider the possibility that different forces may be of primary 
importance in stimulation by the lower and higher members of each of 
the types investigated. This amounts to postulating at least a two- 
phase system for the limiting mechanism in contact chemoreception. 
The hypothesis that small molecules gain access to the receptors in 
part through an aqueous phase, whereas the larger aliphatic molecules 
penetrate chiefly through (or accumulate in) a lipoid phase, would 
appear to offer a basis for reconciling most of the contradictions en- 
countered when it is attempted to fit the facts into a single-phase 
system. 

Movement of the smaller molecules through an aqueous medium 
should occur at rates related inversely to the molecular weight, which 
would help to account for their being more stimulating than is antici- 



CHEMORECEPTION 135 

pated from the relationship found for the higher members of the series, 
although it is doubtful that the entire difference can be explained in 
this way. It may be noted also (Fig. 80) that the inflections in the 
curves relating thresholds to molecular size occur at increasing chain 



bJ 

o 
cc 

UJ 
Q. 

o 
•o 

>- 

CO 

Q 

UJ 

I- 



Ul 

cc 

2 

O 

z 
o 
u 

< 



o 

o 

_J 



00 



-1.0 



-20 



\ 



\ 
\ 

O \ 



\ 



\ 



\ 



o \ 



\ 



o o 



K' 



\o 

\ 

\ 



\ o 



-3.0 



•4.0 



-- ALCOHOLS IN WATER 
O ALCOHOLS IN GLYCOL 

• ALCOHOLS IN MINERAL OIL 



0.0 



0.4 



0.8 



LOG NUMBER OF C ATOMS 



12 



Fig. 79. Rejection thresholds of aqueous, glycol, and oil solutions of 
primary alcohols by Phormia. (From Dethier, 1951.) 

lengths in passing from the less to the more water-soluble species. At 
the same time the predominant importance of lipoid affinity is sugges- 
ted by the logarithmically increasing stimulating power of both 
lower and higher members of all series, as well as by the inverse 
relationship between water solubility and stimulating effectiveness in 
comparisons of the several series with each other. 

K 



136 THE PHYSIOLOGY OF INSECT SENSES 

Further analyses of the date of Dethier and Chadwick (1948 b, 1950) 
suggest that the important factor in stimulation by non-electrolytes 
is adsorption (Davies and Taylor, 1959). When the logarithm of rejec- 
tion thresholds (molar concentration) is plotted against the logarithm 



1.0 



0.0 - 



I— 

Ul 

o 
a: 



o 
to 



>- 

CD 



O 
UJ 



O 



UJ 



o 

o 
o 

q: 
< 

_j 
o 

o 
o 



-1.0 



-2.0 



-3.0 



-4.0 




O ALDEHYDES 
A KETONES 

NORMAL ALCOHOLS 

• SECONDARY ALCOHOLS 



0.0 



0.4 0.8 

LOG NUMBER OF ATOMS 



12 



Fig. 80. Rejection of aldehydes, ketones, and secondary alcohols by 
Phormia. (From Chadwick and Dethier, 1949.) 

of the adsorption constant for an oil/water interface the slope of the 
resulting line is very near that expected for adsorption from solution 
on to a pure lipid membrane. 

Rejection Thresholds - Organic Electrolytes 

The situation with regard to organic electrolytes is less clear than that 
for the non-electrolytes. Tests with a number of fatty acids indicated 
that while the H ion is the principal factor in stimulation with com- 



CHEMORECEPTION 137 

pounds of this type, a contribution is made also by the anion or un- 
dissociated acid, which is effective in inverse proportion to the hydro- 
phile nature of the molecule. The relationship is thus very similar to 
that found with the same class of compounds for human taste (cf., 
e.g., Taylor er^/., 1930). 



i.5r*' 



Q 

_J 
O 
X 
CO 
bJ 

cr 

I 



z 
o 

t- 
o 

UJ 

-3 
UJ 

on 

■z. 
< 

Q 
UJ 



0.75 



• Na 


.SALTS OF FATTY ACI 


A Bo 






i Na SULFONATES 




FORMAMIDE 


9.55 


ACETAMIDE 


7.22 


CHLOROACETAMIDE 


L43 


PROPIONAMIDE 


3.21 


BUTYRAMIDE 


1.92 


VALE 


:ramide 


0.37 




0.50 - 



0.25 - 



4 5 6 7 8 9 10 II 12 13 14 
NUMBER OF C ATOMS 

Fig. 81. Relation between the stimulating efficiency of organic salts 
and chain lengths of the anion. (From Dethier, 1956.) 

Tests with homologous organic salts show that beginning with the 
five-carbon compound there is a logarithmic decrease similar in all 
respects to that observed with non-polar homologues (Fig. 81) 
(Dethier, 1956). 

Acceptance Thresholds 

Among compounds acceptable to insects carbohydrates are the most 
usual and important. Comparisons of the acceptability of various 



138 



THE PHYSIOLOGY OF INSECT SENSES 



carbohydrates have been undertaken with the honeybee (Vogel, 1931 ; 
von Frisch, 1934), Calliphora (Haslinger, 1935), water beetles (Bauer, 
1938), the ants Lasius niger, Myrmica rubra, and M. rubida (Schmidt, 
1938), wireworms (Thorpe et al., 1947), the butterfly Pyrameis 
atalanta (Weis, 1930), the blowfly Phormia (Hassett, Dethier, and 
Gans, 1950; Dethier, 1955). The number of sugars acceptable to these 

Table 6 

(From Dethier, 1953 a) 

Acceptance thresholds of various insects for sugars 

(Molar concentrations) 





PHORMIA (Tarsi) 
(Data from 


CALLIPHORA (Data from 
Haslinger. 1935^ 


APIS (Mouth) (Data 


Sugar 


Hassett, 
Dethier, and 




-~ J — — y 


from von Frisch, 
1930) 










Gans, 1950) 


Tarsi 


Mouth 




Sucrose 


001 


0-0006 


0035 


0625-0-125 


Maltose 


00148 


0-00125 


0-002 


00125 


Trehalose 


0126 


0-14 


002 


0-25 


Lactose 


* 


* 


0-1 


* 


Cellobiose 


5 01 


05 


003 


* 


Melibiose 


* 


N: 


* 


* 


Melezitose 


063 


07 


0-01 


0125-0-25 


Raffinose 


0-275 


01 


0-0071 


* 


Fructose 


0076 


0-0033 


0-004 


0-25 


Fucose 


0-087 


0-02 


0-01 


1-0 


Glucose 


0-114 


0-125 


0-04 


0-25 


Sorbose 


0-218 






... 


Xylose 


0-400 


0-2 


0-14 


* 


Galactose 


0-502 


0-14 


0-09 


2-0 


Arabinose 


0-50 


01 


08 


* 


Mannose 


7-59 


0-2 


0-1 


* 


Ribose 


7-94 






... 


Lyxose 


33-1 




... 


... 


Rhamnose 


* 


* 


10 


* 



* Non-stimulating at all concentrations. 
. . . Not tested. 

species varies, the blowflies being more catholic than either the honey- 
bee or the ants. However, if the data of von Frisch, HasHnger, and 
Hassett et al. are compared (Table 6), allowances made for statistical 
variance, and the sugars divided into three categories (mono-, di-, and 
tri-saccharides), certain general relationships appear. For bees the 
order of effectiveness is : (dissaccharides) sucrose = maltose > 



CHEMORECEPTION 139 

trehalose ; (monosaccharides) fructose = glucose > fucose > galac- 
tose. All other sugars fail to stimulate. For Calliphora legs the order is : 
(disaccharides) sucrose = maltose > trehalose = cellobiose > lactose ; 
(monosaccharides) fructose > fucose > glucose = xylose = galactose 
= arabinose = mannose. For Calliphora mouth-parts the order is: 
(disaccharides) sucrose = maltose > trehalose = cellobiose > lactose ; 
(monosaccharides) fructose > fucose > glucose > arabinose = xylose 
= galactose = mannose. For Phormia legs the order is : (disaccharides) 
sucrose = maltose > trehalose > cellobiose > lactose ; (monosacchar- 
ides) fructose > fucose = glucose > sorbose > xylose = galactose = 
arabinose > mannose = ribose > lyxose. 

For these three species of insects it is true in general that the most 
stimulating disaccharides are the a-glucosides and the most stimulat- 
ing monosaccharides are fructose, glucose, and fucose. From studies 
with Phormia, in which 75 carbohydrates, 8 polyhydric alcohols, 53 
amino acids, and 18 monobasic and dibasic acids have been applied to 
individual labellar hairs, some of the limiting factors in stimulation 
have been revealed (Table 7) (Dethier, 1955 a). For example, trioses, 
tetroses, heptoses, and octoses are uneifective. This finding indicates 
that there is an optimum chain length. The size of the molecule as a 
whole appears to be critical only within certain limits. Thus, at the 
smaller extreme some pentoses stimulate while at the other extreme 
certain trisaccharides stimulate. However, polysaccharides are un- 
effective. For additional details the work of Dethier (1955 a) should be 
consulted. 

Categories of Receptors 

Ultimately, an understanding of the mechanism of action of the re- 
ceptors themselves had to await the application of electrophysio- 
logical techniques. Studies of this sort have been confined to a few 
carefully selected species : the flies Phormia regina, Lucilia caeser, and 
Calliphora vomitoria; the butterfly Vanessa indica; and the Colorado 
Potato Beetle, Leptinotarsa decemlineata. 

The most intensively investigated and well-known receptors are 
those occurring on the tarsi and labellum of the black blowfly, 
Phormia regina. They have been the subject of co-ordinated be- 
havioural, histological, and physiological study and may be taken as a 
model for discussion. The multiplicity of neurons associated with these 
hairs complicated for a while studies of the mechanism of chemo- 
reception. Because of the specificity of the neurons, however, it was 
originally possible to arrive at a considerable understanding of 



140 



THE PHYSIOLOGY OF INSECT SENSES 



.s: 
Si 









< 



On 






o 



is « 

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c c 

a g 
o ^ 



o 



a 
o 



c 



a 

X 






4) 

O 
(-1 



(A 

> 



« Si 

GO (O ;2 

73 in 



CiO 

e 
3 

e 



Cfl 



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^ to 






c 
o 



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GO a O 

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= 1 
g§ 



ffi 73 

2 c 

3 M 



f5 


0194* 
0069* 


§ 


1111+ +il+! 1+ ++ 1 ! 




m-Erythritol 
Penta-erythritol 
Mannitol 
L-Arabitol 
Inositol 
Glycosides 
a-D-methyl glucoside 
[B-D-methyl glucoside 
NOa-benzyl glucoside 
/7-Aminophenyl glucoside 
Monoacetyl NOa-^-glucoside 

Phenyl p-glucoside 

tetraacetate 
a-/)-Methyl mannoside 
/7-Aminophenyl 

p-maltoside 
Nitrophenyl maltoside 
7- Acetyl /7-nitrophenol 

cellobioside 
Substituted sugars 
//-Acetyl glucosamine 




* 
**»** 00** 

1 1 1 oo"^fnT}-mONr>-| 1 1 Orn^toON 
ooooocb<N oooor- 


.V. 

Co 


! 1 1 + + + + + 1 i 1 1 i + + + + 1 


s: 
s: 

a 


Triose 

DL-glyceraldehyde 
Tetroses 

D-erythrose 

L-erythrose 
Pentoses 

£-Fucose 

D-Arabinose 

L-Arabinose 

D-Xylose 

L-Xylose 

Z)-Ribose 

D-Lyxoset 

Ribulose 

L-Rhamnose 

2-Desoxyribose 
Hexoses 

L>-Fructose 

D-Glucose 

L-Sorbose 

L>-Galactose 

D-Mannosef 



CHEMORECEPTION 



141 



6 



oo 
O 



+ + -H + 



I + I ^- I 



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Id 








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JG 




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DO 




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1 


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rr! 


o 


ro 


■*-> 


-^-j 


■*-> 




(L) 


p 


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o 


1> 


CJ 


o 


Ci 


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a 



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(1> 






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s 








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§ 






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CO 


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-maltose 
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glue 
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142 THE PHYSIOLOGY OF INSECT SENSES 

chemoreceptor activity by behavioural techniques. It was shown, for 
example, that a single labellar hair responded to touch, water, certain 
sugars, and a wide variety of electrolytes and non-carbohydrate 
organic compounds. In a hungry, thirsty fly bending a hair, applying 
water, or stimulating with certain sugars eHcited a reflex proboscis 
extension. The application of such compounds as salts, acids, alcohols, 
aldehydes, ketones, glycols, ethers, etc., to the same hair prevented 
extension or elicited retraction if the proboscis was already extended. 

By adapting the hair successively to bending, to water, and to carbo- 
hydrate, and by noting that removing the tip of the hair prevented 
response to chemicals but not to bending, Dethier (1955 a) concluded 
that the neuron whose process terminated at the base of the hair was a 
mechanoreceptor. He concluded further that of the remaining neurons 
one was concerned with acceptance (exclusive of mechanoreception) 
while another was concerned with rejection. In other words, one 
neuron was conceived of as being sensitive to water and certain 
sugars while the other was considered to be sensitive to all of those 
compounds that caused rejection. Later behavioural experiments 
(Dethier, Evans, and Rhoades, 1956) indicated, however, that re- 
jection was in reality not a simple modality because it could be initi- 
ated either by stimulation of the rejection receptor or inhibition of the 
acceptance receptor. Sugars such as mannose, rhamnose, and sorbose, 
which of themselves do not cause rejection, are able- to interfere with 
stimulation by certain other sugars that alone are acceptable. For 
example, mannose inhibits fructose (but not glucose), rhamnose 
inhibits glucose (but not fructose or sucrose), sorbose probably in- 
hibits glucose and fructose. Furthermore, certain rejected salts, 
notably HgClg and CuClg, render sugar receptors reversibly insensi- 
tive. 

Still more recently, behavioural investigations into the mechanisms 
controlling thirst and water satiation suggested that acceptance was 
not a simple modality either and that there must be a water receptor 
distinct from the carbohydrate receptor (Evans, 1961 a; Dethier and 
Evans, 1961). In female flies at certain stages of the reproductive cycle 
acceptance is further broken down into carbohydrate acceptance and 
protein acceptance (Dethier, 1961). 

Conclusions drawn from behavioural studies were borne out to a 
very satisfactory degree when success finally attended attempts to 
record electrically from chemoreceptive hairs. After many people had 
tried and failed to record action potentials by standard techniques, 
Hodgson, Lettvin, and Roeder (1955) and Morita, Doira, Takeda, 



CHEMORECEPTION 143 

and Kuwabara (1957) independently developed a novel technique. It 
consisted of placing a fluid-filled micropipette over the tip of a hair 
and employing it both as a recording electrode and as a source of 
chemical stimulation. More recently a greatly improved technique was 
developed by Morita (1959). It involved puncturing the side wall of the 
hair and recording with the pipette electrode from this point. The tip 
of the hair was thus left free for stimulation by any kind of material 
whether electrolyte or not. The indifferent electrode was inserted into 
the crushed head. 

Originally the potentials from only two neurons were recognized in 
the records obtained from the fly (Hodgson et al. 1955; Hodgson and 
Roeder, 1956). One neuron, designated the L (for large spike) fibre by 



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Fig. 82. Electrical response of a labellar hair ofPhormia to stimulation by 
salt, sucrose, and bending. A, intact hair stimulated with 0-01 M NaCl 
and motion. B, same hair with tip removed. C, cut hair stimulated by 
OOIM NaCl + O-IM i)-fructose. The hair is bent at arrow. D, same 
hair responding to motion after adaptation to chemicals. Time, 0-2 sec. 
Positive potential at recording electrode is down. (From Wolbarsht 
and Dethier, 1958.) 

Hodgson and Roeder (1956), clearly responded to salts, while the 
other, designated as the S (for small spike) fibre, responded to sugars. 
Subsequently, Wolbarsht and Dethier (1958) were able to detect the 
spikes of a third neuron (designated M for mechanoreceptor) which 
responded only to bending of the hair (Fig. 82). Mellon and Evans 
(1961) have now detected spikes from a fourth neuron which responds 
to water. The function of the fifth neuron, present in some hairs, is not 
known. 

Since it is now known that certain hairs contain four distinct re- 
ceptors, conclusions drawn from earlier studies of electrophysiological 
records must be re-evaluated, specifically the conclusions that: low 
concentrations of salt sometimes stimulate both L and S fibres 
(Hodgson and Roeder, 1956), that acids and alcohols stimulate the L 
fibre (Hodgson and Roeder, 1956), that water stimulates L and 5 fibres 



144 THE PHYSIOLOGY OF INSECT SENSES 

(Wolbarsht, 1957), that fructose stimulates L and S (Hodgson, 1957; 
Wolbarsht, 1957; Evans, 1958), that sucrose stimulates two fibres in 
Calliphora vomitoria (Morita, 1959), that bending stimulates L and S 
(Hodgson et a!. 1955; but see also Hodgson and Barton Browne, 
1960), that the primary receptor cell is responsive to chemical, tactile, 
and thermal stimuli within the normal physiological range and hence 
is at variance with the usual concept of single specificities of receptor 
cells (Hodgson and Roeder, 1956; Hodgson, 1958 a, 1958 b). 

Another variable that must be considered is the possible differences 
among hairs. Some hairs clearly respond more vigorously to bending 
or to water than others. Some hairs in the female fly show discharge of 
one fibre when protein such as crystalline haemoglobin or brain-heart 
extract is applied, but in other hairs all fibres are silent when protein is 
appHed (Dethier, 1961). In Vanessa also all hairs are not equally 
sensitive to all compounds. 

In the course of recording from chemoreceptive hairs when mixed 
stimuli were appHed, all workers have observed an interaction between 
activity in the L and S fibres (Hodgson, 1956a, 1957; Morita et al. 
1957; Wolbarsht, 1958; Morita and Takeda, 1959; Morita, 1959; 
Sturckow, 1959; Takeda, 1961). Hodgson (1957) found that the 
presence of 5* impulses is characteristically accompanied by a decrease 
in L impulses and conversely that the stimulation of the L fibre is 
associated with a decrease of S spikes. Since the inverse relationship 
between the frequencies of S and L impulses is not constant, it does 
not appear that the facts can be explained simply as a result of partial 
depolarization of one receptor unit by electrotonic spread from the 
more active adjacent unit. Wolbarsht (1958) also noticed this situation 
and decided that the activity of the L fibre is not related to the activity 
of the S fibre but depends only on the character of the stimulating 
solution. He believed that such properties of the salt as thermo- 
dynamic activity and the diffusivity of the salt can account in part for 
the change in activity reported by Hodgson. On the other hand, 
Takeda (1961) has concluded that the depression of the frequency of 
impulses from the sugar receptor of Vanessa in the presence of NaCl 
represents a direct inhibitory effect. 

At the present time the picture in the blowfly appears to be as 
follows: one neuron is specifically sensitive to sugars; one neuron is 
specifically sensitive to monovalent salts; the neuron whose process 
terminates at the base of the hair is sensitive to mechanical stimula- 
tion ; a fourth neuron, whose exact location has not yet been established 
histologically, has as its adequate stimulus water. 



CHEMORECEPTION 145 

The situation in the butterfly Vanessa indica is not yet so clear. 
Kuwabara (1951, 1952, 1953) has shown that water, sugar, and some- 
times sodium chloride elicit proboscis extension. Both sodium 
chloride and quinine inhibit. There is no behavioural response to 
acids. Morita et al. (1957) concluded that there were more than three 
kinds of impulses from this chemoreceptive hair; one neuron respond- 
ed to sodium chloride, one to sugar; probably there were also fibres 
responding to quinine and water. A later work (Morita and Takeda, 
1959) concluded that there were four sensory neurons responding as 
follows: (1) one responding to concentrations of sodium chloride 
which were less than M/4; (2) one responding to sodium chloride in 
the range IM to M/64; (3) one responding to sodium chloride con- 
centrations greater than M/64; (4) one responding to sugar. Presum- 
ably there is also a mechanoreceptor. A further analysis of the 
situation in this insect has yielded the conclusion that the tarsal hairs 
contain a mechanoreceptor, a sugar receptor, and, in some cases, a 
sugar-NaCl receptor (Takeda, 1961). In 50 per cent of the hairs tested 
there was no response to NaCl. No sensitivity to quinine or acetic 
acid could be detected nor were any other kinds of chemoreceptors 
found. The only histological evidence bearing on this question is the 
description by Eltringham (1933) of the chemoreceptive hairs of 
Vanessa atalanta. No statement is made in this work of the number of 
neurons associated with each hair. 

In Leptinotarsa there are apparently five receptor cells associated 
with each hair, but the electrical picture is still unclear. Sodium chlor- 
ide evokes impulses designated by Stlirckow (1959) as h and n\ 
potassium, impulses designated as h' and n\ Stiirckow suggested that 
h and h' originate in anion receptors and n and n' in cation receptors. 
Water gives isolated low potentials; a sugar receptor is inferred; 
bending the hair provokes no clear spikes attributable to a mechano- 
receptor, although there is an unruly pattern of activity; alkaloids 
associated with plants that are unacceptable as food provoke salvos of 
spikes from two cells. 

Electrical Events Following Stimulation 

It is clear in all cases thus far studied in detail that the hairs subserving 
contact chemoreception are compound organs containing a number 
of chemoreceptors and usually a mechanoreceptor. In the fly at 
least each chemoreceptor is specifically different with regard to the 
chemicals to which it is sensitive. In all cases each receptor performs 
the dual function of reacting to the stimulus and generating nerve 



146 THE PHYSIOLOGY OF INSECT SENSES 

impulses. Each of these functions is currently the subject of intensive 
study. 

The suggestion was made by Dethier (1956) that chemicals de- 
polarize the membrane of the distal process of the neuron at the tip of 
the hair, that this depolarization travels down the nerve fibre to the 
cell body at the base of the hair, and that the action potential is gen- 
erated in this region. Studies of the effects of temperature on thresholds 
and on frequency of impulse discharge lent some support to this idea. 
When the temperature of the tip of the hair, and hence the receptor 
surface, was altered in the range 2°-41° C, no change in behavioural 
threshold occurred (Dethier, 1956), nor was there any change in the 
frequency of impulses (Hodgson, 1956 b; Dethier and Arab, 1958). 
When the temperature of the whole preparation, and hence the cell 
bodies, was altered, however, marked changes in frequency occurred 
(Hodgson and Roeder, 1956; Hodgson, 1956 b). According to 
Hodgson (1956 b), the fibres in some hairs increased their frequency 
with warming while others decreased with warming. 

The most conclusive evidence bearing on the matter came, as might 
be expected, from electrophysiological work. Wolbarsht (1958), seek- 
ing evidence for a slow potential associated with stimulation, dis- 
covered when he placed one electrode on the tip of a hair and the other 
in the crushed head or labellum that there was a resting potential of the 
order of 60 mV. Strangely enough, however, this remained unaltered 
when the hair was stimulated. He concluded that the potential repre- 
sented a difference across the basement membrane which separates 
the general body cavity and the area containing the neurons, associ- 
ated cells, and hypodermis. Later, working exclusively with the 
mechanoreceptor component of the chemoreceptive hair (and with 
simple mechanoreceptors), he recorded a graded slow potential which 
occurred when the hair was stimulated by bending. It was always an 
increase in negativity at the recording electrode. It varied directly with 
the magnitude of the stimulus and showed no overshoot when return- 
ing to the baseline. This is a receptor potential in that it occurs prior 
to the initiation of any impulses, varies smoothly, and must attain a 
critical level before any impulses are generated. It is also either the 
generator potential itself or is associated with it. Evidence was pro- 
duced that suggests that the receptor potential originates at a site that 
is not invaded by the propagated impulses and that this site is distad 
of the site of impulse generation. The geometry of the hair and the 
mechanoreceptor indicates that this must be in the distal process of the 
cell. 



CHEMORECEPTION 147 

Morita (1959), recording through the side wall of the chemorecep- 
tor hair, detected a slow d.c. potential occurring when the tip of the 
hair was stimulated (Fig. 83). When the stimulus was cither sugar or 
sodium chloride the potential was negative at the recording point with 
reference to the base of the hair; when the stimulus was quinine the 
potential was positive. The closer the recording electrode was placed 
to the tip of the hair, the greater the negativity when sugar or sodium 
chloride was applied. On the basis of these recordings Morita has 
concluded that this slow potential is indeed a generator potential 




%U^> ""'^' 




Fig. 83. A. Response of labellar 
chemosensory hair of Calliphora 
to 0-25M sucrose before (top) 
and after (bottom) crushing. B. 
Response of a hair to 0-25M 
sucrose (top), 0-25M sucrose 
plus 0-05M CaCla (middle), and 
0-05M CaCla (bottom). Time, 
-^Q- sec. (Redrawn from Morita 
and Yamashita, 1959.) 



arising at the point of stimulation and initiating impulses at the base 
of the hair. He makes no distinction between receptor potential and 
generator potential, and the presumption is that they are one and the 
same in this hair. 

The electrical sign of the impulses arising from stimulation proved 
puzzling, and an attack on this problem threw some light on the 
question of the site of impulse generation. All workers now agree that 
the initial component of the spike is positive (Morita et al, 1957; 
Wolbarsht, 1958 ; Hodgson, 1958 b). Wolbarsht (1958) interpreted this 
condition as indicating that the distal processes of the chemoreceptive 
cells act as somewhat poorly insulated extensions of the recording 
pipette into the interior of the cell. The spikes of the mechano- 



148 THE PHYSIOLOGY OF INSECT SENSES 

receptors are conceived of as being recorded by electrotonic spread up 
through the contents of the hair, which would be analogous to an 
external electrode opposite a part of the cell membrane that is not 
involved in the propagated impulse. This conception is supported by 
the results of polarization experiments. Anodal polarization produces 
stimulation; cathodal stimulation produces depression, as has been 
seen with intracellular electrodes in the eye of Limulus. 

Arab (1958) found that behavioural responses were evoked by 
cathodal stimulation and would not occur with anodal stimulation. 
Wolbarsht (1958) was able to reconcile this apparent discrepancy. He 
showed that the behavioural responses observed by Arab were due to 
the action of the current on the neurons at the bases of hairs adjacent 
to the one on which the electrodes were placed. In this case the polariz- 
ing current was extracellular; hence, cathodal stimulation was 
excitatory and anodal stimulation, the reverse. 

Working with the ^yLucilia caeser and the butterfly Vanessa indica, 
Morita and his co-workers attempted to pinpoint the site of spike 
generation (Tateda and Morita, 1959; Morita and Takeda, 1959; 
Morita, 1959; Morita and Yamashita, 1959 a, 1959 b). First, they 
showed that spikes were never recorded from the tip of a hair when it 
was severed from its base. They then confirmed the findings of 
Wolbarsht (1958) that anodal stimulation elicited impulses and 
cathodal current blocked them. They found also, as Wolbarsht had, 
that anodal stimulation of one hair blocked activity in the neighbour- 
ing hair, but they did not do a similar experiment with cathodal 
stimulation as Wolbarsht had. 

In an attempt to explain how spikes can be recorded from the tip of 
the hair, Morita (1959) cooled first the middle and then the base of the 
hair, recorded in each case from the tip, and analysed the shape of the 
spike. According to his records, cooHng the middle affected pre- 
dominantly the falHng phase of the spike, while cooling at the base 
aff'ected both the rising and falHng phases. On the basis of this evidence 
he claimed that spikes originate at the base of the hair and fire in both 
directions, that is, back along the distal process to the tip, as well as 
centripetally along the axon to the central nervous system. If this 
condition occurs, it would mean that spikes invade the area of the 
generator potential contrary to the situation found in mechano- 
receptors. 

Morita and Yamashita (1959 b) recorded simultaneously from the 
tip and the base and found that the spike at the tip is generally larger 
than the spike recorded from a hole in the side wall. They observed that 



CHEMORECEPTION 149 

the side-wall spike peaked more quickly, and they took this to mean 
that the differences in height were not due to a gradient of electrotonic 
spread. They also concluded from this result that there is back firing, 
and they argued that impulses are recorded extracellularly and not 
intracellularly as Wolbarsht (1958) concluded. 

Hanson and Wolbarsht (1962) re-examined the situation in 
PJwrmia and found that the impulse is indeed conducted some dis- 
tance down the dendrite, that distance being a large fraction, if not 
the entire length, of the short ones, but only a small fraction of the 
length of longer ones. Electrodes located at various places along the 
dendrite all showed an initially positive phase of the impulse some- 
times followed by a longer negative phase. The following interpreta- 
tion was proposed : the action potential is generated at a considerable 
distance from the recording electrode and is recorded as a positive 
swing. As the action potential invades the dendrite, the active region 
comes beneath the recording electrode and appears as a negative 
deflection. Simultaneous records from several electrodes placed 
along the dendrite show that the active region of the membrane pro- 
ceeds from the cell body toward the trip. The record resulting from 
an algebraic sum of the two phases shows the positive phase being 
abruptly terminated by the longer lasting negative phase. Cocaine, 
xylocaine, procaline, and chloral hydrate reversibly depress or abolish 
this negative phase with a correspondingly longer lasting positive 
phase. Continuous chemical stimulation or injury accentuates and/or 
speeds up the onset of the negative phase. 

The Sugar Receptor 

Since different receptor cells in a contact chemoreceptive hair respond 
specifically to different chemicals, the question of mechanism of 
stimulation, that is, how the chemicals depolarize the dendrite mem- 
brane, should be investigated separately in the various types. The types 
are most clearly delineated in the blowfly. In this insect, as already 
pointed out, there is one cell specifically sensitive to sugars and one to 
monovalent salts. A modestly detailed story of the operation of the 
sugar receptor has been constructed from behavioural studies. The 
task now presented to electrophysiology is that of proof-reading the 
story, filling in the details, and revising where necessary. 

Carbohydrates are the most effective, if not the only, stimuli; how- 
ever, this cell is highly specific and unequally sensitive to the various 
compounds. Behavioural tests in which eighty-two different carbo- 
hydrates were applied to the chemoreceptive hair housing the receptor 



150 THE PHYSIOLOGY OF INSECT SENSES 

revealed a spectrum of activity from complete unresponsiveness to 
extreme sensitivity (Dethier, 1955 a). The most effective compounds 
are certain pentoses, hexoses, and compound sugars possessing an 
a-D-glucopyranoside link. In general, the a-form of a sugar is more 
stimulating than the p-form. Among effective pentoses D-arabinose 
is more stimulating than L-arabinose. It is clear from these tests that 
the structural configuration of a sugar is its most important determi- 
nant as an effective stimulus. On the other hand, no sense can be made 
of the situation on the assumption that there is one key molecular 
structure for stimulation. 

The first intimation that there are multiple and different sites of 
action on the sugar receptor cell arose from a series of studies in which 
mixtures of sugars were found not to be effective at concentrations 
predicted from the threshold values of the individual constituents. 
There were instances of synergism and of competitive inhibition. The 
inhibitory effect of a given sugar varied, however, depending upon 
which other sugar it was mixed with at the time. For example, 
mannose, a weakly stimulating sugar, inhibited fructose, but not 
glucose; rhamnose inhibited glucose but not fructose. There was 
some evidence that sorbose inhibited both fructose and glucose 
(Dethier et aL, 1956). 

Supporting evidence for the idea of multiple sites came from an 
entirely different kind of study. Evans (1961 b) found that feeding 
blowfly larvae on a medium containing a specific sugar depressed the 
sensitivity of the adult to that sugar. Relative sensitivity to glucose 
or fructose could be enhanced or depressed by rearing in the presence 
of the appropriate sugar. Evans interpreted these results as indicating 
that the sugar reduced either the number or the affinity of sites on the 
receptor cell for that particular sugar. 

The nature of the combining action of sugars, while not understood, 
can be narrowed down somewhat by a process of elimination. An 
outstanding feature of stimulation by sugars is that no change in 
threshold can be demonstrated to take place as the temperature of the 
stimulus is changed. Nor is any change in threshold observed when the 
pH of the sugar solution is changed (Dethier, 1956). Another feature 
of stimulation by sugars is that there is no inhibition by any of the 
following metabolic inhibitors: phlorizin, fluoride, azide, idoacetate, 
cyanide (Dethier, 1955 a). This finding indicates that the first step in 
stimulation probably does not involve any steps in the glycolytic 
cycle below those blocked by the compounds listed. The absence of a 
marked temperature and pH change argues against an enzymatic 



CHEMORECEPTION 151 

reaction being involved. It was proposed tentatively (Dethier, 1956) 
that stimulation by sugars involves combination of the sugar mole- 
cules with a specific receptor site or substance by weak forces, such as 
van der Waal, to form a complex which depolarizes the membrane, 
after which (or simultaneously) sugar is removed passively by a shift 
in concentration gradient. 

At this point current knowledge of the sugar receptor ends. Few 
electrophysiological investigations of stimulation by carbohydrates 
have been reported thus far. Hodgson (1957) examined the effects of 
twenty-three carbohydrates. At that time the existence of a water 
fibre was not suspected, and the lack of this information complicated 
the interpretation of records. It appears, nevertheless, that all accept- 
able sugars stimulate one neuron, while unacceptable sugars either 
fail to stimulate or actually inhibit. 

In Vanessa indica the sugar receptor responds to i)-glucose, D- 
fructose, and sucrose in increasing order of effectiveness. Lactose, 
Z)-galactose, inositol, trehalose, and L-sorbitol are non-stimulating 
(Takeda, 1961). Maltose and turanose elicit small deformed spikes 
which have been interpreted by Takeda as indicative of a combined 
stimulatory and inhibitory action. The sugar receptor is sensitive to 
concentrations of sucrose as low as 2-'^ M. In addition to this receptor 
there is one that responds in identical fashion to sucrose and to 
NaCl. 

The Salt Receptor 

It was originally believed that rejection of a solution was triggered 
solely by activity in one neuron, and since so many compounds elicited 
rejection, it was assumed that the single neuron was grossly non- 
specific. Studies on competitive inhibition and on the action of heavy 
metal salts, however, hinted that rejection was not a single modality. 
As a consequence, it was no longer possible to assume that every 
compound that was rejected acted on the same receptor cell. 

Electrophysiological studies, while only just beginning, have par- 
tially answered the question of the adequacy of stimuH for rejection. 
They indicate that many rejected compounds block activity in all fibres 
of the chemoreceptive hairs, but that monovalent salts stimulate one 
cell actively (Hodgson, 1956 a; Morita, 1959). It has been possible to 
come to some understanding of the mechanism of action of this salt 
fibre by acquiring enough data to make the same kind of theoretical 
analysis which Beidler (1954) made of mammalian salt receptors 
(Evans and Mellon, 1962 b). 

L 



152 THE PHYSIOLOGY OF INSECT SENSES 

Beidler assumed that the stimulus reacts with some receptor sub- 
stance and that the reaction obeys the mass action law. His second 
assumption was that the magnitude of response is directly related to the 
number of ions or molecules that have reacted with the receptors. He 
derived an equation which related magnitude of response to the con- 
centration of the applied chemical stimulus. This is clR = (clRm)-\- 
iXjKRm), where c = concentration, R — magnitude of response, 
Rm = magnitude of maximum response, and K = the equilibrium 
constant. The vahdity of the equation can be tested by measuring c 
and R. Beidler found the agreement to be excellent. Now, knowing the 
equilibrium constant, he calculated the free energies of reaction from 
the expression AF = RT\n K, where AF = change of free energy, 
R = the gas constant, and T = the absolute temperature. The low 
value which he found for AF(from —1-22 to —1-37 Cal./mole) for a 
series of sodium salts was taken to indicate that physical rather than 
chemical forces are involved in the interaction between the chemical 
stimulus and the receptors. This conclusion raised the question of what 
the receptor substance may be. 

Beidler argued that the small temperature dependence and the 
low values for AF suggest a reaction similar to those that occur with 
ion binding by proteins and natural polyelectrolytes. Some properties 
of the reacting groups of the receptor substance can be determined 
from a study of the effect of changing pH. Since no effect could be 
demonstrated over the range 3-0-1 1-0, one might conclude that the 
molecules of the receptor substance are strong acidic radicals. The 
relatively weak carboxyl radical of a protein, for example, cannot be 
considered as the reacting group. The phosphate and sulphate radicals 
of such natural polyelectrolytes as nucleic acids and certain poly- 
saccharides are able to bind cations in a manner consistent with the 
properties of the receptors described by Beidler. 

The many complexities of the mammalian taste organs, as, for 
example, the receptor cell being non-neural and synaptically con- 
nected to a neuron, the multiple innervation of a receptor cell, and the 
innervation of more than one cell by a single neuron, obstructed 
further analyses of the nature of the receptor sites and the process of 
stimulation. None of these handicaps are associated with the salt 
receptor of the insect. A quantitative study of the repetitive response 
of the labellar hair receptor to NaCl has shown that Beidler's theory 
applies equally well to this receptor (Evans and Mellon, 1962 b). The 
calculated relative free energy change of the reaction between salt and 
receptor site in this case is the range to — 1 kcal./mole. This value 



CHEMORECEPTION 153 

suggests that weak physical forces are involved, and evidence has been 
obtained that the salt-combining sites are anionic and strongly acidic. 
As a consequence, the cation of a salt largely dominates stimulation. 

The Water Receptor 

The water receptor discovered by Evansand Mellon (1962 a) is the only 
cell in the chemoreceptive hair of P/wrmia that is activated by water. 
The most effective stimulus tested thus far is pure water. Aqueous 
solutions of sucrose appear to depress the activity of the cell as a linear 
function of the logarithm of osmotic pressure. At 5M sucrose the 
frequency of impulses decreases to less than half of the maximum. 
Other non-electrolytes (e.g., glycerol and mannose) also inhibit, but 
no simple relation was found between parameters of the solution and 
the degree of inhibition. Inorganic electrolytes also inhibit water res- 
ponse, but in a more specific manner. Aqueous solutions of NaCl 
begin to inhibit at 0-1 M. Inhibition appears to be complete at about 
0-3M. Calcium chloride solutions inhibit at about 0-01 M. The 
inhibition of water response is unrelated to spike activity in other 
fibres. 

Modalities 

For the blowfly it is clear that water, sugars, protein, and unacceptable 
compounds can be distinguished as different. To what extent these 
four taste categories can be subdivided into other taste modalities is 
not clear. Although there is evidence that different sugars act upon 
different sites at the molecular level, they none the less stimulate the 
same receptor. In the case of unacceptable compounds, that is, salts, 
acids, alkaloids, alcohols, etc., it is probable that different sensory in- 
put results from stimulation by the different compounds. If this 
suggestion is confirmed it provides a peripheral mechanism for dis- 
criminating among a number of compounds and indicates that the 
modality 'unacceptable' is not a homogeneous one. 

Aside from incomplete electrophysiological data obtained with 
Phormia, evidence for taste modalities has been derived principally 
from the following sources: (1) observations of the behaviour of indi- 
viduals conditioned to respond to a given chemical ; (2) determinations 
of the additive or non-additive capacity of diverse stimuli ; (3) measure- 
ment of the amount of sucrose drunk by honeybees after contamina- 
tion with subliminal concentrations of different chemicals ; (4) com- 
parison of the threshold changes for different compounds during 
starvation; (5) localization of specific kinds of receptors. Much of the 



154 THE PHYSIOLOGY OF INSECT SENSES 

information derived from these kinds of experiments is suggestive 
rather than conclusive ; nevertheless, considering all of the available 
evidence, it is highly probable that insects can do better than dis- 
criminating simply between acceptable and unacceptable. 

Bauer (1938) trained Dytiscus marginalis and Hydrous piceus to res- 
pond positively to sucrose; these animals could not be trained simul- 
taneously to avoid glucose, and also reacted positively in the majority 
of cases to some fifteen or twenty other sugars and sugar derivatives. 
As in the experiments of Schaller (1926) and Ritter (1936) with the 
same or related species, the beetles learned readily to distinguish be- 
tween pairs chosen from sucrose, sodium chloride, acids (hydrochloric 
and acetic), and quinine, and could even be trained to accept quinine 
and avoid sodium chloride. But specimens that had learned to avoid 
hydrochloric acid also avoided acetic and could not be taught to 
respond differently to the two; the same result was obtained when 
quinine was matched against salicin or aloin. Bauer concluded that the 
sweet substances (with the possible exception of mannose, which was 
avoided by some individuals) constitute a single homogeneous 
grouping; salts, acids, and bitter substances, normally avoided, are 
distinguished from sweet and from each other, so that taste sub- 
stances can be classified into the same four quahties for these beetles 
as for man. 

As mentioned above in the discussion of methods, von Frisch (1935) 
found additive the stimulatory effects of all sugars acceptable to the 
bee. Summation was noted also between sodium chloride and lithium 
bromide, ammonium bromide, or hydrochloric acid, but the repellent 
effect of quinine was lessened rather than enhanced by the addition of 
acids (hydrochloric, acetic, sulphuric, citric, lactic). When sucrose 
solutions, one containing sodium chloride and another quinine hydro- 
chloride, were prepared and were accepted by equal proportions of 
the bees they were drunk in different amounts. Almost as much of the 
quinine was taken as of the control, but considerably less of the 
solution containing salt. The results would indicate three taste 
qualities: sweet, acid-salt, and bitter. But in other experiments von 
Frisch found that starved bees show no better acceptance of sodium 
chloride than those fully fed, although the threshold for rejection of 
quinine rises eight times and that for hydrochloric acid by a factor of 
five. He concluded therefore that salt represents a quality different 
from either acid or bitter. Furthermore, although there is no summa- 
tion of repellency between quinine and acids, other bitter substances, 
such as aloin, arbutin, colocynthin, and salicin, are rendered more 



CHEMORECEPTION 155 

repugnant by the addition of hydrochloric acid, so that the category 
bitter is not homogeneous for the bee. It is possible that investigations 
of this kind would reveal similarly complex relationships in man. 

Other evidence as to the separation of the taste qualities in insects 
was provided by Ritter ( 1 936), who found that after amputation of the 
maxillary palpi specimens of Hydrous piceus would still react to 
0'007M hydrochloric acid but not to salt, sugar, or quinine. Removal 
of the tips of the labial palpi then abolished the response to acid, 
although animals lacking both sets of palpi and the antennae still 
reacted positively to meat juice, presumably via receptors in the mouth. 
These observations would seem to set the acids apart from the other 
taste substances, but are at variance with the findings of Bauer (1938) 
with the same and related species, and of Hodgson (1951) with 
Laccophihis. Bauer found that amputation of the maxillary palpi left 
the gustatory response to sucrose, etc., unaltered except for an increase 
in threshold. Hodgson found by ablation experiments that all the head 
appendages could mediate responses to acids, salts, and alcohols. 
Thresholds were increased considerably when the antennae were re- 
moved, but less so when either pair of palpi were extirpated. 



CHAPTER VI 



Response to Humidity 



The behavioural responses of insects to water vapour mixed with the 
permanent gases of the atmosphere indicate that these organisms 
somehow perceive the water or differences resulting from changes in 
the concentration of the vapour. A unique feature of water is its pres- 
ence both in the organism and in the environment. The existence of 
water on both sides of the integument poses problems that are not 
encountered in the case of other stimuli. Conceivably water may act on 
the organism independently of what is within (as do, for example, 
odour molecules), or it may cause outward movement of internal water 
so that the insect does not respond directly to a change in external 
environment but rather to a change induced in its own internal 
environment. For these reasons, and because all attempts to under- 
stand the mechanism of hygroreception have been based upon experi- 
ments which correlate the degree of activity or direction of movement 
with the amount of water in the air, decisions must be reached as to 
which relationship of water vapour to atmosphere gases is to be meas- 
ured. If humidity receptors are conceived of as responding to the con- 
centration of water molecules, then the absolute concentration of 
water to which they are exposed should be measured. On the other 
hand, if the humidity reactions are conceived of as operating through 
the agency of evaporation or transpiration, then the drying power 
of the air is the variable to be measured. 

Conventionally there are a number of humidity definitions (Humph- 
reys, 1 940). The absolute humidity is either themass of water vapour per 
unit volume or the gas pressure exerted by the water vapour per unit 
area. Relative humidity is the ratio of the actual mass of water vapour 
in a small volume to the maximum mass that can exist in the same 
volume at the same temperature. It is also defined as the ratio of the 
actual to the maximum pressure of water vapour per unit area that can 
exist in the presence of a flat surface of pure water at the same temper- 
ature. Saturation deficit may be defined as: (1) the amount of water 
vapour in addition to that already present, per unit volume, necessary 
to produce saturation at the existing temperature and pressure; 
(2) the difference between actual and saturation pressure; (3) the ratio 

156 



RESPONSE TO HUMIDITY 157 

of the vapour pressure deficit to the saturation pressure at the existing 
temperature. 

Absolute humidity in mass per volume is difficult to measure. Con- 
ventionally one measures relative humidity. In an attempt to measure 
the drying power of the air many investigators measure saturation 
deficit (Anderson, 1936). Leighly (1937) and Thornthwaite (1940) 
have pointed out that evaporation is a physical process dependent 
upon a vapour pressure gradient between the evaporating surface and 
the air and is not directly related to relative humidity or to saturation 
deficit in the air. Hence, saturation deficit is of no value as an indicator 
of moisture losses by evaporation or transpiration (see also Ramsay, 
1935; WeUington, 1949; Edney, 1957). 

Responses to water vapour include: orientation from a distance to 
high concentrations of water vapour, proboscis responses to water 
vapour in the immediate vicinity, avoidance of regions of high and low 
humidities, and aggregation in zones of preferred humidity. 

Just as the degree of hunger or satiation influences the response of 
insects to food, so also does the state of water balance (and starvation) 
influence the behavioural response to humidity. Desiccated flour 
beetles {Tribolium castaneum) reverse their preference for humid areas 
after water has been provided. The intensity of the reaction to dryness 
also increases with increased starvation (WiUis and Roth, 1950). 
Similarly, the cockroach Blatta orientalis, which prefers lower 
humidities when its water balance is optimum, becomes hygropositive 
when desiccated (Gunn and Cosway, 1938). Comparable reversals 
have been demonstrated for the beetle Ptinus tectus (Bentley, 1944), 
Drosophila (Perttunen and Erkkila, 1952), Aedes, and Tenebrio molitor 
(Dodds and Ewer, 1952). It is clear from these and other studies not 
only that a water deficit in the body elicits a moist reaction but also that 
the presence of a maximum amountof water in the body elicits a dry 
reaction (Perttunen, 1951; Syrjamaki, 1962). Other factors that 
influence response to humidity are age (Perttunen and Ahonen, 1956; 
Perttunen and Salmi, 1956; Syrjamaki, 1962), diurnal rhythms 
(Perttunen, 1953), stage of the reproductive cycle (Perttunen, 1955 a), 
stage of development (Hafez, 1950, 1953), sex (Roth and WiUis, 
1951 c; Perttunen and Ahonen, 1956; Syrjamaki, 1962). 

Most of our speculation regarding the physiology of hygroreceptors 
is based upon analyses of behavioural responses to humidity gradients. 
The following species have been studied in some detail: Locusta 
migratoria migratorioides (Kennedy, 1937), Blatta orientalis (Gunn 
and Cosway, 1938), Culexfatigans (Thomson, 1938), Tenebrio molitor 



158 THE PHYSIOLOGY OF INSECT SENSES 

(Pielou, 1940; Pielou and Gunn, 1940), Pediculus humanus corporis 
(Wiggles worth, 1941), Agriotes osbcurus and A. lineatus (Lees, 1943), 
Ptinus tectus (Bentley, 1944), Choristoneura fumiferana (Wellington, 
1949), Tribolium spp. and Sitophilus (Willis and Roth, 1950; Roth and 
Willis, 1951a, 1951b, 1951 c), Aedes gracilis and Blethisa multipunctata 
(Perttunen, 1951), Blatella germanica and Aedes aegypti (Roth and 
Willis, 1952), Drosophila (Perttunen and Syrjamaki, 1958; Perttunen 
and Erkkila, 1952; Syrjamaki, 1962), Neodiprion americanus bank- 
sianae and A^. lecontei (Green, 1954), Oncopeltus fasciatus (Andersen 
and Ball, 1959), Melanoplus binttatus (Riegert, 1958, 1959, 1960), 
Schistocerca gregaria (Aziz, 1957 a, 1957 b). The strength of reaction 
and the ability to discriminate differences in humidity varies among 
the species. With Locusta migratoria migratorioides, which aggregates 
in dry microclimates, more individuals respond as the gradient be- 
comes steeper. With Culex fatigans, Tenebrio molitor, which avoid 
high humidities, and Agriotes spp., which avoid low humidities, the in- 
tensity of the reaction is related to the highest humidity. Ptinus tectus 
reacts most intensely at low humidities. Culex discriminates 1 per cent 
differences in the range near 100 per cent relative humidity, but reacts 
only to 50 per cent differences in the range of relative humidity from 
30 to 85. rr/Z>6>//wm c<3^/<3«ewm discriminates between humidities differ- 
ing by 15 per cent over the entire range. Reactions to differences of 
5 per cent are weak between R.H. and 5, absent between R.H. 40 and 
45, 45 and 50, and 50 and 55, but strong between R.H. 95 and 100. The 
louse also discriminates better at higher humidities. Wireworms detect 
the difference between R.H. 100 and 95-5. Normal undesiccated 
Drosophila melanogaster of both sexes exhibit an intensity of reaction 
that is correlated with the degree of the higher alternative rather than 
with the difference. When alternate humidities lie between 100 and 
87 per cent R.H., the drier is preferred ; when they He between 77 and 
20 per cent the wetter is preferred (Perttunen and Syrjamaki, 1958). 

The reactions of some species to a given relative humidity have been 
studied at different temperatures. The results have been interpreted as 
indicating that the reactions of Culex and Tenebrio are more in accord 
with relative humidity than with saturation deficiencies, while the 
reverse is true of Agriotes. What this may mean is difficult to know. 
Although the results are interpreted by some as indicating that the 
receptors act as evaporimeters, the lack of correlation between satur- 
ation deficit and evaporation weakens the argument (cf. Thorn thwaite, 
1940). On the other hand, in studies conducted with spruce budworm 
larvae (C. fumiferana) and sawfly larvae of the genus Neodiprion a 



RESPONSE TO TTUMIDITY 



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160 THE PHYSIOLOGY OF INSECT SENSES 

relation between locomotory behaviour and rate of evaporation has 
clearly been demonstrated (Wellington, 1949; Green, 1954). No in- 
formation is available with regard to the receptors involved. It is 
possible that the response is mediated by rather general changes in the 
internal milieu rather than by specific sense organs. 

The identity of humidity receptors is even less firmly established 
than that of olfactory receptors. In Tenebrio responses to humidity are 
aboHshed when the antennae are extirpated or completely covered. 
The most common sensilla are pits and pegs, the latter being confined 
to the seven distal segments. The intensity of response is greatly de- 
creased when the seven distal segments are removed, but complete 
abolition requires removal of the additional segments which bear only 
pits. Asymmetrical amputation has shown that a threshold number of 
pits is required (Pielou, 1940). In Tribolium but not in Sitophiius, 
similar ablation experiments have shown that there is a correlation 
between the number of thin-walled sensilla and the intensity of res- 
ponse (Roth and WilHs, 1951b). The sensilla are simple or multiply 
branched pegs. On the antennae of the human louse there are humidity 
receptors which are distinct from the olfactory receptors (Wiggles- 
worth, 1941). They are tufted sensilla; each consists of a minute cone 
bearing four delicate apical hairs. A number of neurons are associated 
with each sensillum. Similar sensilla are the humidity receptors of the 
larva of Musca domestica (Hafez, 1950, 1953) and of Drosophila 
melanogaster (Benz, 1956). In grasshoppers the sensilla coeloconica 
have been suggested as humidity receptors (Aziz, 1957 b; Riegert, 
1960), but there is no supporting experimental evidence (Slifer, 1961). 
By studying antennaless mutants of Drosophila Begg and Hogben 
(1946) came to the conclusion that the antennal receptors mediated 
positive responses to wet and that responses to dry were mediated by 
receptors at other unknown locations on the body. Perttunen and 
Syrjamaki (1958) came to exactly the opposite conclusions and pro- 
posed an explanation of the discrepancy. Kuwabara and Takeda 
(1956) conditioned honeybees to extend the proboscis when water 
vapour was held near the antennae and then amputated various lengths 
of antennae. They concluded that the sensilla ampullacea were most 
probably the hygroceptors. Bursell (1957) found that the normal 
orthokinetic response of the tsetse fly Glossina morsitans was abolished 
when the branched hairs guarding the thoracic spiracles were 
removed. 

How the hydroreceptors operate is still a mystery. They could res- 
pond directly to water molecules striking the surface; they could 



RESPONSE TO HUMIDITY 161 

permit evaporation of internal water, with a consequent change in 
chemical composition or osmotic pressure in the milieu of the recept- 
ors or by mechanical deformation ; they could respond to temperature 
changes due to evaporation; they could act as hygrometers, i.e., 
structures with special hygroscopic properties (Pielou, 1940). In some 
instances (e.g., spruce budworm) responses may not be mediated by 
special receptors at all but rather by means of general changes in the 
body fluids occasioned by evaporation through non-sensory areas. 
For a recent discussion of these matters, the paper of Syrjamaki (1 962) 
should be consulted. 



CHAPTER VII 



Photoreception 



The range of radiations in the electromagnetic spectrum extends from 
about 10^2 to about 10~^ m,a. Only a very small segment of this spec- 
trum, from about 253 to 700 m[i, can be detected by organisms. The 
prime requisite for receiving the radiant energy of this narrow band of 
the spectrum is a pigment or pigments that will absorb in these wave- 
lengths. For the organism to derive useful information from this 
energy absorption, bioelectric potentials must be produced. In insects, 
cells capable of accomplishing these ends are grouped together in three 
organs: the compound eyes, the dorsal ocelli, the lateral ocelH. Of 
these the compound eyes, by virtue of their predominant role in be- 
haviour and their extraordinarily large complement of cells, are by far 
the most important. These great sensitive spots on the surface of the 
head, with no lids to shield them, are in a continuous state of activity 
from the light impinging upon them during the lifetime of the insect. 

THE COMPOUND EYE 
Structure 

The principal components of the compound eye are the monopolar 
neurons that absorb radiant energy and generate action potentials and 
the transparent areas of the cuticle and internal lenses overlying them. 
Since cuticle overlies all of the body surface, transparency, or at least 
translucency, is a sine qua non for the functioning of the photo- 
receptors. Further modification of the cuticle, however, in respect to 
shape has given it the added property of gathering light. Together with 
clear cellular bodies, the crystalline cones, it constitutes a lens system, 
the dioptric apparatus of the eye. 

The compound eye is a collection of sensilla known as ommatidia 
(Fig. 6). Each ommatidium is constructed of a corneal lens, a crystal- 
line cone, a number of primary neurons, and enveloping cells. In 
primitive insects (e.g., Machilis, one of the Thysanura) the two cells 
which secreted the cornea lie immediately beneath it, that is, between 
the cornea and the crystalline cone. In most insects these cells with- 
draw to a position on either side of the crystaUine cone where, having 
become pigmented, they are called corneal pigment cells. 

162 



PHOTORECEPTION 163 

Beneath the corneal lens lies the crystalline cone. There are three 
types of cones. In one, four cells undergo changes in which a fused 
intracellular body consisting of protoplasmic ground substance and 
glycogen is formed (Fyg, 1960). The nuclei are located at the outer or 
basal border of the cone (eucone type). In another type the cone cells 
secrete a transparent material while themselves remaining distinct 
(pseudocone type). In still other eyes no vitreous body is formed, the 
cone cells being the only occupants of the area (acone type). 

The primitive number of retinula cells in an ommatidium is prob- 
ably eight (Snodgrass, 1926), but one is usually rudimentary or 
eccentrically placed. The arrangement of the remaining seven varies 
greatly from one species to another. Sometimes one occupies a basal 
position so that only six contribute to the formation of the rhabdom. 
Sometimes the cells are clearly arranged in two layers, three proximal 
and four distal. More commonly, all cells are in a single layer around 
a central axis. 

The sensory cells appear like bipolar neurons early in their develop- 
ment (Fyg, 1960), but when fully developed are unipolar, dendrites 
being absent. In the place of dendrites the surfaces of the cells facing 
the central axis are modified into peculiar structures, the rhabdomeres 
(Fig. 6). These are the receptive surfaces of the cells (Schultze, 1868; 
Grenacher, 1879). 

Together the rhabdomeres of all retinal cells form a rod, the 
rhabdom. Some workers had considered the rhabdom to be cuticular 
(Machatschke, 1936), but the specificity of the test upon which this 
claim is based is open to question and other tests for chitin have given 
negative results (Richards, 1951). Other students of the eye had con- 
sidered the rhabdomeres to be modified neurofibrillae traversing the 
interior of the cell. The structure of the rhabdom as revealed by 
electron-microscopy is open to different interpretations. Information 
is now available on Musca domestica. Apis mellifera, the phalaenid 
moth Erebus odora, a species of skipper Epargyreus, two grasshoppers, 
Dissosteira spp. and Schistocerca spp. (Fernandez-Moran, 1956, 
1958), Drosophila melanogaster (Fernandez-Moran, 1956, 1958; 
Wolken, Capenos, and Turano, 1957), Sarcophaga bullata, and 
Anax Junius (Goldsmith and Philpott, 1957). 

The ommatidia of Musca, Sarcophaga, Drosophila, and Apis are 
similar. Each is of the apposition type. Of the eight retinal cells only 
seven contribute to the rhabdom, the eighth being shorter. In cross- 
section each cell is roughly wedge-shaped. The rhabdomere appears as 
a rod or beading extending the length of the medial surface (Fig. 87). 



164 THE PHYSIOLOGY OF INSECT SENSES 

It is 60-70 [I long and about 1 -5 [x in diameter (Mused). A longitudinal 
section of a rhabdomere reveals that it consists of closely packed 
parallel tubules aligned at right angles to the long axis of the cell 
(Fig. 84). Each is about 400 A. in diameter and 1,000-15,000 A. long. 
The most reasonable interpretation of these tubules is that they are 
microvilli, that is, finger-like evaginations of the retinal cell; conse- 
quently, their boundaries are part of the cell membrane and their 
contents are extensions of the cytoplasm (Miller, 1957; Goldsmith and 
Philpott, 1957; Fernandez-Moran, 1958; Slifer, 1961). A fine parti- 
culate component appears in the microvilli in fixed material. Except 
for the small one, the rhabdomeres appear to occur as pairs, one 



Fig. 84. A. Distal tip of retinal cell 
from the compound eye of 
Musca domestica as recon- 
structed by Slifer (1961) from 
electron-micrographs of Fer- 
nandez-Moran (1958). B. 
Cross-section of cell with rhab- 
domer at right. C. Section 
through that part of rhabdomer 
containing microvilli. (Re- 
drawn from Slifer, 1961.) 






member of which lies opposite its twin on the far side of the ommati- 
dium. The longitudinal axes of the microvilli in both members of a 
pair are parallel but in a different plane from those of other pairs. The 
core separating the rhabdomeres is a loose network of fine filaments 
in fixed materials. In the eye of the grasshoppers Dissosteira and 
Schistocerca the fine filaments in the matrix are closely packed and run 
lengthwise in orderly courses. Distally this core disappears as the 
rhabdomeres come together just below the crystalline cone. Here the 
microvillar structure is replaced by an electron-dense structure. In the 
eye of the dragonfly Anax Junius and in the superposition eye of the 
moth Erebus odora there is no central matrix, since the rhabdomeres 
meet axially. The rhabdom of the skipper consists of eight fused 
rhabdomeres. Most workers believe that the visual pigment is located 



PHOTORECEPTION 165 

in the rhabdomeres, that is, in the lumina of the microviUi. In Erebus 
there is an extensive underlying structure, the tapetum, composed of 
tracheoles which are highly reflective (Fernandez-Moran, 1958). 

The retinal cells may occupy one of the two positions with respect to 
the crystalline cone (Fig. 6). In apposition eyes the retinal cells lie 
immediately beneath the crystalline cone; in superposition eyes the 
retinal cells are situated some distance proximad of the crystalline 
cone. The intervening space is transparent. In all eyes each ommati- 
dium is enclosed in pigment cells. The number of pigment cells is not 
constant, but usually there is a distal set (iris pigment cells) surround- 
ing the crystalline cone and another set (retinal pigment cells) 
surrounding the retinal cells. 

At the base of the ommatidia, and marking the proximal limit of the 
retina, is a fenestrated basement membrane. Through the fenestrae 
pass the proximal processes, the axons, of the retinal cells. There is 
usually one axon for each cell. In Erebus, however, there are sometimes 
nine axons from a single ommatidium. This occurrence indicates that 
sometimes the axons begin to branch close to the cell body. Some 
synapse almost immediately with neurons of the optic lobe; others ex- 
tend a considerable distance into the lobe before synapsing. The 
presence of two kinds of retinal fibres, long and short, has been known 
for some time. Hanstrom (1927) had speculated upon the possible 
physiological differences between the two and likened them to the 
rods and cones of the vertebrate eye. 

The optic lobes are in fact a part of the brain, but since so many 
physiological studies of the eye treat them as part of the eye rather 
than as the central nervous system, a brief description at this point will 
be helpful. Most of our knowledge of these complicated structures 
stems from the classical studies of Zawarzin (1914) on the larva of the 
dragonfly Aeschna, Cajal (1909, 191,8) and Cajal and Sanchez (1915) 
on the house fly and the blowfly. In addition, there are the accounts of 
Giinther (1912) and Holste (1923) on Dytiscus, Bretschneider (1921) 
on the moth Deilephila euphorbiae, and Power (1943) on Drosophila. 
The general works of Hanstrom (1928) and Snodgrass (1935) should 
also be consulted. 

The optic lobe (Fig. 85) is divided into three areas: the lamina 
ganglionaris, usually in immediate contact with the basement mem- 
brane of the retina; the medulla externa; the medulla interna. 

The lamina ganglionaris is the first or most distal synaptic layer of 
the optic lobe. It consists of giant monopolar cells, small monopolar 
cells, short retinal fibres, long retinal fibres, and centrifugal fibres. 



166 



THE PHYSIOLOGY OF INSECT SENSES 




Fig. 85. Simplified diagram of the neural pathways within the optic lobe of 
Calliphora. R, retina; I, lamina ganglionaris ; II, medulla externa; 
III, medulla interna; OC, outer chiasma; IC, inner chiasma. (Redrawn 
from Cajal and Sanchez, 1915.) 

After the axons of the retinal cells traverse the basement membrane 
about one from each ommatidium passes directly to the lamina, 
while its five or six companions turn immediately at right angles, 
forming local chiasmata with those of other ommatidia. The axons 
then enter the lamina in groups or bundles, each bundle consisting of 



PHOTORECEPTION 167 

axons from several ommatidia. Each bundle in the lamina becomes 
associated with the axon of a giant monopolar cell, with which most 
of the retinal fibres synapse, and the axon of the centrifugal cell whose 
cell body lies in the medulla externa. The units ('optic cartridges' of 
Power) in the lamina thus consist of a long retinal fibre, a number of 
short retinal fibres, a giant monopolar fibre, and a centrifugal fibre. 
These fibres now enter the outer chiasma. Fibres from the anterior 
ommatidia cross to the posterior region of the medulla externa; 
fibres from the posterior ommatidia cross to the anterior area of the 
medulla externa; fibres from the middle ommatidia pass directly 
through the chiasma without crossing. All fibres from the lamina 
ganglionaris end in the medulla externa. At the present state of our 
knowledge of the eye there is little point in pursuing the complexities 
of the optic lobe beyond this level. 



The Function of the Retinal Cells 

It is generally assumed that the photosensitive pigment is located in 
the retina cells. As yet there is no direct evidence for this. Prior to 1957 
all attempts to isolate a visual pigment failed (Goodwin and Srisukh, 
1949; Wald and Burg, 1957; Wolken, 1957; Wolken, Mellon, and 
Contis, 1957), but Goldsmith (1958 a) was finally able to isolate 
retinene from the heads of honeybees. It had the specific absorption 
peak 664 mii. Since no retinene was obtained from parts of the body 
other than the head and since retinene previously has been found only 
in eye tissues, Goldsmith concluded that it is the chromophore of a 
visual pigment located in the compound eyes and/or ocelli. He found a 
pigment that possesses a wavelength maximum at about 440 mu.. On 
bleaching in light the maximum moves to 370 m[i, probably represent- 
ing the formation of retinene (Goldsmith, 1958 b). Spectral sensitivity 
measurements of the eyes of honeybees reveal several peaks at diff*er- 
ent wavelengths, one at 440 mjx (compound eye of drone). This is the 
only light-sensitive pigment containing retinene that has been ex- 
tracted from insect eyes thus far. Bowness and Wolken (1959) isolated 
from the house fly a yellow pigment with a spectral absorption maxi- 
mum at 437 mil when unbleached and at 440-446 and 350-360 my. 
when bleached, but neither vitamin A nor retinene was detected in this 
pigment. The work on colour vision suggests that there are others with 
maxima at different wave lengths. 



M 



168 THE PHYSIOLOGY OF INSECT SENSES 

Electrical Events 

An electrophysiological attack on the action of retinal cells has been 
pushed with more vigour than the biochemical, but, for reasons that 
will become apparent, the results so far have a high degree of 
ambiguity. 

It has been known for nearly a century that retinae give an electrical 
response to light. This response, the electroretinogram, is usually 
detected by placing one electrode on the surface of the cornea and the 
other at any point on the body. Considering the neural complexity of 
the eye, this is a relatively crude measurement to make. It should be 
apparent that the electroretinogram (ERG) is a mass effect dependent, 
as Granit (1955) has pointed out, upon the favourable orientation of 
certain retinal structures which conduct currents in one direction. 
Furthermore, the second electrode, the so-called indifferent electrode, 
is not necessarily indifferent (cf. Granit, 1955). 

For these reasons and also because the profile of the potential 
changes recorded from the eye differs in form and magnitude with the 
location of the electrodes, the intensity of illumination, the duration of 
illumination, the degree of Hght or dark adaptation, the time of day 
(Jahn and Wulfif, 1941a, 1941b, 1943), the temperature (Ishikawa and 
Hirao, 1960 c), the age of the preparation (Hassenstein, 1957; Naka 
and Kuwabara, 1959), the amount of blood lost (Ruck and Jahn, 
1954), the amount of pressure applied to the body (Autrum and Hoff- 
mann, 1960), the species of insect, the individual (HartHne, 1928), and 
the characteristics of the recording apparatus, it is understandable that 
there is great difficulty in interpreting ERGs and reconciling the results 
reported by one laboratory with those reported by another. These 
difficulties will become apparent below. None the less, hidden in the 
ERG is the code to some of the primary events that occur in photo- 
receptors when they are stimulated by light, and ERGs have been 
studied intensively in the hope that they will yield bits of this infor- 
mation. 

ERGs have been recorded from a large number of insects. The first 
ever obtained (from Melanoplus differ entialis, M. femur-rubrum, 
Chortophaga viridisfasciata, Vanessa atalanta, Bombus pennsyh aniens, 
Musca domesticd) were described by Hartline (1928) as being essen- 
tially similar to one another and consisting exclusively of negative 
components. These included a rapidly rising wave (which he desig- 
nated as A and later workers as b) whose decay was interrupted by a 
slowly rising wave (his B and the c of others). The off-effect was merely 



PHOTORECEPTION 169 

a decay of the c wave. Up to 0-08 seconds the Bunsen-Roscoe law 
held. The many differences in the profiles of the ERGs were interpreted 
as being due to differences in the form and magnitude of the two 
negative waves. 

Melanoplus was again studied ten years later (Jahn and Crescitelli, 
1938; Crescitelli and Jahn, 1939) as were the grasshoppers Trim- 
erotropis citrina and T. maritima (Jahn and Wulff, 1942). The ERG 
was essentially similar to that reported by Hartline; however, this 
time it was reported as beginning with a weak positive wave (a) promi- 
nent in some eyes, absent in others, and abolished by light adaptation. 
In addition, a negative off-effect {d wave) occurred in the form of a 
small hump on the c wave. The moth Samia cecripoa was reported to 
have a similar ERG except that a d wave was never seen (Jahn and 
Crescitelli, 1939). But for Galleria mellonella Taylor and Nickerson 
(1943) reported a, b, c, and occasionally (i waves. 

The ERG of the water beetle Hydrous triangularis showed in its 
most complicated form (high intensity, night eye) a simple negative 
profile consisting of b and c waves only, while Dytiscus fasciventris 
in similar circumstances showed a, b, and c waves (Wulff and Jahn, 
1943). On the other hand, Bernhard (1942) described the ERG of 
Dytiscus as being a simple b and c wave. 

In the grasshopper Dissosteira Carolina the profile obtained was 
totally negative, consisting oib and c waves and only occasionally a d 
wave (Taylor and Crescitelli, 1944). The most marked departure from 
form encountered was an occasional ERG, in which, after the initial 
negative response to illumination, there was a long, slow, positive 
swing. A similar ERG had been reported by Hartline (1928) for 
Chortophaga viridisfasciata. The ERG of the cockroach Periplaneta 
americana was reported as a simple negative wave (Ruck, 1958 a; 
Walther, 1958 a, 1958 b), as were also the ERGs ofTachycines, Dixi- 
ppus, and the nymph of AescJma (Autrum, 1948 a, 1948 b, 1950). 

For all of the species mentioned thus far everyone agrees that the 
usual ERG is essentially a cornea-negative swing. Depending on con- 
ditions and species, it may or may not have an initial a wave and a final 
i/ wave. There may be negative and positive after-effects. 

Disagreement arises when the ERGs for Diptera and Hymenoptera 
from different laboratories are compared. For Musca domestica 
Hartline (1928) stated that the ERG was similar to that of the other 
species he studied, i.e., a negative potential consisting of components 
b and c, but in a later record (Hartline, Wagner, and MacNichol, 
1952) the ERG appeared with a small positive a wave at the on-point 



170 THE PHYSIOLOGY OF INSECT SENSES 

and a small short negative d wave at the off. For Eristalis and Sarco- 
phaga Hassenstein (1957) recorded an ERG with a very pronounced 
positive on-effect followed by a slower negative wave and terminated 
at the end of stimulation with a sharp negative off-efifect. These on- 
and off-effects have the sign and position of the a and d waves res- 
pectively. For Lucilia Kuwabara and Naka (1957) and Naka and 
Kuwabara (1959) showed a simple positive monophasic wave at low 
stimulus intensities. For Phormia regina the records of Ruck (1958 b) 
showed at high intensities a small positive a wave and complex multi- 
phasic waves with prominent negative components. The ERGs for 
Apis mellifera and the dragonfly Pachydiplax longipennis were similar. 
In his original papers Antrum (1948 a, 1948 b) described the ERG of 
Calliphora as a diphasic response consisting of a spike-like positive 
on-effect and a similar but negative off-effect (in these reports the po- 
tential sign was incorrectly reversed but corrected in later papers). 
With short flashes of light the wave was smoothly diphasic; with a 
stimulus of long duration the positive wave returned to a line of zero 
potential which continued until the off-effect. At high stimulus in- 
tensities Antrum reported a *negatives Zwischenpotential*, and in a 
later paper (Antrum and Hoffmann, 1960) figured the 'normal' ERG 
as having a pronounced negative wave between the on- and off-effect. 
The positive on-effect is sometimes preceded by a small negative wave 
(Antrum, 1950; Kirschfeld, 1959). Similar ERGs have been described 
for Apis, Bombus, Vespa, and the adult of Aeschna (Antrum and 
Stoecker, 1950; Antrum and Gallwitz, 1951). 

Antrum decided that there are two fundamentally distinct kinds of 
ERGs in insect eyes, the one, the Dixippus-typQ, purely negative and 
monophasic, the other, the Calliphora-typQ, diphasic. In the first cate- 
gory ('slow') he placed all of the slow-flying, night-flying, and aquatic 
species (e.g., most Orthoptera, Blatteria, Lepidoptera, aquatic 
Coleoptera, and dragonfly nymphs) ; in the second category ('fast'), 
the rapidly flying species (Diptera and Hymenoptera). 

The wave forms of 'slow' and 'fast' eyes do not appear so radically 
different in the records of most workers as they do in the records of 
Antrum, Hassenstein, and Kirschfeld. Whereas the on- and off-effects 
are the prominent features of the 'fast' eye as described and the slow 
negative potential is negligible, the reverse is generally true in records 
from other laboratories. Antrum has maintained that carefully 
handled, fresh preparations are required to give reliable ERGs, and 
both Hassenstein (1957) and Naka and Kuwabara (1959) have shown 
that the ERGs of flies become monophasic as the preparation ages 



PHOTORECEPTION 171 

(about three hours). In all of the earlier work the preparations were in- 
tentionally allowed to stand for approximately three hours in the dark 
to stabilize. On the other hand, it is clear from all records that the 
ERGs of Diptera and Hymenoptera are more complicated than those 
of Orthoptera. Autrum (1950) suggested that those of Lepidoptcra, 
with their small a waves, may represent an intermediate form. 

According to Autrum, there are fundamental physiological differ- 
ences, other than wave form, between 'slow' and 'fast' eyes. The 'slow' 
ERG increases in magnitude with increase in stimulus intensity, it 
changes markedly with light and dark adaptation, it responds poorly 
to flickering light. Above frequencies of forty-fifty flashes per second 
it fails to follow the stimulus. For stimuli of durations up to about 0-08 
seconds, the magnitude of response is related to energy (intensity x 
time). The 'fast' ERG increases in magnitude with an increase of 
stimulus intensity, it is unaffected by light and dark adaptation, its 
absolute sensitivity is less than that of 'slow' eyes {Tachycines is 
approximately 140 times more sensitive than Callfphora), it follows 
flicker up to about 300 flashes per second, the rate depending upon 
stimulus intensity and temperature. The on-effect for all stimuli longer 
than 5 msec, is dependent only upon intensity; the off-effect in the 
range 5-200 msec, is dependent upon the total energy (i.e., intensity x 
time). Ruck (1958 a, 1958 b), on the other hand, maintained that 'slow' 
and 'fast' eyes differ only in their flicker fusion frequency and that the 
wave form of the ERG, absolute sensitivity, and rate of dark adapt- 
ation are independent visual functions not necessarily related to each 
other, to the flicker fusion frequency, or to the form of the ERG. In 
contesting these conclusions, Autrum and Hoffmann (1960) demon- 
strated that subjecting the eye of Calliphora to oxygen lack (0-1 per 
cent O2 plus 99-9 per cent N2) caused the ERG to revert to a mono- 
phasic negative type until reoxygenated. The flicker fusion frequency 
of this negative ERG drops to 60 per second ; it is very sensitive to light 
adaptation. It was also pointed out that damage to the eye and long 
use of preparations leads to the conversion of the diphasic potential 
into a slow monophasic potential. The observations of Hassenstein 
(1957) and Naka and Kuwabara (1959) confirm this. It is noteworthy 
that in practically all of the work reported prior to 1948 preparations 
were held for a period of one to four hours in the dark in order to 
stabilize. 

The shape of even the simple 'slow' type ERG has suggested to all 
workers that it is the summation of several components. Even the 
ERG of Limulus, the simplest of them all, is now believed to be dual 



172 THE PHYSIOLOGY OF INSECT SENSES 

(Wulff, 1950). Hartline (1928) considered that there were two negative 
waves in the ERGs of insects (his A and B). Bernhard (1942) also 
believed that in Dytiscus the ERG is made up of two negative waves, a 
slow (S) and a rapid (R). In the dark-adapted state and at low in- 
tensities R predominates; in the light-adapted state and high 
intensities, S. He believed that R represents receptor activity and S is 
in some way related to adaptation. Jahn and Wulff (1942) beHeved that 
the ERGs of the grasshoppers Trimerotropis citrina and T. maritima 
represent the sum of a positive and a negative wave. Taylor and 
Crescitelli (1944) also assumed two components of opposite sign in 
the ERG of Dissosteira, but did not completely abandon the idea that 
the negative component itself might in fact consist of two waves. In 
Galleria the a wave of the ERG was considered by Taylor and Nicker- 
son (1943) to result from the interaction of two components. For the 
more complicated, i.e., the *fast' type ERG, Antrum (1950) considered 
that the negative off-effect is the homologue of the R component of the 
'slow' type ERG and that the R component is a constant feature of all 
ERGs. 

The compound nature of ERGs suggested that different components 
have different origins. Roeder (1940) had found that extirpation of the 
optic ganglion of Melanoplus did not abolish the slow wave of nega- 
tivity characteristic of the ERG. For Dytiscus, neither removal of the 
ganghon nor its cocainization altered the ERG other than to remove 
the small spikes (nerve action potentials) that had been superimposed 
on the slow wave (Bernhard, 1942). This smooth monophasic wave is 
identical to that recorded when the electrodes are placed on the outer 
and inner surfaces of the retina, and its size decreases as the leads are 
removed proximally away from the retina. In some cases Bernhard 
was able to record from a cornea from which the basement membrane 
and all structures below it had been removed. In these cases the usual 
large negative wave was obtained. This is clear evidence, at least for 
Dytiscus, that the negative potential originates in the retinal cells and 
not in the giant monopolar cells. Working with Trimerotropis, Jahn 
and Wulff (1942) compared the ERGs of normal and deganglionated 
eyes and concluded that the retina contributes a negative component 
and the optic ganglion, a positive component. 

The origin of some of the components in *fast* eyes has been eluci- 
dated by two very ingenious experiments of Antrum and Gallwitz 
(1951). Successive portions of the optic ganglia of Calliphora were 
removed and the ERGs recorded. As more and more of the ganglionic 
mass (medulla interna and medulla externa) was extirpated, the 



PHOTORECEPTION 173 

negativity of the ERG increased. When the medulla interna, medulla 
externa, and all or part of the lamina ganglionaris were removed the 
ERG became a negative monophasic curve resembling that of 
Limulus (Fig. 86). 

In the dragonfly Aeschna cyanea the optic ganglia of the young 
nymph are remote from the retinal layer. As the nymph develops, 
the distance between the ganglia and the retina decreases, until in the 
adult eye the usual situation obtains (Fig. 87) (Viallancs, 1884). 
The ERGs of nymph and adult are distinct - that of the nymph is 





A B 

Fig. 86. A. Simplified scheme of the optic lobe of Calliphora. AK, centri- 
petal cells ; IK, centrifugal cells ; R, retinal cells ; a, ERG from isolated 
retina; b, ERG from retina plus lamina ganglionaris; c, ERG from 
intact lobe. B. Detail of centrifugal cells. (Redrawn from Autrum, 
1959 after Cajal and Sanchez, 1915.) 



the *slow' type, that of the adult, the 'fast' type. The ERG of the 
deganghonated retina of the adult is the *slow' type. 

As a result of these experiments, Autrum (1958) has concluded that 
there is a negative component of the ERG of all insects assignable to 
the retina; it is the receptor potential. He has pointed out that in 
Calliphora under certain conditions (e.g., green or blue light) the posi- 
tive on-wave is preceded by a negative deflexion. This negative wave, 
assignable to the retinal cells, triggers a positive electrical response in 
the centrifugal cells of the lamina ganglionaris. This positive wave 
is considered to be of great importance in connexion with adaptation. 
Dark adaptation has been measured for intact insects (e.g., the honey- 
bee) by behavioural criteria, such as optomotor responses, and has 



174 THE PHYSIOLOGY OF INSECT SENSES 

been found to require up to thirty-five minutes for completion (Wolf 
and Zerrahn-Wolf, 1935 a). In the intact eye of Calliphora, as measured 
electrophysiologically, it has been found to require from minutes to 
hours. In the isolated retina, however, adaptation is complete within 
fractions of a second. It is proposed (Antrum, 1950, 1952, 1958) that 
the positive potential from the centrifugal cells acts as a *bucking 
potential' preventing sustained depolarization of the retinal cells. As 
a corollary of this, resolution of faster rates of flicker becomes 
possible. When the ganglia are removed the resulting monophasic 
ERG is unable to follow flicker at the same high rates as the intact 
eyes. 

Support for the idea that the positive component arises post- 
synaptically has been obtained by poisoning with nicotine, a specific 




ABC 

Fig. 87. Position of the retina (R) in relation to the optic lobe (I, II, III) in 
the developing dragonfly. A, young larva; B, older larva; C, imago. 
(Redrawn from Autrum, 1958 after Viallanes, 1884.) 



synaptic poison. This treatment abohshes the positive components of 
*fast' ERGs, leaving the negative portions unchanged, and has no 
influence on *slow' ERGs, as in Dixippus (Autrum, 1958). 

Ruck (1958 a, 1958 b) has not been able to confirm the relation be- 
tween wave form of the ERG, flicker, and adaptation in the eyes of 
Apis mellifera, the dragonfly Pachydiplax longipennis, and Phormia 
regina. He suggested that the lowering of flicker fusion frequency in 
Antrum's experiments is due to injury and that actually the flicker 
fusion characteristics of an eye are determined by the retinal elements 
themselves. 

Other ideas on the subject of ERG components include Hassen- 
stein's (1957) analysis of the ERG of Sarcophaga and Eristalis into a 
diphasic component and a negative component and Naka's and 
Kuwabara's (1959) conclusion that the ERG ofLucilia is composed of 
a negative and a positive component, both of which originate in the 
receptor layer. Burtt and Catton (1958), on the basis of an observed 



PHOTORECEPTION 175 

reversal of polarity of potentials (also noted by Naka and Kuwabara) 
at a critical depth in the eye (retina plus optic lobes) corresponding to 
the superficial part of the lamina ganglionaris, concluded that cells 
in this layer, probably the giant monopolar cells, are the source of the 
major part of the potential observed when the eye is illuminated. This 
conclusion is in disagreement with the results of Bernhard (1942) from 
Dytiscus, and has been criticized by Antrum (1958) as representing 
pecularities of the recording technique. Ruck (1 957) has argued that an 
interpretation of these data in a manner consistent with the distri- 
bution of current in a volume conductor would in fact localize the site 
of the origin of the ERG to the ommatidia. 

Still another electrical phenomenon observed in the optic tract of 
insects is rhythmic spontaneous activity first found in Dytiscus 
(Adrian, 1937) and subsequently in all eyes in which it was sought 
(Roeder, 1939, 1940; CrescitelH and Jahn, 1942; Jahn and Wulff, 1942; 
Bernhard, 1942; Massera, 1952; Autrum, 1951, 1952; Burkhardt, 
1954; Burtt and Catton, 1958). It is clearly of ganghonic origin, since 
extirpation of the optic ganglion abolishes it (Roeder, 1940; Burk- 
hardt, 1954). 'Fast' eyes produce faster rhythms than 'slow' eyes 
(Autrum, 1951, 1952; Burtt and Catton, 1958). In Dytiscus there are 
differences between the day and night eye, the former having a higher 
flicker fusion frequency than the latter; furthermore, the dark-adapted 
night eye is more than 1 ,000 times more sensitive than the dark-adapted 
eye, and the light-adapted day eye more sensitive than the light- 
adapted night eye (Jahn and Wulff, 1941). The differences are un- 
related to pigment migration in the eye. In Dytiscus there are actually 
two rhythms: a dark rhythm and a bright (fast) rhythm. The latter 
occurs only under maximum illumination, and was visualized by 
Adrian (1937) as representing firing of all neurons. By contrast, 
rhythms in butterflies and grasshoppers are found under any inter- 
mediate conditions (CrescitelH and Jahn, 1942). They occur at high 
temperatures as an after-discharge to a single flash of light and also 
as a result of repetitive stimulation. The dark rhythm in Dytiscus 
was explained by Adrian (1937) as the resting potential of all neurons 
in the system being favoured by injury. In Mantis religiosa and 
Romalea microptera there is also a light and a dark rhythm (Roeder, 
1939, 1940). The light rhythm is somewhat similar to that found in 
Dytiscus and unHke that described by CrescitelH and Jahn (1942). 
Burkhardt (1954) has localized the bright rhythm as originating in the 
medulla externa. This rhythmic excitation is related to the stimulus in 
its amplitude but not in its frequency. The frequency Hes between 100 



176 THE PHYSIOLOGY OF INSECT SENSES 

and 250 per second. The amplitude is related to the number of illumi- 
ated ommatidia, the Hght intensity, and the state of adaptation of the 
eye. As illumination continues the amplitude gradually decreases. If 
illumination is interrupted before the amplitude has dropped to zero 
the rhythm is abruptly terminated. The likelihood is great that these 
rhythms are an important link in the causal chain of central processes 
which occur when an eye is illuminated. 

One conclusion that can be drawn with certainty from all of the 
electrical data obtained from the compound eye is that the ERG, even 
in its simplest form, is the algebraic sum of potentials originating at a 
number of loci. Some of these loci are non-retinal; nevertheless, it is 
now doubtful that even retinal potentials are as simple as once be- 
lieved (cf. Wulff, 1950). The most elegant approach to the whole prob- 
lem has been made in Limulus. As the classical work of Hartline (1928) 
showed, this is a rather simple monophasic cornea-negative wave. 
When a micro-electrode is placed intracellularly in an ommatidium in 
the dark (HartHne, Wagner, and MacNichol, 1952; MacNichol, 
Wagner, and Hartline, 1953) there is a resting potential, negative at the 
recording electrode, of about 50 mV. When the ommatidium is stim- 
ulated there is a change in the positive direction (with intracellular 
recording the recording electrode goes positive when the cell is de- 
polarized). Superimposed on this slow wave are spikes that are related 
linearly to the magnitude of depolarization. These spikes are synchron- 
ized with spikes recorded simultaneously from the axons of the om- 
matidium. Curiously enough, the only cell in the ommatidium which 
appears to be active is the eccentric cell; the others invariably are 
electrically silent. There is little doubt that the slow negative wave 
characterizing the ERG of the Limulus eye is the generator potential 
(and probably also the receptor potential) giving rise to the action 
potential in the nerves. There are now two reports of similar record- 
ings having been made in insects. Burkhardt and Wendler (1960) have 
recorded with intracellular electrodes the ERG from individual retinal 
cells of Calliphora. The ERG is a simple negative monophasic wave 
nearly identical in appearance to that o^ Limulus. Naka and Eguchi 
(1962) have made similar recordings from the drone honeybee (see 
also Ishikawa, 1962). 

Many attempts have been made to deduce from ERGs some of the 
characteristics of the photoreceptors themselves, but as the previous 
discussion has indicated, the ERGs have been much too complicated 
and too poorly understood to have contributed greatly to this end. 
Such attempts have been made by Wulff (1943) and Wulff and Jahn 



PHOTORECEPTION 177 

(1943) and vigorously criticized by Granit (1947). More recently 
Antrum (1953, 1958) has proposed a hypothesis which can be summar- 
ized as follows: Light is absorbed by a photosensitive substance, as a 
result of which the substance is altered and stimulates the retinal cells. 
In 'slow* eyes it decomposes, and the photosensitive substance is re- 
generated. Since these processes require time, adaptation is slow. In 
*fast' eyes, however, decomposition and regeneration is blocked during 
illumination, but when illumination ceases the process proceeds very 
rapidly. In other words, adaptation is very rapid. The blocking is 
accomplished by the positive potential from the centrifugal cells. 
This is a very high potential (20 mV as compared with 1 mV in the 
frog). 

Wulff and his associates (Wulff, Fry, and Linde, 1955; Fry, Wulff, 
and Brust, 1955) have made a different analysis. Following illumina- 
tion of the eye there is always a latency before the first wave of the ERG 
arises. It is assumed that this is the period required for photolysis to 
initiate the retinal action potential. The coupling processes connecting 
these two events is obscure. According to the hypothesis of Wulff e/ al.^ 
there are two processes involved in the sense cells : an electrical pro- 
cess generating the retinal action potential and an auto-csLtalytic rate 
process which controls the latent period. Light acting on a photo- 
sensitive substance generates another substance (C) whose concentra- 
tion manifests itself as a retinal e.m.f. C is presumed to be generated at 
a rate proportional to the intensity of light. The retinal e.m.f. is pro- 
portional to log cone. C. The latency for a flash of light is a hnear 
function of log / over most of the intensity range tested and is relatively 
insensitive to time. Wulff e^ ai. suggested that the failure of 'slow' eyes 
to obey the Bunsen-Roscoe law after 30 msec, may be attributed to 
decay of an electrically active substance rather than to a recovery 
process as Autrum (1950) suggested. 

COLOUR VISION 

From the observations of Plateau (1 888) to the present time there have 
been literally hundreds of recorded observations about insects show- 
ing preferences for one colour or another. Consequently, there is not 
the slightest doubt that insects can distinguish among the various 
coloured objects in nature and that their eyes are sensitive to wave- 
lengths from about 253 m[x (the near ultra-violet) to about 700 mii (the 
infra-red). Lubbock (1886) had shown that ants were less apt to move 
their pupae out of sunlight from which the ultra-violet had been 



178 THE PHYSIOLOGY OF INSECT SENSES 

filtered than out of normal sunlight. At the opposite end of the spec- 
trum Buck (1937) had observed that the firefly Photinus pyralis could 
respond to red flashes (approximately 560-690 mjji) emitted by other 
individuals. What has not always been clear is whether or not the eye is 
equally sensitive to all wavelengths and can distinguish one wave- 
length from another when the energies of the various coloured 
fights are equalized; in other words, whether insects possess colour 
vision. 

A large number of experiments designed to provide information on 
these points have been undertaken. They fall into two categories: 
behavioural and electrophysiological. In both instances some selected 
response is measured at different wavelengths of fight whose spectral 
purity and intensity had been controlled with various degrees of rigor. 
In so far as response to different wavelengths is concerned, the results 
of the majority of tests, regardless of their sophistication, agree in a 
general way in showing that insects as a class are especiaUy sensitive to 
ultra-violet and to blue-green fight (Fig. 88). 

Behavioural experiments have been based on phototactic responses 
(Peterson and Haeussler, 1928;Bertholf, 1931a, 1931b;Sander, 1932, 
1933; Cameron, 1938; Weiss, Soraci, and McCoy, 1941, 1942, 1943; 
Weiss, 1943a, 1943b, 1944, 1946; Weiss, McCoy, and Boyd, 1944; 
Milne and Milne, 1945; Fingerman, 1952; Fingerman and Brown, 
1953; Wolken, 1957; Wolken, Mellon, and Contis, 1957; Heintz, 
1959; Goldsmith, 1960), optomotor responses (Schlegtendal, 1934; 
Rokohl, 1942; Moller-Racke, 1952; Antrum and Stumpf, 1953; 
Schone, 1953; Resch, 1954; Schneider, 1956), training (von Frisch, 
1914; Koehler, 1924; Kiihn, 1927; Kuhn and Pohl, 1921; Bertholf, 
1931a; Use, 1949; Kuwabara, 1957; Hertz, 1939; Daumer, 1956, 
1958), and simple observation (Lubbock, 1886; Hamilton, 1922; Use, 
1928, 1937, 1949; Buck, 1937). Phototactic responses have been em- 
ployed exclusively for studying spectral sensitivity, while other be- 
havioural techniques have been employed in the search for evidence 
of colour vision. 

The relative efficiency of different wavelengths in eliciting photo- 
tactic responses has been measured for a number of species. Bertholf 
presented to Drosophila and Apis two sources of light, one of which was 
the test wavelength and the other, a white standard. In one series of 
tests the intensity of the test colour was kept constant and that of the 
standard varied until both sources were equally attractive. In another 
series of tests each coloured light was matched with a white fight of 
fixed intensity. After the ratio of attractiveness had been found a white 




300 



400 



500 



600 



mfj 



Fig. 88. Relative effectiveness of different vi'avelengths of light in evoking 
positive phototaxis and similar responses of adult insects. In each case, 
open circles indicate one set of experiments and the closed circles, 
another. (Redrawn from Goldsmith, 1961.) 



180 THE PHYSIOLOGY OF INSECT SENSES 

light of variable intensity was substituted for the coloured light, and 
the intensity was found which, when tested against the white stand- 
ard, gave the same ratio of attractiveness as the test colour. Despite 
these attempts at control, Bertholf did not have control over the 
energy of his stimuU (see Weiss, 1943 a, 1943 b, and Goldsmith, 1961, 
for a full discussion). The results of his experiments showed a peak 
sensitivity in the ultra-violet (365 mjjt) and a slight indication of sensi- 
tivity in the blue-green (487 my.) for Drosophila and in the yellow-green 
(553 mji.) for Apis. Sander (1933) adjusted his lights so that the in- 
tensities of the white standard and the test colours were equal. He then 
used the number of insects {Apis) attracted to each as an index of rela- 
tive effectiveness and found peaks in the yellow-green (570 mji.) and 
in the blue (470 m^), but none in the ultra-violet. Cameron (1938) 
employed all of the aforementioned methods in tests with Musca and 
found a maximum in the ultra-violet. Weiss and his co-workers ex- 
posed approximately 1 5,000 insects representing forty species to ten 
wavelengths of light of equal intensities. The composite group be- 
haviour pattern consisted of a peak at 492 m[ji and a maximum at 
365 ra\i. Wolken determined for Drosophila the relative energy re- 
quired to produce a constant phototactic response and found a peak 
in the blue-green and a maximum commencing towards the ultra- 
violet. Heintz measured, as a function of intensity, the number of bees 
that crawled per unit time over a slit in a box illuminated by different 
wavelengths and found a small peak in the green and the maximum 
in the ultra-violet. He suggested that Sander's failure to detect a peak 
in the ultra-violet stemmed from the very high light intensities em- 
ployed. Since these intensities elicited maximum responses in the blue- 
green, no higher response could possibly have been obtained in the 
ultra-violet. Goldsmith (1960), perturbed by Sander's failure to find a 
maximum for the bee in the ultra-violet, tested the phottoactic effective- 
ness of green (546 mfx) and ultra-violet (365 m[j.) lights of equal in- 
tensities and did find a peak at 365 mt^. In short, whether the curves 
describing the relative effectiveness of different wavelengths in eliciting 
phototactic responses are true action spectra (relative energy for a 
constant effect) or not, all show that the most effective part of the 
spectrum for Musca, Apis, and Drosophila is the near ultra-violet and, 
to a lesser degree, the blue-green. This finding has been confirmed in 
whole or in part for so many species by Weiss and his associates that it 
is probably of general occurrence. 

The danger, of course, in interpreting these behavioural tests with- 
out caution as indicative of spectral sensitivity is that the response of an 



PHOTORECEPTION 181 

insect to specific wavelengths may vary with the physiological state. 
Use (1928) has observed, for example, that cabbage butterflies {Pieris 
brassicae) normally land preferentially on blue or yellow flowers or 
paper models of the same colours, while gravid females ready to 
oviposit shift their preference to green and blue-green (1937). On the 
other hand, electrophysiological studies have confirmed the more 
general behavioural findings (Crescitelli and Jahn, 1939; Jahn and 
CrescitelU, 1939; Jahn, 1946; Jahn and Wulff, 1948; Donner and 
Kriszat, 1950; Autrum and Stumpf, 1953; Goldsmith, 1958 a, 1958 b; 
Goldsmith and Ruck, 1958; Walther, 1958 a, 1958 b; Walther and 
Dodt, 1957, 1959). Spectral sensitivity curves were obtained in these 
cases by relating the magnitude of some selected components of the 
ERG to the wavelength of light or, more accurately, by plotting some 
function of the quanta necessary to produce a given response against 
wavelength. For the moth Samia cecropia (Crescitelli and Jahn, 1939) 
and the grasshopper Melanoplus differentialis (Jahn and Crescitelli, 
1939) the greatest sensitivity, exclusive of ultra-violet, which was not 
tested, is in the blue-green (from about 460-530 mfi). The curve for 
night and day eyes of Dytiscus fasciventris also shows a maximum 
in the blue-green (about 520-575 m\L). It is based upon the magnitude 
of the a wave. This was plotted against intensity. From the family of 
curves (one for each colour) obtained, a constant response magnitude 
was selected and plotted against wavelength (Jahn and Wulff, 1948). 
Curves for Musca domestica, Lucilia caesar, Calliphora vomitoria, 
Pollenia rudis, and Drosophila meJanogaster based upon measurements 
of the on-efTect of the ERG at wavelengths of equivalent quantum 
intensity show maxima in the green and in the near ultra-violet 
(Donner and Kriszat, 1950). 

A spectral effectiveness curve for Calliphora erythrocephala shows 
a peak at 540 m(x (blue-green) and one at 630 m\i (red) (Autrum and 
Stumpf, 1953) (Fig. 89). This curve is based on the amplitude of the on- 
effect of the ERG, or the height of the flicker potential occurring as a 
reaction to twenty-seven flashes, produced by stimulation by light of 
different wavelengths but equal quantal value. No tests were made 
with ultra-violet, but the rising curve at the shorter wavelength 
suggested ultra-violet sensitivity. This expectation was realized in tests 
subsequently conducted by Walther (1957) and Walther and Dodt 
(1957, 1959). A spectral sensitivity curve (reciprocal of the quanta 
necessary to generate a constant magnitude of on-effect plotted as a 
percentage of the maximum of 507 m(a against the wavelength) for 
Calliphora shows maxima in the red (about 630 mjx), the blue-green 



182 



THE PHYSIOLOGY OF INSECT SENSES 




500 



400 



500 



600 



IVave Length mu 

Fig. 89. The spectral sensitivity of the compound eye of Calliphora. Data 
from Antrum and Stumpf (1952) (open circles), Walther and Dodt 
(1957) (half-filled circles), and Walther and Dodt (1959) (solid circles). 
(Drawn from Goldsmith, 1961.) 



(540 mji.), and the ultra-violet (341-369 m\i). The curve for Periplaneta 
is similar, but lacks the peak in the red. 

A spectral sensitivity curve for the drone honeybee shows a maxi- 
mum at 400 my. for the compound eye and maxima at 335-340 my. and 
490 my for the median ocellus (Goldsmith, 1958 a, 1958 b; Goldsmith 
and Ruck, 1958). The dorsal ocelli of the cockroaches Periplaneta 



PHOTORECEPTION 183 

americana and Blaberus craniifer show a peak at 500 my. (Goldsmith 
and Ruck, 1958). 

One of the more interesting aspects of all of these descriptions of 
spectral sensitivity is the great stimulating effectiveness of the near 
ultra-violet. Hess (1920) had questioned the sensitivity of the insect 
retina to ultra-violet and suggested the possibility of stimulation 
actually occurring as a result of fluorescence set up in various tissues of 
the eye. Fluorescence may occur (Walther and Dodt, 1959), but 
Merker (1929) and Lutz and Grisewood (1934) showed that crushed 
eyes of Drosophila did not fluoresce in ultra-violet of the wavelength 
to which flies respond. They showed, furthermore, that the cornea 
of Apis and Sarcophaga can transmit in the 253-m[JL band of the 
spectrum. Additional reasons for rejecting Hess's hypothesis are 
mentioned by Walther and Dodt (1959) and discussed by Goldsmith 
(1961). 

Taken at face value, the spectral sensitivity data indicate what may 
constitute brilliance for an insect, and a number of studies bear this 
out wholly or in part (MoUer-Racke, 1952, with Dytiscus, but compare 
Schone, 1953; Rokohl, 1942; Llidtke, 1953, and Resch, 1954, with 
Notonecta). Demonstration of true colour vision has been technically 
more difficult. There is now evidence for colour vision in thirty-three 
genera of insects in six orders. The evidence has been derived princi- 
pally from training experiments, optomotor responses, and electro- 
physiological analyses. 

Von Frisch (1914) trained honeybees to collect food from a dish 
placed on a card of a particular colour. This card was then placed in 
one square of a checkerboard of greys (white to black) of different 
intensities. The position of the coloured card was changed constantly. 
Under these conditions the bees could always pick out a blue or yellow 
card from the checkerboard of greys. Thus, it was demonstrated that 
bees conditioned to blue confused blue-violet and purple, while those 
conditioned to yellow confused yellow, orange, and yellow-green. 
None could distinguish red. Later tests of the papers used by von 
Frisch showed that some of the blues and greens reflected ultra- 
violet, whereas some of the yellows and greens reflected red and blue 
(Lutz, 1924). Similar experiments employing spectral colours pro- 
jected on a white background demonstrated that bees could dis- 
tinguish four regions of the spectrum: yellow-green and orange 
(510-650 m|j.), blue-green (480-500 ma), blue and violet (400-480 m\L\ 
and the near ultra-violet (300-400 m\3) (Kiihn and Pohl, 1921 ; Kiihn, 
1927). These results were confirmed by the training experiments of 

N 



184 THE PHYSIOLOGY OF INSECT SENSES 

Kuwabara (1957) and of Daumer (1956, 1958), who also demon- 
strated that bees can even discriminate between wavelengths within 
these bands, but with less precision. 

Colour vision can also be investigated by colour-matching tests. 
Daumer (1956, 1958) applied these with outstanding success to honey- 
bees by training them to come to a particular colour. The training 
colour was then paired with a colour produced by mixing wave- 
lengths. Various mixtures were tested until one was found which was 
as acceptable to the bees as the training colour. For example, bees can 
distinguish between white light containing ultra-violet and that lack- 
ing ultra-violet. White light with ultra-violet ('bee white') can be 
matched by a mixture of 15 per cent ultra-violet (360 mjx) and 85 per 
cent blue-green (490 mii). The complementariness of ultra-violet and 
blue-green had already been suggested by Hertz (1939), and Use (1937) 
had shown that purple adjacent to white sets up a green colour con- 
trast in the white. Similarly, *bee purple' can be matched by mixtures 
of yellow and ultra-violet. Goldsmith (1961) has summarized Daum- 
er's results in a preliminary chromaticity diagram which is explained 
in Fig. 90. 

From the results of all of his matching experiments, Daumer con- 
cluded that the eye of the honeybee possesses a receptor maximally 
sensitive to ultra-violet, one for blue-violet, and one for green-yellow. 
The existence of two of these has been confirmed by the electrophysio- 
logical analyses of Goldsmith (1958 a, 1958 b, 1959, 1961). The wave 
form of the ERG in the early studies with grasshoppers and Dytiscus 
had shown no change as the wavelength of the stimulus was changed, 
provided the intensities were matched (Crescitelli and Jahn, 1939; 
Jahn, 1946; Jahn and Wulff, 1948). On the other hand, as Walther 
(1958 a) found in the cockroach eye, there are some areas of the eye 
where differences in the form of the ERG arising from differences in 
the colour of the stimulus cannot be matched by adjusting intensity. 
Goldsmith and Ruck (1958) also found that the ERG of the ocellus of 
the bee had at low stimulus intensities a different contour for ultra- 
violet than for green. 

By adapting with lights of different wavelengths it is possible to 
demonstrate the existence of different receptors (Hamilton, 1922; 
Fingerman and Brown, 1953). The dark-adapted eye of the worker 
honeybee shows a peak of sensitivity in the green (535 m^t) and a 
smaller peak in the ultra-violet (Goldsmith, 1960). If the eye is 
adapted with red or yellow light the peak at 535 miJ. diminishes and the 
peak at 340-345 m[j. increases (Fig. 91). The complementary experi- 



PHOTORECEPTION 



185 



375 




Fig. 90. Tentative chromaticity diagram for the honeybee based on the 
work of Daumer (1956). The behavioural experiments of Daumer led 
to the prediction that any colour can be matched for bees by an appro- 
priate mixture of three monochromatic reference stimuli, e.g., ultra- 
violet (360 m[x), blue-violet (440 my.), and yellow (588 my.). Any light, 
therefore, can be represented in Fig. 90 by a point; for example, 'W 
is the white of the xenon emission spectrum. The proportions, in 
fractions of the total energy - the chromaticity co-ordinates - of the 
yellow and blue reference stimuli required for a colourimetric match 
of the light represented by the point are given by the co-ordinates of 
the point, 588 my. on the abscissa and 440 my. on the ordinate. Since 
the sum of the three chromaticity co-ordinates is 1 , the fraction of the 
energy at 360 my. can be calculated by difference. The locus of the 
spectrum is given by the experimental points ; however, as is suggested 
by the dashed line, it may actually lie somewhat outside the triangle, for 
it is questionable whether this kind of experiment is sufficiently precise 
to reveal the necessity for small negative values of one of the chroma- 
ticity co-ordinates. The complementary to 360 my. is 490 my., for both 
wavelengths lie on a straight line passing through the white point. 
Similarly, the point 'p' is the 'bee-purple' complementary to 440 my. 
and is composed of 79 per cent 588 my. and 21 per cent 360 ma. 
(Redrawn from Goldsmith, 1961.) 



186 



THE PHYSIOLOGY OF INSECT SENSES 



20 



1-5 



> 
V) 

C 
-J 



10 



0-5 



Dark Adapted 




During adaptation 
with red light 




300 



Fig. 91. Alteration of the shape of the spectral sensitivity of the worker 
honeybee by selective light adaptation. During a constant level of 
adaptation brought about by red light the ultra-violet receptor system 
contributes more prominently to the spectral sensitivity function 
(open circles) than it does in the dark-adapted eye (filled circles). 
Ordinate: logarithm of the reciprocal of the relative number of quanta 
required to produce a retinal action potential of constant size. 
(Redrawn from Goldsmith, 1961.) 

ment is less striking because the ultra-violet receptor system contri- 
butes less to the ERG than the green system and because the sensitivi- 
ties of the two systems behave differently to different coloured 
adapting hghts. Nevertheless, these experiments confirm the existence 
in the bee of two of Daumer's postulated receptor types. The existence 



PHOTORECEPTION 187 

of a receptor maximally sensitive at about 440 m[i has been demons- 
trated in the drone (Goldsmith, 1958 b). Furthermore, Goldsmith 
(1958 a) has found a retinene-containing pigment with a maximum 
absorption in the blue-violet (440 m|i.). 

Studies of the cockroach eye have also revealed the existence of 
more than one type of receptor (Walther and Dodt, 1957, 1959; 
Walther, 1958 a, 1958 b). In the dorsal area of the eye the sensitivity 
maximum to ultra-violet is higher than that to blue-green; in the 
ventral part of the eye it is lower. Whereas the ventral area shows a 
single-peaked (507 m,u.) sensitivity curve that is unaltered by the state 
of adaptation, the dorsal area shows indication of another peak in the 
ultra-violet. Adaptation with monochromatic lights changes the rela- 
tive spectral sensitivities, and colour specific differences occur in the 
shape of the ERG. 

For Drosophila Hamilton (1922) had produced evidence for the 
existence of a system sensitive to blue-violet and one sensitive to blue- 
green by specific wavelength adaptation. Fingerman and Brown 
(1953), employing a similar technique, concluded that Drosophila also 
possesses sensitivity in the red (650-675 mpt). 

The blowfly Calliphora is unique among the insects studied in that 
the spectral sensitivity curve of its eye, as measured electrophysio- 
logically, exhibits three maxima: ultra-violet, blue-green, and red 
(Autrum and Stumpf, 1953 ; Walther and Dodt, 1958 a, 1958 b). There 
is a discrepancy of about 30 mjx between the positions of the green 
maximum reported by the two papers. 

In their search for evidence of colour vision, Autrum and Stumpf 
combined electrophysiological and flicker fusion techniques. After 
adjusting the intensities of two monochromatic lights they flickered 
them alternately. Thus during the period of stimulation there was 
constant intensity of illumination but flickering wavelengths. If the 
ERG showed with heterochromatic flicker ripple that could not be re- 
moved by adjustment of intensities, then one could conclude that the 
eye discriminated between the two wavelengths. The findings were as 
follows: In the region 690-620 m\L discrimination is slight, but this 
region is sharply distinguished from all other regions ; yellow to blue- 
green (620-650 m[x) is distinguished from all other regions and dis- 
crimination in this band is sharp (a restricted region between 570 and 
590 m.[L cannot be distinguished from colourless light); blue-green 
(480 m.\i) is distinguished from all other colours; on both sides of 
480 m\i there is a region (450-500 m\i and 500-560 m^t) which is dis- 
tinguished from all colours between 560 and 690 mfx. Autrum and 



188 THE PHYSIOLOGY OF INSECT SENSES 

Stumpf concluded that there need be only two receptor systems to 
account for the data, a blue-green receptor and a red receptor. The 
maximum for the blue-green receptor lies between 500 and 550 my.. Its 
sensitivity extends from the region of the near ultra-violet up to about 
660 mil. The maximum for the red receptor lies in the vicinity of 
625 my.. Its sensitivity extends from about 480 up to about 700 my.. 
Several flies were found which were colour-blind when tested with 
flicker and whose spectral sensitivity curves were abnormal. The 
spectral sensitivity curve of one possessed the usual peak in the red but 
none in the blue-green. This fly possessed no colour discrimination in 
the region 400-500 my. as judged by flicker. Another fly lacked the 
peak in the red (630 m^y.) and was totally colour blind. This fly possessed 
the usual red eye-pigments in the pigment cells of the ommatidium. 
Later Antrum (1955 a) described the spectral sensitivity of a white- 
eyed mutant which lacked these pigments. Since this mutant also 
lacked a sensitivity peak in the red (630 my.). Antrum concluded that 
the usual 630-m[x peak resulted from transmission of long wave- 
lengths by the red shielding pigments. 

Behavioural experiments conducted with a revolving drum and 
light of low intensities did not reveal a marked sensitivity in the red 
(Schneider, 1956). To reconcile the behavioural and electrophysio- 
logical results Schneider proposed that since the enveloping pigments 
of the ommatidia are partially transparent to red light, the ERG would 
be higher at red than at other wavelengths because the red would be 
stimulating a greater number of ommatidia. On the other hand, the 
failure of the screening pigments to isolate the ommatidia when the 
eye was illuminated with red light would lead to a loss in visual acuity 
and since the behaviour in a revolving drum depends upon visual 
acuity, it would fail to reveal a sensitivity to red. Antrum (1961) has 
reported, however, that even in a white-eyed mutant, which completely 
lacks screening pigment, the visual acuity equals that of wild-type flies. 

Recently Burkhardt and Antrum (1960) have been able to record 
electrical events directly from single visual cells. The spectral sensi- 
tivity was determined for thirty-nine single retinal cells of the wild type 
of Calliphora and from the white-apricot mutant which lacks screen- 
ing pigments (Antrum and Burkhardt, 1961). The red screening pig- 
ment does not absorb Hght in the region 616 m.y., and in weakly 
illuminated elements the amount of scattered red light is much greater 
than that amount of light coming through the lenses. Except in these 
weakly illuminated elements and in the far red, the screening pigments 
are not relevant to the shape of the sensitivity curves. All cells in the 



PHOTORECEPTION 189 

dorsal part of the eyes were found to have curves with a maximum at 
489 ma and one at 345 mix. Three receptor types were found in the 
ventral region of the eye: a green receptor (maxima at 491 m[x and 
345 m[x); a blue receptor (maxima at 468 m[x and 345 mix); a yellow- 
green receptor (maxima at 524 mix and 345 mix). Some elements show a 
peak at 616 m^x. The numerical relationships among the green, blue, 
and yellow-green receptors is 18:4:3. This is almost the ratio to be 
expected if one assumed that of the seven retinula cells in an ommati- 
dium five are green receptors, one blue, and the remaining one 
yellow-green. Since all have a peak at 345 m[x, corresponding to a 
stable position of the p-absorption in derivatives of vertebrate visual 
pigments, it is possible that the most common visual pigment in 
Calliphora is retinene with a maximum absorption at 490 mjx (Autrum 
and Burkhardt, 1961). 

Some workers have been tempted to think of the insect eye as 
possessing analogues of rods and cones, especially since Hanstrom 
(1927) demonstrated retinal cells with short and long axons and 
suggested the analogy. But Wolf and Zerrahn-Wolf (1935 a), in dis- 
cussing the relation between threshold intensities and time of dark 
adaptation for the honeybee, called attention to the fact that the curve 
describing this relation was, unlike that for the human eye, a smooth 
one. Nor do curves relating visual acuity and flicker fusion frequency 
to intensity exhibit any changes in slope that could be attributable to 
two populations of receptors of different sensitivities analogous to 
rods and cones (Hecht and Wolf, 1929; Wolf, 1933e;HechtandWald, 
1934; Wolf and Zerrahn-Wolf, 1935 b). In Drosophila, however, 
Fingerman and Brown (1952, 1953) reported a 'Purkinje shift', that is, 
a shift of sensitivity of the eye towards shorter wavelengths as the light 
intensity is decreased. They interpreted this as indicating a shift from a 
photopic to a scotopic mechanism. According to their conclusions, 
Drosophila loses its ability to discriminate among wavelengths as 
intensity is lowered. No such change could be demonstrated in the 
cockroach (Walther, 1958 a, 1958 b), nor in the honeybee (Goldsmith, 
1960, 1961). The data of Fingerman and Brown (1952, 1953) have 
been criticized by Goldsmith (1961). On the other hand, Weiss et al. 
(1942) reported that the order of attractiveness of 365 my. and 470- 
528 mjx at low intensities was reversed at high intensities. With 
Calliphora Autrum (1955 a) found that the wavelength of maximum 
sensitivity was 540 mpi at high intensities but shifted to shorter wave 
lengths (480 m^x) as the intensity was dropped. Schneider (1955, 1956) 
reinvestigated this problem by comparing spectral sensitivity curves 



190 THE PHYSIOLOGY OF INSECT SENSES 

obtained in optomotor-type apparatus at high and at low intensities 
with the curve obtained electrophysiologically. The behaviourally de- 
termined curve obtained at low intensities showed a maximum at 
480 ray.. The high-intensity curve shifted towards 540 my.. This shift 
could, as Schneider pointed out, be due to the transparency of envelop- 
ing pigments to long wavelengths, but were this true, the white-eyed 
mutant should exhibit a maximum at 480 my., whereas it actually shows 
a maximum between 510 and 540 my. (Antrum, 1955 a). The shift must 
be due to the participation of a receptor of low threshold, the 'receptor 
for twilight vision', whose maximum sensitivity lies at 480 my. and a 
less-sensitive receptor whose maximum lies above 540 my. (Schneider, 
1956). Walther and Dodt (1957, 1959) have not reported any shift. In 
the back-swimmer (Notonecta) a shift in which red and yellow become 
darker to the animal with advancing dark adaptation (as measured 
by optomotor reactions) has been noted by Resch (1954) and Liidtke 
(1953) and referred to as a Turkinje phenomenon'. 

POLARIZED LIGHT 

In 1948 von Frisch (1948, 1949) opened a new area of investigation in 
insect vision by demonstrating that honeybees could distinguish 
different quadrants of the sky in which the plane of polarization of 
sunlight differed. This conclusion was based on the fact that: (1) bees 
in the hive could orient their communication dances as long as they 
were able to see a patch of blue sky, and (2) the orientation of the dance 
could be altered by interposing a piece of polaroid between the bee and 
the sky. Bees act as though the sun is at right angles to the plane of 
polarization. Since then directional orientation in the presence of 
linearly polarized light has been demonstrated in many arthropods 
(for reviews see von Frisch and Lindauer, 1956; Waterman, 1960). 

Polarized Hght may differ in degree, in type (linear, elliptical, or 
circular), or in orientation of major axis. Practically all polarized light 
in nature is linear (Jander and Waterman, 1960), and only this type is 
known to affect animals. Two basic explanations have been proposed 
to explain its perception. The most direct and obvious explanation is 
that the eye possesses a specific polarization analyser, that is, that 
animals see the direction of vibration of polarized light as distinct from 
such other characteristics as intensity and wavelength (von Frisch, 
1949; von Frisch, Lindauer, and Daumer, 1960; Antrum and Stumpf, 
1950; Vowles, 1950; Menzer and Stockhammer, 1951 ; Stockhammer, 
1956, 1959; de Vries, 1956; Birukow and Busch, 1957; Jander, 1957; 



PHOTORECEPTION 191 

Liidtke, 1957; Jacobs-Jessen, 1959; Waterman, 1960; Jander and 
Waterman, 1960; and a number of investigators studying Crustacea). 
An alternative hypothesis suggests that differential responses to 
various planes of polarization of light depend only upon detection of 
different intensity patterns (Baylor and Smith, 1953; Stephens, 
Fingerman, and Brown, 1953; Bainbridge and Waterman, 1957, 
Baylor and Smith, 1958; Kalmus, 1958, 1959; de Vries and Kuiper, 
1958; Baylor, 1959a, 1959 b; Smith and Baylor, 1960). This later 
hypothesis is consonant to two basic facts: (1) differential reflection, 
refraction, and scattering of polarized light by environmental features 
or dioptric elements of the eye (Waterman, 1954) can produce 
quadrants of maximal and minimal intensities whose positions are 
determined by the direction of vibration ; arthropods respond to light- 
intensity patterns. In further support of the hypothesis is the lack of 
convincing proof of the existence of a polarization analyser in the eye. 
No direct positive proof has been presented to contradict the opposing 
hypothesis. 

Support for the idea that the animals do see the plane of polariz- 
ation as distinct from intensity patterns has recently been summarized 
by Jander and Waterman (1960) in the following terms: 

(1) In Daphnia and the beetle Bidessus, which could be made either 
positively or negatively phototactic, reversal of this sign caused a 
reversal of response to ordinary horizontal light intensity patterns, but 
had no effect on the response to the plane of polarization of a vertically 
directed beam. Therefore, polarized Hght orientation cannot be due to 
horizontal patterns due to scattering and reflection of polarized light. 

(2) In all animals, responses to horizontal patterns of Hght intensity 
are of two sorts only, that is, towards or away, while four basic 
orientation directions have been observed in a vertical beam of linearly 
polarized light. Therefore, two different sensory mechanisms must be 
involved. 

(3) Response to the direction of vibration of polarized light showed 
smaller deviations from the maximally preferred horizontal intensity 
patterns. Therefore, both reactions cannot be intensity responses. 

(4) When the dark intensity patterns due to the scattering of 
polarized Hght are made artificially brighter, the crustacean Mysidium, 
Daphnia, and Bidessus still respond as before to the plane of polariz- 
ation. Therefore response to polarized light is not simply a photo- 
tactic response to brightness. 

(5) The crustacean Mysidium can distinguish between horizontal 



192 THE PHYSIOLOGY OF INSECT SENSES 

light patterns and polarized light presented simultaneously by reacting 
to each as if it were alone. Therefore, polarized light and intensity 
patterns are distinct visual qualities. 

(6) For Daphnia light contrast reaction deteriorates at low overall 
levels of illumination, while reactions to the plane of polarization do 
not. 

(7) Honeybees orient at the same angle with respect to the plane of 
polarization under a polarizer as to that of corresponding quadrants 
of the blue sky, despite large differences in intensity in the two situa- 
tions. 

(8) 'Since bees know the regional distribution of polarized light in 
the sky (von Frisch, 1948, 1949), they must know the direction from 
which it is coming. Yet they cannot with ordinary image vision infer 
the direction of the original source from a hght pattern estabHshed by 
reflection and refraction.' 

(9) 'Under natural conditions reflection and refraction patterns due 
to polarized sky light must to a considerable extent cancel each other 
out because the plane of polarization is different in various parts of the 
sky. In addition such patterns as do arise will be confused by much 
more marked intensity patterns due to direct sunlight, which com- 
prises up to 80 per cent of the total sky light, and to clouds and surface 
details of the earth. To claim that bees could learn sky polarization 
patterns from these reflection-refraction cues observed on their field 
trips seems highly unlikely in view of such conditions.' 

(10) Tn this view, experiments with spiders (Papi, 1955; Corner, 
1957), ants (Jander, 1957) and bees (Jacobs- Jessen, 1959), have shown 
in some instances that when the main intensity pattern is dislocated by 
transposing the sun 180° with a mirror, the animals nevertheless main- 
tain their orientation direction relative to the blue sky.' 

Additional evidence in support of this hypothesis is derived from 
the work of von Frisch (1960) and von Frisch, Lindauer, and Daumer 
(1960). 

If insects do indeed possess a discrete polarized light vision it 
follows that there must be a mechanism in the eye for analysing the 
plane of polarization. This could be located either in the dioptric 
apparatus or in the retinal elements. It could depend on single re- 
fraction according to the Brewster-Fresnel law or upon double re- 
fraction. There is no convincing evidence for the existence of an 
analyser in the dioptric apparatus, and the proposition that analysis 
depends on simple reflection-refraction phenomenon at the corneal 



PHOTORECEPTION 193 

surface (Stephens et al., 1953; Baylor and Smith, 1953) does not con- 
form to a number of experimental facts. For one thing, the necessary 
properties would be realized only in an optically isotropic medium, 
and the corneal lenses of Drosophila are anisotropic (Stockhammer, 
1959). Nor is a mechanism of double refraction present. When the 
dioptric apparatus is observed through a rotating polaroid no change 
in the pattern or intensity of transmitted light is observed (Autrum and 
Stumpf, 1950; de Vries and Kuiper, 1958; Stockhammer, 1959). 
Furthermore, analyses of the ERG have failed to support the hypo- 
thesis (Autrum and Stumpf, 1950; Baylor and Kennedy, 1958; de 
Vries and Kuiper, 1958). 

The on-effect of the ERG is known to depend in its magnitude on 
the intensity of light. When the action potential resulting from the 
stimulation of a total of twelve-fifteen ommatidia by polarized light 
was measured there was no change in magnitude of response as the 
plane of polarization was rotated. It seems unlikely, therefore, that the 
eye as a whole acts as an analyser. Similar results obtained by stimula- 
tion of a single ommatidium also indicated that the single ommati- 
dium does not act as an analyser. However, when the effects of polar- 
ized and non-polarized light of equal intensities were tested the 
polarized light always elicited the greater response (Autrum and 
Stumpf, 1950). From this it was concluded that each of the retinal 
cells (eight in the honeybee and seven in Calliphora) is maximally 
sensitive to light of a definite vibration direction, namely, that per- 
pendicular to the radial direction of the cell within the ommatidium. 
With unpolarized light each cell receives less than maximal stimula- 
tion; with polarized light some receive maximal and some minimal. 
The net result in the ERG is a response of greater magnitude than to 
ordinary light because maximal and minimal effects do not cancel out. 
Thus, the unit of analyses seems to be the single retinal cell, and the 
central nervous system is presumed to integrate the pattern of light and 
dark from each ommatidium. 

This hypothesis is supported by the electrophysiological work of 
Liidtke (1957), Naka and Kuwabara (1959), and Burkhardt and 
Wendler (1960), as well as by field experiments of von Frisch (1950 a, 
1950 b). 

Von Frisch (1950 a, 1950 b) provided support for the hypothesis by 
comparing the actions of bees dancing under a polaroid material with 
the changes observed in the light-intensity pattern of the sky when 
viewed through an artificial ommatidium constructed of eight seg- 
ments of polaroid material each oriented differently. When this model 



194 THE PHYSIOLOGY OF INSECT SENSES 

was held up to the blue sky a different pattern of intensity was seen 
for every part of the sky, depending on the position of the sun. When 
a sheet of polaroid was placed between the model and the sky in such 
an orientation as not to alter the pattern and another sheet was placed 
similarly over dancing bees the dances maintained proper orientation. 
When the covering sheets were rotated until that over the model 
altered the pattern the orientation of the dance changed. The artificial 
pattern produced in the model could usually be found in another part 
of the sky, and it was to this direction that the bees danced. When the 
pattern produced by interposing the polaroid between the model and 
the sky happened to have no normal counterpart in the sky the dance 
of the bees under the same polaroid became disorganized. If the 
pattern as seen through the model happened to occur simultaneously 
in two areas of the sky the bees also oriented their dances in two 
directions. 

In so far as electrophysiological evidence is concerned not all 
workers have been able to confirm the findings of Autrum and Stumpf. 
Baylor and Kennedy (1958), employing especially refined control of 
intensity and wavelength, were unable to detect any difference in the 
ERG related to the presence or absence of polarization. Nor were de 
Vries and Kuiper (1958) able to detect changes in the ERG when the 
eye was subjected to flicker consisting alternately of vertically and 
horizontally polarized light. The insects themselves failed to show 
optomotor reactions in these circumstances. These results not only 
challenge the proposition that analysers are located in the retinal 
cells but also question even the abihty of the eye to possess any 
analyser at all. 

Contrary to these findings is the report of Burkhardt and Wendler 
(1960). By measuring the ERG of individual retinal cells of Calliphora 
with intracellular electrodes and controlHng for adventitious polariz- 
ation of oblique incident light at the corneal and crystalline cone 
boundaries, these workers were able to show that the amplitude of the 
ERG is dependent upon light intensity and the direction of vibration 
of Hnearly polarized light. A rotation of the plane of polarization from 
the most-effective position to the least-effective position changes the 
illumination potential of the cell quantitatively to the same degree as a 
50 per cent reduction of light intensity. 

If the retinal cells are indeed analysers it should be possible to find 
within them the necessary structural modification. Menzer and Stock- 
hammer (1951) proposed that birefringence in the rhabdoms coupled 
with a mechanism for extinguishing one ray provided means of 



PHOTORECEPTION 195 

analysis. They suggested : (1) that the rhabdomeres consists of a doubly 
refracting central column and a surrounding cylinder of different 
refractive index, and (2) that the optical axis of each of the retinal cells 
is different. They reported that there was birefringence in the rhab- 
doms and that between crossed polarizers each rhabdomere ex- 
tinguishes about four times during one complete rotation. Many ob- 
jections to this hypothesis were raised by de Vries (1956), who also 
pointed out that the report of birefringence was based upon examina- 
tions of fixed material and that fresh material showed at best too httle 
birefringence (less than 1 per cent) to meet the requirements of the 
hypothesis (de Vries, 1956; de Vries, Spoor, and Jielof, 1953; de 
Vries and Kuiper, 1958). 

An alternative hypothesis to the effect that analysis is accomplished 
by means of dichroic molecules was advanced by de Vries (1956). 
Organic molecules tend to absorb light polarized in the direction of the 
long axis of the molecules. If all of the photosensitive molecules of a 
sense cell are arranged in parallel and different sense cells are oriented 
differently the visual organ possesses the necessary mechanism for 
analysing polarized light. Indeed, this mechanism works to a minor 
extent in the human eye, which can detect the polarization of Hght by 
Haidinger brushes. These are seen as a yellow shape (figure of eight) 
and are due to orientation (about 50 per cent) of the molecules of the 
yellow macular pigment. Nobody, however, has been able to demon- 
strate dichroism in the insect eye, even though evidence from electron- 
microscopy proves that the microvilli of each pair of rhabdomeres are 
oriented in a different horizontal direction and the visual pigment is 
presumed to be in the microvilH. De Vries (1956) concluded that if 
dichroism is present it must be less than 10 per cent; nevertheless, he 
did not consider that this negative finding disproved his hypothesis. 
Later, however, he concluded that the oriented structure of the 
rhabdomeres has nothing to do with the detection of polarized fight 
and that insects do not *see' polarization (de Vries and Kuiper, 1958). 
He and his co-worker were influenced in drawing these conclusions by 
failure to detect analysers and by the experiments of Baylor and Smith 
(1953, 1957). Stockhammer (1959), in discussing the dichroism 
hypothesis, advanced a number of arguments from structure which 
support the idea. 

Baylor and Smith (1953, 1957) proposed that the responses of 
animals to the plane of polarization of light is in fact a response to a 
non-uniform distribution of intensities in the pattern of fight reflected 
from a substratum (in the case of terrestrial animals) or scattered by 



196 THE PHYSIOLOGY OF INSECT SENSES 

various particles in water (Baylor, 1959 a, 1959 b; Smith and Baylor, 
1960; Kalmus, 1958, 1959; Bainbridge and Waterman, 1957). Some 
of the evidence upon which this view is based has already been given. 
Additionally, it is claimed that the ability of insects to respond photo- 
tacticly to polarized light depends upon whether the substrate is black 
or white (e.g., Kalmus, 1958). 

Evidence against the reflexion hypothesis has already been stated. 
In so far as bees are concerned, recent experiments by von Frisch, 
Lindauer, and Daumer (1960) emphasize the inadequacy of the hypo- 
thesis. With bees, direct analysis of the sky's light during the dance on 
a horizontal comb requires use of the dorsal areas of the eyes, while 
recognition of reflexion patterns of the substrate requires the ventral 
areas. Masking of the upper portions impairs orientation of the dance, 
but masking of the lower portions does not. Furthermore, walking 
bees orient as well on a white substratum as on a black, glossy one. 

Whatever may be the mechanism, the fact remains that many in- 
vertebrates behave as though they can detect differences in the plane of 
polarization of light and utilize this abihty in their economy of living. 

FORM PERCEPTION 

The intrinsic characteristics of the stimulus for a photoreceptor are 
intensity, wavelength, and plane of polarization, but the occurrence of 
stimuli also varies in space and time. In the visual field there is at any 
given time a definite spatial arrangement of the kinds and amounts of 
radiant energy. In other words, there are patterns of light. The fineness 
of form perception depends upon the accuracy with which photo- 
receptors can detect this pattern, that is, upon their resolving power, 
and ultimately upon the faithfulness with which the spatial and tem- 
poral relations are represented in the central nervous system. 

The capacity of the dioptric apparatus to form images that are 
reasonably distinct by human standards is easily demonstrated by 
taking photographs in the focal plane of excised lens systems 
(Gottsche, 1 852 ; Exner, 1891; and many others). In those eyes in which 
each ommatidium is optically isolated from its neighbours by envelop- 
ing pigment cells and in which the rhabdom Hes immediately beneath 
the crystalline cone, a small inverted image is produced at the base of 
each cone. Eyes of this type are termed apposition eyes and are 
characteristic of diurnal insects (Fig. 6). Miiller (1826) proposed that 
these minute images were physiologically unimportant as images. He 
visualized each ommatidium of the apposition eye as a device for 



PHOTORECEPTION 197 

gathering light from a narrow sector of the visual field and projecting 
it as a point on the retinal field. Since each ommatidium sampled, as it 
were, a mean intensity from a particular area, the point of light pro- 
jected by all the ommatidia composed an erect mosaic image. 

Nocturnal and crepuscular insects characteristically possess eyes in 
which the rhabdoms are situated at a considerable distance from the 
crystalline cone. The enveloping pigment migrates back and forth in 
their respective cells as the eye is light- or dark-adapted (Fig. 92). 




A B 

Fig. 92. Image formation in the apposition eye, A, and the superposition 
eye, B. a-f, paths of light rays; P, pigment; IP, position of pigment 
when eye is in the light adapted condition; Rh, rhabdom. (Redrawn 
from Wigglesworth, 1939 after Kuhn.) 

When this eye is dark-adapted the iris pigment moves distally into a 
position surrounding the cones. In this position each cone is isolated 
from its fellows, but the rhabdoms are now no longer shielded. Under 
these conditions light entering one ommatidium at an angle is not 
confined to that ommatidium as in the apposition eye, but may travel 
to neighbouring rhabdoms (Fig. 92). The image produced by a single 
ommatidium is an erect image which becomes larger the farther away 
from the crystalline cone it is projected. At the plane of the rhabdoms 
it is so large that it overlaps many rhabdoms where it is superimposed 
on the images similarly produced by the other lenses corresponding to 



198 THE PHYSIOLOGY OF INSECT SENSES 

those rhabdoms. Microscopic examination of the image at the level 
of the rhabdom reveals a large, somewhat fuzzy, erect image. As the 
microscope is brought to focus closer and closer to the crystalHne 
cones, the rays of light forming the image are seen to retreat into each 
cone. The image at the level of the rhabdoms is a compound of super- 
imposed images; hence, this type of eye is called a superposition eye. 
When the pigment in the superposition eye migrates proximally so that 
the rhabdoms are shielded from one another the eye functions Hke an 
apposition eye. It is noteworthy in this connexion that Antrum (1961) 
in measuring the visual acuity of a white mutant of CaUiphora in which 



Fig. 93. Concentric lamellae 
of different refractive 
index in the dioptric 
apparatus of the om- 
matidium. The refrac- 
tive index is greatest 
along the axis xy. (Re- 
drawn from Exner, 
1891.) 




Proximal Surface 



there was no screening pigment in the eye found no difference between 
the mutant and the wild type. Since the superposition is not total, that 
is, not all the images are congruent, it could be argued that the differ- 
ence between the mosaic image and the superposition image is one of 
degree. 

In order to explain image formation in the two types of eyes Exner 
(1891) proposed that the crystalline cone acted as a lens cyHnder. If it 
were constructed of concentric lamellae of different refractive indices 
(Fig. 93), the refractive index would be greatest along the longitudinal 
axis and would decrease towards the periphery. The path of a ray of 



PHOTORECEPTION 199 

light in such a cylinder is diagrammed in Fig. 94. As a ray xm enters 
the cylinder it is refracted by the surface of each lamella a 'b\ but 
since the lamellae decrease in refractive index progressively from A^to 
ab, the ray is bent less and less until it re-enters regions of higher re- 
fractive index, where its path is now directed back towards xy. It finally 
emerges at^*. If such a cylinder is as long as its focal length it will pro- 



a 










fc 








^„^-' 1 










..^^-^^^ 


^ 


h' 




a 


— ^ 






^N^- - 




/ 


ym 








"^ 


\^ 










c 










d 






Fig. 94. Course followed by light through a cylinder abed corresponding to 
the dioptric apparatus of the ommatidium. A, path of a ray of light. 
B, course of a spherical wave, a -b', layer of equal refringence ; x, point 
of origin of wave; mm, mini, etc.", successive positions of wave front 
indicating changes due to refraction accompanying passage through 
cylinder; y, focal point. (Redrawn from Exner, 1891.) 



duce an inverted image at its base. If a cyhnder is twice as long as its 
focal length it will produce an inverted image at its midpoint (Fig. 95). 
The rays will then diverge from the focal point and continue on straight 
paths. Rays that enter the cylinder obliquely (e.g., from the right) will 
emerge from the same side (i.e., the right). 

If, in the apposition eye, the ommatidium is the optical unit, if it 
perceives Hght primarily from points on or near its axis, if there is 
minimal overlap of ommatidial visual fields and the image which has 
o 



200 THE PHYSIOLOGY OF INSECT SENSES 

significance for the insect is a mosaic of point of light, then visual 
acuity should depend upon the number and spacing of luminous points 
received from the object in the visual field. There should be exact 
correspondence between the minimum angle subtended by adjacent 
ommatidia and the minimum angle subtended by two points that are 
perceived as separate (the reciprocal of the visual angle is termed the 
visual acuity). 




c 

11 , 


■ ''" ^--^-^ ,--- - -. 


a 


!'-''' 


.--'•--''^^'^>3><'''^^----.- 


~^-.^ 




__::-^'^"^^^- - 


^~^-.^ 


^'--""' , 




^ -.^ 




b 



■-/' 



Fig. 95. Course of light rays through a lens cylinder abed whose length is 
(A) equal to its focal length (B) twice the focal distance, m, p, n, q, 
rays from objects in the visual field; q', n', p', m', course of rays after 
passage through cylinder; xy, optic axis; zy, inverted image of object 
at base of cylinder. Note that in B an inverted image is produced at 
mid-point of cylinder. Rays continue through to produce an erect 
image at the rhabdoms. (Redrawn from Exner, 1891.) 

Acuity does indeed depend upon the angle between adjacent direc- 
tional elements, but reducing this angle to increase acuity has limita- 
tions. There is no improvement in acuity when the angle is so close that 
visual overlapping occurs, and there is now evidence that such over- 
lapping is much greater than would be predicted from Muller's theory 
(de Vries, 1956; Burtt and Catton, 1954). Furthermore, as Barlow 
(1952) has pointed out, visual acuity is related to the resolving power of 
each ommatidial lens. 

The resolving power of a lens is limited by its optical properties and 
the wave nature of light. The diameter of the ommatidium is critical, 
and diffraction must be taken into consideration. Because of dif- 



PHOTORECEPTION 201 

fraction, light coming through a small circular aperture produces an 
Airy pattern, a central point of maximum intensity with two concen- 
tric dark rings alternating with light rings. If two point sources are to 
be resolved they must be far enough separated so that the bright image 
centre of one falls no closer than within the first dark ring of the Airy 
pattern of the other. Miiller (1826) had said that an apposition omma- 
tidium was sensitive only to light from a point on or near its axis. It is 
maximally sensitive on its axis and minimally sensitive away from its 
axis, so the diameter determines how close two points can be if one is to 
stimulate maximally and the other minimally. In the honeybee, if the 
eye resolves points separated by twice the minimal ommatidial angle 
the performance of the ommatidia has approached the theoretical 
limit set by diffraction. 

It is by no means certain, however, that the ommatidium is the 
optical unit of the eye. Refined techniques which permit illumination 
of single rhabdomers (in Diptera) have prompted the suggestion that 
it is the retinal cell which is the functional unit of the eye (de Vries, 
1956; de Vries and Kuiper, 1958; see also Burkhardt and Wendler, 
1960; Antrum and Burkhardt, 1961). By cutting transversely through 
an ommatidium in the region of the rhabdom and examining the cut 
end of the rhabdom as light is transmitted through the crystalline cone 
it can be seen that each rhabdom 'looks' at a different part of the visual 
field. Each visual field has a diameter of about 4 degrees, and the fields 
of neighbouringcells overlap so that the centre of one field lies approxi- 
mately at the edge of the neighbouring field. The field of the whole 
ommatidium is about 8 degrees, and it overlaps with that of its 
neighbours. As with the entire ommatidium when it is analysed as a 
unit, the field of the individual cell is controlled by the diameter of the 
rhabdom and the diffraction of Hght. If a point source of light being 
viewed at the cut end of a rhabdomer is displaced more than 2 
degrees from the optical axis of the retinal cell, it shines again, but 
more weakly, by reason of the diffracted hght outside of the first dark 
ring of the Airy pattern. Once a beam has reached a rhabdomer it will, 
unless it deviates too far from the optical axis, be reflected repeatedly 
at the boundaries of the rhabdomer, since it has a higher refractive 
index than surrounding tissues. In this manner the rhabdomer acts as 
a wave-guide, and the cell captures light (see also Demoll, 1917). 
Since the internal reflexion decreases as the angle between the incident 
beam and the axis of the cell increases, there is a directional sensitivity 
in these cells, the Stiles-Crawford effect of human vision (de Vries 
and Kuiper, 1958). 



202 THE PHYSIOLOGY OF INSECT SENSES 

If one recalls that the ommatidium is a multi-innervated sensillum 
and that the neurons of a sensillum may possess quite different 
characteristics (e.g., the chemoreceptive hair of flies), the indepen- 
dence of retinal cells is not unreasonable. On the other hand, the 
significance of the pattern of responses from single retinal cells cannot 
be simple because of the intricacy of synaptic connexions in the lamina 
ganglionaris. For every retinal cell whose axon traverses the area there 
are many that synapse together on giant monopolar neurons. Further- 
more, there are many local chiasmata each involving several ommati- 
dia. Some success towards understanding the extent to which an 
ommatidium is a functional unit of the eye has been achieved by the 
sophisticated functional analyses of movement perception by Hassen- 
stein (1951, 1959) and Hassenstein and Reichardt (1956). 

Behavioural measurements of visual acuity (usually derived from 
optomotor responses) have not always corresponded to the minimal 
ommatidial angle (Hecht and Wolf, 1929; Hecht and Wald, 1934; 
Wolf, 1933 a, 1933 b). Compared with man, whose visual acuity is from 
2 to 2-5, the maximal visual acuity of the bee is 0-017 and ofDrosophila, 
0-0018. In the case of the bee, the value obtained corresponds exactly 
to the smallest ommatidial angle (0-90-1-00 degrees) measured by 
Baumgartner (1928). In other cases, however, the correspondence has 
been less exact, the acuity being either greater or less. 

Where the visual acuity has been less than expected in terms of 
ommatidial angles a number of explanations have been offered. Von 
Buddenbrock and Schulz (1933) proposed that ommatidia might be 
acting not as units but as pairs or groups. This hypothesis would also 
explain observed differences of visual acuity at high and low light 
intensities. As with man, the relation between visual acuity and the 
logarithm of intensity is described by a sigmoid curve (Fig. 96) 
(Hecht and Wald, 1934) which has been interpreted as an integral 
population curve denoting the number of retinal elements active at 
each intensity. In both the bee and Drosophila visual acuity and in- 
tensity discrimination, as measured by optomotor reactions, begin at 
approximately the same intensity and change rapidly within two log 
units (Wolf, 1933 a, 1933 b; Hecht and Wald, 1934). 

It is also possible that visual-acuity measurements obtained from 
behavioural studies depend upon what part of the eye is being stimu- 
lated at the time. Viewed from the outside, the lens surface of a com- 
pound eye is an approximate and imperfect hemisphere. The relative 
area with respect to the head, and the number of ommatidia, vary from 
species to species and often between the sexes. Each of the ommatidia 



PHOTORECEPTION 



203 



200 




Log I (mlLLUamberts) 

Fig. 96. Relation between visual acuity and intensity of illumination 
for the eye of the bee. (Redrawn from Hecht and Wolf, 1929.) 




Log I (tn'dULamberts) 
A 




Log I (mUlUamberts) 
B 



Fig. 97. Relation between visual acuity and illumination in bees in which 
A, the central area of the eye has been opaqued; B, the anterior region 
of the eye has been opaqued. The broken line represents the curve for 
normal individuals. (Redrawn from Hecht and Wolf, 1929.) 



204 THE PHYSIOLOGY OF INSECT SENSES 

faces in a different direction. As a result of these differences in align- 
ment and the fact that the lenses may differ in size from one part of the 
eye to another, the angle subtended by adjacent ommatidia is not 
constant for any given eye (Baumgartner, 1928; del Portillo, 1936). 
Measurements of visual acuity in insects in which various areas of the 
eye have been blacked out have shown that the eye is not uniform 
(Hecht and Wolf, 1929). When the centre of an eye, where the minimal 
ommatidial angle is 1 degree as compared with 4 degrees at the 
periphery, is blacked out the visual acuity decreases (Fig. 97). It also 
decreases as the number of functional units is reduced (Fig. 97). 

Another technique for measuring visual acuity was employed by 
Burtt and Catton (1954) following their discovery in Locusta, Phormia, 
and Calliphora that the movement of illuminated objects in the visual 
field was accompanied by specific electrical discharges in the ventral 
nerve cord. By employing these discharges as a criterion of movement 
perception, Burtt and Catton were able to ascertain that the overlap of 
ommatidial fields, at least in Locusta, is much greater than heretofore 
realized. The angle of the visual field is 20 degrees; the average angle 
subtended by adjacent ommatidia is about 2-4 degrees in the longi- 
tudinal and 1 degree in the vertical meridian. Responses to movement 
were obtained to angular displacements in the visual field as small as 
0-16 degree of arc. The threshold of acuity was independent of light- 
and dark-adaptation. Burtt and Catton suggested that the extensive 
overlapping makes possible the perception of an angle smaller than 
that subtended by adjacent ommatidia; however, the experiments of 
de Vries (1956) suggesting independent action of individual retinal 
cells offer an alternative explanation. 

Whatever their visual acuity may be, there is no doubt that insects 
can resolve patterns. A series of field experiments with honeybees has 
shown them to be fairly efficient in this respect (Hertz, 1929 a, 1929 b, 
1931, 1933a, 1934, 1935a, 1935b, 1935c, 1937a). By training bees to 
associate specific black figures on a white background with food. Hertz 
was able to demonstrate that contrast, contour, and the degree of sub- 
division of the form are perceived. She concluded that the most greatly 
divided pattern is preferred, but that the pattern is recognized as such. 
The results of Zerrahn (1933) and Wolf and Zerrahn-Wolf (1937), 
based on field and laboratory experiments in which bees were per- 
mitted to choose patterns spontaneously, are in essential agreement ; 
however, these workers derived different conclusions. They contended 
that the pattern as such has no meaning. The number of choices of each 
pattern was proportional to the length of its contours, that is, the 



PHOTORECEPTION 205 

length of edges of black against white. This finding suggested that 
recognition and discrimination is based merely upon the degree of 
transitory stimulation produced in the compound eye. To test this 
hypothesis, Wolf and Zerrahn-Wolf mapped on translucent co- 
ordinate paper the points of intersection of the axes of the ommatidia 
with a place located at the same distance from the eye as were patterns 
used in testing. They then placed the co-ordinate paper over a pattern 
and counted the number of ommatidia whose visual fields would be 
black and the number whose fields would be white. They also counted 
the number of ommatidia in which there would be a black-white shift 
when the pattern was moved over a unit distance in any direction. 
Calculations could then be made of the relationships between the area 
of a pattern and the degree of subdivision necessary to provide a con- 
stant transition value. Predictions of discrimination based on these 
calculations were realized in field tests. Other lines of evidence were in 
agreement. For example, bees conditioned to flickering fields of equal 
size but different flicker frequencies exhibited choices that were directly 
proportional to the flicker frequency. These findings are in agreement 
with observations on the natural behaviour of bees in the field (Wolf, 
1933 c). The honeybee reacts much more effectively to moving flowers 
than to stationary ones. 

All of these experiments suggested that movement is of greater sig- 
nificance in form perception than the ability to resolve stationary 
patterns (cf. Exner, 1891). In its response to flicker the insect eye 
exhibits many of the characteristics of the human eye. It obeys Talbot's 
law (the brightness of a fused light produced by flashing it on and off" is 
visually equivalent to the product of the actual source of illumination 
and the proportion of the time it is on) and the Ferry-Porter law 
(critical frequency, that is, the frequency at which a flashing light fuses, 
is proportional to the logarithm of intensity) as does the human eye 
(Wolf and Zerrahn-Wolf, 1935 b; Wolf, 1933 b). It is, however, more 
eflflcient at detecting flicker than is the eye of man. Some of the early 
values obtained for insects by optomotor methods were : 55 per second 
for the bee (Wolf, 1933 b); i 60 per second for dragonfly larvae 
(Salzle, 1932; Crozier, Wolf, and Zerrahn-Wolf, 1937). More highly 
developed behavioural techniques indicated that maximum values are 
actually much higher. The critical flicker frequency for Calliphora is 
about 265 per second, depending upon the number of ommatidia 
stimulated. The maximum of 265 per second drops to 60-165 per 
second when only one to four ommatidia are stimulated. A similar 
relationship holds for the honeybee (Autrum and Stoecker, 1950). 



206 THE PHYSIOLOGY OF INSECT SENSES 

Studies of the electrical response (ERG) of the eye to flickering light 
agree beautifully with recent behavioural studies. As described 
earlier in this chapter, there are oscillations in the ERG which are 
synchronized with the stimulus flashes. In *fast* eyes (e.g., Calliphora, 
Apis) the synchrony persists at even higher frequencies than those 
judged by optomotor responses to be fusing. In 'slow' eyes (e.g., 
Dixippus, Tachycines, Periplanetd) the responses, both behaviourally 
and electrophysiologically, are slower. These findings and the con- 
clusions of others (Zerrahn, 1933 ; Wolf and Zerrahn-Wolf, 1937) that 
the decisive feature of pattern recognition is the transitory stimulation 
ofommatidia suggested to Antrum (1948 a, 1948 b, 1949, 1952, 1955 b) 
the idea of temporal resolution. 

The concept is based upon the assumption that the ommatidium is 
the optical unit of the eye. In rapidly flying insects the angle subtended 
by ommatidia in the horizontal direction is approximately twice that 
in the vertical (del Portillo, 1936). During horizontal movement a 
point being observed remains in the visual field of a single ommatidium 
longer; consequently, the summation time for this stimulus is pro- 
longed. Points of a pattern that succeed each other rapidly fuse less 
readily. Accordingly, the capacity for discrimination is improved 
through movement (Antrum, 1949). Studies of ERGs show that two 
points of light succeeding each other within a critical time fuse if they 
pass over the ommatidial grating vertically, but act as individual 
stimuli if they pass horizontally. The electrophysiological responses of 
*fast' eyes reveal features which tend to favour reception of repetitive 
stimuli of short duration. The ERG shows that the on-effect for stimuli 
of 1-To^ second depends only upon intensity. It is independent of 
duration. The off"-effect depends on the product of intensity and 
duration. Furthermore, in the 'fast' eyes, according to Antrum, a 
positive off'-effect originating in the lamina ganglionaris prevents sus- 
tained depolarization as occurs in 'slow' eyes, and thus 'prepares' the 
eye for the next stimulus. 

Insects also appear to be responsive to stroboscopic (apparent) 
motion. In contrast to the negative findings of Gaffron (1934), 
Antrum and Stocker (1952) demonstrated that this phenomenon 
exists provided that certain critical conditions are met. For strobos- 
copic motion to be perceived the time sequences must be short for those 
insects ('fast') whose eyes possess high temporal resolution and long 
for those ('slow') species whose eyes possess low temporal resolution. 
A close relationship exists between the times that are important in 
motion perception, whether real or apparent, and the times for which 



PHOTORECEPTION 207 

the receptors can still separate separate stimuli. Motion is perceived 
as a vector without spatial connotations when two stimulated omma- 
tidia are separated by an unstimulated one (Hassenstein, 1951). 

OCELLI 

Many insects possess dorsal ocelli in addition to compound eyes. The 
distribution of ocelli within the Class is erratic and is of no assistance 
in the problem of interpreting the role that these organs play. 

The structure is basically similar in all ocelli. It consists of a trans- 
parent cornea which may be perfectly flat on both surfaces, biconvex, 
or plano-convex. Underlying the cornea there is frequently a trans- 
parent layer of corneagen cells and beneath this a layer of retinal cells 
very similar in structure to those of the compound eyes. In the more 
complex ocelli the corneagen cells may be thickened to form a aux- 
iliary refractory organ. The retinal cells are grouped together in units 
of two, three, or four, and each cell of a unit contributes to a central 
rhabdom. In the lateral ocellus of Sympetrum there are about 675 
photoreceptor cells. Beneath them lies a reflecting layer, the tapetum. 
As the sensory axons proceed proximally they soon form synaptic 
connexions with the intra-ocellar terminals of the ocellar nerve fibres 
(Cajal, 1918; Ruck, 1957). The ocellar nerve of the cockroach consists 
of about twenty-five fibres, of which four are very large - 6-10 \l. 
In the dragonfly {Sympetrum) there is one giant fibre (25-38 [x) and 
three or four ranging in diameter from 4-13 [x. The remainder are 
1 [I or less. The neurocytes lie in the brain (Cajal, 1918 ; Satija, 1958 a, 
1958 b). 

Although the corneal lens is capable of forming fairly sharp images, 
everyone who has studied the optics of the system agrees that the image 
has little significance, since it falls a considerable distance behind the 
retina (Homann, 1924; Parry, 1947; Cornwall, 1955). 

Electrical events have been studied in the ocelli of Locusta migra- 
toria migratoroides (Parry, 1947; Hoyle, 1955; Burtt and Catton, 
1958), Periplaneta americana (Ruck, 1957, 1958 a; Goldsmith and 
Ruck, 1958), Blaberus craniifer (Ruck, 1957, 1961a), Melanoplus 
bivittatus (Ruck, 1957), Apis mellifera (Goldsmith and Ruck, 1958; 
Ruck, 1958 b). Pachydiplax longipennis and Phormia regina (Ruck, 
1958 b), Libellula luctuosa (Ruck, 1961 a), Libellula vibrans (Ruck, 
1961 b), Anax Junius, Aeschna sp., and Sympetrum ribicundulum 
(Ruck, 1961 c). Because different workers employed different record- 
ing situations it is difficult to compare their results and to reconcile 



208 THE PHYSIOLOGY OF INSECT SENSES 

differences in the wave form and sign of the ERG. The most compre- 
hensive analysis is that based upon extensive studies of the ocellus of 
the cockroach and dragonfly (Ruck, 1958 a, 1958 b, 1961 a, 1961 b). In 
these insects the total electrical response to light of high intensity 



oscilloscope 



different 




Fig. 98. Components of the ERG of the model ocellus. One photoreceptor 
cell {left) with an expanded sensory ending, and an axon which makes 
synaptic contact with one ©cellar nerve fibre. The two units are con- 
tained in an electrolyte-filled compartment. A 'corneal' electrode 
enters at left; a 'nerve' electrode lifts the nerve into air; an indifferent 
electrode is placed far to the right. Four components of the ERG are 
shown, each in one repetition of the model. Active sites for each 
component are shaded. Current at active sites is indicated by arrows. 
Each component appears at corneal and nerve electrodes. (Redrawn 
from Ruck, 1961 a.) 



consists of four components, of which two originate in the retinal cells 
and two in the ocellar nerve (Fig. 101). The first event is a generator 
potential arising in the distal end of the receptor. It evokes a depolariz- 
ation in the axonal region of the receptor. This in turn evokes a 
hyperpolarizing postsynaptic potential in the fibres of the ocellar 



PHOTORECEPTION 209 

nerve. This component is easily discernible in the ocelli of dragonflies 
but rarely detected in cockroaches. Ruck (1961 b) has suggested that 
the postsynaptic potential is not induced directly by the electrical 
events in the receptor axon, but rather by the liberation of a trans- 
mitter substance at the end of the receptor axon. In the absence of the 
hyperpolarizing potential the fibres of the ocellar nerve discharge 
impulses (component 4). In the dragonfly the ocellar nerve in the dark 
discharges spontaneously, while the cockroach nerve usually dis- 
charges only at off. It is inferred that there is spontaneous receptor cell 
activity which modulates the rhythmic spontaneous discharges in the 
ocellar nerve. 

The ocellus of the dragonfly is a very sensitive receptor. Corneal 
illumination as low as 10~^ ft.-candles produces an ERG (Ruck, 
1958 b). Furthermore, it is to be expected that sensitivity is enhanced 
by the high degree of convergence of receptor axons on ocellar nerve 
fibres, multiple synapsing of single receptor axons with ocellar nerve 
fibres, and the presence of a white tapetum (Ruck, 1961 a). 

The ability of the ocellus to respond to flickering light varies from 
species to species. The flicker fusion frequencies of Apis, Pachydiplax, 
and Phormia are very high, being, respectively, 250-265, 200, and 
+220 per second. For the cockroach maximum flicker fusion fre- 
quencies range from 45 to 60 per second (Ruck, 1958 a). Thus, the 
ocelli of those insects with *fast' eyes are *fast' and those with 'slow' 
eyes, *slow'. As with the compound eyes. Ruck (1958 b) found that 
there is no general relation between flicker fusion frequency and 
sensitivity or rate of dark adaptation. Furthermore, since ocelli do not 
possess a lamina ganglionaris and since in the dragonfly the generator 
potential can respond to higher rates of flicker (220 per second) than 
can the receptor axon responses, the postsynaptic potential and the 
ocellar nerve impulses, the difference between 'fast' and 'slow' ocelli 
is a fundamental characteristic of the photoreceptor cell itself. The 
evidence of Antrum and Gallwitz (1951) that the abihty of 'fast' com- 
pound eyes to follow high rates of flicker depends upon electrical 
interaction between the receptor cells and neurons of the optic 
ganglion cannot be extended to ocelH. 

Dorsal ocelli are sensitive to the same spectrum of wavelengths as 
are compound eyes. The ocelH of Periplaneta have a single sensitivity 
peak at 500 mi^., while those of the honeybee show sensitivity maxima 
at 490 mjj. and at 335-340 m[L (Goldsmith and Ruck, 1958). Because in 
the honeybee the ERG produced by ultra-violet stimulation is quali- 
tatively different from that produced by stimulation of light of 490 mjjt, 



210 THE PHYSIOLOGY OF INSECT SENSES 

Goldsmith and Ruck (1958) believe that there are two types of receptor 
in this organ. 

The exact nature of the contribution of dorsal ocelli to behaviour is 
still elusive. Alone they are insufficient for phototaxis (Homann, 1924 ; 
Bozler, 1926; Muller, 1931; Wellington, 1953; Cornwall, 1955; but 
compare Gotze, 1927 and Wellington, 1953). They are not, however, 
totally without effect in light-directed behaviour. Elimination of ocelli 
may cause phototaxis to be temporarily reversed (Muller, 1931), 
reduce the speed of response to Hght (Bozler, 1926; Muller, 1931), or 
alter the direction of response to two light sources (Muller, 1931). In 
Periplaneta the characteristic persistent daily rhythm depends upon 
stimulation of the oceUi (Marker, 1956). As a consequence of these 
actions the ocelli are generally considered to be * stimulatory' organs 
(Bozler, 1926; Wolsky, 1930, 1931, 1933). 



STEMMATA 

With the possible exception of dermal receptors sensitive to Hght, the 
lateral oceUi or stemmata are the sole visual organs possessed by many 
larval insects. Structurally they vary from forms similar to the dorsal 
ocelli of adults (e.g., larval ocelli of Tenthredinidae) to mere pigment 
spots equipped with refractive bodies. In blowfly larvae the photo- 
receptors are small groups of vacuolated cells pocketed among the 
hypodermal cells of the cephalic region (Bolwig, 1946). 

The most thoroughly studied stemmata are those of lepidopterous 
larvae (Grenacher, 1897; Hesse, 1901; Dethier, 1942, 1943). Each 
resembles an individual ommatidium. It possesses two lenses, one 
corneal, the other analogous to the crystalline cone of compound eyes. 

Table 9 

(From Dethier, 1953 c) 

Optical constants of the six ocelli of Isia Isabella 



Ocellus 


Minimum Angle 

of Resolution 

(Radians) 


/ value 


Dioptric 
Value 


Type of 
Image 


Focal 
Distance 


1 

2 
3 
4 
5 
6 


M X 10--^ 
1-2 X 10-2 
5-3 X 10-3 
7-1 X 10-3 
7-8 X 10-3 
1 X 10-2 


0-93 
0-89 
0-50 
0-67 
0-73 
100 


14,285 
14,084 
14,285 
14,285 
13,888 
14,084 


Triple 
Triple 
Single 
Single 
Single 
Triple 


070 
071 
070 
070 
072 
071 



PHOTORECEPTION 211 

The first is a thick converging concavoconvex or biconvex meniscus 
lens. 

If the secretion products of the three corneagen cells fuse incom- 
pletely during the formation of this lens, as is typical of certain ocelli, 
the cornea acts as a triple lens and forms three images (PL IV). The 
crystaUine lens, like the cornea, is a thick, converging biconvex lens, 
either unitary or tripartite to correspond with the cornea. It also forms 
more or less distinct, real, inverted images. The receptive layer, like 
that of the ommatidium, consists of distal and proximal retinula cells. 
Some of the optical constants obtained from the lenses of the six ocelli 
of the caterpillar Isia Isabella are given in Table 9. The peculiar optical 
properties of the lens system of ommatidia as described by Exner 
(1 89 1) are not characteristic of these lenses. 

Whether the ocellus acts as an eye or merely as a photoreceptor 
depends primarily on : (1) the ability of the dioptric apparatus to form 
images ; (2) the location of the image plane with respect to the rhab- 
dom; (3) the ability of the rhabdom to receive any images formed. By 
determining the image space (that region of space in which all possible 
positions of the image are situated) from the optical constants and by 
actual measurement of the length of the vertical retinal elements, 
Dethier has shown (Fig. 99) that regardless of the distance of an 
object from the ocellus, the image falls somewhere along the length 
of the rhabdom. In this manner a degree of accommodation is obtained 
which would otherwise be impossible with a fixed-lens system. The 
ocellus is analogous in this respect to a fixed-focus camera. 

Vision in insects bearing simple eyes is the sum of the capacities 
of all units operating jointly. Hundertmark's (1936, 1937) experiments 
have shown that larvae which orient to black shapes on a white back- 
ground are directed towards the black-and-white boundary. Dethier 
has postulated that the basic principles of mosaic vision apply equally 
well to lateral ocelH and compound eyes. Since each ocellus gathers 
light from the area at which it is directed and concentrates this light 
at some point along the vertical rhabdom, the six pairs of ocelli 
together form twelve points of light. The ocelli are so arranged on the 
head that little or no overlapping of the visual field exists, hence each 
spot represents the intensity from a different area. Combined they 
provide an exceedingly coarse mosaic of intensities. The paucity of 
units is compensated for in part by the habit, characteristic of many 
larvae, of moving the head from side to side while advancing. By this 
klinotactic-like behaviour a larger visual field is examined, and the 
recognition of changes in intensity, as at a black-white boundary, is 



212 



THE PHYSIOLOGY OF INSECT SENSES 



*,-— 




Fig. 99. A. Camera lucida drawing of an ocellus of the caterpillar of 
Isia Isabella to illustrate the congruity of image space and retinal space 
and the kind of accommodation offered by a vertical rhabdom. 
Oi, O2, O3, representative objects; Ii, Ig, I3, positions of resultant 
images; F, focal point; CO, cornea; CR, crystalline lens; DR, distal 
retinula; PR, proximal retinula. The broken line in the cornea repre- 
sents the ideal lens curvature. B. Graphic construction of images 
formed. O, object; Iv, virtual image; Ir, real image; Fi, focal point of 
corneal lens; Fg, focal point of crystalline lens; F, focal point of entire 
lens system. (From Dethier, 1943.) 



PHOTORECEPTION 213 

facilitated by this motion. Even in those species (e.g., Cicindela) where 
the ocellus consists of a larger number of retinal elements beneath 
each lens, it is believed that all ocelli function together as a unit. 

Little is known about the parameters of the stimuli for stemmata. 
It has been demonstrated that larvae are sensitive to a wide band of 
the spectrum and seem to be able to respond to the plane of polariz- 
ation (Wellington, Sullivan, and Green, 1957). Electrophysiological 
studies have only just been undertaken with these receptors. The 
ERG recorded with the active electrode on the ocellar nerve and the 
reference electrode in the abdomen is simple in appearance. It con- 
sists of a prominent positive wave followed at high intensities of 
stimulation by a slow negative wave. It is believed to consist of two 
components (Ishikawa and Hirao, 1960 a, 1960 b). The stemmata 
become completely dark-adapted in about one hour and completely 
light-adapted in about ten minutes. They follow flicker up to 
25-30 per second. 



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254 THE PHYSIOLOGY OF INSECT SENSES 

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Author Index 



Adams, J. R., 24, 25, 116 

Adrian, E. D., 175 

Ahonen, U., 157 

Alexander, R. D., 91 

Alexandre wicz, J. S., 44 

Alvarez-Buylla, R., 32 

Amouriq, L., 159 

Andersen, L. W., 158 

Anderson, A. L., 126 

Anderson, D. B., 157 

Arab, Y. M., 8, 146, 148 

De Arellano, J. R., 32 

Auger, D., 215 

Autrum, H., 68, 88, 89, 91, 94, 106, 
107, 108, 109, 111, 168, 169, 170, 
171, 172, 173, 174, 175, 177, 178, 
181, 182, 187, 188, 189, 190, 193, 
194, 198, 201, 205, 206, 209 

Aziz, S. A., 158, 159, 160 

Bainbridge, R., 191, 196 

Ball, H. J., 158 

Barany, E., 127, 128 

Barlow, H. B., 200 

Barrows, W. M., 117 

Barton Browne, L., 144 

Bassler, U., 64, 65 

Bauer, L., 126, 138, 154, 155 

Bauers, C, 217 

Baumgartner, H., 202, 204 

Baunacke, W., 71, 72 

Baylor, E. R., 191, 193, 194, 195, 196 

Beams, H. W., 17, 20, 21, 22, 24, 40, 

114, 115 
Bechmann, R., 124 
Becht, G., 63 
Begg, M., 113, 160 
Beidler, L. M., 131, 151, 152 
Belton, P., 95, 97 
Bentley, E. W., 157, 158, 159 
Benz, G., 159, 160 
Berlese, A., 40 
Berman, R., 137 

Bemhard, C. G., 29, 169, 172, 175 
Bertholf, L. M., 178, 179, 180 
Birukow, G., 190 



Boistel, J., 123 

Bolwig, N., 113,210 

Borror, D. J., 91 

Bowness, J. M., 167 

Boyd, W. M., 178 

Bozler, E., 210 

Brauns, A., 67 

Bray, C. W., 89 

Bretschneider, F., 165 

Brink, F., 134 

Broughton, W. B., 91 

Brown, F. A., 178, 184, 187, 189, 191, 

193 
Brust, M., 177 
Buck, J. B., 178 
BiJckmann, D., 75 
Von Buddenbrock, W., 77, 202 
Bullock, T. H., 4, 5 
Burg, S. P., 167 
Burkhardt, D., 60, 61, 62, 64, 65, 175, 

176, 188, 189, 193, 194, 201 
Bursell, E., 159, 160 
Burtt, E. T., 174, 175, 200, 204, 207 
Busch, E., 190 
Busnel, M. C, 91 
Busnel, R. G., 91, 92 
Butenandt, A., 124 

Cajal, S. R., 165, 166, 173, 207 
Cameron, J. W. M., 178, 179, 180 
Capenos, J., 163 
Catton, W. T., 174, 175, 200, 204, 

207 
Chadwick, L. E., 64, 112, 126, 127, 131, 

132, 133, 134, 136 
Chavasse, P., 91 
Child, C. M., 59, 60, 103 
Cole, P., 159 
Contis, G., 167, 178 
Cook, W. C, 121 
Coraboeuf, E., 123 
Comwell, P. P., 207, 210 
Cosway, C. A., 157, 159 
Cragg, J. B., 159 

Cresci'telli, F., 169, 172, 175, 181, 184 
Crisp, D. J., 70, 71, 72, 73, 74 



256 



AUTHOR INDEX 



257 



Crombie, A. C, 118, 138 
Crozier, W. J., 205 

Dahlberg, A. C, 130 

Danneel, R., 222 

Darrah, J. H., 138 

Daumer, K., 178, 179, 184, 185, 186, 

190, 192, 196 

Davies, J. T., 122, 123, 124, 136 

Davis, H., 222 

Day, M. F., 7 

Debaisieux, P., 52, 55, 105, 106 

Debauche, H., 24, 52, 59 

Deegener, P., 78 

Demon, R., 40, 52, 55, 60, 201 

Deonier, C. C, 127 

Dethier, V. G., 8, 24, 30, 34, 66, 112, 
113, 115, 116, 117, 118, 119, 120, 
121, 122, 123, 124, 125, 126, 127, 
128, 129, 130, 131, 132, 133, 134, 
135, 136, 137, 138, 139, 140, 142, 
143, 144, 146, 150, 151, 210, 211, 
212 

Diakonoff, A., 36, 64 

Dingle, H., 63, 64, 69 

Dodds, S. E., 157, 159 

Dodt, E., 181, 182, 183, 187, 190 

Doira, S., 142, 144, 145, 147 

Donner, K. O., 181 

Dostal, B., 113, 114, 118, 120 

Dresden, D., 13, 63 

Edney, E. B., 157 
Eger, H., 126, 127 
Eggers, P., 19, 21, 22, 24, 52, 54, 57, 59, 

60, 66, 74, 78, 79, 85, 94, 105, 106 
Eguchi, E., 176 
Ehrensvard, G., 122, 123 
Erhardt, E., 66 
Erkkila, H., 157, 158 
Ernst, E., 159 
Evans, D. R., 116, 142, 143, 144, 150, 

151, 152, 153 
Ewer, D. W., 157, 159 
Exner, S., 196, 198, 199, 200, 205, 211 
Eyer, J. R., 121 
Eyzaguirre, C, 32 

Farthing, F. R., 137 

Faust, R., 68 

Ferguson, J., 134 

Fernandez-Moran, H., 163, 164, 165 

Fessard, A., 215 

Fingerman, M., 178, 184, 187, 189, 

191, 193 



Finlayson, L. H., 16, 44, 45, 46, 47, 48, 

49, 50, 51, 52, 78 
Fischer, W., 118 
Fishman, I. Y., 131 
Folsom, J. W., 7, 117 
Forel, A., 112 
Fraenkel, G., 63, 64 
Friedman, S., 64 
Friedrich, H., 227 
Frings, H., 77, 91, 94, 115, 121, 127, 

130, 131 
Frings, M., 77, 91, 94, 115 
VonFrisch, K., 112, 113, 114, 117, 125, 

126, 127, 129, 138, 154, 178, 183 

190, 192, 193, 196 
Fry, W. J., 177 
Fulton, B. B., 104 
Fyg, W., 163 

Gaffron, M., 206 

Gallwitz, U., 170, 172, 209 

Gans, J., 138, 140 

Gettrup, E., 228 

Goldsmith, T. H., 163, 164, 167, 178, 
179, 180, 181, 182, 183, 184, 185, 
186, 187, 189, 207, 209, 210 

Goodwin, T. W., 167 

Gomer, P., 192 

Gottsche, C. M., 196 

Gotze, G., 210 

Graber, V., 19, 21, 52, 54, 58, 78 

Grabowski, C. T., 8, 116 

Graham, C. H., 229 

Granit, R., 2, 29, 168, 177 

Gray, E. G., 24, 28, 79, 82, 85, 86, 87, 
89 

Gray, J. A. B., 32, 33 

Green, G. W., 158, 160, 213 

Grenacher, H., 163, 210 

-Griffin, D. R., 99 

Grisewood, E. N., 183 

Gunn, D. L., 157, 158, 159 

Giinther, K., 165 

Hackley, B. E., 117 
Haeussler, G. J., 178 
Hafez, M., 157, 159, 160 
Haffer, O., 10, 24 
Hagemann, J., 78 
Hamilton, M. A., 71 
Hamilton, W. F., 178, 184, 187 
Hanson, F. E., 149 
Hanstrom, B., 9, 10, 165, 189 
Hardiman, C. W., 131 
Harker, J. E., 210 



258 



THE PHYSIOLOGY OF INSECT SENSES 



Hartline, H. K., 168, 169, 172, 176 
Haskell, P. T., 77, 91, 92, 93, 95, 97, 

102, 103, 105 
Haslinger, R, 127, 138 
Hassenstein, B., 168, 170, 171, 174, 202, 

207 
Hassett, C. C, 138, 140 
Hauser, G., 113 
Hecht, S., 189, 202, 203, 204 
Hecker, E., 123, 124 
Heintz, E., 178, 179, 180 
Henke, K., 10 
Heran, H., 64, 65 
Hers, J., 79 
Hertwick, M., 55, 66 
Hertz, M., 178, 184, 204 
Hess, C, 183 
Hess, W. N., 19, 54, 55 
Hesse, R., 210 
Hicks, J. B., 40 
Hill, R., 138 
Hinton, H. E., 99 
Hirao, T., 168, 213 
Hodgson, E. S., 118, 127, 130, 131, 

142, 143, 144, 146, 147, 151, 155 
Hoffmann, C, 168, 170, 171 
Hoffmann, E., 216 
Hogben, L., 113, 160 
Hollick, F. S. J., 64, 65 
Holste, G., 165 
Homann, H., 207, 210 
Hoskins, W. M., 118 
Hoyle, G., 7, 8, 62, 207 
Hsij, P., 16, 23, 24, 28, 40 
Hughes, G. M., 57, 58, 62, 63, 69, 103 
Humphreys, W. J., 156 
Hundertmark, A., 211 

Use, D., 178, 180, 184 
Imamura, S., 127 
Ishikawa, S., 168, 176, 213 



Kennedy, D., 193, 194 

Kennedy, J. S., 157 

Von Kennel, J., 78 

Keppler, E., 236 

Kim, C.-W., 236 

Kirschfeld, K., 170 

Koehler, O., 178 

Kraepelin, K., 112 

Kriszat, G., 181 

Kruming, R., 9, 10 

KufSer, S. W., 32 

Kiihn, A., 178, 183, 197 

Kuiper, J. W., 191, 193, 194, 195, 201 

Kunze, G., 127 

Kuwabara, M., 61, 114, 143, 144, 145, 

147, 159, 160, 168, 170, 171, 174, 

175, 178, 184, 193 

Larsen, J. R., 24, 25, 116 

Larsen, O., 52, 55, 56, 73, 74 

Lecompte, J., 123 

Lees, A. D., 18, 158, 159 

Lehr, R., 52, 59, 66 

Leighly, J., 157 

Lemberger, F., 130 

Lettvin, J. Y., 142, 143, 144 

Leydig, F., 52 

Licklider, J. C. R., 128 

Liebermann, A., 119 

Lindauer, M., 36, 75, 76, 190, 192, 196 

Linde, F. A., 177 

Lissmann, H. W., 35 

Loher, W., 91, 92 

Lotmar, R., 238 

Lx)wenstein, O., 16, 44, 45, 46, 47, 48, 

49, 50, 51, 52, 78 
Lowenstein, W. R., 33 
Lowne, B. T., 36 
Lubbock, J., 177, 178 
Liidtke, H., 183, 190, 191, 193 
Lutz, F. E., 183 



Jacobs-Jessen, U., 191, 192 

Jahn, T. L., 168, 169, 172, 175, 176, 

181, 184 
Jander, R., 190, 191, 192 
Jielof, R., 195 
Johnson, B., 65 
Johnston, C, 59, 60, 103 
Jordan, K., 78 

Kalmus, H., 191, 196 
Kamerling, S. E., 131 
Katsuki, Y., 61, 92 
Katz, B., 32, 33 



Machatschke, J. W., 163 

MacNichol, E. F., 169, 176 

Markl, H., 36, 76 

Marshall, J., 112, 127 

Massera, M. G., 175 

Mayer, A. M., 60, 103, 104 

McCoy, E. E., 178, 189 

McDonald, P. R., 231 

Mclndoo, N. E., 8, 40, 112, 114, 118 

Medler, J. T., 121 

Melin, D., 114 

Mellon, A. D., 116, 151, 167, 178 

Mellon, D., 143, 152, 153 



AUTHOR INDEX 



259 



Mcnzer, G., 190, 104 

Merker, E., 183 

Miller, W.H., 164 

Milne, L. J., 178 

Milne, M. J., 178 

Minnich, D. E., 100, 112, 126, 127 

Mittelstaedt, H., 36, 37, 38, 39, 63, 68 

Moller, H., 74 

Moller-Racke, I., 178, 183 

Moncrieff, R. W., 126, 130 

Morita, H., 113, 123, 125, 142, 143, 

144, 145, 147, 148, 151 
Muller, E., 210 
Muller, J., 78, 196,200,201 
Mullins, L. J., 122, 123 

Naka, K., 168, 170, 171, 174, 175, 176, 

193 
Nedel, J. O., 36, 75, 76 
Neuhaus, W., 123 
Newton, H. C. P., 10, 40 
Nickerson, M., 169, 172 
Nijenhuis, E. D,, 13, 63 

Oevermann, H., 68, 69, 71 
O'Neal, B. R., 127, 131 
Orlov, J., 15, 16 
Osborne, M. P., 45 
Osterhout, W. J. V., 131 
Owen, W. B., 241 

Papi, F., 192 

Parry, D. A., 207 

Pasquinelly, P., 91, 92 

Penczek, E. S., 130 

Perttunen, V., 157, 158, 159, 160 

Peters, W., 10, 36, 116 

Peterson, A., 178 

Pflugstaedt, H., 19, 40, 67 

Philpott, D. C, 163, 164 

Pielemeier, W. H., 91 

Pielou, D. P., 119, 158, 159, 160, 161 

Pierce, G. W., 91 

Pilgrim, P. J., 130 

Pirenne, M. H., 127 

Plateau, P., 177 

Pohl, R., 178, 183 

Del Portillo, J., 204, 206 

Postemak, J. M., 134 

Power, M. E., 165, 167 

Prestage, J. J., 17, 20, 21, 22, 24, 40, 

114, 115 
Pringle, J. W. S., 12, 13, 28, 36, 37, 38, 

39, 40, 41, 42, 43, 44, 53, 54, 62, 63, 

64, 66, 67, 68, 78, 95 



Pumphrey, R. J., 24, 28, 34, 58, 77, 88, 
90, 91, 92, 93, 94, 100, 101, 102, 103 

Rabc, W., 69 

Radl, E., 54, 55 

Ramsay, J. A., 157 

Vom Rath, O., 9, 10 

Rau, P., 244 

Rawdon-Smith, A. P., 58, 90, 91, 92, 

100, 101, 102, 103 
Redikorzew, W., 224 
Reed, M. R., 117 
Regen, J., 89, 91, 93 
Reichardt, W., 202 
Resch, B., 178, 183, 190 
Rhoades, M. V., 129, 130, 142, 150 
Richard, G., 15, 16, 28, 59 
Richards, A. G., 113, 163 
Riegert, P. W., 158, 159, 160 
Ritter, E., 118, 127, 154, 155 
Roeder, K. D., 7, 8, 79, 81, 82, 84, 92, 

94, 95, 96, 97, 98, 99, 142, 143, 144, 

146, 172, 175 
Rogosina, M., 44 
Rohler, E., 112 
Rokohl, R., 178, 183 
Ronsch, G., 10 
Rosenfeld, A. H., 1 
Roth, L. M., 104, 105, 119, 120, 157, 

158, 159, 160 
Roys, C., 123 
Ruck, P., 168, 169, 170, 171, 174, 175, 

181, 182, 183, 184, 207, 208, 209, 

210 
Ruderman, M. A., 1 

Salmi, H., 157 

Salzle, K., 205 

Sanchez, D., 165, 166, 173 

Sander, W., 178, 179, 180 

Satija, R. C, 207 

Sato, M., 32, 33 

Schaller, A., 154 

Schaller, P., 68, 78, 94, 99 

Schanz, M., 121 

Schenk, O., 18, 113, 114, 118 

Schlegtendal, A., 178 

Schlieper, C, 247 

Schmidt, A., 138 

Schneider, D., 60, 61, 64, 65, 113, 123, 

124, 125 
Schneider, G., 68, 178, 188, 189. 190 
Schneider, W., 106, 107, 108, 109, 110, 

111 
Schon, A., 52, 54, 56, 106 



260 



THE PHYSIOLOGY 



Schone, H., 69, 178, 183 

Schultze, M., 163 

Schulz, E., 202 

Schutz, H. G., 130 

Schwabe, J., 19, 54, 57, 79, 80, 85, 86, 

106 
Schwarz, E., 94 
Schwarz, R., 117, 118, 123 
Siebold, T., 52, 78 
Sihler, H., 24, 40, 100 
Skogland, C. R., 29 
Slifer, E. H., 17, 20, 21, 22, 24, 40, 45, 

113, 114, 115, 160, 164 
Smith, F. E., 191, 193, 195, 196 
Smith, M. H., 128 
Smyth, T., 123 
Snodgrass, R. E., 8, 10, 13, 14, 15, 18, 

22, 24, 28, 40, 52, 54, 59, 114, 163, 

165 
Soraci, F. A., 178, 189 
Sotavalta, O., 66 
Speyer, E. R., 121 
Spoor, A., 195 
Srisukh, S., 167 
Stamm, D., 124 
Stanley, W. M., 131 
Steiner, G., 159 
Stephens, G. C, 191, 193 
Stobbe, R., 94 
Stocker, M., 68, 206 
Stockhammer, K., 190, 193, 194, 195 
Stoecker, M., 170, 205 
Studnitz, G., 70 
Stumpf, H., 178, 181, 182, 187, 188, 

190, 193, 194 
Sturckow, B., 116, 144, 145 
Suga, N., 92 
Sullivan, C. R., 213 
Swinton, A., 78 
Syrjamaki, J., 157, 158, 159, 160, 161 

Taguti, R., 104 

Takeda, K., 114, 142, 144, 145, 147, 

148, 151, 159, 160 
Tateda, H., 148 

Taylor, F. H., 122, 123, 124, 136 
Taylor, I. R., 169, 172 
Taylor, N. W., 137 
Thompson, D. W., 6 
Thomson, R. C. M., 157 
Thornthwaite, C. W., 157, 158 
Thorpe, W. H., 70, 71, 72, 73, 74, 

138 
Timm, C, 94 
Tischner, H., 250 



OF INSECT SENSES 

Tonner, F., 69 

Treat, A. E., 8, 79, 81, 82, 84, 92, 94, 

95, 96, 97, 98, 99 
Turano, A., 163 
Turner, C. H., 94 

Uchiyama, H., 61 
Urvoy, J., 59 

Verlaine, L., 127, 131 

Viallanes, H., 173, 174 

Vogel, B., 138 

Vogel, R., 8, 10, 19, 24, 40, 52, 54, 66, 

78,79,83,84,95, 113, 114, 118 
Vowles, D. M., 75, 76, 190 
De Vries, H., 190, 191, 193, 194, 195, 

200, 201, 204 

Wagner, H. G., 169, 176 

Wagner- Jauregg, T., 117 

Wald, G., 167, 189, 202 

Walther, J. B., 169, 181, 182, 183, 184, 

187, 189, 190 
Wardle, R. A., 7 
Warnke, G., 113, 117, 118, 121 
Waterman, T. H., 190, 191, 196 
Webb, C. S., 94 
Wefelscheid, H., 78 
Weis, I., 127, 138 
Weis-Fogh, T., 62, 63, 64 
Weiss, H. B., 178, 180, 189 
Wellington, W. G., 157, 158, 160, 210, 

213 
Wendler, L., 176, 193, 194, 201 
Wever, E. G., 89, 90 
White, F. B., 94 
Wiersma, C. A. G., 253 
Wieting, J. O. G., 117, 118 
Wigglesworth, V. B., 8, 10, 11, 12, 

14, 24, 28, 64, 113, 158, 159, 160, 

197 
Willis, E. R., 119, 120, 157, 158, 159, 

160 
Wilson, D. M., 62, 63, 66 
Wilson, V. J., 243 
Wirth, W., 117, 118 
Wolbarsht, M. L., 28, 29, 30, 31, 32, 33, 

34, 35, 66, 116, 143, 144, 146, 147, 

148, 149 
Wolf, E., 174, 189, 202, 204, 205 
Wolff, B., 70, 71 
Wolken, J. J., 163, 167, 178, 179, 

180 
Wolsky, A., 210 



AUTHOR INDEX 261 

Wulff, V. J., 168, 169, 172, 175, 176, Zdcwilichowski, J., 53, 54, 66, 67 

177' 181 184 Zawarzin, A., 14, 16, 44, 165 

Zerrahn, B., 204, 206 

Yagi N 104 Zerrahn-Wolf, G., 174, 189, 204, 205, 
Yamkshita, S., 113, 123, 125, 147, 148 206 

Yost, M. T., 118, 122, 123, 124 Zeutzschel, B.. 222 



Subject Index 



Acceptance thresholds, 137-41 
Acids, stimulation by, 126, 130-1 
Aciliiis sulcatus, 69 
Acronycta, 98 
Action potential, 4 
Adaptation, 36, 39, 44, 142, 186 

in mechanoreceptors, 32 
Aedes, 64, 65, 157 

aegypti, 104, 105, 158, 159 

gracilis, 158 
Aeschna, 52, 165, 169, 170, 207 

cyanea, 173 

juncea, 45, 49 
Agriotes, 158, 159 

line at us y 158 

osbcurus, 158 
Alcohols, stimulation by, 118, 121, 

122, 131-6 
Alternation, 102 
Amblycorypha oblongifolia, 89 
Anax, 68 

Junius, 163, 164, 207 
Anopheles quadrimaculatus, 104 
Ant, (see Formica, Myrmica, Lasius, 

Camponotus) 
Antenna, 8 
Antenna, in aquatic insects, 69, 74 

in gravity response, 75, 76 

Johnston's organ, 59-62 

mechanoreceptors on, 34, 35 

olfactory receptors, 113, 125 

role in flight, 64, 65 
Antheraea pernyi, 46, 47, 48, 49 
Aphelocheirus, 56, 70, 72, 73 
Apis, 64, 109, 138, 163, 170, 178, 179, 
180, 183, 206, 209 

mellifera, 163, 170, 174, 207 

mellifica, 159 
Apposition eye, 197-200 
Arctia caj'a, 95 
Arphia sulphur ea, 90 
Axons, fusion of, 12 

Bat detection, 94, 99 
Belostoma, 74 
Benacus griseus, 63 



Bidessus, 191 
Blaberus, 45 

craniifer, 183, 207 
Blatella germanica, 158, 159 
Blatta orientalis, 16, 157, 159 
Blethisa multipunctata, 158, 159 
Blidius bicornis, 75 
Blowfly (see Phormia, Sarcophaga, 

Lucilia) 
Bombus, 106, 170 

pennsylvanicus, 168 
Bombyx, 125 

mori, 116, 123, 124, 125 

Calliphora, 36, 63, 64, 65, 67, 68, 105, 
109, 116, 138, 139, 147, 166, 170, 
171, 172, 173, 174, 176, 181, 182, 
187, 188, 189, 193, 194, 198, 204, 
205, 206 
erythrocephala, 16, 60, 127, 181 
vomit oria, 127, 139, 144, 181 

Campaniform sensilla, 11, 13, 16, 17, 
18, 19, 38, 40^4, 66-68, 78 

Camponotus, 109 

Carabus, 106 

Carausius morosus, 63 

Cercus, 16 
sound receptors, 101, 102 
sound thresholds, 101 

Cercyonis pegala, 95 

Chemoreception, 112-55 

Chemoreceptors, specificity of, 112, 
139-45 

Chordotonal organs, 19, 20, 21, 22, 
105-11 

Chordotonal sensilla, 52-62, 67, 78, 
84 

Choristoneura fumiferana, 158 

Chorthippus, 92 

Chortophaga viridisfasciata, 168, 169 

Cicada (see Tibicina, Cicadetta) 

Cicadetta coriaria, 19, 84 

Cicindela, 213 

Cochliomyia americana, 127 

Cockroach (see Periplaneta, Blaberus, 
Blatta, Blatella) 



262 



SUBJECT INDEX 



263 



Coleoptera (see Leptinotarsa, Hydrous, 
DytiscuSy Afelolontha, Geotrupes, 
Tribolium, Tenebrio) 
Colour matching, 184 
Colour vision, 177-90, 213 
Compound eye, 8 

structure, 162-7 
Compression receptors, 40-44 
Contact chemoreception, discrimina- 
tion, 129-30 

electrical events, 145-9 

modalities, 153-5 

sensitivity, 126-9 

thresholds, 126-39 
Contact chemoreceptors, 115-16 

categories of, 1 39-45 
Corethra plumicornis, 58 
Corixa, 69, 78, 99 
Culex, 104, 158 

fatigans, 157, 158 

pipiens, 104 

pipiens pollens, 1 04 
Ciilicidae, 105 

Danaus, 126 
Daphnia, 191, 192 
Decticus, 19, 89, 108 
Deilephila euphorbiae, 165 
Dendrites, 24, 25, 82, 86, 101 , 1 1 3, 1 1 5, 

163 
Dioptric apparatus, 196-201, 212 
Diptera (see Mucina, Eristalis, Droso- 

phila, Stomoxys, Phormia, Calli- 

phora, Musca, Tabanus) 
Dissosteira, 163, 164, 172 

Carolina, 169 
Dixippiis, 169, 170, 174, 206 
Dragonfly (see also Aeschna, Anax, 

Sympetrum, Libellula, Pachydi- 

plax), 44, 45, 51, 52, 68, 173, 174 
Droposphila, 64, 113, 157, 158, 160, 

163, 165, 178, 179, 180, 183, 187, 

189, 193, 202 
melanogaster, 159, 160, 163, 181 
Dytisciis, 57, 69, 165, 169, 172, 175, 

183, 184 
asciventris, 169, 181 
marginal is, 69, 154 

Electrolytes, stimulation by, 130-1 
Electroretinogram, 168-77, 193, 194 

of ocelli, 208 
Empis, 53 
Environment, marine, 6 

terrestrial, 1, 6 



Epargyreus, 163 
Equilibration, 102 
Erebus, 165 

odor a, 163, 164 
Eristalis, 109, 170, 174 

Female anal plate, mechanoreceptors 

on, 31, 32 
Flicker, 171-3, 187, 205, 206, 209, 

213 
Flying, role of mechanoreception in, 

63-68 
Form perception, 196-207, 211 
Formica rufa, 88 
sanguinea, 56 
Frequency doubling, 102 
Galleria, 172 

mellonella, 169 
Ganglion cells, peripheral, 10 
Generator potential, 4, 29, 30, 146, 

147, 209 
Geotrupes, 107, 109, 118 
sylvaticus, 113 
vernalis, 113 
Giant fibres, 7 
Glossina morsitans, 159, 160 
Graphiphora, 98 

Grasshopper (see also Gryllus, Locusta, 
Melanoplus, Schistocerca, Lie- 
gryllus, Thamnotrizon), 17, 20-22, 
30, 34, 35, 46, 78, 79, 80, 82, 84, 
89-94, 114, 115 
Gravitational force, 1, 26 
Gravity, responses to, 75-76 
Gryllus, 19, 100, 101 
assimilis, 89 
bimaculatus, 159 
domesticus, 16, 159 
Gyrinus, 74 
marinus, 74 
natator, 74 

Habrobracon, 118 
Hair plates, 36-39, 64, 75, 76 
Hairs, as sound receptors, 100-3 
Haltere, 16 
function, 68 
sensilla, 54, 67-68 
Hemiptera (see Rhodnius, Aphelo- 

cheirus, Lethocerus, Notonecta, 

Corixa, Nepa) 
Honeybee (see also Apis), 18, 45, 64, 

75, 76, 109, 114, 118, 120, 125, 

129, 159, 163, 167, 170, 179, 180, 

183, 186, 193,203,204 



264 



THE PHYSIOLOGY OF INSECT SENSES 



Humidity, 156-61 

definition of, 156-7 
Hydrous, 118, 127 

piceuSy 154, 155 

triangularis, 169 
Hygroreceptors, 157-61 

Isiaisabella, 210,211,212 

Johnston's organ, 55, 59-62, 64, 78 

of Culicidae, 103-5 

in swimming, 69, 74 
Joint receptors, 36-39 

Laccophilus, 127, 130, 155 
Lasius niger, 138 
Latheticus oryzae, 120 
Lepidoptera (see also Vanessa, Pro- 
denia, Bombyx, Pieris, Antheraea, 
Lucania, Danaus, Isia, Galleria), 
78, 79, 81, 82, 84, 94-99 

stretch receptors, 46, 47 

tactile hair, 23 

tympanic organ, 56 
Leptinotarsa, 145 

decemlineata, 139 
Lethocerus, 74 

americanus, 63 
Libellula luctuosa, 207 

vibrans, 207 
Limulus, 148, 171, 173, 176 
Liogryllus, 107 

campestris, 89 
Locusta, 57, 61, 89, 90, 91, 93, 94, 105, 
204 

migratoria migratorioides, 85, 90, 
157, 158, 207 
Lucania, 98 
Lucilia, 170, 174 

caeser, 139, 148, 181 

cuprina, 159 

sericata, 159 

Machilis, 106, 162 

Macropanesthia rhinocerus, 7 

Macrotorixa, 68 

Malacosoma, 118 

Male clasper, mechano receptors on, 

29, 33 
Mantis, 36-39, 175 
Mantis religiosa, 175 
Mechanoreception, 26-76 
Melanoplus, 34, 35, 169, 172 

bivittatus, 158, 159, 207 

different ialis, 113, 168, 181 



Melanoplus, femur-rubrum, 168 
Melolontha, 14, 15, 107, 109 

vulgaris, 16 
Membrane potential, 4 
Modalities, contact chemoreception, 
153-5 
odour, 125-6 
Monohammus confusor, 55 
Mosquitoes (see also Aedes, Culex, 
Anopheles), Johnston's organ, 59, 
60, 103, 105 
Motor system, 7, 8 
Musca, 163, 164, 179, 180 

domestica, 116, 118, 127, 159, 160, 
163, 164, 168, 169, 181 
Muscina, 64, 65 
stabulans, 64 
Muscle receptor, crustacean, 32, 44, 

49 
Muscle spindle, frog, 32, 44 
My r mica, 88 
rubida, 138 
rubra, 138 
Mysidium, 191 

Naucoris, 68, 69 
Necrophorus, 118 

tomentosus, 113 

vespilloides, 113 
Neodiprion, 158 

americanus banksianae, 158 

lecontei, 158 
Nepa, 70, 71, 72 
Nervous system, economy in, 7-9 

motor, 7 
Neurilemma, 11, 14 
Neuron, Type T, 14, 16, 17 

Type II, 14, 15, 16 
Noctua c-nigrum, 96 
Non-electrolytes, stimulation by 131-6 
Notonecta, 68, 69, 183, 190 

Ocelli, 207-10 
Odour, 116-26 

qualities, 125-6 
Olfaction, 116-26 

acuity, 116-21 

adequate stimuli, 121-2 

mechanism, 122-5 

thresholds, 117, 118, 119 
Olfactory pit, 119 
Olfactory receptors, 113-15 
Ommatidium, 13, 162-5 

appositional, 13, 163 

superpositional, 13 



SUBJECT INDEX 



265 



Oncopeltus fascia t us, 1 58 

Oodes gracilis, 1 59 

Optic lobe, 165, 166, 173, 175 

Optomotor responses, 178, 205 

Organic electrolytes, stimulation by, 

136-7 
Orientation, primary, 26 
Oryctes, 15 

Pachydiplax, 209 

longipemiis, 170, 174, 207 
Pacinian corpuscle, 32 
Panorpa communis, 53 
Pediculiis, 19 

humamts corporis, 158, 159 
Periplaneta, 37, 38, 39, 43, 44, 63, 64, 
78, 107, 182, 206, 209, 210 

americana, 7, 16, 45, 62, 100, 130, 
169, 182, 207 
Phalera biicephala, 95 
Phormia, 25, 29, 31, 32, 33, 63, 66, 116, 
122, 123, 127, 129, 130, 131, 132, 
135, 136, 138, 139, 143, 149, 153, 
204, 209 

regina, 113, 115, 118, 119, 121, 127, 
139, 140, 159, 170, 174, 207 
Photinus pyralis, 178 
Photoreception, 162-213 
Pier is, 127, 130 

brassicae, 181 

rapae, 23, 118 
Plea, 69 

Polarized light, 190-6, 213 
Pollenia rudis, 181 
Position receptors, 36-39 
Posture, 26 

Pressure sense, 70, 71-74 
Prey capture, 36-39 
Primary neurons, 9, 10, 14 
Prodenia eridania, 95 
Proprioceptors, 17, 35-62 
Proprioceptors, definition, 35 
Psorophora confinnis, 104 
Pterophylla camellifolia, 89 
Pterostrichus, 106 
Ptinus tectus, 157, 158, 159 
Purkinje shift, 189 
Pyrameis, 107, 126 

atalanta, 138 

Ranatra, 74 

Receptor, characteristics, 3 

primary cells, 9, 14 
Receptor potential, 4, 28, 29, 30, 31, 
146, 147 



Rejection thresholds, electrolytes, 
130-1 

non-electrolytes, 131-6 

organic electrolytes, 136-7 
Repellent, 117 
Resolving power, 200 
Resolving power, temporal, 206 
Respiratory behaviour, 56, 57, 58 
Responsiveness, 3 
Retina, function of, 167 

pigment, 167 

structure of, 163-5 
Retinal cells, independence of, 201, 202 
Rhabdom, 163, 164 
Rhagonycha, 106 
Rhodnius, 8, 10, 11, 12 

prolixus, 10 
Rhyzopertha dominica, 120 
Romalea microptera, 113, 175 

Salt, stimulation by, 126, 130-1, 137 
Salt receptor, 151-3 
Samia cecropia, 130, 169, 181 
Sarcophaga, 28, 31, 163, 170, 174, 183 

bullata, 163 
Schistocerca, 64, 163, 164 

gregaria, 62, 158, 159 
Scolopoid body, 82, 86 
Scolopoid sensillum, 19, 21, 22 
Scolopoid sheath, 24, 28, 55, 59, 114 
Sense cells, categories, 14 

development of, 9, 10, 11 

number, 8, 12 
Sense organ, definition, 2 
Sensillum, categories, 18 

definition, 18 

structure of, 22, 24, 25 
Sensillum basiconicum, 20, 21, 22, 113, 

114, 125 
Sensillum coeloconicum, 22, 113 
Sensillum placodeum, 18, 19, 113 
Sensillum scolopophorum, 19, 20, 21, 

22 
Sensillum trichodeum, 23, 27-35, 

36-39,66,78, 105, 115 
Sensillum trichodeum, as sound re- 
ceptor, 100-3 
Sensitivity, 3 
Sex attractant, 123^ 
Silpha americana, 113 

noveboracensis, 113 
Sitophilus, 158, 160 
Skeleton, 6 
Sound, definition, 77 

frequency discrimination, 92 



266 



THE PHYSIOLOGY OF INSECT SENSES 



Sound, localization, 93-94, 98 

production, 77, 91, 93 

reception, 65, 77-1 1 1 

thresholds, 90, 101 
Spectral sensitivity, 180-4, 186, 188 
Spectral sensitivity, of ocelli, 209 
Statocysts, 69, 70, 74 
Stemmata, 69, 210-13 
Stiles-Crawford effect, 201 
Stomoxys calcitrans, 116 
Stretch receptors, 8, 44-51, 78 
Stridulation, 77, 91, 93 
Stroboscopic motion, 206 
Subepidermal plexus, 14, 15, 16 
Subgenual organs, 55, 78, 80, 83, 90, 

106-11 
Sugar receptor, 149-51 
Sugars, stimulation by, 126, 128, 129, 

137^1 
Superposition eye, 197-200 
Swimming, role of mechanoreception 

in, 68-74 
Sympetrum, 207 

nbicimdulum, 207 

Tabanus, 126, 127 

sulcifrons, 130 
Tachycines, 169, 171, 206 
Tactile hair, 11, 12, 23 

electrical events, 28-35 
Tactile sense, 27-35 
Tarsal reflex, 63 
Taste, 126-55 
Temperature, effect on chemorecep- 

tion, 146 
Temporal resolution, 206 
Tenebrio, 158, 160 

molitor, 119, 157, 158, 159 



Thamnotrizon aptenis, 89 
Tibicina haematodes, 83 
Tipula paludosa, 54 
Tormogen, 9,11 
Tribolium, 119, 160 

castaneum, 120, 157, 158, 159 

confusuiriy 120, 158, 159 
Trichogen, 9, 1 1 
Trimerotropis, 111 

citrina, 169, 172 

maritima, 169, 172 
Tropidacris latreillei, 7 
Tympanic organ, 56, 78-99 
Tympanic organs. Cicada, 83-84 

Hemiptera, 99 

Lepidoptera, 94-99 

Orthoptera, 89-94 
Type II receptors, 44-51 

Vanessa, 144 

atalanta, 145, 168 

indica, 138, 145, 148, 151 

urticae, 23 
Vespa, 63, 106, 170 

saxonica, 76 
Vibration, thresholds, 107-10 
Vibration sense, 105-11 
Vision, 162-213 
Visual acuity, 198, 202^ 

Walking, role of mechanoreceptors in, 
62-63 

Water receptor, 1 53 

Wing, campaniform sensilla, 53, 66 
chordotonal sensilla, 53, 66 
mechanoreceptors on, 28, 31, 34 
sensilla trichodea, 66 



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