THE SENSE OF OLFACTION IN LOWER ANIMALS
Olfaction is generally felt to be the lowest, the most animal, of the
senses, so much so that in polite society it is scarcely good manners to
mention smells, and I am well aware of the risks I run in writing a book
on the subject. And yet this feeling is by no means false modesty,
because it is, first and foremost, to the animal in us that smell makes
its appeal. None of the other senses brings so frankly to notice our
kinship with the brute.
Olfaction is, indeed, one of the primitive senses of animal life. And in
man, as it happens, while vision has constructed for itself a highly
complicated camera-like end-organ, and hearing has produced an apparatus
even more elaborate, the olfactory organ, on the other hand, remains
primitive, its essential structure having undergone no apparent
evolutionary change from the simplest and earliest type.
This, perhaps, is scarcely the proper way of expressing the situation.
Evolutionary change has, as a matter of fact, occurred, but it reaches
its highest development not in man, but in terrestrial mammals otherwise
inferior to him—in the dog, for example.
For once, man does not occupy the apex of the evolutionary pyramid.
Olfactory development, high or low, is linked up with the natural habits
of the different species. Thus, mammals which go about on all fours,
whose visual outlook is restricted and whose muzzle is near the ground,
are the most highly gifted; those, again, like the seals, porpoises,
whales, and walruses, which have reverted from a terrestrial to an
aqueous environment, where smell is of less value to them, show poorly
developed olfactory organs; and finally, the apes and man, living
habitually above the ground, the former in trees, the latter on his hind
legs, and relying chiefly upon vision, also show a decline from the high
point reached by four-footed mammalians.
The animals of this kingdom are thus divided into macrosmatic and
microsmatic groups. To the latter man belongs, but we must add that his
olfactory sense has not yet degenerated so completely as that of certain
other species (porpoises, etc.).
It is, of course, common knowledge that in most of the animals we are
closely acquainted with the sense of smell is infinitely more delicate
and acute than ours, so much so, indeed, that the imagination can on
occasion scarcely conceive theirs to be of the same nature. As a matter
of fact, many authorities incline to the belief that not only mammalians
and other vertebrates, but also insects, must be guided to their food
and to their love-mates by some kind of perception, by some mysterious
sense, of which we are totally devoid.
As this is a division of our subject of the highest interest, and one to
which we shall have occasion to recur at intervals throughout this
treatise, we shall discuss the matter as fully as the space at our
disposal will permit.
The unit of the olfactory sense-organ is the olfactory cell. This, which
does not vary in structure from one end of the animal kingdom to the
other, is microscopically seen to consist of an elongated body like a
tiny rod, bearing on its free end a small enlargement or prominence, on
the surface of which is a cluster of extremely fine protoplasmic
filaments, the olfactory hairs. These hairs project into and are
immersed in a thin layer of mucus, at all events in air-breathing
animals, an environment which is necessary for their functional
activity, because, if the nose becomes desiccated, as it does in some
diseases, the sense of smell is lost (anosmia). The hairs are, without
doubt, the true receptive elements of the olfactory cells. It is these
which come into contact with and are stimulated by odours—whatever the
nature of Odour may be.
The deep (proximal) end of the rod-like olfactory cell tapers into a
nerve-fibre, which passes by way of the olfactory nerve to a special
lobe of the brain—the olfactory lobe—in the vertebrates, or to a
nerve-ganglion in the invertebrates.
Olfactory cells in man are only found in the upper—the olfactory—region
of the nose, spread over a surface of about one square inch, the
olfactory area—part lying on the outer (lateral) wall of each nasal
passage and part on the septum, or partition between the nasal passages.
In macrosmatic animals the olfactory area is relatively greater than in
man, but there is apparently no other difference between them.
Olfactory cells are held in place by ordinary epithelial cells—the
sustentacular cells—which contain pigment. Olfactory cells are found in
animals as low in the scale as the sea-anemone. They occur in the
integument of the animal, and their structure is the same as in man, the
only difference evolution has brought about being that in the higher
animals they are protected by lodgment in a _cul-de-sac_. Their function
in the sea-anemone is probably limited to the sensing of food, but we do
not yet know much about this particular organism.
It is otherwise with the olfaction of insects. Here the work of
painstaking observers like Lubbock, Fabre, and Forel, has supplied us
with a mass of information of the utmost interest, which we shall now
proceed to discuss in some detail, commencing with the work of that
remarkable French naturalist, Fabre, whose interest in the subject was
aroused by an accident—the accident of which the genius of observation
knows so well how to take advantage.
Having by chance a living female Great Peacock moth captive in his
house, Fabre was surprised one night by the advent of some forty others
of the same species—males in search of a mate. At once the question
arose in his mind: How was it that they had been attracted?
Sight could not have guided them, because, apart from the comparative
rarity of this moth in that particular district, the night of their
arrival was dark and stormy, his house was screened by trees and shrubs,
and the female was ensconced under a gauze cover. He observed, besides,
that the males did not make straight for their objective, as is
characteristic of movement when directed by sight. They blundered and
went astray, some of them wandering into rooms other than that in which
the female was lying. They behaved, that is to say, as we ourselves do
when we are trying to locate the source of a sound or a smell. But sound
was ruled out by the fact that they must have been summoned from
distances of a mile or a mile and a half.
Olfaction remains, and with this in his mind Fabre undertook several
experiments, some of which, as it happens, support, while others oppose,
the theory of an olfactory cause.
When the female was sequestered under the gauze cover, and in drawers or
in boxes with loosely-fitting lids, the males always succeeded in
discovering her. But when she was placed under a glass cover, or in a
sealed receptacle, no male at all appeared. Further, Fabre found that
cotton-wool stuffed into the openings and cracks of her receptacle was
also sufficient to prevent the summons reaching the males. This last
observation should be borne in mind in view of further discussion later
on regarding the nature of the lure.
Similar observations and experiments were made on the Lesser Peacock,
with very much the same kind of result. But in dealing with this moth
Fabre made an observation which, if it was accurate, tells against the
theory of olfaction, or at least against such olfaction as we ourselves
experience. At the time when he was carrying out his experiments the
mistral was blowing hard from the north, and as nevertheless males
arrived, they must all have come with the wind; no moth ever hatched
could beat up against the mistral. But then, if the guide is an odour,
the wind, blowing it to the south, would have prevented it ever reaching
the males! Here, then, we have a circumstance which leaves us groping
for an explanation.
In watching the behaviour of the third moth on his list, the Banded
Monk, on the other hand, Fabre discerned a circumstance very strongly
suggestive of the operation of an odorous lure. He found that, if the
female was left for a time in contact with some absorbent material and
was afterwards shifted, the males were attracted, not to her new
situation, but to the place where she had originally been lying.
Subsequent experiment showed that a period of about half an hour was
necessary to lead to the impregnation of the neighbourhood with the
effluvium she elaborated.
The obvious test was employed of trying to drown the supposed odour of
the female by filling the room she was in with powerful aromas, like
naphthaline, paraffin, the alkaline sulphides, and the like. But in
spite of the presence of these stenches, in our experience overwhelming
to fainter exhalations, the males still continued to arrive in droves.
This result led Fabre to doubt whether it could really have been an
odour that attracted them. But surely this negative conclusion ignores
the possibility of the moths being anosmic to these gross scents while
highly specialised for one particular olfactory stimulus to which, as a
matter of fact, we ourselves are wholly insensitive.
Apart from this particular problem, however, to which we return below,
biologists agree that insects undoubtedly possess an olfactory sense
capable of appreciating the same kind of odours as ours does. Lubbock,
for example, demonstrated that ants give signs of perceiving the
presence of musk and other perfumes. There is no doubt, indeed, that the
olfactory sense plays a great, it may be a preponderating part in their
life-activity.
The olfactory organ of insects is situated at the bottom of little
crypts in the antennæ and in the palpi of the mouth apparatus, more
particularly in the antennæ. And those insects, like bees, wasps,
butterflies and moths, that frequent flowers, are attracted to them by
their perfumes as well as by their colours. It has been found, for
example, that covering up flowers from view does not put a stop to the
visits of insects. Some naturalists go so far, indeed, as to say that
odour is their principal guide. At all events, the sarcophagic and
stercophagic insects are attracted to their food chiefly, if not
entirely, by odour. Fabre has recorded how such insects are lured to
their death by certain insectivorous plants which exhale a smell like
that of putrid beef.
In this connection I may interpolate here an experience which shows that
this class of insect may be attracted solely by odour. Incidentally, it
also manifests how the olfactory sense of insects can be utilised in the
matter of hygiene.
A clever plumber of my acquaintance was once called to a large
drapery establishment in the West End of London, because the
dressmakers at work in one of the rooms were making complaints of an
evil smell that haunted the place. So much had they been troubled,
indeed, that several of them had been made ill by it. On examining
the workroom my friend found everything apparently faultless. It was
a large, well-lighted and airy apartment, and he himself was unable
to detect anything amiss in the atmosphere. Plans were consulted,
but no evidence could be found of any possible source of unpleasant
odour. His opinion therefore was, that the ladies were—ladies, that
is to say, fanciful, and the matter was dropped. But the ladies were
not consenting parties to this opinion, and the complaints
continued. More of the assistants fell ill as a consequence, they
said, of the smell, so that he was again sent for. On this occasion,
it being the height of summer, he called, on his way to the draper’s
emporium, at a butcher’s shop, and much to that man’s surprise,
asked permission to capture a few of his bluebottle flies. These he
took with him to the draper’s, and, the suspected room having been
emptied of furniture and occupants, he closed all the windows and
doors and released his flies. After waiting patiently for some time,
he observed that these amateur detectives of his had all made for
one part of the room, where they were settling on the wall. Here he
had an opening made, and found hidden behind the plaster an open
drain-pipe, old and foul, which had formerly been connected with a
lavatory, and had been enclosed and forgotten during some
alterations made on the building several years before.
The olfactory sense of insects has been credited with perhaps even more
wonderful powers than those we have just been writing about. For
instance, both Lubbock and Forel have shown that the extraordinary
aptitude ants possess for finding their way back to their nest after
their peregrinations in the mazy labyrinth of their world depends upon
the sense of smell. On their return to the nest they follow the scent
left by their own footsteps.
This “homing” instinct, or “orientation,” which is found in many species
of insects and animals, has long been a matter of interest to scientific
naturalists. The subject is, however, much too large for us to enter
fully into on the present occasion.
Winged insects like bees and wasps manifest also the homing instinct. In
their case the return to the nest or hive is effected probably
altogether under the guidance of vision. This is what we should expect,
as elevation in the air secures for these creatures a wide and unimpeded
view of their world. Circumstances are obviously different in the case
of ants and other creeping things, whose immediate outlook, like that of
four-footed mammals, is circumscribed to an area of but a few inches or
feet at the most.
Investigating the orientation of ants, Forel found, first of all, that
while the covering of their eyes with an opaque varnish “embarrassed”
them to some extent, they went hopelessly astray when their antennæ were
removed.
He also repeated Lubbock’s well-known experiments of supplying the ants
with bridges over obstacles in the neighbourhood of their nests, noting
their behaviour when the bridges were changed, removed, or reversed,
with the result that he came to credit the olfactory system of ants with
much greater powers than the more cautious Lubbock would have believed.
These insects, says Forel, exploring with their mobile antennæ the
fields of odour they encounter, form in their memory a kind of “chemical
topography.”
Thus when an ant sets out from her nest she distinguishes the various
odours and varying strengths of odours she comes upon, noting and
memorising them as in two main fields, one on her left side, the other
on her right. In order to find her way back again all she has to do is
to unwind, so to speak, the roll in her memory, transposing right and
left, and this successfully accomplished will bring her back to the
point she started from.
If, he concludes, we ourselves were endowed with such a perfect
olfactory mechanism situated in long, flexible whip-lashes, which we
could move and tap with each step, the world for us would be
transformed. Odour would become a sense of forms. Thus the orientation
of ants can be explained without assuming the existence of an unknown
sense. (It has recently been suggested, by the way, that bats owe the
exquisite power they manifest of steering their flight among obstacles
to the use of their squeaks, the echoes from which enable them to form
“sound-pictures” of their environment. In the same way a blind man in
the street tapping the pavement with his stick forms a more or less
well-defined sound-picture of the walls, doorways, and alleys about
him.)
In the immediately foregoing paragraphs we have been dealing with the
ability of insects to smell the smells that we smell. But Fabre’s
experiments have familiarised us also with the notion that there are
insects which can smell smells we cannot smell.
We shall see in the following section that the same may also be true of
some of the higher animals.
In fish olfaction is, unlike that of air-breathing animals, effected by
odorous material in solution. Whether or not their olfactory sense is as
acute it is impossible in the present state of our knowledge to say.
Anatomically the end-organ of fishes is simpler, but there are some
species, the dog-fishes for example, which possess a large olfactory
lobe in the brain; and this certainly suggests that they, at all events,
are gifted with an olfactory sense of relatively high development.
Experiment on fish is difficult, nevertheless it has been definitely
proved that they do smell, and it seems probable that the sense is used
by them for food-perception. Moreover, that it may be highly sensitive
seems likely from the fact that sharks (which belong to the same order
as dog-fish) can be attracted from great distances to putrid meat thrown
into the water as bait, the high dilution of which resembles the
behaviour of odour in an air medium.
The belief that life in water, however, is less favourable than life on
land to the fullest development of the sense is supported by the fact we
have already mentioned that mammals living in water are extremely
microsmatic.
In the macrosmatic terrestrial animals not only is the olfactory sense
relatively highly organised, but it is absolutely the predominant sense.
Vision is subsidiary to it. In their brains the olfactory region
constitutes by far the largest component. (The same, by the way, is true
of the Reptilia.)
In other words, it is upon the olfactory sense that these animals
chiefly depend for their knowledge of the world. By it they are directed
to their food, warned of their enemies, and attracted to their mates.
Their universe is a universe of odour.
In order to become more intimate with the details of this part of our
subject, we shall pass in review some of the olfactory habits and
characteristics of the macrosmatic animal most familiar to us, namely,
the dog.
There can be no doubt of the all-important part that smell plays in the
life of the dog. Every one is familiar with it, and yet we do not often
stop to think what its meaning is for the canine brain and
understanding. One of the mysteries that must, one would suppose, for
ever remain hidden from us, is what aspect the world we both share in
company bears to this our closest animal friend. Who can tell what is
passing through his mind as he sniffs at us? He can recognise his master
by sight, no doubt, yet, as we know, he is never perfectly satisfied
until he has taken stock also of the scent, the more precisely to do so
bringing his snout into actual contact with the person he is examining.
It is as if his eyes might deceive him, but never his nose.
The greyhound courses by sight, but all other dogs hunt by scent, and
the speed and certainty of foxhounds in full cry bear a new significance
when we recollect that it is scent that is directing them. Could vision
be any more swift and sure?
We may heartily wish, as a child once remarked to a friend of mine, that
Rover had a prettier way of saying “How d’ye do?” to his canine friends.
But that and other even more objectionable habits do not prevent his
_entrée_ into the most exclusive circles of human society. He is taken
at his own valuation, and that, to be sure, is considerable. But the
minute, the meticulous, olfactory scrutiny he makes of other dogs is but
one more example of the predominance of this sense in his brain. (See
also later.)
When you take him for a walk also, how busy his nose makes him!
Burrowing here and there among the grass and undergrowth, picking up an
interesting trail that leads him a little way, until it crosses another,
fresher, perhaps, or more interesting, that has to be taken up—here a
cat’s, there a rat’s, further on a rabbit’s, and then, with short
squeals, scrapings in the ground, and buryings of his muzzle, a
weasel’s!—the whole intermixed and intermingled with whiffs of something
like old decayed bones, or of another and an unfriendly dog, or of some
ardent lady-love who has passed this way but shortly since!—is not this
a richer, a fuller, a more attractive, world than ours, with its fickle
sunlight, its pallid greys, its mournful purples, its unattainable
horizon-blue? For our life is primarily one of vision.
I am sure his dreams, also, are compounded of the gorgeous odours of
some other world, such odours as even our woods in autumn know nothing
of.
But we must return again to science and Fabre. This time we shall
accompany him on an excursion with the wonderful dog who is trained to
discover for the _gourmet_ the truffles that are growing deep in the
soil.
Left to his own devices, we learn, the truffle-hunting dog indicates the
position not only of truffles, but also of all manner of hypogean
(underground) fungi, “the large and the small, the fresh and the putrid,
the scented and the unscented, the fragrant and the stinking.” Only, he
never at any time indicates the presence of the ordinary mushroom, not
even while it is still underground, before it sprouts up as the fungus
we know. And yet to our nostrils the mushroom has the same smell as many
of the hypogean fungi he does indicate. Consequently, therefore, the dog
is not guided to the deep fungi by what may be called the general odour
common to all fungi. He must be able, that is to say, to distinguish the
hypogean varieties by some quality which is not odour, or, at least, not
odour as we understand it.
There is, as it happens, something like a truffle-hunter among the
insects also, what is known as the Bolboceros beetle. This little
creature feeds on the _hydnocystis arenaria_, a hypogean fungus. Fabre,
having captured some of these insects, placed them on earth in which he
had buried the fungus at depths of six or seven inches. It was found
that the beetles, without making any trial bores, sank vertical shafts
through the soil direct to their food.
We may insert here also, as bearing upon the problem which is now
emerging into clearness, an observation and a suggestion similar, as we
shall see, to that of Fabre, on the badger by Mr. Douglas Gordon
(_Spectator_, August 6th, 1921):
“The real damage wrought by the badger is microscopic. His diet
mainly consists of roots, green herbs, mice, frogs, and insects.
Like the fox, he has a great partiality for whorts and blackberries
when in season, and he is particularly fond of grubs. For the sake
of these he will dig out every wasp’s nest he can find. A
considerable number of rabbit ‘stops’ also fall to his share, and in
unearthing the latter he practises a somewhat remarkable piece of
woodcraft. The hole which contains the nest may run to the depth of
several feet, and the nest itself be situated ten feet from any
entrance, but this does not trouble the badger. He makes no attempt
to follow the tortuous passage, as a man when digging would be
obliged to do. His unerring nose locates the exact spot where the
young rabbits lie, and from the most convenient point he bores for
them. Should it be a ‘ground-burrow,’ he sinks a vertical shaft. In
the case of a steep bank he drives a horizontal tunnel, and, shallow
or deep, with unvarying accuracy.
“Not long ago I saw a striking case of this on Haldon Hill, near
Exeter. The burrow opened on to a little gully, and ran back some
distance under the heath. At least five paces from the nearest hole
was the badger’s freshly cut shaft, about three feet deep, and
around it were littered the ruins of the nest—the little tale of
bloodstained fur so eloquent of tragedy. There on the earth drawn
from the shaft the raider’s spoor was plain enough, but no imprint
of his pads could I find upon the impressionable mould anywhere near
the holes. This meant that he must have found the nest while
traversing the heather—sensed it beneath him, in fact. And here an
interesting point arises. What sense did he employ? Could he
possibly ‘smell’ the rabbits through three feet of packed mould?
Earth is a potent deodoriser. Do certain animals possess a sixth
sense—a sympathy something akin to that of the divining rod? If so,
this goes farther to explain the much-discussed principle of scent
than anything yet suggested.”
Is this sense, then, as we see it in operation in the badger, in the
truffle-hunting dog, in the Bolboceros beetle, and still more
wonderfully in the Peacock and Banded Monk moths, drawn to their mates
“from the edge of the horizon,” and, it may be, against the wind—is this
sense the same as our own sense of olfaction, only much more acute?
Fabre finds some difficulty in believing that it can really be the same.
“Odour,” he argues, “is molecular diffusion.” But nothing material,
nothing our senses can perceive, is emitted by these moths, and yet they
can summon their mates from relatively enormous distances. However fine
may be the divisibility of matter, Fabre’s mind refuses to entertain the
suggestion that this far-flung summons is addressed to a sense of smell
of the same nature as ours. It would be tantamount, he says, “to
reddening a lake with an atom of carmine, to filling immensity with
nothing.”
It is impossible not to sympathise with this opinion, but caution
compels us to say that for the most striking of these observations, that
of the calling of the males against a high wind, we should like to have
confirmation by some independent observer.
Besides, I think perhaps Fabre would have hesitated to express his
scepticism regarding the power of insect olfaction had he known more of
the marvels of the human sense.
Vanillin, for example, is perceptible by us as a smell when it amounts
to no more than 0·000000005 gram in a litre of air; and we can perceive
mercaptan, a substance with a garlicky odour, in a dilution of
1/460,000,000 of a milligram in fifty cubic centimetres of air
(approximately 0·0000000026 of a grain in a little over three cubic
inches of air!) (See also p. 108.)
What is this but immensity filled with nothing? And yet we, even we,
microsmatic though we are, can perceive that “nothing.”
But we must pick up again the thread of Fabre’s argument. Baffled as he
feels himself to be when he regards olfaction in the light of these
observations of his, he goes on: “For emission substitute undulation,
and the problem of the Great Peacock is explained. Without losing any of
its substance a luminous point shakes the ether with its vibrations and
fills a circle[1] of indefinite width with light....
Footnote 1:
A sphere rather.
“It does not emit molecules; it vibrates; it sets in motion waves
capable of spreading to distances incompatible with a real diffusion of
matter.
“In its entirety smell would thus seem to have two domains: that of
particles dissolved in the air and that of ethereal waves. The first
alone is known to us....
“The second, which is far superior in its range through space, escapes
us altogether, because we lack the necessary sensory equipment. The
Great Peacock and the Banded Monk know it at the time of the nuptial
rejoicings. And many others must share it in various degrees according
to the exigencies of their mode of life.”
In criticism of this conclusion of Fabre, however, we must again draw
attention to the fact that in the case of the Greater Peacock he found
that a plug of cotton-wool was sufficient to prevent the emanation
leaving the immediate neighbourhood of the female, a circumstance
strongly in favour of some material exhalation which was caught and held
by the cotton-wool filter. Again, in the case of the Banded Monk, the
suggestion of odour is unmistakable in the tainting, as it were, of
substances in her vicinity with her emanation. Further, if the guide to
the males were something like a luminous undulation we should expect
that, like the Bolboceros beetle and the badger, there would have been
no blundering and going astray; they would have precipitated themselves
straight on to the female, or as near to her as they could get.
Moreover, although we are ourselves unable to detect any odorous
emanation, may not our inability be due simply to the fact that our
olfactory hairs are not susceptible to this particular stimulus? It may
be of the same nature as odour, and yet we may be unable to perceive it,
just as the moths themselves seemed anosmic to what we would call the
stenches Fabre filled his room with.
These critical questions seem to me to be difficult to answer.
Nevertheless, our imagination is certainly staggered by the fact of a
tiny creature like a moth being able to disseminate in the immensity of
atmospheric space an odour capable of perception at such great distances
as a mile or a mile and a half. Hero, with the Great Peacock’s power,
could have summoned Leander from a hundred miles away.
Apart, however, from such considerations for and against his opinions,
one of the modern theories of odour, and of odour belonging to Fabre’s
first, or material, order, is, as we shall see later on, that even it is
a vibratory and not a material quality.
But leaving that development aside, and admitting for the moment the
validity of Fabre’s contentions, I am bold enough to ask: Are we human
beings so ignorant of the second domain of olfaction as he supposes? Is
it true that we are, as he says, lacking in the equipment necessary for
the exploration of that mysterious region? To answering these questions
we shall presently address ourselves. In the meantime, I may forestall
what I shall then say by remarking that I count it a very remarkable
circumstance, if not, indeed, a significant coincidence, that, before I
had become acquainted with Fabre’s writings, I had, considering the
phenomena of human olfaction and psychology alone, actually asked myself
the same question as he asks, and had come to very much the same
conclusion.